Mitochondrial PIWI-interacting RNAs are novel biomarkers for clear cell renal cell carcinoma

go back to reference Ljungberg B, Campbell SC, Choi HY, Jacqmin D, Lee JE, Weikert S, Kiemeney LA (2011) The epidemiology of renal cell carcinoma. Eur Urol 60(4):615–621. https://doi.org/10.1016/j.eururo.2011.06.049 CrossRefPubMed Ljungberg B, Campbell SC, Choi HY, Jacqmin D, Lee JE, Weikert S, Kiemeney LA (2011) The epidemiology of renal cell carcinoma. Eur Urol 60(4):615–621. https://​doi.​org/​10.​1016/​j.​eururo.​2011.​06.​049 CrossRefPubMed

go back to reference Capitanio U, Cloutier V, Zini L, Isbarn H, Jeldres C, Shariat SF, Perrotte P, Antebi E, Patard JJ, Montorsi F, Karakiewicz PI (2009) A critical assessment of the prognostic value of clear cell, papillary and chromophobe histological subtypes in renal cell carcinoma: a population-based study. BJU Int 103(11):1496–1500. https://doi.org/10.1111/j.1464-410X.2008.08259.x CrossRef Capitanio U, Cloutier V, Zini L, Isbarn H, Jeldres C, Shariat SF, Perrotte P, Antebi E, Patard JJ, Montorsi F, Karakiewicz PI (2009) A critical assessment of the prognostic value of clear cell, papillary and chromophobe histological subtypes in renal cell carcinoma: a population-based study. BJU Int 103(11):1496–1500. https://​doi.​org/​10.​1111/​j.​1464-410X.​2008.​08259.​x CrossRef

go back to reference Johnson DC, Vukina J, Smith AB, Meyer AM, Wheeler SB, Kuo TM, Tan HJ, Woods ME, Raynor MC, Wallen EM, Pruthi RS, Nielsen ME (2015) Preoperatively misclassified, surgically removed benign renal masses: a systematic review of surgical series and United States population level burden estimate. J Urol 193(1):30–35. https://doi.org/10.1016/j.juro.2014.07.102 CrossRefPubMed Johnson DC, Vukina J, Smith AB, Meyer AM, Wheeler SB, Kuo TM, Tan HJ, Woods ME, Raynor MC, Wallen EM, Pruthi RS, Nielsen ME (2015) Preoperatively misclassified, surgically removed benign renal masses: a systematic review of surgical series and United States population level burden estimate. J Urol 193(1):30–35. https://​doi.​org/​10.​1016/​j.​juro.​2014.​07.​102 CrossRefPubMed

go back to reference Dabestani S, Marconi L, Kuusk T, Bex A (2018) Follow-up after curative treatment of localised renal cell carcinoma. World J Urol. https://doi.org/10.1007/s00345-018-2338-z CrossRefPubMed Dabestani S, Marconi L, Kuusk T, Bex A (2018) Follow-up after curative treatment of localised renal cell carcinoma. World J Urol. https://​doi.​org/​10.​1007/​s00345-018-2338-z CrossRefPubMed

go back to reference Choueiri TK, Motzer RJ (2017) Systemic therapy for metastatic renal-cell carcinoma. N Engl J Med 376(4):354–366. https://doi.org/10.1056/NEJMra1601333 CrossRefPubMed Choueiri TK, Motzer RJ (2017) Systemic therapy for metastatic renal-cell carcinoma. N Engl J Med 376(4):354–366. https://​doi.​org/​10.​1056/​NEJMra1601333 CrossRefPubMed

go back to reference Klatte T, Rossi SH, Stewart GD (2018) Prognostic factors and prognostic models for renal cell carcinoma: a literature review. World J Urol. https://doi.org/10.1007/s00345-018-2309-4 CrossRefPubMedPubMedCentral Klatte T, Rossi SH, Stewart GD (2018) Prognostic factors and prognostic models for renal cell carcinoma: a literature review. World J Urol. https://​doi.​org/​10.​1007/​s00345-018-2309-4 CrossRefPubMedPubMedCentral

go back to reference Sullenger BA, Nair S (2016) From the RNA world to the clinic. Science 352(6292):1417–1420. https://doi.org/10.1126/science.aad8709 CrossRefPubMedPubMedCentral Sullenger BA, Nair S (2016) From the RNA world to the clinic. Science 352(6292):1417–1420. https://​doi.​org/​10.​1126/​science.​aad8709 CrossRefPubMedPubMedCentral

