Sod1 loss induces intrinsic superoxide accumulation leading to p53-mediated growth arrest and apoptosis

International Journal of Molecular Sciences

Volumn 14, Issue 6, 2013, Pages 10998-11010

  Watanabe, Kenji ^a   Shibuya, Shuichi ^a   Koyama, Hirofumi ^a   Ozawa, Yusuke ^a   Toda, Toshihiko ^a   Yokote, Koutaro ^a   Shimizu, Takahiko ^a  

^a CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; p53; Reactive oxygen species; Superoxide dismutase; Vitamin C

Indexed keywords

ANTIOXIDANT; ASCORBIC ACID DERIVATIVE; ASCORBYL 2 PHOSPHATE 6 PALMITATE; COPPER ZINC SUPEROXIDE DISMUTASE; DNA; PROTEIN P53; SUPEROXIDE; UNCLASSIFIED DRUG; ASCORBIC ACID; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL CYCLE ARREST; CELL GROWTH; CELL PROLIFERATION; CELL STRAIN 3T3; CONTROLLED STUDY; CYTOPLASM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; ENZYME DEFICIENCY; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PROTEIN FUNCTION; SKIN ATROPHY; SKIN FIBROBLAST; UPREGULATION; ANIMAL; ATROPHY; CELL CULTURE; CELL CYCLE CHECKPOINT; CELL SURVIVAL; CYTOLOGY; DEFICIENCY; DERMIS; DRUG EFFECTS; FIBROBLAST; METABOLISM;

ANIMALS; APOPTOSIS; ASCORBIC ACID; ATROPHY; CELL CYCLE CHECKPOINTS; CELL SURVIVAL; CELLS, CULTURED; DERMIS; FIBROBLASTS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; PHENOTYPE; SUPEROXIDE DISMUTASE; SUPEROXIDES; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84878448319     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140610998     Document Type: Article

References (31)

