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Published in: Diagnostic Pathology 1/2017

Open Access 01-12-2017 | Research

Evaluation of the correlation of vasculogenic mimicry, ALDH1, KiSS-1, and MACC1 in the prediction of metastasis and prognosis in ovarian carcinoma

Authors: Lan Yu, Bo Zhu, Shiwu Wu, Lei Zhou, Wenqing Song, Xiaomeng Gong, Danna Wang

Published in: Diagnostic Pathology | Issue 1/2017

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Abstract

Background

Recurrence and metastasis are the usual manifestations of treatment failure of epithelial ovarian carcinoma (EOC). Vasculogenic mimicry (VM; blood supply development often seen in highly aggressive cancers), aldehyde dehydrogenase 1 (ALDH1, cancer stem cell biomarker), KiSS-1 (suppressor of tumor metastasis), and metastasis associated in colon cancer-1 (MACC1) are all useful predictive factors for metastasis and prognosis in various cancers. In this study, we analyzed associations among VM, ALDH1, KiSS-1, and MACC1 in EOC, and their respective correlations with clinicopathological characteristics and survival in EOC.

Methods

Positive rates of VM, ALDH1, KiSS-1, and MACC1 in 207 whole EOC tissue samples were detected by immunohistochemistry. Patients’ clinical data were also collected.

Results

Levels of VM, ALDH1, and MACC1 were significantly higher, and levels of KiSS-1 significantly lower, in EOC tissues than in benign ovary tumors. Levels of VM, ALDH1, KiSS-1, and MACC1 were associated significantly with tumor/lymph node/metastasis (LNM) grade, implantation, and International Federation of Gynecology and Obstetrics (FIGO) stage, and with patients’ overall survival (OS); whereas the KiSS-1+ subgroup had significantly longer OS than did the KiSS-1− subgroup. In multivariate analysis, high VM, ALDH1 or MACC1 levels, FIGO stage, implantation and low KiSS-1 levels were independently associated with shorter OS in patients with EOC.

