Inhibitor of apoptosis proteins and apoptosis
Yunbo Wei,
Tingjun Fan,
Miaomiao Yu,
Yunbo Wei
Department of Marine Biology, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
Search for more papers by this authorCorresponding Author
Tingjun Fan
Department of Marine Biology, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
*Corresponding author: Tel, 86-532-82031637; Fax, 86-532-82031637; E-mail, [email protected]Search for more papers by this authorMiaomiao Yu
Department of Marine Biology, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
Search for more papers by this authorYunbo Wei,
Tingjun Fan,
Miaomiao Yu,
Yunbo Wei
Department of Marine Biology, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
Search for more papers by this authorCorresponding Author
Tingjun Fan
Department of Marine Biology, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
*Corresponding author: Tel, 86-532-82031637; Fax, 86-532-82031637; E-mail, [email protected]Search for more papers by this authorMiaomiao Yu
Department of Marine Biology, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
Search for more papers by this authorThis work was supported by a grant from the National High Technology Research and Development Program of China (863 Program) (No. 2006AA10A401)
Abstract
Apoptosis is a physiological cell death process that plays a critical role in development, homeostasis, and immune defense of multicellular animals. Inhibitor of apoptosis proteins (IAPs) constitute a family of proteins that possess between one and three baculovirus IAP repeats. Some of them also have a really interesting new gene finger domain, and can prevent cell death by binding and inhibiting active caspases, but are regulated by IAP antagonists. Some evidence also indicates that IAP can modulate the cell cycle and signal transduction. The three main factors, IAPs, IAP antagonists, and caspases, are involved in regulating the progress of apoptosis in many species. Many studies and assumptions have been focused on the anfractuous interactions between these three main factors to explore their real functional model in order to develop potential anticancer drugs. In this review, we describe the classification, molecular structures, and properties of IAPs and discuss the mechanisms of apoptosis. We also discuss the promising significance of clinical applications of IAPs in the diagnosis and treatment of malignancy.
References
- 1 Schimmer A. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 2004, 64: 7183–7190.
- 2 Nachmias B, Ashhab Y, Ben-Yehuda D. The inhibitor of apoptosis protein family (IAPs): an emerging therapeutic target in cancer. Semin Cancer Biol 2004, 14: 231–243.
- 3 Crook N, Clem R, Miller L. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 1993, 67: 2168–2174.
- 4 Higashi K, Takasawa R, Yoshimori A, Goh T, Tanuma S, Kuchitsu K. Identification of a novel gene family, paralogs of inhibitor of apoptosis proteins present in plants, fungi, and animals. Apoptosis 2005, 10: 471–480.
- 5 Tsuchiya Y, Murai S, Yamashita S. Apoptosis-inhibiting activities of BIR family proteins inXenopus egg extracts. FEBS J 2005, 272: 2237–2250.
- 6 Huang Q, Deveraux QL, Maeda S, Salvesen GS, Stennicke HR, Hammock BD, Reed JC. 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.
- 7 Fan TJ, Han LH, Cong RS, Liang J. Caspase family proteases and apoptosis. Acta Biochem Biophys Sin 2005, 37: 719–727.
- 8 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.
- 9 Cheung HH, Kelly N, Liston P, Korneluk R. Involvement of caspase-2 and caspase-9 in endoplasmic reticulum stress-induced apoptosis: a role for the IAPs. Exp Cell Res 2006, 312: 2347–2357.
- 10 Deveraux QL, Leo E, Stennicke H, Welsh K, Salvesen GS, Reed JC. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J 1999, 18: 5242–5251.
- 11 Davoodi J, Lin L, Kelly J, Liston P, MacKenzie A. Neuronal apoptosis-inhibitory protein does not interact with Smac and requires ATP to bind caspase-9. J Biol Chem 2004, 279: 40622–40628.
