Mesothelin confers pancreatic cancer cell resistance to TNF-α-induced apoptosis through Akt/PI3K/NF-κB activation and IL-6/Mcl-1 overexpression

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Bharadwaj, Uddalak ^a   Marin Muller, Christian ^a   Li, Min ^a,b   Chen, Changyi ^a   Yao, Qizhi ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Mesothelin; Pancreatic cancer; TNF

Indexed keywords

CASPASE 3; CYCLIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MESOTHELIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; PROTEIN MCL 1; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; WEDELOLACTONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; CHROMONE DERIVATIVE; COUMARIN DERIVATIVE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; I KAPPA B KINASE; MORPHOLINE DERIVATIVE; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; RECOMBINANT PROTEIN; RENILLA LUCIFERIN 2 MONOOXYGENASE;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER RESISTANCE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME INHIBITION; GENE OVEREXPRESSION; GENE SILENCING; GROWTH INHIBITION; HUMAN; HUMAN CELL; PANCREAS CANCER; UPREGULATION; WESTERN BLOTTING; BIOSYNTHESIS; CELL CYCLE S PHASE; CELL SURVIVAL; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; ENZYME ACTIVATION; GENE EXPRESSION; GENETICS; METABOLISM; PANCREAS TUMOR; PROTEIN TRANSPORT; REPORTER GENE; RNA INTERFERENCE; TUMOR CELL LINE;

AGOUTI PACA;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; CHROMONES; COUMARINS; CYCLIN A; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; GPI-LINKED PROTEINS; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-6; LUCIFERASES, RENILLA; MORPHOLINES; NF-KAPPA B; PANCREATIC NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RECOMBINANT PROTEINS; RNA INTERFERENCE; S PHASE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80052143814     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-106     Document Type: Article

References (49)

1. Bharadwaj U, Li M, Chen C, Yao Q. Mesothelin-induced pancreatic cancer cell proliferation involves alteration of cyclin E via activation of signal transducer and activator of transcription protein 3. Mol Cancer Res 2008, 6:1755-1765. 10.1158/1541-7786.MCR-08-0095, 2929833, 19010822.
2. Hassan R, Ho M. Mesothelin targeted cancer immunotherapy. Eur J Cancer 2008, 44:46-53. 10.1016/j.ejca.2007.08.028, 2265108, 17945478.
3. Li M, Bharadwaj U, Zhang R, Zhang S, Mu H, Fisher WE, Brunicardi FC, Chen C, Yao Q. Mesothelin is a malignant factor and therapeutic vaccine target for pancreatic cancer. Mol Cancer Ther 2008, 7:286-296. 10.1158/1535-7163.MCT-07-0483, 2929838, 18281514.
4. Uehara N, Matsuoka Y, Tsubura A. Mesothelin promotes anchorage-independent growth and prevents anoikis via extracellular signal-regulated kinase signaling pathway in human breast cancer cells. Mol Cancer Res 2008, 6:186-193. 10.1158/1541-7786.MCR-07-0254, 18245228.
5. Cheng WF, Huang CY, Chang MC, Hu YH, Chiang YC, Chen YL, Hsieh CY, Chen CA. High mesothelin correlates with chemoresistance and poor survival in epithelial ovarian carcinoma. Br J Cancer 2009, 100:1144-1153. 10.1038/sj.bjc.6604964, 2669998, 19293794.
6. Koorstra JB, Hustinx SR, Offerhaus GJ, Maitra A. Pancreatic carcinogenesis. Pancreatology 2008, 8:110-125. 10.1159/000123838, 2663569,2663569, 18382097.
7. Szlosarek P, Charles KA, Balkwill FR. Tumour necrosis factor-alpha as a tumour promoter. Eur J Cancer 2006, 42:745-750. 10.1016/j.ejca.2006.01.012, 16517151.
8. Balkwill F. TNF-alpha in promotion and progression of cancer. Cancer Metastasis Rev 2006, 25:409-416. 10.1007/s10555-006-9005-3, 16951987.
