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Published in: Journal of Translational Medicine 1/2014

Open Access 01-12-2014 | Research

Yin Yang 1 contributes to gastric carcinogenesis and its nuclear expression correlates with shorter survival in patients with early stage gastric adenocarcinoma

Authors: Wei Kang, Joanna HM Tong, Anthony WH Chan, Junhong Zhao, Yujuan Dong, Shiyan Wang, Weiqin Yang, Frankie MC Sin, Simon SM Ng, Jun Yu, Alfred SL Cheng, Ka Fai To

Published in: Journal of Translational Medicine | Issue 1/2014

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Abstract

Background

Yin Yang 1 (YY1) is a transcription factor that regulates diverse biological processes and increasing recognized to have important roles in carcinogenesis. The function and clinical significance of YY1 in gastric adenocarcinoma (GAC) have not been elucidated.

Methods

In this study, the functional role of YY1 in gastric cancer was investigated by MTT proliferation assays, monolayer colony formation, cell cycle analysis, signaling pathway analysis, Western blot analysis and in vivo study through YY1 knockdown or overexpression. Immunohistochemical study with YY1 antibody was performed on tissue microarray consisting of 247 clinical GAC samples. The clinical correlation and prognosis significance were evaluated.

Results

YY1 expression was up-regulated in gastric cancer cell lines and primary gastric cancers. Knocking down YY1 by siYY1 inhibited cell growth, inducing G1 phase accumulation and apoptosis. Ectopic YY1 expression enhanced cell proliferation in vitro and in vivo. Knocking down YY1 in gastric cancer cells suppressed proliferation by inhibiting Wnt/β-catenin pathway, whereas its overexpression exerted oncogenic property by activating Wnt/β-catenin pathway. In primary GAC samples, YY1 nuclear expression correlated with shorter survival and predicted poor prognosis in early stage GACs.

