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Zinc-rich inhibitor of apoptosis proteins (IAPs) as regulatory factors in the epithelium of normal and inflamed airways

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Abstract

Integrity of the airway epithelium (AE) is important in the context of inhaled allergens and noxious substances, particularly during asthma-related airway inflammation where there is increased vulnerability of the AE to cell death. Apoptosis involves a number of signaling pathways which activate procaspases leading to cleavage of critical substrates. Understanding the factors which regulate AE caspases is important for development of strategies to minimize AE damage and airway inflammation, and therefore to better control asthma. One such factor is the essential dietary metal zinc. Zinc deficiency results in enhanced AE apoptosis, and worsened airway inflammation. This has implications for asthma, where abnormalities in zinc homeostasis have been observed. Zinc is thought to suppress the steps involved in caspase-3 activation. One target of zinc is the family of inhibitor of apoptosis proteins (IAPs) which are endogenous regulators of caspases. More studies are needed to identify the roles of IAPs in regulating apoptosis in normal and inflamed airways and to study their interaction with labile zinc ions. This new information will provide a framework for future clinical studies aimed at monitoring and management of airway zinc levels as well as minimising airway damage and inflammation in asthma.

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Abbreviations

AE:

Airway epithelium

AEC:

Airway epithelial cell

BALF:

Bronchoalveolar lavage fluid

BIR:

Baculoviral IAP repeat

Cytochrome c :

Cyt c

IAP:

Inhibitors of apoptosis

OVA:

Ovalbumin

ROS:

Reactive oxygen species

RING:

Really Interesting New Gene

Smac:

Second mitochondria-derived activator of caspase

References

  • Adams R, Ruffin R, Wakefield M, Campbell D, Smith B (1997) Asthma prevalence, morbidity and management practices in South Australia, 1992–1995. ANZ J Med 27(6):672–679

    CAS  Google Scholar 

  • Aird KM, Ghanayem RB, Peplinski S, Lyerly HK, Devi GR (2010) X-linked inhibitor of apoptosis protein inhibits apoptosis in inflammatory breast cancer cells with acquired resistance to an ErbB1/2 tyrosine kinase inhibitor. Mol Cancer Ther 9(5):1432–1442. doi:10.1158/1535-7163.MCT-10-0160

    Article  PubMed  CAS  Google Scholar 

  • Altieri DC (2010) Survivin and IAP proteins in cell-death mechanisms. Biochem J 430(2):199–205. doi:10.1042/BJ20100814

    Article  PubMed  CAS  Google Scholar 

  • Bao S, Knoell DL (2006) Zinc modulates airway epithelium susceptibility to death receptor-mediated apoptosis. Am J Physiol Lung Cell Mol Physiol 290(3):L433–L441. doi:10.1152/ajplung.00341.2005

    Article  PubMed  CAS  Google Scholar 

  • Barnes PJ, Chung KF, Page CP (1998) Inflammatory mediators of asthma: an update. Pharmacol Rev 50(4):515–596

    PubMed  CAS  Google Scholar 

  • Bartemes KR, Kita H (2012) Dynamic role of epithelium-derived cytokines in asthma. Clin Immunol 143(3):222–235. doi:10.1016/j.clim.2012.03.001

    Article  PubMed  CAS  Google Scholar 

  • Bates JH, Rincon M, Irvin CG (2009) Animal models of asthma. Am J Physiol Lung Cell Mol Physiol 297(3):L401–L410. doi:10.1152/ajplung.00027.2009

    Article  PubMed  CAS  Google Scholar 

  • Beug ST, Cheung HH, Lacasse EC, Korneluk RG (2012) Modulation of immune signalling by inhibitors of apoptosis. Trends Immunol 33(11):535–545. doi:10.1016/j.it.2012.06.004

    Article  PubMed  CAS  Google Scholar 

  • Birnbaum MJ, Clem RJ, Miller LK (1994) An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J Virol 68(4):2521–2528

    PubMed  CAS  Google Scholar 

  • Blankenship JW, Varfolomeev E, Goncharov T, Fedorova AV, Kirkpatrick DS, Izrael-Tomasevic A, Phu L, Arnott D, Aghajan M, Zobel K, Bazan JF, Fairbrother WJ, Deshayes K, Vucic D (2009) Ubiquitin binding modulates IAP antagonist-stimulated proteasomal degradation of c-IAP1 and c-IAP2(1). Biochem J 417(1):149–160. doi:10.1042/BJ20081885

    Article  PubMed  CAS  Google Scholar 

  • Brady GF, Galban S, Liu X, Basrur V, Gitlin JD, Elenitoba-Johnson KS, Wilson TE, Duckett CS (2010) Regulation of the copper chaperone CCS by XIAP-mediated ubiquitination. Mol Cell Biol 30(8):1923–1936. doi:10.1128/MCB.00900-09

    Article  PubMed  CAS  Google Scholar 

  • Bratton SB, Cohen GM (2003) Death receptors leave a caspase footprint that Smacs of XIAP. Cell Death Differ 10(1):4–6. doi:10.1038/sj.cdd.4401176

    Article  PubMed  CAS  Google Scholar 

  • Bratton SB, Walker G, Srinivasula SM, Sun XM, Butterworth M, Alnemri ES, Cohen GM (2001) Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J 20(5):998–1009. doi:10.1093/emboj/20.5.998

    Article  PubMed  CAS  Google Scholar 

  • Bucchieri F, Puddicombe SM, Lordan JL, Richter A, Buchanan D, Wilson SJ, Ward J, Zummo G, Howarth PH, Djukanovic R, Holgate ST, Davies DE (2002) Asthmatic bronchial epithelium is more susceptible to oxidant-induced apoptosis. Am J Respir Cell Mol Biol 27(2):179–185

    Article  PubMed  CAS  Google Scholar 

  • Burke SP, Smith L, Smith JB (2010) cIAP1 cooperatively inhibits procaspase-3 activation by the caspase-9 apoptosome. J Biol Chem 285(39):30061–30068. doi:10.1074/jbc.M110.125955

    Article  PubMed  CAS  Google Scholar 

  • Burstein E, Ganesh L, Dick RD, van De Sluis B, Wilkinson JC, Klomp LW, Wijmenga C, Brewer GJ, Nabel GJ, Duckett CS (2004) A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J 23(1):244–254. doi:10.1038/sj.emboj.7600031

    Article  PubMed  CAS  Google Scholar 

  • Callus BA, Vaux DL (2007) Caspase inhibitors: viral, cellular and chemical. Cell Death Differ 14(1):73–78. doi:10.1038/sj.cdd.4402034

    Article  PubMed  CAS  Google Scholar 

  • Carter JE, Truong-Tran AQ, Grosser D, Ho L, Ruffin RE, Zalewski PD (2002) Involvement of redox events in caspase activation in zinc-depleted airway epithelial cells. Biochem Biophys Res Commun 297(4):1062–1070

    Article  PubMed  CAS  Google Scholar 

  • Chang TS, Jeong W, Lee DY, Cho CS, Rhee SG (2004) The RING-H2-finger protein APC11 as a target of hydrogen peroxide. Free Radic Biol Med 37(4):521–530. doi:10.1016/j.freeradbiomed.2004.05.006

