Intracellular Calcium Signaling Pathways during Liver Ischemia and Reperfusion

REFERENCES

• Nieuwenhuijs VB, De Bruijn MT, Padbury RT, Hepatic ischemia-reperfusion injury: roles of Ca2+ and other intracellular mediators of impaired bile flow and hepatocyte damage. Dig Dis Sci. 2006;51:1087–1102.
   PubMedGoogle Scholar
• Lopez-Neblina F, Toledo AH, Toledo-Pereyra LH. Molecular biology of apoptosis in ischemia and reperfusion. J Invest Surg. 2005;18:335–350.
   PubMed Web of Science ®Google Scholar
• Ono T, Imai K, Kohno H, Tauroursodeoxycholic acid protects cholestasis in rat reperfused livers—its roles in hepatic calcium mobilization. Dig Dis Sci. 1998;43:2201–2210.
   Google Scholar
• Mattson MP, Chan SL. Calcium orchestrates apoptosis. Nat Cell Biol. 2003;5:1041–1043.
   PubMed Web of Science ®Google Scholar
• Dong Z, Salkumar P, Weinberg JM, Calcium in cell injury and death. Annu Rev Pathol. 2006;1;405–434.
   Google Scholar
• Carafoli E, Crompton M. The regulation of intracellular calcium. Curr Topics Memb Transport. 1978;10:151–216.
   Google Scholar
• Blaustein MP, Ratzlaff R, Kendrick N. The regulation of intracellular calcium in presynaptic nerve terminals. Proc NY Acad Sci. 1978;307:195–212.
   Google Scholar
• Mitchell P, Moyle J. Chemiosmotic hypothesis of oxidative phosphorylation. Nature. 1967;213:137–139.
   PubMed Web of Science ®Google Scholar
• White BC, Wiegenstein JG, Winegar CD. Brain ischemia and anoxia: mechanisms of injury. J Am Med Assoc. 1984;251:1586–1590.
   PubMed Web of Science ®Google Scholar
• Hatanaka N, Kamike W, Shimizu S, Ca2+ release from mitochondria induces cytosolic enzyme leakage in anoxic liver. J Surg Res. 1995;58:485–490.
   Google Scholar
• Farber JL, Chien KR, Mittnacht S. The pathogenesis of irreversible cell injury in ischemia. Amer J Pathol. 1981;102:271–281.
   PubMed Web of Science ®Google Scholar
• Wolfe LS. Eicosanoids: prostaglandins, thromboxanes, leukotrienes and other derivatives of carbon-20 unsaturated fatty acids. J Neurochem. 1982;38:1–14.
   PubMed Web of Science ®Google Scholar
• Babbs CF. Role of iron ions in the genesis of reperfusion injury following successful cardiopulmonary resuscitation: preliminary data and a biochemical hypothesis. Ann Emerg Med. 1985;14:777–783.
   PubMed Web of Science ®Google Scholar
• Walsh KB, Toledo AH, Rivera-Chavez FA, Inflammatory mediators of liver ischemia-reperfusion injury. Exp Clin Transplant. 2009;7:78–93.
   PubMed Web of Science ®Google Scholar
• Tien M, Aust SD. Comparative aspects of several models of lipid peroxidation systems. In: Lipid Peroxides in Biology and Medicine. Yagi K, ed. New York: Academic Press; 1982:23–39.
   Google Scholar
• Klebanoff SJ. Phagocytic cells: products of oxygen metabolism. In: Inflammation: Basic Principles and Clinical Correlates. Gallin JI, Goldstein IM, Snyderman R, eds. New York: Raven Press; 1988:391–444.
   Google Scholar
• McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Eng J Med. 1985;312:159–163.
   PubMed Web of Science ®Google Scholar
• Kleihues K, Kobayashi K, Hossman KA. Purine nucleotide metabolism in the cat brain after one hour of complete ischemia. J Neurochem. 1974;23:417–425.
   Google Scholar
• Safar P. Cerebral resuscitation after cardiac arrest. A review. Circulation. 1986;74 (suppl IV):138.
