Protective signalling effect of manganese superoxide dismutase in hypoxia-reoxygenation of hepatocytes

References

• Lemasters JJ. The mitochondrial permeability transition and the calcium, oxygen and pH paradoxes: one paradox after another. Cardiovasc Res 1999;44:470–473.
   Google Scholar
• Lemasters JJ, DiGuiseppi J, Nieminen AL, Herman B. Blebbing, free Ca2+ and mitochondrial membrane potential preceding cell death in hepatocytes. Nature 1987;325:78–81.
   PubMed Web of Science ®Google Scholar
• Fridovich I. Superoxide dismutases: defence against endogenous superoxide radical. Ciba Found Symp 1978;65:77–93.
   Google Scholar
• Pardo M, Budick-Harmelin N, Tirosh B, Tirosh O. Antioxidant defense in hepatic ischemia-reperfusion injury is regulated by damage-associated molecular pattern signal molecules. Free Radic Biol Med 2008;45:1073–1083.
   PubMedGoogle Scholar
• Yang J, Marden JJ, Fan C, Sanlioglu S, Weiss RM, Ritchie TC, Davisson RL, Engelhardt JF. Genetic redox preconditioning differentially modulates AP-1 and NF kappa B responses following cardiac ischemia/reperfusion injury and protects against necrosis and apoptosis. Mol Ther 2003;7:341–353.
   PubMed Web of Science ®Google Scholar
• Tanaka T, Hakoda S, Takeyama N. Reoxygenation-induced mitochondrial damage is caused by the Ca2+-dependent mitochondrial inner membrane permeability transition. Free Radic Biol Med 1998;25:26–32.
   Google Scholar
• Su YT, Chang HL, Shyue SK, Hsu SL. Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway. Biochem Pharmacol 2005;70:229–241.
   PubMed Web of Science ®Google Scholar
• Kokoszka JE, Coskun P, Esposito LA, Wallace DC. Increased mitochondrial oxidative stress in the Sod2 (+/−) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc Natl Acad Sci USA 2001;98:2278–2283.
   PubMed Web of Science ®Google Scholar
• Leonard MO, Kieran NE, Howell K, Burne MJ, Varadarajan R, Dhakshinamoorthy S, Porter AG, O'Farrelly C, Rabb H, Taylor CT. Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. Faseb J 2006;20:2624–2626.
   PubMed Web of Science ®Google Scholar
• Taylor RC, Acquaah-Mensah G, Singhal M, Malhotra D, Biswal S. Network inference algorithms elucidate Nrf2 regulation of mouse lung oxidative stress. PLoS Comput Biol 2008;4:e1000166–
   Google Scholar
• Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 2004;36:1199–1207.
   PubMed Web of Science ®Google Scholar
• Surh YJ, Kundu JK, Na HK. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med 2008;74:1526–1539.
   PubMed Web of Science ®Google Scholar
• Kim YJ, Ahn JY, Liang P, Ip C, Zhang Y, Park YM. Human prx1 gene is a target of Nrf2 and is up-regulated by hypoxia/reoxygenation: implication to tumor biology. Cancer Res 2007;67:546–554.
   PubMed Web of Science ®Google Scholar
• Chiu PY, Luk KF, Leung HY, Ng KM, Ko KM. Schisandrin B stereoisomers protect against hypoxia/reoxygenation-induced apoptosis and inhibit associated changes in Ca2+-induced mitochondrial permeability transition and mitochondrial membrane potential in H9c2 cardiomyocytes. Life Sci 2008;82:1092–1101.
   PubMed Web of Science ®Google Scholar
• Downey T. Analysis of a multifactor microarray study using Partek genomics solution. Methods Enzymol 2006;411:256–270.
   Google Scholar
• Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001;125:279–284.
   PubMed Web of Science ®Google Scholar
• Pardo M, Melendez JA, Tirosh O. Manganese superoxide dismutase inactivation during Fas (CD95)-mediated apoptosis in Jurkat T cells. Free Radic Biol Med 2006;41:1795–1806.
   Google Scholar
• Patel V, Chivukula IV, Roy S, Khanna S, He G, Ojha N, Mehrotra A, Dias LM, Hunt TK, Sen CK. Oxygen: from the benefits of inducing VEGF expression to managing the risk of hyperbaric stress. Antioxid Redox Signal 2005;7:1377–1387.
