Sequential Cdk1 and Plk1 phosphorylation of caspase-8 triggers apoptotic cell death during mitosis

Molecular Oncology

Volumn 8, Issue 3, 2014, Pages 596-608

  Matthess, Yves ^a,b   Raab, Monika ^a,c   Knecht, Rainald ^c   Becker, Sven ^a   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; Cell cycle; Polo like kinase

Indexed keywords

CASPASE 8; CYCLIN B1; EPITOPE; FAS ANTIGEN; POLO LIKE KINASE 1; PROCASPASE 8; CDK1 PROTEIN, HUMAN; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

APOPTOSIS; ARTICLE; BINDING SITE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MITOSIS; PRIORITY JOURNAL; RNA INTERFERENCE; STIMULATION; ANTAGONISTS AND INHIBITORS; CELL CYCLE; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MUTATION; NEOPLASM; PATHOLOGY; PHOSPHORYLATION;

APOPTOSIS; CASPASE 8; CELL CYCLE; CELL CYCLE PROTEINS; CYCLIN-DEPENDENT KINASES; HELA CELLS; HUMANS; MITOSIS; MUTATION; NEOPLASMS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS;

EID: 84899139994     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.12.013     Document Type: Article

References (54)

1. Allan L.A., Clarke P.R. Phosphorylation of caspase-9 by CDK1/cyclin B1 protects mitotic cells against apoptosis. Mol. Cell 2007, 26:301-310.
2. 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.
3. Andersen J.L., Johnson C.E., Freel C.D., Parrish A.B., Day J.L., Buchakjian M.R., Nutt L.K., Thompson J.W., Moseley M.A., Kornbluth S. Restraint of apoptosis during mitosis through interdomain phosphorylation of caspase-2. EMBO J. 2009, 28:3216-3227.
4. Archambault V., D'Avino P.P., Deery M.J., Lilley K.S., Glover D.M. Sequestration of polo kinase to microtubules by phosphopriming-independent binding to Map205 is relieved by phosphorylation at a CDK site in mitosis. Genes Dev. 2008, 22:2707-2720.
5. Boatright K.M., Renatus M., Scott F.L., Sperandio S., Shin H., Pedersen I.M., Ricci J.E., Edris W.A., Sutherlin D.P., Green D.R., Salvesen G.S. A unified model for apical caspase activation. Mol. Cell 2003, 11:529-541.
6. Cox A., Dunning A.M., Garcia-Closas M., Balasubramanian S., Reed M.W., Pooley K.A., Scollen S., Baynes C., Ponder B.A., Chanock S., Lissowska J., Brinton L., Peplonska B., Southey M.C., Hopper J.L., McCredie M.R., Giles G.G., Fletcher O., Johnson N., dos Santos Silva I., Gibson L., Bojesen S.E., Nordestgaard B.G., Axelsson C.K., Torres D., Hamann U., Justenhoven C., Brauch H., Chang-Claude J., Kropp S., Risch A., Wang-Gohrke S., Schurmann P., Bogdanova N., Dork T., Fagerholm R., Aaltonen K., Blomqvist C., Nevanlinna H., Seal S., Renwick A., Stratton M.R., Rahman N., Sangrajrang S., Hughes D., Odefrey F., Brennan P., Spurdle A.B., Chenevix-Trench G., Beesley J., Mannermaa A., Hartikainen J., Kataja V., Kosma V.M., Couch F.J., Olson J.E., Goode E.L., Broeks A., Schmidt M.K., Hogervorst F.B., Van't Veer L.J., Kang D., Yoo K.Y., Noh D.Y., Ahn S.H., Wedren S., Hall P., Low Y.L., Liu J., Milne R.L., Ribas G., Gonzalez-Neira A., Benitez J., Sigurdson A.J., Stredrick D.L., Alexander B.H., Struewing J.P., Pharoah P.D., Easton D.F. A common coding variant in CASP8 is associated with breast cancer risk. Nat. Genet. 2007, 39:352-358.
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. Elia A.E., Cantley L.C., Yaffe M.B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 2003, 299:1228-1231.
