Loss of manganese superoxide dismutase leads to abnormal growth and signal transduction in mouse embryonic fibroblasts

Free Radical Biology and Medicine

Volumn 49, Issue 8, 2010, Pages 1255-1262

  Zhang, Yiqiang ^a,b   Zhang, Hong Mei ^a,c   Shi, Yun ^a   Lustgarten, Michael ^a   Li, Yan ^a   Qi, Wenbo ^a   Zhang, Bin Xian ^a   Van Remmen, Holly ^a,b,d  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Free radicals; MnSOD; Oxidative stress; ROS; Signal transduction

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; CALCIUM; FREE RADICAL; G PROTEIN COUPLED RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; MAMMALIAN TARGET OF RAPAMYCIN; MANGANESE SUPEROXIDE DISMUTASE; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; MNTBAP; PEROXIREDOXIN 3; PRDX3; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; FIBROBLAST; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; AUTOPHAGY; CELL PROLIFERATION; CELLS, CULTURED; FIBROBLASTS; GLYCOGEN SYNTHASE KINASE 3; GROWTH INHIBITORS; MICE; MICE, KNOCKOUT; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PEROXIREDOXINS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; SUPEROXIDES; TOR SERINE-THREONINE KINASES;

MUS;

EID: 77956551895     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.07.006     Document Type: Article

References (65)