    Article  PubMed  CAS  Google Scholar 

  • Choi YE, Butterworth M, Malladi S, Duckett CS, Cohen GM, Bratton SB (2009) The E3 ubiquitin ligase cIAP1 binds and ubiquitinates caspase-3 and -7 via unique mechanisms at distinct steps in their processing. J Biol Chem 284(19):12772–12782. doi:10.1074/jbc.M807550200

    Article  PubMed  CAS  Google Scholar 

  • Christiansen SC, Proud D, Cochrane CG (1987) Detection of tissue kallikrein in the bronchoalveolar lavage fluid of asthmatic subjects. J Clin Invest 79(1):188–197. doi:10.1172/JCI112782

    Article  PubMed  CAS  Google Scholar 

  • Christiansen SC, Proud D, Sarnoff RB, Juergens U, Cochrane CG, Zuraw BL (1992) Elevation of tissue kallikrein and kinin in the airways of asthmatic subjects after endobronchial allergen challenge. Am Rev Respir Dis 145(4 Pt 1):900–905

    Article  PubMed  CAS  Google Scholar 

  • Christie LA, Su JH, Tu CH, Dick MC, Zhou J, Cotman CW (2007) Differential regulation of inhibitors of apoptosis proteins in Alzheimer’s disease brains. Neurobiol Dis 26(1):165–173. doi:10.1016/j.nbd.2006.12.017

    Article  PubMed  CAS  Google Scholar 

  • Cohen L, EX Tarsi J, Ramkumar T, Horiuchi TK, Cochran R, DeMartino S, Schechtman KB, Hussain I, Holtzman MJ, Castro M, the NSARP (2007) Epithelial cell proliferation contributes to airway remodeling in severe asthma. Am J Respir Crit Care Med 176(2):138–145. doi:10.1164/rccm.200607-1062OC

    Article  PubMed  CAS  Google Scholar 

  • Cousins RJ (2010) Gastrointestinal factors influencing zinc absorption and homeostasis. Int J Vitam Nutr Res 80(4–5):243–248. doi:10.1024/0300-9831/a000030

    Article  PubMed  CAS  Google Scholar 

  • Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC (1994) CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10(1):38–47

    Article  PubMed  CAS  Google Scholar 

  • Crook NE, Clem RJ, Miller LK (1993) An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 67(4):2168–2174

    PubMed  CAS  Google Scholar 

  • Crystal RG, Randell SH, Engelhardt JF, Voynow J, Sunday ME (2008) Airway epithelial cells: current concepts and challenges. Proc Am Thorac Soc 5(7):772–777. doi:10.1513/pats.200805-041HR

    Article  PubMed  Google Scholar 

  • Csomos RA, Brady GF, Duckett CS (2009) Enhanced cytoprotective effects of the inhibitor of apoptosis protein cellular IAP1 through stabilization with TRAF2. J Biol Chem 284(31):20531–20539. doi:10.1074/jbc.M109.029983

    Article  PubMed  CAS  Google Scholar 

  • Damgaard RB, Gyrd-Hansen M (2011) Inhibitor of apoptosis (IAP) proteins in regulation of inflammation and innate immunity. Discov Med 11(58):221–231

    PubMed  Google Scholar 

  • Darding M, Meier P (2012) IAPs: guardians of RIPK1. Cell Death Differ 19(1):58–66. doi:10.1038/cdd.2011.163

    Article  PubMed  CAS  Google Scholar 

  • Davoodi J, Ghahremani MH, Es-Haghi A, Mohammad-Gholi A, Mackenzie A (2010) Neuronal apoptosis inhibitory protein, NAIP, is an inhibitor of procaspase-9. Int J Biochem Cell Biol 42(6):958–964. doi:10.1016/j.biocel.2010.02.008

    Article  PubMed  CAS  Google Scholar 

  • de Rivero Vaccari JP, Lotocki G, Marcillo AE, Dietrich WD, Keane RW (2008) A molecular platform in neurons regulates inflammation after spinal cord injury. J Neurosci 28(13):3404–3414. doi:10.1523/JNEUROSCI.0157-08.2008

    Article  PubMed  CAS  Google Scholar 

  • de Rivero Vaccari JP, Lotocki G, Alonso OF, Bramlett HM, Dietrich WD, Keane RW (2009) Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J Cereb Blood Flow Metab 29(7):1251–1261. doi:10.1038/jcbfm.2009.46

    Article  PubMed  CAS  Google Scholar 

  • Dean EJ, Ranson M, Blackhall F, Holt SV, Dive C (2007) Novel therapeutic targets in lung cancer: inhibitor of apoptosis proteins from laboratory to clinic. Cancer Treat Rev 33(2):203–212. doi:10.1016/j.ctrv.2006.11.002

    Article  PubMed  CAS  Google Scholar 

  • Deveraux QL, Reed JC (1999) IAP family proteins–suppressors of apoptosis. Genes Dev 13(3):239–252

    Article  PubMed  CAS  Google Scholar 

  • Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 17(8):2215–2223. doi:10.1093/emboj/17.8.2215

    Article  PubMed  CAS  Google Scholar 

  • Dubrez-Daloz L, Dupoux A, Cartier J (2008) IAPs: more than just inhibitors of apoptosis proteins. Cell Cycle 7(8):1036–1046

    Article  PubMed  CAS  Google Scholar 

  • Eckelman BP, Salvesen GS (2006) The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J Biol Chem 281(6):3254–3260. doi:10.1074/jbc.M510863200

    Article  PubMed  CAS  Google Scholar 

  • Eckelman BP, Salvesen GS, Scott FL (2006) Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 7(10):988–994. doi:10.1038/sj.embor.7400795

    Article  PubMed  CAS  Google Scholar 

  • Eichler T, Ma Q, Kelly C, Mishra J, Parikh S, Ransom RF, Devarajan P, Smoyer WE (2006) Single and combination toxic metal exposures induce apoptosis in cultured murine podocytes exclusively via the extrinsic caspase 8 pathway. Toxicol Sci 90(2):392–399. doi:10.1093/toxsci/kfj106

    Article  PubMed  CAS  Google Scholar 

  • Emamaullee JA, Shapiro AM (2006) Interventional strategies to prevent beta-cell apoptosis in islet transplantation. Diabetes 55(7):1907–1914. doi:10.2337/db05-1254

    Article  PubMed  CAS  Google Scholar 

  • Fanzo JC, Reaves SK, Cui L, Zhu L, Wu JY, Wang YR, Lei KY (2001) Zinc status affects p53, gadd45, and c-fos expression and caspase-3 activity in human bronchial epithelial cells. Am J Physiol Cell Physiol 281(3):C751–C757

    PubMed  CAS  Google Scholar 

  • Ferreira MA (2004) Inflammation in allergic asthma: initiating events, immunological response and risk factors. Respirology 9(1):16–24. doi:10.1111/j.1440-1843.2003.00516.x

    Article  PubMed  Google Scholar 

  • Ferretti M, Gattorno M, Chiocchetti A, Mesturini R, Orilieri E, Bensi T, Sormani MP, Cappellano G, Cerutti E, Nicola S, Biava A, Bardelli C, Federici S, Ceccherini I, Baldi M, Santoro C, Dianzani I, Martini A, Dianzani U (2009) The 423Q polymorphism of the X-linked inhibitor of apoptosis gene influences monocyte function and is associated with periodic fever. Arthritis Rheum 60(11):3476–3484. doi:10.1002/art.24905

