Skip to main content
Top
Published in: Molecular Cancer 1/2016

Open Access 01-12-2016 | Review

Choosing the right cell line for renal cell cancer research

Authors: Klaudia K. Brodaczewska, Cezary Szczylik, Michal Fiedorowicz, Camillo Porta, Anna M. Czarnecka

Published in: Molecular Cancer | Issue 1/2016

Login to get access

Abstract

Cell lines are still a tool of choice for many fields of biomedical research, including oncology. Although cancer is a very complex disease, many discoveries have been made using monocultures of established cell lines. Therefore, the proper use of in vitro models is crucial to enhance our understanding of cancer. Therapeutics against renal cell cancer (RCC) are also screened with the use of cell lines. Multiple RCC in vitro cultures are available, allowing in vivo heterogeneity in the laboratory, but at the same time, these can be a source of errors. In this review, we tried to sum up the data on the RCC cell lines used currently. An increasing amount of data on RCC shed new light on the molecular background of the disease; however, it revealed how much still needs to be done. As new types of RCC are being distinguished, novel cell lines and the re-exploration of old ones seems to be indispensable to create effective in vitro tools for drug screening and more.
Appendix
Available only for authorised users
Literature
1.
go back to reference Sharma SV, Haber DA, Settleman J. Cell line-based platforms to evaluate the therapeutic efficacy of candidate anticancer agents. Nat Rev Cancer. 2010;10(4):241–53.PubMedCrossRef Sharma SV, Haber DA, Settleman J. Cell line-based platforms to evaluate the therapeutic efficacy of candidate anticancer agents. Nat Rev Cancer. 2010;10(4):241–53.PubMedCrossRef
2.
go back to reference Shoemaker RH. The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer. 2006;6(10):813–23.PubMedCrossRef Shoemaker RH. The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer. 2006;6(10):813–23.PubMedCrossRef
3.
go back to reference Stinson SF, Alley MC, Kopp WC, Fiebig HH, Mullendore LA, Pittman AF, Kenney S, Keller J, Boyd MR. Morphological and immunocytochemical characteristics of human tumor cell lines for use in a disease-oriented anticancer drug screen. Anticancer Res. 1992;12(4):1035–53.PubMed Stinson SF, Alley MC, Kopp WC, Fiebig HH, Mullendore LA, Pittman AF, Kenney S, Keller J, Boyd MR. Morphological and immunocytochemical characteristics of human tumor cell lines for use in a disease-oriented anticancer drug screen. Anticancer Res. 1992;12(4):1035–53.PubMed
4.
go back to reference Monks A, Scudiero D, Skehan P, Shoemaker R, Paull K, Vistica D, Hose C, Langley J, Cronise P, Vaigro-Wolff A, et al. Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J Natl Cancer Inst. 1991;83(11):757–66.PubMedCrossRef Monks A, Scudiero D, Skehan P, Shoemaker R, Paull K, Vistica D, Hose C, Langley J, Cronise P, Vaigro-Wolff A, et al. Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J Natl Cancer Inst. 1991;83(11):757–66.PubMedCrossRef
5.
go back to reference Zieba J, Ksiazkiewcz M, Janik K, Banaszczyk M, Peciak J, Piaskowski S, Lipinski M, Olczak M, Stoczynska-Fidelus E, Rieske P. Sensitivity of neoplastic cells to senescence unveiled under standard cell culture conditions. Anticancer Res. 2015;35(5):2759–68.PubMed Zieba J, Ksiazkiewcz M, Janik K, Banaszczyk M, Peciak J, Piaskowski S, Lipinski M, Olczak M, Stoczynska-Fidelus E, Rieske P. Sensitivity of neoplastic cells to senescence unveiled under standard cell culture conditions. Anticancer Res. 2015;35(5):2759–68.PubMed
7.
go back to reference Arul M, Roslani AC, Ng CL, Cheah SH. Culture of low passage colorectal cancer cells and demonstration of variation in selected tumour marker expression. Cytotechnology. 2014;66(3):481–91.PubMedCrossRef Arul M, Roslani AC, Ng CL, Cheah SH. Culture of low passage colorectal cancer cells and demonstration of variation in selected tumour marker expression. Cytotechnology. 2014;66(3):481–91.PubMedCrossRef
8.
go back to reference Benien P, Swami A. 3D tumor models: history, advances and future perspectives. Future Oncol. 2014;10(7):1311–27.PubMedCrossRef Benien P, Swami A. 3D tumor models: history, advances and future perspectives. Future Oncol. 2014;10(7):1311–27.PubMedCrossRef
9.
go back to reference Berg EL, Hsu YC, Lee JA. Consideration of the cellular microenvironment: physiologically relevant co-culture systems in drug discovery. Adv Drug Deliv Rev. 2014;69–70:190–204.CrossRef Berg EL, Hsu YC, Lee JA. Consideration of the cellular microenvironment: physiologically relevant co-culture systems in drug discovery. Adv Drug Deliv Rev. 2014;69–70:190–204.CrossRef
10.
go back to reference Hutchinson L, Kirk R. High drug attrition rates--where are we going wrong? Nat Rev Clin Oncol. 2011;8(4):189–90.PubMedCrossRef Hutchinson L, Kirk R. High drug attrition rates--where are we going wrong? Nat Rev Clin Oncol. 2011;8(4):189–90.PubMedCrossRef
11.
go back to reference Tuveson D, Hanahan D. Translational medicine: Cancer lessons from mice to humans. Nature. 2011;471(7338):316–7.PubMedCrossRef Tuveson D, Hanahan D. Translational medicine: Cancer lessons from mice to humans. Nature. 2011;471(7338):316–7.PubMedCrossRef
12.
go back to reference Siemeister G, Weindel K, Mohrs K, Barleon B, Martiny-Baron G, Marmé D. Reversion of deregulated expression of vascular endothelial growth factor in human renal carcinoma cells by von Hippel-Lindau tumor suppressor protein. Cancer Res. 1996;56(10):2299–301.PubMed Siemeister G, Weindel K, Mohrs K, Barleon B, Martiny-Baron G, Marmé D. Reversion of deregulated expression of vascular endothelial growth factor in human renal carcinoma cells by von Hippel-Lindau tumor suppressor protein. Cancer Res. 1996;56(10):2299–301.PubMed
13.
14.
go back to reference Kane RC, Farrell AT, Saber H, Tang S, Williams G, Jee JM, Liang C, Booth B, Chidambaram N, Morse D, et al. Sorafenib for the treatment of advanced renal cell carcinoma. Clin Cancer Res. 2006;12(24):7271–8.PubMedCrossRef Kane RC, Farrell AT, Saber H, Tang S, Williams G, Jee JM, Liang C, Booth B, Chidambaram N, Morse D, et al. Sorafenib for the treatment of advanced renal cell carcinoma. Clin Cancer Res. 2006;12(24):7271–8.PubMedCrossRef
15.
go back to reference Amundson SA, Do KT, Vinikoor LC, Lee RA, Koch-Paiz CA, Ahn J, Reimers M, Chen Y, Scudiero DA, Weinstein JN, et al. Integrating global gene expression and radiation survival parameters across the 60 cell lines of the National Cancer Institute Anticancer Drug Screen. Cancer Res. 2008;68(2):415–24.PubMedCrossRef Amundson SA, Do KT, Vinikoor LC, Lee RA, Koch-Paiz CA, Ahn J, Reimers M, Chen Y, Scudiero DA, Weinstein JN, et al. Integrating global gene expression and radiation survival parameters across the 60 cell lines of the National Cancer Institute Anticancer Drug Screen. Cancer Res. 2008;68(2):415–24.PubMedCrossRef
16.
go back to reference Anglard P, Trahan E, Liu S, Latif F, Merino MJ, Lerman MI, Zbar B, Linehan WM. Molecular and cellular characterization of human renal cell carcinoma cell lines. Cancer Res. 1992;52(2):348–56.PubMed Anglard P, Trahan E, Liu S, Latif F, Merino MJ, Lerman MI, Zbar B, Linehan WM. Molecular and cellular characterization of human renal cell carcinoma cell lines. Cancer Res. 1992;52(2):348–56.PubMed
17.
go back to reference Ebert T, Bander NH, Finstad CL, Ramsawak RD, Old LJ. Establishment and characterization of human renal cancer and normal kidney cell lines. Cancer Res. 1990;50(17):5531–6.PubMed Ebert T, Bander NH, Finstad CL, Ramsawak RD, Old LJ. Establishment and characterization of human renal cancer and normal kidney cell lines. Cancer Res. 1990;50(17):5531–6.PubMed
18.
go back to reference Greshock J, Nathanson K, Martin AM, Zhang L, Coukos G, Weber BL, Zaks TZ. Cancer cell lines as genetic models of their parent histology: analyses based on array comparative genomic hybridization. Cancer Res. 2007;67(8):3594–600.PubMedCrossRef Greshock J, Nathanson K, Martin AM, Zhang L, Coukos G, Weber BL, Zaks TZ. Cancer cell lines as genetic models of their parent histology: analyses based on array comparative genomic hybridization. Cancer Res. 2007;67(8):3594–600.PubMedCrossRef
19.
go back to reference Czarnecka AM, Kornakiewicz A, Kukwa W, Szczylik C. Frontiers in clinical and molecular diagnostics and staging of metastatic clear cell renal cell carcinoma. Future Oncol. 2014;10(6):1095–111.PubMedCrossRef Czarnecka AM, Kornakiewicz A, Kukwa W, Szczylik C. Frontiers in clinical and molecular diagnostics and staging of metastatic clear cell renal cell carcinoma. Future Oncol. 2014;10(6):1095–111.PubMedCrossRef
20.
go back to reference Czarnecka AM, Kukwa W, Kornakiewicz A, Lian F, Szczylik C. Clinical and molecular prognostic and predictive biomarkers in clear cell renal cell cancer. Future Oncol. 2014;10(15):2493–508.PubMedCrossRef Czarnecka AM, Kukwa W, Kornakiewicz A, Lian F, Szczylik C. Clinical and molecular prognostic and predictive biomarkers in clear cell renal cell cancer. Future Oncol. 2014;10(15):2493–508.PubMedCrossRef
21.
go back to reference Mizumoto A, Yamamoto K, Nakayama Y, Takara K, Nakagawa T, Hirano T, Hirai M. Induction of epithelial-mesenchymal transition via activation of epidermal growth factor receptor contributes to sunitinib resistance in human renal cell carcinoma cell lines. J Pharmacol Exp Ther. 2015;355(2):152–8.PubMedCrossRef Mizumoto A, Yamamoto K, Nakayama Y, Takara K, Nakagawa T, Hirano T, Hirai M. Induction of epithelial-mesenchymal transition via activation of epidermal growth factor receptor contributes to sunitinib resistance in human renal cell carcinoma cell lines. J Pharmacol Exp Ther. 2015;355(2):152–8.PubMedCrossRef
22.
go back to reference Hutson TE, Al-Shukri S, Stus VP, Lipatov ON, Shparyk Y, Bair AH, Rosbrook B, Andrews GI, Vogelzang NJ. Axitinib Versus Sorafenib in First-Line Metastatic Renal Cell Carcinoma: Overall Survival From a Randomized Phase III Trial. Clin Genitourin Cancer 2016. doi:10.1016/j.clgc.2016.05.008. [Epub ahead of print] Hutson TE, Al-Shukri S, Stus VP, Lipatov ON, Shparyk Y, Bair AH, Rosbrook B, Andrews GI, Vogelzang NJ. Axitinib Versus Sorafenib in First-Line Metastatic Renal Cell Carcinoma: Overall Survival From a Randomized Phase III Trial. Clin Genitourin Cancer 2016. doi:10.​1016/​j.​clgc.​2016.​05.​008. [Epub ahead of print]
23.
go back to reference Anglesio MS, Wiegand KC, Melnyk N, Chow C, Salamanca C, Prentice LM, Senz J, Yang W, Spillman MA, Cochrane DR, et al. Type-specific cell line models for type-specific ovarian cancer research. PLoS One. 2013;8(9):e72162.PubMedPubMedCentralCrossRef Anglesio MS, Wiegand KC, Melnyk N, Chow C, Salamanca C, Prentice LM, Senz J, Yang W, Spillman MA, Cochrane DR, et al. Type-specific cell line models for type-specific ovarian cancer research. PLoS One. 2013;8(9):e72162.PubMedPubMedCentralCrossRef
24.
go back to reference Tani T, Laitinen L, Kangas L, Lehto VP, Virtanen I. Expression of E- and N-cadherin in renal cell carcinomas, in renal cell carcinoma cell lines in vitro and in their xenografts. Int J Cancer. 1995;64(6):407–14.PubMedCrossRef Tani T, Laitinen L, Kangas L, Lehto VP, Virtanen I. Expression of E- and N-cadherin in renal cell carcinomas, in renal cell carcinoma cell lines in vitro and in their xenografts. Int J Cancer. 1995;64(6):407–14.PubMedCrossRef
25.
go back to reference Crumley SM, Divatia M, Truong L, Shen S, Ayala AG, Ro JY. Renal cell carcinoma: Evolving and emerging subtypes. World J Clin Cases. 2013;1(9):262–75.PubMedPubMedCentral Crumley SM, Divatia M, Truong L, Shen S, Ayala AG, Ro JY. Renal cell carcinoma: Evolving and emerging subtypes. World J Clin Cases. 2013;1(9):262–75.PubMedPubMedCentral
26.
