Elevated oxidative stress in erythrocytes due to a SOD1 deficiency causes anaemia and triggers autoantibody production

Biochemical Journal

Volumn 402, Issue 2, 2007, Pages 219-227

  Iuchi, Yoshihito ^a   Okada, Futoshi ^a   Onuma, Kunishige ^a   Onoda, Tadashi ^b   Asao, Hironobu ^b   Kobayashi, Masanobu ^c   Fujii, Junichi ^a  

^a YAMAGATA UNIVERSITY   (Japan)

^b YAMAGATA UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Anaemia; Autoantibody; Carbonic anhydrase; Oxidative stress; SOD1 deficiency

Indexed keywords

ANTIBODIES; DISEASES; LIPIDS; OXIDATION; OXIDATIVE STRESS; PROTEINS;

ANAEMIA; AUTOANTIBODY; CARBONIC ANHYDRASE; SOD1 DEFICIENCY;

CYTOLOGY;

ACETYLCYSTEINE; ANTIOXIDANT; AUTOANTIBODY; COPPER ZINC SUPEROXIDE DISMUTASE; IMMUNOGLOBULIN G; SUPEROXIDE DISMUTASE;

ANEMIA; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; ENZYME DEFICIENCY; ERYTHROCYTE; ERYTHROPOIESIS; FLOW CYTOMETRY; IMMUNOBLOTTING; LIPID PEROXIDATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; SUPEROXIDE DISMUTASE 1 DEFICIENCY; ANIMAL; BIOSYNTHESIS; DRUG EFFECT; ENZYMOLOGY; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOUSE MUTANT; OXIDATION REDUCTION REACTION; PATHOLOGY;

MUS;

ACETYLCYSTEINE; ANEMIA; ANIMALS; ANTIOXIDANTS; AUTOANTIBODIES; ERYTHROCYTES; INFLAMMATION; MICE; MICE, KNOCKOUT; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHENOTYPE; SUPEROXIDE DISMUTASE;

EID: 33847757480     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061386     Document Type: Article

References (43)

