全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
Cells  2013 

Regulation of Apoptosis by Inhibitors of Apoptosis (IAPs)

DOI: 10.3390/cells2010163

Keywords: DIAP1, XIAP, cIAPs, apoptosis, caspases, RIP, apoptosome, IAP antagonists

Full-Text   Cite this paper   Add to My Lib

Abstract:

Inhibitors of Apoptosis (IAPs) are a family of proteins with various biological functions including regulation of innate immunity and inflammation, cell proliferation, cell migration and apoptosis. They are characterized by the presence of at least one N-terminal baculoviral IAP repeat (BIR) domain involved in protein-protein interaction. Most of them also contain a C-terminal RING domain conferring an E3-ubiquitin ligase activity. In drosophila, IAPs are essential to ensure cell survival, preventing the uncontrolled activation of the apoptotic protease caspases. In mammals, IAPs can also regulate apoptosis through controlling caspase activity and caspase-activating platform formation. Mammalian IAPs, mainly X-linked IAP (XIAP) and cellular IAPs (cIAPs) appeared to be important determinants of the response of cells to endogenous or exogenous cellular injuries, able to convert the survival signal into a cell death-inducing signal. This review highlights the role of IAP in regulating apoptosis in Drosophila and Mammals.

References

[1]  Clarke, T.E.; Clem, R.J. Insect defenses against virus infection: The role of apoptosis. Int. Rev. Immunol. 2003, 22, 401–424, doi:10.1080/08830180305215.
[2]  Crook, N.E.; Clem, R.J.; Miller, L.K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 1993, 67, 2168–2174.
[3]  Orme, M.; Meier, P. Inhibitor of apoptosis proteins in Drosophila: Gatekeepers of death. Apoptosis 2009, 14, 950–960, doi:10.1007/s10495-009-0358-2.
[4]  Marivin, A.; Berthelet, J.; Plenchette, S.; Dubrez, L. The inhibitor of apoptosis (IAPs) in adaptive response to cellular stress. Cells 2012, 1, 711–737, doi:10.3390/cells1040711.
[5]  Beug, S.T.; Cheung, H.H.; Lacasse, E.C.; Korneluk, R.G. Modulation of immune signalling by inhibitors of apoptosis. Trends Immunol. 2012, 33, 535–545, doi:10.1016/j.it.2012.06.004.
[6]  Gyrd-Hansen, M.; Meier, P. IAPs: From caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat. Rev. Cancer 2010, 10, 561–574, doi:10.1038/nrc2889.
[7]  Wertz, I.E.; Dixit, V.M. Regulation of death receptor signaling by the ubiquitin system. Cell Death Differ. 2010, 17, 14–24, doi:10.1038/cdd.2009.168.
[8]  Silke, J.; Brink, R. Regulation of TNFRSF and innate immune signalling complexes by TRAFs and cIAPs. Cell Death Differ. 2010, 17, 35–45.
[9]  Dupoux, A.; Cartier, J.; Cathelin, S.; Filomenko, R.; Solary, E.; Dubrez-Daloz, L. cIAP1-dependent TRAF2 degradation regulates the differentiation of monocytes into macrophages and their response to CD40 ligand. Blood 2009, 113, 175–185, doi:10.1182/blood-2008-02-137919.
[10]  Dogan, T.; Harms, G.S.; Hekman, M.; Karreman, C.; Oberoi, T.K.; Alnemri, E.S.; Rapp, U.R.; Rajalingam, K. X-Linked and cellular IAPs modulate the stability of C-RAF kinase and cell motility. Nat. Cell Biol. 2008, 10, 1447–1455, doi:10.1038/ncb1804.
[11]  Xu, L.; Zhu, J.; Hu, X.; Zhu, H.; Kim, H.T.; LaBaer, J.; Goldberg, A.; Yuan, J. c-IAP1 cooperates with Myc by acting as a ubiquitin ligase for Mad1. Mol. Cell 2007, 28, 914–922, doi:10.1016/j.molcel.2007.10.027.
[12]  Cartier, J.; Berthelet, J.; Marivin, A.; Gemble, S.; Edmond, V.; Plenchette, S.; Lagrange, B.; Hammann, A.; Dupoux, A.; Delva, L.; et al. Cellular Inhibitor of Apoptosis Protein-1 (cIAP1) Can Regulate E2F1 transcription factor-mediated control of cyclin transcription. J. Biol. Chem. 2011, 286, 26406–26417, doi:10.1074/jbc.M110.191239.
[13]  Lens, S.M.; Vader, G.; Medema, R.H. The case for Survivin as mitotic regulator. Curr. Opin. Cell Biol. 2006, 18, 616–622, doi:10.1016/j.ceb.2006.08.016.
[14]  Birnbaum, M.J.; Clem, R.J.; Miller, L.K. An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J. Virol. 1994, 68, 2521–2528.
[15]  Hinds, M.G.; Norton, R.S.; Vaux, D.L.; Day, C.L. Solution structure of a baculoviral inhibitor of apoptosis (IAP) repeat. Nat. Struct. Biol. 1999, 6, 648–651, doi:10.1038/10701.
[16]  Eckelman, B.P.; Drag, M.; Snipas, S.J.; Salvesen, G.S. The mechanism of peptide-binding specificity of IAP BIR domains. Cell Death Differ. 2008, 15, 920–928, doi:10.1038/cdd.2008.6.
[17]  Srinivasula, S.M.; Hegde, R.; Saleh, A.; Datta, P.; Shiozaki, E.; Chai, J.; Lee, R.A.; Robbins, P.D.; Fernandes-Alnemri, T.; Shi, Y.; Alnemri, E.S. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001, 410, 112–116, doi:10.1038/35065125.
[18]  Liu, Z.; Sun, C.; Olejniczak, E.T.; Meadows, R.P.; Betz, S.F.; Oost, T.; Herrmann, J.; Wu, J.C.; Fesik, S.W. Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature 2000, 408, 1004–1008, doi:10.1038/35050006.
[19]  Lu, M.; Lin, S.C.; Huang, Y.; Kang, Y.J.; Rich, R.; Lo, Y.C.; Myszka, D.; Han, J.; Wu, H. XIAP induces NF-kappaB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol. Cell 2007, 26, 689–702, doi:10.1016/j.molcel.2007.05.006.
