Dynamics within the CD95 death-inducing signaling complex decide life and death of cells

Molecular Systems Biology

Volumn 6, Issue , 2010, Pages

  Neumann, Leo ^a,c   Pforr, Carina ^a   Beaudouin, Joel ^a,c   Pappa, Alexander ^a,b   Fricker, Nicolai ^a   Krammer, Peter H ^a   Lavrik, Inna N ^a   Eils, Roland ^a,c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b MEDAC GMBH   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Apoptosis; CD95 signaling; DISC; Model reduction; NF B

Indexed keywords

DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; FAS ANTIGEN; FLICE INHIBITORY PROTEIN; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROCASPASE 8; PROTEIN P43; CASPASE;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DECISION MAKING; EXPERIMENTAL STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; KINETICS; LIFE; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN INTERACTION; VALIDATION STUDY; BIOLOGICAL MODEL; CELL LINEAGE; CELL SURVIVAL; ENZYME ACTIVATION; GENETICS; HELA CELL; METABOLISM; PROTEIN BINDING; SIGNAL TRANSDUCTION;

ANTIGENS, CD95; APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASES; CELL DEATH; CELL LINEAGE; CELL SURVIVAL; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEINS; ENZYME ACTIVATION; HELA CELLS; HUMANS; I-KAPPA B KINASE; KINETICS; MODELS, BIOLOGICAL; NF-KAPPA B; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 77949405660     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2010.6     Document Type: Article

References (59)