    Article  PubMed  CAS  Google Scholar 

  • Fischer U, Janicke RU, Schulze-Osthoff K (2003) Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ 10(1):76–100. doi:10.1038/sj.cdd.4401160

    Article  PubMed  CAS  Google Scholar 

  • Foster M, Samman S (2012) Zinc and regulation of inflammatory cytokines: implications for cardiometabolic disease. Nutrients 4(7):676–694. doi:10.3390/nu4070676

    Article  PubMed  CAS  Google Scholar 

  • Frederickson CJ, Koh JY, Bush AI (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6(6):449–462. doi:10.1038/nrn1671

    Article  PubMed  CAS  Google Scholar 

  • Galban S, Duckett CS (2010) XIAP as a ubiquitin ligase in cellular signaling. Cell Death Differ 17(1):54–60. doi:10.1038/cdd.2009.81

    Article  PubMed  CAS  Google Scholar 

  • GINA (2011) Global strategy for asthma management and prevention: NHLBI/WHOreport. National Institutes of Health, National Heart, Lung and Blood Institute. http://www.ginasthma.com. Accessed 7 May 2011

  • Goettig P, Magdolen V, Brandstetter H (2010) Natural and synthetic inhibitors of kallikrein-related peptidases (KLKs). Biochimie 92(11):1546–1567. doi:10.1016/j.biochi.2010.06.022

    Article  PubMed  CAS  Google Scholar 

  • Gregory CD, Pound JD (2011) Cell death in the neighbourhood: direct microenvironmental effects of apoptosis in normal and neoplastic tissues. J Pathol 223(2):177–194. doi:10.1002/path.2792

    Article  PubMed  CAS  Google Scholar 

  • Guerrerio AL, Berg JM (2004) Metal ion affinities of the zinc finger domains of the metal responsive element-binding transcription factor-1 (MTF1). Biochemistry 43(18):5437–5444. doi:10.1021/bi0358418

    Article  PubMed  CAS  Google Scholar 

  • Gyrd-Hansen M, Meier P (2010) IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer 10(8):561–574. doi:10.1038/nrc2889

    Article  PubMed  CAS  Google Scholar 

  • 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(11):1309–1317. doi:10.1038/ncb1789

    Article  PubMed  CAS  Google Scholar 

  • Herman MD, Moche M, Flodin S, Welin M, Tresaugues L, Johansson I, Nilsson M, Nordlund P, Nyman T (2009) Structures of BIR domains from human NAIP and cIAP2. Acta Crystallogr Sect F 65(Pt 11):1091–1096. doi:10.1107/S1744309109038597

    Article  CAS  Google Scholar 

  • Hirsch T, Marchetti P, Susin SA, Dallaporta B, Zamzami N, Marzo I, Geuskens M, Kroemer G (1997) The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15(13):1573–1581. doi:10.1038/sj.onc.1201324

    Article  PubMed  CAS  Google Scholar 

  • Holgate ST (2007) The epithelium takes centre stage in asthma and atopic dermatitis. Trends Immunol 28(6):248–251. doi:10.1016/j.it.2007.04.007

    Article  PubMed  CAS  Google Scholar 

  • Holgate ST (2008) The airway epithelium is central to the pathogenesis of asthma. Allergol Int 57(1):1–10. doi:10.2332/allergolint.R-07-154

    Article  PubMed  CAS  Google Scholar 

  • Holgate ST (2012a) Trials and tribulations in identifying new biologic treatments for asthma. Trends Immunol 33(5):238–246. doi:10.1016/j.it.2012.02.003

    Article  PubMed  CAS  Google Scholar 

  • Holgate ST (2012b) Innate and adaptive immune responses in asthma. Nat Med 18(5):673–683. doi:10.1038/nm.2731

    Article  PubMed  CAS  Google Scholar 

  • Holgate ST, Lackie PM, Davies DE, Roche WR, Walls AF (1999) The bronchial epithelium as a key regulator of airway inflammation and remodelling in asthma. Clin Exp Allergy 29(Suppl 2):90–95

    Article  PubMed  Google Scholar 

  • Holgate ST, Davies DE, Puddicombe S, Richter A, Lackie P, Lordan J, Howarth P (2003) Mechanisms of airway epithelial damage: epithelial-mesenchymal interactions in the pathogenesis of asthma. Eur Respir J Suppl 44:24s–29s

    Article  PubMed  CAS  Google Scholar 

  • Holt PG, Strickland DH, Sly PD (2012) Virus infection and allergy in the development of asthma: what is the connection? Curr Opin Allergy Clin Immunol 12(2):151–157. doi:10.1097/ACI.0b013e3283520166

    Article  PubMed  CAS  Google Scholar 

  • Hotchkiss RS, Strasser A, McDunn JE, Swanson PE (2009) Cell death. N Engl J Med 361(16):1570–1583. doi:10.1056/NEJMra0901217

    Article  PubMed  CAS  Google Scholar 

  • Huber KL, Hardy JA (2012) Mechanism of zinc-mediated inhibition of caspase-9. Protein Sci 21(7):1056–1065. doi:10.1002/pro.2090

    Article  PubMed  CAS  Google Scholar 

  • Hunter AM, LaCasse EC, Korneluk RG (2007) The inhibitors of apoptosis (IAPs) as cancer targets. Apoptosis 12(9):1543–1568. doi:10.1007/s10495-007-0087-3

    Article  PubMed  CAS  Google Scholar 

  • Imai N, Matsuda N, Tanaka K, Nakano A, Matsumoto S, Kang W (2003) Ubiquitin ligase activities of Bombyx mori nucleopolyhedrovirus RING finger proteins. J Virol 77(2):923–930

    Article  PubMed  CAS  Google Scholar 

  • Imre G, Larisch S, Rajalingam K (2011) Ripoptosome: a novel IAP-regulated cell death-signalling platform. J Mol Cell Biol 3(6):324–326. doi:10.1093/jmcb/mjr034

    Article  PubMed  CAS  Google Scholar 

  • Jayaram L, Chunilal S, Pickering S, Ruffin RE, Zalewski PD (2011) Sputum zinc concentration and clinical outcome in older asthmatics. Respirology 16(3):459–466. doi:10.1111/j.1440-1843.2011.01932.x

    Article  PubMed  Google Scholar 

  • Kampf C, Relova AJ, Sandler S, Roomans GM (1999) Effects of TNF-alpha, IFN-gamma and IL-beta on normal human bronchial epithelial cells. Eur Respir J 14(1):84–91

    Article  PubMed  CAS  Google Scholar 

  • Karimpour S, Davoodi J, Ghahremani MH (2011) Integrity of ATP binding site is essential for effective inhibition of the intrinsic apoptosis pathway by NAIP. Biochem Biophys Res Commun 407(1):158–162. doi:10.1016/j.bbrc.2011.02.130

    Article  PubMed  CAS  Google Scholar 

  • Karlovic D, Jakopec S, Dubravcic K, Batinic D, Buljan D, Osmak M (2007) Lithium increases expression of p21(WAF/Cip1) and survivin in human glioblastoma cells. Cell Biol Toxicol 23(2):83–90. doi:10.1007/s10565-006-0126-9

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann T, Strasser A, Jost PJ (2012) Fas death receptor signalling: roles of Bid and XIAP. Cell Death Differ 19(1):42–50. doi:10.1038/cdd.2011.121

    Article  PubMed  CAS  Google Scholar 

  • Knight DA, Holgate ST (2003) The airway epithelium: structural and functional properties in health and disease. Respirology 8(4):432–446