[20]  Samuel, T.; Welsh, K.; Lober, T.; Togo, S.H.; Zapata, J.M.; Reed, J.C. Distinct BIR domains of cIAP1 mediate binding to and ubiquitination of tumor necrosis factor receptor-associated factor 2 and second mitochondrial activator of caspases. J. Biol. Chem. 2006, 281, 1080–1090.
[21]  Mace, P.D.; Smits, C.; Vaux, D.L.; Silke, J.; Day, C.L. Asymmetric recruitment of cIAPs by TRAF2. J. Mol. Biol. 2010, 400, 8–15, doi:10.1016/j.jmb.2010.04.055.
[22]  Broemer, M.; Tenev, T.; Rigbolt, K.T.; Hempel, S.; Blagoev, B.; Silke, J.; Ditzel, M.; Meier, P. Systematic in vivo RNAi analysis identifies IAPs as NEDD8-E3 ligases. Mol. Cell 2010, 40, 810–822, doi:10.1016/j.molcel.2010.11.011.
[23]  Zhuang, M.; Guan, S.; Wang, H.; Burlingame, A.L.; Wells, J.A. Substrates of IAP Ubiquitin ligases identified with a designed orthogonal E3 ligase, the NEDDylator. Mol. Cell 2013, 49, 273–282, doi:10.1016/j.molcel.2012.10.022.
[24]  Silke, J.; Kratina, T.; Chu, D.; Ekert, P.G.; Day, C.L.; Pakusch, M.; Huang, D.C.; Vaux, D.L. Determination of cell survival by RING-mediated regulation of inhibitor of apoptosis (IAP) protein abundance. Proc. Natl. Acad. Sci. USA 2005, 102, 16182–16187.
[25]  Mace, P.D.; Linke, K.; Feltham, R.; Schumacher, F.R.; Smith, C.A.; Vaux, D.L.; Silke, J.; Day, C.L. Structures of the cIAP2 RING domain reveal conformational changes associated with ubiquitin-conjugating enzyme (E2) recruitment. J. Biol. Chem. 2008, 283, 31633–31640.
[26]  Rajalingam, K.; Sharma, M.; Paland, N.; Hurwitz, R.; Thieck, O.; Oswald, M.; Machuy, N.; Rudel, T. IAP-IAP complexes required for apoptosis resistance of C. trachomatis-infected cells. PLoS Pathog. 2006, 2, e114, doi:10.1371/journal.ppat.0020114.
[27]  Lopez, J.; John, S.W.; Tenev, T.; Rautureau, G.J.; Hinds, M.G.; Francalanci, F.; Wilson, R.; Broemer, M.; Santoro, M.M.; Day, C.L.; et al. CARD-Mediated autoinhibition of cIAP1’s E3 ligase activity suppresses cell proliferation and migration. Mol. Cell 2011, 42, 569–583, doi:10.1016/j.molcel.2011.04.008.
[28]  Blankenship, J.W.; Varfolomeev, E.; Goncharov, T.; Fedorova, A.V.; Kirkpatrick, D.S.; Izrael-Tomasevic, A.; Phu, L.; Arnott, D.; Aghajan, M.; Zobel, K.; et al. Ubiquitin binding modulates IAP antagonist-stimulated proteasomal degradation of c-IAP1 and c-IAP2(1). Biochem. J. 2009, 417, 149–160, doi:10.1042/BJ20081885.
[29]  Gyrd-Hansen, M.; Darding, M.; Miasari, M.; Santoro, M.M.; Zender, L.; Xue, W.; Tenev, T.; da Fonseca, P.C.; Zvelebil, M.; Bujnicki, J.M.; et al. IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat. Cell Biol. 2008, 10, 1309–1317, doi:10.1038/ncb1789.
[30]  Kulathila, R.; Vash, B.; Sage, D.; Cornell-Kennon, S.; Wright, K.; Koehn, J.; Stams, T.; Clark, K.; Price, A. The structure of the BIR3 domain of cIAP1 in complex with the N-terminal peptides of SMAC and caspase-9. Acta Crystallogr. D Biol. Crystallogr. 2009, 65, 58–66, doi:10.1107/S0907444908039243.
[31]  Chowdhury, I.; Tharakan, B.; Bhat, G.K. Caspases—An update. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008, 151, 10–27, doi:10.1016/j.cbpb.2008.05.010.
[32]  Ryoo, H.D.; Baehrecke, E.H. Distinct death mechanisms in Drosophila development. Curr. Opin. Cell Biol. 2010, 22, 889–895, doi:10.1016/j.ceb.2010.08.022.
[33]  Wang, S.L.; Hawkins, C.J.; Yoo, S.J.; Muller, H.A.; Hay, B.A. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 1999, 98, 453–463, doi:10.1016/S0092-8674(00)81974-1.
[34]  White, K.; Grether, M.E.; Abrams, J.M.; Young, L.; Farrell, K.; Steller, H. Genetic control of programmed cell death in Drosophila. Science 1994, 264, 677–683.
[35]  Grether, M.E.; Abrams, J.M.; Agapite, J.; White, K.; Steller, H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 1995, 9, 1694–1708, doi:10.1101/gad.9.14.1694.
[36]  Vucic, D.; Kaiser, W.J.; Harvey, A.J.; Miller, L.K. Inhibition of reaper-induced apoptosis by interaction with inhibitor of apoptosis proteins (IAPs). Proc. Natl. Acad. Sci. USA 1997, 94, 10183–10188.
[37]  Goyal, L.; McCall, K.; Agapite, J.; Hartwieg, E.; Steller, H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 2000, 19, 589–597, doi:10.1093/emboj/19.4.589.
[38]  Meier, P.; Silke, J.; Leevers, S.J.; Evan, G.I. The Drosophila caspase DRONC is regulated by DIAP1. EMBO J. 2000, 19, 598–611, doi:10.1093/emboj/19.4.598.
[39]  Hawkins, C.J.; Yoo, S.J.; Peterson, E.P.; Wang, S.L.; Vernooy, S.Y.; Hay, B.A. The Drosophila caspase DRONC cleaves following glutamate or aspartate and is regulated by DIAP1, HID, and GRIM. J. Biol. Chem. 2000, 275, 27084–27093.