Conclusions

VM and expressions of ALDH1, KiSS-1, and MACC1 represent promising markers for metastasis and prognosis, and potential therapeutic targets for EOC.
Literature
1.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.CrossRefPubMed Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.CrossRefPubMed
2.
go back to reference Liu Y, Song N, Ren K, Meng S, Xie Y, Long Q, Chen X, Zhao X. Expression loss and revivification of RhoB gene in ovary carcinoma carcinogenesis and development. PLoS One. 2013;8:e78477.CrossRef Liu Y, Song N, Ren K, Meng S, Xie Y, Long Q, Chen X, Zhao X. Expression loss and revivification of RhoB gene in ovary carcinoma carcinogenesis and development. PLoS One. 2013;8:e78477.CrossRef
3.
go back to reference Parking DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer. 2001;94:153–6.CrossRef Parking DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer. 2001;94:153–6.CrossRef
4.
go back to reference Kaku T, Ogawa S, Kawano Y, Ohishi Y, Kobayashi H, Hirakawa T, Nakano H. Histological classification of ovarian cancer. Med Electron Microsc. 2003;36:9–17.CrossRefPubMed Kaku T, Ogawa S, Kawano Y, Ohishi Y, Kobayashi H, Hirakawa T, Nakano H. Histological classification of ovarian cancer. Med Electron Microsc. 2003;36:9–17.CrossRefPubMed
5.
go back to reference Vredenburgh JJ, Desjardins A, Herndon IIJE, Dowell JM, Reardon DA, Quinn JA, Rich JN, Sathornsumetee S, Gururangan S, Wagner M, Bigner DD, Friedman AH, Friedman HS. Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res. 2007;13:1253–9.CrossRefPubMed Vredenburgh JJ, Desjardins A, Herndon IIJE, Dowell JM, Reardon DA, Quinn JA, Rich JN, Sathornsumetee S, Gururangan S, Wagner M, Bigner DD, Friedman AH, Friedman HS. Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res. 2007;13:1253–9.CrossRefPubMed
6.
go back to reference Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe’er J, Trent JM, Meltzer PS, Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999;155:739–52.CrossRefPubMedPubMedCentral Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe’er J, Trent JM, Meltzer PS, Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999;155:739–52.CrossRefPubMedPubMedCentral
7.
go back to reference Zhang JT, Sun W, Zhang WZ, Ge CY, Liu ZY, Zhao ZM, Lu XS, Fan YZ. Norcantharidin inhibits tumor growth and vasculogenic mimicry of human gallbladder carcinomas by suppression of the PI3-K/MMPs/Ln-5γ2 signaling pathway. BMC Cancer. 2014;14:193.CrossRefPubMedPubMedCentral Zhang JT, Sun W, Zhang WZ, Ge CY, Liu ZY, Zhao ZM, Lu XS, Fan YZ. Norcantharidin inhibits tumor growth and vasculogenic mimicry of human gallbladder carcinomas by suppression of the PI3-K/MMPs/Ln-5γ2 signaling pathway. BMC Cancer. 2014;14:193.CrossRefPubMedPubMedCentral
8.
go back to reference Wu S, Yu L, Wang D, Zhou L, Cheng Z, Chai D, Ma L, Tao Y. Aberrant expression of CD133 in non-small cell lung cancer and its relationship to vasculogenic mimicry. BMC Cancer. 2012;12:535.CrossRefPubMedPubMedCentral Wu S, Yu L, Wang D, Zhou L, Cheng Z, Chai D, Ma L, Tao Y. Aberrant expression of CD133 in non-small cell lung cancer and its relationship to vasculogenic mimicry. BMC Cancer. 2012;12:535.CrossRefPubMedPubMedCentral
9.
go back to reference Xu X, Yang L, Zheng L, Pan Y, Cao Z, Zhang Z, Zhou Q, Yang B, Cao C. Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses vasculogenic mimicry and proliferation of highly aggressive pancreatic cancer PaTu8988 cells. BMC Cancer. 2014;14:373.CrossRefPubMedPubMedCentral Xu X, Yang L, Zheng L, Pan Y, Cao Z, Zhang Z, Zhou Q, Yang B, Cao C. Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses vasculogenic mimicry and proliferation of highly aggressive pancreatic cancer PaTu8988 cells. BMC Cancer. 2014;14:373.CrossRefPubMedPubMedCentral
