PERK 1/2 inhibit Caspase-8 induced apoptosis in cancer cells by phosphorylating it in a cell cycle specific manner

Molecular Oncology

Volumn 8, Issue 2, 2014, Pages 232-249

  Mandal, Ranadip ^a,b   Raab, Monika ^a,c   Matthess, Yves ^a,b   Becker, Sven ^a   Knecht, Rainald ^c   Strebhardt, Klaus ^a,b  

^a GOETHE UNIVERSITY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Apoptosis; Caspase 8; Cell cycle; PERK 1 2

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CASPASE 8; CYCLIN DEPENDENT KINASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VASCULOTROPIN RECEPTOR;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERPHASE; MITOSIS; NONHUMAN; OVARY CANCER; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RNA INTERFERENCE; BREAST CANCER CELL LINE; CELL CYCLE; IN VIVO STUDY; MASS SPECTROMETRY; OVARIAN CANCER CELL LINE;

APOPTOSIS; CASPASE-8; CELL-CYCLE; PERK 1/2;

APOPTOSIS; BREAST NEOPLASMS; CASPASE 8; CELL CYCLE; CELL LINE, TUMOR; FEMALE; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; PHOSPHORYLATION;

EID: 84894305596     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.11.003     Document Type: Article

References (58)

1. Alvarado-Kristensson M., Melander F., Leandersson K., Ronnstrand L., Wernstedt C., Andersson T. p38-MAPK signals survival by phosphorylation of caspase-8 and caspase-3 in human neutrophils. J.Exp. Med. 2004, 199:449-458.
2. Anastassiadis T., Deacon S.W., Devarajan K., Ma H., Peterson J.R. Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat. Biotechnol. 2011, 29:1039-1045.
3. Bellail A.C., Qi L., Mulligan P., Chhabra V., Hao C. TRAIL agonists on clinical trials for cancer therapy: the promises and the challenges. Rev. Recent Clin. Trials 2009, 4:34-41.
4. Brunet A., Roux D., Lenormand P., Dowd S., Keyse S., Pouyssegur J. Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 1999, 18:664-674.
5. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X. Biochemical pathways of caspase activation during apoptosis. Ann. Rev. Cell Dev. Biol. 1999, 15:269-290.
6. Chambard J.C., Lefloch R., Pouyssegur J., Lenormand P. ERK implication in cell cycle regulation. Biochim. Biophys. Acta 2007, 1773:1299-1310.
7. Cursi S., Rufini A., Stagni V., Condo I., Matafora V., Bachi A., Bonifazi A.P., Coppola L., Superti-Furga G., Testi R., Barila D. Src kinase phosphorylates Caspase-8 on Tyr380: a novel mechanism of apoptosis suppression. EMBO J. 2006, 25:1895-1905.
8. Davis M.I., Hunt J.P., Herrgard S., Ciceri P., Wodicka L.M., Pallares G., Hocker M., Treiber D.K., Zarrinkar P.P. Comprehensive analysis of kinase inhibitor selectivity. Nat. Biotechnol. 2011, 29:1046-1051.
9. Dong Y., Sui L., Tai Y., Sugimoto K., Tokuda M. The overexpression of cyclin-dependent kinase (CDK) 2 in laryngeal squamous cell carcinomas. Anticancer Res. 2001, 21:103-108.
10. Eskes R., Desagher S., Antonsson B., Martinou J.C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell. Biol. 2000, 20:929-935.
11. Fernandez-Medarde A., Santos E. Ras in cancer and developmental diseases. Genes Cancer 2011, 2:344-358.
12. Ferreira K.S., Kreutz C., Macnelly S., Neubert K., Haber A., Bogyo M., Timmer J., Borner C. Caspase-3 feeds back on caspase-8, Bid and XIAP in type I Fas signaling in primary mouse hepatocytes. Apopt. Int. J. Program. Cell Death 2012, 17:503-515.
13. Fulda S. Caspase-8 in cancer biology and therapy. Cancer Lett. 2009, 281:128-133.
14. Fulda S., Debatin K.M. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006, 25:4798-4811.
15. Fulda S., Meyer E., Debatin K.M. Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene 2002, 21:2283-2294.
16. Gillissen B., Richter A., Richter A., Overkamp T., Essmann F., Hemmati P.G., Preissner R., Belka C., Daniel P.T. Targeted therapy of the XIAP/proteasome pathway overcomes TRAIL-resistance in carcinoma by switching apoptosis signaling to a Bax/Bak-independent 'type I' mode. Cell Death Dis. 2013, 4:e643.
17. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
18. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
19. Harding A., Giles N., Burgess A., Hancock J.F., Gabrielli B.G. Mechanism of mitosis-specific activation of MEK1. J.Biol. Chem. 2003, 278:16747-16754.
20. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407:770-776.
21. Holmstrom T.H., Chow S.C., Elo I., Coffey E.T., Orrenius S., Sistonen L., Eriksson J.E. Suppression of Fas/APO-1-mediated apoptosis by mitogen-activated kinase signaling. J.Immunol. 1998, 160:2626-2636.
22. Holmstrom T.H., Schmitz I., Soderstrom T.S., Poukkula M., Johnson V.L., Chow S.C., Krammer P.H., Eriksson J.E. MAPK/ERK signaling in activated T cells inhibits CD95/Fas-mediated apoptosis downstream of DISC assembly. EMBO J. 2000, 19:5418-5428.
23. Hu B., Mitra J., van den Heuvel S., Enders G.H. S and G2 phase roles for Cdk2 revealed by inducible expression of a dominant-negative mutant in human cells. Mol. Cell. Biol. 2001, 21:2755-2766.
24. Kappel S., Matthess Y., Kaufmann M., Strebhardt K. Silencing of mammalian genes by tetracycline-inducible shRNA expression. Nature Prot. 2007, 2:3257-3269.
25. Kurokawa M., Kornbluth S. Caspases and kinases in a death grip. Cell 2009, 138:838-854.
26. Lawen A. Apoptosis-an introduction. Bioessays 2003, 25:888-896.
27. Lee M.W., Bach J.H., Lee H.J., Lee D.Y., Joo W.S., Kim Y.S., Park S.C., Kim K.Y., Lee W.B., Kim S.S. The activation of ERK1/2 via a tyrosine kinase pathway attenuates trail-induced apoptosis in HeLa cells. Cancer Invest 2005, 23:586-592.
28. Lev D.C., Kim L.S., Melnikova V., Ruiz M., Ananthaswamy H.N., Price J.E. Dual blockade of EGFR and ERK1/2 phosphorylation potentiates growth inhibition of breast cancer cells. Br. J. Cancer 2004, 91:795-802.
29. Liu X., Yan S., Zhou T., Terada Y., Erikson R.L. The MAP kinase pathway is required for entry into mitosis and cell survival. Oncogene 2004, 23:763-776.
30. Lo R.S. Receptor tyrosine kinases in cancer escape from BRAF inhibitors. Cell Res. 2012, 22:945-947.
31. Matthess Y., Raab M., Sanhaji M., Lavrik I.N., Strebhardt K. Cdk1/cyclin B1 controls Fas-mediated apoptosis by regulating caspase-8 activity. Mol. Cell. Biol. 2010, 30:5726-5740.
32. McCubrey J.A., Steelman L.S., Chappell W.H., Abrams S.L., Wong E.W., Chang F., Lehmann B., Terrian D.M., Milella M., Tafuri A., Stivala F., Libra M., Basecke J., Evangelisti C., Martelli A.M., Franklin R.A. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim. Biophys. Acta 2007, 1773:1263-1284.
33. Meloche S. Cell cycle reentry of mammalian fibroblasts is accompanied by the sustained activation of p44mapk and p42mapk isoforms in the G1 phase and their inactivation at the G1/S transition. J.Cell Physiol. 1995, 163:577-588.
34. Meloche S., Pouyssegur J. The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. Oncogene 2007, 26:3227-3239.
35. Ozoren N., El-Deiry W.S. Defining characteristics of Types I and II apoptotic cells in response to TRAIL. Neoplasia 2002, 4:551-557.
36. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 2001, 22:153-183.
37. Pearson M.A., Fabbro D. Targeting protein kinases in cancer therapy: a success?. Expert Rev. Anticancer Ther. 2004, 4:1113-1124.
38. Peng C., Cho Y.Y., Zhu F., Zhang J., Wen W., Xu Y., Yao K., Ma W.Y., Bode A.M., Dong Z. Phosphorylation of caspase-8 (Thr-263) by ribosomal S6 kinase 2 (RSK2) mediates caspase-8 ubiquitination and stability. J.Biol. Chem. 2011, 286:6946-6954.
39. Pucci B., Indelicato M., Paradisi V., Reali V., Pellegrini L., Aventaggiato M., Karpinich N.O., Fini M., Russo M.A., Farber J.L., Tafani M. ERK-1 MAP kinase prevents TNF-induced apoptosis through bad phosphorylation and inhibition of Bax translocation in HeLa Cells. J.Cell Biochem. 2009, 108:1166-1174.