Conclusion

Our data demonstrated that YY1 contributes to gastric carcinogenesis in gastric cancer. In early stage GACs YY1 might serve as a poor prognostic marker and possibly as a potential therapeutic target.
Appendix
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Literature
1.
go back to reference Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ: Cancer statistics, 2007. CA Cancer J Clin. 2007, 57: 43-66. 10.3322/canjclin.57.1.43.CrossRefPubMed Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ: Cancer statistics, 2007. CA Cancer J Clin. 2007, 57: 43-66. 10.3322/canjclin.57.1.43.CrossRefPubMed
2.
go back to reference Vrdoljak E, Wojtukiewicz MZ, Pienkowski T, Bodoky G, Berzinec P, Finek J, Todorovic V, Borojevic N, Croitoru A: Cancer epidemiology in Central, South and Eastern European countries. Croat Med J. 2011, 52: 478-487. 10.3325/cmj.2011.52.478.PubMedCentralCrossRefPubMed Vrdoljak E, Wojtukiewicz MZ, Pienkowski T, Bodoky G, Berzinec P, Finek J, Todorovic V, Borojevic N, Croitoru A: Cancer epidemiology in Central, South and Eastern European countries. Croat Med J. 2011, 52: 478-487. 10.3325/cmj.2011.52.478.PubMedCentralCrossRefPubMed
3.
go back to reference Milne AN, Carneiro F, O’Morain C, Offerhaus GJ: Nature meets nurture: molecular genetics of gastric cancer. Hum Genet. 2009, 126: 615-628. 10.1007/s00439-009-0722-x.PubMedCentralCrossRefPubMed Milne AN, Carneiro F, O’Morain C, Offerhaus GJ: Nature meets nurture: molecular genetics of gastric cancer. Hum Genet. 2009, 126: 615-628. 10.1007/s00439-009-0722-x.PubMedCentralCrossRefPubMed
4.
go back to reference Shi Y, Seto E, Chang LS, Shenk T: Transcriptional repression by YY1, a human GLI-Kruppel-related protein, and relief of repression by adenovirus E1A protein. Cell. 1991, 67: 377-388. 10.1016/0092-8674(91)90189-6.CrossRefPubMed Shi Y, Seto E, Chang LS, Shenk T: Transcriptional repression by YY1, a human GLI-Kruppel-related protein, and relief of repression by adenovirus E1A protein. Cell. 1991, 67: 377-388. 10.1016/0092-8674(91)90189-6.CrossRefPubMed
5.
go back to reference Zaravinos A, Spandidos DA: Yin yang 1 expression in human tumors. Cell Cycle. 2010, 9: 512-522. 10.4161/cc.9.3.10588.CrossRefPubMed Zaravinos A, Spandidos DA: Yin yang 1 expression in human tumors. Cell Cycle. 2010, 9: 512-522. 10.4161/cc.9.3.10588.CrossRefPubMed
6.
go back to reference Lee HY, Chaudhary J, Walsh GL, Hong WK, Kurie JM: Suppression of c-Fos gene transcription with malignant transformation of human bronchial epithelial cells. Oncogene. 1998, 16: 3039-3046. 10.1038/sj.onc.1201843.CrossRefPubMed Lee HY, Chaudhary J, Walsh GL, Hong WK, Kurie JM: Suppression of c-Fos gene transcription with malignant transformation of human bronchial epithelial cells. Oncogene. 1998, 16: 3039-3046. 10.1038/sj.onc.1201843.CrossRefPubMed
7.
go back to reference Liao WR, Hsieh RH, Hsu KW, Wu MZ, Tseng MJ, Mai RT, Wu Lee YH, Yeh TS: The CBF1-independent Notch1 signal pathway activates human c-myc expression partially via transcription factor YY1. Carcinogenesis. 2007, 28: 1867-1876. 10.1093/carcin/bgm092.CrossRefPubMed Liao WR, Hsieh RH, Hsu KW, Wu MZ, Tseng MJ, Mai RT, Wu Lee YH, Yeh TS: The CBF1-independent Notch1 signal pathway activates human c-myc expression partially via transcription factor YY1. Carcinogenesis. 2007, 28: 1867-1876. 10.1093/carcin/bgm092.CrossRefPubMed
8.