[40]  Igaki, T.; Yamamoto-Goto, Y.; Tokushige, N.; Kanda, H.; Miura, M. Down-Regulation of DIAP1 triggers a novel Drosophila cell death pathway mediated by Dark and DRONC. J. Biol. Chem. 2002, 277, 23103–23106.
[41]  Quinn, L.M.; Dorstyn, L.; Mills, K.; Colussi, P.A.; Chen, P.; Coombe, M.; Abrams, J.; Kumar, S.; Richardson, H. An essential role for the caspase dronc in developmentally programmed cell death in Drosophila. J. Biol. Chem. 2000, 275, 40416–40424, doi:10.1074/jbc.M002935200.
[42]  Chew, S.K.; Akdemir, F.; Chen, P.; Lu, W.J.; Mills, K.; Daish, T.; Kumar, S.; Rodriguez, A.; Abrams, J.M. The apical caspase dronc governs programmed and unprogrammed cell death in Drosophila. Dev. Cell 2004, 7, 897–907, doi:10.1016/j.devcel.2004.09.016.
[43]  Daish, T.J.; Mills, K.; Kumar, S. Drosophila caspase DRONC is required for specific developmental cell death pathways and stress-induced apoptosis. Dev. Cell 2004, 7, 909–915, doi:10.1016/j.devcel.2004.09.018.
[44]  Muro, I.; Hay, B.A.; Clem, R.J. The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC. J. Biol. Chem. 2002, 277, 49644–49650, doi:10.1074/jbc.M203464200.
[45]  Yuan, S.; Yu, X.; Topf, M.; Dorstyn, L.; Kumar, S.; Ludtke, S.J.; Akey, C.W. Structure of the Drosophila apoptosome at 6.9 a resolution. Structure 2011, 19, 128–140, doi:10.1016/j.str.2010.10.009.
[46]  Yu, X.; Wang, L.; Acehan, D.; Wang, X.; Akey, C.W. Three-Dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J. Mol. Biol. 2006, 355, 577–589, doi:10.1016/j.jmb.2005.10.040.
[47]  Dorstyn, L.; Kumar, S. A cytochrome c-free fly apoptosome. Cell Death Differ. 2006, 13, 1049–1051, doi:10.1038/sj.cdd.4401918.
[48]  Dorstyn, L.; Kumar, S. A biochemical analysis of the activation of the Drosophila caspase DRONC. Cell Death Differ. 2008, 15, 461–470, doi:10.1038/sj.cdd.4402288.
[49]  Kilpatrick, Z.E.; Cakouros, D.; Kumar, S. Ecdysone-Mediated up-regulation of the effector caspase DRICE is required for hormone-dependent apoptosis in Drosophila cells. J. Biol. Chem. 2005, 280, 11981–11986, doi:10.1074/jbc.M413971200.
[50]  Xu, D.; Wang, Y.; Willecke, R.; Chen, Z.; Ding, T.; Bergmann, A. The effector caspases drICE and dcp-1 have partially overlapping functions in the apoptotic pathway in Drosophila. Cell Death Differ. 2006, 13, 1697–1706, doi:10.1038/sj.cdd.4401920.
[51]  Lisi, S.; Mazzon, I.; White, K. Diverse domains of THREAD/DIAP1 are required to inhibit apoptosis induced by REAPER and HID in Drosophila. Genetics 2000, 154, 669–678.
[52]  Chandraratna, D.; Lawrence, N.; Welchman, D.P.; Sanson, B. An in vivo model of apoptosis: Linking cell behaviours and caspase substrates in embryos lacking DIAP1. J. Cell Sci. 2007, 120, 2594–2608, doi:10.1242/jcs.03472.
[53]  Kaiser, W.J.; Vucic, D.; Miller, L.K. The Drosophila inhibitor of apoptosis D-IAP1 suppresses cell death induced by the caspase drICE. FEBS Lett. 1998, 440, 243–248, doi:10.1016/S0014-5793(98)01465-3.
[54]  Wilson, R.; Goyal, L.; Ditzel, M.; Zachariou, A.; Baker, D.A.; Agapite, J.; Steller, H.; Meier, P. The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis. Nat. Cell Biol. 2002, 4, 445–450, doi:10.1038/ncb799.
[55]  Chai, J.; Yan, N.; Huh, J.R.; Wu, J.W.; Li, W.; Hay, B.A.; Shi, Y. Molecular mechanism of Reaper-Grim-Hid-mediated suppression of DIAP1-dependent Dronc ubiquitination. Nat. Struct. Biol. 2003, 10, 892–898, doi:10.1038/nsb989.
[56]  Zachariou, A.; Tenev, T.; Goyal, L.; Agapite, J.; Steller, H.; Meier, P. IAP-Antagonists exhibit non-redundant modes of action through differential DIAP1 binding. EMBO J. 2003, 22, 6642–6652, doi:10.1093/emboj/cdg617.
[57]  Shapiro, P.J.; Hsu, H.H.; Jung, H.; Robbins, E.S.; Ryoo, H.D. Regulation of the Drosophila apoptosome through feedback inhibition. Nat. Cell Biol. 2008, 10, 1440–1446, doi:10.1038/ncb1803.
[58]  Lee, T.V.; Fan, Y.; Wang, S.; Srivastava, M.; Broemer, M.; Meier, P.; Bergmann, A. Drosophila IAP1-mediated ubiquitylation controls activation of the initiator caspase DRONC independent of protein degradation. PLoS Genet. 2011, 7, e1002261, doi:10.1371/journal.pgen.1002261.
[59]  Tenev, T.; Zachariou, A.; Wilson, R.; Ditzel, M.; Meier, P. IAPs are functionally non-equivalent and regulate effector caspases through distinct mechanisms. Nat. Cell Biol. 2005, 7, 70–77, doi:10.1038/ncb1204.
[60]  Tenev, T.; Ditzel, M.; Zachariou, A.; Meier, P. The antiapoptotic activity of insect IAPs requires activation by an evolutionarily conserved mechanism. Cell Death Differ. 2007, 14, 1191–1201, doi:10.1038/sj.cdd.4402118.