9. Elia A.E., Rellos P., Haire L.F., Chao J.W., Ivins F.J., Hoepker K., Mohammad D., Cantley L.C., Smerdon S.J., Yaffe M.B. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 2003, 115:83-95.
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. Fischer U., Stroh C., Schulze-Osthoff K. Unique and overlapping substrate specificities of caspase-8 and caspase-10. Oncogene 2006, 25:152-159.
12. Fulda S. Caspase-8 in cancer biology and therapy. Cancer Lett. 2009, 281:128-133.
13. Fulda S., Debatin K.M. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006, 25:4798-4811.
14. Fulda S., Meyer E., Debatin K.M. Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene 2002, 21:2283-2294.
15. 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.
16. Golks A., Brenner D., Fritsch C., Krammer P.H., Lavrik I.N. c-FLIPR, a new regulator of death receptor-induced apoptosis. J.Biol. Chem. 2005, 280:14507-14513.
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. Harley M.E., Allan L.A., Sanderson H.S., Clarke P.R. Phosphorylation of Mcl-1 by CDK1-cyclin B1 initiates its Cdc20-dependent destruction during mitotic arrest. EMBO J. 2010, 29:2407-2420.
20. Jang M.S., Lee S.J., Kang N.S., Kim E. Cooperative phosphorylation of FADD by Aur-A and Plk1 in response to taxol triggers both apoptotic and necrotic cell death. Cancer Res. 2011, 71:7207-7215.
21. Jang M.S., Lee S.J., Kim C.J., Lee C.W., Kim E. Phosphorylation by polo-like kinase 1 induces the tumor-suppressing activity of FADD. Oncogene 2011, 30:471-481.
22. Jang Y.J., Lin C.Y., Ma S., Erikson R.L. Functional studies on the role of the C-terminal domain of mammalian polo-like kinase. Proc. Nat. Acad. Sci. U. S. A. 2002, 99:1984-1989.
23. Kischkel F.C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P.H., Peter M.E. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 1995, 14:5579-5588.
24. Krammer P.H., Arnold R., Lavrik I.N. Life and death in peripheral T cells. Nat. Rev. Immunol. 2007, 7:532-542.
25. Lee K.S., Grenfell T.Z., Yarm F.R., Erikson R.L. Mutation of the polo-box disrupts localization and mitotic functions of the mammalian polo kinase Plk. Proc. Nat. Acad. Sci. U. S. A. 1998, 95:9301-9306.
26. Lee K.S., Park J.E., Kang Y.H., Zimmerman W., Soung N.K., Seong Y.S., Kwak S.J., Erikson R.L. Mechanisms of mammalian polo-like kinase 1 (Plk1) localization: self- versus non-self-priming. Cell Cycle 2008, 7:141-145.
27. Litvak V., Argov R., Dahan N., Ramachandran S., Amarilio R., Shainskaya A., Lev S. Mitotic phosphorylation of the peripheral Golgi protein Nir2 by Cdk1 provides a docking mechanism for Plk1 and affects cytokinesis completion. Mol. Cell 2004, 14:319-330.
28. Mac Fhearraigh S., Mc Gee M.M. Cyclin B1 interacts with the BH3-only protein Bim and mediates its phosphorylation by Cdk1 during mitosis. Cell Cycle 2011, 10:3886-3896.
29. Mansilla S., Priebe W., Portugal J. Mitotic catastrophe results in cell death by caspase-dependent and caspase-independent mechanisms. Cell Cycle 2006, 5:53-60.
30. 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.
31. McInnes C., Wyatt M.D. PLK1 as an oncology target: current status and future potential. Drug Discov. Today 2011, 16:619-625.
32. Muzio M., Chinnaiyan A.M., Kischkel F.C., O'Rourke K., Shevchenko A., Ni J., Scaffidi C., Bretz J.D., Zhang M., Gentz R., Mann M., Krammer P.H., Peter M.E., Dixit V.M. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 1996, 85:817-827.
