IAPs limit activation of RIP kinases by TNF receptor 1 during development

EMBO Journal

Volumn 31, Issue 7, 2012, Pages 1679-1691

  Moulin, Maryline ^a   Anderton, Holly ^a,b   Voss, Anne K ^b,c   Thomas, Tim ^b,c   Wong, Wendy Wei Lynn ^a   Bankovacki, Aleksandra ^a   Feltham, Rebecca ^a   Chau, Diep ^a   Cook, Wendy D ^a   Silke, John ^a,b,c   Vaux, David L ^a,b,c  

^a LA TROBE UNIVERSITY   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Apoptosis; IAP; NF B; RIP kinase; TNF

Indexed keywords

CASPASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN KINASE 1; RECEPTOR INTERACTING PROTEIN KINASE 3; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR MALFORMATION; CELL DEATH; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; FEMALE; FIBROBLAST; GENE DELETION; HEMIZYGOSITY; HETEROZYGOSITY; MALE; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL;

ANIMALS; FEMALE; GENE DELETION; INHIBITOR OF APOPTOSIS PROTEINS; MALE; MICE; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; SIGNAL TRANSDUCTION;

INTRACISTERNAL A-PARTICLES; MUS;

EID: 84859424337     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.18     Document Type: Article

References (50)

1. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, Barker PA (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 30: 689-700 (Pubitemid 351818251)
2. Birnbaum MJ, Clem RJ, Miller LK (1994) An apoptosis inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with cys/his sequence motif. J Virol 68: 2521-2528 (Pubitemid 24091932)
3. Bossen C, Ingold K, Tardivel A, Bodmer JL, Gaide O, Hertig S, Ambrose C, Tschopp J, Schneider P (2006) Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human. J Biol Chem 281: 13964-13971 (Pubitemid 43848322)
4. Caserta TM, Smith AN, Gultice AD, Reedy MA, Brown TL (2003) Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis 8: 345-352 (Pubitemid 36935206)
5. Ch'en IL, Tsau JS, Molkentin JD, Komatsu M, Hedrick SM (2011) Mechanisms of necroptosis in T cells. J Exp Med 208: 633-641
6. Conte D, Holcik M, Lefebvre CA, Lacasse E, Picketts DJ, Wright KE, Korneluk RG (2006) Inhibitor of apoptosis protein cIAP2 is essential for lipopolysaccharide-induced macrophage survival. Mol Cell Biol 26: 699-708 (Pubitemid 43090921)
7. Conze DB, Albert L, Ferrick DA, Goeddel DV, Yeh WC, Mak T, Ashwell JD (2005) Posttranscriptional downregulation of c-IAP2 by the ubiquitin protein ligase c-IAP1 in vivo. Mol Cell Biol 25: 3348-3356 (Pubitemid 40464334)
8. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O, Teng X, Abbott D, Cuny GD, Yuan C, Wagner G, Hedrick SM, Gerber SA, Lugovskoy A, Yuan J (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4: 313-321 (Pubitemid 351550892)
9. Duckett CS, Nava VE, Gedrich RW, Clem RJ, Vandongen JL, Gilfillan MC, Shiels H, Hardwick JM, Thompson CB (1996) A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J 15: 2685-2694 (Pubitemid 26176246)
10. Eckelman BP, Salvesen GS, Scott FL (2006) Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 7: 988-994 (Pubitemid 44480512)
11. Feltham R, Bettjeman B, Budhidarmo R, Mace PD, Shirley S, Condon SM, Chunduru SK, McKinlay MA, Vaux DL, Silke J, Day CL (2011) Smac mimetics activate the E3 ligase activity of cIAP1 protein by promoting RING domain dimerization. J Biol Chem 286: 17015-17028
12. Feltham R, Moulin M, Vince JE, Mace PD, Wong WW, Anderton H, Day CL, Vaux DL, Silke J (2010) Tumor necrosis factor (TNF) signaling, but not TWEAK (TNF-like weak inducer of apoptosis)-triggered cIAP1 (cellular inhibitor of apoptosis protein 1) degradation, requires cIAP1 RING dimerization and E2 binding. J Biol Chem 285: 17525-17536