   Google Scholar
• Hardy KJ, Tancheroen S, Shulkes A. Hepatic ischemia-reperfusion injury modification during liver surgery in rats: pretreatment with nifedipine or misoprostol. Liver Transpl Surg. 1995;1:302–310.
   Google Scholar
• Carini R, Castino R, DeCesaris MG, Preconditioning-induced cytoprotection in hepatocytes requires calcium- dependent exocytosis of lysosomes. J Cell Sci. 2004; 117:1065–1077.
   Google Scholar
• Crenesse D, Hugues M, Ferre C, Inhibition of calcium influx during hypoxia/reoxygenation in primary cultured rat hepatocytes. Pharmacology. 1999;58:160–170.
   Google Scholar
• Gasbarrini A, Borle AB, Farghali H, Effect of anoxia on intracellular ATP, Na+i, Ca2+i, Mg2+i, and cytotoxicity in rat hepatocytes. J Biol Chem. 1992;267:6654–6663.
   PubMed Web of Science ®Google Scholar
• Barritt GJ, Chen J, Rychkov GY. Ca2+ permeable channels in the hepatocyte plasma membrane and their roles in hepatocyte physiology. Biochim Biophys Acta. 2008;1783:651–672.
   Google Scholar
• Glantzounis GK, Salacinski HJ, Yang W, The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: a review. Liver Transpl. 2005;11:1031–1047.
   PubMed Web of Science ®Google Scholar
• Phillips L, Toledo AH, Lopez-Neblina F, Nitric oxide mechanism of protection in ischemia and reperfusion injury. J Invest Surg. 2009;22:46–55.
   PubMed Web of Science ®Google Scholar
• Ernster L. Biochemistry of reoxygenation injury. Crit Care Med. 1988;16:947–953.
   PubMedGoogle Scholar
• Farmer DG, Amersi F, Kupiec-Weglinski J, Current status of ischemia and reperfusion injury in the liver. Transplant Rev. 2000;14:106–126.
   Google Scholar
• Suehiro T, Yanaga K, Itasaka H, Beneficial effect of thromboxane A2 synthetase inhibitor on cold-stored rat liver. Transplantation. 1994;58:768–773.
   Google Scholar
• Hanazaki K, Kuroda T, Haba Y, Protective effect of the thromboxane A2 receptor antagonist ONO 3708 on ischemia-reperfusion injury in the dog liver. Surgery. 1994;116:896–903.
   Google Scholar
• Putney JW, Broad LM, Braun FJ, Mechanisms of capacitative calcium entry. J Cell Sci. 2001 (Jun);114:2223–2229.
   PubMed Web of Science ®Google Scholar
• Marzo I, Brenner C, Zamzami N, Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 1998;281:2027–2031.
   PubMed Web of Science ®Google Scholar
• Wang HG, Pathan N, Ethell IM, Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science. 1999;284:339–343.
   PubMed Web of Science ®Google Scholar
• Yi X, Yin XM, Dong Z. Inhibition of BID-induced apoptosis by Bcl-2. tBid insertion, Bax translocation, and Bax/Bak oligomerization suppressed. J Biol Chem. 2003;278:16992–16999.
   PubMed Web of Science ®Google Scholar
• Ott M, Robertson JD, Gogvadze V, Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA. 2002;99:1259–1263.
   PubMed Web of Science ®Google Scholar
• Halestrap AP. The mitochondrial permeability transition: its molecular mechanism and role in reperfusion injury. Biochem Soc Symp. 1999;66:181–203.
   PubMedGoogle Scholar
• Lam M, Dubyak G, Chen L, Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc Natl Acad Sci USA. 1994;91:6569–6573.
   PubMed Web of Science ®Google Scholar
• Meyer T, Hanson PI, Stryer L, Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science. 1992;256:1199–1202.
   PubMed Web of Science ®Google Scholar
• Cohen P. The structure and regulation of protein phosphatases. Annu Rev Biochem. 1989;58:453–508.