10.
go back to reference Mao JM, Liu J, Guo G, Mao XG, Li CX. Glioblastoma vasculogenic mimicry: signaling pathways progression and potential anti-angiogenesis targets. Biomarker Res. 2015;3:8.CrossRef Mao JM, Liu J, Guo G, Mao XG, Li CX. Glioblastoma vasculogenic mimicry: signaling pathways progression and potential anti-angiogenesis targets. Biomarker Res. 2015;3:8.CrossRef
11.
go back to reference Wang L, Lin L, Chen X, Sun L, Liao Y, Huang N, Liao W. Metastasis-associated in colon cancer-1 promotes vasculogenic mimicry in gastric cancer by upregulating Twist1/2. Oncotarget. 2015;6:11492–506.CrossRefPubMedPubMedCentral Wang L, Lin L, Chen X, Sun L, Liao Y, Huang N, Liao W. Metastasis-associated in colon cancer-1 promotes vasculogenic mimicry in gastric cancer by upregulating Twist1/2. Oncotarget. 2015;6:11492–506.CrossRefPubMedPubMedCentral
12.
go back to reference Zhao N, Sun BC, Zhao XL, Wang Y, Meng J, Che N, Dong XY, Gu Q. Role of Bcl-2 and its associated miRNAs in vasculogenic mimicry of hepatocellular carcinoma. Int J Clin Exp Pathol. 2015;8:15759–68.PubMedPubMedCentral Zhao N, Sun BC, Zhao XL, Wang Y, Meng J, Che N, Dong XY, Gu Q. Role of Bcl-2 and its associated miRNAs in vasculogenic mimicry of hepatocellular carcinoma. Int J Clin Exp Pathol. 2015;8:15759–68.PubMedPubMedCentral
13.
go back to reference Tang NN, Zhu H, Zhang HJ, Zhang WF, Jin HL, Wang L, Wang P, Hu GJ, Hao B, Shi RH. HIF-1αinduces VE-cadherin expression and modulates vasculogenic mimicry in esophageal carcinoma cells. World J Gastroenterol. 2014;20:17894–904.PubMedPubMedCentral Tang NN, Zhu H, Zhang HJ, Zhang WF, Jin HL, Wang L, Wang P, Hu GJ, Hao B, Shi RH. HIF-1αinduces VE-cadherin expression and modulates vasculogenic mimicry in esophageal carcinoma cells. World J Gastroenterol. 2014;20:17894–904.PubMedPubMedCentral
14.
15.
go back to reference Alison MR, Islan S, Wright NA. Stem cells in cancer: instigators and propagators? J Cell Sci. 2010;123:2357–68.CrossRefPubMed Alison MR, Islan S, Wright NA. Stem cells in cancer: instigators and propagators? J Cell Sci. 2010;123:2357–68.CrossRefPubMed
17.
go back to reference Kim IG, Lee JH, Kim SY, Kim JY, Cho EW. Fibulin-3 negatively regulates ALDH1 via c-MET suppression and increases c-radiation-induced sensitivity in some pancreatic cancer cell lines. Biochem Biophy Res Commun. 2014;454:369–75.CrossRef Kim IG, Lee JH, Kim SY, Kim JY, Cho EW. Fibulin-3 negatively regulates ALDH1 via c-MET suppression and increases c-radiation-induced sensitivity in some pancreatic cancer cell lines. Biochem Biophy Res Commun. 2014;454:369–75.CrossRef
18.
19.
go back to reference Huo W, Du M, Pan X, Zhu X, Li Z. Prognostic value of ALDH1 expression in lung cancer: a meta-analysis. Int J Clin Exp Med. 2015;8(2):2045–51.PubMedPubMedCentral Huo W, Du M, Pan X, Zhu X, Li Z. Prognostic value of ALDH1 expression in lung cancer: a meta-analysis. Int J Clin Exp Med. 2015;8(2):2045–51.PubMedPubMedCentral
20.
go back to reference Ayub TH, Kewer-Paik MD, Debald M, Rostamzadeh B, Thiesler T, Schröder L, Barchet W, Abramian A, Kaiser C, Kristiansen G, Kuhn W, Kübler K. Accumulation of ALDH1-positive cells after neoadjuvant chemotherapy predicts treatment resistance and prognosticates poor outcome in ovarian cancer. Oncotarget. 2015;6(18):16437–48.CrossRefPubMedPubMedCentral Ayub TH, Kewer-Paik MD, Debald M, Rostamzadeh B, Thiesler T, Schröder L, Barchet W, Abramian A, Kaiser C, Kristiansen G, Kuhn W, Kübler K. Accumulation of ALDH1-positive cells after neoadjuvant chemotherapy predicts treatment resistance and prognosticates poor outcome in ovarian cancer. Oncotarget. 2015;6(18):16437–48.CrossRefPubMedPubMedCentral