13. Feng S, Yang Y, Mei Y, Ma L, Zhu DE, Hoti N, Castanares M, Wu M (2007) Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell Signal 19: 2056-2067 (Pubitemid 47353808)
14. Gardam S, Turner VM, Carter H, Limaye S, Basten A, Koentgen F, Vaux DL, Silke J, Brink R (2011) Deletion of cIAP1 and cIAP2 in B lymphocytes constitutively activates cell survival pathways and inactivates the germinal center response. Blood 117: 4041-4051
15. Geserick P, Hupe M, Moulin M, WongWW, Feoktistova M, Kellert B, Gollnick H, Silke J, Leverkus M (2009) Cellular IAPs inhibit a cryptic CD95-induced cell death by limiting RIP1 kinase recruitment. J Cell Biol 187: 1037-1054
16. Gyrd-Hansen M, Darding M, Miasari M, Santoro MM, Zender L, Xue W, Tenev T, da Fonseca PC, Zvelebil M, Bujnicki JM, Lowe S, Silke J, Meier P (2008) IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat Cell Biol 10: 1309-1317
17. Gyrd-Hansen M, Meier P (2010) IAPs: from caspase inhibitors to modulators of NF-kappa B, inflammation and cancer. Nat Rev Cancer 10: 561-574
18. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, Rieser E, Feltham R, Vince J, Warnken U, Wenger T, Koschny R, Komander D, Silke J, Walczak H (2009) Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol Cell 36: 831-844
19. Harlin H, Reffey SB, Duckett CS, Lindsten T, Thompson CB (2001) Characterization of XIAP-deficient mice. Mol Cell Biol 21: 3604-3608 (Pubitemid 32381796)
20. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132: 344-362
21. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ, Yuan J (2008) Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135: 1311-1323
22. Hogan BL, Costantini F, Lacy E (1986) Manipulating the mouse Embryo: A Laboratory Manual, 1st edn, pp 232-228, Plainview, NY: Cold Spring Harbor Laboratory Press
23. Hughes ED, Qu YY, Genik SJ, Lyons RH, Pacheco CD, Lieberman AP, Samuelson LC, Nasonkin IO, Camper SA, Van Keuren ML, Saunders TL (2007) Genetic variation in C57BL/6 ES cell lines and genetic instability in the Bruce4 C57BL/6 ES cell line. Mamm Genome 18: 549-558 (Pubitemid 47497926)
24. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, Caspary T, Mocarski ES (2011) RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471: 368-372
25. Koentgen F, Suss G, Stewart C, Steinmetz M, Bluethmann H (1993) Targeted disruption of the Mhc class-Ii Aa gene in C57bl/6 mice. Int Immunol 5: 957-964 (Pubitemid 23241767)
26. Liston P, Lefebvre C, Fong WG, Xuan JY, Korneluk RG (1997) Genomic characterization of the mouse inhibitor of apoptosis protein 1 and 2 genes. Genomics 46: 495-503 (Pubitemid 28063303)
27. Liston P, Roy N, Tamai K, Lefebvre C, Baird S, Chertonhorvat G, Farahani R, Mclean M, Ikeda JE, Mackenzie A, Korneluk RG (1996) Suppression of apoptosis in mammalian cells by naip and a related family of iap genes. Nature 379: 349-353 (Pubitemid 26033078)
28. Mahoney DJ, Cheung HH, Mrad RL, Plenchette S, Simard C, Enwere E, Arora V, Mak TW, Lacasse EC, Waring J, Korneluk RG (2008) Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc Natl Acad Sci USA 105: 11778-11783
29. Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114: 181-190 (Pubitemid 36936912)
30. Nguyen LT, Duncan GS, Mirtsos C, Ng M, Speiser DE, Shahinian A, Marino MW, Mak TW, Ohashi PS, Yeh WC (1999) TRAF2 deficiency results in hyperactivity of certain TNFR1 signals and impairment of CD40-mediated responses. Immunity 11: 379-389 (Pubitemid 29463246)
31. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C, Hakem R, Salvesen GS, Green DR (2011) Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471: 363-367
32. Pastorino JG, Tafani M, Farber JL (1999) Tumor necrosis factor induces phosphorylation and translocation of BAD through a phosphatidylinositide-3-OH kinase-dependent pathway. J Biol Chem 274: 19411-19416
33. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM (2000) High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 25: 139-140 (Pubitemid 30394979)
34. Rosenfeld ME, Prichard L, Shiojiri N, Fausto N (2000) Prevention of hepatic apoptosis and embryonic lethality in RelA/TNFR-1 double knockout mice. Am J Pathol 156: 997-1007 (Pubitemid 30626957)
35. Rothe M, Pan MG, Henzel WJ, Ayres TM, Goeddel DV (1995) The tnfr2-traf signaling complex contains two novel proteins related to baculoviral-inhibitor of apoptosis proteins. Cell 83: 1243-1252 (Pubitemid 26007814)
36. Santoro MM, Samuel T, Mitchell T, Reed JC, Stainier DY (2007) Birc2 (cIap1) regulates endothelial cell integrity and blood vessel homeostasis. Nat Genet 39: 1397-1402 (Pubitemid 350035006)
37. Schwenk F, Baron U, Rajewsky K (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxp-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081 (Pubitemid 26012492)
38. Shafey D, Korneluk R, Holcik M (2006) Distinct patterns of expression of the inhibitor of apoptosis protein cIAP2 during murine embryogenesis. Apoptosis 11: 1257-1259 (Pubitemid 44035973)
39. Takaesu G, Surabhi RM, Park KJ, Ninomiya-Tsuji J, Matsumoto K, Gaynor RB (2003) TAK1 is critical for IkappaB kinase-mediated activation of the NF-kappaB pathway. J Mol Biol 326: 105-115 (Pubitemid 36279361)
40. Tenev T, Zachariou A, Wilson R, Ditzel M, Meier P (2005) IAPs are functionally non-equivalent and regulate effector caspases through distinct mechanisms. Nat Cell Biol 7: 70-77 (Pubitemid 40123385)
41. Thomas T, Voss AK, Chowdhury K, Gruss P (2000) Querkopf, a MYST family histone acetyltransferase, is required for normal cerebral cortex development. Development 127: 2537-2548 (Pubitemid 30426802)
42. Uren AG, Pakusch M, Hawkins CJ, Puls KL, Vaux DL (1996) Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc Natl Acad Sci USA 93: 4974-4978
43. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, Zobel K, Dynek JN, Elliott LO, Wallweber HJ, Flygare JA, Fairbrother WJ, Deshayes K, Dixit VM, Vucic D (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 131: 669-681 (Pubitemid 350087204)
44. Varfolomeev E, Goncharov T, Fedorova AV, Dynek JN, Zobel K, Deshayes K, Fairbrother WJ, Vucic D (2008) c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J Biol Chem 283: 24295-24299
45. Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, Mett IL, Rebrikov D, Brodianski VM, Kemper OC, Kollet O, Lapidot T, Soffer D, Sobe T, Avraham KB, Goncharov T, Holtmann H, Lonai P, Wallach D (1998) 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 9: 267-276 (Pubitemid 28400040)
46. Vince JE, Chau D, Callus B, Wong WW, Hawkins CJ, Schneider P, McKinlay M, Benetatos CA, Condon SM, Chunduru SK, Yeoh G, Brink R, Vaux DL, Silke J (2008) TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J Cell Biol 182: 171-184 (Pubitemid 352008630)
47. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA, Chunduru SK, Condon SM, McKinlay M, Brink R, Leverkus M, Tergaonkar V, Schneider P, Callus BA, Koentgen F, Vaux DL, Silke J (2007) IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 131: 682-693 (Pubitemid 350103599)
48. Yeh WC, Delapompa JL, Mccurrach ME, Shu HB, Elia AJ, Shahinian A, Ng M, Wakeham A, Khoo W, Mitchell K, Eldeiry WS, Lowe SW, Goeddel DV, Mak TW (1998) Fadd-essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279: 1954-1958 (Pubitemid 28168653)
49. Yeh WC, Itie A, Elia AJ, Ng M, Shu HB, Wakeham A, Mirtsos C, Suzuki N, Bonnard M, Goeddel DV, Mak TW (2000) Requirement for casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12: 633-642
50. Zhang H, Zhou X, McQuade T, Li J, Chan FK, Zhang J (2011) Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 471: 373-376