9. Carswell EA, Old LJ, Kassel RL, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci USA 1975, 72:3666-3670. 10.1073/pnas.72.9.3666, 433057, 1103152.
10. Fernandez A, Marin MC, McDonnell T, Ananthaswamy HN. Differential sensitivity of normal and Ha-ras-transformed C3H mouse embryo fibroblasts to tumor necrosis factor: induction of bcl-2, c-myc, and manganese superoxide dismutase in resistant cells. Oncogene 1994, 9:2009-2017.
11. Komori A, Yatsunami J, Suganuma M, Okabe S, Abe S, Sakai A, Sasaki K, Fujiki H. Tumor necrosis factor acts as a tumor promoter in BALB/3T3 cell transformation. Cancer Res 1993, 53:1982-1985.
12. Murugesan SR, King CR, Osborn R, Fairweather WR, O'Reilly EM, Thornton MO, Wei LL. Combination of human tumor necrosis factor-alpha (hTNF-alpha) gene delivery with gemcitabine is effective in models of pancreatic cancer. Cancer Gene Ther 2009,
13. Weichselbaum RR, Kufe D. Translation of the radio- and chemo-inducible TNFerade vector to the treatment of human cancers. Cancer Gene Ther 2009, 16:609-619. 10.1038/cgt.2009.37, 19444302.
14. Lyu MA, Kurzrock R, Rosenblum MG. The immunocytokine scFv23/TNF targeting HER-2/neu induces synergistic cytotoxic effects with 5-fluorouracil in TNF-resistant pancreatic cancer cell lines. Biochem Pharmacol 2008, 75:836-846. 10.1016/j.bcp.2007.10.013, 18082672.
15. Wang CY, Cusack EV, Liu R, Baldwin EV. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat Med 1999, 5:412-417. 10.1038/7410, 10202930.
16. Schmiegel WH, Caesar J, Kalthoff H, Greten H, Schreiber HW, Thiele HG. Antiproliferative effects exerted by recombinant human tumor necrosis factor-alpha (TNF-alpha) and interferon-gamma (IFN-gamma) on human pancreatic tumor cell lines. Pancreas 1988, 3:180-188. 10.1097/00006676-198804000-00012, 3131759.
17. Aggarwal BB, Shishodia S, Sandur SK, Pandey MK, Sethi G. Inflammation and cancer: how hot is the link?. Biochem Pharmacol 2006, 72:1605-1621. 10.1016/j.bcp.2006.06.029, 16889756.
18. Aggarwal BB. Signalling pathways of the TNF superfamily: a double-edged sword. Nat Rev Immunol 2003, 3:745-756. 10.1038/nri1184, 12949498.
19. Schmiegel W, Roeder C, Schmielau J, Rodeck U, Kalthoff H. Tumor necrosis factor alpha induces the expression of transforming growth factor alpha and the epidermal growth factor receptor in human pancreatic cancer cells. Proc Natl Acad Sci USA 1993, 90:863-867. 10.1073/pnas.90.3.863, 45770, 8430098.
20. Giri DK, Aggarwal BB. Constitutive activation of NF-kappaB causes resistance to apoptosis in human cutaneous T cell lymphoma HuT-78 cells. Autocrine role of tumor necrosis factor and reactive oxygen intermediates. J Biol Chem 1998, 273:14008-14014. 10.1074/jbc.273.22.14008, 9593751.
21. Deng X, Kornblau SM, Ruvolo PP, May EV. Regulation of Bcl2 phosphorylation and potential significance for leukemic cell chemoresistance. J Natl Cancer Inst Monogr 2001, 30-37.
22. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002, 2:647-656. 10.1038/nrc883, 12209154.
23. Downward J. How BAD phosphorylation is good for survival. Nat Cell Biol 1999, 1:E33-35. 10.1038/10026, 10559890.
24. Datta SR, Ranger AM, Lin MZ, Sturgill JF, Ma YC, Cowan CW, Dikkes P, Korsmeyer SJ, Greenberg ME. Survival factor-mediated BAD phosphorylation raises the mitochondrial threshold for apoptosis. Dev Cell 2002, 3:631-643. 10.1016/S1534-5807(02)00326-X, 12431371.