   PubMed Web of Science ®Google Scholar
• Chen F, Demers LM, Vallyathan V, Impairment of NF-kappaB activation and modulation of gene expression by calpastatin. Am J Physiol Cell Physiol. 2000 (Sep);279: C709–C716.
   PubMedGoogle Scholar
• Moldoveanu T, Hosfield CM, Lim D, A calcium switch aligns the active site of calpain. Cell. 2002;108:649–660.
   PubMed Web of Science ®Google Scholar
• Welm AL, Timchenko NA, Ono Y, C/EBP alpha is required for proteolytic cleavage of cyclin A by calpain 3 in myeloid precursor cells. J Biol Chem. 2002;277:33848–33856.
   Google Scholar
• Frame MC, Fincham VJ, Carragher NO, v-Src hold over actin and cell adhesions. Nat Rev Mol Cell Biol. 2002;3:233–245.
   PubMed Web of Science ®Google Scholar
• Goll DE, Thompson VF, Li H, The calpain system. Physiol Rev. 2003;83:731–801.
   PubMed Web of Science ®Google Scholar
• Vanderklish PW, Bahr BA. The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states. Int J Exp Pathol. 2000;81:323–339.
   PubMed Web of Science ®Google Scholar
• Liu X, Van Vleet T, Schnellmann RG. The role of calpain in oncotic cell death. Annu Rev Pharmacol Toxicol. 2004;44:349–370.
   PubMed Web of Science ®Google Scholar
• Edelstein CL, Ling H, Schrier RW. The nature of renal cell injury. Kidney Int. 1997;51:1341–1345.
   PubMed Web of Science ®Google Scholar
• Wang M, Sakon M, Miyoshi H, Prostacyclin analog-suppressed ischemia-reperfusion injury of the rat liver: evaluation by calpain-μ activation. J Surg Res. 1997;73:101–106.
   Google Scholar
• Wang M, Sakon M, Umeshita K, Determination of a safe vascular clamping method for liver surgery: evaluation by measuring activation of calpain-μ. Arch Surg. 1998;133:983–987.
   PubMedGoogle Scholar
• Miyoshi H, Umeshita K, Sakon M, Calpain activation in plasma membrane bleb formation during tert-butylhydroperoxide-induced rat hepatocyte injury. Gastroenterology. 1996;110:1897–1904.
   PubMed Web of Science ®Google Scholar
• Nakagawa T, Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol. 2000;150:887–894.
   PubMed Web of Science ®Google Scholar
• Ling YH, Liebes L, Ng B, PS-341, a novel proteasome inhibitor, induces Bcl-2 phosphorylation and cleavage in association with G2-M phase arrest and apoptosis. Mol Cancer Ther. 2002;1:841–849.
   PubMed Web of Science ®Google Scholar
• Arora AS, de Groen PC, Croall DE, Hepatocellular carcinoma cells resist necrosis during anoxia by preventing phospholipase-mediated calpain activation. J Cell Physiol. 1996;167:434–442.
   Google Scholar
• Arora AS, de-Groen P, Emori Y, A cascade of degradative hydrolase activity contributes to hepatocyte necrosis during anoxia. Am J Physiol. 1996;270:G238–G245.
   Google Scholar
• Murachi T, Tanaka K, Hatanaka M, Intracellular Ca2+-dependent protease (calpain) and its high molecular-weight endogenous inhibitor (calpastatin). Adv Enzyme Regul. 1980;19:407–424.
   PubMedGoogle Scholar
• Moldoveanu T, Hosfield CM, Lim D, A calcium switch aligns the active site of calpain. Cell. 2002;108:649–660.
   PubMed Web of Science ®Google Scholar
• Hajnoczky G, Csordas G, Madesh M, Control of apoptosis by IP3 and ryanodine receptor-driven calcium signals. Cell Calcium. 2000;28:349–363.
   PubMed Web of Science ®Google Scholar
• Nowycky MC, Thomas AP. Intracellular calcium signaling. J Cell Sci. 2002;115:3715–3716.