   Google Scholar
• Serviddio G, Bellanti F, Tamborra R, Rollo T, Capitanio N, Romano AD, Sastre J, Vendemiale G, Altomare E. Uncoupling protein-2 (UCP2) induces mitochondrial proton leak and increases susceptibility of non-alcoholic steatohepatitis (NASH) liver to ischaemia-reperfusion injury. Gut 2008;57:957–965.
   PubMed Web of Science ®Google Scholar
• Dolgachev V, Oberley LW, Huang TT, Kraniak JM, Tainsky MA, Hanada K, Separovic D. A role for manganese superoxide dismutase in apoptosis after photosensitization. Biochem Biophys Res Commun 2005;332:411–417.
   PubMed Web of Science ®Google Scholar
• Sarsour EH, Agarwal M, Pandita TK, Oberley LW, Goswami PC. Manganese superoxide dismutase protects the proliferative capacity of confluent normal human fibroblasts. J Biol Chem 2005;280:18033–18041.
   Google Scholar
• Haga S, Terui K, Fukai M, Oikawa Y, Irani K, Furukawa H, Todo S, Ozaki M. Preventing hypoxia/reoxygenation damage to hepatocytes by p66(shc) ablation: up-regulation of anti-oxidant and anti-apoptotic proteins. J Hepatol 2008;48:422–432.
   PubMedGoogle Scholar
• Hirai F, Motoori S, Kakinuma S, Tomita K, Indo HP, Kato H, Yamaguchi T, Yen HC, St Clair DK, Nagano T, Ozawa T, Saisho H, Majima HJ. Mitochondrial signal lacking manganese superoxide dismutase failed to prevent cell death by reoxygenation following hypoxia in a human pancreatic cancer cell line, KP4. Antioxid Redox Signal 2004;6:523–535.
   PubMed Web of Science ®Google Scholar
• Xue H, Guo H, Li YC, Hao ZM. Heme oxygenase-1 induction by hemin protects liver cells from ischemia/reperfusion injury in cirrhotic rats. World J Gastroenterol 2007;13:5384–5390.
   PubMed Web of Science ®Google Scholar
• Murley JS, Kataoka Y, Baker KL, Diamond AM, Morgan WF, Grdina DJ. Manganese superoxide dismutase (SOD2)-mediated delayed radioprotection induced by the free thiol form of amifostine and tumor necrosis factor alpha. Radiat Res 2007;167:465–474.
   PubMed Web of Science ®Google Scholar
• van de Wetering CI, Coleman MC, Spitz DR, Smith BJ, Knudson CM. Manganese superoxide dismutase gene dosage affects chromosomal instability and tumor onset in a mouse model of T cell lymphoma. Free Radic Biol Med 2008;44:1677–1686.
   PubMed Web of Science ®Google Scholar
• Kowluru RA, Kowluru V, Xiong Y, Ho YS. Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress. Free Radic Biol Med 2006;41:1191–1196.
   PubMed Web of Science ®Google Scholar
• Chen CS, Zhao Q, Wang J, Rong JJ, Yuan QS, Guo QL, Wu WT. Enhanced anti-tumor effects achieved in a murine tumor model using combination therapy of recombinant human manganese superoxide dismutase and adriamycin. Biochem Biophys Res Commun 2008;370:663–668.
   Google Scholar
• Sarsour EH, Venkataraman S, Kalen AL, Oberley LW, Goswami PC. Manganese superoxide dismutase activity regulates transitions between quiescent and proliferative growth. Aging Cell 2008;7:405–417.
   PubMed Web of Science ®Google Scholar
• Dasgupta J, Subbaram S, Connor KM, Rodriguez AM, Tirosh O, Beckman JS, Jourd'Heuil D, Melendez JA. Manganese superoxide dismutase protects from TNF-alpha-induced apoptosis by increasing the steady-state production of H2O2. Antioxid Redox Signal 2006;8:1295–1305.
   PubMed Web of Science ®Google Scholar
• Dioum EM, Chen R, Alexander MS, Zhang Q, Hogg RT, Gerard RD, Garcia JA. Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science 2009;324:1289–1293.
