MUC16 mucin (CA125) attenuates TRAIL-induced apoptosis by decreasing TRAIL receptor R2 expression and increasing c-FLIP expression

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Matte, Isabelle ^a   Lane, Denis ^a   Boivin, Marianne ^a   Rancourt, Claudine ^a   Piché, Alain ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Apoptosis; Death receptors; MUC16 CA125; Mucins; Ovarian cancer; TRAIL

Indexed keywords

CA 125 ANTIGEN; CASPASE 8; CASPASE 8 INHIBITOR; DEATH RECEPTOR 5; FLICE INHIBITORY PROTEIN; MESSENGER RNA; MUCIN; MUCIN16; PROCASPASE 8; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; UNCLASSIFIED DRUG; CFLAR PROTEIN, HUMAN; MEMBRANE PROTEIN; MUC16 PROTEIN, HUMAN; TNFSF10 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER CELL; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL SURFACE; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; OVARY CANCER; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BIOSYNTHESIS; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

APOPTOSIS; CA-125 ANTIGEN; CARCINOGENESIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASE 8; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE PROTEINS; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; PROTEOLYSIS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA, SMALL INTERFERING; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSCRIPTION, GENETIC;

EID: 84899130785     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-234     Document Type: Article

References (44)

1. Goncharenko-Khaider N, Lane D, Matte I, Rancourt C, Piché A. Targeted ovarian cancer treatment: the TRAILs of resistance. Am J Cancer Res 2012, 2:75-92. 3236573, 22206047.
2. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998, 281:1305-1308.
3. Ashkenazi A, Holland P, Eckhardt SG. Ligand-based targeting of apoptosis in cancer: the potential of recombinant human apoptosis ligand 2/Tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J Clin Oncol 2008, 26:3621-3630. 10.1200/JCO.2007.15.7198, 18640940.
4. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 1999, 5:157-163. 10.1038/5517, 9930862.
5. Ozoren N, El-Deiry WS. Cell surface death receptor signaling in normal and cancer cells. Semin Cancer Biol 2003, 13:135-147. 10.1016/S1044-579X(02)00131-1, 12654257.
6. Wajant H, Pfizenmaier K, Scheurich P. TNF-related apoptosis inducing ligand (TRAIL) and its receptors in tumor surveillance and cancer therapy. Apoptosis 2002, 7:449-459. 10.1023/A:1020039225764, 12207178.
7. Lane D, Cartier A, L'Espérance S, Côté M, Rancourt C, Piché A. Differential induction of apoptosis by tumor necrosis factor-related apoptosis-inducing ligand in human ovarian carcinoma cells. Gynecol Oncol 2004, 93:594-604. 10.1016/j.ygyno.2004.03.029, 15196850.
8. Kischkel FC, Lawrence DA, Chuntharapai A, Schow P, Kim KJ, Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 2000, 12:611-620. 10.1016/S1074-7613(00)80212-5, 10894161.
9. Degli-Esposti MA, Smolak PJ, Walczak H, Waugh J, Huang CP, DuBose RF, Goodwin RG, Smith CA. Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor family. J Exp Med 1997, 186:1165-1170. 10.1084/jem.186.7.1165, 2199077, 9314565.
10. Degli-Esposti MA, Dougall WC, Smolak PJ, Waugh JY, Smith CA, Goodwin RG. The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 1997, 7:813-820. 10.1016/S1074-7613(00)80399-4, 9430226.
11. Emery JG, McDonnell P, Burke MB, Deen KC, Lyn S, Silverman C, Dul E, Appelbaum ER, Eichman C, DiPrinzio R, Dodds RA, James IE, Rosenberg M, Lee JC, Young PR. Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J Biol Chem 1998, 273:14363-14367. 10.1074/jbc.273.23.14363, 9603945.
12. Kischkel FC, Hellbardt S, Berhmann I, Germer M, Pawlita M, Krammer PH, Peter ME. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 1995, 14:5579-5588. 394672, 8521815.