   PubMed Web of Science ®Google Scholar
• Kotlikoff MI. Calcium-induced calcium release in smooth muscle: the case for loose coupling. Prog Biophys Mol Biol. 2003;83:171–191.
   Google Scholar
• Putney JW, Broad LM, Braun FJ, Mechanisms of capacitative calcium entry. J Cell Sci. 2001;114:2223–2229.
   PubMed Web of Science ®Google Scholar
• Lopez-Neblina F, Toledo-Pereyra LH, Toledo AH, Ryanodine receptor antagonism protects the ischemia liver and modulates TNF-alpha and IL-10. J Surg Res. 2007;140:121–128.
   PubMedGoogle Scholar
• Lee HC. Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu Rev Pharmacol Toxicol. 2001;41:317–345.
   PubMed Web of Science ®Google Scholar
• Janicki PK, Wise PE, Belous AE, Interspecies differences in hepatic Ca(2+)-ATPase activity and the effect of cold preservation on porcine liver Ca(2+)-ATPase function. Liver Transpl. 2001;7:132–139.
   PubMedGoogle Scholar
• Mandic A, Hansson J, Linder S, Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J Biol Chem. 2003;278:9100–9106.
   PubMed Web of Science ®Google Scholar
• Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase12 mediates endoplasmic reticulum specific apoptosis and cytotoxicity by amyloid-beta. Nature. 2000;403:98–100.
   PubMed Web of Science ®Google Scholar
• Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M. Activation of caspase12, an endoplasmic reticulum resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem. 2001;276:13935–13940.
   PubMed Web of Science ®Google Scholar
• Nakagawa T, Zhu H, Morishima N, Caspase12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature. 2000;403:98–103.
   PubMed Web of Science ®Google Scholar
• Urano F, Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287:664–666.
   PubMed Web of Science ®Google Scholar
• Duchen MR. Mitochondria and calcium: from cell signaling to cell death. J Physiol. 2000;529:57–68.
   PubMed Web of Science ®Google Scholar
• Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium apoptosis link. Nat Rev Mol Cell Biol. 2003;4:552–565.
   PubMed Web of Science ®Google Scholar
• Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J. 1999;341:233–249.
   PubMed Web of Science ®Google Scholar
• Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev. 1999;79:1127–1155.
   PubMed Web of Science ®Google Scholar
• Lemasters JJ, Nieminen AL, Qian T, The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis, and autophagy. Biochem Biophys Acta. 1998;1366:177–196.
   PubMed Web of Science ®Google Scholar
• Frenkel RA, McGarry JD. Carnitine Biosynthesis, Metabolism and Functions. New York: Academic Press; 1980:321–340.
   Google Scholar
• Karmazyn M. The 1990 Merck Frost Award. Ischemic and reperfusion injury in the heart: cellular mechanisms and pharmacological interventions. Can J Physiol Pharmacol. 1991;69:719–730.
   Google Scholar
• Liu, X, Kim, CN, Yang, J, Induction of apoptotic program in cell free extracts: requirements for dATP and cytochrome c. Cell. 1996;86:147–157.
   PubMed Web of Science ®Google Scholar
• Du, C, Fang M, Li Y, SMAC, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 2000;102:33–42.
   PubMed Web of Science ®Google Scholar
• Verhagen AM, Ekert PG, Pakusch M, Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 2000;102:43–53.
   PubMed Web of Science ®Google Scholar
• Susin S, Zamzami N, Castedo M, Bcl-2 inhibits the mitochondrial release of apoptogenic protease. J Exp Med. 1996;184:1331–1341.
   PubMed Web of Science ®Google Scholar
• Joza N, Susin SA, Daugas E, Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature. 2001;410:549–554.
   PubMed Web of Science ®Google Scholar
• Crompton M, Barksby E, Johnson N, Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie. 2002;83:143–152.
   Google Scholar
• Halestrap AP, Doran E, Gillespie JP, Mitochondria and cell death. Biochem Soc Trans. 2000;28:170–177.