1. Finkel, T.; Holbrook, N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408, 239-247.
2. Ditch, S.; Paull, T.T. The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 2012, 37, 15-22.
3. Kumari, U.; Jun, W.Y.; Bay, B.H.; Lyakhovich, A. Evidence of mitochondrial dysfunction and impaired ROS detoxifying machinery in Fanconi Anemia cells. Oncogene 2012, doi:10.1038/onc.2012.583.
4. Rufini, A.; Tucci, P.; Celardo, I.; Melino, G. Senescence and aging: The critical roles of p53. Oncogene 2013, doi:10.1038/onc.2012.640.
5. Okado-Matsumoto, A.; Fridovich, I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J. Biol. Chem. 2001, 276, 38388-38393.
6. Imamura, Y.; Noda, S.; Hashizume, K.; Shinoda, K.; Yamaguchi, M.; Uchiyama, S.; Shimizu, T.; Mizushima, Y.; Shirasawa, T.; Tsubota, K. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: A model of age-related macular degeneration. Proc. Natl. Acad. Sci. USA 2006, 103, 11282-11287.
7. Uchiyama, S.; Shimizu, T.; Shirasawa, T. CuZn-SOD deficiency causes ApoB degradation and induces hepatic lipid accumulation by impaired lipoprotein secretion in mice. J. Biol. Chem. 2006, 281, 31713-31719.
8. Murakami, K.; Inagaki, J.; Saito, M.; Ikeda, Y.; Tsuda, C.; Noda, Y.; Kawakami, S.; Shirasawa, T.; Shimizu, T. Skin atrophy in cytoplasmic SOD-deficient mice and its complete recovery using a vitamin C derivative. Biochem. Biophys. Res. Commun. 2009, 382, 457-461.
9. Nojiri, H.; Saita, Y.; Morikawa, D.; Kobayashi, K.; Tsuda, C.; Miyazaki, T.; Saito, M.; Marumo, K.; Yonezawa, I.; Kaneko, K.; et al. Cytoplasmic superoxide causes bone fragility owing to low-turnover osteoporosis and impaired collagen cross-linking. J. Bone Miner. Res. 2011, 26, 2682-2694.
10. Murakami, K.; Murata, N.; Noda, Y.; Tahara, S.; Kaneko, T.; Kinoshita, N.; Hatsuta, H.; Murayama, S.; Barnham, K.J.; Irie, K.; et al. SOD1 (copper/zinc superoxide dismutase) deficiency drives amyloid β protein oligomerization and memory loss in mouse model of Alzheimer disease. J. Biol. Chem. 2011, 286, 44557-44568.
11. Noda, Y.; Ota, K.; Shirasawa, T.; Shimizu, T. Copper/zinc superoxide dismutase insufficiency impairs progesterone secretion and fertility in female mice. Biol. Reprod. 2012, 86, 1-8.
12. Kojima, T.; Wakamatsu, T.H.; Dogru, M.; Ogawa, Y.; Igarashi, A.; Ibrahim, O.M.; Inaba, T.; Shimizu, T.; Noda, S.; Obata, H.; et al. Age-related dysfunction of the lacrimal gland and oxidative stress: Evidence from the Cu, Zn-superoxide dismutase-1 (Sod1) knockout mice. Am. J. Pathol. 2012, 180, 1879-1896.
13. 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.
14. Muller, F.L.; Song, W.; Liu, Y.; Chaudhuri, A.; Pieke-Dahl, S.; Strong, R.; Huang, T.T.; Epstein, C.J.; Roberts, L.J.; Csete, M.; 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.
15. Iuchi, Y.; Okada, F.; Onuma, K.; Onoda, T.; Asao, H.; Kobayashi, M.; Fujii, J. Elevated oxidative stress in erythrocytes due to a SOD1 deficiency causes anaemia and triggers autoantibody production. Biochem. J. 2007, 402, 219-227.
16. 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.
17. Brenner, C.; Moulin, M. Physiological roles of the permeability transition pore. Circ. Res. 2012, 111, 1237-1247.
18. Vurusaner, B.; Poli, G.; Basaga, H. Tumor suppressor genes and ROS: Complex networks of interactions. Free Radic. Biol. Med. 2012, 52, 7-18.
19. Shibuya, S.; Kinoshita, K.; Shimizu, T. Handbook of Diet, Nutrition and the Skin, 2nd ed.; Wageningen Academic Publishers: Wageningen, The Netherlands, 2012; pp. 351-366.
20. Muller, F.L.; Liu, Y.; van Remmen, H. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 2004, 279, 49064-49073.
21. Jang, Y.C.; Liu, Y.; Hayworth, C.R.; Bhattacharya, A.; Lustgarten, M.S.; Muller, F.L.; Chaudhuri, A.; Qi, W.; Li, Y.; Huang, J.Y.; et al. Dietary restriction attenuates age-associated muscle atrophy by lowering oxidative stress in mice even in complete absence of CuZnSOD. Aging Cell 2012, 11, 770-782.
22. Kruse, J.P.; Gu, W. Modes of p53 regulation. Cell 2009, 137, 609-622.
23. Gajjar, M.; Candeias, M.M.; Malbert-Colas, L.; Mazars, A.; Fujita, J.; Olivares-Illana, V.; Fåhraeus, R. The p53 mRNA-Mdm2 interaction controls Mdm2 nuclear trafficking and is required for p53 activation following DNA damage. Cancer Cell 2012, 21, 25-35.
24. Hamard, P.J.; Manfredi, J.J. Mdm2's dilemma: To degrade or to translate p53? Cancer Cell 2012, 21, 3-5.
25. Mbaya, E.; Oulès, B.; Caspersen, C.; Tacine, R.; Massinet, H.; Pennuto, M.; Chrétien, D.; Munnich, A.; Rötig, A.; Rizzuto, R.; et al. Calcium signalling-dependent mitochondrial dysfunction and bioenergetics regulation in respiratory chain Complex II deficiency. Cell Death Differ. 2010, 17, 1855-1866.
26. Jiang, P.; Du, W.; Mancuso, A.; Wellen, K.E.; Yang, X. Reciprocal regulation of p53 and malic enzymes modulates metabolism and senescence. Nature 2013, 493, 689-693.
27. Tyner, S.D.; Venkatachalam, S.; Choi, J.; Jones, S.; Ghebranious, N.; Igelmann, H.; Lu, X.; Soron, G.; Cooper, B.; Brayton, C.; et al. p53 mutant mice that display early ageing-associated phenotypes. Nature 2002, 415, 45-53.
28. Gannon, H.S.; Donehower, L.A.; Lyle, S.; Jones, S.N. Mdm2-p53 signaling regulates epidermal stem cell senescence and premature aging phenotypes in mouse skin. Dev. Biol. 2011, 353, 1-9.
29. Peterkofsky, B. Ascorbate requirement for hydroxylation and secretion of procollagen: Relationship to inhibition of collagen synthesis in scurvy. Am. J. Clin. Nutr. 1991, 54, S1135-S1140.
30. Murakami, K.; Murata, N; Ozawa, Y.; Kinoshita, N.; Irie, K.; Shirasawa, T.; Shimizu, T. Vitamin C restores behavioral deficits and amyloid-β oligomerization without affecting plaque formation in a mouse model of Alzheimer's disease. J. Alzheimers Dis. 2011, 26, 7-18.
31. Kalyanaraman, B.; Darley-Usmar, V.; Davies, K.J.; Dennery, P.A.; Forman, H.J.; Grisham, M.B.; Mann, G.E.; Moore, K.; Roberts, L.J.; Ischiropoulos, H. Measuring reactive oxygen and nitrogen species with fluorescent probes: Challenges and limitations. Free Radic. Biol. Med. 2012, 52, 1-6.