[61]  Li, X.; Wang, J.; Shi, Y. Structural mechanisms of DIAP1 auto-inhibition and DIAP1-mediated inhibition of drICE. Nat. Commun. 2011, 2, 408, doi:10.1038/ncomms1418.
[62]  Yokokura, T.; Dresnek, D.; Huseinovic, N.; Lisi, S.; Abdelwahid, E.; Bangs, P.; White, K. Dissection of DIAP1 functional domains via a mutant replacement strategy. J. Biol. Chem. 2004, 279, 52603–52612.
[63]  Ditzel, M.; Wilson, R.; Tenev, T.; Zachariou, A.; Paul, A.; Deas, E.; Meier, P. Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat. Cell Biol. 2003, 5, 467–473, doi:10.1038/ncb984.
[64]  Ditzel, M.; Broemer, M.; Tenev, T.; Bolduc, C.; Lee, T.V.; Rigbolt, K.T.; Elliott, R.; Zvelebil, M.; Blagoev, B.; Bergmann, A.; et al. Inactivation of effector caspases through nondegradative polyubiquitylation. Mol. Cell 2008, 32, 540–553, doi:10.1016/j.molcel.2008.09.025.
[65]  Herman-Bachinsky, Y.; Ryoo, H.D.; Ciechanover, A.; Gonen, H. Regulation of the Drosophila ubiquitin ligase DIAP1 is mediated via several distinct ubiquitin system pathways. Cell Death Differ. 2007, 14, 861–871, doi:10.1038/sj.cdd.4402079.
[66]  Huh, J.R.; Foe, I.; Muro, I.; Chen, C.H.; Seol, J.H.; Yoo, S.J.; Guo, M.; Park, J.M.; Hay, B.A. The Drosophila inhibitor of apoptosis (IAP) DIAP2 is dispensable for cell survival, required for the innate immune response to gram-negative bacterial infection, and can be negatively regulated by the reaper/hid/grim family of IAP-binding apoptosis inducers. J. Biol. Chem. 2007, 282, 2056–2068.
[67]  Meinander, A.; Runchel, C.; Tenev, T.; Chen, L.; Kim, C.H.; Ribeiro, P.S.; Broemer, M.; Leulier, F.; Zvelebil, M.; Silverman, N.; et al. Ubiquitylation of the initiator caspase DREDD is required for innate immune signalling. EMBO J. 2012, 31, 2770–2783, doi:10.1038/emboj.2012.121.
[68]  Kaplan, Y.; Gibbs-Bar, L.; Kalifa, Y.; Feinstein-Rotkopf, Y.; Arama, E. Gradients of a ubiquitin E3 ligase inhibitor and a caspase inhibitor determine differentiation or death in spermatids. Dev. Cell 2010, 19, 160–173, doi:10.1016/j.devcel.2010.06.009.
[69]  Vucic, D.; Kaiser, W.J.; Miller, L.K. Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by Drosophila proteins HID and GRIM. Mol. Cell Biol. 1998, 18, 3300–3309.
[70]  Wu, J.W.; Cocina, A.E.; Chai, J.; Hay, B.A.; Shi, Y. Structural analysis of a functional DIAP1 fragment bound to grim and hid peptides. Mol. Cell 2001, 8, 95–104, doi:10.1016/S1097-2765(01)00282-9.
[71]  Yoo, S.J.; Huh, J.R.; Muro, I.; Yu, H.; Wang, L.; Wang, S.L.; Feldman, R.M.; Clem, R.J.; Muller, H.A.; Hay, B.A. Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 2002, 4, 416–424, doi:10.1038/ncb793.
[72]  Tenev, T.; Zachariou, A.; Wilson, R.; Paul, A.; Meier, P. Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1. EMBO J. 2002, 21, 5118–5129, doi:10.1093/emboj/cdf530.
[73]  Christich, A.; Kauppila, S.; Chen, P.; Sogame, N.; Ho, S.I.; Abrams, J.M. The damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, and hid. Curr. Biol. 2002, 12, 137–140, doi:10.1016/S0960-9822(01)00658-3.
[74]  Wing, J.P.; Karres, J.S.; Ogdahl, J.L.; Zhou, L.; Schwartz, L.M.; Nambu, J.R. Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 2002, 12, 131–135, doi:10.1016/S0960-9822(01)00664-9.
[75]  Srinivasula, S.M.; Datta, P.; Kobayashi, M.; Wu, J.W.; Fujioka, M.; Hegde, R.; Zhang, Z.; Mukattash, R.; Fernandes-Alnemri, T.; Shi, Y.; et al. Sickle, a novel Drosophila death gene in the reaper/hid/grim region, encodes an IAP-inhibitory protein. Curr. Biol. 2002, 12, 125–130, doi:10.1016/S0960-9822(01)00657-1.
[76]  Hays, R.; Wickline, L.; Cagan, R. Morgue mediates apoptosis in the Drosophila melanogaster retina by promoting degradation of DIAP1. Nat. Cell Biol. 2002, 4, 425–431, doi:10.1038/ncb794.
[77]  Holley, C.L.; Olson, M.R.; Colon-Ramos, D.A.; Kornbluth, S. Reaper eliminates IAP proteins through stimulated IAP degradation and generalized translational inhibition. Nat. Cell Biol. 2002, 4, 439–444, doi:10.1038/ncb798.
[78]  Ryoo, H.D.; Bergmann, A.; Gonen, H.; Ciechanover, A.; Steller, H. Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat. Cell Biol. 2002, 4, 432–438, doi:10.1038/ncb795.
[79]  Ince, I.A.; Westenberg, M.; Vlak, J.M.; Demirbag, Z.; Nalcacioglu, R.; van Oers, M.M. Open reading frame 193R of Chilo iridescent virus encodes a functional inhibitor of apoptosis (IAP). Virology 2008, 376, 124–131, doi:10.1016/j.virol.2008.03.009.
[80]  Li, Q.; Liston, P.; Schokman, N.; Ho, J.M.; Moyer, R.W. Amsacta moorei Entomopoxvirus inhibitor of apoptosis suppresses cell death by binding Grim and Hid. J. Virol. 2005, 79, 3684–3691, doi:10.1128/JVI.79.6.3684-3691.2005.