25. Eisenmann KM, VanBrocklin MW, Staffend NA, Kitchen SM, Koo HM. Mitogen-activated protein kinase pathway-dependent tumor-specific survival signaling in melanoma cells through inactivation of the proapoptotic protein bad. Cancer Res 2003, 63:8330-8337.
26. Spyridopoulos I, Mayer P, Shook KS, Axel DI, Viebahn R, Karsch KR. Loss of cyclin A and G1-cell cycle arrest are a prerequisite of ceramide-induced toxicity in human arterial endothelial cells. Cardiovasc Res 2001, 50:97-107. 10.1016/S0008-6363(01)00196-1, 11282082.
27. Volland S, Amtmann E, Sauer G. TNF accelerates the S-phase of the cell cycle in tumor cells. Int J Cancer 1994, 56:698-705. 10.1002/ijc.2910560515, 8314347.
28. Satyanarayana A, Kaldis P. Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 2009, 28:2925-2939. 10.1038/onc.2009.170, 19561645.
29. Liu CJ, Lo JF, Kuo CH, Chu CH, Chen LM, Tsai FJ, Tsai CH, Tzang BS, Kuo WW, Huang CY. Akt Mediates 17 beta-Estradiol and/or Estrogen Receptor alpha Inhibition of LPS-Induced Tumor Necrosis Factor-alpha Expression and Myocardial Cell Apoptosis by Suppressing the JNK1/2-NFkappaB Pathway. J Cell Mol Med 2009,
30. Qiu J, Xiao J, Han C, Li N, Shen X, Jiang H, Cao X. Potentiation of tumor necrosis factor-alpha-induced tumor cell apoptosis by a small molecule inhibitor for anti-apoptotic protein hPEBP4. J Biol Chem 285:12241-12247.
31. Bharadwaj U, Marin-Muller C, Li M, Chen C, Yao Q. Mesothelin Overexpression Promotes Autocrine IL-6/sIL-6R Trans-signaling to stimulate Pancreatic Cancer Cell Proliferation. Carcinogenesis 2011, 32:1013-1024. 10.1093/carcin/bgr075, 21515913.
32. Choi SE, Choi KM, Yoon IH, Shin JY, Kim JS, Park WY, Han DJ, Kim SC, Ahn C, Kim JY, et al. IL-6 protects pancreatic islet beta cells from pro-inflammatory cytokines-induced cell death and functional impairment in vitro and in vivo. Transpl Immunol 2004, 13:43-53. 10.1016/j.trim.2004.04.001, 15203128.
33. Cavarretta IT, Neuwirt H, Untergasser G, Moser PL, Zaki MH, Steiner H, Rumpold H, Fuchs D, Hobisch A, Nemeth JA, Culig Z. The antiapoptotic effect of IL-6 autocrine loop in a cellular model of advanced prostate cancer is mediated by Mcl-1. Oncogene 2007, 26:2822-2832. 10.1038/sj.onc.1210097, 17072336.
34. Bai J, Sui J, Demirjian A, Vollmer EV, Marasco W, Callery MP. Predominant Bcl-XL knockdown disables antiapoptotic mechanisms: tumor necrosis factor-related apoptosis-inducing ligand-based triple chemotherapy overcomes chemoresistance in pancreatic cancer cells in vitro. Cancer Res 2005, 65:2344-2352. 10.1158/0008-5472.CAN-04-3502, 15781649.
35. Argani P, Iacobuzio-Donahue C, Ryu B, Rosty C, Goggins M, Wilentz RE, Murugesan SR, Leach SD, Jaffee E, Yeo CJ, et al. Mesothelin is overexpressed in the vast majority of ductal adenocarcinomas of the pancreas: identification of a new pancreatic cancer marker by serial analysis of gene expression (SAGE). Clin Cancer Res 2001, 7:3862-3868.
36. Catalan MP, Subira D, Reyero A, Selgas R, Ortiz-Gonzalez A, Egido J, Ortiz A. Regulation of apoptosis by lethal cytokines in human mesothelial cells. Kidney Int 2003, 64:321-330. 10.1046/j.1523-1755.2003.00062.x, 12787425.