    Article  PubMed  Google Scholar 

  • Knight DA, Stick SM, Hackett TL (2011) Defective function at the epithelial junction: a novel therapeutic frontier in asthma? J Allergy Clin Immunol 128(3):557–558. doi:10.1016/j.jaci.2011.07.031

    Article  PubMed  CAS  Google Scholar 

  • Koonin EV, Aravind L (2000) The NACHT family - a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem Sci 25(5):223–224

    Article  PubMed  CAS  Google Scholar 

  • Korichneva I, Hoyos B, Chua R, Levi E, Hammerling U (2002) Zinc release from protein kinase C as the common event during activation by lipid second messenger or reactive oxygen. J Biol Chem 277(46):44327–44331. doi:10.1074/jbc.M205634200

    Article  PubMed  CAS  Google Scholar 

  • Krezel A, Maret W (2006) Zinc-buffering capacity of a eukaryotic cell at physiological pZn. J Biol Inorg Chem 11(8):1049–1062. doi:10.1007/s00775-006-0150-5

    Article  PubMed  CAS  Google Scholar 

  • Kumar S (2007) Caspase function in programmed cell death. Cell Death Differ 14(1):32–43. doi:10.1038/sj.cdd.4402060

    Article  PubMed  CAS  Google Scholar 

  • Kuwano K (2007) Epithelial cell apoptosis and lung remodeling. Cell Mol Immunol 4(6):419–429

    PubMed  CAS  Google Scholar 

  • Kuwano K, Hara N (2000) Signal transduction pathways of apoptosis and inflammation induced by the tumor necrosis factor receptor family. Am J Respir Cell Mol Biol 22(2):147–149

    Article  PubMed  CAS  Google Scholar 

  • Labbe K, McIntire CR, Doiron K, Leblanc PM, Saleh M (2011) Cellular inhibitors of apoptosis proteins cIAP1 and cIAP2 are required for efficient caspase-1 activation by the inflammasome. Immunity 35(6):897–907. doi:10.1016/j.immuni.2011.10.016

    Article  PubMed  CAS  Google Scholar 

  • Lacasse EC, Kandimalla ER, Winocour P, Sullivan T, Agrawal S, Gillard JW, Durkin J (2005) Application of XIAP antisense to cancer and other proliferative disorders: development of AEG35156/GEM640. Ann NY Acad Sci 1058:215–234. doi:10.1196/annals.1359.032

    Article  PubMed  CAS  Google Scholar 

  • Lambrecht BN, Hammad H (2012) The airway epithelium in asthma. Nat Med 18(5):684–692. doi:10.1038/nm.2737

    Article  PubMed  CAS  Google Scholar 

  • Lang C, Murgia C, Leong M, Tan LW, Perozzi G, Knight D, Ruffin R, Zalewski P (2007) Anti-inflammatory effects of zinc and alterations in zinc transporter mRNA in mouse models of allergic inflammation. Am J Physiol Lung Cell Mol Physiol 292(2):L577–L584. doi:10.1152/ajplung.00280.2006

    Article  PubMed  CAS  Google Scholar 

  • Larabee JL, Hocker JR, Hanas JS (2005) Cys redox reactions and metal binding of a Cys2His2 zinc finger. Arch Biochem Biophys 434(1):139–149. doi:10.1016/j.abb.2004.10.024

    Article  PubMed  CAS  Google Scholar 

  • Larche M (2007) Regulatory T cells in allergy and asthma. Chest 132(3):1007–1014. doi:10.1378/chest.06-2434

    Article  PubMed  CAS  Google Scholar 

  • Lau R, Pratt MA (2012) The opposing roles of cellular inhibitor of apoptosis proteins in cancer. ISRN Oncol 2012:928120. doi:10.5402/2012/928120

    PubMed  CAS  Google Scholar 

  • LeBlanc AC (2003) Natural cellular inhibitors of caspases. Prog Neuropsychopharmacol Biol Psychiatry 27(2):215–229. doi:10.1016/S0278-5846(03)00017-4

    Article  PubMed  CAS  Google Scholar 

  • Levkau B, Garton KJ, Ferri N, Kloke K, Nofer JR, Baba HA, Raines EW, Breithardt G (2001) xIAP induces cell-cycle arrest and activates nuclear factor-kappaB : new survival pathways disabled by caspase-mediated cleavage during apoptosis of human endothelial cells. Circ Res 88(3):282–290

    Article  PubMed  CAS  Google Scholar 

  • Li X, Yang Y, Ashwell JD (2002) TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature 416(6878):345–347. doi:10.1038/416345a

    Article  PubMed  Google Scholar 

  • Li L, Thomas RM, Suzuki H, De Brabander JK, Wang X, Harran PG (2004) A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death. Science 305(5689):1471–1474. doi:10.1126/science.1098231

    Article  PubMed  CAS  Google Scholar 

  • Lichten LA, Cousins RJ (2009) Mammalian zinc transporters: nutritional and physiologic regulation. Annu Rev Nutr 29:153–176. doi:10.1146/annurev-nutr-033009-083312

    Article  PubMed  Google Scholar 

  • Lin SC, Huang Y, Lo YC, Lu M, Wu H (2007) Crystal structure of the BIR1 domain of XIAP in two crystal forms. J Mol Biol 372(4):847–854. doi:10.1016/j.jmb.2007.07.019

    Article  PubMed  CAS  Google Scholar 

  • Liuzzi JP, Lichten LA, Rivera S, Blanchard RK, Aydemir TB, Knutson MD, Ganz T, Cousins RJ (2005) Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc Natl Acad Sci USA 102(19):6843–6848. doi:10.1073/pnas.0502257102

    Article  PubMed  CAS  Google Scholar 

  • Lopez J, John SW, Tenev T, Rautureau GJ, Hinds MG, Francalanci F, Wilson R, Broemer M, Santoro MM, Day CL, Meier P (2011) CARD-mediated autoinhibition of cIAP1’s E3 ligase activity suppresses cell proliferation and migration. Mol Cell 42(5):569–583. doi:10.1016/j.molcel.2011.04.008

    Article  PubMed  CAS  Google Scholar 

  • Luque LE, Grape KP, Junker M (2002) A highly conserved arginine is critical for the functional folding of inhibitor of apoptosis (IAP) BIR domains. Biochemistry 41(46):13663–13671

    Article  PubMed  CAS  Google Scholar 

  • Mace PD, Linke K, Feltham R, Schumacher FR, Smith CA, Vaux DL, Silke J, Day CL (2008) Structures of the cIAP2 RING domain reveal conformational changes associated with ubiquitin-conjugating enzyme (E2) recruitment. J Biol Chem 283(46):31633–31640. doi:10.1074/jbc.M804753200

    Article  PubMed  CAS  Google Scholar 

  • Mace PD, Smits C, Vaux DL, Silke J, Day CL (2010) Asymmetric recruitment of cIAPs by TRAF2. J Mol Biol 400(1):8–15. doi:10.1016/j.jmb.2010.04.055

    Article  PubMed  CAS  Google Scholar 

  • Maine GN, Mao X, Muller PA, Komarck CM, Klomp LW, Burstein E (2009) COMMD1 expression is controlled by critical residues that determine XIAP binding. Biochem J 417(2):601–609. doi:10.1042/BJ20080854