21.
go back to reference Grosse-Wilde A, Fouquier d’Hérouël A, McIntosh E, Ertaylan G, Skupin A, Kuestner RE, del Sol A, Walters KA, Huang S. Stemness of the bybrid epithelial/mesenchymal state in breast cancer and its association with poor prognosis. PLoS One. 2015;10:e0126522.CrossRefPubMedPubMedCentral Grosse-Wilde A, Fouquier d’Hérouël A, McIntosh E, Ertaylan G, Skupin A, Kuestner RE, del Sol A, Walters KA, Huang S. Stemness of the bybrid epithelial/mesenchymal state in breast cancer and its association with poor prognosis. PLoS One. 2015;10:e0126522.CrossRefPubMedPubMedCentral
22.
go back to reference Welch DR, Chen P, Miele ME, McGary CT, Bower JM, Stanbridge EJ, Weissman BE. Microcell-mediated transfer of chromosome 6 into metastatic human C8161 melanoma cells suppresses metastasis but does not inhibit tumorigenicity. Oncogene. 1994;9(1):255–62.PubMed Welch DR, Chen P, Miele ME, McGary CT, Bower JM, Stanbridge EJ, Weissman BE. Microcell-mediated transfer of chromosome 6 into metastatic human C8161 melanoma cells suppresses metastasis but does not inhibit tumorigenicity. Oncogene. 1994;9(1):255–62.PubMed
23.
go back to reference Babwah AV, Pampillo M, Min L, Kaiser UB, Bhattacharya M. Single-cell analyses reveal that KISS1R-expressing cells undergo sustained kisspeptin-induced signaling that is dependent upon an influx of extracellular Ca2+. Endocrinology. 2012;153:5875–87.CrossRefPubMedPubMedCentral Babwah AV, Pampillo M, Min L, Kaiser UB, Bhattacharya M. Single-cell analyses reveal that KISS1R-expressing cells undergo sustained kisspeptin-induced signaling that is dependent upon an influx of extracellular Ca2+. Endocrinology. 2012;153:5875–87.CrossRefPubMedPubMedCentral
24.
go back to reference Sanchez-Carbayo M, Capodieci P, Cordon-Cardo C. Tumor suppressor role of KiSS-1 in bladder cancer: lose of KiSS-1 expression is association with bladder cancer progression and clinical outcome. Am J Pathol. 2003;162:609–17.CrossRefPubMedPubMedCentral Sanchez-Carbayo M, Capodieci P, Cordon-Cardo C. Tumor suppressor role of KiSS-1 in bladder cancer: lose of KiSS-1 expression is association with bladder cancer progression and clinical outcome. Am J Pathol. 2003;162:609–17.CrossRefPubMedPubMedCentral
25.
go back to reference Quevedo EG, Aguilar GM, Aguilar LA, Rubio SA, Martínez SE, Rodríguez IP, Corona JS, Morán MI, Gómez RC, Moguel MC. Polymorphisms rs12998 and rs5780218 in KiSS1 suppressor metastasis gene in Mexican patients with breast cancer. Dis Markers. 2015;2015:365845.PubMed Quevedo EG, Aguilar GM, Aguilar LA, Rubio SA, Martínez SE, Rodríguez IP, Corona JS, Morán MI, Gómez RC, Moguel MC. Polymorphisms rs12998 and rs5780218 in KiSS1 suppressor metastasis gene in Mexican patients with breast cancer. Dis Markers. 2015;2015:365845.PubMed
26.
go back to reference Yu G, Chen Y, Ni C, Wang G, Qian J, Wang J. Reduced protein expression of metastasis- related genes (nm23, KISS1, KAI1 and p53)in lymph node and liver metastases of gastric cancer. Int J Exp Pathol. 2007;88:175–83.CrossRef Yu G, Chen Y, Ni C, Wang G, Qian J, Wang J. Reduced protein expression of metastasis- related genes (nm23, KISS1, KAI1 and p53)in lymph node and liver metastases of gastric cancer. Int J Exp Pathol. 2007;88:175–83.CrossRef
27.