1. Arnold R, Liou J, Drexler HC, Weiss A, Kiefer F (2001) Caspase-mediated cleavage of hematopoietic progenitor kinase 1 (HPK1) converts an activator of NFkappaB into an inhibitor of NFkappaB. J Biol Chem 276: 14675-14684
2. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281: 1305-1308
3. Bagci EZ, Vodovotz Y, Billiar TR, Ermentrout GB, Bahar I (2006) Bistability in apoptosis: roles of Bax, Bcl-2, and mitochondrial permeability transition pores. Biophys J 90: 1546-1559
4. Barnhart BC, Legembre P, Pietras E, Bubici C, Franzoso G, Peter ME (2004) CD95 ligand induces motility and invasiveness of apoptosisresistant tumor cells. EMBO J 23: 3175-3185
5. Bentele M, Lavrik I, Ulrich M, Stosser S, Heermann DW, Kalthoff H, Krammer PH, Eils R (2004) Mathematical modeling reveals threshold mechanism in CD95-induced apoptosis. J Cell Biol 166: 839-851
6. Budd RC, Yeh WC, Tschopp J (2006) cFLIP regulation of lymphocyte activation and development. Nat Rev Immunol 6: 196-204
7. Chang DW, Xing Z, Pan Y, Algeciras-Schimnich A, Barnhart BC, Yaish-Ohad S, Peter ME, Yang X (2002) c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J 21: 3704-3714
8. Chaudhary PM, Eby MT, Jasmin A, Kumar A, Liu L, Hood L (2000) Activation of the NF-kappaB pathway by caspase 8 and its homologs. Oncogene 19: 4451-4460
9. CheongR,BergmannA,Werner SL, Regal J,HoffmannA,Levchenko A (2006) Transient I kappa B kinase activity mediates temporal NF-kappa B dynamics in response to a wide range of tumor necrosis factor-alpha doses. J Biol Chem 281: 2945-2950
10. Cheong R, Hoffmann A, Levchenko A (2008) Understanding NF-kappaB signaling via mathematical modeling. Mol Syst Biol 4: 192
11. Diessenbacher P, Hupe M, Sprick MR, Kerstan A, Geserick P, Haas TL, WachterT, NeumannM,WalczakH,SilkeJ,Leverkus M(2008) NF-kappaB inhibition reveals differential mechanisms of TNF versus TRAIL-induced apoptosis upstream or at the level of caspase-8 activation independent of cIAP2. J Invest Dermatol 128: 1134-1147
12. Dohrman A, Kataoka T, Cuenin S, Russell JQ, Tschopp J, Budd RC (2005) Cellular FLIP (long form) regulates CD8(+) Tcell activation through caspase-8-dependent NF-kappa B activation. J Immunol 174: 5270-5278
13. Eissing T, Conzelmann H, Gilles ED, Allgower F, Bullinger E, Scheurich P (2004) Bistability analyses of a caspase activation model for receptor-induced apoptosis. J Biol Chem 279: 36892-36897
14. Fischer U, Janicke RU, Schulze-Osthoff K (2003) Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ 10: 76-100
15. Fussenegger M, Bailey JE, Varner J (2000) A mathematical model of caspase function in apoptosis. Nat Biotechnol 18: 768-774
16. Golks A, Brenner D, Fritsch C, Krammer PH, Lavrik IN (2005) c-FLIPR, a new regulator of death receptor-induced apoptosis. J Biol Chem 280: 14507-14513
17. Golks A, Brenner D, Krammer PH, Lavrik IN (2006a) The c-FLIP-NH2 terminus (p22-FLIP) induces NF-kappa B activation. J Exp Med 203: 1295-1305
18. Golks A, Brenner D, Schmitz I, Watzl C, Krueger A, Krammer PH, Lavrik IN (2006b) The role of CAP3 in CD95 signaling: new insights into the mechanism of procaspase-8 activation. Cell Death Differ 13: 489-498
19. Hayden MS, Ghosh S (2004) Signaling to NF-kappaB. Genes Dev 18: 2195-2224
20. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544
21. Hoffmann A, Levchenko A, Scott ML, Baltimore D (2002) The I kappa B-NF-kappa B signaling module: temporal control and selective gene activation. Science 298: 1241-1245
22. Hu WH, Johnson H, Shu HB (2000) Activation of NF-kappaB byFADD, Casper, and caspase-8. J Biol Chem 275: 10838-10844
23. Hua F, Cornejo MG, Cardone MH, Stokes CL, Lauffenburger DA (2005) Effects of Bcl-2 levels on Fas signaling-induced caspase-3 activation: molecular genetic tests of computational model predictions. J Immunol 175: 985-995
24. Hughes MA, HarperN, ButterworthM,CainK,Cohen GM, MacFarlane M (2009) Reconstitution of the death-inducing signaling complex reveals a substrate switch that determines CD95-mediated death or survival. Mol Cell 35: 265-279
25. Janes KA, Albeck JG, Gaudet S, Sorger PK, Lauffenburger DA, Yaffe MB (2005) A systems model of signaling identifies a molecular basis set for cytokine-induced apoptosis. Science 310: 1646-1653
26. Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221-227
27. Kataoka T, Budd RC, Holler N, Thome M, Martinon F, Irmler M, Burns K, Hahne M, Kennedy N, Kovacsovics M, Tschopp J (2000) The caspase-8 inhibitor FLIP promotes activation of NF-kappaB and Erk signaling pathways. Curr Biol 10: 640-648
28. Kataoka T, Tschopp J (2004) N-terminal fragment of c-FLIP(L) processed by caspase 8 specifically interacts with TRAF2 and induces activation of the NF-kappaB signaling pathway. Mol Cell Biol 24: 2627-2636
29. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14: 5579-5588
30. Krammer PH (2000) CD95's deadly mission in the immune system. Nature 407: 789-795
31. Krammer PH, Arnold R, Lavrik IN (2007) Life and death in peripheral T cells. Nat Rev Immunol 7: 532-542