- 12 Wilkinson J, Wilkinson A, Scott F, Csomos R, Salvesen G, Duckett C. Neutralization of Smac/Diablo by inhibitors of apoptosis (IAPs). A caspase-independent mechanism for apoptotic inhibition. J Biol Chem 2004, 279: 51082–51090.
- 13 Eckelman B, Salvesen G. The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J Biol Chem 2006, 281: 3254–3260.
- 14 Vaux DL, Silke J. IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 2005, 6: 287–297.
- 15 Bartke T, Pohl C, Pyrowolakis G, Jentsch S. Dual role of BRUCE as an antiapoptotic IAP and a chimeric E2/E3 ubiquitin ligase. Mol Cell 2004, 14: 801–811.
- 16 Vaux DL, Silke J. IAPs—the ubiquitin connection. Cell Death Differ 2005, 12: 1205–1207.
- 17 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.
- 18 Silke J, Kratina T, Chu D, Ekert P, Day C, Pakusch M, Huang D et al. Determination of cell survival by RING-mediated regulation of inhibitor of apoptosis (IAP) protein abundance. Proc Natl Acad Sci USA 2005, 102: 16182–16187.
- 19 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.
- 20 Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 2001, 8: 613–621.
- 21 Liston P, Fong WG, Kelly NL, Toji S, Miyazaki T, Conte D, Tamai K et al. Identification of XAF1 as an antagonist of XIAP anti-caspase activity. Nat Cell Biol 2001, 3: 128–133.
- 22 Hegde R, Srinivasula SM, Datta P, Madesh M, Wassell R, Zhang Z, Cheong N et al. The polypeptide chain-releasing factor GSPT1/eRF3 is proteolytically processed into an IAP-binding protein. J Biol Chem 2003, 278: 38699–38706.
- 23 Fahrenkrog B, Sauder U, Aebi U. The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J Cell Sci 2004, 117: 115–126.
- 24 Zhang C, Xie L, Cheng H, Wang Y. TRAF3 interacts with Smac/DIABLO and enhances the proapoptotic effect of Smac/DIABLO in cytoplasm. Acta Biochim Biophys Sin 2007, 39: 108–116.
- 25 Fu J, Jin Y, Arend LJ. Smac3, a novel Smac/DIABLO splicing variant, attenuates the stability and apoptosis-inhibiting activity of X-linked inhibitor of apoptosis protein. J Biol Chem 2003, 278: 52660–52672.
- 26 Gordon GJ, Mani M, Mukhopadhyay L, Dong L, Yeap BY, Sugarbaker DJ, Bueno R. Inhibitor of apoptosis proteins are regulated by tumour necrosis factor-alpha in malignant pleural mesothelioma. J Pathol 2007, 211: 439–446.
- 27 Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, Zobel K et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-?B activation, and TNFα-depen-dent apoptosis. Cell 2007, 131: 669–681.
- 28 Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA et al. IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 2007, 131: 682–693.
- 29 Vassina EM, Yousefi S, Simon D, Zwicky C, Conus S, Simon HU. cIAP-2 and survivin contribute to cytokine-mediated delayed eosi-nophil apoptosis. Eur J Immunol 2006, 36: 1975–1984.
- 30 Verhagen AM, Kratina TK, Hawkins CJ, Silke J, Ekert PG, Vaux DL. Identification of mammalian mitochondrial proteins that interact with IAPs via N-terminal IAP binding motifs. Cell Death Differ 2007, 14: 348–357.
- 31 Wang ZL, Cuddy M, Samuel T, Welsh K, Schimmer A, Hanaii F, Houghten R et al. Cellular, biochemical, and genetic analysis of mechanism of small molecule IAP inhibitors. Biochem J 2004, 279: 48168–48176.
- 32 Duckett C. IAP proteins: sticking it to Smac. Biochem J 2005, 385: el–e2.
- 33 Green MC, Monser KP, Clem RJ. Ubiquitin protein ligase activity of the anti-apoptotic baculovirus protein Op-IAP3. Virus Research 2004, 105: 89–96.