go back to reference Stein U, Walther W, Arlt F, Schwabe H, Smith J, Fichtner I, Birchmeier W, Schlag PM. MACC1, a newly identified key regulator of HGF-MET signaling, predicts colon cancer metastasis. Nat Med. 2009;15:59–67.CrossRefPubMed Stein U, Walther W, Arlt F, Schwabe H, Smith J, Fichtner I, Birchmeier W, Schlag PM. MACC1, a newly identified key regulator of HGF-MET signaling, predicts colon cancer metastasis. Nat Med. 2009;15:59–67.CrossRefPubMed
28.
go back to reference Stein U, Smith J, Walther W, Arlt F. MACC1 controls Met: what a difference an Sp1 site makes. Cell Cycle. 2009;8:2467–9.CrossRefPubMed Stein U, Smith J, Walther W, Arlt F. MACC1 controls Met: what a difference an Sp1 site makes. Cell Cycle. 2009;8:2467–9.CrossRefPubMed
29.
go back to reference Wang L, Wu Y, Lin L, Liu P, Huang H, Liao W, Zheng D, Zuo Q, Sun L, Huang N, Shi M, Liao Y, Liao W. Metastasis-associated in colon cancer-1 upregulation predicts a poor prognosis of gastric cancer, and promotes tumor cell proliferation and invasion. Int J Cancer. 2013;133:1419–30.CrossRefPubMed Wang L, Wu Y, Lin L, Liu P, Huang H, Liao W, Zheng D, Zuo Q, Sun L, Huang N, Shi M, Liao Y, Liao W. Metastasis-associated in colon cancer-1 upregulation predicts a poor prognosis of gastric cancer, and promotes tumor cell proliferation and invasion. Int J Cancer. 2013;133:1419–30.CrossRefPubMed
30.
go back to reference Koelzer VH, Herrmann P, Zlobec I, Karamitopoulou E, Luqli A, Stein U. Heterogeneity analysis of metastasis associated in colon cancer 1 (MACC1) for survival prognosis of colorectal cancer patients: a retrospective cohort study. BMC Cancer. 2015;15:160.CrossRefPubMedPubMedCentral Koelzer VH, Herrmann P, Zlobec I, Karamitopoulou E, Luqli A, Stein U. Heterogeneity analysis of metastasis associated in colon cancer 1 (MACC1) for survival prognosis of colorectal cancer patients: a retrospective cohort study. BMC Cancer. 2015;15:160.CrossRefPubMedPubMedCentral
31.
go back to reference Chundong G, Uramoto H, Onitsuka T, Shimokawa H, Iwanami T, Nakagawa M, Oyama T, Tanaka F. Molecular diagnosis of MACC1 status in lung adenocarcinoma by immunohistochemical analysis. Anticancer Res. 2011;31:1141–5.PubMed Chundong G, Uramoto H, Onitsuka T, Shimokawa H, Iwanami T, Nakagawa M, Oyama T, Tanaka F. Molecular diagnosis of MACC1 status in lung adenocarcinoma by immunohistochemical analysis. Anticancer Res. 2011;31:1141–5.PubMed
32.
go back to reference Yue WY, Chen ZP. Does vasculogenic mimicry exist in astrocytoma? J Histochem Cytochem. 2005;53:997–1002.CrossRefPubMed Yue WY, Chen ZP. Does vasculogenic mimicry exist in astrocytoma? J Histochem Cytochem. 2005;53:997–1002.CrossRefPubMed
33.
go back to reference Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Viñals F, Inoue M, Bergers G, Hanahan D, Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15:220–31.CrossRefPubMedPubMedCentral Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Viñals F, Inoue M, Bergers G, Hanahan D, Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15:220–31.CrossRefPubMedPubMedCentral
34.
go back to reference Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009;15:232–9.CrossRefPubMedPubMedCentral Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009;15:232–9.CrossRefPubMedPubMedCentral
35.
go back to reference Liu X, Wang JH, Li S, Li LL, Huang M, Zhang YH, Liu Y, Yang YT, Ding R, Ke YQ. Histone deacetylase 3 expression correlates with vasculogenic mimicry through the phosphoinositide3 –kinase/ERK-MMP-laminin5γ2 signaling pathway. Cancer Sci. 2015;106:857–66.CrossRefPubMedPubMedCentral Liu X, Wang JH, Li S, Li LL, Huang M, Zhang YH, Liu Y, Yang YT, Ding R, Ke YQ. Histone deacetylase 3 expression correlates with vasculogenic mimicry through the phosphoinositide3 –kinase/ERK-MMP-laminin5γ2 signaling pathway. Cancer Sci. 2015;106:857–66.CrossRefPubMedPubMedCentral