go back to reference Ng KW, Anderson C, Marshall EA, Minatel BC, Enfield KS, Saprunoff HL, Lam WL, Martinez VD (2016) Piwi-interacting RNAs in cancer: emerging functions and clinical utility. Mol Cancer 15:5. https://doi.org/10.1186/s12943-016-0491-9 CrossRefPubMedPubMedCentral Ng KW, Anderson C, Marshall EA, Minatel BC, Enfield KS, Saprunoff HL, Lam WL, Martinez VD (2016) Piwi-interacting RNAs in cancer: emerging functions and clinical utility. Mol Cancer 15:5. https://​doi.​org/​10.​1186/​s12943-016-0491-9 CrossRefPubMedPubMedCentral

go back to reference Kwon C, Tak H, Rho M, Chang HR, Kim YH, Kim KT, Balch C, Lee EK, Nam S (2014) Detection of PIWI and piRNAs in the mitochondria of mammalian cancer cells. Biochem Biophys Res Commun 446(1):218–223. https://doi.org/10.1016/j.bbrc.2014.02.112 CrossRefPubMed Kwon C, Tak H, Rho M, Chang HR, Kim YH, Kim KT, Balch C, Lee EK, Nam S (2014) Detection of PIWI and piRNAs in the mitochondria of mammalian cancer cells. Biochem Biophys Res Commun 446(1):218–223. https://​doi.​org/​10.​1016/​j.​bbrc.​2014.​02.​112 CrossRefPubMed

go back to reference Chung IF, Chang SJ, Chen CY, Liu SH, Li CY, Chan CH, Shih CC, Cheng WC (2017) YM500v3: a database for small RNA sequencing in human cancer research. Nucleic Acids Res 45(D1):D925–D931. https://doi.org/10.1093/nar/gkw1084 CrossRefPubMed Chung IF, Chang SJ, Chen CY, Liu SH, Li CY, Chan CH, Shih CC, Cheng WC (2017) YM500v3: a database for small RNA sequencing in human cancer research. Nucleic Acids Res 45(D1):D925–D931. https://​doi.​org/​10.​1093/​nar/​gkw1084 CrossRefPubMed

go back to reference Blondeau JJ, Deng M, Syring I, Schrodter S, Schmidt D, Perner S, Muller SC, Ellinger J (2015) Identification of novel long non-coding RNAs in clear cell renal cell carcinoma. Clin epigenet 7:10. https://doi.org/10.1186/s13148-015-0047-7 CrossRef Blondeau JJ, Deng M, Syring I, Schrodter S, Schmidt D, Perner S, Muller SC, Ellinger J (2015) Identification of novel long non-coding RNAs in clear cell renal cell carcinoma. Clin epigenet 7:10. https://​doi.​org/​10.​1186/​s13148-015-0047-7 CrossRef

go back to reference Zhao C, Tolkach Y, Schmidt D, Kristiansen G, Muller SC, Ellinger J (2018) 5′-tRNA halves are dysregulated in clear cell renal cell carcinoma. J Urol 199(2):378–383. https://doi.org/10.1016/j.juro.2017.07.082 CrossRefPubMed Zhao C, Tolkach Y, Schmidt D, Kristiansen G, Muller SC, Ellinger J (2018) 5′-tRNA halves are dysregulated in clear cell renal cell carcinoma. J Urol 199(2):378–383. https://​doi.​org/​10.​1016/​j.​juro.​2017.​07.​082 CrossRefPubMed

go back to reference Suzuki R, Honda S, Kirino Y (2012) PIWI expression and function in cancer. Front Genet 3:204. https://doi.org/10.3389/fgene.2012.00204 CrossRefPubMedPubMedCentral Suzuki R, Honda S, Kirino Y (2012) PIWI expression and function in cancer. Front Genet 3:204. https://​doi.​org/​10.​3389/​fgene.​2012.​00204 CrossRefPubMedPubMedCentral

go back to reference Watanabe T, Lin H (2014) Posttranscriptional regulation of gene expression by Piwi proteins and piRNAs. Mol Cell 56(1):18–27. https://doi.org/10.1016/j.molcel.2014.09.012 CrossRefPubMedPubMedCentral Watanabe T, Lin H (2014) Posttranscriptional regulation of gene expression by Piwi proteins and piRNAs. Mol Cell 56(1):18–27. https://​doi.​org/​10.​1016/​j.​molcel.​2014.​09.​012 CrossRefPubMedPubMedCentral

go back to reference Fu A, Jacobs DI, Hoffman AE, Zheng T, Zhu Y (2015) PIWI-interacting RNA 021285 is involved in breast tumorigenesis possibly by remodeling the cancer epigenome. Carcinogenesis 36(10):1094–1102. https://doi.org/10.1093/carcin/bgv105 CrossRefPubMedPubMedCentral Fu A, Jacobs DI, Hoffman AE, Zheng T, Zhu Y (2015) PIWI-interacting RNA 021285 is involved in breast tumorigenesis possibly by remodeling the cancer epigenome. Carcinogenesis 36(10):1094–1102. https://​doi.​org/​10.​1093/​carcin/​bgv105 CrossRefPubMedPubMedCentral