32. Kreuz S, Siegmund D, Rumpf JJ, Samel D, Leverkus M, Janssen O, Hacker G, Dittrich-Breiholz O, Kracht M, Scheurich P, Wajant H (2004) NF kappa B activation by Fas is mediated through FADD, caspase-8, and RIP and is inhibited by FLIP. J Cell Biol 166: 369-380
33. Krueger A, Schmitz I, Baumann S, Krammer PH, Kirchhoff S (2001) Cellular flice-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the cd95 death-inducing signaling complex. J Biol Chem 276: 20633-20640
34. Lavrik I, Krueger A, Schmitz I, Baumann S, Weyd H, Krammer PH, Kirchhoff S (2003) The active caspase-8 heterotetramer is formed at the CD95 DISC. Cell Death Differ 10: 144-145
35. Lavrik IN, Golks A, Krammer PH (2005) Caspases: pharmacological manipulation of cell death. J Clin Invest 115: 2665-2672
36. Lavrik IN, Golks A, Riess D, Bentele M, Eils R, Krammer PH (2007) Analysis of CD95 threshold signaling: triggering of CD95 (FAS/ APO-1) at low concentrations primarily results in survival signaling. J Biol Chem 282: 13664-13671
37. Legembre P, Barnhart BC, Zheng LX, Vijayan S, Straus SE, Puck J, Dale JK, Lenardo M, Peter ME (2004) Induction of apoptosis and activation of NF-kappa B by CD95 require different signalling thresholds. EMBO Rep 5: 1084-1089
38. Legewie S, Bluthgen N, Herzel H (2006) Mathematical modeling identifies inhibitors of apoptosis as mediators of positive feedback and bistability. PLoS Comput Biol 2: e120
39. Lens SM, Kataoka T, Fortner KA, Tinel A, Ferrero I, MacDonald RH, Hahne M, Beermann F, Attinger A, Orbea HA, Budd RC, Tschopp J (2002) The caspase 8 inhibitor c-FLIP(L) modulates T-cell receptor-induced proliferation but not activation-induced cell death of lymphocytes. Mol Cell Biol 22: 5419-5433
40. Micheau O, Thome M, Schneider P, Holler N, Tschopp J, Nicholson DW, Briand C, Grutter MG (2002) The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem 277: 45162-45171
41. Misra RS, Jelley-Gibbs DM, Russell JQ, Huston G, Swain SL, Budd RC (2005) Effector CD4(+) Tcells generate intermediate caspase activity and cleavage of caspase-8 substrates. J Immunol 174: 3999-4009
42. MuzioM,Chinnaiyan AM, Kischkel FC, O'RourkeK, ShevchenkoA, Ni J, Scaffidi C, Bretz JD, Zhang M, Gentz R, Mann M, Krammer PH, Peter ME, Dixit VM (1996) FLICE, a novel FADD-homologous ICE/ CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85: 817-827
43. Nelson DE, Ihekwaba AEC, ElliottM,Johnson JR, Gibney CA, Foreman BE, NelsonG,SeeV,Horton CA, Spiller DG,Edwards SW, McDowell HP, Unitt JF, Sullivan E, Grimley R, Benson N, Broomhead D, Kell DB, White MRH (2004) Oscillations in NF-kappa B signaling control the dynamics of gene expression. Science 306: 704-708
44. Park SG, Lee T, Kang HY, Park K, Cho KH, Jung GH (2006) The influence of the signal dynamics of activated form of IKK on NF-kappa B and anti-apoptotic gene expressions: a systems biology approach. FEBS Lett 580: 822-830
45. Peter ME, Budd RC, Desbarats J, Hedrick SM, Hueber AO, Newell MK, Owen LB, Tschopp J, Wajant H, Wallach D, Wiltrout RH, Zornig M, Lynch DH (2007) The CD95 receptor: apoptosis revisited. Cell 129: 447-450
46. Rehm M, Huber HJ, Dussmann H, Prehn JHM (2006) Systems analysis of effector caspase activation and its control by X-linked inhibitor of apoptosis protein. EMBO J 25: 4338-4349
47. Santos SD, Verveer PJ, Bastiaens PI (2007) Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat Cell Biol 9: 324-330
48. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH, Peter ME (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17: 1675-1687
49. Scaffidi C, Medema JP, Krammer PH, Peter ME (1997) FLICE is predominantly expressed as two functionally active isoforms, caspase-8/a and caspase-8/b. J Biol Chem 272: 26953-26958
50. Scaffidi C, Schmitz I, Krammer PH, Peter ME (1999) The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 274: 1541-1548
51. Snapp EL, Hegde RS, Francolini M, Lombardo F, Colombo S, Pedrazzini E, Borgese N, Lippincott-Schwartz J (2003) Formation of stacked ER cisternae by low affinity protein interactions. J Cell Biol 163: 257-269
52. Sprick M, Rieser E, Stahl H, Grosse-Wilde A, Weigand M, Walczak H (2002) Caspase-10 is recruited to and activated at the native TRAIL and CD95 death-inducing signalling complexes in a FADD-dependent manner but can not functionally substitute caspase-8. EMBO J 21: 4520-4530
53. Su H, Bidere N, Zheng L, Cubre A, Sakai K, Dale J, Salmena L, Hakem R, Straus S, Lenardo M (2005) Requirement for caspase-8 in NF-kappaB activation by antigen receptor. Science 307: 1465-1468
54. Sun N, Zhao HY (2004) Genomic approaches in dissecting complex biological pathways. Pharmacogenomics 5: 163-179
55. Trauth BC, Klas C, Peters AM, Matzku S, Moller P, Falk W, Debatin KM, Krammer PH (1989) Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 245: 301-305
56. Wagner KW, Engels IH, Deveraux QL (2004) Caspase-2 can function upstream of bid cleavage in the TRAIL apoptosis pathway. J Biol Chem 279: 35047-35052
57. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163
58. Xiong W, Ferrell JE (2003) A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426: 460-465
59. Zhang N, He YW (2005) An essential role for c-FLIP in the efficient development of mature T lymphocytes. J Exp Med 202: 395-404