36.
go back to reference Qi H, Sun B, Zhao X, Du J, Gu Q, Liu Y, Cheng R, Dong X. Wnt5αpromotes vasculogenic mimicry and epithelial-mesenchymal transition via protein kinase Cαin epithelial ovarian cancer. Oncol Rep. 2014;32:771–9.PubMed Qi H, Sun B, Zhao X, Du J, Gu Q, Liu Y, Cheng R, Dong X. Wnt5αpromotes vasculogenic mimicry and epithelial-mesenchymal transition via protein kinase Cαin epithelial ovarian cancer. Oncol Rep. 2014;32:771–9.PubMed
37.
go back to reference Januchowski R, Wojtowicz K, Zabel M. The role of aldehyde dehydrogenase (ALDH) in cancer drug resistance. Biomed Pharmacother. 2013;67:669–80.CrossRefPubMed Januchowski R, Wojtowicz K, Zabel M. The role of aldehyde dehydrogenase (ALDH) in cancer drug resistance. Biomed Pharmacother. 2013;67:669–80.CrossRefPubMed
38.
go back to reference Shen JX, Liu J, Li GW, Huang YT, Wu HT. Mining distinct aldehyde dehydrogenase 1 (ALDH1) isoenzyme in gastric cancer. Oncotarget. 2016;7:25340–9.PubMedPubMedCentral Shen JX, Liu J, Li GW, Huang YT, Wu HT. Mining distinct aldehyde dehydrogenase 1 (ALDH1) isoenzyme in gastric cancer. Oncotarget. 2016;7:25340–9.PubMedPubMedCentral
39.
go back to reference Shao C, Sullivan JP, Girard L, Augustyn A, Yenerall P, Rodriguez-Canales J, Liu H, Behrens C, Shay JW, Wistuba II, Minna JD. Essential role of aldehyde dehydrogenase 1A3 for the maintenance of non-small cell lung cancer stem cells is associated with the STAT3 pathway. Clin Cancer Res. 2014;20:4154–66.CrossRefPubMedPubMedCentral Shao C, Sullivan JP, Girard L, Augustyn A, Yenerall P, Rodriguez-Canales J, Liu H, Behrens C, Shay JW, Wistuba II, Minna JD. Essential role of aldehyde dehydrogenase 1A3 for the maintenance of non-small cell lung cancer stem cells is associated with the STAT3 pathway. Clin Cancer Res. 2014;20:4154–66.CrossRefPubMedPubMedCentral
40.
go back to reference Kuroda T, Hirohashi Y, Torigoe T, Yasuda K, Takhashi A, Asanuma H, Morita R, Mariya T, Asano T, Mizuuchi M, Saito T, Sato M. ALDH1-high ovarian cancer stem-like cells can be isolated from serous and clear cell adenocarcinoma cells, and ALDH1 high expression is associated with poor prognosis. PLoS One. 2013;8:e65158.CrossRefPubMedPubMedCentral Kuroda T, Hirohashi Y, Torigoe T, Yasuda K, Takhashi A, Asanuma H, Morita R, Mariya T, Asano T, Mizuuchi M, Saito T, Sato M. ALDH1-high ovarian cancer stem-like cells can be isolated from serous and clear cell adenocarcinoma cells, and ALDH1 high expression is associated with poor prognosis. PLoS One. 2013;8:e65158.CrossRefPubMedPubMedCentral
41.
go back to reference Jiang Y, Berk M, Singh LS, Tan H, Yin L, Powell CT, Xu Y. KiSS1 suppresses metastasis in human ovarian cancer via inhibition of protein kinase C alpha. Clin Exp Metastasis. 2005;22:369–76.CrossRefPubMed Jiang Y, Berk M, Singh LS, Tan H, Yin L, Powell CT, Xu Y. KiSS1 suppresses metastasis in human ovarian cancer via inhibition of protein kinase C alpha. Clin Exp Metastasis. 2005;22:369–76.CrossRefPubMed
42.
go back to reference Schmid F, Burock S, Klockmeier K, Schlag PM, Stein U. SNPs in the coding region of the metastasis-inducing gene MACC1 and clinical outcome in colorectal cancer. Mol Cancer. 2012;11:49.CrossRefPubMedPubMedCentral Schmid F, Burock S, Klockmeier K, Schlag PM, Stein U. SNPs in the coding region of the metastasis-inducing gene MACC1 and clinical outcome in colorectal cancer. Mol Cancer. 2012;11:49.CrossRefPubMedPubMedCentral
43.
