Par-4 downregulation confers cisplatin resistance in pancreatic cancer cells via PI3K/Akt pathway-dependent EMT

Toxicology Letters

Volumn 224, Issue 1, 2014, Pages 7-15

  Tan, Jiaxin ^a   You, Yu ^a   Xu, Tubin ^a   Yu, Peng ^a   Wu, Dingguo ^a   Deng, Hao ^a   Zhang, Yujun ^a   Bie, Ping ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

CDDP, Cisplatin; EMT, Epithelial to mesenchymal transition; Pancreatic cancer; Par 4, prostate apoptosis response 4; PI3K Akt

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CISPLATIN; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTATE APOPTOSIS RESPONSE 4; PROTEIN KINASE B; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; IN VIVO STUDY; MOUSE; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR VOLUME; TUMOR XENOGRAFT; WESTERN BLOTTING;

CDDP, CISPLATIN; EMT, EPITHELIAL TO MESENCHYMAL TRANSITION; PANCREATIC CANCER; PAR-4, PROSTATE APOPTOSIS RESPONSE-4; PI3K/AKT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; BASE SEQUENCE; CELL LINE, TUMOR; CISPLATIN; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PANCREATIC NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84887215930     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.10.008     Document Type: Article

References (33)

1. Alvarez J.V., Pan T.C., Ruth J., Feng Y., Zhou A., Pant D., Grimley J.S., Wandless T.J., Demichele A., Chodosh L.A. Par-4 downregulation promotes breast cancer recurrence by preventing multinucleation following targeted therapy. Cancer Cell 2013, 24:30-44.
2. 2+ signaling in mouse lung alveolar epithelial cells. Life Sci. 2007, 81:794-802.
3. Arumugam T., Ramachandran V., Fournier K.F., Wang H., Marquis L., Abbruzzese J.L., Gallick G.E., Logsdon C.D., McConkey D.J., Choi W. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 2009, 69:5820-5828.
4. Azmi A.S., Wang Z., Burikhanov R., Rangnekar V.M., Wang G., Chen J., Wang S., Sarkar F.H., Mohammad R.M. Critical role of prostate apoptosis response-4 in determining the sensitivity of pancreatic cancer cells to small-molecule inhibitor-induced apoptosis. Mol. Cancer Ther. 2008, 7:2884-2893.
5. Bardeesy N., DePinho R.A. Pancreatic cancer biology and genetics. Nat. Rev. Cancer 2002, 2:897-909.
6. Barradas M., Monjas A., Diaz-Meco M.T., Serrano M., Moscat J. The downregulation of the pro-apoptotic protein Par-4 is critical for Ras-induced survival and tumor progression. EMBO J. 1999, 18:6362-6369.
7. Bergmann M., Kukoc-Zivojnov N., Chow K.U., Trepohl B., Hoelzer D., Weidmann E., Mitrou P.S., Boehrer S. Prostate apoptosis response gene-4 sensitizes neoplastic lymphocytes to CD95-induced apoptosis. Ann. Hematol. 2004, 83:646-653.
8. Blume-Jensen P., Hunter T. Oncogenic kinase signalling. Nature 2001, 411:355-365.
9. Boehrer S., Nowak D., Puccetti E., Ruthardt M., Sattler N., Trepohl B., Schneider B., Hoelzer D., Mitrou P.S., Chow K.U. Prostate-apoptosis-response-gene-4 increases sensitivity to TRAIL-induced apoptosis. Leuk. Res. 2006, 30:597-605.
10. Burikhanov R., Zhao Y., Goswami A., Qiu S., Schwarze S.R., Rangnekar V.M. The tumor suppressor Par-4 activates an extrinsic pathway for apoptosis. Cell 2009, 138:377-388.
11. Cantore M., Fiorentini G., Luppi G., Rosati G., Caudana R., Piazza E., Comella G., Ceravolo C., Miserocchi L., Mambrini A., Del Freo A., Zamagni D., Aitini E., Marangolo M. Randomised trial of gemcitabine versus flec regimen given intra-arterially for patients with unresectable pancreatic cancer. J. Exp. Clin. Cancer Res. 2003, 22:51-57.
12. Cook J., Krishnan S., Ananth S., Sells S.F., Shi Y., Walther M.M., Linehan W.M., Sukhatme V.P., Weinstein M.H., Rangnekar V.M. Decreased expression of the pro-apoptotic protein Par-4 in renal cell carcinoma. Oncogene 1999, 18:1205-1208.
13. Diaz-Meco M.T., Abu-Baker S. The Par-4/PTEN connection in tumor suppression. Cell Cycle 2009, 8:2518-2522.
14. Diaz-Meco M.T., Moscat J. Akt regulation and lung cancer: a novel role and mechanism of action for the tumor suppressor Par-4. Cell Cycle 2008, 7:2817-2820.
15. El-Guendy N., Zhao Y., Gurumurthy S., Burikhanov R., Rangnekar V.M. Identification of a unique core domain of par-4 sufficient for selective apoptosis induction in cancer cells. Mol. Cell. Biol. 2003, 23:5516-5525.