go back to reference Allouche A, Nolens G, Tancredi A, Delacroix L, Mardaga J, Fridman V, Winkler R, Boniver J, Delvenne P, Begon DY: The combined immunodetection of AP-2alpha and YY1 transcription factors is associated with ERBB2 gene overexpression in primary breast tumors. Breast Cancer Res. 2008, 10: R9-10.1186/bcr1851.PubMedCentralCrossRefPubMed Allouche A, Nolens G, Tancredi A, Delacroix L, Mardaga J, Fridman V, Winkler R, Boniver J, Delvenne P, Begon DY: The combined immunodetection of AP-2alpha and YY1 transcription factors is associated with ERBB2 gene overexpression in primary breast tumors. Breast Cancer Res. 2008, 10: R9-10.1186/bcr1851.PubMedCentralCrossRefPubMed
9.
go back to reference Begon DY, Delacroix L, Vernimmen D, Jackers P, Winkler R: Yin Yang 1 cooperates with activator protein 2 to stimulate ERBB2 gene expression in mammary cancer cells. J Biol Chem. 2005, 280: 24428-24434. 10.1074/jbc.M503790200.CrossRefPubMed Begon DY, Delacroix L, Vernimmen D, Jackers P, Winkler R: Yin Yang 1 cooperates with activator protein 2 to stimulate ERBB2 gene expression in mammary cancer cells. J Biol Chem. 2005, 280: 24428-24434. 10.1074/jbc.M503790200.CrossRefPubMed
10.
go back to reference Wan M, Huang W, Kute TE, Miller LD, Zhang Q, Hatcher H, Wang J, Stovall DB, Russell GB, Cao PD, Deng Z, Wang W, Zhang Q, Lei M, Torti SV, Akman SA, Sui G: Yin Yang 1 plays an essential role in breast cancer and negatively regulates p27. Am J Pathol. 2012, 180: 2120-2133. 10.1016/j.ajpath.2012.01.037.PubMedCentralCrossRefPubMed Wan M, Huang W, Kute TE, Miller LD, Zhang Q, Hatcher H, Wang J, Stovall DB, Russell GB, Cao PD, Deng Z, Wang W, Zhang Q, Lei M, Torti SV, Akman SA, Sui G: Yin Yang 1 plays an essential role in breast cancer and negatively regulates p27. Am J Pathol. 2012, 180: 2120-2133. 10.1016/j.ajpath.2012.01.037.PubMedCentralCrossRefPubMed
12.
go back to reference Wu S, Murai S, Kataoka K, Miyagishi M: Cooperative regulation of p73 promoter by Yin Yang 1 and E2F1. Nucleic Acids Symp Ser (Oxf). 2007, 51: 347-348. 10.1093/nass/nrm174.CrossRef Wu S, Murai S, Kataoka K, Miyagishi M: Cooperative regulation of p73 promoter by Yin Yang 1 and E2F1. Nucleic Acids Symp Ser (Oxf). 2007, 51: 347-348. 10.1093/nass/nrm174.CrossRef
13.
go back to reference Gronroos E, Terentiev AA, Punga T, Ericsson J: YY1 inhibits the activation of the p53 tumor suppressor in response to genotoxic stress. Proc Natl Acad Sci U S A. 2004, 101: 12165-12170. 10.1073/pnas.0402283101.PubMedCentralCrossRefPubMed Gronroos E, Terentiev AA, Punga T, Ericsson J: YY1 inhibits the activation of the p53 tumor suppressor in response to genotoxic stress. Proc Natl Acad Sci U S A. 2004, 101: 12165-12170. 10.1073/pnas.0402283101.PubMedCentralCrossRefPubMed
14.
go back to reference Castellano G, Torrisi E, Ligresti G, Malaponte G, Militello L, Russo AE, McCubrey JA, Canevari S, Libra M: The involvement of the transcription factor Yin Yang 1 in cancer development and progression. Cell Cycle. 2009, 8: 1367-1372. 10.4161/cc.8.9.8314.CrossRefPubMed Castellano G, Torrisi E, Ligresti G, Malaponte G, Militello L, Russo AE, McCubrey JA, Canevari S, Libra M: The involvement of the transcription factor Yin Yang 1 in cancer development and progression. Cell Cycle. 2009, 8: 1367-1372. 10.4161/cc.8.9.8314.CrossRefPubMed
15.
go back to reference Palmer MB, Majumder P, Cooper JC, Yoon H, Wade PA, Boss JM: Yin yang 1 regulates the expression of snail through a distal enhancer. Mol Cancer Res. 2009, 7: 221-229. 10.1158/1541-7786.MCR-08-0229.PubMedCentralCrossRefPubMed Palmer MB, Majumder P, Cooper JC, Yoon H, Wade PA, Boss JM: Yin yang 1 regulates the expression of snail through a distal enhancer. Mol Cancer Res. 2009, 7: 221-229. 10.1158/1541-7786.MCR-08-0229.PubMedCentralCrossRefPubMed