[81]  Huang, Q.; Deveraux, Q.L.; Maeda, S.; Salvesen, G.S.; Stennicke, H.R.; Hammock, B.D.; Reed, J.C. Evolutionary conservation of apoptosis mechanisms: Lepidopteran and baculoviral inhibitor of apoptosis proteins are inhibitors of mammalian caspase-9. Proc. Natl. Acad. Sci. USA 2000, 97, 1427–1432.
[82]  Wright, C.W.; Clem, R.J. Sequence requirements for Hid binding and apoptosis regulation in the baculovirus inhibitor of apoptosis Op-IAP. Hid binds Op-IAP in a manner similar to Smac binding of XIAP. J. Biol. Chem. 2002, 277, 2454–2462.
[83]  Varfolomeev, E.; Wayson, S.M.; Dixit, V.M.; Fairbrother, W.J.; Vucic, D. The inhibitor of apoptosis protein fusion c-IAP2.MALT1 stimulates NF-kappaB activation independently of TRAF1 AND TRAF2. J. Biol. Chem. 2006, 281, 29022–29029.
[84]  Eckelman, B.P.; Salvesen, G.S.; Scott, F.L. Human inhibitor of apoptosis proteins: Why XIAP is the black sheep of the family. EMBO Rep. 2006, 7, 988–994, doi:10.1038/sj.embor.7400795.
[85]  Deveraux, Q.L.; Leo, E.; Stennicke, H.R.; Welsh, K.; Salvesen, G.S.; Reed, J.C. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J. 1999, 18, 5242–5251, doi:10.1093/emboj/18.19.5242.
[86]  Conze, D.B.; Albert, L.; Ferrick, D.A.; Goeddel, D.V.; Yeh, W.C.; Mak, T.; Ashwell, J.D. Posttranscriptional downregulation of c-IAP2 by the ubiquitin protein ligase c-IAP1 in vivo. Mol. Cell Biol. 2005, 25, 3348–3356, doi:10.1128/MCB.25.8.3348-3356.2005.
[87]  Harlin, H.; Reffey, S.B.; Duckett, C.S.; Lindsten, T.; Thompson, C.B. Characterization of XIAP-deficient mice. Mol. Cell Biol. 2001, 21, 3604–3608, doi:10.1128/MCB.21.10.3604-3608.2001.
[88]  Moulin, M.; Anderton, H.; Voss, A.K.; Thomas, T.; Wong, W.W.; Bankovacki, A.; Feltham, R.; Chau, D.; Cook, W.D.; Silke, J.; et al. IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J. 2012, 31, 1679–1691, doi:10.1038/emboj.2012.18.
[89]  Wurstle, M.L.; Laussmann, M.A.; Rehm, M. The central role of initiator caspase-9 in apoptosis signal transduction and the regulation of its activation and activity on the apoptosome. Exp. Cell Res. 2012, 318, 1213–1220, doi:10.1016/j.yexcr.2012.02.013.
[90]  Mace, P.D.; Riedl, S.J. Molecular cell death platforms and assemblies. Curr. Opin. Cell Biol. 2010, 22, 828–836, doi:10.1016/j.ceb.2010.08.004.
[91]  Silke, J.; Verhagen, A.M.; Ekert, P.G.; Vaux, D.L. Sequence as well as functional similarity for DIABLO/Smac and Grim, Reaper and Hid? Cell Death Differ. 2000, 7, 1275, doi:10.1038/sj.cdd.4400790.
[92]  Hegde, R.; Srinivasula, S.M.; Zhang, Z.; Wassell, R.; Mukattash, R.; Cilenti, L.; DuBois, G.; Lazebnik, Y.; Zervos, A.S.; Fernandes-Alnemri, T.; et al. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 2002, 277, 432–438.
[93]  Micheau, O.; Tschopp, J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003, 114, 181–190, doi:10.1016/S0092-8674(03)00521-X.
[94]  Tenev, T.; Bianchi, K.; Darding, M.; Broemer, M.; Langlais, C.; Wallberg, F.; Zachariou, A.; Lopez, J.; MacFarlane, M.; Cain, K.; et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 2011, 43, 432–448, doi:10.1016/j.molcel.2011.06.006.
[95]  Feoktistova, M.; Geserick, P.; Kellert, B.; Dimitrova, D.P.; Langlais, C.; Hupe, M.; Cain, K.; MacFarlane, M.; Hacker, 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, doi:10.1016/j.molcel.2011.06.011.
[96]  Imre, G.; Heering, J.; Takeda, A.N.; Husmann, M.; Thiede, B.; zu Heringdorf, D.M.; Green, D.R.; van der Goot, F.G.; Sinha, B.; Dotsch, V.; et al. Caspase-2 is an initiator caspase responsible for pore-forming toxin-mediated apoptosis. EMBO J. 2012, 31, 2615–2628, doi:10.1038/emboj.2012.93.
[97]  Upton, J.P.; Austgen, K.; Nishino, M.; Coakley, K.M.; Hagen, A.; Han, D.; Papa, F.R.; Oakes, S.A. Caspase-2 cleavage of BID is a critical apoptotic signal downstream of endoplasmic reticulum stress. Mol. Cell Biol. 2008, 28, 3943–3951, doi:10.1128/MCB.00013-08.
[98]  Malladi, S.; Challa-Malladi, M.; Fearnhead, H.O.; Bratton, S.B. The Apaf-1*procaspase-9 apoptosome complex functions as a proteolytic-based molecular timer. EMBO J. 2009, 28, 1916–1925, doi:10.1038/emboj.2009.152.
[99]  Saikumar, P.; Mikhailova, M.; Pandeswara, S.L. Regulation of caspase-9 activity by differential binding to the apoptosome complex. Front. Biosci. 2007, 12, 3343–3354, doi:10.2741/2317.
[100]  Bratton, S.B.; Walker, G.; Srinivasula, S.M.; Sun, X.M.; Butterworth, M.; Alnemri, E.S.; Cohen, G.M. Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J. 2001, 20, 998–1009, doi:10.1093/emboj/20.5.998.
[101]  Shiozaki, E.N.; Chai, J.; Rigotti, D.J.; Riedl, S.J.; Li, P.; Srinivasula, S.M.; Alnemri, E.S.; Fairman, R.; Shi, Y. Mechanism of XIAP-mediated inhibition of caspase-9. Mol. Cell 2003, 11, 519–527, doi:10.1016/S1097-2765(03)00054-6.