    Article  PubMed  CAS  Google Scholar 

  • Makhov P, Golovine K, Uzzo RG, Rothman J, Crispen PL, Shaw T, Scoll BJ, Kolenko VM (2008) Zinc chelation induces rapid depletion of the X-linked inhibitor of apoptosis and sensitizes prostate cancer cells to TRAIL-mediated apoptosis. Cell Death Differ 15(11):1745–1751. doi:10.1038/cdd.2008.106

    Article  PubMed  CAS  Google Scholar 

  • Manian P (1997) Genetics of asthma: a review. Chest 112(5):1397–1408

    Article  PubMed  CAS  Google Scholar 

  • Mao AP, Li S, Zhong B, Li Y, Yan J, Li Q, Teng C, Shu HB (2010) Virus-triggered ubiquitination of TRAF3/6 by cIAP1/2 is essential for induction of interferon-beta (IFN-beta) and cellular antiviral response. J Biol Chem 285(13):9470–9476. doi:10.1074/jbc.M109.071043

    Article  PubMed  CAS  Google Scholar 

  • Martinon F (2007) Orchestration of pathogen recognition by inflammasome diversity: variations on a common theme. Eur J Immunol 37(11):3003–3006. doi:10.1002/eji.200737871

    Article  PubMed  CAS  Google Scholar 

  • Mawhinney LJ, de Rivero Vaccari JP, Dale GA, Keane RW, Bramlett HM (2011) Heightened inflammasome activation is linked to age-related cognitive impairment in Fischer 344 rats. BMC Neurosci 12:123. doi:10.1186/1471-2202-12-123

    Article  PubMed  CAS  Google Scholar 

  • McComb S, Cheung HH, Korneluk RG, Wang S, Krishnan L, Sad S (2012) cIAP1 and cIAP2 limit macrophage necroptosis by inhibiting Rip1 and Rip3 activation. Cell Death Differ 19(11):1791–1801. doi:10.1038/cdd.2012.59

    Article  PubMed  CAS  Google Scholar 

  • Mercer EA, Korhonen L, Skoglosa Y, Olsson PA, Kukkonen JP, Lindholm D (2000) NAIP interacts with hippocalcin and protects neurons against calcium-induced cell death through caspase-3-dependent and -independent pathways. EMBO J 19(14):3597–3607. doi:10.1093/emboj/19.14.3597

    Article  PubMed  CAS  Google Scholar 

  • Mogil J (2007) Many asthma patients experience persistent symptoms despite appropriate clinical and guideline-based treatment with inhaled corticosteroids. J Am Acad Nurse Pract 19(9):459–470. doi:10.1111/j.1745-7599.2007.00247.x

    Article  PubMed  Google Scholar 

  • Morris DR, Levenson CW (2012) Ion channels and zinc: mechanisms of neurotoxicity and neurodegeneration. J Toxicol 2012:785647. doi:10.1155/2012/785647

    PubMed  Google Scholar 

  • Mufti AR, Burstein E, Csomos RA, Graf PC, Wilkinson JC, Dick RD, Challa M, Son JK, Bratton SB, Su GL, Brewer GJ, Jakob U, Duckett CS (2006) XIAP Is a copper binding protein deregulated in Wilson’s disease and other copper toxicosis disorders. Mol Cell 21(6):775–785. doi:10.1016/j.molcel.2006.01.033

    Article  PubMed  CAS  Google Scholar 

  • Mufti AR, Burstein E, Duckett CS (2007) XIAP: cell death regulation meets copper homeostasis. Arch Biochem Biophys 463(2):168–174. doi:10.1016/j.abb.2007.01.033

    Article  PubMed  CAS  Google Scholar 

  • Murgia C, Lang CJ, Truong-Tran AQ, Grosser D, Jayaram L, Ruffin RE, Perozzi G, Zalewski PD (2006) Zinc and its specific transporters as potential targets in airway disease. Curr Drug Targets 7(5):607–627

    Article  PubMed  CAS  Google Scholar 

  • Murgia C, Grosser D, Truong-Tran AQ, Roscioli E, Michalczyk A, Ackland ML, Stoltenberg M, Danscher G, Lang C, Knight D, Perozzi G, Ruffin RE, Zalewski P (2011) Apical localization of zinc transporter ZnT4 in human airway epithelial cells and its loss in a murine model of allergic airway inflammation. Nutrients 3(11):910–928. doi:10.3390/nu3110910

    Article  PubMed  CAS  Google Scholar 

  • Murphy DM, O’Byrne PM (2010) Recent advances in the pathophysiology of asthma. Chest 137(6):1417–1426. doi:10.1378/chest.09-1895

    Article  PubMed  CAS  Google Scholar 

  • Nakamura H, Kawakami A, Yamasaki S, Nakashima T, Kamachi M, Migita K, Kawabe Y, Nakamura T, Koji T, Hayashi Y, Eguchi K (2000) Expression and function of X chromosome-linked inhibitor of apoptosis protein in Sjogren’s syndrome. Lab Invest 80(9):1421–1427

    Article  PubMed  CAS  Google Scholar 

  • Ortiz J, Chou LL (2012) Calcium upregulated survivin expression and associated osteogenesis of normal human osteoblasts. J Biomed Mater Res A 100(7):1770–1776. doi:10.1002/jbm.a.34103

    PubMed  Google Scholar 

  • O’Sullivan MP, Tyner JW, Holtzman MJ (2003) Apoptosis in the airways: another balancing act in the epithelial program. Am J Respir Cell Mol Biol 29(1):3–7. doi:10.1165/rcmb.F273

    Article  PubMed  CAS  Google Scholar 

  • Ovaere P, Lippens S, Vandenabeele P, Declercq W (2009) The emerging roles of serine protease cascades in the epidermis. Trends Biochem Sci 34(9):453–463. doi:10.1016/j.tibs.2009.08.001

    Article  PubMed  CAS  Google Scholar 

  • Petraki CD, Karavana VN, Skoufogiannis PT, Little SP, Howarth DJ, Yousef GM, Diamandis EP (2001) The spectrum of human kallikrein 6 (zyme/protease M/neurosin) expression in human tissues as assessed by immunohistochemistry. J Histochem Cytochem 49(11):1431–1441

    Article  PubMed  CAS  Google Scholar 

  • Petraki CD, Karavana VN, Luo LY, Diamandis EP (2002) Human kallikrein 10 expression in normal tissues by immunohistochemistry. J Histochem Cytochem 50(9):1247–1261

    Article  PubMed  CAS  Google Scholar 

  • Petraki CD, Papanastasiou PA, Karavana VN, Diamandis EP (2006) Cellular distribution of human tissue kallikreins: immunohistochemical localization. Biol Chem 387(6):653–663. doi:10.1515/BC.2006.084

    Article  PubMed  CAS  Google Scholar 

  • Planque C, Blechet C, Ayadi-Kaddour A, Heuze-Vourc’h N, Dumont P, Guyetant S, Diamandis EP, El Mezni F, Courty Y (2008) Quantitative RT-PCR analysis and immunohistochemical localization of the kallikrein-related peptidases 13 and 14 in lung. Biol Chem 389(6):781–786. doi:10.1515/BC.2008.089

    Article  PubMed  CAS  Google Scholar 

  • Pohl C, Jentsch S (2008) Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 132(5):832–845. doi:10.1016/j.cell.2008.01.012