16.
go back to reference de Nigris F, Rossiello R, Schiano C, Arra C, Williams-Ignarro S, Barbieri A, Lanza A, Balestrieri A, Giuliano MT, Ignarro LJ, Napoli C: Deletion of Yin Yang 1 protein in osteosarcoma cells on cell invasion and CXCR4/angiogenesis and metastasis. Cancer Res. 2008, 68: 1797-1808. 10.1158/0008-5472.CAN-07-5582.CrossRefPubMed de Nigris F, Rossiello R, Schiano C, Arra C, Williams-Ignarro S, Barbieri A, Lanza A, Balestrieri A, Giuliano MT, Ignarro LJ, Napoli C: Deletion of Yin Yang 1 protein in osteosarcoma cells on cell invasion and CXCR4/angiogenesis and metastasis. Cancer Res. 2008, 68: 1797-1808. 10.1158/0008-5472.CAN-07-5582.CrossRefPubMed
17.
go back to reference de Nigris F, Botti C, de Chiara A, Rossiello R, Apice G, Fazioli F, Fiorito C, Sica V, Napoli C: Expression of transcription factor Yin Yang 1 in human osteosarcomas. Eur J Cancer. 2006, 42: 2420-2424. 10.1016/j.ejca.2006.06.008.CrossRefPubMed de Nigris F, Botti C, de Chiara A, Rossiello R, Apice G, Fazioli F, Fiorito C, Sica V, Napoli C: Expression of transcription factor Yin Yang 1 in human osteosarcomas. Eur J Cancer. 2006, 42: 2420-2424. 10.1016/j.ejca.2006.06.008.CrossRefPubMed
18.
go back to reference de Nigris F, Zanella L, Cacciatore F, De Chiara A, Fazioli F, Chiappetta G, Apice G, Infante T, Monaco M, Rossiello R, De Rosa G, Alberghini M, Napoli C: YY1 overexpression is associated with poor prognosis and metastasis-free survival in patients suffering osteosarcoma. BMC Cancer. 2011, 11: 472-10.1186/1471-2407-11-472.CrossRefPubMed de Nigris F, Zanella L, Cacciatore F, De Chiara A, Fazioli F, Chiappetta G, Apice G, Infante T, Monaco M, Rossiello R, De Rosa G, Alberghini M, Napoli C: YY1 overexpression is associated with poor prognosis and metastasis-free survival in patients suffering osteosarcoma. BMC Cancer. 2011, 11: 472-10.1186/1471-2407-11-472.CrossRefPubMed
19.
go back to reference Castellano G, Torrisi E, Ligresti G, Nicoletti F, Malaponte G, Traval S, McCubrey JA, Canevari S, Libra M: Yin Yang 1 overexpression in diffuse large B-cell lymphoma is associated with B-cell transformation and tumor progression. Cell Cycle. 2010, 9: 557-563. 10.4161/cc.9.3.10554.CrossRefPubMed Castellano G, Torrisi E, Ligresti G, Nicoletti F, Malaponte G, Traval S, McCubrey JA, Canevari S, Libra M: Yin Yang 1 overexpression in diffuse large B-cell lymphoma is associated with B-cell transformation and tumor progression. Cell Cycle. 2010, 9: 557-563. 10.4161/cc.9.3.10554.CrossRefPubMed
20.
go back to reference Deng Z, Wan M, Cao P, Rao A, Cramer SD, Sui G: Yin Yang 1 regulates the transcriptional activity of androgen receptor. Oncogene. 2009, 28: 3746-3757. 10.1038/onc.2009.231.PubMedCentralCrossRefPubMed Deng Z, Wan M, Cao P, Rao A, Cramer SD, Sui G: Yin Yang 1 regulates the transcriptional activity of androgen receptor. Oncogene. 2009, 28: 3746-3757. 10.1038/onc.2009.231.PubMedCentralCrossRefPubMed
21.
go back to reference Zheng H, Chu J, Zeng Y, Loh HH, Law PY: Yin Yang 1 phosphorylation contributes to the differential effects of mu-opioid receptor agonists on microRNA-190 expression. J Biol Chem. 2010, 285: 21994-22002. 10.1074/jbc.M110.112607.PubMedCentralCrossRefPubMed Zheng H, Chu J, Zeng Y, Loh HH, Law PY: Yin Yang 1 phosphorylation contributes to the differential effects of mu-opioid receptor agonists on microRNA-190 expression. J Biol Chem. 2010, 285: 21994-22002. 10.1074/jbc.M110.112607.PubMedCentralCrossRefPubMed