go back to reference Yin H, Lin H (2007) An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450(7167):304–308. https://doi.org/10.1038/nature06263 CrossRefPubMed Yin H, Lin H (2007) An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450(7167):304–308. https://​doi.​org/​10.​1038/​nature06263 CrossRefPubMed

go back to reference Yang OC, Maxwell PH, Pollard PJ (2013) Renal cell carcinoma: translational aspects of metabolism and therapeutic consequences. Kidney Int 84(4):667–681. https://doi.org/10.1038/ki.2013.245 CrossRefPubMed Yang OC, Maxwell PH, Pollard PJ (2013) Renal cell carcinoma: translational aspects of metabolism and therapeutic consequences. Kidney Int 84(4):667–681. https://​doi.​org/​10.​1038/​ki.​2013.​245 CrossRefPubMed

go back to reference Martinez VD, Vucic EA, Thu KL, Hubaux R, Enfield KS, Pikor LA, Becker-Santos DD, Brown CJ, Lam S, Lam WL (2015) Unique somatic and malignant expression patterns implicate PIWI-interacting RNAs in cancer-type specific biology. Sci Rep 5:10423. https://doi.org/10.1038/srep10423 CrossRefPubMedPubMedCentral Martinez VD, Vucic EA, Thu KL, Hubaux R, Enfield KS, Pikor LA, Becker-Santos DD, Brown CJ, Lam S, Lam WL (2015) Unique somatic and malignant expression patterns implicate PIWI-interacting RNAs in cancer-type specific biology. Sci Rep 5:10423. https://​doi.​org/​10.​1038/​srep10423 CrossRefPubMedPubMedCentral

go back to reference Li Y, Wu X, Gao H, Jin JM, Li AX, Kim YS, Pal SK, Nelson RA, Lau CM, Guo C, Mu B, Wang J, Wang F, Wang J, Zhao Y, Chen W, Rossi JJ, Weiss LM, Wu H (2015) Piwi-interacting RNAs (piRNAs) are dysregulated in renal cell carcinoma and associated with tumor metastasis and cancer-specific survival. Mol Med 21:381–388. https://doi.org/10.2119/molmed.2014.00203 CrossRefPubMedPubMedCentral Li Y, Wu X, Gao H, Jin JM, Li AX, Kim YS, Pal SK, Nelson RA, Lau CM, Guo C, Mu B, Wang J, Wang F, Wang J, Zhao Y, Chen W, Rossi JJ, Weiss LM, Wu H (2015) Piwi-interacting RNAs (piRNAs) are dysregulated in renal cell carcinoma and associated with tumor metastasis and cancer-specific survival. Mol Med 21:381–388. https://​doi.​org/​10.​2119/​molmed.​2014.​00203 CrossRefPubMedPubMedCentral

go back to reference Busch J, Ralla B, Jung M, Wotschofsky Z, Trujillo-Arribas E, Schwabe P, Kilic E, Fendler A, Jung K (2015) Piwi-interacting RNAs as novel prognostic markers in clear cell renal cell carcinomas. J Exp Clin Cancer Res 34:61. https://doi.org/10.1186/s13046-015-0180-3 CrossRefPubMedPubMedCentral Busch J, Ralla B, Jung M, Wotschofsky Z, Trujillo-Arribas E, Schwabe P, Kilic E, Fendler A, Jung K (2015) Piwi-interacting RNAs as novel prognostic markers in clear cell renal cell carcinomas. J Exp Clin Cancer Res 34:61. https://​doi.​org/​10.​1186/​s13046-015-0180-3 CrossRefPubMedPubMedCentral

go back to reference Iliev R, Fedorko M, Machackova T, Mlcochova H, Svoboda M, Pacik D, Dolezel J, Stanik M, Slaby O (2016) Expression levels of PIWI-interacting RNA, piR-823, are deregulated in tumor tissue, blood serum and urine of patients with renal cell carcinoma. Anticancer Res 36(12):6419–6423. https://doi.org/10.21873/anticanres.11239 CrossRefPubMed Iliev R, Fedorko M, Machackova T, Mlcochova H, Svoboda M, Pacik D, Dolezel J, Stanik M, Slaby O (2016) Expression levels of PIWI-interacting RNA, piR-823, are deregulated in tumor tissue, blood serum and urine of patients with renal cell carcinoma. Anticancer Res 36(12):6419–6423. https://​doi.​org/​10.​21873/​anticanres.​11239 CrossRefPubMed