37. Gordon GJ, Mani M, Mukhopadhyay L, Dong L, Yeap BY, Sugarbaker DJ, Bueno R. Inhibitor of apoptosis proteins are regulated by tumour necrosis factor-alpha in malignant pleural mesothelioma. J Pathol 2007, 211:439-446. 10.1002/path.2120, 17253597.
38. Yang H, Bocchetta M, Kroczynska B, Elmishad AG, Chen Y, Liu Z, Bubici C, Mossman BT, Pass HI, Testa JR, et al. TNF-alpha inhibits asbestos-induced cytotoxicity via a NF-kappaB-dependent pathway, a possible mechanism for asbestos-induced oncogenesis. Proc Natl Acad Sci USA 2006, 103:10397-10402. 10.1073/pnas.0604008103, 1502469, 16798876.
39. Kalthoff H, Roeder C, Humburg I, Thiele HG, Greten H, Schmiegel W. Modulation of platelet-derived growth factor A- and B-chain/c-sis mRNA by tumor necrosis factor and other agents in adenocarcinoma cells. Oncogene 1991, 6:1015-1021.
40. Yip KW, Reed JC. Bcl-2 family proteins and cancer. Oncogene 2008, 27:6398-6406. 10.1038/onc.2008.307, 18955968.
41. Deng X, Ruvolo P, Carr B, May EV. Survival function of ERK1/2 as IL-3-activated, staurosporine-resistant Bcl2 kinases. Proc Natl Acad Sci USA 2000, 97:1578-1583. 10.1073/pnas.97.4.1578, 26477, 10677502.
42. Bergmann A. Survival signaling goes BAD. Dev Cell 2002, 3:607-608. 10.1016/S1534-5807(02)00328-3, 12431365.
43. Chao OS, Clement MV. Epidermal growth factor and serum activate distinct pathways to inhibit the BH3 only protein BAD in prostate carcinoma LNCaP cells. Oncogene 2006, 25:4458-4469. 10.1038/sj.onc.1209421, 16767165.
44. Ricci MS, Kim SH, Ogi K, Plastaras JP, Ling J, Wang W, Jin Z, Liu YY, Dicker DT, Chiao PJ, et al. Reduction of TRAIL-induced Mcl-1 and cIAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 2007, 12:66-80. 10.1016/j.ccr.2007.05.006, 17613437.
45. Wang X, Chen W, Zeng W, Bai L, Tesfaigzi Y, Belinsky SA, Lin Y. Akt-mediated eminent expression of c-FLIP and Mcl-1 confers acquired resistance to TRAIL-induced cytotoxicity to lung cancer cells. Mol Cancer Ther 2008, 7:1156-1163. 10.1158/1535-7163.MCT-07-2183, 2715176, 18483303.
46. Huang S, Sinicrope FA. BH3 mimetic ABT-737 potentiates TRAIL-mediated apoptotic signaling by unsequestering Bim and Bak in human pancreatic cancer cells. Cancer Res 2008, 68:2944-2951. 10.1158/0008-5472.CAN-07-2508, 2948486, 18413764.
47. Chang MC, Chen CA, Hsieh CY, Lee CN, Su YN, Hu YH, Cheng WF. Mesothelin inhibits paclitaxel-induced apoptosis through the PI3K pathway. Biochem J 2009, 424:449-458. 10.1042/BJ20082196, 19747165.
48. Hou LQ, Wang YH, Liu LJ, Guo J, Teng LP, Cao LH, Shi H, Yuan L, De W. Expression and localization of mesothelin in developing rat pancreas. Dev Growth Differ 2008, 50:531-541. 10.1111/j.1440-169X.2008.01047.x, 18505465.
49. Ledda-Columbano GM, Curto M, Piga R, Zedda AI, Menegazzi M, Sartori C, Shinozuka H, Bluethmann H, Poli V, Ciliberto G, Columbano A. In vivo hepatocyte proliferation is inducible through a TNF and IL-6-independent pathway. Oncogene 1998, 17:1039-1044. 10.1038/sj.onc.1202018, 9747883.