22.
go back to reference Beezhold K, Liu J, Kan H, Meighan T, Castranova V, Shi X, Chen F: miR-190-mediated downregulation of PHLPP contributes to arsenic-induced Akt activation and carcinogenesis. Toxicol Sci. 2011, 123: 411-420. 10.1093/toxsci/kfr188.PubMedCentralCrossRefPubMed Beezhold K, Liu J, Kan H, Meighan T, Castranova V, Shi X, Chen F: miR-190-mediated downregulation of PHLPP contributes to arsenic-induced Akt activation and carcinogenesis. Toxicol Sci. 2011, 123: 411-420. 10.1093/toxsci/kfr188.PubMedCentralCrossRefPubMed
23.
go back to reference Lee MH, Lahusen T, Wang RH, Xiao C, Xu X, Hwang YS, He WW, Shi Y, Deng CX: Yin Yang 1 positively regulates BRCA1 and inhibits mammary cancer formation. Oncogene. 2012, 31: 116-127. 10.1038/onc.2011.217.CrossRefPubMed Lee MH, Lahusen T, Wang RH, Xiao C, Xu X, Hwang YS, He WW, Shi Y, Deng CX: Yin Yang 1 positively regulates BRCA1 and inhibits mammary cancer formation. Oncogene. 2012, 31: 116-127. 10.1038/onc.2011.217.CrossRefPubMed
24.
go back to reference Lieberthal JG, Kaminsky M, Parkhurst CN, Tanese N: The role of YY1 in reduced HP1alpha gene expression in invasive human breast cancer cells. Breast Cancer Res. 2009, 11: R42-10.1186/bcr2329.PubMedCentralCrossRefPubMed Lieberthal JG, Kaminsky M, Parkhurst CN, Tanese N: The role of YY1 in reduced HP1alpha gene expression in invasive human breast cancer cells. Breast Cancer Res. 2009, 11: R42-10.1186/bcr2329.PubMedCentralCrossRefPubMed
25.
go back to reference Wang CC, Tsai MF, Dai TH, Hong TM, Chan WK, Chen JJ, Yang PC: Synergistic activation of the tumor suppressor, HLJ1, by the transcription factors YY1 and activator protein 1. Cancer Res. 2007, 67: 4816-4826. 10.1158/0008-5472.CAN-07-0504.CrossRefPubMed Wang CC, Tsai MF, Dai TH, Hong TM, Chan WK, Chen JJ, Yang PC: Synergistic activation of the tumor suppressor, HLJ1, by the transcription factors YY1 and activator protein 1. Cancer Res. 2007, 67: 4816-4826. 10.1158/0008-5472.CAN-07-0504.CrossRefPubMed
26.
go back to reference Wang CC, Tsai MF, Hong TM, Chang GC, Chen CY, Yang WM, Chen JJ, Yang PC: The transcriptional factor YY1 upregulates the novel invasion suppressor HLJ1 expression and inhibits cancer cell invasion. Oncogene. 2005, 24: 4081-4093. 10.1038/sj.onc.1208573.CrossRefPubMed Wang CC, Tsai MF, Hong TM, Chang GC, Chen CY, Yang WM, Chen JJ, Yang PC: The transcriptional factor YY1 upregulates the novel invasion suppressor HLJ1 expression and inhibits cancer cell invasion. Oncogene. 2005, 24: 4081-4093. 10.1038/sj.onc.1208573.CrossRefPubMed
27.
go back to reference Naidoo K, Clay V, Hoyland JA, Swindell R, Linton K, Illidge T, Radford JA, Byers RJ: YY1 expression predicts favourable outcome in follicular lymphoma. J Clin Pathol. 2011, 64: 125-129. 10.1136/jcp.2010.078188.CrossRefPubMed Naidoo K, Clay V, Hoyland JA, Swindell R, Linton K, Illidge T, Radford JA, Byers RJ: YY1 expression predicts favourable outcome in follicular lymphoma. J Clin Pathol. 2011, 64: 125-129. 10.1136/jcp.2010.078188.CrossRefPubMed
28.
go back to reference Kang W, Tong JH, Chan AW, Lee TL, Lung RW, Leung PP, So KK, Wu K, Fan D, Yu J, Sung JJ, To KF: Yes-associated protein 1 exhibits oncogenic property in gastric cancer and its nuclear accumulation associates with poor prognosis. Clin Cancer Res. 2011, 17: 2130-2139. 10.1158/1078-0432.CCR-10-2467.CrossRefPubMed Kang W, Tong JH, Chan AW, Lee TL, Lung RW, Leung PP, So KK, Wu K, Fan D, Yu J, Sung JJ, To KF: Yes-associated protein 1 exhibits oncogenic property in gastric cancer and its nuclear accumulation associates with poor prognosis. Clin Cancer Res. 2011, 17: 2130-2139. 10.1158/1078-0432.CCR-10-2467.CrossRefPubMed