go back to reference Dietrich D, Meller S, Uhl B, Ralla B, Stephan C, Jung K, Ellinger J, Kristiansen G (2014) Nucleic acid-based tissue biomarkers of urologic malignancies. Crit Rev Clin Lab Sci 51(4):173–199. https://doi.org/10.3109/10408363.2014.906130 CrossRefPubMed Dietrich D, Meller S, Uhl B, Ralla B, Stephan C, Jung K, Ellinger J, Kristiansen G (2014) Nucleic acid-based tissue biomarkers of urologic malignancies. Crit Rev Clin Lab Sci 51(4):173–199. https://​doi.​org/​10.​3109/​10408363.​2014.​906130 CrossRefPubMed

go back to reference Turajlic S, Xu H, Litchfield K, Rowan A, Horswell S, Chambers T, O’Brien T, Lopez JI, Watkins TBK, Nicol D, Stares M, Challacombe B, Hazell S, Chandra A, Mitchell TJ, Au L, Eichler-Jonsson C, Jabbar F, Soultati A, Chowdhury S, Rudman S, Lynch J, Fernando A, Stamp G, Nye E, Stewart A, Xing W, Smith JC, Escudero M, Huffman A, Matthews N, Elgar G, Phillimore B, Costa M, Begum S, Ward S, Salm M, Boeing S, Fisher R, Spain L, Navas C, Gronroos E, Hobor S, Sharma S, Aurangzeb I, Lall S, Polson A, Varia M, Horsfield C, Fotiadis N, Pickering L, Schwarz RF, Silva B, Herrero J, Luscombe NM, Jamal-Hanjani M, Rosenthal R, Birkbak NJ, Wilson GA, Pipek O, Ribli D, Krzystanek M, Csabai I, Szallasi Z, Gore M, McGranahan N, Van Loo P, Campbell P, Larkin J, Swanton C, TRACERx Renal Consortium (2018) Deterministic evolutionary trajectories influence primary tumor growth: TRACERx renal. Cell 173(3):595–610. https://doi.org/10.1016/j.cell.2018.03.043 CrossRefPubMedPubMedCentral Turajlic S, Xu H, Litchfield K, Rowan A, Horswell S, Chambers T, O’Brien T, Lopez JI, Watkins TBK, Nicol D, Stares M, Challacombe B, Hazell S, Chandra A, Mitchell TJ, Au L, Eichler-Jonsson C, Jabbar F, Soultati A, Chowdhury S, Rudman S, Lynch J, Fernando A, Stamp G, Nye E, Stewart A, Xing W, Smith JC, Escudero M, Huffman A, Matthews N, Elgar G, Phillimore B, Costa M, Begum S, Ward S, Salm M, Boeing S, Fisher R, Spain L, Navas C, Gronroos E, Hobor S, Sharma S, Aurangzeb I, Lall S, Polson A, Varia M, Horsfield C, Fotiadis N, Pickering L, Schwarz RF, Silva B, Herrero J, Luscombe NM, Jamal-Hanjani M, Rosenthal R, Birkbak NJ, Wilson GA, Pipek O, Ribli D, Krzystanek M, Csabai I, Szallasi Z, Gore M, McGranahan N, Van Loo P, Campbell P, Larkin J, Swanton C, TRACERx Renal Consortium (2018) Deterministic evolutionary trajectories influence primary tumor growth: TRACERx renal. Cell 173(3):595–610. https://​doi.​org/​10.​1016/​j.​cell.​2018.​03.​043 CrossRefPubMedPubMedCentral

go back to reference Saeed K, Ojamies P, Pellinen T, Eldfors S, Turkki R, Lundin J, Jarvinen P, Nisen H, Taari K, af Hallstrom TM, Rannikko A, Mirtti T, Kallioniemi O, Ostling P (2018) Clonal heterogeneity influences drug responsiveness in renal cancer assessed by ex vivo drug testing of multiple patient-derived cancer cells. Int J Cancer. https://doi.org/10.1002/ijc.31815 CrossRefPubMed Saeed K, Ojamies P, Pellinen T, Eldfors S, Turkki R, Lundin J, Jarvinen P, Nisen H, Taari K, af Hallstrom TM, Rannikko A, Mirtti T, Kallioniemi O, Ostling P (2018) Clonal heterogeneity influences drug responsiveness in renal cancer assessed by ex vivo drug testing of multiple patient-derived cancer cells. Int J Cancer. https://​doi.​org/​10.​1002/​ijc.​31815 CrossRefPubMed