- 34 Vucic D, Franklin MC, Wallweber HJ, Das K, Eckelman BP, Shin H, Elliott LO et al. Engineering ML-IAP to produce an extraordinarily potent caspase 9 inhibitor: Implications for Smac-dependent anti-apoptotic activity of ML-IAP. Biochem J 2005, 385: 11–20.
- 35 Dohi T, Okada K, Xia F, Wilford CE, Samuel T, Welsh K, Marusawa H et al. An IAP-IAP complex inhibits apoptosis. J Biol Chem 2004, 279: 34087–34090.
- 36 Ceballos-Cancino G, Espinosa M, Maldonado V, Melendez-Zajgla J. Regulation of mitochondrial Smac/DIABLO-selective release by survivin. Oncogene 2007, 26: 7569–7575.
- 37 Yoo SJ, Huh JR, Muro I, Yu H, Wang L, Wang SL, Feldman RM et al. Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat Cell Biol 2002, 4: 416–424.
- 38 Creagh EM, Murphy BM, Duriez PJ, Duckett CS, Martin SJ. Smac/Diablo antagonizes ubiquitin ligase activity of inhibitor of apoptosis proteins. J Biol Chem 2004, 279: 26906–26914.
- 39 Denault JB, Eckelman BP, Shin H, Pop C, Salvesen GS. Caspase 3 attenuates XIAP (X-linked inhibitor of apoptosis protein)-medi-ated inhibition of caspase 9. Biochem J 2007, 405: 11–19.
- 40 Canovas PM, Guadagno TM. Functional analysis of survivin in spindle assembly in Xenopus egg extracts. J Cell Biochem 2007, 100: 217–229.
- 41 Samuel T, Okada K, Hyer M, Welsh K, Zapata JM, Reed JC. cIAP1 localizes to the nuclear compartment and modulates the cell cycle. Cancer Res 2005, 65: 210–218.
- 42 Furusu A, Nakayama K, Xu Q, Konta T, Kitamura M. MAP kinase-dependent, NF-?B-independent regulation of inhibitor of apoptosis protein genes by TNF-α. J Cell Physiol 2007, 210: 703–710.
- 43 Yu LF, Wang J, Zou B, Lin MC, Wu YL, Xia HH, Sun YW et al. XAF1 mediates apoptosis through an extracellular signal-regulated kinase pathway in colon cancer. Cancer 2007, 109: 1996–2003.
- 44 Semba S, Trapasso F, Fabbri M, McCorkell KA, Volinia S, Druck T, Iliopoulos D et al. Fhit modulation of the Akt-survivin pathway in lung cancer cells: Fhit-tyrosine 114 (Y114) is essential. Oncogene 2006, 25: 2860–2872.
- 45 Yu XR, Jia GR, Gao GD, Wang SH, Han Y, Cao W. Neuroprotection of insulin against oxidative stress-induced apoptosis in cultured retinal neurons: involvement of phosphoinositide 3-kinase/Akt signal pathway. Acta Biochim Biophys Sin 2006, 38: 241–248.
- 46 Jiang H, Zhang J, Zhu H, Li H, Zhang X. Nerve growth factor prevents the apoptosis-associated increase in acetylcholinesterase activity after hydrogen peroxide treatment by activating Akt. Acta Biochim Biophys Sin 2007, 39: 46–56.
- 47 Watson RW, Fitzpatrick JM. Targeting apoptosis in prostate cancer: focus on caspases and inhibitors of apoptosis proteins. BJU Int 2005, 96: 30–34.
- 48 Peng XH, Karna P, O'Regan RM, Liu X, Naithani R, Moriarty RM, Wood WC et al. Down-regulation of inhibitor of apoptosis proteins by deguelin selectively induces apoptosis in breast cancer cells. Mol Pharmacol 2007, 71: 101–111.