go back to reference Escudier B, Porta C, Schmidinger M, Algaba F, Patard JJ, Khoo V, Eisen T, Horwich A. Renal cell carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25 Suppl 3:iii49–56.PubMedCrossRef Escudier B, Porta C, Schmidinger M, Algaba F, Patard JJ, Khoo V, Eisen T, Horwich A. Renal cell carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25 Suppl 3:iii49–56.PubMedCrossRef
27.
go back to reference Delahunt B, Eble JN. Papillary renal cell carcinoma: a clinicopathologic and immunohistochemical study of 105 tumors. Mod Pathol. 1997;10(6):537–44.PubMed Delahunt B, Eble JN. Papillary renal cell carcinoma: a clinicopathologic and immunohistochemical study of 105 tumors. Mod Pathol. 1997;10(6):537–44.PubMed
28.
go back to reference Schmidt L, Duh FM, Chen F, Kishida T, Glenn G, Choyke P, Scherer SW, Zhuang Z, Lubensky I, Dean M, et al. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nat Genet. 1997;16(1):68–73.PubMedCrossRef Schmidt L, Duh FM, Chen F, Kishida T, Glenn G, Choyke P, Scherer SW, Zhuang Z, Lubensky I, Dean M, et al. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nat Genet. 1997;16(1):68–73.PubMedCrossRef
29.
go back to reference Furge KA, Dykema K, Petillo D, Westphal M, Zhang Z, Kort EJ, Teh BT. Combining differential expression, chromosomal and pathway analyses for the molecular characterization of renal cell carcinoma. Can Urol Assoc J. 2007;1(2 Suppl):S21–7.PubMedPubMedCentral Furge KA, Dykema K, Petillo D, Westphal M, Zhang Z, Kort EJ, Teh BT. Combining differential expression, chromosomal and pathway analyses for the molecular characterization of renal cell carcinoma. Can Urol Assoc J. 2007;1(2 Suppl):S21–7.PubMedPubMedCentral
30.
go back to reference Liddell H, Mare A, Heywood S, Bennett G, Chan HF. Clear cell papillary renal cell carcinoma: a potential mimic of conventional clear cell renal carcinoma on core biopsy. Case Rep Urol. 2015;2015:423908.PubMedPubMedCentral Liddell H, Mare A, Heywood S, Bennett G, Chan HF. Clear cell papillary renal cell carcinoma: a potential mimic of conventional clear cell renal carcinoma on core biopsy. Case Rep Urol. 2015;2015:423908.PubMedPubMedCentral
31.
go back to reference Srigley JR, Delahunt B, Eble JN, Egevad L, Epstein JI, Grignon D, Hes O, Moch H, Montironi R, Tickoo SK, et al. The International Society of Urological Pathology (ISUP) Vancouver Classification of Renal Neoplasia. Am J Surg Pathol. 2013;37(10):1469–89.PubMedCrossRef Srigley JR, Delahunt B, Eble JN, Egevad L, Epstein JI, Grignon D, Hes O, Moch H, Montironi R, Tickoo SK, et al. The International Society of Urological Pathology (ISUP) Vancouver Classification of Renal Neoplasia. Am J Surg Pathol. 2013;37(10):1469–89.PubMedCrossRef
32.
go back to reference Shuch B, Amin A, Armstrong AJ, Eble JN, Ficarra V, Lopez-Beltran A, Martignoni G, Rini BI, Kutikov A. Understanding pathologic variants of renal cell carcinoma: distilling therapeutic opportunities from biologic complexity. Eur Urol. 2015;67(1):85–97.PubMedCrossRef Shuch B, Amin A, Armstrong AJ, Eble JN, Ficarra V, Lopez-Beltran A, Martignoni G, Rini BI, Kutikov A. Understanding pathologic variants of renal cell carcinoma: distilling therapeutic opportunities from biologic complexity. Eur Urol. 2015;67(1):85–97.PubMedCrossRef
33.
go back to reference Nickerson ML, Jaeger E, Shi Y, Durocher JA, Mahurkar S, Zaridze D, Matveev V, Janout V, Kollarova H, Bencko V, et al. Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. Clin Cancer Res. 2008;14(15):4726–34.PubMedPubMedCentralCrossRef Nickerson ML, Jaeger E, Shi Y, Durocher JA, Mahurkar S, Zaridze D, Matveev V, Janout V, Kollarova H, Bencko V, et al. Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. Clin Cancer Res. 2008;14(15):4726–34.PubMedPubMedCentralCrossRef
35.
go back to reference Van Bergen NJ, Wood JP, Chidlow G, Trounce IA, Casson RJ, Ju WK, Weinreb RN, Crowston JG. Recharacterization of the RGC-5 retinal ganglion cell line. Invest Ophthalmol Vis Sci. 2009;50(9):4267–72.PubMedCrossRef Van Bergen NJ, Wood JP, Chidlow G, Trounce IA, Casson RJ, Ju WK, Weinreb RN, Crowston JG. Recharacterization of the RGC-5 retinal ganglion cell line. Invest Ophthalmol Vis Sci. 2009;50(9):4267–72.PubMedCrossRef
36.
go back to reference Boonstra JJ, van der Velden AW, Beerens EC, van Marion R, Morita-Fujimura Y, Matsui Y, Nishihira T, Tselepis C, Hainaut P, Lowe AW, et al. Mistaken identity of widely used esophageal adenocarcinoma cell line TE-7. Cancer Res. 2007;67(17):7996–8001.PubMedCrossRef Boonstra JJ, van der Velden AW, Beerens EC, van Marion R, Morita-Fujimura Y, Matsui Y, Nishihira T, Tselepis C, Hainaut P, Lowe AW, et al. Mistaken identity of widely used esophageal adenocarcinoma cell line TE-7. Cancer Res. 2007;67(17):7996–8001.PubMedCrossRef
37.
38.
go back to reference van Staveren WC, Solis DY, Hebrant A, Detours V, Dumont JE, Maenhaut C. Human cancer cell lines: Experimental models for cancer cells in situ? For cancer stem cells? Biochim Biophys Acta. 2009;1795(2):92–103.PubMed van Staveren WC, Solis DY, Hebrant A, Detours V, Dumont JE, Maenhaut C. Human cancer cell lines: Experimental models for cancer cells in situ? For cancer stem cells? Biochim Biophys Acta. 2009;1795(2):92–103.PubMed
39.
go back to reference Lauvrak SU, Munthe E, Kresse SH, Stratford EW, Namlos HM, Meza-Zepeda LA, Myklebost O. Functional characterisation of osteosarcoma cell lines and identification of mRNAs and miRNAs associated with aggressive cancer phenotypes. Br J Cancer. 2013;109(8):2228–36.PubMedPubMedCentralCrossRef Lauvrak SU, Munthe E, Kresse SH, Stratford EW, Namlos HM, Meza-Zepeda LA, Myklebost O. Functional characterisation of osteosarcoma cell lines and identification of mRNAs and miRNAs associated with aggressive cancer phenotypes. Br J Cancer. 2013;109(8):2228–36.PubMedPubMedCentralCrossRef
40.
go back to reference Perrier-Trudova V, Huimin BW, Kongpetch S, Huang D, Ong P, Le Formal A, Poon SL, Siew EY, Myint SS, Gad S, et al. Fumarate Hydratase-deficient Cell Line NCCFH1 as a New In Vitro Model of Hereditary Papillary Renal Cell Carcinoma Type 2. Anticancer Res. 2015;35(12):6639–53.PubMed Perrier-Trudova V, Huimin BW, Kongpetch S, Huang D, Ong P, Le Formal A, Poon SL, Siew EY, Myint SS, Gad S, et al. Fumarate Hydratase-deficient Cell Line NCCFH1 as a New In Vitro Model of Hereditary Papillary Renal Cell Carcinoma Type 2. Anticancer Res. 2015;35(12):6639–53.PubMed
41.
go back to reference Hirobe M, Masumori N, Tanaka T, Kitamura H, Tsukamoto T. Establishment of an ASPL-TFE3 renal cell carcinoma cell line (S-TFE). Cancer Biol Ther. 2013;14(6):502–10.PubMedPubMedCentralCrossRef Hirobe M, Masumori N, Tanaka T, Kitamura H, Tsukamoto T. Establishment of an ASPL-TFE3 renal cell carcinoma cell line (S-TFE). Cancer Biol Ther. 2013;14(6):502–10.PubMedPubMedCentralCrossRef
42.
go back to reference Korhonen M, Sariola H, Gould VE, Kangas L, Virtanen I. Integrins and laminins in human renal carcinoma cells and tumors grown in nude mice. Cancer Res. 1994;54(16):4532–8.PubMed Korhonen M, Sariola H, Gould VE, Kangas L, Virtanen I. Integrins and laminins in human renal carcinoma cells and tumors grown in nude mice. Cancer Res. 1994;54(16):4532–8.PubMed
43.
go back to reference Hakimi AA, Chevinsky M, Hsieh JJ, Sander C, Sinha R. Mp23-11 Genomic Comparison of Renal Cell Carcinoma Cell Lines to Human Tumors. J Urol. 2014;191(4):e247.CrossRef Hakimi AA, Chevinsky M, Hsieh JJ, Sander C, Sinha R. Mp23-11 Genomic Comparison of Renal Cell Carcinoma Cell Lines to Human Tumors. J Urol. 2014;191(4):e247.CrossRef
44.
go back to reference Schmidt L, Junker K, Nakaigawa N, Kinjerski T, Weirich G, Miller M, Lubensky I, Neumann HP, Brauch H, Decker J, et al. Novel mutations of the MET proto-oncogene in papillary renal carcinomas. Oncogene. 1999;18(14):2343–50.PubMedCrossRef Schmidt L, Junker K, Nakaigawa N, Kinjerski T, Weirich G, Miller M, Lubensky I, Neumann HP, Brauch H, Decker J, et al. Novel mutations of the MET proto-oncogene in papillary renal carcinomas. Oncogene. 1999;18(14):2343–50.PubMedCrossRef
45.
go back to reference Kovacs G, Fuzesi L, Emanual A, Kung HF. Cytogenetics of papillary renal cell tumors. Genes Chromosomes Cancer. 1991;3(4):249–55.PubMedCrossRef Kovacs G, Fuzesi L, Emanual A, Kung HF. Cytogenetics of papillary renal cell tumors. Genes Chromosomes Cancer. 1991;3(4):249–55.PubMedCrossRef
46.
go back to reference Shinojima T, Oya M, Takayanagi A, Mizuno R, Shimizu N, Murai M. Renal cancer cells lacking hypoxia inducible factor (HIF)-1alpha expression maintain vascular endothelial growth factor expression through HIF-2alpha. Carcinogenesis. 2007;28(3):529–36.PubMedCrossRef Shinojima T, Oya M, Takayanagi A, Mizuno R, Shimizu N, Murai M. Renal cancer cells lacking hypoxia inducible factor (HIF)-1alpha expression maintain vascular endothelial growth factor expression through HIF-2alpha. Carcinogenesis. 2007;28(3):529–36.PubMedCrossRef
47.
go back to reference Kucejova B, Pena-Llopis S, Yamasaki T, Sivanand S, Tran TA, Alexander S, Wolff NC, Lotan Y, Xie XJ, Kabbani W, et al. Interplay between pVHL and mTORC1 pathways in clear-cell renal cell carcinoma. Mol Cancer Res. 2011;9(9):1255–65.PubMedPubMedCentralCrossRef Kucejova B, Pena-Llopis S, Yamasaki T, Sivanand S, Tran TA, Alexander S, Wolff NC, Lotan Y, Xie XJ, Kabbani W, et al. Interplay between pVHL and mTORC1 pathways in clear-cell renal cell carcinoma. Mol Cancer Res. 2011;9(9):1255–65.PubMedPubMedCentralCrossRef
48.
go back to reference Ashida S, Nishimori I, Tanimura M, Onishi S, Shuin T. Effects of von Hippel-Lindau gene mutation and methylation status on expression of transmembrane carbonic anhydrases in renal cell carcinoma. J Cancer Res Clin Oncol. 2002;128(10):561–8.PubMedCrossRef Ashida S, Nishimori I, Tanimura M, Onishi S, Shuin T. Effects of von Hippel-Lindau gene mutation and methylation status on expression of transmembrane carbonic anhydrases in renal cell carcinoma. J Cancer Res Clin Oncol. 2002;128(10):561–8.PubMedCrossRef
49.
go back to reference Lovell M, Lott ST, Wong P, El-Naggar A, Tucker S, Killary AM. The genetic locus NRC-1 within chromosome 3p12 mediates tumor suppression in renal cell carcinoma independently of histological type, tumor microenvironment, and VHL mutation. Cancer Res. 1999;59(9):2182–9.PubMed Lovell M, Lott ST, Wong P, El-Naggar A, Tucker S, Killary AM. The genetic locus NRC-1 within chromosome 3p12 mediates tumor suppression in renal cell carcinoma independently of histological type, tumor microenvironment, and VHL mutation. Cancer Res. 1999;59(9):2182–9.PubMed
50.
