XPC inhibits NSCLC cell proliferation and migration by enhancing E-Cadherin expression

Oncotarget

Volumn 6, Issue 12, 2015, Pages 10060-10072

  Cui, Tiantian ^a   Srivastava, Amit Kumar ^a   Han, Chunhua ^a   Yang, Linlin ^a   Zhao, Ran ^a   Zou, Ning ^a   Qu, Meihua ^a   Duan, Wenrui ^a   Zhang, Xiaoli ^a   Wang, Qi En ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

E cadherin; ERK pathway; Non small cell lung cancer; Snail; XPC

Indexed keywords

SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; XERODERMA PIGMENTOSUM GROUP C PROTEIN; CADHERIN; DNA BINDING PROTEIN; MESSENGER RNA; TRANSCRIPTION FACTOR; XPC PROTEIN, HUMAN;

ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER SURVIVAL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; E CADHERIN GENE; FEMALE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LUNG CANCER CELL LINE; MIGRATION INHIBITION; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TUMOR XENOGRAFT; XPC GENE; BIOSYNTHESIS; CELL MOTION; DOWN REGULATION; GENETIC TRANSFECTION; GENETICS; LUNG TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CADHERINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DNA DAMAGE; DNA-BINDING PROTEINS; DOWN-REGULATION; HUMANS; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; RNA, MESSENGER; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84929603440     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3542     Document Type: Article