40. Raab M., Kappel S., Kramer A., Sanhaji M., Matthess Y., Kurunci-Csacsko E., Calzada-Wack J., Rathkolb B., Rozman J., Adler T., Busch D.H., Esposito I., Fuchs H., Gailus-Durner V., Klingenspor M., Wolf E., Sanger N., Prinz F., Angelis M.H., Seibler J., Yuan J., Bergmann M., Knecht R., Kreft B., Strebhardt K. Toxicity modelling of Plk1-targeted therapies in genetically engineered mice and cultured primary mammalian cells. Nature Comm. 2011, 2:395.
41. Roux P.P., Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 2004, 68:320-344.
42. Satyamoorthy K., Li G., Gerrero M.R., Brose M.S., Volpe P., Weber B.L., Van Belle P., Elder D.E., Herlyn M. Constitutive mitogen-activated protein kinase activation in melanoma is mediated by both BRAF mutations and autocrine growth factor stimulation. Cancer Res. 2003, 63:756-759.
43. Schungel S., Buitrago-Molina L.E., Nalapareddy P., Lebofsky M., Manns M.P., Jaeschke H., Gross A., Vogel A. The strength of the Fas ligand signal determines whether hepatocytes act as type 1 or type 2 cells in murine livers. Hepatology 2009, 50:1558-1566.
44. Spankuch-Schmitt B., Bereiter-Hahn J., Kaufmann M., Strebhardt K. Effect of RNA silencing of polo-like kinase-1 (PLK1) on apoptosis and spindle formation in human cancer cells. J.Natl. Cancer Inst. 2002, 94:1863-1877.
45. Spankuch B., Matthess Y., Knecht R., Zimmer B., Kaufmann M., Strebhardt K. Cancer inhibition in nude mice after systemic application of U6 promoter-driven short hairpin RNAs against PLK1. J.Natl. Cancer Inst. 2004, 96:862-872.
46. Steinmetz R., Wagoner H.A., Zeng P., Hammond J.R., Hannon T.S., Meyers J.L., Pescovitz O.H. Mechanisms regulating the constitutive activation of the extracellular signal-regulated kinase (ERK) signaling pathway in ovarian cancer and the effect of ribonucleic acid interference for ERK1/2 on cancer cell proliferation. Mol. Endocrinol. 2004, 18:2570-2582.
47. Towatari M., Iida H., Tanimoto M., Iwata H., Hamaguchi M., Saito H. Constitutive activation of mitogen-activated protein kinase pathway in acute leukemia cells. Leukemia 1997, 11:479-484.
48. Tran S.E., Holmstrom T.H., Ahonen M., Kahari V.M., Eriksson J.E. MAPK/ERK overrides the apoptotic signaling from Fas, TNF, and TRAIL receptors. J.Biol. Chem. 2001, 276:16484-16490.
49. Wada T., Penninger J.M. Mitogen-activated protein kinases in apoptosis regulation. Oncogene 2004, 23:2838-2849.
50. Wagner K.W., Engels I.H., Deveraux Q.L. Caspase-2 can function upstream of bid cleavage in the TRAIL apoptosis pathway. J.Biol. Chem. 2004, 279:35047-35052.
51. Weibrecht I., Leuchowius K.J., Clausson C.M., Conze T., Jarvius M., Howell W.M., Kamali-Moghaddam M., Soderberg O. Proximity ligation assays: a recent addition to the proteomics toolbox. Exp. Rev. Proteom. 2010, 7:401-409.
52. Westphal S., Kalthoff H. Apoptosis: targets in pancreatic cancer. Mol. Cancer 2003, 2:6.
53. Yamamoto T., Ebisuya M., Ashida F., Okamoto K., Yonehara S., Nishida E. Continuous ERK activation downregulates antiproliferative genes throughout G1 phase to allow cell-cycle progression. Curr. Biol. 2006, 16:1171-1182.
54. Yuan J., Sanhaji M., Kramer A., Reindl W., Hofmann M., Kreis N.N., Zimmer B., Berg T., Strebhardt K. Polo-box domain inhibitor poloxin activates the spindle assembly checkpoint and inhibits tumor growth invivo. Am. J. Pathol. 2011, 179:2091-2099.
55. Yuan J., Yan R., Kramer A., Eckerdt F., Roller M., Kaufmann M., Strebhardt K. Cyclin B1 depletion inhibits proliferation and induces apoptosis in human tumor cells. Oncogene 2004, 23:5843-5852.
56. Zhang L., Fang B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther. 2005, 12:228-237.
57. Zhang X.D., Borrow J.M., Zhang X.Y., Nguyen T., Hersey P. Activation of ERK1/2 protects melanoma cells from TRAIL-induced apoptosis by inhibiting Smac/DIABLO release from mitochondria. Oncogene 2003, 22:2869-2881.
58. Zhou L., Tan X., Kamohara H., Wang W., Wang B., Liu J., Egami H., Baba H., Dai X. MEK1 and MEK2 isoforms regulate distinct functions in pancreatic cancer cells. Oncol. Rep. 2010, 24:251-255.