[102]  Zou, H.; Yang, R.; Hao, J.; Wang, J.; Sun, C.; Fesik, S.W.; Wu, J.C.; Tomaselli, K.J.; Armstrong, R.C. Regulation of the Apaf-1/caspase-9 apoptosome by caspase-3 and XIAP. J. Biol. Chem. 2003, 278, 8091–8098, doi:10.1074/jbc.M204783200.
[103]  Wright, K.M.; Linhoff, M.W.; Potts, P.R.; Deshmukh, M. Decreased apoptosome activity with neuronal differentiation sets the threshold for strict IAP regulation of apoptosis. J. Cell Biol. 2004, 167, 303–313, doi:10.1083/jcb.200406073.
[104]  Potts, M.B.; Vaughn, A.E.; McDonough, H.; Patterson, C.; Deshmukh, M. Reduced Apaf-1 levels in cardiomyocytes engage strict regulation of apoptosis by endogenous XIAP. J. Cell Biol. 2005, 171, 925–930, doi:10.1083/jcb.200504082.
[105]  Davoodi, J.; Lin, L.; Kelly, J.; Liston, P.; MacKenzie, A.E. Neuronal apoptosis-inhibitory protein does not interact with Smac and requires ATP to bind caspase-9. J. Biol. Chem. 2004, 279, 40622–40628.
[106]  Roy, N.; Mahadevan, M.S.; McLean, M.; Shutler, G.; Yaraghi, Z.; Farahani, R.; Baird, S.; Besner-Johnston, A.; Lefebvre, C.; Kang, X.; et al. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 1995, 80, 167–178, doi:10.1016/0092-8674(95)90461-1.
[107]  Fritz, J.H.; Ferrero, R.L.; Philpott, D.J.; Girardin, S.E. Nod-Like proteins in immunity, inflammation and disease. Nat. Immunol. 2006, 7, 1250–1257, doi:10.1038/ni1412.
[108]  Davoodi, J.; Ghahremani, M.H.; Es-Haghi, A.; Mohammad-Gholi, A.; Mackenzie, A. Neuronal apoptosis inhibitory protein, NAIP, is an inhibitor of procaspase-9. Int. J. Biochem. Cell Biol. 2010, 42, 958–964, doi:10.1016/j.biocel.2010.02.008.
[109]  Deveraux, Q.L.; Takahashi, R.; Salvesen, G.S.; Reed, J.C. X-Linked IAP is a direct inhibitor of cell-death proteases. Nature 1997, 388, 300–304.
[110]  Takahashi, R.; Deveraux, Q.; Tamm, I.; Welsh, K.; Assa-Munt, N.; Salvesen, G.S.; Reed, J.C. A single BIR domain of XIAP sufficient for inhibiting caspases. J. Biol. Chem. 1998, 273, 7787–7790.
[111]  Silke, J.; Ekert, P.G.; Day, C.L.; Hawkins, C.J.; Baca, M.; Chew, J.; Pakusch, M.; Verhagen, A.M.; Vaux, D.L. Direct inhibition of caspase 3 is dispensable for the anti-apoptotic activity of XIAP. EMBO J. 2001, 20, 3114–3123, doi:10.1093/emboj/20.12.3114.
[112]  Chai, J.; Shiozaki, E.; Srinivasula, S.M.; Wu, Q.; Datta, P.; Alnemri, E.S.; Shi, Y. Structural basis of caspase-7 inhibition by XIAP. Cell 2001, 104, 769–780, doi:10.1016/S0092-8674(01)00272-0.
[113]  Riedl, S.J.; Fuentes-Prior, P.; Renatus, M.; Kairies, N.; Krapp, S.; Huber, R.; Salvesen, G.S.; Bode, W. Structural basis for the activation of human procaspase-7. Proc. Natl. Acad. Sci. USA 2001, 98, 14790–14795, doi:10.1073/pnas.221580098.
[114]  Eckelman, B.P.; Salvesen, G.S. The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J. Biol. Chem. 2006, 281, 3254–3260, doi:10.1074/jbc.M510863200.
[115]  Schile, A.J.; Garcia-Fernandez, M.; Steller, H. Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes Dev. 2008, 22, 2256–2266, doi:10.1101/gad.1663108.
[116]  Suzuki, Y.; Nakabayashi, Y.; Takahashi, R. Ubiquitin-Protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc. Natl. Acad. Sci. USA 2001, 98, 8662–8667.
[117]  Choi, Y.E.; Butterworth, M.; Malladi, S.; Duckett, C.S.; Cohen, G.M.; Bratton, S.B. The E3 ubiquitin ligase cIAP1 binds and ubiquitinates caspase-3 and -7 via unique mechanisms at distinct steps in their processing. J. Biol. Chem. 2009, 284, 12772–12782.
[118]  Huang, H.; Joazeiro, C.A.; Bonfoco, E.; Kamada, S.; Leverson, J.D.; Hunter, T. The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7. J. Biol. Chem. 2000, 275, 26661–26664.
[119]  Declercq, W.; Vanden Berghe, T.; Vandenabeele, P. RIP kinases at the crossroads of cell death and survival. Cell 2009, 138, 229–232, doi:10.1016/j.cell.2009.07.006.
[120]  Haas, T.L.; Emmerich, C.H.; Gerlach, B.; Schmukle, A.C.; Cordier, S.M.; Rieser, E.; Feltham, R.; Vince, J.; Warnken, U.; Wenger, T.; et al. Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol. Cell 2009, 36, 831–844, doi:10.1016/j.molcel.2009.10.013.
[121]  Bertrand, M.J.; Milutinovic, S.; Dickson, K.M.; Ho, W.C.; Boudreault, A.; Durkin, J.; Gillard, J.W.; Jaquith, J.B.; Morris, S.J.; Barker, P.A. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 2008, 30, 689–700, doi:10.1016/j.molcel.2008.05.014.
[122]  Dynek, J.N.; Goncharov, T.; Dueber, E.C.; Fedorova, A.V.; Izrael-Tomasevic, A.; Phu, L.; Helgason, E.; Fairbrother, W.J.; Deshayes, K.; Kirkpatrick, D.S.; et al. c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. Embo J. 2010, 29, 4198–4209, doi:10.1038/emboj.2010.300.
