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

Free Radical Research

Volumn 43, Issue 12, 2009, Pages 1225-1239

  Pardo, Michal ^a   Tirosh, Oren ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Apoptosis; Microarray; Mitochondrial defense; Reactive oxygen species; Redox signaling

Indexed keywords

GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEME OXYGENASE 1; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ADAPTATION; ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL DEATH; CELL HYPOXIA; CELL PROTECTION; CELL STRESS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENE TRANSLOCATION; LIPID PEROXIDATION; LIVER CELL; MEDIATOR; MICROARRAY ANALYSIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REOXYGENATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL HYPOXIA; CELL LINE; CELL SURVIVAL; DOWN-REGULATION; GLUTATHIONE; HEPATOCYTES; LIPID PEROXIDATION; MICE; OXYGEN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 70449653432     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715760903271256     Document Type: Article

References (45)

1. Lemasters JJ. The mitochondrial permeability transition and the calcium, oxygen and pH paradoxes: one paradox after another. Cardiovasc Res 1999;44:470-473
2. 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.
3. Fridovich I. Superoxide dismutases: defence against endogenous superoxide radical. Ciba Found Symp 1978;65:77-93.
4. 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.
5. Yang J, Marden JJ, Fan C, Sanlioglu S, Weiss RM, Ritchie TC, Davisson RL, Engelhardt JF Genetic redox precondi tioning 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.
6. 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.
7. 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.
8. 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.
9. Leonard MO, Kieran NE, Howell K, Burne MJ, Varadarajan R, Dhakshinamoorthy S, Porter AG, O'Farrelly C, Rabb H, Taylor CT Reoxygenation-specifi c activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. Faseb J 2006; 20:2624-2626.
10. 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:el000166.
11. Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 2004; 36:1199-1207.
12. 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 phytochem-icals. Planta Med 2008;74:1526-1539.
13. Kim YJ, Ahn JY, Liang P, Ip C, Zhang Y, Park YM. Human prxl gene is a target of Nrf2 and is up-regulated byhypoxia/ reoxygenation: implication to tumor biology. Cancer Res 2007;67:546-554.
14. 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 mito chondrial membrane potential in H9c2 cardiomyocytes. Life Sci 2008;82: 1092-1101.
15. Downey T Analysis of a multifactor microarray study using Partek genomics solution. Methods Enzymol 2006;411: 256-270.
16. 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.
17. Pardo M, Melendez JA, Tirosh O. Manganese super oxide dismutase inactivation during Fas (CD95)-mediated apoptosis in Jurkat T cells. Free Radic Biol Med 2006;41:1795-1806.
18. Patel V, Chivukula IV, Roy S, Khanna S, He G, Ojha N, Mehrotra A, Dias LM, Hunt TK, Sen CK. Oxygen: from the benefi ts of inducing VEGF expression to managing the risk of hyperbaric stress. Antioxid Redox Signal 2005;7:1377-1387.
19. Serviddio G, Bellanti F, Tamborra R, Rollo T, Capitanio N, Romano AD, Sastre J, Vendemiale G, Altomare E. Uncou pling 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.
20. Dolgachev V, Oberley LW, Huang TT, Kraniak JM, Tainsky MA, Hanada K, Separovic D. A role for manganese super oxide dismutase in apoptosis after photosensitization. Bio chem Biophys Res Commun 2005;332:411-417
21. Sarsour EH, Agarwal M, Pandita TK, Oberley LW, Goswami PC. Manganese superoxide dismutase protects the prolifera-tive capacity of confl uent normal human fi broblasts. J Biol Chem 2005;280:18033-18041.
22. 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.
23. 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.
24. Xue H, Guo H, Li YC, Hao ZM. Heme oxygenase-1 induction by hemin protects liver cells from ischemia/reperfu sion injury in cirrhotic rats. World J Gastroenterol 2007; 13: 5384-5390.
25. 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
26. 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.
27. 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.
28. 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.
29. 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
30. 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.
31. 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.
32. 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 Epasl-/-mice. Nat Genet 2003;35:331-340.
33. Na HK, Kim EH, Jung JH, Lee HH, Hyun JW, Surh YJ. (-)-Epigallocatechin gallate induces Nrf2-mediated anti-oxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells. Arch Biochem Biophys 2008; 476:171-177.
34. 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.
35. Seng S, Avraham HK, Birrane G, Jiang S, Li H, Katz G, Bass CE, Zagozdzon R, Avraham S. NRP/B mutations impair Nrf2-dependent NQOl induction in human primary brain tumors. Oncogene 2008;28:378-389.
36. 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.
37. Lu SC. Regulation of glutathione synthesis. Mol Aspects Med 2008;l-2:42-59. [Epub ahead of print].
38. Fokkelman K, Haase E, Stevens J, Idikio H, Korbutt G, Bigam D, Cheung PY Tissue-specifi c changes in glutathione content of hypoxic newborn pigs reoxygenated with 21% or 100% oxygen. Eur J Pharmacol 2007;562:132-137. (Pubitemid 46466758)
39. 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.
40. 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. (Pubitemid 24167855)
41. 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.
42. 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 po tential and generation of reactive oxygen species in early programmed cell death. J Exp Med 1995;182:367-377.
43. Sutton A, Imbert A, Igoudjil A, Descatoire V, Cazanave S, Pessayre D, Degoul F. The manganese superoxide dismutase Alal6Val dimorphism modulates both mitochondrial import and mRNA stability. Pharmacogenet Genomics 2005; 15:311-319.
44. 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. Onco-gene 2005;24:77-89.
45. 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.