Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
권호 표지

Immunohistochemical identification and quantitative analysis of cytoplasmic Cu/Zn superoxide dismutase in mouse organogenesis

Yon, Jung-Min;Baek, In-Jeoung;Lee, Se-Ra;Kim, Mi-Ra;Lee, Beom-Jun;Yun, Young-Won;Nam, Sang-Yoon

  • Published : 20080900
⟨ Previous Next ⟩

Abstract

Cytoplasmic Cu/Zn superoxide dismutase (SOD1) is an antioxidant enzyme that converts superoxide to hydrogen peroxide in cells. Its spatial distribution matches that of superoxide production, allowing it to protect cells from oxidative stress. SOD1 deficiencies result in embryonic lethality and a wide range of pathologies in mice, but little is known about normal SOD1 protein expression in developing embryos. In this study, the expression pattern of SOD1 was investigated in post-implantation mouse embryos and extraembryonic tissues, including placenta, using Western blotting and immunohistochemical analyses. SOD1 was detected in embryos and extraembryonic tissues from embryonic day (ED) 8.5 to 18.5. The signal in embryos was observed at the lowest level on ED 9.5-11.5, and the highest level on ED 17.5-18.5, while levels remained constant in the surrounding extraembryonic tissues during all developmental stages examined. Immunohistochemical analysis of SOD1 expression on ED 13.5-18.5 revealed its ubiquitous distribution throughout developing organs. In particular, high levels of SOD1 expression were observed in the ependymal epithelium of the choroid plexus, ganglia, sensory cells of the olfactory and vestibulocochlear epithelia, blood cells and vessels, hepatocytes and hematopoietic cells of the liver, lymph nodes, osteogenic tissues, and skin. Thus, SOD1 is highly expressed at late stages of embryonic development in a cell- and tissue-specific manner, and can function as an important antioxidant enzyme during organogenesis in mouse embryos.

