DOI QR코드

DOI QR Code

Enhancement of potency and stability of human extracellular superoxide dismutase

  • Kim, Sunghwan (Department of Dermatology, College of Medicine, The Catholic University of Korea) ;
  • Kim, Hae-Young (Department of Dermatology, College of Medicine, The Catholic University of Korea) ;
  • Kim, Jung-Ho (Department of Dermatology, College of Medicine, The Catholic University of Korea) ;
  • Choi, Jung-Hye (Department of Dermatology, College of Medicine, The Catholic University of Korea) ;
  • Ham, Won-Kook (Department of Dermatology, College of Medicine, The Catholic University of Korea) ;
  • Jeon, Yoon-Jae (Department of Dermatology, College of Medicine, The Catholic University of Korea) ;
  • Kang, Hara (Division of Life Science, College of Life Science and Bioengineering, Incheon National University) ;
  • Kim, Tae-Yoon (Department of Dermatology, College of Medicine, The Catholic University of Korea)
  • Received : 2014.05.02
  • Accepted : 2014.05.23
  • Published : 2015.02.28

Abstract

Cells express several antioxidant enzymes to scavenge reactive oxygen species (ROS) responsible for oxidative damages and various human diseases. Therefore, antioxidant enzymes are considered biomedicine candidates. Among them, extracellular superoxide dismutase (SOD3) had showed prominent efficacy against asthma and inflammation. Despite its advantages as a biomedicine, the difficulty in obtaining large quantity of active recombinant human SOD3 (rhSOD3) has limited its clinical applications. We found that a significant fraction of over-expressed rhSOD3 was composed of the inactive apo-enzyme and its potency against inflammation depended on the rate of metal incorporation. Also, purified rhSOD3 was unstable and lost its activity very quickly. Here, we suggest an ideal preparative method to express, purify, and store highly active rhSOD3. The enzymatic activity of rhSOD3 was maximized by incorporating metal ions into rhSOD3 after purification. Also, albumin or polyethylene glycol prevented rapid inactivation or degradation of rhSOD3 during preparative procedures and long-term storage.