1. Knight J.A. Free radicals: their history and current status in aging and disease. Ann. Clin. Lab. Sci. 1998, 28:331-346.
2. McCord J.M. Superoxide dismutase in aging and disease: an overview. Methods Enzymol. 2002, 349:331-341.
3. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem. Soc. Trans. 2008, 36(Pt 3):343-347.
4. Bashan N., Kovsan J., Kachko I., Ovadia H., Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol. Rev. 2009, 89:27-71.
5. Henderson J.R., Swalwell H., Boulton S., Manning P., McNeil C.J., Birch-Machin M.A. Direct, real-time monitoring of superoxide generation in isolated mitochondria. Free Radic. Res. 2009, 43:796-802.
6. Li Y., et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 1995, 11:376-381.
7. Lebovitz R.M., Zhang H., Vogel H., Cartwright J., Dionne L., Lu N., Huang S., Matzuk M.M. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl. Acad. Sci. USA 1996, 93:9782-9787.
8. Huang T.T., Carlson E.J., Raineri I., Gillespie A.M., Kozy H., Epstein C.J. The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann. NY Acad. Sci. 1999, 893:95-112.
9. Van Remmen H., et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genomics 2003, 16:29-37.
10. Williams M.D., Van Remmen H., Conrad C.C., Huang T.T., Epstein C.J., Richardson A. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J. Biol. Chem. 1998, 273:28510-28515.
11. Van Remmen H., Salvador C., Yang H., Huang T.T., Epstein C.J., Richardson A. Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch. Biochem. Biophys. 1999, 363:91-97.
12. Van Remmen H., Williams M.D., Guo Z., Estlack L., Yang H., Carlson E.J., Epstein C.J., Huang T.T., Richardson A. Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H1422-H1432.
13. Strassburger M., et al. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic. Biol. Med. 2005, 38:1458-1470.
14. Huang T.T., Yasunami M., Carlson E.J., Gillespie A.M., Reaume A.G., Hoffman E.K., Chan P.H., Scott R.W., Epstein C.J. Superoxide-mediated cytotoxicity in superoxide dismutase-deficient fetal fibroblasts. Arch. Biochem. Biophys. 1997, 344:424-432.
15. Tsan M.F., White J.E., Caska B., Epstein C.J., Lee C.Y. Susceptibility of heterozygous MnSOD gene-knockout mice to oxygen toxicity. Am. J. Respir. Cell. Mol. Biol. 1998, 19:114-120.
16. Kokoszka J.E., Coskun P., Esposito L.A., Wallace D.C. 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.
17. Asikainen T.M., Huang T.T., Taskinen E., Levonen A.L., Carlson E., Lapatto R., Epstein C.J., Raivio K.O. Increased sensitivity of homozygous Sod2 mutant mice to oxygen toxicity. Free Radic. Biol. Med. 2002, 32:175-186.
18. Sarsour E.H., Venkataraman S., Kalen A.L., Oberley L.W., Goswami P.C. Manganese superoxide dismutase activity regulates transitions between quiescent and proliferative growth. Aging Cell 2008, 7:405-417.
19. Reiling J.H., Sabatini D.M. Stress and mTORture signaling. Oncogene 2006, 25:6373-6383.
20. Schieke S.M., Finkel T. Mitochondrial signaling, TOR, and life span. Biol. Chem. 2006, 387:1357-1361.
21. Schieke S.M., Phillips D., McCoy J.P., Aponte A.M., Shen R.F., Balaban R.S., Finkel T. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 2006, 281:27643-27652.
22. Perez de Obanos M.P., Lopez-Zabalza M.J., Arriazu E., Modol T., Prieto J., Herraiz M.T., Iraburu M.J. Reactive oxygen species (ROS) mediate the effects of leucine on translation regulation and type I collagen production in hepatic stellate cells. Biochim. Biophys. Acta 2007, 1773:1681-1688.
23. 2+/CaM signaling to hVps34. Cell Metab. 2008, 7:456-465.
24. Ballou L.M., Jiang Y.P., Du G., Frohman M.A., Lin R.Z. Ca(2+)- and phospholipase D-dependent and -independent pathways activate mTOR signaling. FEBS Lett. 2003, 550:51-56.
25. Zhang Y.Q., Herman B. Expression and modification of ARC (apoptosis repressor with a CARD domain) is distinctly regulated by oxidative stress in cancer cells. J. Cell. Biochem. 2008, 194:818-825.
26. 2+ from mitochondria. Am. J. Physiol. Cell Physiol. 2006, 290:C1321-C1333.
27. Muller F.L., et al. Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radic. Biol. Med. 2006, 40:1993-2004.
28. Roberts L.J., Oates J.A., Linton M.F., Fazio S., Meador B.P., Gross M.D., Shyr Y., Morrow J.D. The relationship between dose of vitamin E and suppression of oxidative stress in humans. Free Radic. Biol. Med. 2007, 43:1388-1393.
29. Zielonka J., Vasquez-Vivar J., Kalyanaraman B. Detection of 2-hydroxyethidium in cellular systems: a unique marker product of superoxide and hydroethidine. Nat. Protoc. 2008, 3:8-21.
30. Elchuri S., Oberley T.D., Qi W., Eisenstein R.S., Jackson Roberts L., Van Remmen H., Epstein C.J., Huang T.T. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 2005, 24:367-380.
31. 2+ and ROS. Front. Biosci. 2009, 14:1197-1218.
32. 2+ homeostasis in SOD1G93A mice. Mol. Pharmacol. 2009, 75:478-489.
33. Zhang H.M., Dang H., Yeh C., Zhang B. Linoleic acid-induced mitochondrial Ca(2+) efflux causes peroxynitrite generation and protein nitrotyrosylation, 8. PLoS ONE 2009, 4:60.
34. 2+ efflux. J. Biol. Chem. 2008, 283:7580-7589.