References (49)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015; 65:5-29.
2. Howlader N, Noone AM, Yu M, Cronin KA. Use of imputed population-based cancer registry data as a method of accounting for missing information: application to estrogen receptor status for breast cancer. Am J Epidemiol. 2012; 176:347-356.
3. Legerski R, Peterson C. Expression cloning of a human DNA repair gene involved in xeroderma pigmentosum group C. Nature. 1992; 359:70-73.
4. Despras E, Pfeiffer P, Salles B, Calsou P, Kuhfittig-Kulle S, Angulo JF, Biard DS. Long-term XPC silencing reduces DNA double-strand break repair. Cancer Res. 2007; 67:2526-2534.
5. D'Errico M, Parlanti E, Teson M, de Jesus BM, Degan P, Calcagnile A, Jaruga P, Bjoras M, Crescenzi M, Pedrini AM, Egly JM, Zambruno G, Stefanini M, Dizdaroglu M, Dogliotti E. New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J. 2006; 25:4305-4315.
6. Sands AT, Abuin A, Sanchez A, Conti CJ, Bradley A. High susceptibility to ultraviolet-induced carcinogenesis in mice lacking XPC. Nature. 1995; 377:162-165.
7. Cheo DL, Meira LB, Hammer RE, Burns DK, Doughty AT, Friedberg EC. Synergistic interactions between XPC and p53 mutations in double-mutant mice: neural tube abnormalities and accelerated UV radiation-induced skin cancer. Curr Biol. 1996; 6:1691-1694.
8. Cheo DL, Burns DK, Meira LB, Houle JF, Friedberg EC. Mutational inactivation of the xeroderma pigmentosum group C gene confers predisposition to 2-acetylaminofluorene-induced liver and lung cancer and to spontaneous testicular cancer in Trp53-/- mice. Cancer Res. 1999; 59:771-775.
9. Melis JP, Wijnhoven SW, Beems RB, Roodbergen M, Van den Berg J, Moon H, Friedberg E, Van der Horst GT, Hoeijmakers JH, Vijg J, van SH. Mouse models for xeroderma pigmentosum group A and group C show divergent cancer phenotypes. Cancer Res. 2008; 68:1347-1353.
10. Yang PW, Hsieh CY, Kuo FT, Huang PM, Hsu HH, Kuo SW, Chen JS, Lee JM. The survival impact of XPA and XPC genetic polymorphisms on patients with esophageal squamous cell carcinoma. Ann Surg Oncol. 2013; 20:562-571.
11. Hollander MC, Philburn RT, Patterson AD, Velasco-Miguel S, Friedberg EC, Linnoila RI, Fornace AJ, Jr. Deletion of XPC leads to lung tumors in mice and is associated with early events in human lung carcinogenesis. Proc Natl Acad Sci U S A. 2005; 102:13200-13205.
12. Yang J, Xu Z, Li J, Zhang R, Zhang G, Ji H, Song B, Chen Z. XPC epigenetic silence coupled with p53 alteration has a significant impact on bladder cancer outcome. J Urol. 2010; 184:336-343.
13. Wu YH, Wu TC, Liao JW, Yeh KT, Chen CY, Lee H. p53 dysfunction by xeroderma pigmentosum group C defects enhance lung adenocarcinoma metastasis via increased MMP1 expression. Cancer Res. 2010; 70:10422-10432.
14. Wang QE, Han C, Zhang B, Sabapathy K, Wani AA. Nucleotide excision repair factor XPC enhances DNA damage-induced apoptosis by downregulating the antiapoptotic short isoform of caspase-2. Cancer Res. 2012; 72:666-675.
15. Jeanes A, Gottardi CJ, Yap AS. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene. 2008; 27:6920-6929.
16. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 2008; 68:3645-3654.
17. Birchmeier W, Behrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim Biophys Acta. 1994; 1198:11-26.
18. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002; 2:442-454.
19. Yang YL, Chen MW, Xian L. Prognostic and clinicopathological significance of downregulated E-cadherin expression in patients with non-small cell lung cancer (NSCLC): a meta-analysis. PLoS One. 2014; 9:e99763-20.
20. Yan HB, Wang XF, Zhang Q, Tang ZQ, Jiang YH, Fan HZ, Sun YH, Yang PY, Liu F. Reduced expression of the chromatin remodeling gene ARID1A enhances gastric cancer cell migration and invasion via downregulation of E-cadherin transcription. Carcinogenesis. 2014; 35:867-876.
21. Tripathi V, Popescu NC, Zimonjic DB. DLC1 induces expression of E-cadherin in prostate cancer cells through Rho pathway and suppresses invasion. Oncogene. 2014; 33:724-733.
22. Wu YH, Tsai Chang JH, Cheng YW, Wu TC, Chen CY, Lee H. Xeroderma pigmentosum group C gene expression is predominantly regulated by promoter hypermethylation and contributes to p53 mutation in lung cancers. Oncogene. 2007; 26:4761-4773.
23. Stockinger A, Eger A, Wolf J, Beug H, Foisner R. E-cadherin regulates cell growth by modulating proliferation-dependent beta-catenin transcriptional activity. J Cell Biol. 2001; 154:1185-1196.
24. Pecina-Slaus N. Tumor suppressor gene E-cadherin and its role in normal and malignant cells. Cancer Cell Int. 2003; 3:17-25.
25. Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene. 2008; 27:6958-6969.