33. Muzio M., Stockwell B.R., Stennicke H.R., Salvesen G.S., Dixit V.M. An induced proximity model for caspase-8 activation. J.Biol. Chem. 1998, 273:2926-2930.
34. Nakajima H., Toyoshima-Morimoto F., Taniguchi E., Nishida E. Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J.Biol. Chem. 2003, 278:25277-25280.
35. Nigg E.A. Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2001, 2:21-32.
36. O'Donovan D.S., MacFhearraigh S., Whitfield J., Swigart L.B., Evan G.I., Mc Gee M.M. Sequential Cdk1 and Plk1 phosphorylation of protein tyrosine phosphatase 1B promotes mitotic cell death. Cell Death Dis. 2013, 4:e468.
37. Oberst A., Green D.R. It cuts both ways: reconciling the dual roles of caspase 8 in cell death and survival. Nat. Rev. Mol. Cell Biol. 2011, 12:757-763.
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. 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 Commun. 2011, 2:395.
40. Reindl W., Yuan J., Kramer A., Strebhardt K., Berg T. Inhibition of polo-like kinase 1 by blocking polo-box domain-dependent protein-protein interactions. Chem. Biol. 2008, 15:459-466.
41. Rizzolio F., Tuccinardi T., Caligiuri I., Lucchetti C., Giordano A. CDK inhibitors: from the bench to clinical trials. Curr. Drug Targets 2010, 11:279-290.
42. Sprick M.R., Weigand M.A., Rieser E., Rauch C.T., Juo P., Blenis J., Krammer P.H., Walczak H. FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2. Immunity 2000, 12:599-609.
43. Steegmaier M., Hoffmann M., Baum A., Lenart P., Petronczki M., Krssak M., Gurtler U., Garin-Chesa P., Lieb S., Quant J., Grauert M., Adolf G.R., Kraut N., Peters J.M., Rettig W.J. BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth invivo. Curr. Biol. 2007, 17:316-322.
44. Strebhardt K. Multifaceted polo-like kinases: drug targets and antitargets for cancer therapy. Nat. Rev. Drug Discov. 2010, 9:643-660.
45. Suda T., Takahashi T., Golstein P., Nagata S. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 1993, 75:1169-1178.
46. Terrano D.T., Upreti M., Chambers T.C. Cyclin-dependent kinase 1-mediated Bcl-xL/Bcl-2 phosphorylation acts as a functional link coupling mitotic arrest and apoptosis. Mol. Cell. Biol. 2010, 30:640-656.
47. Trauth B.C., Klas C., Peters A.M., Matzku S., Moller P., Falk W., Debatin K.M., Krammer P.H. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 1989, 245:301-305.
48. Walczak H., Sprick M.R. Biochemistry and function of the DISC. Trends Biochem. Sci. 2001, 26:452-453.
49. Wu Z.Q., Liu X. Role for Plk1 phosphorylation of Hbo1 in regulation of replication licensing. Proc. Nat. Acad. Sci. U. S. A. 2008, 105:1919-1924.
50. Yonehara S., Ishii A., Yonehara M. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J.Exp. Med. 1989, 169:1747-1756.
51. Yuan J., Kramer A., Matthess Y., Yan R., Spankuch B., Gatje R., Knecht R., Kaufmann M., Strebhardt K. Stable gene silencing of cyclin B1 in tumor cells increases susceptibility to taxol and leads to growth arrest invivo. Oncogene 2006, 25:1753-1762.
52. Yuan K., Hu H., Guo Z., Fu G., Shaw A.P., Hu R., Yao X. Phospho-regulation of HsCdc14A by polo-like kinase 1 is essential for mitotic progression. J.Biol. Chem. 2007, 282:27414-27423.
53. Zhang L., Fang B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther. 2005, 12:228-237.
54. Zhang L., Yu J., Park B.H., Kinzler K.W., Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science 2000, 290:989-992.