[123]  O’Donnell, M.A.; Legarda-Addison, D.; Skountzos, P.; Yeh, W.C.; Ting, A.T. Ubiquitination of RIP1 regulates an NF-kappaB-independent cell-death switch in TNF signaling. Curr. Biol. 2007, 17, 418–424, doi:10.1016/j.cub.2007.01.027.
[124]  Vandenabeele, P.; Galluzzi, L.; Vanden Berghe, T.; Kroemer, G. Molecular mechanisms of necroptosis: An ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11, 700–714, doi:10.1038/nrm2970.
[125]  Park, S.M.; Yoon, J.B.; Lee, T.H. Receptor interacting protein is ubiquitinated by cellular inhibitor of apoptosis proteins (c-IAP1 and c-IAP2) in vitro. FEBS Lett. 2004, 566, 151–156, doi:10.1016/j.febslet.2004.04.021.
[126]  Geserick, P.; Hupe, M.; Moulin, M.; Wong, W.W.; Feoktistova, M.; Kellert, B.; Gollnick, H.; Silke, J.; Leverkus, M. Cellular IAPs inhibit a cryptic CD95-induced cell death by limiting RIP1 kinase recruitment. J. Cell Biol. 2009, 187, 1037–1054, doi:10.1083/jcb.200904158.
[127]  Varfolomeev, E.; Goncharov, T.; Fedorova, A.V.; Dynek, J.N.; Zobel, K.; Deshayes, K.; Fairbrother, W.J.; Vucic, D. c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J. Biol. Chem. 2008, 283, 24295–24299, doi:10.1074/jbc.C800128200.
[128]  Bertrand, M.J.; Lippens, S.; Staes, A.; Gilbert, B.; Roelandt, R.; de Medts, J.; Gevaert, K.; Declercq, W.; Vandenabeele, P. cIAP1/2 are direct E3 ligases conjugating diverse types of ubiquitin chains to receptor interacting proteins kinases 1 to 4 (RIP1–4). PLoS One 2011, 6, e22356.
[129]  Vanlangenakker, N.; Vanden Berghe, T.; Bogaert, P.; Laukens, B.; Zobel, K.; Deshayes, K.; Vucic, D.; Fulda, S.; Vandenabeele, P.; Bertrand, M.J. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 2011, 18, 656–665, doi:10.1038/cdd.2010.138.
[130]  Verhagen, A.M.; Kratina, T.K.; Hawkins, C.J.; Silke, J.; Ekert, P.G.; Vaux, D.L. Identification of mammalian mitochondrial proteins that interact with IAPs via N-terminal IAP binding motifs. Cell Death Differ. 2007, 14, 348–357, doi:10.1038/sj.cdd.4402001.
[131]  Du, C.; Fang, M.; Li, Y.; Li, L.; Wang, X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000, 102, 33–42, doi:10.1016/S0092-8674(00)00008-8.
[132]  Huang, Y.; Rich, R.L.; Myszka, D.G.; Wu, H. Requirement of both the second and third BIR domains for the relief of X-linked inhibitor of apoptosis protein (XIAP)-mediated caspase inhibition by Smac. J. Biol. Chem. 2003, 278, 49517–49522, doi:10.1074/jbc.M310061200.
[133]  Morizane, Y.; Honda, R.; Fukami, K.; Yasuda, H. X-Linked inhibitor of apoptosis functions as ubiquitin ligase toward mature caspase-9 and cytosolic Smac/DIABLO. J. Biochem. 2005, 137, 125–132, doi:10.1093/jb/mvi029.
[134]  Hu, S.; Yang, X. Cellular inhibitor of apoptosis 1 and 2 are ubiquitin ligases for the apoptosis inducer Smac/DIABLO. J. Biol. Chem. 2003, 278, 10055–10060.
[135]  Yang, Q.H.; Du, C. Smac/DIABLO selectively reduces the levels of c-IAP1 and c-IAP2 but not that of XIAP and livin in HeLa cells. J. Biol. Chem. 2004, 279, 16963–16970, doi:10.1074/jbc.M401253200.
[136]  Verhagen, A.M.; Silke, J.; Ekert, P.G.; Pakusch, M.; Kaufmann, H.; Connolly, L.M.; Day, C.L.; Tikoo, A.; Burke, R.; Wrobel, C.; et al. HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J. Biol. Chem. 2002, 277, 445–454.
[137]  Yang, Q.H.; Church-Hajduk, R.; Ren, J.; Newton, M.L.; Du, C. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev. 2003, 17, 1487–1496, doi:10.1101/gad.1097903.
[138]  Jin, S.; Kalkum, M.; Overholtzer, M.; Stoffel, A.; Chait, B.T.; Levine, A.J. CIAP1 and the serine protease HTRA2 are involved in a novel p53-dependent apoptosis pathway in mammals. Genes Dev. 2003, 17, 359–367, doi:10.1101/gad.1047003.
[139]  Gottfried, Y.; Rotem, A.; Lotan, R.; Steller, H.; Larisch, S. The mitochondrial ARTS protein promotes apoptosis through targeting XIAP. EMBO J. 2004, 23, 1627–1635, doi:10.1038/sj.emboj.7600155.
[140]  Bornstein, B.; Gottfried, Y.; Edison, N.; Shekhtman, A.; Lev, T.; Glaser, F.; Larisch, S. ARTS binds to a distinct domain in XIAP-BIR3 and promotes apoptosis by a mechanism that is different from other IAP-antagonists. Apoptosis 2011, 16, 869–881, doi:10.1007/s10495-011-0622-0.
[141]  Garrison, J.B.; Correa, R.G.; Gerlic, M.; Yip, K.W.; Krieg, A.; Tamble, C.M.; Shi, R.; Welsh, K.; Duggineni, S.; Huang, Z.; et al. ARTS and Siah collaborate in a pathway for XIAP degradation. Mol. Cell 2011, 41, 107–116, doi:10.1016/j.molcel.2010.12.002.
[142]  Garcia-Fernandez, M.; Kissel, H.; Brown, S.; Gorenc, T.; Schile, A.J.; Rafii, S.; Larisch, S.; Steller, H. Sept4/ARTS is required for stem cell apoptosis and tumor suppression. Genes Dev. 2010, 24, 2282–2293, doi:10.1101/gad.1970110.