1. Fridovich, I. (1995) Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 64, 97-112
2. Frank, S., Stallmeyer, B., Kampfer, H., Kolb, N. and Pfeilschifter, J. (1999) Nitric oxide triggers enhanced induction of vascular endothelial growth factor expression in cultured keratinocytes (HaCaT) and during cutaneous wound repair. FASEB J. 13, 2002-2014
3. Frank, S., Kampfer, H., Podda, M., Kaufmann, R. and Pfeilschifter, J. (2000) Identification of copper/zinc superoxide dismutase as a nitric oxide-regulated gene in human (HaCaT) keratinocytes: implications for keratinocyte proliferation. Biochem. J. 346, 719-728
4. Wong, G. H. and Goeddel, D. V. (1988) Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science 242, 941-944
5. Visner, G. A., Dougall, W. C., Wilson, J. M., Burr, I. A. and Nick, H. S. (1990) Regulation of manganese superoxide dismutase by lipopolysaccharide, interleukin-1, and tumor necrosis factor. Role in the acute inflammatory response. J. Biol. Chem. 265, 2856-2864
6. Okado-Matsumoto, A. and Fridovich, I. (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu.Zn-SOD in mitochondria. J. Biol. Chem. 276, 38388-38393
7. Valentine, J. S., Doucette, P. A. and Potter, S. Z. (2005) Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu. Rev. Biochem. 74, 563-593
8. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J. P., Deng, H. X. et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62
9. Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H. X. et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775
10. Wong, P. C., Pardo, C. A., Borchelt, D. R., Lee, M. K., Copeland, N. G., Jenkins, N. A., Sisodia, S. S., Cleveland, D. W. and Price, D. L. (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14, 1105-1116
11. Reaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J., Siwek, D. F., Wilcox, H. M., Flood, D. G., Beal, M. F., Brown, Jr, R. H. et al. (1996) Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 3, 43-47
12. Ho, Y. S., Gargano, M., Cao, J., Bronson, R. T., Heimler, I. and Hutz, R. J. (1998) Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J. Biol. Chem. 273, 7765-7769
13. Matzuk, M. M., Dionne, L., Guo, Q., Kumar, T. R. and Lebovitz, R. M. (1998) Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 139, 4008-4011
14. McFadden, S. L., Ding, D., Reaume, A. G., Flood, D. G. and Salvi, R. J. (1999) Age-related cochlear hair cell loss is enhanced in mice lacking copper/zinc superoxide dismutase. Neurobiol. Aging 20, 1-8
15. Didion, S. P., Ryan, M. J., Didion, L. A., Fegan, P. E., Sigmund, C. D. and Faraci, F. M. (2002) Increased superoxide and vascular dysfunction in CuZnSOD-deficient mice. Circ. Res. 91, 938-944
16. Li, Y., Huang, T. T., Carlson, E. J., Melov, S., Ursell, P. C., Olson, J. L., Noble, L. J., Yoshimura, M. P., Berger, C., Chan, P. H. et al. (1995) Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11, 376-381
17. Shefner, J. M., Reaume, A. G., Flood, D. G., Scott, R. W., Kowall, N. W., Ferrante, R. J., Siwek, D. F., Upton-Rice, M. and Brown, Jr, R. H. (1999) Mice lacking cytosolic copper/zinc superoxide dismutase display a distinctive motor axonopathy. Neurology 53, 1239-1246
18. Yoshida, T., Maulik, N., Engelman, R. M., Ho, Y. S. and Das, D. K. (2000) Targeted disruption of the mouse Sod I gene makes the hearts vulnerable to ischemic reperfusion injury. Circ. Res. 86, 264-269
19. Ishii, T., Matsuki, S., Iuchi, Y., Okada, F., Toyosaki, S., Tomita, Y., Ikeda, Y. and Fujii, J. (2005) Accelerated impairment of spermatogenic cells in sod1-knockout mice under heat stress. Free Radical Res. 39, 697-705
20. Elchuri, S., Oberley, T. D., Qi, W., Eisenstein, R. S., Jackson Roberts, L., Van Remmen, H., Epstein, C. J. and Huang, T. T. (2005) CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24, 367-380
21. Busuttil, R. A., Garcia, A. M., Cabrera, C., Rodriguez, A., Suh, Y., Kim, W. H., Huang, T. T. and Vijg, J. (2005) Organ-specific increase in mutation accumulation and apoptosis rate in CuZn-superoxide dismutase-deficient mice. Cancer Res. 65, 11271-11275
22. Friedman, J. S., Lopez, M. F., Fleming, M. D., Rivera, A., Martin, F. M., Welsh, M. L., Boyd, A., Doctrow, S. R. and Burakoff, S. J. (2004) SOD2-deficiency anemia: protein oxidation and altered protein expression reveal targets of damage, stress response, and antioxidant responsiveness. Blood 104, 2565-2573
