Co-operative and Hierarchical Binding of c-FLIP and Caspase-8: A Unified Model Defines How c-FLIP Isoforms Differentially Control Cell Fate

Molecular Cell

Volumn 61, Issue 6, 2016, Pages 834-849

  Hughes, Michelle A ^a   Powley, Ian R ^a   Jukes Jones, Rebekah ^a   Horn, Sebastian ^c   Feoktistova, Maria ^d   Fairall, Louise ^b   Schwabe, John W R ^b   Leverkus, Martin ^d   Cain, Kelvin ^a   MacFarlane, Marion ^a  

^a MRC TOXICOLOGY UNIT   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; DEATH RECEPTOR; FLICE INHIBITORY PROTEIN; HETERODIMER; ISOPROTEIN; OLIGOMER; PROCASPASE 8; CFLAR PROTEIN, HUMAN; FADD PROTEIN, HUMAN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; PROTEIN BINDING;

APOPTOSIS; ARTICLE; CELL FATE; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOLECULAR MODEL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; CELL LINEAGE; GENETICS; METABOLISM; MUTAGENESIS; TANDEM MASS SPECTROMETRY;

APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASE 8; CELL LINEAGE; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; HUMANS; MUTAGENESIS; PROTEIN BINDING; PROTEIN ISOFORMS; TANDEM MASS SPECTROMETRY;

EID: 84962604276     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.02.023     Document Type: Article

References (45)

1. Boatright K.M., Deis C., Denault J.B., Sutherlin D.P., Salvesen G.S. Activation of caspases-8 and -10 by FLIP(L). Biochem. J. 2004, 382:651-657.
2. Chang D.W., Xing Z., Pan Y., Algeciras-Schimnich A., Barnhart B.C., Yaish-Ohad S., Peter M.E., Yang X. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J. 2002, 21:3704-3714.
3. Dickens L.S., Boyd R.S., Jukes-Jones R., Hughes M.A., Robinson G.L., Fairall L., Schwabe J.W., Cain K., MacFarlane M. A death effector domain chain DISC model reveals a crucial role for caspase-8 chain assembly in mediating apoptotic cell death. Mol. Cell 2012, 47:291-305.
4. Dickens L.S., Powley I.R., Hughes M.A., MacFarlane M. The 'complexities' of life and death: death receptor signalling platforms. Exp. Cell Res. 2012, 318:1269-1277.
5. Dillon C.P., Oberst A., Weinlich R., Janke L.J., Kang T.B., Ben-Moshe T., Mak T.W., Wallach D., Green D.R. Survival function of the FADD-CASPASE-8-cFLIP(L) complex. Cell Rep. 2012, 1:401-407.
6. Esposito D., Sankar A., Morgner N., Robinson C.V., Rittinger K., Driscoll P.C. Solution NMR investigation of the CD95/FADD homotypic death domain complex suggests lack of engagement of the CD95 C terminus. Structure 2010, 18:1378-1390.
7. Feoktistova M., Geserick P., Kellert B., Dimitrova D.P., Langlais C., Hupe M., Cain K., MacFarlane M., Häcker G., Leverkus M. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 2011, 43:449-463.
8. Feoktistova M., Geserick P., Panayotova-Dimitrova D., Leverkus M. Pick your poison: the Ripoptosome, a cell death platform regulating apoptosis and necroptosis. Cell Cycle 2012, 11:460-467.
9. Fricker N., Beaudouin J., Richter P., Eils R., Krammer P.H., Lavrik I.N. Model-based dissection of CD95 signaling dynamics reveals both a pro- and antiapoptotic role of c-FLIPL. J. Cell Biol. 2010, 190:377-389.
10. Harper N., Hughes M., MacFarlane M., Cohen G.M. Fas-associated death domain protein and caspase-8 are not recruited to the tumor necrosis factor receptor 1 signaling complex during tumor necrosis factor-induced apoptosis. J. Biol. Chem. 2003, 278:25534-25541.
11. Hinshaw-Makepeace J., Huston G., Fortner K.A., Russell J.Q., Holoch D., Swain S., Budd R.C. c-FLIP(S) reduces activation of caspase and NF-kappaB pathways and decreases T cell survival. Eur. J. Immunol. 2008, 38:54-63.
12. Hughes M.A., Harper N., Butterworth M., Cain K., Cohen G.M., MacFarlane M. Reconstitution of the death-inducing signaling complex reveals a substrate switch that determines CD95-mediated death or survival. Mol. Cell 2009, 35:265-279.
13. Hughes M.A., Langlais C., Cain K., MacFarlane M. Isolation, characterisation and reconstitution of cell death signalling complexes. Methods 2013, 61:98-104.
14. Irmler M., Thome M., Hahne M., Schneider P., Hofmann K., Steiner V., Bodmer J.L., Schröter M., Burns K., Mattmann C., et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997, 388:190-195.
15. Kaiser W.J., Upton J.W., Long A.B., Livingston-Rosanoff D., Daley-Bauer L.P., Hakem R., Caspary T., Mocarski E.S. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011, 471:368-372.
16. Kavuri S.M., Geserick P., Berg D., Dimitrova D.P., Feoktistova M., Siegmund D., Gollnick H., Neumann M., Wajant H., Leverkus M. Cellular FLICE-inhibitory protein (cFLIP) isoforms block CD95- and TRAIL death receptor-induced gene induction irrespective of processing of caspase-8 or cFLIP in the death-inducing signaling complex. J. Biol. Chem. 2011, 286:16631-16646.
17. Keller N., Mares J., Zerbe O., Grütter M.G. Structural and biochemical studies on procaspase-8: new insights on initiator caspase activation. Structure 2009, 17:438-448.
18. 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.
19. Koenig A., Buskiewicz I.A., Fortner K.A., Russell J.Q., Asaoka T., He Y.W., Hakem R., Eriksson J.E., Budd R.C. The c-FLIPL cleavage product p43FLIP promotes activation of extracellular signal-regulated kinase (ERK), nuclear factor κB (NF-κB), and caspase-8 and T cell survival. J. Biol. Chem. 2014, 289:1183-1191.
20. Krueger A., Baumann S., Krammer P.H., Kirchhoff S. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol. Cell. Biol. 2001, 21:8247-8254.
21. Krueger A., Schmitz I., Baumann S., Krammer P.H., Kirchhoff S. Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem. 2001, 276:20633-20640.
22. MacFarlane M., Merrison W., Dinsdale D., Cohen G.M. Active caspases and cleaved cytokeratins are sequestered into cytoplasmic inclusions in TRAIL-induced apoptosis. J. Cell Biol. 2000, 148:1239-1254.
23. Majkut J., Sgobba M., Holohan C., Crawford N., Logan A.E., Kerr E., Higgins C.A., Redmond K.L., Riley J.S., Stasik I., et al. Differential affinity of FLIP and procaspase 8 for FADD's DED binding surfaces regulates DISC assembly. Nat. Commun. 2014, 5:3350.
24. Micheau O., Thome M., Schneider P., Holler N., Tschopp J., Nicholson D.W., Briand C., Grütter M.G. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J. Biol. Chem. 2002, 277:45162-45171.
25. Oberst A., Pop C., Tremblay A.G., Blais V., Denault J.B., Salvesen G.S., Green D.R. Inducible dimerization and inducible cleavage reveal a requirement for both processes in caspase-8 activation. J. Biol. Chem. 2010, 285:16632-16642.
26. Oberst A., Dillon C.P., Weinlich R., McCormick L.L., Fitzgerald P., Pop C., Hakem R., Salvesen G.S., Green D.R. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011, 471:363-367.
27. Oztürk S., Schleich K., Lavrik I.N. Cellular FLICE-like inhibitory proteins (c-FLIPs): fine-tuners of life and death decisions. Exp. Cell Res. 2012, 318:1324-1331.
28. Pop C., Oberst A., Drag M., Van Raam B.J., Riedl S.J., Green D.R., Salvesen G.S. FLIP(L) induces caspase 8 activity in the absence of interdomain caspase 8 cleavage and alters substrate specificity. Biochem. J. 2011, 433:447-457.
29. Rasper D.M., Vaillancourt J.P., Hadano S., Houtzager V.M., Seiden I., Keen S.L., Tawa P., Xanthoudakis S., Nasir J., Martindale D., et al. Cell death attenuation by 'Usurpin', a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ. 1998, 5:271-288.
30. Salmena L., Lemmers B., Hakem A., Matysiak-Zablocki E., Murakami K., Au P.Y., Berry D.M., Tamblyn L., Shehabeldin A., Migon E., et al. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 2003, 17:883-895.
31. Scaffidi C., Schmitz I., Krammer P.H., Peter M.E. The role of c-FLIP in modulation of CD95-induced apoptosis. J. Biol. Chem. 1999, 274:1541-1548.
32. Schleich K., Warnken U., Fricker N., Oztürk S., Richter P., Kammerer K., Schnölzer M., Krammer P.H., Lavrik I.N. Stoichiometry of the CD95 death-inducing signaling complex: experimental and modeling evidence for a death effector domain chain model. Mol. Cell 2012, 47:306-319.
33. Scott F.L., Stec B., Pop C., Dobaczewska M.K., Lee J.J., Monosov E., Robinson H., Salvesen G.S., Schwarzenbacher R., Riedl S.J. The Fas-FADD death domain complex structure unravels signalling by receptor clustering. Nature 2009, 457:1019-1022.
34. Shen C., Yue H., Pei J., Guo X., Wang T., Quan J.M. Crystal structure of the death effector domains of caspase-8. Biochem. Biophys. Res. Commun. 2015, 463:297-302.
35. Shu H.B., Halpin D.R., Goeddel D.V. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity 1997, 6:751-763.
36. Siegel R.M., Martin D.A., Zheng L., Ng S.Y., Bertin J., Cohen J., Lenardo M.J. Death-effector filaments: novel cytoplasmic structures that recruit caspases and trigger apoptosis. J. Cell Biol. 1998, 141:1243-1253.
37. Silva J.C., Gorenstein M.V., Li G.Z., Vissers J.P.C., Geromanos S.J. Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol. Cell. Proteomics 2006, 5:144-156.
38. Tenev T., Bianchi K., Darding M., Broemer M., Langlais C., Wallberg F., Zachariou A., Lopez J., MacFarlane M., Cain K., Meier P. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 2011, 43:432-448.
39. Thome M., Tschopp J. Regulation of lymphocyte proliferation and death by FLIP. Nat. Rev. Immunol. 2001, 1:50-58.
40. Vajjhala P.R., Lu A., Brown D.L., Pang S.W., Sagulenko V., Sester D.P., Cridland S.O., Hill J.M., Schroder K., Stow J.L., et al. The inflammasome adaptor ASC induces procaspase-8 death effector domain filaments. J. Biol. Chem. 2015, 290:29217-29230.
41. Vanlangenakker N., Vanden Berghe T., Vandenabeele P. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ. 2012, 19:75-86.
42. Varfolomeev E.E., Schuchmann M., Luria V., Chiannilkulchai N., Beckmann J.S., Mett I.L., Rebrikov D., Brodianski V.M., Kemper O.C., Kollet O., et al. Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 1998, 9:267-276.
43. Wang L., Yang J.K., Kabaleeswaran V., Rice A.J., Cruz A.C., Park A.Y., Yin Q., Damko E., Jang S.B., Raunser S., et al. The Fas-FADD death domain complex structure reveals the basis of DISC assembly and disease mutations. Nat. Struct. Mol. Biol. 2010, 17:1324-1329.
44. Yang J.K., Wang L., Zheng L., Wan F., Ahmed M., Lenardo M.J., Wu H. Crystal structure of MC159 reveals molecular mechanism of DISC assembly and FLIP inhibition. Mol. Cell 2005, 20:939-949.
45. Yu J.W., Jeffrey P.D., Shi Y. Mechanism of procaspase-8 activation by c-FLIPL. Proc. Natl. Acad. Sci. USA 2009, 106:8169-8174.