go back to reference Robb VA, Karbowniczek M, Klein-Szanto AJ, Henske EP. Activation of the mTOR signaling pathway in renal clear cell carcinoma. J Urol. 2007;177(1):346–52.PubMedCrossRef Robb VA, Karbowniczek M, Klein-Szanto AJ, Henske EP. Activation of the mTOR signaling pathway in renal clear cell carcinoma. J Urol. 2007;177(1):346–52.PubMedCrossRef
51.
go back to reference Campbell L, Al-Jayyoussi G, Gutteridge R, Gumbleton N, Griffiths R, Gumbleton S, Smith MW, Griffiths DF, Gumbleton M. Caveolin-1 in renal cell carcinoma promotes tumour cell invasion, and in co-operation with pERK predicts metastases in patients with clinically confined disease. J Transl Med. 2013;11:255.PubMedPubMedCentralCrossRef Campbell L, Al-Jayyoussi G, Gutteridge R, Gumbleton N, Griffiths R, Gumbleton S, Smith MW, Griffiths DF, Gumbleton M. Caveolin-1 in renal cell carcinoma promotes tumour cell invasion, and in co-operation with pERK predicts metastases in patients with clinically confined disease. J Transl Med. 2013;11:255.PubMedPubMedCentralCrossRef
52.
go back to reference Hsu RJ, Ho JY, Cha TL, Yu DS, Wu CL, Huang WP, Chu P, Chen YH, Chen JT, Yu CP. WNT10A plays an oncogenic role in renal cell carcinoma by activating WNT/beta-catenin pathway. PLoS One. 2012;7(10):e47649.PubMedPubMedCentralCrossRef Hsu RJ, Ho JY, Cha TL, Yu DS, Wu CL, Huang WP, Chu P, Chen YH, Chen JT, Yu CP. WNT10A plays an oncogenic role in renal cell carcinoma by activating WNT/beta-catenin pathway. PLoS One. 2012;7(10):e47649.PubMedPubMedCentralCrossRef
53.
go back to reference Ding XF, Zhou J, Hu QY, Liu SC, Chen G. The tumor suppressor pVHL down-regulates never-in-mitosis A-related kinase 8 via hypoxia-inducible factors to maintain cilia in human renal cancer cells. J Biol Chem. 2015;290(3):1389–94.PubMedCrossRef Ding XF, Zhou J, Hu QY, Liu SC, Chen G. The tumor suppressor pVHL down-regulates never-in-mitosis A-related kinase 8 via hypoxia-inducible factors to maintain cilia in human renal cancer cells. J Biol Chem. 2015;290(3):1389–94.PubMedCrossRef
54.
go back to reference Iliopoulos O, Kibel A, Gray S, Kaelin WG. Tumour suppression by the human von Hippel-Lindau gene product. Nat Med. 1995;1(8):822–6.PubMedCrossRef Iliopoulos O, Kibel A, Gray S, Kaelin WG. Tumour suppression by the human von Hippel-Lindau gene product. Nat Med. 1995;1(8):822–6.PubMedCrossRef
55.
go back to reference Kozlowski JM, Fidler IJ, Campbell D, Xu ZL, Kaighn ME, Hart IR. Metastatic behavior of human tumor cell lines grown in the nude mouse. Cancer Res. 1984;44(8):3522–9.PubMed Kozlowski JM, Fidler IJ, Campbell D, Xu ZL, Kaighn ME, Hart IR. Metastatic behavior of human tumor cell lines grown in the nude mouse. Cancer Res. 1984;44(8):3522–9.PubMed
56.
go back to reference Miyake M, Goodison S, Lawton A, Zhang G, Gomes-Giacoia E, Rosser CJ. Erythropoietin is a JAK2 and ERK1/2 effector that can promote renal tumor cell proliferation under hypoxic conditions. J Hematol Oncol. 2013;6:65.PubMedPubMedCentralCrossRef Miyake M, Goodison S, Lawton A, Zhang G, Gomes-Giacoia E, Rosser CJ. Erythropoietin is a JAK2 and ERK1/2 effector that can promote renal tumor cell proliferation under hypoxic conditions. J Hematol Oncol. 2013;6:65.PubMedPubMedCentralCrossRef
57.
go back to reference Jiang Y, Zhang W, Kondo K, Klco JM, St Martin TB, Dufault MR, Madden SL, Kaelin Jr WG, Nacht M. Gene expression profiling in a renal cell carcinoma cell line: dissecting VHL and hypoxia-dependent pathways. Mol Cancer Res. 2003;1(6):453–62.PubMed Jiang Y, Zhang W, Kondo K, Klco JM, St Martin TB, Dufault MR, Madden SL, Kaelin Jr WG, Nacht M. Gene expression profiling in a renal cell carcinoma cell line: dissecting VHL and hypoxia-dependent pathways. Mol Cancer Res. 2003;1(6):453–62.PubMed
58.
go back to reference Lin Y, Yang Z, Xu A, Dong P, Huang Y, Liu H, Li F, Wang H, Xu Q, Wang Y, et al. PIK3R1 negatively regulates the epithelial-mesenchymal transition and stem-like phenotype of renal cancer cells through the AKT/GSK3beta/CTNNB1 signaling pathway. Sci Rep. 2015;5:8997.PubMedPubMedCentralCrossRef Lin Y, Yang Z, Xu A, Dong P, Huang Y, Liu H, Li F, Wang H, Xu Q, Wang Y, et al. PIK3R1 negatively regulates the epithelial-mesenchymal transition and stem-like phenotype of renal cancer cells through the AKT/GSK3beta/CTNNB1 signaling pathway. Sci Rep. 2015;5:8997.PubMedPubMedCentralCrossRef
59.
go back to reference Zhang L, Jiao M, Wu K, Li L, Zhu G, Wang X, He D, Wu D. TNF-alpha induced epithelial mesenchymal transition increases stemness properties in renal cell carcinoma cells. Int J Clin Exp Med. 2014;7(12):4951–8.PubMedPubMedCentral Zhang L, Jiao M, Wu K, Li L, Zhu G, Wang X, He D, Wu D. TNF-alpha induced epithelial mesenchymal transition increases stemness properties in renal cell carcinoma cells. Int J Clin Exp Med. 2014;7(12):4951–8.PubMedPubMedCentral
60.
go back to reference Boysen G, Bausch-Fluck D, Thoma CR, Nowicka AM, Stiehl DP, Cima I, Luu VD, von Teichman A, Hermanns T, Sulser T, et al. Identification and functional characterization of pVHL-dependent cell surface proteins in renal cell carcinoma. Neoplasia. 2012;14(6):535–46.PubMedPubMedCentralCrossRef Boysen G, Bausch-Fluck D, Thoma CR, Nowicka AM, Stiehl DP, Cima I, Luu VD, von Teichman A, Hermanns T, Sulser T, et al. Identification and functional characterization of pVHL-dependent cell surface proteins in renal cell carcinoma. Neoplasia. 2012;14(6):535–46.PubMedPubMedCentralCrossRef
61.
go back to reference Ho MY, Tang SJ, Chuang MJ, Cha TL, Li JY, Sun GH, Sun KH. TNF-alpha induces epithelial-mesenchymal transition of renal cell carcinoma cells via a GSK3beta-dependent mechanism. Mol Cancer Res. 2012;10(8):1109–19.PubMedCrossRef Ho MY, Tang SJ, Chuang MJ, Cha TL, Li JY, Sun GH, Sun KH. TNF-alpha induces epithelial-mesenchymal transition of renal cell carcinoma cells via a GSK3beta-dependent mechanism. Mol Cancer Res. 2012;10(8):1109–19.PubMedCrossRef
62.
go back to reference Strube A, Stepina E, Mumberg D, Scholz A, Hauff P, Käkönen S-M. Characterization of a new renal cell carcinoma bone metastasis mouse model. Clin Exp Metastasis. 2010;27(5):319–30.PubMedCrossRef Strube A, Stepina E, Mumberg D, Scholz A, Hauff P, Käkönen S-M. Characterization of a new renal cell carcinoma bone metastasis mouse model. Clin Exp Metastasis. 2010;27(5):319–30.PubMedCrossRef
63.
go back to reference Xie C, Schwarz EM, Sampson ER, Dhillon RS, Li D, O’Keefe RJ, Tyler W. Unique angiogenic and vasculogenic properties of renal cell carcinoma in a xenograft model of bone metastasis are associated with high levels of vegf-a and decreased ang-1 expression. J Orthop Res. 2012;30(2):325–33.PubMedCrossRef Xie C, Schwarz EM, Sampson ER, Dhillon RS, Li D, O’Keefe RJ, Tyler W. Unique angiogenic and vasculogenic properties of renal cell carcinoma in a xenograft model of bone metastasis are associated with high levels of vegf-a and decreased ang-1 expression. J Orthop Res. 2012;30(2):325–33.PubMedCrossRef
64.
go back to reference Pan T, Fong ELS, Martinez M, Harrington DA, Lin S-H, Farach-Carson MC, Satcher RL. Three-dimensional (3D) culture of bone-derived human 786-O renal cell carcinoma retains relevant clinical characteristics of bone metastases. Cancer Lett. 2015;365(1):89–95.PubMedPubMedCentralCrossRef Pan T, Fong ELS, Martinez M, Harrington DA, Lin S-H, Farach-Carson MC, Satcher RL. Three-dimensional (3D) culture of bone-derived human 786-O renal cell carcinoma retains relevant clinical characteristics of bone metastases. Cancer Lett. 2015;365(1):89–95.PubMedPubMedCentralCrossRef
65.
go back to reference Lichner Z, Saleh C, Subramaniam V, Seivwright A, Prud'homme GJ, Yousef GM. miR-17 inhibition enhances the formation of kidney cancer spheres with stem cell/tumor initiating cell properties. Oncotarget 2015;6(8):5567–81.PubMedCrossRef Lichner Z, Saleh C, Subramaniam V, Seivwright A, Prud'homme GJ, Yousef GM. miR-17 inhibition enhances the formation of kidney cancer spheres with stem cell/tumor initiating cell properties. Oncotarget 2015;6(8):5567–81.PubMedCrossRef
66.
go back to reference Liu YH, Lin CY, Lin WC, Tang SW, Lai MK, Lin JY. Up-Regulation of Vascular Endothelial Growth Factor-D Expression in Clear Cell Renal Cell Carcinoma by CD74: A Critical Role in Cancer Cell Tumorigenesis. J Immunol. 2008;181(9):6584–94.PubMedCrossRef Liu YH, Lin CY, Lin WC, Tang SW, Lai MK, Lin JY. Up-Regulation of Vascular Endothelial Growth Factor-D Expression in Clear Cell Renal Cell Carcinoma by CD74: A Critical Role in Cancer Cell Tumorigenesis. J Immunol. 2008;181(9):6584–94.PubMedCrossRef
67.
go back to reference Glube N, Giessl A, Wolfrum U, Langguth P. Caki-1 cells represent an in vitro model system for studying the human proximal tubule epithelium. Nephron Exp Nephrol. 2007;107(2):e47–56.PubMedCrossRef Glube N, Giessl A, Wolfrum U, Langguth P. Caki-1 cells represent an in vitro model system for studying the human proximal tubule epithelium. Nephron Exp Nephrol. 2007;107(2):e47–56.PubMedCrossRef
68.
go back to reference Pulkkanen KJ, Parkkinen JJ, Kettunen MI, Kauppinen RA, Lappalainen M, Ala-Opas MY, Yla-Herttuala S. Characterization of a new animal model for human renal cell carcinoma. In Vivo. 2000;14(3):393–400.PubMed Pulkkanen KJ, Parkkinen JJ, Kettunen MI, Kauppinen RA, Lappalainen M, Ala-Opas MY, Yla-Herttuala S. Characterization of a new animal model for human renal cell carcinoma. In Vivo. 2000;14(3):393–400.PubMed
69.
go back to reference Pulkkanen KJ, Parkkinen JJ, Laukkanen JM, Kettunen MI, Tyynela K, Kauppinen RA, Ala-Opas MY, Yla-Herttuala S. HSV-tk gene therapy for human renal cell carcinoma in nude mice. Cancer Gene Ther. 2001;8(7):529–36.PubMedCrossRef Pulkkanen KJ, Parkkinen JJ, Laukkanen JM, Kettunen MI, Tyynela K, Kauppinen RA, Ala-Opas MY, Yla-Herttuala S. HSV-tk gene therapy for human renal cell carcinoma in nude mice. Cancer Gene Ther. 2001;8(7):529–36.PubMedCrossRef
70.
go back to reference Furge KA, Chen J, Koeman J, Swiatek P, Dykema K, Lucin K, Kahnoski R, Yang XJ, Teh BT. Detection of DNA copy number changes and oncogenic signaling abnormalities from gene expression data reveals MYC activation in high-grade papillary renal cell carcinoma. Cancer Res. 2007;67(7):3171–6.PubMedCrossRef Furge KA, Chen J, Koeman J, Swiatek P, Dykema K, Lucin K, Kahnoski R, Yang XJ, Teh BT. Detection of DNA copy number changes and oncogenic signaling abnormalities from gene expression data reveals MYC activation in high-grade papillary renal cell carcinoma. Cancer Res. 2007;67(7):3171–6.PubMedCrossRef
71.