go back to reference Li H, Zhang H, Zhao S, Shi Y, Yao J, Zhang Y, Guo H, Liu X. Overexpression of MACC1 and the association hepatocyte growth factor/c-Met in epithelial ovarian cancer. Oncol Lett. 2015;9:1989–96.PubMedPubMedCentral Li H, Zhang H, Zhao S, Shi Y, Yao J, Zhang Y, Guo H, Liu X. Overexpression of MACC1 and the association hepatocyte growth factor/c-Met in epithelial ovarian cancer. Oncol Lett. 2015;9:1989–96.PubMedPubMedCentral
44.
go back to reference Sheng XJ, Li Z, Sun M, Wang ZH, Zhou DM, Li JQ, Zhao Q, Sun XF, Liu QC. MACC1 induces metastasis in ovarian carcinoma by upregulating hepatocyte growth factor receptor c-Met. Oncol Lett. 2014;8:891–7.PubMedPubMedCentral Sheng XJ, Li Z, Sun M, Wang ZH, Zhou DM, Li JQ, Zhao Q, Sun XF, Liu QC. MACC1 induces metastasis in ovarian carcinoma by upregulating hepatocyte growth factor receptor c-Met. Oncol Lett. 2014;8:891–7.PubMedPubMedCentral
45.
go back to reference Hilbe W, Dirnhofer S, Oberwasserlechner F, Schmid T, Gunsilius E, Hilbe G, Wöll E, Kähler CM. CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J Clin Pathol. 2004;57:965–9.CrossRefPubMedPubMedCentral Hilbe W, Dirnhofer S, Oberwasserlechner F, Schmid T, Gunsilius E, Hilbe G, Wöll E, Kähler CM. CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J Clin Pathol. 2004;57:965–9.CrossRefPubMedPubMedCentral
46.
go back to reference Wang R, Chadalavad K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010;468:829–33.CrossRefPubMed Wang R, Chadalavad K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010;468:829–33.CrossRefPubMed
47.
go back to reference Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871–90.CrossRefPubMed Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871–90.CrossRefPubMed
48.
go back to reference Sun T, Sun BC, Zhao XL, Zhao N, Dong XY, Che N, Yao Z, Ma YM, Gu Q, Zong WK, Liu ZY. Promotion of tumor cell metastasis and vasculogenic mimicry by way of transcription coactivation by Bcl-2 and Twist1: a study of hepatocellular carcinoma. Hepatology. 2011;54:1690–706.CrossRefPubMed Sun T, Sun BC, Zhao XL, Zhao N, Dong XY, Che N, Yao Z, Ma YM, Gu Q, Zong WK, Liu ZY. Promotion of tumor cell metastasis and vasculogenic mimicry by way of transcription coactivation by Bcl-2 and Twist1: a study of hepatocellular carcinoma. Hepatology. 2011;54:1690–706.CrossRefPubMed
49.
go back to reference Liu Z, Sun B, Qi L, Li H, Gao J, Leng X. Zinc finger E-box binding homeobox 1 promotes vasculogenic mimicry in colorectal cancer through induction of epithelial-to-mesenchymal transition. Cancer Sci. 2012;103:813–20.CrossRefPubMed Liu Z, Sun B, Qi L, Li H, Gao J, Leng X. Zinc finger E-box binding homeobox 1 promotes vasculogenic mimicry in colorectal cancer through induction of epithelial-to-mesenchymal transition. Cancer Sci. 2012;103:813–20.CrossRefPubMed
50.
go back to reference Takeda T, Kikuchi E, Mikami S, Suzuki E, Matsumoto K, Miyajima A, Okada Y, Oya M. Prognostic role of KiSS-1 and possibility of the therapeutic modality of metastin, the final peptide of the KiSS-1 gene in urothelial carcinoma. Mol Cancer Ther. 2012;44:853–63.CrossRef Takeda T, Kikuchi E, Mikami S, Suzuki E, Matsumoto K, Miyajima A, Okada Y, Oya M. Prognostic role of KiSS-1 and possibility of the therapeutic modality of metastin, the final peptide of the KiSS-1 gene in urothelial carcinoma. Mol Cancer Ther. 2012;44:853–63.CrossRef
Metadata
Title
Evaluation of the correlation of vasculogenic mimicry, ALDH1, KiSS-1, and MACC1 in the prediction of metastasis and prognosis in ovarian carcinoma
Authors
Lan Yu
Bo Zhu
Shiwu Wu
Lei Zhou
Wenqing Song
Xiaomeng Gong
Danna Wang
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2017
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/s13000-017-0612-9

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