Keywords

References

  1. Barkats M, Horellou P, Colin P, Millecamps S, Faucon-Biguet N, Mallet J. 1-Methyl-4-phenylpyridinium neurotoxicity is attenuated by adenoviral gene transfer of human Cu/Zn superoxide dismutase. J Neurosci Res 2006, 83, 233-242 https://doi.org/10.1002/jnr.20696
  2. Chen EY, Fujinaga M, Giaccia AJ. Hypoxic microenvironment within an embryo induces apoptosis and is essential for proper morphological development. Teratology 1999, 60, 215-225 https://doi.org/10.1002/(SICI)1096-9926(199910)60:4<215::AID-TERA6>3.0.CO;2-2
  3. Chen SY, Sulik KK. Free radicals and ethanol-induced cytotoxicity in neural crest cells. Alcohol Clin Exp Res 1996, 20, 1071-1076 https://doi.org/10.1111/j.1530-0277.1996.tb01948.x
  4. Crapo JD, Oury T, Rabouille C, Slot JW, Chang LY. Copper,zinc superoxide dismutase is primarily a cytosolic protein in human cells. Proc Natl Acad Sci USA 1992, 89, 10405-10409
  5. Cuzzocrea S, Mazzon E, Paola RD, Genovese T, Muià C, Caputi AP, Salvemini D. Effects of combination M40403 and dexamethasone therapy on joint disease in a rat model of collagen-induced arthritis. Arthritis Rheum 2005, 52, 1929-1940 https://doi.org/10.1002/art.21044
  6. Dennery PA. Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today 2007, 81, 155-162 https://doi.org/10.1002/bdrc.20098
  7. Didion SP, Ryan MJ, Didion LA, Fegan PE, Sigmund CD, Faraci FM. Increased superoxide and vascular dysfunction in CuZnSOD-deficient mice. Circ Res 2002, 91, 938-944 https://doi.org/10.1161/01.RES.0000043280.65241.04
  8. Elchuri S, Oberley TD, Qi W, Eisenstein RS, Jackson Roberts L, Van Remmen H, Epstein CJ, Huang TT. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 2005, 24, 367-380 https://doi.org/10.1038/sj.onc.1208207
  9. Frederiks WM, Bosch KS. Localization of superoxide dismutase activity in rat tissues. Free Radic Biol Med 1997, 22, 241-248 https://doi.org/10.1016/S0891-5849(96)00328-0
  10. Hanson LA. Session 1: Feeding and infant development breast-feeding and immune function. Proc Nutr Soc 2007, 66, 384-396
  11. Ho YS, Gargano M, Cao J, Bronson RT, Heimler I, Hutz RJ. Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J Biol Chem 1998, 273, 7765-7769 https://doi.org/10.1074/jbc.273.13.7765
  12. 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 anemia and triggers autoantibody production. Biochem J 2007, 402, 219-227 https://doi.org/10.1042/BJ20061386
  13. Keithley EM, Canto C, Zheng QY, Wang X, Fischel-Ghodsian N, Johnson KR. Cu/Zn superoxide dismutase and age-related hearing loss. Hear Res 2005, 209, 76-85 https://doi.org/10.1016/j.heares.2005.06.009
  14. Khan JY, Black SM. Developmental changes in murine brain antioxidant enzymes. Pediatr Res 2003, 54, 77-82 https://doi.org/10.1203/01.PDR.0000065736.69214.20
  15. McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 1969, 244, 6049-6055
  16. McFadden SL, Ding D, Reaume AG, Flood DG, Salvi RJ. Age-related cochlear hair cell loss is enhanced in mice lacking copper/zinc superoxide dismutase. Neurobiol Aging 1999, 20, 1-8 https://doi.org/10.1016/S0197-4580(99)00018-4
  17. Muller FL, Song W, Liu Y, Chaudhuri A, Pieke-Dahl S, Strong R, Huang TT, Epstein CJ, Roberts LJ 2nd, Csete M, Faulkner JA, Van Remmen H. 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 https://doi.org/10.1016/j.freeradbiomed.2006.01.036
  18. Munim A, Asayama K, Dobashi K, Suzuki K, Kawaoi A, Kato K. Immunohistochemical localization of superoxide dismutases in fetal and neonatal rat tissues. J Histochem Cytochem 1992, 40, 1705-1713 https://doi.org/10.1177/40.11.1431059
  19. Ogawa T, Ohira A, Amemiya T. Manganese and copper-zinc superoxide dismutases in the developing rat retina. Acta Histochem 1997, 99, 1-12 https://doi.org/10.1016/S0065-1281(97)80002-5
  20. 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 https://doi.org/10.1074/jbc.M105395200
  21. Pardo CA, Xu Z, Borchelt DR, Price DL, Sisodia SS, Cleveland DW. Superoxide dismutase is an abundant component in cell bodies, dendrites, and axons of motor neurons and in a subset of other neurons. Proc Natl Acad Sci USA 1995, 92, 954-958
  22. Perez MJ, Cederbaum AI. Adenovirus-mediated expression of Cu/Zn- or Mn-superoxide dismutase protects against CYP2E1-dependent toxicity. Hepatology 2003, 38, 1146-1158 https://doi.org/10.1053/jhep.2003.50479
  23. Sha SH, Zajic G, Epstein CJ, Schacht J. Overexpression of copper/zinc-superoxide dismutase protects from kanamycininduced hearing loss. Audiol Neurootol 2001, 6, 117-123 https://doi.org/10.1159/000046818
  24. Shaw PJ, Ince PG, Falkous G, Mantle D. Oxidative damage to protein in sporadic motor neuron disease spinal cord. Ann Neurol 1995, 38, 691-695 https://doi.org/10.1002/ana.410380424
  25. Sheppard FR, Kelher MR, Moore EE, McLaughlin NJ, Banerjee A, Silliman CC. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J Leukoc Biol 2005, 78, 1025-1042 https://doi.org/10.1189/jlb.0804442
  26. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007, 39, 44-84 https://doi.org/10.1016/j.biocel.2006.07.001
  27. Wang Y, Walsh SW. Increased superoxide generation is associated with decreased superoxide dismutase activity and mRNA expression in placental trophoblast cells in preeclampsia. Placenta 2001, 22, 206-212 https://doi.org/10.1053/plac.2000.0608
  28. Weisiger RA, Fridovich I. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 1973, 248, 4793-4796
  29. Wentzel P, Eriksson UJ. Antioxidants diminish developmental damage induced by high glucose and cyclooxygenase inhibitors in rat embryos in vitro. Diabetes 1998, 47, 677-684 https://doi.org/10.2337/diabetes.47.4.677
  30. Yon JM, Baek IJ, Lee SR, Jin Y, Kim MR, Nahm SS, Kim JS, Ahn B, Lee BJ, Yun YW, Nam SY. The spatio-temporal expression pattern of cytoplasmic Cu/Zn superoxide dismutase (SOD1) mRNA during mouse embryogenesis. J Mol Histol 2008, 39, 95-103 https://doi.org/10.1007/s10735-007-9134-1