23. Lee, J. M., Chan, K., Kan, Y. W. and Johnson, J. A. (2001) Targeted disruption of Nrf2 causes regenerative immune-mediated hemolytic anemia. Proc. Natl. Acad. Sci. U.S.A. 101, 9751-9756
24. Otsu, K., Ikeda, Y. and Fujii, J. (2004) Accumulation of manganese superoxide dismutase under metal-depleted conditions: proposed role for zinc ions in cellular redox balance. Biochem. J. 377, 241-248
25. Fujii, T., Endo, T., Fujii, J. and Taniguchi, N. (2002) Differential expression of glutathione reductase and cytosolic glutathione peroxidase, GPX1, in developing rat lungs and kidneys. Free Radical Res. 36, 1041-1049
26. Kayanoki, Y., Fujii, J., Suzuki, K., Kawata, S., Matsuzawa, Y. and Taniguchi, N. (1994) Suppression of antioxidative enzyme expression by transforming growth factor-β1 in rat hepatocytes. J. Biol. Chem. 269, 15488-15492
27. Okado-Matsumoto, A., Matsumoto, A., Fujii, J. and Taniguchi, N. (2000) Peroxiredoxin IV is a secretable protein with heparin-binding properties under reduced conditions. J. Biochem. 127, 493-501
28. Bosman, G. J., Willekens, F. L. and Werre, J. M. (2005) Erythrocyte aging: a more than superficial resemblance to apoptosis? Cell. Physiol. Biochem. 16, 1-8
29. Kelly, G. S. (1998) Clinical applications of N-acetylcysteine. Altern. Med. Rev. 3, 114-127
30. Friedman, J. S., Rebel, V. I., Derby, R., Bell, K., Huang, T. T., Kuypers, F. A., Epstein, C. J. and Burakoff, S. J. (2001) Absence of mitochondrial superoxide dismutase results in a murine hemolytic anemia responsive to therapy with a catalytic antioxidant. J. Exp. Med. 193, 925-934
31. Neumann, C. A., Krause, D. S., Carman, C. V., Das, S., Dubey, D. P., Abraham, J. L., Bronson, R. T., Fujiwara, Y., Orkin, S. H. and Van Etten, R. A. (2003) Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424, 561-565
32. Lee, T. H., Kim, S. U., Yu, S. L., Kim, S. H., Park, Do, S., Moon, H. B., Dho, S. H., Kwon, K. S., Kwon, H. J., Han, Y. H. et al. (2003) Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood 101, 5033-5038
33. Skrzydlewska, E. and Farbiszewski, R. (1997) Glutathione consumption and inactivation of glutathione-related enzymes in liver, erythrocytes and serum of rats after methanol intoxication. Arch. Toxicol. 71, 741-745
34. Asahi, M., Fujii, J., Takao, T., Kuzuya, T., Hori, M., Shimonishi, Y. and Taniguchi, N. (1997) The oxidation of selenocysteine is involved in the inactivation of glutathione peroxidase by nitric oxide donor. J. Biol. Chem. 272, 19152-19157
35. Fagan, J. M. and Waxman, L. (1991) Purification of a protease in red blood cells that degrades oxidatively damaged haemoglobin. Biochem. J. 277, 779-786
36. Fujino, T., Ando, K., Beppu, M. and Kikugawa, K. (2000) Enzymatic removal of oxidized protein aggregates from erythrocyte membranes. J. Biochem. 127, 1081-1086
37. Inagaki, Y., Jinno-Yoshida, Y., Hamasaki, Y. and Ueki, H. (1991) A novel autoantibody reactive with carbonic anhydrase in sera from patients with systemic lupus erythematosus and Sjogren's syndrome. J. Dermatol. Sci. 2, 147-154
38. Nishimori, I., Bratanova, T., Toshkov, I., Caffrey, T., Mogaki, M., Shibata, Y. and Hollingsworth, M. A. (1995) Induction of experimental autoimmune sialoadenitis by immunization of PL/J mice with carbonic anhydrase II. J. Immunol. 154, 4865-4873
39. Beppu, M., Mizukami, A., Nagoya, M. and Kikugawa, K. (1990) Binding of anti-band 3 autoantibody to oxidatively damaged erythrocytes. Formation of senescent antigen on erythrocyte surface by an oxidative mechanism. J. Biol. Chem. 265, 3226-3233
40. Shen, C. R., Youssef, A. R., Devine, A., Bowie, L., Hall, A. M., Wraith, D. C., Elson, C. J. and Barker, R. N. (2003) Peptides containing a dominant T-cell epitope from red cell band 3 have in vivo immunomodulatory properties in NZB mice with autoimmune hemolytic anemia. Blood 102, 3800-3806
41. Akagawa, M., Ito, S., Toyoda, K., Ishii, Y., Tatsuda, E., Shibata, T., Yamaguchi, S., Kawai, Y., Ishino, K., Kishi, Y. et al. (2006) Bispecific abs against modified protein and DNA with oxidized lipids. Proc. Natl. Acad. Sci. U.S.A. 103, 6160-6165
42. Signorini, C., Ferrali, M., Ciccoli, L., Sugherini, L., Magnani, A. and Comporti, M. (1995) Iron release, membrane protein oxidation and erythrocyte ageing. FEBS Lett. 362, 165-170
43. Whitacre, C. C. (2001) Sex differences in autoimmune disease. Nat. Immunol. 2, 777-780