   PubMed Web of Science ®Google Scholar
• Scortegagna M, Ding K, Oktay Y, Gaur A, Thurmond F, Yan LJ, Marck BT, Matsumoto AM, Shelton JM, Richardson JA, Bennett MJ, Garcia JA. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1 −/− mice. Nat Genet 2003;35:331–340.
   PubMedGoogle Scholar
• Na HK, Kim EH, Jung JH, Lee HH, Hyun JW, Surh YJ. (−)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells. Arch Biochem Biophys 2008;476:171–177.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Kelly VP, Motohashi H, Nakajima O, Takahashi S, Nishimura S, Yamamoto M. Deletion of the selenocysteine tRNA gene in macrophages and liver results in compensatory gene induction of cytoprotective enzymes by Nrf2. J Biol Chem 2008;283:2021–2030.
   PubMed Web of Science ®Google Scholar
• Seng S, Avraham HK, Birrane G, Jiang S, Li H, Katz G, Bass CE, Zagozdzon R, Avraham S. NRP/B mutations impair Nrf2-dependent NQO1 induction in human primary brain tumors. Oncogene 2008;28:378–389.
   Google Scholar
• Partridge J, Carlsen H, Enesa K, Chaudhury H, Zakkar M, Luong L, Kinderlerer A, Johns M, Blomhoff R, Mason JC, Haskard DO, Evans PC. Laminar shear stress acts as a switch to regulate divergent functions of NF-kappaB in endothelial cells. Faseb J 2007;21:3553–3561.
   PubMed Web of Science ®Google Scholar
• Lu SC. Regulation of glutathione synthesis. Mol Aspects Med 2008;1–2:42–59. [Epub ahead of print].
   Google Scholar
• Fokkelman K, Haase E, Stevens J, Idikio H, Korbutt G, Bigam D, Cheung PY. Tissue-specific changes in glutathione content of hypoxic newborn pigs reoxygenated with 21% or 100% oxygen. Eur J Pharmacol 2007;562:132–137.
   Google Scholar
• Ding Y, Choi KJ, Kim JH, Han X, Piao Y, Jeong JH, Choe W, Kang I, Ha J, Forman HJ, Lee J, Yoon KS, Kim SS. Endogenous hydrogen peroxide regulates glutathione redox via nuclear factor erythroid 2-related factor 2 downstream of phosphatidylinositol 3-kinase during muscle differentiation. Am J Pathol 2008;172:1529–1541.
   PubMed Web of Science ®Google Scholar
• Caraceni P, Rosenblum ER, Van Thiel DH, Borle AB. Reoxygenation injury in isolated rat hepatocytes: relation to oxygen free radicals and lipid peroxidation. Am J Physiol 1994;266:G799–G806.
   PubMed Web of Science ®Google Scholar
• McDermott BJ, McWilliams S, Smyth K, Kelso EJ, Spiers JP, Zhao Y, Bell D, Mirakhur RK. Protection of cardiomyocyte function by propofol during simulated ischemia is associated with a direct action to reduce pro-oxidant activity. J Mol Cell Cardiol 2007;42:600–608.
   Google Scholar
• Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 1995;182:367–377.
   PubMed Web of Science ®Google Scholar
• Sutton A, Imbert A, Igoudjil A, Descatoire V, Cazanave S, Pessayre D, Degoul F. The manganese superoxide dismutase Ala16Val dimorphism modulates both mitochondrial import and mRNA stability. Pharmacogenet Genomics 2005;15:311–319.
   PubMed Web of Science ®Google Scholar
• Venkataraman S, Jiang X, Weydert C, Zhang Y, Zhang HJ, Goswami PC, Ritchie JM, Oberley LW, Buettner GR. Manganese superoxide dismutase overexpression inhibits the growth of androgen-independent prostate cancer cells. Oncogene 2005;24:77–89.
   PubMed Web of Science ®Google Scholar
• Inarrea P, Moini H, Han D, Rettori D, Aguilo I, Alava MA, Iturralde M, Cadenas E. Mitochondrial respiratory chain and thioredoxin reductase regulate intermembrane Cu,Zn-superoxide dismutase activity: implications for mitochondrial energy metabolism and apoptosis. Biochem J 2007;405:173–179.
   PubMedGoogle Scholar