   PubMed Web of Science ®Google Scholar
• Andreyev A, Fiskum G. Calcium-induced release of mitochondrial cytochrome c by different mechanisms selective for brain versus liver. Cell Death Differ. 1999;6:825–832.
   PubMed Web of Science ®Google Scholar
• Petrosillo G, Ruggiero FM, Pistolese M, Ca-induced reactive oxygen species production promotes cytochrome c release from rat liver mitochondria via mitochondrial permeability transition (MPT)-dependent and MPT-independent mechanisms. J Biol Chem. 2004;271(51):53103–53108.
   Google Scholar
• Schild L, Keilhoff G, Augustin W, Distinct Ca2+ thresholds determine cytochrome c release or permeability transition pore opening in brain mitochondria. FASEB J. 2001;15:565–567.
   PubMed Web of Science ®Google Scholar
• Gogvadze V, Robertson JD, Zhivotovsky B, Cytochrome c release occurs via Ca2+-dependent and Ca2+-independent mechanisms that are regulated by Bax. J Biol Chem. 2001;276:19066–19071.
   PubMed Web of Science ®Google Scholar
• Kowaltowski AJ, Castilho RF, Vercesi AE. Ca(2+)-induced mitochondrial membrane permeabilization: role of coenzyme Q redox state. Am J Physiol. 1995;269:C141–C147.
   PubMedGoogle Scholar
• Kowaltowski AJ, Castilho F, Vercesi AE. Mitochondrial permeability transition and oxidative stress. FEBS Lett. 2001;495:12–15.
   PubMed Web of Science ®Google Scholar
• Starkov AA, Polster BM, Fiskum G. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J Neurochem. 2002;83:220–228.
   PubMed Web of Science ®Google Scholar
• Kanno T, Sato EF, Muranaka S, Oxidative stress underlies the mechanism for Ca2+-induced permeability transition of mitochondria. Free Radic Res. 2004;38:27–35.
   PubMed Web of Science ®Google Scholar
• Grijalba MT, Vercesi AE, Schreier S. Ca2+-induced increased lipid packing and domain formation in submitochondrial particles. A possible early step in the mechanism of Ca2+- stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry. 1999;38:13279–13287.
   PubMed Web of Science ®Google Scholar
• Castilho RF, Kowaltowsi AJ, Meinicke AR, Permeabilization of the inner mitochondrial membrane by Ca2+ ions is stimulated by t-butyl hydroperoxide and mediated by reactive oxygen species generated by mitochondria. Free Radic Biol Med. 1995;18:479–486.
   PubMed Web of Science ®Google Scholar
• Kowaltowski AJ, Vercesi AE, Castilho RF. Mitochondrial membrane protein thiol reactivity with N-ethylmaleimide or mersalyl is modified by Ca2+ -correlation with mitochondrial permeability transition. Biochim Biophys Acta. 1997;1318:395–402.
   Google Scholar
• Grijalba MT, Vercesi AE, Schreier S. Ca-induced increased lipid packing and domain formation in submitochondrial particles. A possible early step in the mechanism of Ca-stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry. 1999;38:13279–13287.
   PubMed Web of Science ®Google Scholar
• Petrosillo G, Ruggiero FM, Pistolese M, Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation: possible role in the apoptosis. FEBS Lett. 2001;509:435–438.
   PubMed Web of Science ®Google Scholar
• Asumendi A, Morales MC, Alvarez A. Implication of mitochondria-derived ROS and cardiolipin peroxidation in N-(4-hydroxyphenyl) retinamide-induced apoptosis. Br J Cancer. 2002;86:1951–1956.
   Google Scholar
• Petrosillo G, Ruggiero FM, Paradies G. Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. FASEB J. 2003;17:2202–2208.
   PubMed Web of Science ®Google Scholar
• Colell A, Garcia-Ruiz C, Mari M, FEBS Lett. Mitochondrial permeability transition induced by reactive oxygen species is independent of cholesterol-regulated membrane fluidity. 2004;60:63–68.