    Article  PubMed  CAS  Google Scholar 

  • Poon AH, Eidelman DH, Martin JG, Laprise C, Hamid Q (2012) Pathogenesis of severe asthma. Clin Exp Allergy 42(5):625–637. doi:10.1111/j.1365-2222.2012.03983.x

    Article  PubMed  CAS  Google Scholar 

  • Prasad AS (1995) Zinc: an overview. Nutrition 11(1 Suppl):93–99

    PubMed  CAS  Google Scholar 

  • Prasad AS (2012) Discovery of human zinc deficiency: 50 years later. J Trace Elem Med Biol 26(2–3):66–69. doi:10.1016/j.jtemb.2012.04.004

    Article  PubMed  CAS  Google Scholar 

  • Puddicombe SM, Torres-Lozano C, Richter A, Bucchieri F, Lordan JL, Howarth PH, Vrugt B, Albers R, Djukanovic R, Holgate ST, Wilson SJ, Davies DE (2003) Increased expression of p21(waf) cyclin-dependent kinase inhibitor in asthmatic bronchial epithelium. Am J Respir Cell Mol Biol 28(1):61–68

    Article  PubMed  CAS  Google Scholar 

  • Quirce S, Bobolea I, Barranco P (2012) Emerging drugs for asthma. Expert Opin Emerg Drugs 17(2):219–237. doi:10.1517/14728214.2012.683410

    Article  PubMed  CAS  Google Scholar 

  • Raeburn D, Webber SE (1994) Proinflammatory potential of the airway epithelium in bronchial asthma. Eur Respir J 7(12):2226–2233

    Article  PubMed  CAS  Google Scholar 

  • Rajalingam K, Dikic I (2009) Inhibitors of apoptosis catch ubiquitin. Biochem J 417(1):e1–e3. doi:10.1042/BJ20082215

    Article  PubMed  CAS  Google Scholar 

  • Ranaldi G, Ferruzza S, Canali R, Leoni G, Zalewski PD, Sambuy Y, Perozzi G, Murgia C (2012) Intracellular zinc is required for intestinal cell survival signals triggered by the inflammatory cytokine TNFalpha. J Nutr Biochem. doi:10.1016/j.jnutbio.2012.06.020

    PubMed  Google Scholar 

  • Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, Liddington RC, Salvesen GS (2001) Structural basis for the inhibition of caspase-3 by XIAP. Cell 104(5):791–800

    Article  PubMed  CAS  Google Scholar 

  • 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(7):1243–1252

    Article  PubMed  CAS  Google Scholar 

  • Roy N, Deveraux QL, Takahashi R, Salvesen GS, Reed JC (1997) The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J 16(23):6914–6925. doi:10.1093/emboj/16.23.6914

    Article  PubMed  CAS  Google Scholar 

  • Salvesen GS, Abrams JM (2004) Caspase activation—stepping on the gas or releasing the brakes? Lessons from humans and flies. Oncogene 23(16):2774–2784. doi:10.1038/sj.onc.1207522

    Article  PubMed  CAS  Google Scholar 

  • Sanna MG, da Silva Correia J, Luo Y, Chuang B, Paulson LM, Nguyen B, Deveraux QL, Ulevitch RJ (2002) ILPIP, a novel anti-apoptotic protein that enhances XIAP-mediated activation of JNK1 and protection against apoptosis. J Biol Chem 277(34):30454–30462. doi:10.1074/jbc.M203312200

    Article  PubMed  CAS  Google Scholar 

  • Scott FL, Denault JB, Riedl SJ, Shin H, Renatus M, Salvesen GS (2005) XIAP inhibits caspase-3 and -7 using two binding sites: evolutionarily conserved mechanism of IAPs. EMBO J 24(3):645–655. doi:10.1038/sj.emboj.7600544

    Article  PubMed  CAS  Google Scholar 

  • Shi Y (2004) Caspase activation, inhibition, and reactivation: a mechanistic view. Protein Sci 13(8):1979–1987. doi:10.1110/ps.04789804

    Article  PubMed  CAS  Google Scholar 

  • Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM, Alnemri ES, Fairman R, Shi Y (2003) Mechanism of XIAP-mediated inhibition of caspase-9. Mol Cell 11(2):519–527

    Article  PubMed  CAS  Google Scholar 

  • Silke J, Hawkins CJ, Ekert PG, Chew J, Day CL, Pakusch M, Verhagen AM, Vaux DL (2002) The anti-apoptotic activity of XIAP is retained upon mutation of both the caspase 3- and caspase 9-interacting sites. J Cell Biol 157(1):115–124. doi:10.1083/jcb.200108085

    Article  PubMed  CAS  Google Scholar 

  • Song Z, Yao X, Wu M (2003) Direct interaction between survivin and Smac/DIABLO is essential for the anti-apoptotic activity of survivin during taxol-induced apoptosis. J Biol Chem 278(25):23130–23140. doi:10.1074/jbc.M300957200

    Article  PubMed  CAS  Google Scholar 

  • Srinivasula SM, Ashwell JD (2008) IAPs: what’s in a name? Mol Cell 30(2):123–135. doi:10.1016/j.molcel.2008.03.008

    Article  PubMed  CAS  Google Scholar 

  • Stennicke HR, Ryan CA, Salvesen GS (2002) Reprieval from execution: the molecular basis of caspase inhibition. Trends Biochem Sci 27(2):94–101

    Article  PubMed  CAS  Google Scholar 

  • Sun C, Cai M, Gunasekera AH, Meadows RP, Wang H, Chen J, Zhang H, Wu W, Xu N, Ng SC, Fesik SW (1999) NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP. Nature 401(6755):818–822. doi:10.1038/44617

    Article  PubMed  CAS  Google Scholar 

  • Sun C, Cai M, Meadows RP, Xu N, Gunasekera AH, Herrmann J, Wu JC, Fesik SW (2000) NMR structure and mutagenesis of the third Bir domain of the inhibitor of apoptosis protein XIAP. J Biol Chem 275(43):33777–33781. doi:10.1074/jbc.M006226200

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Nakabayashi Y, Takahashi R (2001) 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 98(15):8662–8667. doi:10.1073/pnas.161506698

    Article  PubMed  CAS  Google Scholar 

  • Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, Wallberg F, Zachariou A, Lopez J, MacFarlane M, Cain K, Meier P (2011) The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell 43(3):432–448. doi:10.1016/j.molcel.2011.06.006

    Article  PubMed  CAS  Google Scholar 

  • Thompson PJ (1998) Unique role of allergens and the epithelium in asthma. Clin Exp Allergy 28 Suppl 5:110–116; discussion 117–118

    Google Scholar 

  • Tran HB, Lewis MD, Tan LW, Lester SE, Baker LM, Ng J, Hamilton-Bruce MA, Hill CL, Koblar SA, Rischmueller M, Ruffin RE, Wormald PJ, Zalewski PD, Lang CJ (2012) Immunolocalization of NLRP3 Inflammasome in Normal Murine Airway Epithelium and Changes following Induction of Ovalbumin-Induced Airway Inflammation. J Allergy (Cairo) 2012:819176. doi:10.1155/2012/819176

    Google Scholar 

  • Trautmann A, Schmid-Grendelmeier P, Kruger K, Crameri R, Akdis M, Akkaya A, Brocker EB, Blaser K, Akdis CA (2002) T cells and eosinophils cooperate in the induction of bronchial epithelial cell apoptosis in asthma. J Allergy Clin Immunol 109(2):329–337