go back to reference Looyenga BD, Furge KA, Dykema KJ, Koeman J, Swiatek PJ, Giordano TJ, West AB, Resau JH, Teh BT, MacKeigan JP. Chromosomal amplification of leucine-rich repeat kinase-2 (LRRK2) is required for oncogenic MET signaling in papillary renal and thyroid carcinomas. Proc Natl Acad Sci U S A. 2011;108(4):1439–44.PubMedPubMedCentralCrossRef Looyenga BD, Furge KA, Dykema KJ, Koeman J, Swiatek PJ, Giordano TJ, West AB, Resau JH, Teh BT, MacKeigan JP. Chromosomal amplification of leucine-rich repeat kinase-2 (LRRK2) is required for oncogenic MET signaling in papillary renal and thyroid carcinomas. Proc Natl Acad Sci U S A. 2011;108(4):1439–44.PubMedPubMedCentralCrossRef
72.
go back to reference Blondeau JJ, Deng M, Syring I, Schrodter S, Schmidt D, Perner S, Muller SC, Ellinger J. Identification of novel long non-coding RNAs in clear cell renal cell carcinoma. Clin Epigenetics. 2015;7(1):10.PubMedPubMedCentralCrossRef Blondeau JJ, Deng M, Syring I, Schrodter S, Schmidt D, Perner S, Muller SC, Ellinger J. Identification of novel long non-coding RNAs in clear cell renal cell carcinoma. Clin Epigenetics. 2015;7(1):10.PubMedPubMedCentralCrossRef
73.
go back to reference Zaravinos A, Pieri M, Mourmouras N, Anastasiadou N, Zouvani I, Delakas D, Deltas C. Altered metabolic pathways in clear cell renal cell carcinoma: A meta-analysis and validation study focused on the deregulated genes and their associated networks. Oncoscience. 2014;1(2):117–31.PubMedPubMedCentralCrossRef Zaravinos A, Pieri M, Mourmouras N, Anastasiadou N, Zouvani I, Delakas D, Deltas C. Altered metabolic pathways in clear cell renal cell carcinoma: A meta-analysis and validation study focused on the deregulated genes and their associated networks. Oncoscience. 2014;1(2):117–31.PubMedPubMedCentralCrossRef
74.
go back to reference Roos FC, Evans AJ, Brenner W, Wondergem B, Klomp J, Heir P, Roche O, Thomas C, Schimmel H, Furge KA, et al. Deregulation of E2-EPF ubiquitin carrier protein in papillary renal cell carcinoma. Am J Pathol. 2011;178(2):853–60.PubMedPubMedCentralCrossRef Roos FC, Evans AJ, Brenner W, Wondergem B, Klomp J, Heir P, Roche O, Thomas C, Schimmel H, Furge KA, et al. Deregulation of E2-EPF ubiquitin carrier protein in papillary renal cell carcinoma. Am J Pathol. 2011;178(2):853–60.PubMedPubMedCentralCrossRef
75.
go back to reference Williams RD, Elliott AY, Stein N, Fraley EE. In vitro cultivation of human renal cell cancer. I. Establishment of cells in culture. In Vitro. 1976;12(9):623–7.PubMedCrossRef Williams RD, Elliott AY, Stein N, Fraley EE. In vitro cultivation of human renal cell cancer. I. Establishment of cells in culture. In Vitro. 1976;12(9):623–7.PubMedCrossRef
76.
go back to reference Huang B, Huang YJ, Yao ZJ, Chen X, Guo SJ, Mao XP, Wang DH, Chen JX, Qiu SP. Cancer stem cell-like side population cells in clear cell renal cell carcinoma cell line 769P. PLoS One. 2013;8(7):e68293.PubMedPubMedCentralCrossRef Huang B, Huang YJ, Yao ZJ, Chen X, Guo SJ, Mao XP, Wang DH, Chen JX, Qiu SP. Cancer stem cell-like side population cells in clear cell renal cell carcinoma cell line 769P. PLoS One. 2013;8(7):e68293.PubMedPubMedCentralCrossRef
77.
go back to reference Harten SK, Esteban MA, Shukla D, Ashcroft M, Maxwell PH. Inactivation of the von Hippel-Lindau tumour suppressor gene induces Neuromedin U expression in renal cancer cells. Mol Cancer. 2011;10:89.PubMedPubMedCentralCrossRef Harten SK, Esteban MA, Shukla D, Ashcroft M, Maxwell PH. Inactivation of the von Hippel-Lindau tumour suppressor gene induces Neuromedin U expression in renal cancer cells. Mol Cancer. 2011;10:89.PubMedPubMedCentralCrossRef
78.
go back to reference Razorenova OV, Finger EC, Colavitti R, Chernikova SB, Boiko AD, Chan CK, Krieg A, Bedogni B, LaGory E, Weissman IL, et al. VHL loss in renal cell carcinoma leads to up-regulation of CUB domain-containing protein 1 to stimulate PKC{delta}-driven migration. Proc Natl Acad Sci U S A. 2011;108(5):1931–6.PubMedPubMedCentralCrossRef Razorenova OV, Finger EC, Colavitti R, Chernikova SB, Boiko AD, Chan CK, Krieg A, Bedogni B, LaGory E, Weissman IL, et al. VHL loss in renal cell carcinoma leads to up-regulation of CUB domain-containing protein 1 to stimulate PKC{delta}-driven migration. Proc Natl Acad Sci U S A. 2011;108(5):1931–6.PubMedPubMedCentralCrossRef
79.
go back to reference Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 1999;399(6733):271–5.PubMedCrossRef Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 1999;399(6733):271–5.PubMedCrossRef
80.
go back to reference Harada H, Itasaka S, Zhu Y, Zeng L, Xie X, Morinibu A, Shinomiya K, Hiraoka M. Treatment regimen determines whether an HIF-1 inhibitor enhances or inhibits the effect of radiation therapy. Br J Cancer. 2009;100(5):747–57.PubMedPubMedCentralCrossRef Harada H, Itasaka S, Zhu Y, Zeng L, Xie X, Morinibu A, Shinomiya K, Hiraoka M. Treatment regimen determines whether an HIF-1 inhibitor enhances or inhibits the effect of radiation therapy. Br J Cancer. 2009;100(5):747–57.PubMedPubMedCentralCrossRef
81.
go back to reference Esteban MA, Tran MG, Harten SK, Hill P, Castellanos MC, Chandra A, Raval R, O’Brien TS, Maxwell PH. Regulation of E-cadherin expression by VHL and hypoxia-inducible factor. Cancer Res. 2006;66(7):3567–75.PubMedCrossRef Esteban MA, Tran MG, Harten SK, Hill P, Castellanos MC, Chandra A, Raval R, O’Brien TS, Maxwell PH. Regulation of E-cadherin expression by VHL and hypoxia-inducible factor. Cancer Res. 2006;66(7):3567–75.PubMedCrossRef
82.
go back to reference Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol. 2005;25(13):5675–86.PubMedPubMedCentralCrossRef Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol. 2005;25(13):5675–86.PubMedPubMedCentralCrossRef
83.
go back to reference Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, Zeller KI, Dang CV, Semenza GL. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell. 2007;11(5):407–20.PubMedCrossRef Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, Zeller KI, Dang CV, Semenza GL. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell. 2007;11(5):407–20.PubMedCrossRef
84.
go back to reference Miyao N, Tsukamoto T, Kumamoto Y. Establishment of three human renal cell carcinoma cell lines (SMKT-R- SMKT-R-2, and SMKT-R-3) and their characters. Urol Res. 1989;17:317–24. 1 SRC - GoogleScholar.PubMedCrossRef Miyao N, Tsukamoto T, Kumamoto Y. Establishment of three human renal cell carcinoma cell lines (SMKT-R- SMKT-R-2, and SMKT-R-3) and their characters. Urol Res. 1989;17:317–24. 1 SRC - GoogleScholar.PubMedCrossRef
85.
go back to reference Tanaka T, Torigoe T, Hirohashi Y, Sato E, Honma I, Kitamura H, Masumori N, Tsukamoto T, Sato N. Hypoxia-inducible factor (HIF)-independent expression mechanism and novel function of HIF prolyl hydroxylase-3 in renal cell carcinoma. J Cancer Res Clin Oncol. 2014;140(3):503–13.PubMedCrossRef Tanaka T, Torigoe T, Hirohashi Y, Sato E, Honma I, Kitamura H, Masumori N, Tsukamoto T, Sato N. Hypoxia-inducible factor (HIF)-independent expression mechanism and novel function of HIF prolyl hydroxylase-3 in renal cell carcinoma. J Cancer Res Clin Oncol. 2014;140(3):503–13.PubMedCrossRef
86.
go back to reference Tochizawa S, Masumori N, Yanai Y, Ohmoto Y, Yabuuchi Y, Tsukamoto T. Antitumor effects of a combination of interferon-alpha and sorafenib on human renal carcinoma cell lines. Biomed Res. 2008;29(6):271–8.PubMedCrossRef Tochizawa S, Masumori N, Yanai Y, Ohmoto Y, Yabuuchi Y, Tsukamoto T. Antitumor effects of a combination of interferon-alpha and sorafenib on human renal carcinoma cell lines. Biomed Res. 2008;29(6):271–8.PubMedCrossRef
87.
go back to reference Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, Tarpey P, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883–92.PubMedPubMedCentralCrossRef Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, Tarpey P, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883–92.PubMedPubMedCentralCrossRef
88.
go back to reference Kudo D, Rayman P, Horton C, Cathcart MK, Bukowski RM, Thornton M, Tannenbaum C, Finke JH. Gangliosides expressed by the renal cell carcinoma cell line SK-RC-45 are involved in tumor-induced apoptosis of T cells. Cancer Res 2003;63(7):1676–83.PubMed Kudo D, Rayman P, Horton C, Cathcart MK, Bukowski RM, Thornton M, Tannenbaum C, Finke JH. Gangliosides expressed by the renal cell carcinoma cell line SK-RC-45 are involved in tumor-induced apoptosis of T cells. Cancer Res 2003;63(7):1676–83.PubMed
89.
go back to reference Das T, Sa G, Paszkiewicz-Kozik E, Hilston C, Molto L, Rayman P, Kudo D, Biswas K, Bukowski RM, Finke JH, et al. Renal cell carcinoma tumors induce T cell apoptosis through receptor-dependent and receptor-independent pathways. J Immunol. 2008;180(7):4687–96.PubMedCrossRef Das T, Sa G, Paszkiewicz-Kozik E, Hilston C, Molto L, Rayman P, Kudo D, Biswas K, Bukowski RM, Finke JH, et al. Renal cell carcinoma tumors induce T cell apoptosis through receptor-dependent and receptor-independent pathways. J Immunol. 2008;180(7):4687–96.PubMedCrossRef
90.
go back to reference Zhong Y, Guan K, Guo S, Zhou C, Wang D, Ma W, Zhang Y, Li C, Zhang S. Spheres derived from the human SK-RC-42 renal cell carcinoma cell line are enriched in cancer stem cells. Cancer Lett. 2010;299(2):150–60.PubMedCrossRef Zhong Y, Guan K, Guo S, Zhou C, Wang D, Ma W, Zhang Y, Li C, Zhang S. Spheres derived from the human SK-RC-42 renal cell carcinoma cell line are enriched in cancer stem cells. Cancer Lett. 2010;299(2):150–60.PubMedCrossRef
91.
go back to reference Sjolund J, Johansson M, Manna S, Norin C, Pietras A, Beckman S, Nilsson E, Ljungberg B, Axelson H. Suppression of renal cell carcinoma growth by inhibition of Notch signaling in vitro and in vivo. J Clin Invest. 2008;118(1):217–28.PubMedCrossRef Sjolund J, Johansson M, Manna S, Norin C, Pietras A, Beckman S, Nilsson E, Ljungberg B, Axelson H. Suppression of renal cell carcinoma growth by inhibition of Notch signaling in vitro and in vivo. J Clin Invest. 2008;118(1):217–28.PubMedCrossRef
92.
go back to reference Shin KH, Ku JL, Kim WH, Lee SE, Lee C, Kim SW, Park JG. Establishment and characterization of seven human renal cell carcinoma cell lines. BJU Int. 2000;85(1):130–8.PubMedCrossRef Shin KH, Ku JL, Kim WH, Lee SE, Lee C, Kim SW, Park JG. Establishment and characterization of seven human renal cell carcinoma cell lines. BJU Int. 2000;85(1):130–8.PubMedCrossRef
93.
go back to reference Tan X, He S, Han Y, Yu Y, Xiao J, Xu D, Wang G, Du Y, Chang W, Yin J, et al. Establishment and characterization of clear cell renal cell carcinoma cell lines with different metastatic potential from Chinese patients. Cancer Cell Int. 2013;13(1):20.PubMedPubMedCentralCrossRef Tan X, He S, Han Y, Yu Y, Xiao J, Xu D, Wang G, Du Y, Chang W, Yin J, et al. Establishment and characterization of clear cell renal cell carcinoma cell lines with different metastatic potential from Chinese patients. Cancer Cell Int. 2013;13(1):20.PubMedPubMedCentralCrossRef
94.
go back to reference Myszczyszyn A, Czarnecka AM, Matak D, Szymanski L, Lian F, Kornakiewicz A, Bartnik E, Kukwa W, Kieda C, Szczylik C. The Role of Hypoxia and Cancer Stem Cells in Renal Cell Carcinoma Pathogenesis. Stem Cell Rev. 2015;11(6):919–43.PubMedPubMedCentralCrossRef Myszczyszyn A, Czarnecka AM, Matak D, Szymanski L, Lian F, Kornakiewicz A, Bartnik E, Kukwa W, Kieda C, Szczylik C. The Role of Hypoxia and Cancer Stem Cells in Renal Cell Carcinoma Pathogenesis. Stem Cell Rev. 2015;11(6):919–43.PubMedPubMedCentralCrossRef
95.
