DNA mismatch repair gene MLH1 induces apoptosis in prostate cancer cells

Oncotarget

Volumn 5, Issue 22, 2014, Pages 11297-11307

  Fukuhara, Shinichiro ^a,b,c   Chang, Inik ^a,d   Mitsui, Yozo ^a,b,e   Chiyomaru, Takeshi ^a,b,f   Yamamura, Soichiro ^a,b   Majid, Shahana ^a,b   Saini, Sharanjot ^a,b   Hirata, Hiroshi ^a,b   Deng, Guoren ^a,b   Gill, Ankurpreet ^a   Wong, Darryn K ^a   Shiina, Hiroaki ^e   Nonomura, Norio ^c   Dahiya, Rajvir ^a,b   Tanaka, Yuichiro ^a,b  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d Yonsei University College of Dentistry   (South Korea)

^e SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

^f KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

Apoptosis; c Abl; MLH1; Prostate cancer

Indexed keywords

ABELSON KINASE; PROTEIN MLH1; SMALL INTERFERING RNA; BENZAMIDE DERIVATIVE; IMATINIB; MLH1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PIPERAZINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CARCINOGENICITY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MISMATCH REPAIR; MLH1 GENE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; TUMOR INVASION; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PROSTATE TUMOR; TUMOR CELL LINE; XENOGRAFT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BENZAMIDES; CELL LINE, TUMOR; DNA MISMATCH REPAIR; HETEROGRAFTS; HUMANS; IMATINIB MESYLATE; MALE; MICE; MICE, NUDE; NUCLEAR PROTEINS; PHOSPHORYLATION; PIPERAZINES; PROSTATIC NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-ABL; PYRIMIDINES; TRANSFECTION;

EID: 84917695868     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2315     Document Type: Article