29.
go back to reference Zhang S, Jiang T, Feng L, Sun J, Lu H, Wang Q, Pan M, Huang D, Wang X, Wang L, Jin H: Yin Yang-1 suppresses differentiation of hepatocellular carcinoma cells through the downregulation of CCAAT/enhancer-binding protein alpha. J Mol Med (Berl). 2012, 90: 1069-1077. 10.1007/s00109-012-0879-y.CrossRef Zhang S, Jiang T, Feng L, Sun J, Lu H, Wang Q, Pan M, Huang D, Wang X, Wang L, Jin H: Yin Yang-1 suppresses differentiation of hepatocellular carcinoma cells through the downregulation of CCAAT/enhancer-binding protein alpha. J Mol Med (Berl). 2012, 90: 1069-1077. 10.1007/s00109-012-0879-y.CrossRef
30.
go back to reference Tang S, Mishra M, Frazier DP, Moore ML, Inoue K, Deora R, Sui G, Dubey P: Positive and negative regulation of prostate stem cell antigen expression by Yin Yang 1 in prostate epithelial cell lines. PLoS One. 2012, 7: e35570-10.1371/journal.pone.0035570.PubMedCentralCrossRefPubMed Tang S, Mishra M, Frazier DP, Moore ML, Inoue K, Deora R, Sui G, Dubey P: Positive and negative regulation of prostate stem cell antigen expression by Yin Yang 1 in prostate epithelial cell lines. PLoS One. 2012, 7: e35570-10.1371/journal.pone.0035570.PubMedCentralCrossRefPubMed
31.
go back to reference Moseley SC, Rizkallah R, Tremblay DC, Anderson BR, Hurt MM, Chadwick BP: YY1 associates with the macrosatellite DXZ4 on the inactive X chromosome and binds with CTCF to a hypomethylated form in some male carcinomas. Nucleic Acids Res. 2012, 40: 1596-1608. 10.1093/nar/gkr964.PubMedCentralCrossRefPubMed Moseley SC, Rizkallah R, Tremblay DC, Anderson BR, Hurt MM, Chadwick BP: YY1 associates with the macrosatellite DXZ4 on the inactive X chromosome and binds with CTCF to a hypomethylated form in some male carcinomas. Nucleic Acids Res. 2012, 40: 1596-1608. 10.1093/nar/gkr964.PubMedCentralCrossRefPubMed
32.
go back to reference Ishii H, Hulett MD, Li JM, Santiago FS, Parish CR, Khachigian LM: Yin Yang-1 inhibits tumor cell growth and inhibits p21WAF1/Cip1 complex formation with cdk4 and cyclin D1. Int J Oncol. 2012, 40: 1575-1580.PubMed Ishii H, Hulett MD, Li JM, Santiago FS, Parish CR, Khachigian LM: Yin Yang-1 inhibits tumor cell growth and inhibits p21WAF1/Cip1 complex formation with cdk4 and cyclin D1. Int J Oncol. 2012, 40: 1575-1580.PubMed
33.
go back to reference Nicholson S, Whitehouse H, Naidoo K, Byers RJ: Yin Yang 1 in human cancer. Crit Rev Oncog. 2011, 16: 245-260. 10.1615/CritRevOncog.v16.i3-4.80.CrossRefPubMed Nicholson S, Whitehouse H, Naidoo K, Byers RJ: Yin Yang 1 in human cancer. Crit Rev Oncog. 2011, 16: 245-260. 10.1615/CritRevOncog.v16.i3-4.80.CrossRefPubMed
34.
35.
go back to reference Joo M, Wright JG, Hu NN, Sadikot RT, Park GY, Blackwell TS, Christman JW: Yin Yang 1 enhances cyclooxygenase-2 gene expression in macrophages. Am J Physiol Lung Cell Mol Physiol. 2007, 292: L1219-L1226. 10.1152/ajplung.00474.2006.CrossRefPubMed Joo M, Wright JG, Hu NN, Sadikot RT, Park GY, Blackwell TS, Christman JW: Yin Yang 1 enhances cyclooxygenase-2 gene expression in macrophages. Am J Physiol Lung Cell Mol Physiol. 2007, 292: L1219-L1226. 10.1152/ajplung.00474.2006.CrossRefPubMed
36.