go back to reference Czarnecka M, Cezary Szczylik A. Renal Cell Carcinoma Cancer Stem Cells as Therapeutic Targets. Curr Signal Transduction Ther. 2013;8(3):203–9.CrossRef Czarnecka M, Cezary Szczylik A. Renal Cell Carcinoma Cancer Stem Cells as Therapeutic Targets. Curr Signal Transduction Ther. 2013;8(3):203–9.CrossRef
96.
go back to reference Hasmim M, Bruno S, Azzi S, Gallerne C, Michel JG, Chiabotto G, Lecoz V, Romei C, Spaggiari GM, Pezzolo A, et al. Isolation and characterization of renal cancer stem cells from patient-derived xenografts. Oncotarget. 2016;7(13):15507–24.PubMed Hasmim M, Bruno S, Azzi S, Gallerne C, Michel JG, Chiabotto G, Lecoz V, Romei C, Spaggiari GM, Pezzolo A, et al. Isolation and characterization of renal cancer stem cells from patient-derived xenografts. Oncotarget. 2016;7(13):15507–24.PubMed
97.
go back to reference Lucarelli G, Galleggiante V, Rutigliano M, Vavallo A, Ditonno P, Battaglia M. Isolation and characterization of cancer stem cells in renal cell carcinoma. Urologia. 2015;82(1):46–53.PubMedCrossRef Lucarelli G, Galleggiante V, Rutigliano M, Vavallo A, Ditonno P, Battaglia M. Isolation and characterization of cancer stem cells in renal cell carcinoma. Urologia. 2015;82(1):46–53.PubMedCrossRef
98.
go back to reference Ueda K, Ogasawara S, Akiba J, Nakayama M, Todoroki K, Sanada S, Suekane S, Noguchi M, Matsuoka K, Yano H. Aldehyde dehydrogenase 1 identifies cells with cancer stem cell-like properties in a human renal cell carcinoma cell line. PLoS One. 2013;8(10):e75463.PubMedPubMedCentralCrossRef Ueda K, Ogasawara S, Akiba J, Nakayama M, Todoroki K, Sanada S, Suekane S, Noguchi M, Matsuoka K, Yano H. Aldehyde dehydrogenase 1 identifies cells with cancer stem cell-like properties in a human renal cell carcinoma cell line. PLoS One. 2013;8(10):e75463.PubMedPubMedCentralCrossRef
99.
go back to reference Wang L, Park P, La Marca F, Than KD, Lin CY. BMP-2 inhibits tumor-initiating ability in human renal cancer stem cells and induces bone formation. J Cancer Res Clin Oncol. 2015;141(6):1013–24.PubMedCrossRef Wang L, Park P, La Marca F, Than KD, Lin CY. BMP-2 inhibits tumor-initiating ability in human renal cancer stem cells and induces bone formation. J Cancer Res Clin Oncol. 2015;141(6):1013–24.PubMedCrossRef
100.
go back to reference Khan MI, Czarnecka AM, Helbrecht I, Bartnik E, Lian F, Szczylik C. Current approaches in identification and isolation of human renal cell carcinoma cancer stem cells. Stem Cell Res Ther. 2015;6:178.PubMedPubMedCentralCrossRef Khan MI, Czarnecka AM, Helbrecht I, Bartnik E, Lian F, Szczylik C. Current approaches in identification and isolation of human renal cell carcinoma cancer stem cells. Stem Cell Res Ther. 2015;6:178.PubMedPubMedCentralCrossRef
101.
go back to reference Bussolati B, Bruno S, Grange C, Ferrando U, Camussi G. Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 2008;22(10):3696–705.PubMedCrossRef Bussolati B, Bruno S, Grange C, Ferrando U, Camussi G. Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 2008;22(10):3696–705.PubMedCrossRef
102.
go back to reference Kim K, Park BH, Ihm H, Kim KM, Jeong J, Chang JW, Cho YM. Expression of stem cell marker CD133 in fetal and adult human kidneys and pauci-immune crescentic glomerulonephritis. Histol Histopathol. 2011;26(2):223–32.PubMed Kim K, Park BH, Ihm H, Kim KM, Jeong J, Chang JW, Cho YM. Expression of stem cell marker CD133 in fetal and adult human kidneys and pauci-immune crescentic glomerulonephritis. Histol Histopathol. 2011;26(2):223–32.PubMed
103.
go back to reference Wang D, Lu P, Zhang H, Luo M, Zhang X, Wei X, Gao J, Zhao Z, Liu C. Oct-4 and Nanog promote the epithelial-mesenchymal transition of breast cancer stem cells and are associated with poor prognosis in breast cancer patients. Oncotarget. 2014;5(21):10803–15.PubMedPubMedCentralCrossRef Wang D, Lu P, Zhang H, Luo M, Zhang X, Wei X, Gao J, Zhao Z, Liu C. Oct-4 and Nanog promote the epithelial-mesenchymal transition of breast cancer stem cells and are associated with poor prognosis in breast cancer patients. Oncotarget. 2014;5(21):10803–15.PubMedPubMedCentralCrossRef
104.
go back to reference Nishizawa S, Hirohashi Y, Torigoe T, Takahashi A, Tamura Y, Mori T, Kanaseki T, Kamiguchi K, Asanuma H, Morita R, et al. HSP DNAJB8 controls tumor-initiating ability in renal cancer stem-like cells. Cancer Res. 2012;72(11):2844–54.PubMedCrossRef Nishizawa S, Hirohashi Y, Torigoe T, Takahashi A, Tamura Y, Mori T, Kanaseki T, Kamiguchi K, Asanuma H, Morita R, et al. HSP DNAJB8 controls tumor-initiating ability in renal cancer stem-like cells. Cancer Res. 2012;72(11):2844–54.PubMedCrossRef
105.
go back to reference Lu J, Cui Y, Zhu J, He J, Zhou G, Yue Z. Biological characteristics of Rh123 stem-like cells in a side population of 786-O renal carcinoma cells. Oncol Lett. 2013;5(6):1903–8.PubMedPubMedCentral Lu J, Cui Y, Zhu J, He J, Zhou G, Yue Z. Biological characteristics of Rh123 stem-like cells in a side population of 786-O renal carcinoma cells. Oncol Lett. 2013;5(6):1903–8.PubMedPubMedCentral
106.
go back to reference Detrisac CJ, Sens MA, Garvin AJ, Spicer SS, Sens DA. Tissue culture of human kidney epithelial cells of proximal tubule origin. Kidney Int. 1984;25(2):383–90.PubMedCrossRef Detrisac CJ, Sens MA, Garvin AJ, Spicer SS, Sens DA. Tissue culture of human kidney epithelial cells of proximal tubule origin. Kidney Int. 1984;25(2):383–90.PubMedCrossRef
107.
go back to reference Valente MJ, Henrique R, Costa VL, Jeronimo C, Carvalho F, Bastos ML, de Pinho PG, Carvalho M. A rapid and simple procedure for the establishment of human normal and cancer renal primary cell cultures from surgical specimens. PLoS One. 2011;6(5):e19337.PubMedPubMedCentralCrossRef Valente MJ, Henrique R, Costa VL, Jeronimo C, Carvalho F, Bastos ML, de Pinho PG, Carvalho M. A rapid and simple procedure for the establishment of human normal and cancer renal primary cell cultures from surgical specimens. PLoS One. 2011;6(5):e19337.PubMedPubMedCentralCrossRef
108.
go back to reference Giron-Michel J, Azzi S, Khawam K, Mortier E, Caignard A, Devocelle A, Ferrini S, Croce M, Francois H, Lecru L, et al. Interleukin-15 plays a central role in human kidney physiology and cancer through the gammac signaling pathway. PLoS One. 2012;7(2):e31624.PubMedPubMedCentralCrossRef Giron-Michel J, Azzi S, Khawam K, Mortier E, Caignard A, Devocelle A, Ferrini S, Croce M, Francois H, Lecru L, et al. Interleukin-15 plays a central role in human kidney physiology and cancer through the gammac signaling pathway. PLoS One. 2012;7(2):e31624.PubMedPubMedCentralCrossRef
109.
go back to reference Baer PC, Bereiter-Hahn J, Schubert R, Geiger H. Differentiation status of human renal proximal and distal tubular epithelial cells in vitro: Differential expression of characteristic markers. Cells Tissues Organs. 2006;184(1):16–22.PubMedCrossRef Baer PC, Bereiter-Hahn J, Schubert R, Geiger H. Differentiation status of human renal proximal and distal tubular epithelial cells in vitro: Differential expression of characteristic markers. Cells Tissues Organs. 2006;184(1):16–22.PubMedCrossRef
110.
go back to reference Ryan MJ, Johnson G, Kirk J, Fuerstenberg SM, Zager RA, Torok-Storb B. HK- an immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int. 1994;45:48–57. 2 SRC - GoogleScholar.PubMedCrossRef Ryan MJ, Johnson G, Kirk J, Fuerstenberg SM, Zager RA, Torok-Storb B. HK- an immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int. 1994;45:48–57. 2 SRC - GoogleScholar.PubMedCrossRef
111.
go back to reference Wieser M, Stadler G, Jennings P, Streubel B, Pfaller W, Ambros P, Riedl C, Katinger H, Grillari J, Grillari-Voglauer R. hTERT alone immortalizes epithelial cells of renal proximal tubules without changing their functional characteristics. Am J Physiol Renal Physiol. 2008;295(5):F1365–75.PubMedCrossRef Wieser M, Stadler G, Jennings P, Streubel B, Pfaller W, Ambros P, Riedl C, Katinger H, Grillari J, Grillari-Voglauer R. hTERT alone immortalizes epithelial cells of renal proximal tubules without changing their functional characteristics. Am J Physiol Renal Physiol. 2008;295(5):F1365–75.PubMedCrossRef
112.
go back to reference Jenkinson SE, Chung GW, van Loon E, Bakar NS, Dalzell AM, Brown CD. The limitations of renal epithelial cell line HK-2 as a model of drug transporter expression and function in the proximal tubule. Pflugers Arch - Eur J Physiol. 2012;464(6):601–11.CrossRef Jenkinson SE, Chung GW, van Loon E, Bakar NS, Dalzell AM, Brown CD. The limitations of renal epithelial cell line HK-2 as a model of drug transporter expression and function in the proximal tubule. Pflugers Arch - Eur J Physiol. 2012;464(6):601–11.CrossRef
113.
go back to reference Tramonti G, Romiti N, Norpoth M, Chieli E. P-glycoprotein in HK-2 proximal tubule cell line. Ren Fail. 2001;23:331–7. SRC - GoogleScholar.PubMedCrossRef Tramonti G, Romiti N, Norpoth M, Chieli E. P-glycoprotein in HK-2 proximal tubule cell line. Ren Fail. 2001;23:331–7. SRC - GoogleScholar.PubMedCrossRef
114.
go back to reference Simon BR, Wilson MJ, Wickliffe JK. The RPTEC/TERT1 cell line models key renal cell responses to the environmental toxicants, benzo[a]pyrene and cadmium. Toxicol Rep. 2014;1:231–42.PubMedPubMedCentralCrossRef Simon BR, Wilson MJ, Wickliffe JK. The RPTEC/TERT1 cell line models key renal cell responses to the environmental toxicants, benzo[a]pyrene and cadmium. Toxicol Rep. 2014;1:231–42.PubMedPubMedCentralCrossRef
115.
go back to reference Handa RK. Characterization and Signaling of the AT4 Receptor in Human Proximal Tubule Epithelial (HK-2) Cells. J Am Soc Nephrol. 2001;12(3):440–9.PubMed Handa RK. Characterization and Signaling of the AT4 Receptor in Human Proximal Tubule Epithelial (HK-2) Cells. J Am Soc Nephrol. 2001;12(3):440–9.PubMed
116.
go back to reference Baba M, Hirai S, Kawakami S, Kishida T, Sakai N, Kaneko S, Yao M, Shuin T, Kubota Y, Hosaka M, et al. Tumor suppressor protein VHL is induced at high cell density and mediates contact inhibition of cell growth. Oncogene. 2001;20(22):2727–36.PubMedCrossRef Baba M, Hirai S, Kawakami S, Kishida T, Sakai N, Kaneko S, Yao M, Shuin T, Kubota Y, Hosaka M, et al. Tumor suppressor protein VHL is induced at high cell density and mediates contact inhibition of cell growth. Oncogene. 2001;20(22):2727–36.PubMedCrossRef
117.
go back to reference Graham FL, Smiley J, Russell WC, Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977;36(1):59–74.PubMedCrossRef Graham FL, Smiley J, Russell WC, Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977;36(1):59–74.PubMedCrossRef
118.
go back to reference Thomas P, Smart TG. HEK293 cell line: a vehicle for the expression of recombinant proteins. J Pharmacol Toxicol Methods. 2005;51(3):187–200.PubMedCrossRef Thomas P, Smart TG. HEK293 cell line: a vehicle for the expression of recombinant proteins. J Pharmacol Toxicol Methods. 2005;51(3):187–200.PubMedCrossRef
119.