   Google Scholar
• Lutter M, Perkins GA, Wang X. The pro-apoptotic Bcl-2 family member tBid localizes to mitochondrial contact sites. BMC Cell Biol. 2001;2:22.
   PubMedGoogle Scholar
• Hsu YT, Wolter KG, Youle RJ. Cytosol-to-membrane redistribution of Bax and Bcl-Xl during apoptosis. Proc Natl Acad Sci. 1997;94:3669–3672.
   Google Scholar
• Wolter KG, Hsu YT, Smith CL, Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol. 1997;139:1281–1292.
   PubMed Web of Science ®Google Scholar
• Smaili SS, Hsu YT, Carvalho ACP, Mitochondria, calcium and pro-apoptotic proteins as mediators in cell death signaling. Braz J Med Biol Res. 2003;36:183–190.
   Google Scholar
• Nutt LK, Pataer A, Pahler J, Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial Ca2+ stores. J Biol Chem. 2002;277:9219– 9225.
   PubMed Web of Science ®Google Scholar
• Nutt LK, Chandra J, Pataer A, Bax-mediated Ca2+ mobilization promotes cytochrome c release during apoptosis. J Biol Chem. 2000;277:20301–20308.
   Google Scholar
• Csordas G, Madesh M, Antonsson B, tcBid promotes Ca2+ signal propagation to the mitochondria: control of Ca2+ permeation through the outer mitochondrial membrane. EMBO J. 2002;21:2198–2206.
   PubMed Web of Science ®Google Scholar
• Sakon M, Ariyoshi H, Umeshita K, Ischemia-reperfusion injury of the liver with special reference to calcium-dependent mechanisms. Surg Today 2002;32:1–12.
   Google Scholar
• Lane RD, Allan DM, Mellgren RL. A comparison of the intracellular distribution of mu-calpain, m-calpain, and calpastatin in proliferating human A431 cells. Exp Cell Res. 1992;203:5–16.
   PubMedGoogle Scholar
• Ikeda M, Ariyoshi H, Sakon M, A role for local calcium gradients upon hypoxic injury in human umbilical vein endothelial cells (HUVEC). Cell Calcium. 1998;23:49–57.
   Google Scholar
• Vanags DM, Porn-Ares MI, Coppola S, Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J Biol Chem. 1996;271:31075–31085.
   PubMed Web of Science ®Google Scholar
• Robertson JD, Enoksson M, Suomela M, Caspase-2 acts upstream of mitochondria to promote cytochrome c release during etoposide-induced apoptosis. J Biol Chem. 2002;277:29803–29809.
   PubMed Web of Science ®Google Scholar
• Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science. 2002;297:1352–1354.
   PubMed Web of Science ®Google Scholar
• Beresford PJ, Granzyme A activates an endoplasmic reticulum-associated caspase-independent nuclease to induce single-stranded DNA nicks. J Biol Chem. 2001;276:43285–43293.
   PubMedGoogle Scholar
• Fan Z, Beresford PJ, Oh DY, Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell. 2003;112:659–672.
   PubMed Web of Science ®Google Scholar
• Tacchini L, Radice L, Bernelli-Zazzera A. Differential activation of some transcription factors during rat liver ischemia, reperfusion, and heat shock. J Cell Physiol. 1999;180:255–262.
   PubMed Web of Science ®Google Scholar
• Latanich CA, Toledo-Pereyra LH. Searching for NF-kappaB based treatments of ischemia reperfusion injury. J Invest Surg. 2009;22:301–315.
   PubMed Web of Science ®Google Scholar
• Stehlik C, de Martin R, Kumabashiri I, Nuclear factor (NF)-kappaB-regulated X-chromosome-linked IAP gene expression protects endothelial cells from tumor necrosis factor alpha-induced necrosis. J Exp Med. 1999;188:211–216.
   Google Scholar
• Sheikh S, Huang Y. Death receptor activation complexes: it takes two to activate TNF receptor 1. Cell Cycle. 2003;2:549–551.
   Web of Science ®Google Scholar