26. Peinado H, Ballestar E, Esteller M, Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/ histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol. 2004; 24:306-319.
27. Bolos V, Peinado H, Perez-Moreno MA, Fraga MF, Esteller M, Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci. 2003; 116:499-511.
28. Singh AB, Sharma A, Smith JJ, Krishnan M, Chen X, Eschrich S, Washington MK, Yeatman TJ, Beauchamp RD, Dhawan P. Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology. 2011; 141:2140-2153.
29. Lau MT, Leung PC. The PI3K/Akt/mTOR signaling pathway mediates insulin-like growth factor 1-induced E-cadherin down-regulation and cell proliferation in ovarian cancer cells. Cancer Lett. 2012; 326:191-198.
30. Hsu YL, Hou MF, Kuo PL, Huang YF, Tsai EM. Breast tumor-associated osteoblast-derived CXCL5 increases cancer progression by ERK/MSK1/Elk-1/snail signaling pathway. Oncogene. 2013; 32:4436-4447.
31. Tang D, Wu D, Hirao A, Lahti JM, Liu L, Mazza B, Kidd VJ, Mak TW, Ingram AJ. ERK activation mediates cell cycle arrest and apoptosis after DNA damage independently of p53. J Biol Chem. 2002; 277:12710-12717.
32. Rezvani HR, Kim AL, Rossignol R, Ali N, Daly M, Mahfouf W, Bellance N, Taieb A, de VH, Mazurier F, Bickers DR. XPC silencing in normal human keratinocytes triggers metabolic alterations that drive the formation of squamous cell carcinomas. J Clin Invest. 2011; 121:195-211.
33. Han W, Soltani K, Ming M, He YY. Deregulation of XPC and CypA by cyclosporin A: an immunosuppressionindependent mechanism of skin carcinogenesis. Cancer Prev Res (Phila). 2012; 5:1155-1162.
34. Wu YH, Cheng YW, Chang JT, Wu TC, Chen CY, Lee H. Reduced XPC messenger RNA level may predict a poor outcome of patients with nonsmall cell lung cancer. Cancer. 2007; 110:215-223.
35. Nollet F, Berx G, van RF. The role of the E-cadherin/catenin adhesion complex in the development and progression of cancer. Mol Cell Biol Res Commun. 1999; 2:77-85.
36. Yanagisawa M, Anastasiadis PZ. p120 catenin is essential for mesenchymal cadherin-mediated regulation of cell motility and invasiveness. J Cell Biol. 2006; 174:1087-1096.
37. Soto E, Yanagisawa M, Marlow LA, Copland JA, Perez EA, Anastasiadis PZ. p120 catenin induces opposing effects on tumor cell growth depending on E-cadherin expression. J Cell Biol. 2008; 183:737-749.
38. Tsukamoto T, Nigam SK. Cell-cell dissociation upon epithelial cell scattering requires a step mediated by the proteasome. J Biol Chem. 1999; 274:24579-24584.
39. Wijnhoven BP, Dinjens WN, Pignatelli M. E-cadherincatenin cell-cell adhesion complex and human cancer. Br J Surg. 2000; 87:992-1005.
40. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya-Feldstein J, Reinhardt F, Onder TT, Valastyan S, Westermann F, Speleman F, Vandesompele J, Weinberg RA. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010; 12:247-256.
41. Hsu YL, Huang MS, Yang CJ, Hung JY, Wu LY, Kuo PL. Lung tumor-associated osteoblast-derived bone morphogenetic protein-2 increased epithelial-tomesenchymal transition of cancer by Runx2/Snail signaling pathway. J Biol Chem. 2011; 286:37335-37346.
42. Zhang HM, Li L, Papadopoulou N, Hodgson G, Evans E, Galbraith M, Dear M, Vougier S, Saxton J, Shaw PE. Mitogen-induced recruitment of ERK and MSK to SRE promoter complexes by ternary complex factor Elk-1. Nucleic Acids Res. 2008; 36:2594-2607.
43. Chen H, Zhu G, Li Y, Padia RN, Dong Z, Pan ZK, Liu K, Huang S. Extracellular signal-regulated kinase signaling pathway regulates breast cancer cell migration by maintaining slug expression. Cancer Res. 2009; 69:9228-9235.
44. Marchetti A, Colletti M, Cozzolino AM, Steindler C, Lunadei M, Mancone C, Tripodi M. ERK5/MAPK is activated by TGFbeta in hepatocytes and required for the GSK-3beta-mediated Snail protein stabilization. Cell Signal. 2008; 20:2113-2118.
45. Wei F, Yan J, Tang D. Extracellular signal-regulated kinases modulate DNA damage response - a contributing factor to using MEK inhibitors in cancer therapy. Curr Med Chem. 2011; 18:5476-5482.
46. Fong YW, Inouye C, Yamaguchi T, Cattoglio C, Grubisic I, Tjian R. A DNA repair complex functions as an Oct4/Sox2 coactivator in embryonic stem cells. Cell. 2011; 147:120-131.
47. Wang QE, Zhu Q, Wani G, El-Mahdy MA, Li J, Wani AA. DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res. 2005; 33:4023-4034.
48. Han C, Zhao R, Liu X, Srivastava A, Gong L, Mao H, Qu M, Zhao W, Yu J, Wang QE. DDB2 suppresses tumorigenicity by limiting the cancer stem cell population in ovarian cancer. Mol Cancer Res. 2014; 12:784-794.
49. Gottardi CJ, Wong E, Gumbiner BM. E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J Cell Biol. 2001; 153:1049-1060.