- 49 Esposito I, Kleeff J, Abiatari I, Shi X, Giese N, Bergmann F, Roth W et al. Overexpression of cellular inhibitor of apoptosis protein 2 is an early event in the progression of pancreatic cancer. J Clin Pathol 2007, 60: 885–895.
- 50 Zhang S, Ding F, Luo A, Chen A, Yu Z, Ren S, Liu Z et al. XIAP is highly expressed in esophageal cancer and its downregulation by RNAi sensitizes esophageal carcinoma cell lines to chemotherapeutics. Cancer Biol Ther 2007, 6: 973–980.
- 51 Zhu XD, Lin GJ, Qian LP, Chen ZQ. Expression of survivin in human gastric carcinoma and gastric carcinoma model of rats. World J Gastroenterol 2003, 9: 1435–1438.
- 52 Kluger HM, McCarthy MM, Alvero AB, Sznol M, Ariyan S, Camp RL, Rimm DL et al. The X-linked inhibitor of apoptosis protein (XIAP) is up-regulated in metastatic melanoma, and XIAP cleavage by Phenoxodiol is associated with Carboplatin sensitization. J Transl Med 2007, 5: 6.
- 53 Choi S, Lew KL, Xiao H, Herman-Antosiewicz A, Xiao D, Brown CK, Singh SV. D,L-Sulforaphane-induced cell death in human prostate cancer cells is regulated by inhibitor of apoptosis family proteins and Apaf-1. Carcinogenesis 2007, 28: 151–162.
- 54 Zheng JN, Sun YF, Pei DS, Liu JJ, Chen JC, Li W, Sun XQ et al. Inhibition of proliferation and induction of apoptosis in human renal carcinoma cells by anti-telomerase small interfering RNAs. Acta Biochim Biophys Sin 2006, 38: 500–506.
- 55 Sun L, Cai L, Yu Y, Meng Q, Cheng X, Zhao Y, Sui G et al. Knockdown of S-phase kinase-associated protein-2 expression in MCF-7 inhibits cell growth and enhances the cytotoxic effects of epirubicin. Acta Biochim Biophys Sin 2007, 39: 999–1007.
- 56 Lei X, Huang Z, Zhong M, Zhu B, Tang S, Liao D. Bcl-XL small interfering RNA sensitizes cisplatin-resistant human lung adeno-carcinoma cells. Acta Biochim Biophys Sin 2007, 39: 344–350.
- 57 Huang Z, Lei X, Zhong M, Zhu B, Tang S, Liao D. Bcl-2 small interfering RNA sensitizes cisplatin-resistant human lung adeno-carcinoma A549/DDP cell to cisplatin and diallyl disulfide. Acta Biochim Biophys Sin 2007, 39: 835–843.
- 58 Romagnoli M, Trichet V, David C, Clement M, Moreau P, Bataille R, Barille-Nion S. Significant impact of survivin on myeloma cell growth. Leukemia 2007, 21: 1070–1078.
- 59 Zheng JN, Sun YF, Pei DS, Liu JJ, Ma TX, Han RF, Li W et al. Treatment with vector-expressed small hairpin RNAs against Ki67 RNA-induced cell growth inhibition and apoptosis in human renal carcinoma cells. Acta Biochim Biophys Sin 2006, 38: 254–261.
- 60 Vischioni B. Van Der Valk P, Span SW, Kruyt FA, Rodriguez JA, Giaccone G. Expression and localization of inhibitor of apoptosis proteins in normal human tissues. Hum Pathol 2006, 37: 78–86.
- 61 Gupta S. A role of inhibitor of apoptosis (IAP) proteins in increased lymphocyte apoptosis in aged humans. Mech Ageing Dev 2004, 125: 99–101.
- 62 Li J, Kim JM, Liston P, Li M, Miyazaki T, Mackenzie AE, Korneluk RG et al. Expression of inhibitor of apoptosis proteins (IAPs) in rat granulosa cells during ovarian follicular development and atresia. Endocrinology 1998, 139: 1321–1328.