35. D'Autreaux B., Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell. Biol. 2007, 8:813-824.
36. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
37. Klionsky D.J., et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
38. Morten K.J., Ackrell B.A., Melov S. Mitochondrial reactive oxygen species in mice lacking superoxide dismutase 2: attenuation via antioxidant treatment. J. Biol. Chem. 2006, 281:3354-3359.
39. Melov S., Doctrow S.R., Schneider J.A., Haberson J., Patel M., Coskun P.E., Huffman K., Wallace D.C., Malfroy B. Lifespan extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nullizygous mice treated with superoxide dismutase-catalase mimetics. J. Neurosci. 2001, 21:8348-8353.
40. Cuzzocrea S., Costantino G., Mazzon E., Zingarelli B., De Sarro A., Caputi A.P. Protective effects of Mn(III)tetrakis (4-benzoic acid) porphyrin (MnTBAP), a superoxide dismutase mimetic, in paw oedema induced by carrageenan in the rat. Biochem. Pharmacol. 1999, 58:171-176.
41. Sharma S.S., Gupta S. Neuroprotective effect of MnTMPyP, a superoxide dismutase/catalase mimetic in global cerebral ischemia is mediated through reduction of oxidative stress and DNA fragmentation. Eur. J. Pharmacol. 2007, 561:72-79.
42. Van Remmen H., et al. Multiple deficiencies in antioxidant enzymes in mice result in a compound increase in sensitivity to oxidative stress. Free Radic. Biol. Med. 2004, 36:1625-1634.
43. Blagosklonny M.V. Aging: ROS or TOR. Cell Cycle 2008, 7:3344-3354.
44. Perez V.I., Van Remmen H., Bokov A., Epstein C.J., Vijg J., Richardson A. The overexpression of major antioxidant enzymes does not extend the lifespan of mice. Aging Cell 2009, 8:73-75.
45. Muller F.L., Lustgarten M.S., Jang Y., Richardson A., Van Remmen H. Trends in oxidative aging theories. Free Radic. Biol. Med. 2007, 43:477-503.
46. Jang Y.C., Remmen V.H. The mitochondrial theory of aging: insight from transgenic and knockout mouse models. Exp. Gerontol. 2009, 44:256-260.
47. Chevallet M., Wagner E., Luche S., van Dorsselaer A., Leize-Wagner E., Rabilloud T. Regeneration of peroxiredoxins during recovery after oxidative stress: only some overoxidized peroxiredoxins can be reduced during recovery after oxidative stress. J. Biol. Chem. 2003, 278:37146-37153.
48. Chiribau C.B., Cheng L., Cucoranu I.C., Yu Y.S., Clempus R.E., Sorescu D. FOXO3A regulates peroxiredoxin III expression in human cardiac fibroblasts. J. Biol. Chem. 2008, 283:8211-8217.
49. Takada S., et al. Generation and characterization of cells that can be conditionally depleted of mitochondrial SOD2. Biochem. Biophys. Res. Commun. 2009, 379:233-238.
50. Kim A., Joseph S., Khan A., Epstein C.J., Sobel R., Huang T.T. Enhanced expression of mitochondrial superoxide dismutase leads to prolonged in vivo cell cycle progression and up-regulation of mitochondrial thioredoxin. Free Radic. Biol. Med. 2010, 48:1501-1512.
51. Kalen A.L., Sarsour E.H., Venkataraman S., Goswami P.C. Mn-superoxide dismutase overexpression enhances G2 accumulation and radioresistance in human oral squamous carcinoma cells. Antioxid. Redox Signaling 2006, 8:1273-1281.
52. Kannoji A., Phukan S., Sudher Babu V., Balaji V.N. GSK3beta: a master switch and a promising target. Expert Opin. Ther. Targets 2008, 12:1443-1455.
53. Moore M.N. Autophagy as a second level protective process in conferring resistance to environmentally-induced oxidative stress. Autophagy 2008, 4:254-256.
54. Vellai T., Bicsak B., Toth M.L., Takacs-Vellai K., Kovacs A.L. Regulation of cell growth by autophagy. Autophagy 2008, 4:507-509.
55. Scherz-Shouval R., Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 2007, 17:422-427.
56. Hidalgo C., Donoso P. Crosstalk between calcium and redox signaling: from molecular mechanisms to health implications. Antioxid. Redox Signaling 2008, 10:1275-1312.
57. Whitaker M. Calcium signalling in early embryos. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:1401-1418.
58. 2+ signaling. Am. J. Physiol. Cell Physiol. 2006, 291:C1082-C1088.
59. Gordeeva A.V., Zvyagilskaya R.A., Labas Y.A. Cross-talk between reactive oxygen species and calcium in living cells. Biochemistry (Moscow) 2003, 68:1077-1080.
60. Genestra M. Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell. Signal. 2007, 19:1807-1819.
61. Afanas'ev I.B. Signaling functions of free radicals superoxide & nitric oxide under physiological & pathological conditions. Mol. Biotechnol. 2007, 37:2-4.
62. Finkel T. Reactive oxygen species and signal transduction. IUBMB Life 2001, 52:3-6.
63. Wu A.L., Kim J.H., Zhang C., Unterman T.G., Chen J. Forkhead box protein O1 negatively regulates skeletal myocyte differentiation through degradation of mammalian target of rapamycin pathway components. Endocrinology 2008, 149:1407-1414.
64. Kamata H., Honda S., Maeda S., Chang L., Hirata H., Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005, 120:649-6461.
65. Pelaia G., et al. Effects of hydrogen peroxide on MAPK activation, IL-8 production and cell viability in primary cultures of human bronchial epithelial cells. J. Cell. Biochem. 2004, 93:142-152.