go back to reference Hu HM, Kanda K, Zhang L, Boxer LM: Activation of the c-myc p1 promoter in Burkitt’s lymphoma by the hs3 immunoglobulin heavy-chain gene enhancer. Leukemia. 2007, 21: 747-753.PubMed Hu HM, Kanda K, Zhang L, Boxer LM: Activation of the c-myc p1 promoter in Burkitt’s lymphoma by the hs3 immunoglobulin heavy-chain gene enhancer. Leukemia. 2007, 21: 747-753.PubMed
37.
go back to reference de Nigris F, Crudele V, Giovane A, Casamassimi A, Giordano A, Garban HJ, Cacciatore F, Pentimalli F, Marquez-Garban DC, Petrillo A, Cito L, Sommese L, Fiore A, Petrillo M, Siani A, Barbieri A, Arra C, Rengo F, Hayashi T, Al-Omran M, Ignarro LJ, Napoli C: CXCR4/YY1 inhibition impairs VEGF network and angiogenesis during malignancy. Proc Natl Acad Sci U S A. 2010, 107: 14484-14489. 10.1073/pnas.1008256107.PubMedCentralCrossRefPubMed de Nigris F, Crudele V, Giovane A, Casamassimi A, Giordano A, Garban HJ, Cacciatore F, Pentimalli F, Marquez-Garban DC, Petrillo A, Cito L, Sommese L, Fiore A, Petrillo M, Siani A, Barbieri A, Arra C, Rengo F, Hayashi T, Al-Omran M, Ignarro LJ, Napoli C: CXCR4/YY1 inhibition impairs VEGF network and angiogenesis during malignancy. Proc Natl Acad Sci U S A. 2010, 107: 14484-14489. 10.1073/pnas.1008256107.PubMedCentralCrossRefPubMed
38.
go back to reference Wu S, Kasim V, Kano MR, Tanaka S, Ohba S, Miura Y, Miyata K, Liu X, Matsuhashi A, Chung UI, Yang L, Kataoka K, Nishiyama N, Miyagishi M: Transcription factor YY1 contributes to tumor growth by stabilizing hypoxia factor HIF-1alpha in a p53-independent manner. Cancer Res. 2013, 73: 1787-1799. 10.1158/0008-5472.CAN-12-0366.CrossRefPubMed Wu S, Kasim V, Kano MR, Tanaka S, Ohba S, Miura Y, Miyata K, Liu X, Matsuhashi A, Chung UI, Yang L, Kataoka K, Nishiyama N, Miyagishi M: Transcription factor YY1 contributes to tumor growth by stabilizing hypoxia factor HIF-1alpha in a p53-independent manner. Cancer Res. 2013, 73: 1787-1799. 10.1158/0008-5472.CAN-12-0366.CrossRefPubMed
39.
go back to reference Zhang N, Li X, Wu CW, Dong Y, Cai M, Mok MT, Wang H, Chen J, Ng SS, Chen M, Sung JJ, Yu J: microRNA-7 is a novel inhibitor of YY1 contributing to colorectal tumorigenesis. Oncogene. 2012, 32: 5078-5088.CrossRefPubMed Zhang N, Li X, Wu CW, Dong Y, Cai M, Mok MT, Wang H, Chen J, Ng SS, Chen M, Sung JJ, Yu J: microRNA-7 is a novel inhibitor of YY1 contributing to colorectal tumorigenesis. Oncogene. 2012, 32: 5078-5088.CrossRefPubMed
40.
go back to reference Monzon FA, Lyons-Weiler M, Buturovic LJ, Rigl CT, Henner WD, Sciulli C, Dumur CI, Medeiros F, Anderson GG: Multicenter validation of a 1,550-gene expression profile for identification of tumor tissue of origin. J Clin Oncol. 2009, 27: 2503-2508. 10.1200/JCO.2008.17.9762.CrossRefPubMed Monzon FA, Lyons-Weiler M, Buturovic LJ, Rigl CT, Henner WD, Sciulli C, Dumur CI, Medeiros F, Anderson GG: Multicenter validation of a 1,550-gene expression profile for identification of tumor tissue of origin. J Clin Oncol. 2009, 27: 2503-2508. 10.1200/JCO.2008.17.9762.CrossRefPubMed
Metadata
Title
Yin Yang 1 contributes to gastric carcinogenesis and its nuclear expression correlates with shorter survival in patients with early stage gastric adenocarcinoma
Authors
Wei Kang
Joanna HM Tong
Anthony WH Chan
Junhong Zhao
Yujuan Dong
Shiyan Wang
Weiqin Yang
Frankie MC Sin
Simon SM Ng
Jun Yu
Alfred SL Cheng
Ka Fai To
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2014
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/1479-5876-12-80

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