    Article  PubMed  Google Scholar 

  • Truong-Tran AQ, Ruffin RE, Zalewski PD (2000) Visualization of labile zinc and its role in apoptosis of primary airway epithelial cells and cell lines. Am J Physiol Lung Cell Mol Physiol 279(6):L1172–L1183

    PubMed  CAS  Google Scholar 

  • Truong-Tran AQ, Ruffin RE, Foster PS, Koskinen AM, Coyle P, Philcox JC, Rofe AM, Zalewski PD (2002) Altered zinc homeostasis and caspase-3 activity in murine allergic airway inflammation. Am J Respir Cell Mol Biol 27(3):286–296

    Article  PubMed  CAS  Google Scholar 

  • Truong-Tran AQ, Grosser D, Ruffin RE, Murgia C, Zalewski PD (2003) Apoptosis in the normal and inflamed airway epithelium: role of zinc in epithelial protection and procaspase-3 regulation. Biochem Pharmacol 66(8):1459–1468

    Article  PubMed  CAS  Google Scholar 

  • Tumes DJ, Connolly A, Dent LA (2009) Expression of survivin in lung eosinophils is associated with pathology in a mouse model of allergic asthma. Int Immunol 21(6):633–644. doi:10.1093/intimm/dxp032

    Article  PubMed  CAS  Google Scholar 

  • Twiddy D, Cohen GM, Macfarlane M, Cain K (2006) Caspase-7 is directly activated by the approximately 700-kDa apoptosome complex and is released as a stable XIAP-caspase-7 approximately 200-kDa complex. J Biol Chem 281(7):3876–3888. doi:10.1074/jbc.M507393200

    Article  PubMed  CAS  Google Scholar 

  • Uhlen M, Bjorling E, Agaton C, Szigyarto CA, Amini B, Andersen E, Andersson AC, Angelidou P, Asplund A, Asplund C, Berglund L, Bergstrom K, Brumer H, Cerjan D, Ekstrom M, Elobeid A, Eriksson C, Fagerberg L, Falk R, Fall J, Forsberg M, Bjorklund MG, Gumbel K, Halimi A, Hallin I, Hamsten C, Hansson M, Hedhammar M, Hercules G, Kampf C, Larsson K, Lindskog M, Lodewyckx W, Lund J, Lundeberg J, Magnusson K, Malm E, Nilsson P, Odling J, Oksvold P, Olsson I, Oster E, Ottosson J, Paavilainen L, Persson A, Rimini R, Rockberg J, Runeson M, Sivertsson A, Skollermo A, Steen J, Stenvall M, Sterky F, Stromberg S, Sundberg M, Tegel H, Tourle S, Wahlund E, Walden A, Wan J, Wernerus H, Westberg J, Wester K, Wrethagen U, Xu LL, Hober S, Ponten F (2005) A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics 4(12):1920–1932. doi:10.1074/mcp.M500279-MCP200

    Article  PubMed  CAS  Google Scholar 

  • Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, Zwahlen M, Kampf C, Wester K, Hober S, Wernerus H, Bjorling L, Ponten F (2010) Towards a knowledge-based Human Protein Atlas. Nat Biotechnol 28(12):1248–1250. doi:10.1038/nbt1210-1248

    Article  PubMed  CAS  Google Scholar 

  • Ungvari I, Hadadi E, Virag V, Bikov A, Nagy A, Semsei AF, Galffy G, Tamasi L, Horvath I, Szalai C (2012) Implication of BIRC5 in asthma pathogenesis. Int Immunol 24(5):293–301. doi:10.1093/intimm/dxs007

    Article  PubMed  CAS  Google Scholar 

  • Uren AG, Wong L, Pakusch M, Fowler KJ, Burrows FJ, Vaux DL, Choo KH (2000) Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr Biol 10(21):1319–1328

    Article  PubMed  CAS  Google Scholar 

  • Vanlangenakker N, Vanden Berghe T, Bogaert P, Laukens B, Zobel K, Deshayes K, Vucic D, Fulda S, Vandenabeele P, Bertrand MJ (2011) cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ 18(4):656–665. doi:10.1038/cdd.2010.138

    Article  PubMed  CAS  Google Scholar 

  • 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(4):669–681. doi:10.1016/j.cell.2007.10.030

    Article  PubMed  CAS  Google Scholar 

  • Varfolomeev E, Goncharov T, Maecker H, Zobel K, Komuves LG, Deshayes K, Vucic D (2012) Cellular inhibitors of apoptosis are global regulators of NF-kappaB and MAPK activation by members of the TNF family of receptors. Sci Signal 5 (216):ra22. doi:10.1126/scisignal.2001878

  • Vaux DL, Silke J (2005) IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 6(4):287–297. doi:10.1038/nrm1621

    Article  PubMed  CAS  Google Scholar 

  • Verhagen AM, Coulson EJ, Vaux DL (2001) Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol 2 (7):REVIEWS3009

    Google Scholar 

  • Verhagen AM, Silke J, Ekert PG, Pakusch M, Kaufmann H, Connolly LM, Day CL, Tikoo A, Burke R, Wrobel C, Moritz RL, Simpson RJ, Vaux DL (2002) HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J Biol Chem 277(1):445–454. doi:10.1074/jbc.M109891200

    Article  PubMed  CAS  Google Scholar 

  • Vince JE, Pantaki D, Feltham R, Mace PD, Cordier SM, Schmukle AC, Davidson AJ, Callus BA, Wong WW, Gentle IE, Carter H, Lee EF, Walczak H, Day CL, Vaux DL, Silke J (2009) TRAF2 must bind to cellular inhibitors of apoptosis for tumor necrosis factor (tnf) to efficiently activate nf-{kappa}b and to prevent tnf-induced apoptosis. J Biol Chem 284(51):35906–35915. doi:10.1074/jbc.M109.072256

    Article  PubMed  CAS  Google Scholar 

  • Vischioni B, van der Valk P, Span SW, Kruyt FA, Rodriguez JA, Giaccone G (2006) Expression and localization of inhibitor of apoptosis proteins in normal human tissues. Hum Pathol 37(1):78–86. doi:10.1016/j.humpath.2005.09.022

    Article  PubMed  CAS  Google Scholar 

  • Vucic D, Kaiser WJ, Miller LK (1998) Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by Drosophila proteins HID and GRIM. Mol Cell Biol 18(6):3300–3309

    PubMed  CAS  Google Scholar 

  • Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS Jr (1998) NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281(5383):1680–1683

    Article  PubMed  CAS  Google Scholar 

  • Weber A, Kirejczyk Z, Besch R, Potthoff S, Leverkus M, Hacker G (2010) Proapoptotic signalling through Toll-like receptor-3 involves TRIF-dependent activation of caspase-8 and is under the control of inhibitor of apoptosis proteins in melanoma cells. Cell Death Differ 17(6):942–951. doi:10.1038/cdd.2009.190

    Article  PubMed  CAS  Google Scholar 

  • Webster JC, Huber RM, Hanson RL, Collier PM, Haws TF, Mills JK, Burn TC, Allegretto EA (2002) Dexamethasone and tumor necrosis factor-alpha act together to induce the cellular inhibitor of apoptosis-2 gene and prevent apoptosis in a variety of cell types. Endocrinology 143(10):3866–3874