[143]  Hegde, R.; Srinivasula, S.M.; Datta, P.; Madesh, M.; Wassell, R.; Zhang, Z.; Cheong, N.; Nejmeh, J.; Fernandes-Alnemri, T.; Hoshino, S.; et al. The polypeptide chain-releasing factor GSPT1/eRF3 is proteolytically processed into an IAP-binding protein. J. Biol. Chem. 2003, 278, 38699–38706, doi:10.1074/jbc.M303179200.
[144]  Varfolomeev, E.; Blankenship, J.W.; Wayson, S.M.; Fedorova, A.V.; Kayagaki, N.; Garg, P.; Zobel, K.; Dynek, J.N.; Elliott, L.O.; Wallweber, H.J.; et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007, 131, 669–681, doi:10.1016/j.cell.2007.10.030.
[145]  Vince, J.E.; Wong, W.W.; Khan, N.; Feltham, R.; Chau, D.; Ahmed, A.U.; Benetatos, C.A.; Chunduru, S.K.; Condon, S.M.; McKinlay, M.; et al. IAP Antagonists Target cIAP1 to Induce TNFalpha-Dependent Apoptosis. Cell 2007, 131, 682–693, doi:10.1016/j.cell.2007.10.037.
[146]  Petersen, S.L.; Wang, L.; Yalcin-Chin, A.; Li, L.; Peyton, M.; Minna, J.; Harran, P.; Wang, X. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 2007, 12, 445–456, doi:10.1016/j.ccr.2007.08.029.
[147]  Gaither, A.; Porter, D.; Yao, Y.; Borawski, J.; Yang, G.; Donovan, J.; Sage, D.; Slisz, J.; Tran, M.; Straub, C.; et al. A Smac mimetic rescue screen reveals roles for inhibitor of apoptosis proteins in tumor necrosis factor-alpha signaling. Cancer Res. 2007, 67, 11493–11498, doi:10.1158/0008-5472.CAN-07-5173.
[148]  Vince, J.E.; Chau, D.; Callus, B.; Wong, W.W.; Hawkins, C.J.; Schneider, P.; McKinlay, M.; Benetatos, C.A.; Condon, S.M.; Chunduru, S.K.; et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J. Cell Biol. 2008, 182, 171–184, doi:10.1083/jcb.200801010.
[149]  Yang, Y.; Fang, S.; Jensen, J.P.; Weissman, A.M.; Ashwell, J.D. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 2000, 288, 874–877, doi:10.1126/science.288.5467.874.
[150]  West, T.; Stump, M.; Lodygensky, G.; Neil, J.J.; Deshmukh, M.; Holtzman, D.M. Lack of X-linked inhibitor of apoptosis protein leads to increased apoptosis and tissue loss following neonatal brain injury. ASN Neuro. 2009, 1, e00004.
[151]  Russell, J.C.; Whiting, H.; Szuflita, N.; Hossain, M.A. Nuclear translocation of X-linked inhibitor of apoptosis (XIAP) determines cell fate after hypoxia ischemia in neonatal brain. J. Neurochem. 2008, 106, 1357–1370, doi:10.1111/j.1471-4159.2008.05482.x.
[152]  Holcik, M.; Thompson, C.S.; Yaraghi, Z.; Lefebvre, C.A.; MacKenzie, A.E.; Korneluk, R.G. The hippocampal neurons of neuronal apoptosis inhibitory protein 1 (NAIP1)-deleted mice display increased vulnerability to kainic acid-induced injury. Proc. Natl. Acad. Sci. USA 2000, 97, 2286–2290.
[153]  Goffredo, D.; Rigamonti, D.; Zuccato, C.; Tartari, M.; Valenza, M.; Cattaneo, E. Prevention of cytosolic IAPs degradation: A potential pharmacological target in Huntington's Disease. Pharmacol. Res. 2005, 52, 140–150, doi:10.1016/j.phrs.2005.01.006.
[154]  Weiss, K.H.; Runz, H.; Noe, B.; Gotthardt, D.N.; Merle, U.; Ferenci, P.; Stremmel, W.; Fullekrug, J. Genetic analysis of BIRC4/XIAP as a putative modifier gene of Wilson disease. J. Inherit. Metab. Dis. 2010, doi:10.1007/s10545-010-9123-5.
[155]  Lau, R.; Pratt, M.A. The opposing roles of cellular inhibitor of apoptosis proteins in cancer. ISRN Oncol. 2012, 2012, 928120.
[156]  Warnakulasuriyarachchi, D.; Cerquozzi, S.; Cheung, H.H.; Holcik, M. Translational induction of the inhibitor of apoptosis protein HIAP2 during endoplasmic reticulum stress attenuates cell death and is mediated via an inducible internal ribosome entry site element. J. Biol. Chem. 2004, 279, 17148–17157, doi:10.1074/jbc.M308737200.
[157]  Van Eden, M.E.; Byrd, M.P.; Sherrill, K.W.; Lloyd, R.E. Translation of cellular inhibitor of apoptosis protein 1 (c-IAP1) mRNA is IRES mediated and regulated during cell stress. RNA 2004, 10, 469–481, doi:10.1261/rna.5156804.
[158]  Holcik, M.; Lefebvre, C.; Yeh, C.; Chow, T.; Korneluk, R.G. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat. Cell Biol. 1999, 1, 190–192, doi:10.1038/11109.
[159]  Holcik, M.; Yeh, C.; Korneluk, R.G.; Chow, T. Translational upregulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death. Oncogene 2000, 19, 4174–4177, doi:10.1038/sj.onc.1203765.
[160]  Fulda, S.; Vucic, D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug. Discov. 2012, 11, 109–124, doi:10.1038/nrd3627.
[161]  Darding, M.; Feltham, R.; Tenev, T.; Bianchi, K.; Benetatos, C.; Silke, J.; Meier, P. Molecular determinants of Smac mimetic induced degradation of cIAP1 and cIAP2. Cell Death Differ. 2011, 18, 1376–1386, doi:10.1038/cdd.2011.10.

Full-Text

comments powered by Disqus

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133

WeChat 1538708413