13. Krueger A, Baumann S, Krammer PH, Kirchhoff S. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol Cell Biol 2001, 21:8247-8254. 10.1128/MCB.21.24.8247-8254.2001, 99990, 11713262.
14. Bagnoli M, Canevari S, Mezzanzanica D. Cellular FLICE-inhibitory protein (c-FLIP) signalling: a key regulator of receptor-mediated apoptosis in physiologic context and in cancer. Int J Biochem Cell Biol 2010, 42:210-213. 10.1016/j.biocel.2009.11.015, 19932761.
15. O'Brien TJ, Beard JB, Underwood LJ, Dennis RA, Santin AD, York L. The CA 125 gene: an extracellular superstructure dominated by repeat sequences. Tumour Biol 2001, 22:348-366. 10.1159/000050638, 11786729.
16. O'Brien TJ, Beard JB, Underwood LJ, Shigemasa K. The CA 125 gene: a newly discovered extension of the glycosylated N-terminal domain doubles the size of this extracellular superstructure. Tumour Biol 2002, 23:154-169. 10.1159/000064032, 12218296.
17. Yin BW, Lloyd KO. Molecular cloning of the CA125 ovarian cancer antigen: identification as a new mucin, MUC16. J Biol Chem 2001, 276:27371-27375. 10.1074/jbc.M103554200, 11369781.
18. Yin BW, Dnistrian A, Lloyd KO. Ovarian cancer antigen CA125 is encoded by the MUC16 mucin gene. Int J Cancer 2002, 98:737-740. 10.1002/ijc.10250, 11920644.
19. Kabawat SE, Bast RC, Welch WR, Knapp RC, Colvin RB. Immunopathologic characterization of a monoclonal antibody that recognizes common surface antigens of human ovarian tumors of serous, endometrioid, and clear cell types. Am J Clin Pathol 1983, 79:98-104.
20. Gubbels JA, Belisle J, Onda M, Rancourt C, Migneault M, Ho M, Bera TK, Connor J, Sathyanarayana BK, Lee B, Pastan I, Patankar MS. Mesothelin-MUC16 binding is a high affinity, N-glycan dependent interaction that facilitates peritoneal metastasis of ovarian tumors. Mol Cancer 2006, 5:50. 10.1186/1476-4598-5-50, 1635730, 17067392.
21. Kaneko O, Gong L, Zhang J, Hansen JK, Hassan R, Lee B, Ho M. A binding domain on mesothelin for CA125/MUC16. J Biol Chem 2009, 284:3739-3749. 10.1074/jbc.M806776200, 2635045, 19075018.
22. Rump A, Morikawa Y, Tanaka M, Minami S, Umesaki N, Takeuchi M, Miyajima A. Binding of ovarian cancer antigen CA125/MUC16 to mesothelin mediates cell adhesion. J Biol Chem 2004, 279:9190-9198. 10.1074/jbc.M312372200, 14676194.
23. Argueso P, Guzman-Aranguez A, Mantelli F, Cao Z, Ricciuto J, Panjwani N. Association of cell surface mucins with galectin-3 contributes to the ocular surface epithelial barrier. J Biol Chem 2009, 284:23037-23045. 10.1074/jbc.M109.033332, 2755710, 19556244.
24. Belisle JA, Horibata S, Jennifer GA, Petrie S, Kapur A, André S, Gabius HJ, Rancourt C, Connor J, Paulson JC, Patankar MS. Identification of Siglec-9 as the receptor for MUC16 on human NK cells, B cells, and monocytes. Mol Cancer 2010, 9:118. 10.1186/1476-4598-9-118, 2890604, 20497550.
25. Gubbels JA, Felder M, Horibata S, Belisle JA, Kapur A, Holden H, Petrie S, Migneault M, Rancourt C, Connor JP, Patankar MS. MUC16 provides immune protection by inhibiting synapse formation between NK cells and ovarian tumor cells. Mol Cancer 2010, 9:11. 10.1186/1476-4598-9-11, 2818693, 20089172.
26. Thériault C, Pinard M, Comamala M, Migneault M, Beaudin J, Matte I, Boivin M, Piché A, Rancourt C. MUC16 (CA125) regulates epithelial ovarian cancer cell growth, tumorigenesis and metastasis. Gynecol Oncol 2011, 121:434-443. 10.1016/j.ygyno.2011.02.020, 21421261.
27. Boivin M, Lane D, Piché A, Rancourt C. CA125 (MUC16) tumor antigen selectively modulates the sensitivity of ovarian cancer cells to genotoxic drug-induced apoptosis. Gynecol Oncol 2009, 115:407-413. 10.1016/j.ygyno.2009.08.007, 19747716.
28. Lane D, Côté M, Grondin M, Couture MC, Piché A. Acquired resistance to TRAIL-induced apoptosis in human ovarian cancer cells is conferred by increased turnover of mature caspase-3. Mol Cancer Ther 2006, 5:509-521. 10.1158/1535-7163.MCT-05-0362, 16546965.