go back to reference Madhusudana SN, Sundaramoorthy S, Ullas PT. Utility of human embryonic kidney cell line HEK-293 for rapid isolation of fixed and street rabies viruses: comparison with Neuro-2a and BHK-21 cell lines. Int J Infect Dis. 2010;14(12):e1067–71.PubMedCrossRef Madhusudana SN, Sundaramoorthy S, Ullas PT. Utility of human embryonic kidney cell line HEK-293 for rapid isolation of fixed and street rabies viruses: comparison with Neuro-2a and BHK-21 cell lines. Int J Infect Dis. 2010;14(12):e1067–71.PubMedCrossRef
120.
go back to reference Shaw G, Morse S, Ararat M, Graham FL. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 2002;16(8):869–71.PubMed Shaw G, Morse S, Ararat M, Graham FL. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 2002;16(8):869–71.PubMed
121.
go back to reference Ashokkumar B, Vaziri ND, Said HM. Thiamin uptake by the human-derived renal epithelial (HEK-293) cells: cellular and molecular mechanisms. Am J Physiol Renal Physiol. 2006;291(4):F796–805.PubMedCrossRef Ashokkumar B, Vaziri ND, Said HM. Thiamin uptake by the human-derived renal epithelial (HEK-293) cells: cellular and molecular mechanisms. Am J Physiol Renal Physiol. 2006;291(4):F796–805.PubMedCrossRef
122.
go back to reference Waly MI, Al Moundhri MS, Ali BH. Effect of Curcumin on Cisplatin-and Oxaliplatin-Induced Oxidative Stress in Human Embryonic Kidney (HEK) 293 Cells. Ren Fail 2011;33(5):518–23.PubMedCrossRef Waly MI, Al Moundhri MS, Ali BH. Effect of Curcumin on Cisplatin-and Oxaliplatin-Induced Oxidative Stress in Human Embryonic Kidney (HEK) 293 Cells. Ren Fail 2011;33(5):518–23.PubMedCrossRef
123.
go back to reference De Araujo Junior RF, Leitao Oliveira AL, de Melo Silveira RF, de Oliveira Rocha HA, de Franca Cavalcanti P, de Araujo AA. Telmisartan induces apoptosis and regulates Bcl-2 in human renal cancer cells. Exp Biol Med (Maywood). 2015;240(1):34–44.CrossRef De Araujo Junior RF, Leitao Oliveira AL, de Melo Silveira RF, de Oliveira Rocha HA, de Franca Cavalcanti P, de Araujo AA. Telmisartan induces apoptosis and regulates Bcl-2 in human renal cancer cells. Exp Biol Med (Maywood). 2015;240(1):34–44.CrossRef
124.
go back to reference Weber KL, Pathak S, Multani AS, Price JE. Characterization of a renal cell carcinoma cell line derived from a human bone metastasis and establishment of an experimental nude mouse model. J Urol. 2002;168(2):774–9.PubMedCrossRef Weber KL, Pathak S, Multani AS, Price JE. Characterization of a renal cell carcinoma cell line derived from a human bone metastasis and establishment of an experimental nude mouse model. J Urol. 2002;168(2):774–9.PubMedCrossRef
125.
go back to reference Avnet S, Cenni E, Granchi D, Perut F, Amato I, Battistelli L, Brandi ML, Giunti A, Baldini N. Isolation and characterization of a new cell line from a renal carcinoma bone metastasis. Anticancer Res. 2004;24(3a):1705–11.PubMed Avnet S, Cenni E, Granchi D, Perut F, Amato I, Battistelli L, Brandi ML, Giunti A, Baldini N. Isolation and characterization of a new cell line from a renal carcinoma bone metastasis. Anticancer Res. 2004;24(3a):1705–11.PubMed
126.
go back to reference Maita S, Yuasa T, Tsuchiya N, Mitobe Y, Narita S, Horikawa Y, Hatake K, Fukui I, Kimura S, Maekawa T, et al. Antitumor effect of sunitinib against skeletal metastatic renal cell carcinoma through inhibition of osteoclast function. Int J Cancer. 2012;130(3):677–84.PubMedCrossRef Maita S, Yuasa T, Tsuchiya N, Mitobe Y, Narita S, Horikawa Y, Hatake K, Fukui I, Kimura S, Maekawa T, et al. Antitumor effect of sunitinib against skeletal metastatic renal cell carcinoma through inhibition of osteoclast function. Int J Cancer. 2012;130(3):677–84.PubMedCrossRef
127.
go back to reference Weber KL1, Pathak S, Multani AS, Price JE. Characterization of a renal cell carcinoma cell line derived from a human bone metastasis and establishment of an experimental nude mouse model. J Urol 2002;168(2):774-9. Weber KL1, Pathak S, Multani AS, Price JE. Characterization of a renal cell carcinoma cell line derived from a human bone metastasis and establishment of an experimental nude mouse model. J Urol 2002;168(2):774-9.
128.
go back to reference Satcher RL, Pan T, Cheng CJ, Lee YC, Lin SC, Yu G, Li X, Hoang AG, Tamboli P, Jonasch E, et al. Cadherin-11 in renal cell carcinoma bone metastasis. PLoS One. 2014;9(2):e89880.PubMedPubMedCentralCrossRef Satcher RL, Pan T, Cheng CJ, Lee YC, Lin SC, Yu G, Li X, Hoang AG, Tamboli P, Jonasch E, et al. Cadherin-11 in renal cell carcinoma bone metastasis. PLoS One. 2014;9(2):e89880.PubMedPubMedCentralCrossRef
129.
go back to reference Yang Y, Valera V, Sourbier C, Vocke CD, Wei M, Pike L, Huang Y, Merino MA, Bratslavsky G, Wu M, et al. A novel fumarate hydratase-deficient HLRCC kidney cancer cell line, UOK268: a model of the Warburg effect in cancer. Cancer Genet. 2012;205(7-8):377–90.PubMedPubMedCentralCrossRef Yang Y, Valera V, Sourbier C, Vocke CD, Wei M, Pike L, Huang Y, Merino MA, Bratslavsky G, Wu M, et al. A novel fumarate hydratase-deficient HLRCC kidney cancer cell line, UOK268: a model of the Warburg effect in cancer. Cancer Genet. 2012;205(7-8):377–90.PubMedPubMedCentralCrossRef
130.
go back to reference Yang Y, Valera VA, Padilla-Nash HM, Sourbier C, Vocke CD, Vira MA, Abu-Asab MS, Bratslavsky G, Tsokos M, Merino MJ, et al. UOK 262: Fumarate Hydratase (-/-) Hereditary Leiomyomatosis Renal Cell Carcinoma: In Vitro and In Vivo Model of an Aberrant Energy Metabolic Pathway in Human Cancer. Cancer Genet Cytogenet. 2010;196(1):45–55.PubMedPubMedCentralCrossRef Yang Y, Valera VA, Padilla-Nash HM, Sourbier C, Vocke CD, Vira MA, Abu-Asab MS, Bratslavsky G, Tsokos M, Merino MJ, et al. UOK 262: Fumarate Hydratase (-/-) Hereditary Leiomyomatosis Renal Cell Carcinoma: In Vitro and In Vivo Model of an Aberrant Energy Metabolic Pathway in Human Cancer. Cancer Genet Cytogenet. 2010;196(1):45–55.PubMedPubMedCentralCrossRef
131.
go back to reference TCGAR Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013;499:43–9.CrossRef TCGAR Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013;499:43–9.CrossRef
132.
go back to reference Ricketts CJ, Morris MR, Gentle D, Shuib S, Brown M, Clarke N, Wei W, Nathan P, Latif F, Maher ER. Methylation profiling and evaluation of demethylating therapy in renal cell carcinoma. Clin Epigenetics. 2013;5:16.PubMedPubMedCentralCrossRef Ricketts CJ, Morris MR, Gentle D, Shuib S, Brown M, Clarke N, Wei W, Nathan P, Latif F, Maher ER. Methylation profiling and evaluation of demethylating therapy in renal cell carcinoma. Clin Epigenetics. 2013;5:16.PubMedPubMedCentralCrossRef
133.
go back to reference Pawlowski R, Muhl SM, Sulser T, Krek W, Moch H, Schraml P. Loss of PBRM1 expression is associated with renal cell carcinoma progression. Int J Cancer. 2013;132(2):E11–7.PubMedCrossRef Pawlowski R, Muhl SM, Sulser T, Krek W, Moch H, Schraml P. Loss of PBRM1 expression is associated with renal cell carcinoma progression. Int J Cancer. 2013;132(2):E11–7.PubMedCrossRef
135.
go back to reference Chowdhury B, Porter EG, Stewart JC, Ferreira CR, Schipma MJ, Dykhuizen EC. PBRM1 Regulates the Expression of Genes Involved in Metabolism and Cell Adhesion in Renal Clear Cell Carcinoma. PLoS One. 2016;11(4):e0153718.PubMedPubMedCentralCrossRef Chowdhury B, Porter EG, Stewart JC, Ferreira CR, Schipma MJ, Dykhuizen EC. PBRM1 Regulates the Expression of Genes Involved in Metabolism and Cell Adhesion in Renal Clear Cell Carcinoma. PLoS One. 2016;11(4):e0153718.PubMedPubMedCentralCrossRef
136.
go back to reference Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, Jia M, Shepherd R, Leung K, Menzies A, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 2011;39:D945–50.PubMedCrossRef Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, Jia M, Shepherd R, Leung K, Menzies A, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 2011;39:D945–50.PubMedCrossRef
137.
go back to reference Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, Davies H, Jones D, Lin ML, Teague J, et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature. 2011;469(7331):539–42.PubMedPubMedCentralCrossRef Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, Davies H, Jones D, Lin ML, Teague J, et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature. 2011;469(7331):539–42.PubMedPubMedCentralCrossRef
138.
go back to reference Peña-Llopis S, Vega-Rubín-de-Celis S, Liao A, Leng N, Pavía-Jiménez A, Wang S, Yamasaki T, Zhrebker L, Sivanand S, Spence P, et al. BAP1 loss defines a new class of renal cell carcinoma. Nat Genet. 2012;44:751–9.PubMedPubMedCentralCrossRef Peña-Llopis S, Vega-Rubín-de-Celis S, Liao A, Leng N, Pavía-Jiménez A, Wang S, Yamasaki T, Zhrebker L, Sivanand S, Spence P, et al. BAP1 loss defines a new class of renal cell carcinoma. Nat Genet. 2012;44:751–9.PubMedPubMedCentralCrossRef
139.
go back to reference Piva F, Santoni M, Matrana MR, Satti S, Giulietti M, Occhipinti G, Massari F, Cheng L, Lopez-Beltran A, Scarpelli M, Principato G, Cascinu S, Montironi R. BAP1, PBRM1 and SETD2 in clear-cell renal cell carcinoma: molecular diagnostics and possible targets for personalized therapies. Expert Rev Mol Diagn 2015;15(9):1201–10.PubMedCrossRef Piva F, Santoni M, Matrana MR, Satti S, Giulietti M, Occhipinti G, Massari F, Cheng L, Lopez-Beltran A, Scarpelli M, Principato G, Cascinu S, Montironi R. BAP1, PBRM1 and SETD2 in clear-cell renal cell carcinoma: molecular diagnostics and possible targets for personalized therapies. Expert Rev Mol Diagn 2015;15(9):1201–10.PubMedCrossRef
140.
go back to reference Feng C, Sun Y, Ding G, Wu Z, Jiang H, Wang L, Ding Q, Wen H. PI3Kβ Inhibitor TGX221 Selectively Inhibits Renal Cell Carcinoma Cells with Both VHL and SETD2 mutations and Links Multiple Pathways. Scientific Reports, Published online: 8 April 2015; | doi: 10.1038/srep09465 2015. Feng C, Sun Y, Ding G, Wu Z, Jiang H, Wang L, Ding Q, Wen H. PI3Kβ Inhibitor TGX221 Selectively Inhibits Renal Cell Carcinoma Cells with Both VHL and SETD2 mutations and Links Multiple Pathways. Scientific Reports, Published online: 8 April 2015; | doi: 10.​1038/​srep09465 2015.