16. Ellenrieder V., Hendler S.F., Ruhland C., Boeck W., Adler G., Gress T.M. TGF-beta-induced invasiveness of pancreatic cancer cells is mediated by matrix metalloproteinase-2 and the urokinase plasminogen activator system. Int. J. Cancer 2001, 93:204-211.
17. Fernandez-Marcos P.J., Abu-Baker S., Joshi J., Galvez A., Castilla E.A., Canamero M., Collado M., Saez C., Moreno-Bueno G., Palacios J., Leitges M., Serrano M., Moscat J., Diaz-Meco M.T. Simultaneous inactivation of Par-4 and PTEN in vivo leads to synergistic NF-kappaB activation and invasive prostate carcinoma. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12962-12967.
18. Haslehurst A.M., Koti M., Dharsee M., Nuin P., Evans K., Geraci J., Childs T., Chen J., Li J., Weberpals J., Davey S., Squire J., Park P.C., Feilotter H. EMT transcription factors snail and slug directly contribute to cisplatin resistance in ovarian cancer. BMC Cancer 2012, 12:91.
19. Joshi J., Fernandez-Marcos P.J., Galvez A., Amanchy R., Linares J.F., Duran A., Pathrose P., Leitges M., Canamero M., Collado M., Salas C., Serrano M., Moscat J., Diaz-Meco M.T. Par-4 inhibits Akt and suppresses Ras-induced lung tumorigenesis. EMBO J. 2008, 27:2181-2193.
20. Kang Y., Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 2004, 118:277-279.
21. Kline C.L., Shanmugavelandy S.S., Kester M., Irby R.B. Delivery of PAR-4 plasmid in vivo via nanoliposomes sensitizes colon tumor cells subcutaneously implanted into nude mice to 5-FU. Cancer Biol. Ther. 2009, 8:1831-1837.
22. Leake K., Singhal J., Nagaprashantha L.D., Awasthi S., Singhal S.S. RLIP76 regulates PI3K/Akt signaling and chemo-radiotherapy resistance in pancreatic cancer. PLoS ONE 2012, 7:e34582.
23. Maseki S., Ijichi K., Tanaka H., Fujii M., Hasegawa Y., Ogawa T., Murakami S., Kondo E., Nakanishi H. Acquisition of EMT phenotype in the gefitinib-resistant cells of a head and neck squamous cell carcinoma cell line through Akt/GSK-3beta/snail signalling pathway. Br. J. Cancer 2012, 106:1196-1204.
24. Nagai M.A., Gerhard R., Salaorni S., Fregnani J.H., Nonogaki S., Netto M.M., Soares F.A. Down-regulation of the candidate tumor suppressor gene PAR-4 is associated with poor prognosis in breast cancer. Int. J. Oncol. 2010, 37:41-49.
25. Osaki M., Oshimura M., Ito H. PI3K-Akt pathway: its functions and alterations in human cancer. Apoptosis 2004, 9:667-676.
26. Rah B., Amin H., Yousuf K., Khan S., Jamwal G., Mukherjee D., Goswami A. A novel MMP-2 inhibitor 3-azidowithaferin A (3-azidoWA) abrogates cancer cell invasion and angiogenesis by modulating extracellular Par-4. PLoS ONE 2012, 7:e44039.
27. Sells S.F., Han S.S., Muthukkumar S., Maddiwar N., Johnstone R., Boghaert E., Gillis D., Liu G., Nair P., Monnig S., Collini P., Mattson M.P., Sukhatme V.P., Zimmer S.G., Wood D.P., McRoberts J.W., Shi Y., Rangnekar V.M. Expression and function of the leucine zipper protein Par-4 in apoptosis. Mol. Cell. Biol. 1997, 17:3823-3832.
28. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2002, 2:442-454.
29. Vivanco I., Sawyers C.L. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2002, 2:489-501.
30. Wang B.D., Kline C.L., Pastor D.M., Olson T.L., Frank B., Luu T., Sharma A.K., Robertson G., Weirauch M.T., Patierno S.R., Stuart J.M., Irby R.B., Lee N.H. Prostate apoptosis response protein 4 sensitizes human colon cancer cells to chemotherapeutic 5-FU through mediation of an NF kappaB and microRNA network. Mol. Cancer 2010, 9:98.
31. Wang X.J., Feng C.W., Li M. ADAM17 mediates hypoxia-induced drug resistance in hepatocellular carcinoma cells through activation of EGFR/PI3K/Akt pathway. Mol. Cell. Biochem. 2013, 380:57-66.
32. West K.A., Castillo S.S., Dennis P.A. Activation of the PI3K/Akt pathway and chemotherapeutic resistance. Drug Resist. Updat. 2002, 5:234-248.
33. Witta S.E., Gemmill R.M., Hirsch F.R., Coldren C.D., Hedman K., Ravdel L., Helfrich B., Dziadziuszko R., Chan D.C., Sugita M., Chan Z., Baron A., Franklin W., Drabkin H.A., Girard L., Gazdar A.F., Minna J.D., Bunn P.A. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res. 2006, 66:944-950.