References (36)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64:9-29.
2. Buermeyer AB, Deschenes SM, Baker SM, Liskay RM. Mammalian DNA mismatch repair. Annu Rev Genet. 1999; 33:533-564.
3. Kunkel TA, Erie DA. DNA mismatch repair. Annu Rev Biochem. 2005; 74:681-710.
4. Kinzler KW, Vogelstein B. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature. 1997; 386:761, 763.
5. Li GM. The role of mismatch repair in DNA damageinduced apoptosis. Oncol Res. 1999; 11:393-400.
6. O'Brien V, Brown R. Signalling cell cycle arrest and cell death through the MMR System. Carcinogenesis. 2006; 27:682-692.
7. Soravia C, van der Klift H, Brundler MA, Blouin JL, Wijnen J, Hutter P, Fodde R, Delozier-Blanchet C. Prostate cancer is part of the hereditary non-polyposis colorectal cancer (HNPCC) tumor spectrum. Am J Med Genet A. 2003; 121A:159-162.
8. Raymond VM, Mukherjee B, Wang F, Huang SC, Stoffel EM, Kastrinos F, Syngal S, Cooney KA, Gruber SB. Elevated risk of prostate cancer among men with Lynch syndrome. J Clin Oncol. 2013; 31:1713-1718.
9. Grindedal EM, Moller P, Eeles R, Stormorken AT, Bowitz-Lothe IM, Landro SM, Clark N, Kvale R, Shanley S, Maehle L. Germ-line mutations in mismatch repair genes associated with prostate cancer. Cancer Epidemiol Biomarkers Prev. 2009; 18:2460-2467.
10. Peltomaki P, Vasen H. Mutations associated with HNPCC predisposition -- Update of ICG-HNPCC/INSiGHT mutation database. Dis Markers. 2004; 20:269-276.
11. Boyer JC, Umar A, Risinger JI, Lipford JR, Kane M, Yin S, Barrett JC, Kolodner RD, Kunkel TA. Microsatellite instability, mismatch repair deficiency, and genetic defects in human cancer cell lines. Cancer Res. 1995; 55:6063- 6070.
12. Chen Y, Wang J, Fraig MM, Metcalf J, Turner WR, Bissada NK, Watson DK, Schweinfest CW. Defects of DNA mismatch repair in human prostate cancer. Cancer Res. 2001; 61:4112-4121.
13. Yeh CC, Lee C, Dahiya R. DNA mismatch repair enzyme activity and gene expression in prostate cancer. Biochem Biophys Res Commun. 2001; 285:409-413.
14. Chen Y, Wang J, Fraig MM, Henderson K, Bissada NK, Watson DK, Schweinfest CW. Alterations in PMS2, MSH2 and MLH1 expression in human prostate cancer. Int J Oncol. 2003; 22:1033-1043.
15. Soni A, Bansal A, Singh LC, Mishra AK, Majumdar M, Regina T, Mohanty NK, Saxena S. Gene expression profile and mutational analysis of DNA mismatch repair genes in carcinoma prostate in Indian population. OMICS. 2011; 15:319-324.
16. Li LS, Morales JC, Hwang A, Wagner MW, Boothman DA. DNA mismatch repair-dependent activation of c-Abl/ p73alpha/GADD45alpha-mediated apoptosis. J Biol Chem. 2008; 283:21394-21403.
17. Fink D, Nebel S, Aebi S, Zheng H, Cenni B, Nehme A, Christen RD, Howell SB. The role of DNA mismatch repair in platinum drug resistance. Cancer Res. 1996; 56:4881- 4886.
18. Papouli E, Cejka P, Jiricny J. Dependence of the cytotoxicity of DNA-damaging agents on the mismatch repair status of human cells. Cancer Res. 2004; 64:3391- 3394.
19. Zhang H, Richards B, Wilson T, Lloyd M, Cranston A, Thorburn A, Fishel R, Meuth M. Apoptosis induced by overexpression of hMSH2 or hMLH1. Cancer Res. 1999; 59:3021-3027.
20. Kolodner RD, Hall NR, Lipford J, Kane MF, Morrison PT, Finan PJ, Burn J, Chapman P, Earabino C, Merchant E, Bishop DT. Structure of the human MLH1 locus and analysis of a large hereditary nonpolyposis colorectal carcinoma kindred for mlh1 mutations. Cancer Res. 1995; 55:242-248.
21. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM. Yama/ CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 1995; 81:801-809.
22. Margolin N, Raybuck SA, Wilson KP, Chen W, Fox T, Gu Y, Livingston DJ. Substrate and inhibitor specificity of interleukin-1 beta-converting enzyme and related caspases. J Biol Chem. 1997; 272:7223-7228.
23. Hassen S, Ali N, Chowdhury P. Molecular signaling mechanisms of apoptosis in hereditary non-polyposis colorectal cancer. World J Gastrointest Pathophysiol. 2012; 3:71-79.
24. Koi M, Umar A, Chauhan DP, Cherian SP, Carethers JM, Kunkel TA, Boland CR. Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N'-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res. 1994; 54:4308-4312.
25. Hawn MT, Umar A, Carethers JM, Marra G, Kunkel TA, Boland CR, Koi M. Evidence for a connection between the mismatch repair system and the G2 cell cycle checkpoint. Cancer Res. 1995; 55:3721-3725.
26. Ding X, Mohd AB, Huang Z, Baba T, Bernardini MQ, Lyerly HK, Berchuck A, Murphy SK, Buermeyer AB, Devi GR. MLH1 expression sensitises ovarian cancer cells to cell death mediated by XIAP inhibition. Br J Cancer. 2009; 101:269-277.
27. Ruzov A, Shorning B, Mortusewicz O, Dunican DS, Leonhardt H, Meehan RR. MBD4 and MLH1 are required for apoptotic induction in xDNMT1-depleted embryos. Development. 2009; 136:2277-2286.
28. Nehme A, Baskaran R, Nebel S, Fink D, Howell SB, Wang JY, Christen RD. Induction of JNK and c-Abl signalling by cisplatin and oxaliplatin in mismatch repair-proficient and -deficient cells. Br J Cancer. 1999; 79:1104-1110.
29. Kim WJ, Rajasekaran B, Brown KD. MLH1- and ATMdependent MAPK signaling is activated through c-Abl in response to the alkylator N-methyl-N'-nitro-N'- nitrosoguanidine. J Biol Chem. 2007; 282:32021-32031.
30. Wagner MW, Li LS, Morales JC, Galindo CL, Garner HR, Bornmann WG, Boothman DA. Role of c-Abl kinase in DNA mismatch repair-dependent G2 cell cycle checkpoint arrest responses. J Biol Chem. 2008; 283:21382-21393.
31. Hantschel O, Superti-Furga G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol. 2004; 5:33-44.
32. Chen S, O'Reilly LP, Smithgall TE, Engen JR. Tyrosine phosphorylation in the SH3 domain disrupts negative regulatory interactions within the c-Abl kinase core. J Mol Biol. 2008; 383:414-423.
33. Meyn MA, 3rd, Wilson MB, Abdi FA, Fahey N, Schiavone AP, Wu J, Hochrein JM, Engen JR, Smithgall TE. Src family kinases phosphorylate the Bcr-Abl SH3-SH2 region and modulate Bcr-Abl transforming activity. J Biol Chem. 2006; 281:30907-30916.
34. Shafman T, Khanna KK, Kedar P, Spring K, Kozlov S, Yen T, Hobson K, Gatei M, Zhang N, Watters D, Egerton M, Shiloh Y, Kharbanda S, Kufe D, Lavin MF. Interaction between ATM protein and c-Abl in response to DNA damage. Nature. 1997; 387:520-523.
35. Baskaran R, Wood LD, Whitaker LL, Canman CE, Morgan SE, Xu Y, Barlow C, Baltimore D, Wynshaw-Boris A, Kastan MB, Wang JY. Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature. 1997; 387:516-519.
36. Wang X, Zeng L, Wang J, Chau JF, Lai KP, Jia D, Poonepalli A, Hande MP, Liu H, He G, He L, Li B. A positive role for c-Abl in Atm and Atr activation in DNA damage response. Cell Death Differ. 2011; 18:5-15.