141.
go back to reference Duns G, van den Berg E, van Duivenbode I, Osinga J, Hollema H, Hofstra RMW, Kok K. Histone Methyltransferase Gene SETD2 Is a Novel Tumor Suppressor Gene in Clear Cell Renal Cell Carcinoma. Cancer Res. 2010;70:4287–91.PubMedCrossRef Duns G, van den Berg E, van Duivenbode I, Osinga J, Hollema H, Hofstra RMW, Kok K. Histone Methyltransferase Gene SETD2 Is a Novel Tumor Suppressor Gene in Clear Cell Renal Cell Carcinoma. Cancer Res. 2010;70:4287–91.PubMedCrossRef
142.
go back to reference Dalgliesh GL, Furge K, Greenman C, Chen L, Bignell G, Butler A, Davies H, Edkins S, Hardy C, Latimer C, et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature. 2010;463(7279):360–3.PubMedPubMedCentralCrossRef Dalgliesh GL, Furge K, Greenman C, Chen L, Bignell G, Butler A, Davies H, Edkins S, Hardy C, Latimer C, et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature. 2010;463(7279):360–3.PubMedPubMedCentralCrossRef
143.
go back to reference Kanu N, Grönroos E, Martinez P, Burrell RA, Goh XY, Bartkova J, Maya-Mendoza A, Mistrík M, Rowan AJ, Patel H, et al. SETD2 loss-of-function promotes renal cancer branched evolution through replication stress and impaired DNA repair. Oncogene. 2015;34(46):5699–708.PubMedPubMedCentralCrossRef Kanu N, Grönroos E, Martinez P, Burrell RA, Goh XY, Bartkova J, Maya-Mendoza A, Mistrík M, Rowan AJ, Patel H, et al. SETD2 loss-of-function promotes renal cancer branched evolution through replication stress and impaired DNA repair. Oncogene. 2015;34(46):5699–708.PubMedPubMedCentralCrossRef
144.
go back to reference Li L, Shen C, Nakamura E, Ando K, Signoretti S, Beroukhim R, Cowley GS, Lizotte P, Liberzon E, Bair S, et al. SQSTM1 is a Pathogenic Target of 5q Copy Number Gains in Kidney Cancer. Cancer Cell. 2013;24(6):738–50.PubMedPubMedCentralCrossRef Li L, Shen C, Nakamura E, Ando K, Signoretti S, Beroukhim R, Cowley GS, Lizotte P, Liberzon E, Bair S, et al. SQSTM1 is a Pathogenic Target of 5q Copy Number Gains in Kidney Cancer. Cancer Cell. 2013;24(6):738–50.PubMedPubMedCentralCrossRef
145.
go back to reference Reiter RE, Anglard P, Liu S, Gnarra JR, Linehan WM. Chromosome 17p deletions and p53 mutations in renal cell carcinoma. Cancer Res. 1993;53(13):3092–7.PubMed Reiter RE, Anglard P, Liu S, Gnarra JR, Linehan WM. Chromosome 17p deletions and p53 mutations in renal cell carcinoma. Cancer Res. 1993;53(13):3092–7.PubMed
146.
go back to reference Strefford JC, Stasevich I, Lane TM, Lu YJ, Oliver T, Young BD. A combination of molecular cytogenetic analyses reveals complex genetic alterations in conventional renal cell carcinoma. Cancer Genet Cytogenet. 2005;159(1):1–9.PubMedCrossRef Strefford JC, Stasevich I, Lane TM, Lu YJ, Oliver T, Young BD. A combination of molecular cytogenetic analyses reveals complex genetic alterations in conventional renal cell carcinoma. Cancer Genet Cytogenet. 2005;159(1):1–9.PubMedCrossRef
147.
go back to reference Alimov A, Kost-Alimova M, Liu J, Li C, Bergerheim U, Imreh S, Klein G, Zabarovsky ER. Combined LOH/CGH analysis proves the existence of interstitial 3p deletions in renal cell carcinoma. Oncogene. 2000;19(11):1392–9.PubMedCrossRef Alimov A, Kost-Alimova M, Liu J, Li C, Bergerheim U, Imreh S, Klein G, Zabarovsky ER. Combined LOH/CGH analysis proves the existence of interstitial 3p deletions in renal cell carcinoma. Oncogene. 2000;19(11):1392–9.PubMedCrossRef
148.
go back to reference Network TCGAR: Comprehensive Molecular Characterization of Papillary Renal-Cell Carcinoma. http://dxdoiorg/101056/NEJMoa1505917 2016. Network TCGAR: Comprehensive Molecular Characterization of Papillary Renal-Cell Carcinoma. http://​dxdoiorg/​101056/​NEJMoa1505917 2016.
149.
go back to reference Lee YH, Morrison BL, Bottaro DP. Synergistic Signaling of Tumor Cell Invasiveness by Hepatocyte Growth Factor and Hypoxia*. J Biol Chem. 2014;289:20448–61.PubMedPubMedCentralCrossRef Lee YH, Morrison BL, Bottaro DP. Synergistic Signaling of Tumor Cell Invasiveness by Hepatocyte Growth Factor and Hypoxia*. J Biol Chem. 2014;289:20448–61.PubMedPubMedCentralCrossRef
150.
go back to reference Lee YH, Apolo AB, Agarwal PK, Bottaro DP. Characterization of HGF/Met Signaling in Cell Lines Derived From Urothelial Carcinoma of the Bladder. Cancers. 2014;6(4):2313–29.PubMedPubMedCentralCrossRef Lee YH, Apolo AB, Agarwal PK, Bottaro DP. Characterization of HGF/Met Signaling in Cell Lines Derived From Urothelial Carcinoma of the Bladder. Cancers. 2014;6(4):2313–29.PubMedPubMedCentralCrossRef
151.
go back to reference Gibney GT, Aziz SA, Camp RL, Conrad P, Schwartz BE, Chen CR, Kelly WK, Kluger HM. c-Met is a prognostic marker and potential therapeutic target in clear cell renal cell carcinoma. Ann Oncol. 2013;24(2):343–9.PubMedCrossRef Gibney GT, Aziz SA, Camp RL, Conrad P, Schwartz BE, Chen CR, Kelly WK, Kluger HM. c-Met is a prognostic marker and potential therapeutic target in clear cell renal cell carcinoma. Ann Oncol. 2013;24(2):343–9.PubMedCrossRef
152.
go back to reference Ibragimova I, Maradeo ME, Dulaimi E, Cairns P. Aberrant promoter hypermethylation of PBRM1, BAP1, SETD2, KDM6A and other chromatin-modifying genes is absent or rare in clear cell RCC. Epigenetics. 2013;8:486–93.PubMedPubMedCentralCrossRef Ibragimova I, Maradeo ME, Dulaimi E, Cairns P. Aberrant promoter hypermethylation of PBRM1, BAP1, SETD2, KDM6A and other chromatin-modifying genes is absent or rare in clear cell RCC. Epigenetics. 2013;8:486–93.PubMedPubMedCentralCrossRef
153.
go back to reference Shen C, Beroukhim R, Schumacher SE, Zhou J, Chang M, Signoretti S, Kaelin WG. Genetic and Functional Studies Implicate HIF1α as a 14q Kidney Cancer Suppressor Gene. Cancer Discov. 2011;1(3):222–35.PubMedPubMedCentralCrossRef Shen C, Beroukhim R, Schumacher SE, Zhou J, Chang M, Signoretti S, Kaelin WG. Genetic and Functional Studies Implicate HIF1α as a 14q Kidney Cancer Suppressor Gene. Cancer Discov. 2011;1(3):222–35.PubMedPubMedCentralCrossRef
154.
go back to reference Girgin C, Tarhan H, Hekimgil M, Sezer A, Gurel G. P53 mutations and other prognostic factors of renal cell carcinoma. Urol Int. 2001;66(2):78–83.PubMedCrossRef Girgin C, Tarhan H, Hekimgil M, Sezer A, Gurel G. P53 mutations and other prognostic factors of renal cell carcinoma. Urol Int. 2001;66(2):78–83.PubMedCrossRef
155.
go back to reference Abaan OD, Polley EC, Davis SR, Zhu YJ, Bilke S, Walker RL, Pineda M, Gindin Y, Jiang Y, Reinhold WC, et al. The Exomes of the NCI-60 Panel: a Genomic Resource for Cancer Biology and Systems Pharmacology. Cancer Res. 2013;73(14):4372–82.PubMedPubMedCentralCrossRef Abaan OD, Polley EC, Davis SR, Zhu YJ, Bilke S, Walker RL, Pineda M, Gindin Y, Jiang Y, Reinhold WC, et al. The Exomes of the NCI-60 Panel: a Genomic Resource for Cancer Biology and Systems Pharmacology. Cancer Res. 2013;73(14):4372–82.PubMedPubMedCentralCrossRef
156.
go back to reference Tomita Y, Bilim V, Kawasaki T, Takahashi K, Okan I, Magnusson KP, Wiman KG. Frequent expression of Bcl-2 in renal-cell carcinomas carrying wild-type p53. Int J Cancer. 1996;66(3):322–5.PubMedCrossRef Tomita Y, Bilim V, Kawasaki T, Takahashi K, Okan I, Magnusson KP, Wiman KG. Frequent expression of Bcl-2 in renal-cell carcinomas carrying wild-type p53. Int J Cancer. 1996;66(3):322–5.PubMedCrossRef
157.
go back to reference Noon AP, Vlatković N, Polański R, Maguire M, Shawki H, Parsons K, Boyd MT. p53 and MDM2 in Renal Cell Carcinoma: Biomarkers for Disease Progression and Future Therapeutic Targets? Cancer. 2010;116(4):780–90.PubMedPubMedCentralCrossRef Noon AP, Vlatković N, Polański R, Maguire M, Shawki H, Parsons K, Boyd MT. p53 and MDM2 in Renal Cell Carcinoma: Biomarkers for Disease Progression and Future Therapeutic Targets? Cancer. 2010;116(4):780–90.PubMedPubMedCentralCrossRef
158.
go back to reference Zigeuner R, Ratschek M, Rehak P, Schips L, Langner C. Value of p53 as a prognostic marker in histologic subtypes of renal cell carcinoma: a systematic analysis of primary and metastatic tumor tissue. Urology. 2004;63(4):651–5.PubMedCrossRef Zigeuner R, Ratschek M, Rehak P, Schips L, Langner C. Value of p53 as a prognostic marker in histologic subtypes of renal cell carcinoma: a systematic analysis of primary and metastatic tumor tissue. Urology. 2004;63(4):651–5.PubMedCrossRef
159.
go back to reference Warburton HE, Brady M, Vlatković N, Linehan WM, Parsons K, Boyd MT. p53 Regulation and Function in Renal Cell Carcinoma. Cancer Res. 2005;65:6498–503.PubMedCrossRef Warburton HE, Brady M, Vlatković N, Linehan WM, Parsons K, Boyd MT. p53 Regulation and Function in Renal Cell Carcinoma. Cancer Res. 2005;65:6498–503.PubMedCrossRef
160.
go back to reference Galbán S, Martindale JL, Mazan-Mamczarz K, de Silanes López I, Fan J, Wang W, Decker J, Gorospe M. Influence of the RNA-Binding Protein HuR in pVHL-Regulated p53 Expression in Renal Carcinoma Cells. Mol Cell Biol. 2003;23:7083–95.PubMedPubMedCentralCrossRef Galbán S, Martindale JL, Mazan-Mamczarz K, de Silanes López I, Fan J, Wang W, Decker J, Gorospe M. Influence of the RNA-Binding Protein HuR in pVHL-Regulated p53 Expression in Renal Carcinoma Cells. Mol Cell Biol. 2003;23:7083–95.PubMedPubMedCentralCrossRef
161.
go back to reference Flanagan SP. ‘Nude’, a new hairless gene with pleiotropic effects in the mouse. Genet Res. 1966;8(3):295–309.PubMedCrossRef Flanagan SP. ‘Nude’, a new hairless gene with pleiotropic effects in the mouse. Genet Res. 1966;8(3):295–309.PubMedCrossRef
162.
go back to reference Bosma MJ, Carroll AM. The SCID mouse mutant: definition, characterization, and potential uses. Annu Rev Immunol. 1991;9:323–50.PubMedCrossRef Bosma MJ, Carroll AM. The SCID mouse mutant: definition, characterization, and potential uses. Annu Rev Immunol. 1991;9:323–50.PubMedCrossRef
163.
go back to reference Morton CL, Houghton PJ. Establishment of human tumor xenografts in immunodeficient mice. Nat Protoc. 2007;2(2):247–50.PubMedCrossRef Morton CL, Houghton PJ. Establishment of human tumor xenografts in immunodeficient mice. Nat Protoc. 2007;2(2):247–50.PubMedCrossRef
164.
go back to reference Taghian A, Budach W, Zietman A, Freeman J, Gioioso D, Ruka W, Suit HD. Quantitative comparison between the transplantability of human and murine tumors into the subcutaneous tissue of NCr/Sed-nu/nu nude and severe combined immunodeficient mice. Cancer Res. 1993;53(20):5012–7.PubMed Taghian A, Budach W, Zietman A, Freeman J, Gioioso D, Ruka W, Suit HD. Quantitative comparison between the transplantability of human and murine tumors into the subcutaneous tissue of NCr/Sed-nu/nu nude and severe combined immunodeficient mice. Cancer Res. 1993;53(20):5012–7.PubMed
165.
go back to reference Budhu S, Wolchok J, Merghoub T. The importance of animal models in tumor immunity and immunotherapy. Curr Opin Genet Dev. 2014;24:46–51.PubMedCrossRef Budhu S, Wolchok J, Merghoub T. The importance of animal models in tumor immunity and immunotherapy. Curr Opin Genet Dev. 2014;24:46–51.PubMedCrossRef
166.
go back to reference An Z, Jiang P, Wang X, Moossa AR, Hoffman RM. Development of a high metastatic orthotopic model of human renal cell carcinoma in nude mice: benefits of fragment implantation compared to cell-suspension injection. Clin Exp Metastasis. 1999;17(3):265–70.PubMedCrossRef An Z, Jiang P, Wang X, Moossa AR, Hoffman RM. Development of a high metastatic orthotopic model of human renal cell carcinoma in nude mice: benefits of fragment implantation compared to cell-suspension injection. Clin Exp Metastasis. 1999;17(3):265–70.PubMedCrossRef
167.