    Article  PubMed  CAS  Google Scholar 

  • Wen LP, Madani K, Fahrni JA, Duncan SR, Rosen GD (1997) Dexamethasone inhibits lung epithelial cell apoptosis induced by IFN-gamma and Fas. Am J Physiol 273(5 Pt 1):L921–L929

    PubMed  CAS  Google Scholar 

  • Wenzel SE (2012) Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med 18(5):716–725. doi:10.1038/nm.2678

    Article  PubMed  CAS  Google Scholar 

  • White SR (2011) Apoptosis and the airway epithelium. J Allergy (Cairo) 2011:948406. doi:10.1155/2011/948406

    Google Scholar 

  • Wijesinghe M, Weatherall M, Perrin K, Crane J, Beasley R (2009) International trends in asthma mortality rates in the 5- to 34-year age group: a call for closer surveillance. Chest 135(4):1045–1049. doi:10.1378/chest.08-2082

    Article  PubMed  Google Scholar 

  • Wilson DH, Adams RJ, Appleton SL, Hugo G, Wilkinson D, Hiller J, Ryan P, Cheek J, Ruffin RE (2003) Prevalence of asthma and asthma action plans in South Australia: population surveys from 1990 to 2001. Med J Aust 178(10):483–485

    PubMed  Google Scholar 

  • Wright CW, Duckett CS (2005) Reawakening the cellular death program in neoplasia through the therapeutic blockade of IAP function. J Clin Invest 115(10):2673–2678. doi:10.1172/JCI26251

    Article  PubMed  CAS  Google Scholar 

  • Wu H, Panakanti R, Li F, Mahato RI (2010) XIAP gene expression protects beta-cells and human islets from apoptotic cell death. Mol Pharm. doi:10.1021/mp100070j

    Google Scholar 

  • Xiao C, Puddicombe SM, Field S, Haywood J, Broughton-Head V, Puxeddu I, Haitchi HM, Vernon-Wilson E, Sammut D, Bedke N, Cremin C, Sones J, Djukanovic R, Howarth PH, Collins JE, Holgate ST, Monk P, Davies DE (2011) Defective epithelial barrier function in asthma. J Allergy Clin Immunol 128 (3):549–556, e1–e12. doi:10.1016/j.jaci.2011.05.038

    Google Scholar 

  • Yang YL, Li XM (2000) The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res 10(3):169–177. doi:10.1038/sj.cr.7290046

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Yu X (2003) Regulation of apoptosis: the ubiquitous way. FASEB J 17(8):790–799. doi:10.1096/fj.02-0654rev

    Article  PubMed  CAS  Google Scholar 

  • Yun YJ, Li SH, Cho YS, Park JW, Chun YS (2010) Survivin mediates prostate cell protection by HIF-1alpha against zinc toxicity. Prostate 70(11):1179–1188. doi:10.1002/pros.21152

    Article  PubMed  CAS  Google Scholar 

  • Zalewski PD, Ruffin RE (2008) Apoptosis-regulatory factors as potential drug targets in the epithelium of normal and inflamed airways. Curr Mol Pharmacol 1(1):38–49

    PubMed  CAS  Google Scholar 

  • Zalewski PD, Forbes IJ, Betts WH (1993) Correlation of apoptosis with change in intracellular labile Zn(II) using zinquin [(2-methyl-8-p-toluenesulphonamido-6-quinolyloxy)acetic acid], a new specific fluorescent probe for Zn(II). Biochem J 296(Pt 2):403–408

    PubMed  CAS  Google Scholar 

  • Zalewski P, Truong-Tran A, Lincoln S, Ward D, Shankar A, Coyle P, Jayaram L, Copley A, Grosser D, Murgia C, Lang C, Ruffin R (2006) Use of a zinc fluorophore to measure labile pools of zinc in body fluids and cell-conditioned media. Biotechniques 40(4):509–520

    Article  PubMed  CAS  Google Scholar 

  • Zehntner SP, Bourbonniere L, Moore CS, Morris SJ, Methot D, St Jean M, Lacasse E, Hebb AL, Robertson GS, Durkin J, Gillard JW, Owens T (2007) X-linked inhibitor of apoptosis regulates T cell effector function. J Immunol 179(11):7553–7560

    PubMed  CAS  Google Scholar 

  • Zhang HG, Huang N, Liu D, Bilbao L, Zhang X, Yang P, Zhou T, Curiel DT, Mountz JD (2000) Gene therapy that inhibits nuclear translocation of nuclear factor kappaB results in tumor necrosis factor alpha-induced apoptosis of human synovial fibroblasts. Arthritis Rheum 43(5):1094–1105. doi:10.1002/1529-0131(200005)43:5<1094:AID-ANR20>3.0.CO;2-V

    Article  PubMed  CAS  Google Scholar 

  • Zhou C, Yin G, Liu J, Liu X, Zhao S (2011) Epithelial apoptosis and loss in airways of children with asthma. J Asthma 48(4):358–365. doi:10.3109/02770903.2011.565848

    Article  PubMed  Google Scholar 

  • Zuo J, Schmitt SM, Zhang Z, Prakash J, Fan Y, Bi C, Kodanko JJ, Dou QP (2012) Novel Polypyridyl chelators deplete cellular zinc and destabilize the X-linked inhibitor of apoptosis protein (XIAP) prior to induction of apoptosis in human prostate and breast cancer cells. J Cell Biochem 113(8):2567–2575. doi:10.1002/jcb.24132

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to acknowledge Mr Joshua Hallett for assistance with the IAP immunohistochemistry studies. This work was supported in part by NHMRC grants 519206 and 627223, as well as by a Hospital Research Foundation Scholarship. CM work in PZ laboratory was supported by the Grant EU “Microgennet” (EU Project Number 269210) funded within the Marie Curie Actions—International Research Staff Exchange Scheme (IRSES), see http://www.microgennet.org. The 16HBE14o- AEC line described by Cozens et al. (Cozens et al. 1994), were kindly provided by Dr Dieter Gruenert. We would like to acknowledge The American Journal of Physiology Lung Cellular and Molecular Physiology for their kind permission for the use of our Fig. 2b.

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Authors and Affiliations

  1. Discipline of Medicine, The Basil Hetzel Institute for Translational Research, The Queen Elizabeth Hospital, University of Adelaide, Woodville, SA, 5011, Australia

    Eugene Roscioli, Rhys Hamon & Peter Zalewski

  2. Rheumatology Unit, Queen Elizabeth Hospital, The Basil Hetzel Institute for Translational Research, Woodville, SA, 5011, Australia

    Susan Lester

  3. National Research Institute of Food and Nutrition (INRAN), Via Ardeatina, 546, Rome, Italy

    Chiara Murgia

  4. Discipline of Medicine, Population Research & Outcome Studies, University of Adelaide, Adelaide, SA, 5000, Australia

    Janet Grant

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  1. Eugene Roscioli
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  2. Rhys Hamon
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  5. Janet Grant
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  6. Peter Zalewski
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Correspondence to Eugene Roscioli.

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Roscioli, E., Hamon, R., Lester, S. et al. Zinc-rich inhibitor of apoptosis proteins (IAPs) as regulatory factors in the epithelium of normal and inflamed airways. Biometals 26, 205–227 (2013). https://doi.org/10.1007/s10534-013-9618-2

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  • DOI: https://doi.org/10.1007/s10534-013-9618-2

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