29. Ott M, Norberg E, Zhivotovsky B, Orrenius S. Mitochondrial targeting of tBid/Bax: a role for the TOM complex?. Cell Death Differ 2009, 16:1075-1082. 10.1038/cdd.2009.61, 19521421.
30. Kim K, Fisher MJ, Xu SQ, El-Deiry WS. Molecular determinants of response to TRAIL in killing of normal and cancer cells. Clin Cancer Res 2000, 6:335-346.
31. Bast RC, Klug TL, St John E, Jenison E, Niloff JM, Lazarus H, Berkowitz RS, Leavitt T, Griffiths CT, Parker L, Zurawski VR, Knapp RC. A radioimmunoassay using a monoclonal antibody to monitor the course of epithelial ovarian cancer. N Engl J Med 1983, 309:883-887. 10.1056/NEJM198310133091503, 6310399.
32. Hogdall EV, Christensen L, Kjaer SK, Blaakaer J, Kjaerbye-Thygesen A, Gayther S, Jacobs IJ, Hogdall CK. CA125 expression pattern, prognosis and correlation with serum CA125 in ovarian tumor patients. From the Danish " MALOVA" ovarian cancer study. Gynecol Oncol 2007, 104:508-515. 10.1016/j.ygyno.2006.09.028, 17113137.
33. Hilkens J, Ligtenberg MJ, Vos HL, Litvinov SV. Cell membrane-associated mucins and their adhesion-modulating property. Trends Biochem Sci 1992, 17:359-363. 10.1016/0968-0004(92)90315-Z, 1412714.
34. Wesseling J, van der Valk SW, Vos HL, Sonnenberg A, Hilkens J. Episialin (MUC1) overexpression inhibits integrin-mediated cell adhesion to extracellular matrix components. J Cell Biol 1995, 129:255-265. 10.1083/jcb.129.1.255, 2120361, 7698991.
35. Komatsu M, Jepson S, Arango ME, Carothers Carraway CA, Carraway KL. Muc4/sialomucin complex, an intramembrane modulator of ErbB2/HER2/Neu, potentiates primary tumor growth and suppresses apoptosis in a xenotransplanted tumor. Oncogene 2001, 20:461-470. 10.1038/sj.onc.1204106, 11313977.
36. Satoh S, Hinoda Y, Hayashi T, Burdick MD, Imai K, Hollingsworth MA. Enhancement of metastatic properties of pancreatic cancer cells by MUC1 gene encoding an anti-adhesion molecule. Int J Cancer 2000, 88:507-518. 10.1002/1097-0215(20001115)88:4<507::AID-IJC1>3.0.CO;2-0, 11058865.
37. Singh AP, Moniaux N, Chauhan SC, Meza JL, Batra SK. Inhibition of MUC4 expression suppresses pancreatic tumor cell growth and metastasis. Cancer Res 2004, 64:622-630. 10.1158/0008-5472.CAN-03-2636, 14744777.
38. McDermott KM, Crocker PR, Harris A, Burdick MD, Hinoda Y, Hayashi T, Imai K, Hollingsworth MA. Overexpression of MUC1 reconfigures the binding properties of tumor cells. Int J Cancer 2001, 94:783-791. 10.1002/ijc.1554, 11745478.
39. Agata N, Ahmad R, Kawano T, Raina D, Kharbanda S, Kufe D. MUC1 oncoprotein blocks death receptor-mediated apoptosis by inhibiting recruitment of caspase-8. Cancer Res 2008, 68:6136-6144. 10.1158/0008-5472.CAN-08-0464, 2536759, 18676836.
40. Ren J, Agata N, Chen D, Li Y, Yu WH, Huang L, Raina D, Chen W, Kharbanda S, Kufe D. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell 2004, 5:163-175. 10.1016/S1535-6108(04)00020-0, 14998492.
41. Rancourt C, Matte I, Lane D, Piché A. The role of MUC16 mucin (CA125) in the pathogenesis of ovarian cancer. Ovarian cancer: basic science perspective. Volume 1 2012, 67-84. Croatia: InTech, Farghaly SA, 1.
42. Goncharenko-Khaider N, Lane D, Matte I, Rancourt C, Piché A. Biological significance of apoptosis in ovarian cancer: TRAIL therapeutic targeting. Ovarian cancer: a clinical and translational update. Volume 1 2013, 227-250. Croatia: InTech, Diaz-Padilla I, 1.
43. Lakshmanan I, Ponnusamy MP, Das S, Chakraborty S, Haridas D, Mukhopadhyay P, Lele SM, Batra SK. MUC16 induced rapid G2/M transition via interactions with JAK2 for increased proliferation and anti-apoptosis in breast cancer cells. Oncogene 2012, 31:805-817. 10.1038/onc.2011.297, 3288594, 21785467.
44. Dodier P, Piché A. Bcl-X(L) is functionally non-equivalent for the regulation of growth and survival in human ovarian cancer cells. Gynecol Oncol 2006, 100:254-263. 10.1016/j.ygyno.2005.08.028, 16188300.