go back to reference Naito S, von Eschenbach AC, Giavazzi R, Fidler IJ. Growth and metastasis of tumor cells isolated from a human renal cell carcinoma implanted into different organs of nude mice. Cancer Res. 1986;46(8):4109–15.PubMed Naito S, von Eschenbach AC, Giavazzi R, Fidler IJ. Growth and metastasis of tumor cells isolated from a human renal cell carcinoma implanted into different organs of nude mice. Cancer Res. 1986;46(8):4109–15.PubMed
168.
go back to reference Ruggeri BA, Camp F, Miknyoczki S. Animal models of disease: pre-clinical animal models of cancer and their applications and utility in drug discovery. Biochem Pharmacol. 2014;87(1):150–61.PubMedCrossRef Ruggeri BA, Camp F, Miknyoczki S. Animal models of disease: pre-clinical animal models of cancer and their applications and utility in drug discovery. Biochem Pharmacol. 2014;87(1):150–61.PubMedCrossRef
169.
go back to reference Chapman DW, Jans HS, Ma I, Mercer JR, Wiebe LI, Wuest M, Moore RB. Detecting functional changes with [(18)F]FAZA in a renal cell carcinoma mouse model following sunitinib therapy. EJNMMI Res. 2014;4(1):27–0027.PubMedPubMedCentralCrossRef Chapman DW, Jans HS, Ma I, Mercer JR, Wiebe LI, Wuest M, Moore RB. Detecting functional changes with [(18)F]FAZA in a renal cell carcinoma mouse model following sunitinib therapy. EJNMMI Res. 2014;4(1):27–0027.PubMedPubMedCentralCrossRef
170.
go back to reference Dos Santos C, Tijeras-Raballand A, Serova M, Sebbagh S, Slimane K, Faivre S, de Gramont A, Raymond E. Effects of preset sequential administrations of sunitinib and everolimus on tumour differentiation in Caki-1 renal cell carcinoma. Br J Cancer. 2015;112(1):86–94.PubMedCrossRef Dos Santos C, Tijeras-Raballand A, Serova M, Sebbagh S, Slimane K, Faivre S, de Gramont A, Raymond E. Effects of preset sequential administrations of sunitinib and everolimus on tumour differentiation in Caki-1 renal cell carcinoma. Br J Cancer. 2015;112(1):86–94.PubMedCrossRef
171.
go back to reference Joshi S, Singh AR, Durden DL. Pan-PI-3 kinase inhibitor SF1126 shows antitumor and antiangiogenic activity in renal cell carcinoma. Cancer Chemother Pharmacol. 2015;75(3):595–608.PubMedCrossRef Joshi S, Singh AR, Durden DL. Pan-PI-3 kinase inhibitor SF1126 shows antitumor and antiangiogenic activity in renal cell carcinoma. Cancer Chemother Pharmacol. 2015;75(3):595–608.PubMedCrossRef
172.
go back to reference Wu P, Zhang N, Wang X, Zhang C, Li T, Ning X, Gong K. The erythropoietin/erythropoietin receptor signaling pathway promotes growth and invasion abilities in human renal carcinoma cells. PLoS One. 2012;7(9):e45122. doi:10.1371/journal.pone.0045122. Wu P, Zhang N, Wang X, Zhang C, Li T, Ning X, Gong K. The erythropoietin/erythropoietin receptor signaling pathway promotes growth and invasion abilities in human renal carcinoma cells. PLoS One. 2012;7(9):e45122. doi:10.​1371/​journal.​pone.​0045122.
173.
go back to reference Valta MP1, Zhao H, Ingels A, Thong AE, Nolley R, Saar M, Peehl DM. Development of a realistic in vivo bone metastasis model of human renal cell carcinoma. Clin Exp Metastasis 2014;31(5):573-84. doi:10.1007/s10585-014-9651-8. Valta MP1, Zhao H, Ingels A, Thong AE, Nolley R, Saar M, Peehl DM. Development of a realistic in vivo bone metastasis model of human renal cell carcinoma. Clin Exp Metastasis 2014;31(5):573-84. doi:10.​1007/​s10585-014-9651-8.
174.
go back to reference Beniers AJ, Peelen WP, Schaafsma HE, Beck JL, Ramaekers FC, Debruyne FM, Schalken JA. Establishment and characterization of five new human renal tumor xenografts. Am J Pathol. 1992;140(2):483–95.PubMedPubMedCentral Beniers AJ, Peelen WP, Schaafsma HE, Beck JL, Ramaekers FC, Debruyne FM, Schalken JA. Establishment and characterization of five new human renal tumor xenografts. Am J Pathol. 1992;140(2):483–95.PubMedPubMedCentral
175.
go back to reference Sharkey FE, Fogh J. Metastasis of human tumors in athymic nude mice. Int J Cancer. 1979;24(6):733–8.PubMedCrossRef Sharkey FE, Fogh J. Metastasis of human tumors in athymic nude mice. Int J Cancer. 1979;24(6):733–8.PubMedCrossRef
176.
go back to reference Garofalo A, Chirivi RG, Scanziani E, Mayo JG, Vecchi A, Giavazzi R. Comparative study on the metastatic behavior of human tumors in nude, beige/nude/xid and severe combined immunodeficient mice. Invasion Metastasis. 1993;13(2):82–91.PubMed Garofalo A, Chirivi RG, Scanziani E, Mayo JG, Vecchi A, Giavazzi R. Comparative study on the metastatic behavior of human tumors in nude, beige/nude/xid and severe combined immunodeficient mice. Invasion Metastasis. 1993;13(2):82–91.PubMed
177.
go back to reference Kobayashi M, Morita T, Chun NA, Matsui A, Takahashi M, Murakami T. Effect of host immunity on metastatic potential in renal cell carcinoma: the assessment of optimal in vivo models to study metastatic behavior of renal cancer cells. Tumour Biol. 2012;33(2):551–9.PubMedCrossRef Kobayashi M, Morita T, Chun NA, Matsui A, Takahashi M, Murakami T. Effect of host immunity on metastatic potential in renal cell carcinoma: the assessment of optimal in vivo models to study metastatic behavior of renal cancer cells. Tumour Biol. 2012;33(2):551–9.PubMedCrossRef
178.
go back to reference Bear A, Clayman RV, Elbers J, Limas C, Wang N, Stone K, Gebhard R, Prigge W, Palmer J. Characterization of two human cell lines (TK-10, TK-164) of renal cell cancer. Cancer Res. 1987;47(14):3856–62.PubMed Bear A, Clayman RV, Elbers J, Limas C, Wang N, Stone K, Gebhard R, Prigge W, Palmer J. Characterization of two human cell lines (TK-10, TK-164) of renal cell cancer. Cancer Res. 1987;47(14):3856–62.PubMed
179.
go back to reference Grossman HB, Wedemeyer G, Ren LQ. Human renal carcinoma: characterization of five new cell lines. J Surg Oncol. 1985;28(3):237–44.PubMedCrossRef Grossman HB, Wedemeyer G, Ren LQ. Human renal carcinoma: characterization of five new cell lines. J Surg Oncol. 1985;28(3):237–44.PubMedCrossRef
180.
go back to reference van Moorselaar RJA, Schalken JA, Oosterhof GON, Debruyne FMJ. Use of animal models in diagnosis and treatment of renal cell carcinoma. World J Urol. 1991;9(4):192–7.CrossRef van Moorselaar RJA, Schalken JA, Oosterhof GON, Debruyne FMJ. Use of animal models in diagnosis and treatment of renal cell carcinoma. World J Urol. 1991;9(4):192–7.CrossRef
181.
go back to reference Pan C, Kumar C, Bohl S, Klingmueller U, Mann M. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol Cell Proteomics. 2009;8(3):443–50.PubMedPubMedCentralCrossRef Pan C, Kumar C, Bohl S, Klingmueller U, Mann M. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol Cell Proteomics. 2009;8(3):443–50.PubMedPubMedCentralCrossRef
183.
go back to reference Hughes P, Marshall D, Reid Y, Parkes H, Gelber C. The costs of using unauthenticated, over-passaged cell lines: how much more data do we need? BioTechniques. 2007;43(5):575. 577-578, 581-572 passim.PubMedCrossRef Hughes P, Marshall D, Reid Y, Parkes H, Gelber C. The costs of using unauthenticated, over-passaged cell lines: how much more data do we need? BioTechniques. 2007;43(5):575. 577-578, 581-572 passim.PubMedCrossRef
184.
go back to reference Ertel A, Verghese A, Byers SW, Ochs M, Tozeren A. Pathway-specific differences between tumor cell lines and normal and tumor tissue cells. Mol Cancer. 2006;5(1):55.PubMedPubMedCentralCrossRef Ertel A, Verghese A, Byers SW, Ochs M, Tozeren A. Pathway-specific differences between tumor cell lines and normal and tumor tissue cells. Mol Cancer. 2006;5(1):55.PubMedPubMedCentralCrossRef
185.
go back to reference Park JG, Ku JL, Park SY. Isolation and culture of renal cancer cell lines. Methods Mol Med. 2004;88:111–9.PubMed Park JG, Ku JL, Park SY. Isolation and culture of renal cancer cell lines. Methods Mol Med. 2004;88:111–9.PubMed
186.
go back to reference Batchelder CA, Martinez ML, Duru N, Meyers FJ, Tarantal AF. Three Dimensional Culture of Human Renal Cell Carcinoma Organoids. PLoS One. 2015;10(8):e0136758.PubMedPubMedCentralCrossRef Batchelder CA, Martinez ML, Duru N, Meyers FJ, Tarantal AF. Three Dimensional Culture of Human Renal Cell Carcinoma Organoids. PLoS One. 2015;10(8):e0136758.PubMedPubMedCentralCrossRef
188.
go back to reference Steffens S, Janssen M, Roos FC, Becker F, Schumacher S, Seidel C, Wegener G, Thuroff JW, Hofmann R, Stockle M, et al. Incidence and long-term prognosis of papillary compared to clear cell renal cell carcinoma--a multicentre study. Eur J Cancer. 2012;48(15):2347–52.PubMedCrossRef Steffens S, Janssen M, Roos FC, Becker F, Schumacher S, Seidel C, Wegener G, Thuroff JW, Hofmann R, Stockle M, et al. Incidence and long-term prognosis of papillary compared to clear cell renal cell carcinoma--a multicentre study. Eur J Cancer. 2012;48(15):2347–52.PubMedCrossRef
189.
go back to reference Thoma CR, Zimmermann M, Agarkova I, Kelm JM, Krek W. 3D cell culture systems modeling tumor growth determinants in cancer target discovery. Adv Drug Deliv Rev. 2014;69–70:29–41.PubMedCrossRef Thoma CR, Zimmermann M, Agarkova I, Kelm JM, Krek W. 3D cell culture systems modeling tumor growth determinants in cancer target discovery. Adv Drug Deliv Rev. 2014;69–70:29–41.PubMedCrossRef
190.
go back to reference Bielecka ZF, Maliszewska-Olejniczak K, Safir IJ, Szczylik C, Czarnecka AM. Three-dimensional cell culture model utilization in cancer stem cell research. Biol Rev Camb Philos Soc. 2016. doi: 10.1111/brv.12293 Bielecka ZF, Maliszewska-Olejniczak K, Safir IJ, Szczylik C, Czarnecka AM. Three-dimensional cell culture model utilization in cancer stem cell research. Biol Rev Camb Philos Soc. 2016. doi: 10.​1111/​brv.​12293
191.
go back to reference Pickl M, Ries CH. Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene. 2009;28(3):461–8.PubMedCrossRef Pickl M, Ries CH. Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene. 2009;28(3):461–8.PubMedCrossRef
192.
go back to reference Krausz E, de Hoogt R, Gustin E, Cornelissen F, Grand-Perret T, Janssen L, Vloemans N, Wuyts D, Frans S, Axel A, et al. Translation of a tumor microenvironment mimicking 3D tumor growth co-culture assay platform to high-content screening. J Biomol Screen. 2013;18(1):54–66.PubMedCrossRef Krausz E, de Hoogt R, Gustin E, Cornelissen F, Grand-Perret T, Janssen L, Vloemans N, Wuyts D, Frans S, Axel A, et al. Translation of a tumor microenvironment mimicking 3D tumor growth co-culture assay platform to high-content screening. J Biomol Screen. 2013;18(1):54–66.PubMedCrossRef
193.
go back to reference Geraghty RJ, Capes-Davis A, Davis JM, Downward J, Freshney RI, Knezevic I, Lovell-Badge R, Masters JR, Meredith J, Stacey GN, et al. Guidelines for the use of cell lines in biomedical research. Br J Cancer. 2014;111(6):1021–46.PubMedPubMedCentralCrossRef Geraghty RJ, Capes-Davis A, Davis JM, Downward J, Freshney RI, Knezevic I, Lovell-Badge R, Masters JR, Meredith J, Stacey GN, et al. Guidelines for the use of cell lines in biomedical research. Br J Cancer. 2014;111(6):1021–46.PubMedPubMedCentralCrossRef
Metadata
Title
Choosing the right cell line for renal cell cancer research
Authors
Klaudia K. Brodaczewska
Cezary Szczylik
Michal Fiedorowicz
Camillo Porta
Anna M. Czarnecka
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2016
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-016-0565-8

Other articles of this Issue 1/2016

Molecular Cancer 1/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine