Caspase-8 cleaves its substrates from the plasma membrane upon CD95-induced apoptosis

Cell Death and Differentiation

Volumn 20, Issue 4, 2013, Pages 599-610

  Beaudouin, J ^a   Liesche, C ^a   Aschenbrenner, S ^a   Horner M ^a,b   Eils, R ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Apoptosis; Caspase sensor; Live cell imaging; Quantitative biology

Indexed keywords

CASPASE 3; CASPASE 8; DEATH RECEPTOR; FAS ANTIGEN; PROTEIN BID;

APOPTOSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL DEATH; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; MOLECULAR PROBE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SPATIOTEMPORAL ANALYSIS;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANTIGENS, CD95; APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CALNEXIN; CASPASE 3; CASPASE 6; CASPASE 8; CELL MEMBRANE; CYCLOHEXIMIDE; ENZYME ACTIVATION; FLUORESCENT DYES; HELA CELLS; HUMANS; KERATIN-8; MITOCHONDRIAL PROTEINS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84874950506     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2012.156     Document Type: Article

References (56)

1. Degterev A, Boyce M, Yuan J. A decade of caspases. Oncogene 2003; 22: 8543-8567.
2. Grutter MG. Caspases: key players in programmed cell death. Curr Opin Struct Biol 2000; 10: 649-655.
3. Siegel RM. Caspases at the crossroads of immune-cell life and death. Nat Rev Immunol 2006; 6: 308-317.
4. Fuentes-Prior P, Salvesen GS. The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem J 2004; 384(Pt 2): 201-232.
5. Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM et al. A unified model for apical caspase activation. Mol Cell 2003 2003/2 11: 529-541.
6. van Raam BJ, Salvesen GS. Proliferative versus apoptotic functions of caspase-8 Hetero or homo: the caspase-8 dimer controls cell fate. Biochim Biophys Acta 2012; 1824: 113-122.
7. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 1995; 14: 5579-5588.
8. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 1996; 85: 803-815.
9. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J et al. 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.
10. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ et al. Two CD95 (APO-1/ Fas) signaling pathways. EMBO J 1998; 17: 1675-1687.
11. Wachmann K, Pop C, van Raam BJ, Drag M, Mace PD, Snipas SJ et al. Activation and specificity of human caspase-10. Biochemistry 2010; 49: 8307-8315.
12. Hughes MA, Harper N, Butterworth M, Cain K, Cohen GM, 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. Keller N, Mares J, Zerbe O, Grutter MG. Structural and biochemical studies on procaspase- 8: new insights on initiator caspase activation. Structure 2009; 17: 438-448.
14. Oberst A, Pop C, Tremblay AG, Blais Vr, Denault J-B, Salvesen GS et al. Inducible dimerization and inducible cleavage reveal a requirement for both processes in caspase-8 activation. J Biol Chem 2010; 285: 16632-16642.
15. Kang TB, Oh GS, Scandella E, Bolinger B, Ludewig B, Kovalenko A et al. Mutation of a selfprocessing site in caspase-8 compromises its apoptotic but not its nonapoptotic functions in bacterial artificial chromosome-transgenic mice. J Immunol 2008; 181: 2522-2532.
16. Keller N, Grutter MG, Zerbe O. Studies of the molecular mechanism of caspase-8 activation by solution NMR. Cell Death Differ 2010; 17: 710-718.
17. Golks A, Brenner D, Schmitz I, Watzl C, Krueger A, Krammer PH et al. The role of CAP3 in CD95 signaling: new insights into the mechanism of procaspase-8 activation. Cell Death Differ 2006; 13: 489-498.
18. Martin DA, Siegel RM, Zheng L, Lenardo MJ. Membrane oligomerization and cleavage activates the caspase-8 (FLICE/MACHalpha1) death signal. J Biol Chem 1998; 273: 4345-4349.
19. Koenig A, Russell JQ, Rodgers WA, Budd RC. Spatial differences in active caspase-8 defines its role in T-cell activation versus cell death. Cell Death Differ 2008; 15: 1701-1711.
20. Gonzalvez F, Schug ZT, Houtkooper RH, MacKenzie ED, Brooks DG, Wanders RJ et al. Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J Cell Biol 2008; 183: 681-696.
21. Schug ZT, Gonzalvez F, Houtkooper RH, Vaz FM, Gottlieb E. BID is cleaved by caspase-8 within a native complex on the mitochondrial membrane. Cell Death Differ 2011; 18: 538-548.
22. Kantari C, Walczak H. Caspase-8 and bid: caught in the act between death receptors and mitochondria. Biochim Biophys Acta 2011; 1813: 558-563.
23. Strasser A, Jost PJ, Nagata S. The many roles of FAS receptor signaling in the immune system. Immunity 2009; 30: 180-192.
24. Granell S, Baldini G, Mohammad S, Nicolin V, Narducci P, Storrie B. Sequestration of mutated alpha1-antitrypsin into inclusion bodies is a cell-protective mechanism to maintain endoplasmic reticulum function. Mol Biol Cell 2008; 19: 572-586.
25. Wiley SE, Murphy AN, Ross SA, van der Geer P, Dixon JE. MitoNEET is an iron-containing outer mitochondrial membrane protein that regulates oxidative capacity. Proc Natl Acad Sci USA 2007; 104: 5318-5323.
26. Chen Y, MacDonald PJ, Skinner JP, Patterson GH, Muller JD. Probing nucleocytoplasmic transport by two-photon activation of PA-GFP. Microsc Res Tech 2006; 69: 220-226.
27. Wei X, Henke VG, Strubing C, Brown EB, Clapham DE. Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys J 2003; 84(2 Pt 1): 1317-1327.
28. Albeck JG, Burke JM, Aldridge BB, Zhang M, Lauffenburger DA, Sorger PK. Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol Cell 2008; 30: 11-25.
29. Stennicke HR, Renatus M, Meldal M, Salvesen GS. Internally quenched fluorescent peptide substrates disclose the subsite preferences of human caspases 1, 3, 6, 7 and 8. Biochem J 2000; 350(Pt 2): 563-568.
30. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003; 114: 181-190.
31. Tchikov V, Bertsch U, Fritsch J, Edelmann B, Schutze S. Subcellular compartmentalization of TNF receptor-1 and CD95 signaling pathways. Eur J Cell Biol 2011; 90: 467-475.
32. Boya P, Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008; 27: 6434-6451.
33. Caruso JA, Mathieu PA, Joiakim A, Zhang H, Reiners JJ Jr. Aryl hydrocarbon receptor modulation of tumor necrosis factor-alpha-induced apoptosis and lysosomal disruption in a hepatoma model that is caspase-8-independent. J Biol Chem 2006; 281: 10954-10967.
34. Heinrich M, Neumeyer J, Jakob M, Hallas C, Tchikov V, Winoto-Morbach S et al. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ 2004; 11: 550-563.
35. Cowling V, Downward J. Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Differ 2002; 9: 1046-1056.
36. Inoue S, Browne G, Melino G, Cohen GM. Ordering of caspases in cells undergoing apoptosis by the intrinsic pathway. Cell Death Differ 2009; 16: 1053-1061.
37. Slee EA, Adrain C, Martin SJ. Executioner caspase-3, -6, and -7 perform distinct, nonredundant roles during the demolition phase of apoptosis. J Biol Chem 2001; 276: 7320-7326.
38. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 1999; 144: 281-292.
39. Deveraux QL, Takahashi R, Salvesen GS, Reed JC. X-linked IAP is a direct inhibitor of celldeath proteases. Nature 1997; 388: 300-304.
40. Klaiman G, Champagne N, LeBlanc AC. Self-activation of Caspase-6 in vitro and in vivo: caspase-6 activation does not induce cell death in HEK293T cells. Biochim Biophys Acta 2009; 1793: 592-601.
41. Wang XJ, Cao Q, Liu X, Wang KT, Mi W, Zhang Y et al. Crystal structures of human caspase 6 reveal a new mechanism for intramolecular cleavage self-activation. EMBO Rep 2010; 11: 841-847.
42. Albeck JG, Burke JM, Spencer SL, Lauffenburger DA, Sorger PK. Modeling a snap-action, variable-delay switch controlling extrinsic cell death. PLoS Biol 2008; 6: 2831-2852.
43. Dickens LS, Boyd RS, Jukes-Jones R, Hughes MA, Robinson GL, Fairall L et al. 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.
44. Schleich K, Warnken U, Fricker N, Ozturk S, Richter P, Kammerer K et al. 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.
45. Lee KH, Feig C, Tchikov V, Schickel R, Hallas C, Schutze S et al. The role of receptor internalization in CD95 signaling. EMBO J 2006; 25: 1009-1023.
46. Jin Z, Li Y, Pitti R, Lawrence D, Pham VC, Lill JR et al. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 2009; 137: 721-735.
47. Hellwig CT, Kohler BF, Lehtivarjo AK, Dussmann H, Courtney MJ, Prehn JH et al. Real time analysis of tumor necrosis factor-related apoptosis-inducing ligand/cycloheximideinduced caspase activities during apoptosis initiation. J Biol Chem 2008; 283: 21676-21685.
48. Rehm M, Dussmann H, Janicke RU, Tavare JM, Kogel D, Prehn JHM. Single-cell fluorescence resonance energy transfer analysis demonstrates that caspase activation during apoptosis is a rapid process. J Biol Chem 2002; 277: 24506-24514.
49. Rehm M, Huber HJ, Dussmann H, Prehn JH. Systems analysis of effector caspase activation and its control by X-linked inhibitor of apoptosis protein. EMBO J 2006; 25: 4338-4349.
50. Reichenzeller M, Burzlaff A, Lichter P, Herrmann H. In vivo observation of a nuclear channel-like system: evidence for a distinct interchromosomal domain compartment in interphase cells. J Struct Biol 2000; 129: 175-185.
51. Beaudouin J, Gerlich D, Daigle N, Eils R, Ellenberg J. Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 2002; 108: 83-96.
52. Snapp EL, Hegde RS, Francolini M, Lombardo F, Colombo S, Pedrazzini E et al. Formation of stacked ER cisternae by low affinity protein interactions. J Cell Biol 2003; 163: 257-269.
53. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 2004; 22: 1567-1572.
54. Ortiz-Ferron G, Tait SW, Robledo G, de Vries E, Borst J, Lopez-Rivas A. The mitogenactivated protein kinase pathway can inhibit TRAIL-induced apoptosis by prohibiting association of truncated Bid with mitochondria. Cell Death Differ 2006; 13: 1857-1865.
55. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002; 296: 913-916.
56. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 1999; 5: 157-163.