Keywords

References

  1. Finkel T (2005) Radical medicine: treating ageing to cure disease. Nat Rev Mol Cell Biol 6, 971-976 https://doi.org/10.1038/nrm1763
  2. Rosanna DP and Salvatore C (2012) Reactive oxygen species, inflammation, and lung diseases. Curr Pharm Des 18, 3889-3900 https://doi.org/10.2174/138161212802083716
  3. Niwa Y (1989) Lipid peroxides and superoxide dismutase (SOD) induction in skin inflammatory diseases, and treatment with SOD preparations. Dermatologica 179 Suppl 1, 101-106 https://doi.org/10.1159/000248458
  4. Kim BH, Na KM, Oh I et al (2013) Kurarinone regulates immune responses through regulation of the JAK/STAT and TCR-mediated signaling pathways. Biochem Pharmacol 85, 1134-1144 https://doi.org/10.1016/j.bcp.2013.01.005
  5. Sunitha K, Hemshekhar M, Thushara RM et al (2013) N-Acetylcysteine amide: a derivative to fulfill the promises of N-Acetylcysteine. Free Radic Res 47, 357-367 https://doi.org/10.3109/10715762.2013.781595
  6. Traber MG and Stevens JF (2011) Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med 51, 1000-1013 https://doi.org/10.1016/j.freeradbiomed.2011.05.017
  7. Yamakura F and Kawasaki H (2010) Post-translational modifications of superoxide dismutase. Biochim Biophys Acta 1804, 318-325 https://doi.org/10.1016/j.bbapap.2009.10.010
  8. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64, 97-112 https://doi.org/10.1146/annurev.bi.64.070195.000525
  9. Zelko IN, Mariani TJ and Folz RJ (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 33, 337-349 https://doi.org/10.1016/S0891-5849(02)00905-X
  10. Lee YS, Cheon IS, Kim BH, Kwon MJ, Lee HW and Kim TY (2013) Loss of Extracellular Superoxide Dismutase Induces Severe IL-23-Mediated Skin Inflammation in Mice. J Invest Dermatol 133, 732-741 https://doi.org/10.1038/jid.2012.406
  11. Asikainen TM, Huang TT, Taskinen E et al (2002) Increased sensitivity of homozygous Sod2 mutant mice to oxygen toxicity. Free Radic Biol Med 32, 175-186 https://doi.org/10.1016/S0891-5849(01)00776-6
  12. Kwon MJ, Jeon YJ, Lee KY and Kim TY (2012) Superoxide dismutase 3 controls adaptive immune responses and contributes to the inhibition of ovalbumin-induced allergic airway inflammation in mice. Antioxid Redox Signal 17, 1376-1392 https://doi.org/10.1089/ars.2012.4572
  13. Kwon MJ, Han J, Kim BH, Lee YS and Kim TY (2012) Superoxide dismutase 3 suppresses hyaluronic acid fragments mediated skin inflammation by inhibition of toll-like receptor 4 signaling pathway: superoxide dismutase 3 inhibits reactive oxygen species-induced trafficking of toll-like receptor 4 to lipid rafts. Antioxid Redox Signal 16, 297-313 https://doi.org/10.1089/ars.2011.4066
  14. Tominaga T, Hachiya M, Shibata T, Sakamoto Y, Taki K and Akashi M (2012) Exogenously-added copper/zinc superoxide dismutase rescues damage of endothelial cells from lethal irradiation. J Clin Biochem Nutr 50, 78-83 https://doi.org/10.3164/jcbn.11-15
  15. Kim DW, Hwang HS, Kim DS et al (2011) Effect of silk fibroin peptide derived from silkworm Bombyx mori on the anti-inflammatory effect of Tat-SOD in a mice edema model. BMB Rep 44, 787-792 https://doi.org/10.5483/BMBRep.2011.44.12.787
  16. Na K, Kim KE, Park ST and Kim, T. Y. (2007) EC-SOD suppresses contact hypersensitivity in mouse skin by impairing Langerhans cell migration. J Invest Dermatol 127, 1930-1937 https://doi.org/10.1038/sj.jid.5700802
  17. Kim Y, Kim BH, Lee H et al (2011) Regulation of skin inflammation and angiogenesis by EC-SOD via HIF-1alpha and NF-kappaB pathways. Free Radic Biol Med 51, 1985-1995 https://doi.org/10.1016/j.freeradbiomed.2011.08.027
  18. Jaarsma D, Haasdijk ED, Grashorn JA et al (2000) Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis 7, 623-643 https://doi.org/10.1006/nbdi.2000.0299
  19. Uematsu T, Nagashima S, Umemura K, Kanamaru M and Nakashima M (1994) Pharmacokinetics and safety of intravenous recombinant human superoxide dismutase (NK341) in healthy subjects. Int J Clin Pharmacol Ther 32, 638-641
  20. Karlsson K, Sandstrom J, Edlund A, Edlund T and Marklund SL (1993) Pharmacokinetics of extracellular-superoxide dismutase in the vascular system. Free Radic Biol Med 14, 185-190 https://doi.org/10.1016/0891-5849(93)90009-J
  21. Bowler RP, Nicks M, Olsen DA et al (2002) Furin proteolytically processes the heparin-binding region of extracellular superoxide dismutase. J Biol Chem 277, 16505-16511 https://doi.org/10.1074/jbc.M105409200
  22. Enghild JJ, Thogersen IB, Oury TD, Valnickova Z, Hojrup P and Crapo JD (1999) The heparin-binding domain of extracellular superoxide dismutase is proteolytically processed intracellularly during biosynthesis. J Biol Chem 274, 14818-14822 https://doi.org/10.1074/jbc.274.21.14818
  23. Petersen SV, Thogersen IB, Valnickova Z et al (2010) The concentration of extracellular superoxide dismutase in plasma is maintained by LRP-mediated endocytosis. Free Radic Biol Med 49, 894-899 https://doi.org/10.1016/j.freeradbiomed.2010.06.019
  24. Jeney V, Itoh S, Wendt M et al (2005) Role of antioxidant-1 in extracellular superoxide dismutase function and expression. Circ Res 96, 723-729 https://doi.org/10.1161/01.RES.0000162001.57896.66
  25. Ahl IM, Lindberg MJ and Tibell LA (2004) Coexpression of yeast copper chaperone (yCCS) and CuZn-superoxide dismutases in Escherichia coli yields protein with high copper contents. Protein Expr Purif 37, 311-319 https://doi.org/10.1016/j.pep.2004.06.006
  26. Kim JI, Jang HS and Park KM (2010) Endotoxin-induced renal tolerance against ischemia and reperfusion injury is removed by iNOS, but not eNOS, gene-deletion. BMB Rep 43, 629-634 https://doi.org/10.5483/BMBRep.2010.43.9.629
  27. Adachi T, Ohta H, Hayashi K, Hirano K and Marklund SL (1992) The site of nonenzymic glycation of human extracellular-superoxide dismutase in vitro. Free Radic Biol Med 13, 205-210 https://doi.org/10.1016/0891-5849(92)90016-A
  28. Arai K, Maguchi S, Fujii S, Ishibashi H, Oikawa K and Taniguchi N (1987) Glycation and inactivation of human Cu-Zn-superoxide dismutase. Identification of the in vitro glycated sites. J Biol Chem 262, 16969-16972
  29. Petersen SV, Olsen DA, Kenney JM et al (2005) The high concentration of Arg213-->Gly extracellular superoxide dismutase (EC-SOD) in plasma is caused by a reduction of both heparin and collagen affinities. Biochem J 385, 427-432 https://doi.org/10.1042/BJ20041218
  30. Petersen SV, Oury TD, Valnickova Z et al (2003) The dual nature of human extracellular superoxide dismutase: one sequence and two structures. Proc Natl Acad Sci U S A 100, 13875-13880 https://doi.org/10.1073/pnas.2436143100
  31. Tibell L, Hjalmarsson K, Edlund T, Skogman G, Engstrom A and Marklund SL (1987) Expression of human extracellular superoxide dismutase in Chinese hamster ovary cells and characterization of the product. Proc Natl Acad Sci U S A 84, 6634-6638 https://doi.org/10.1073/pnas.84.19.6634
  32. Son YJ, Bae JY, Chong SH et al (2010) Expression, high cell density culture and purification of recombinant EC-SOD in Escherichia coli. Appl Biochem Biotechnol 162, 1585-1598 https://doi.org/10.1007/s12010-010-8940-1
  33. Chen HL, Yen CC, Tsai TC et al (2006) Production and characterization of human extracellular superoxide dismutase in the methylotrophic yeast Pichia pastoris. J Agric Food Chem 54, 8041-8047 https://doi.org/10.1021/jf061379x
  34. Bae JY, Koo BK, Ryu HB et al (2013) Cu/Zn incorporation during purification of soluble human EC-SOD from E. coli stabilizes proper disulfide bond formation. Appl Biochem Biotechnol 169, 1633-1647 https://doi.org/10.1007/s12010-012-0025-x

Cited by

  1. Protective effect of α-mangostin against iodixanol-induced apoptotic damage in LLC-PK1 cells vol.26, pp.15, 2016, https://doi.org/10.1016/j.bmcl.2016.05.031
  2. N-Adamantyl-4-Methylthiazol-2-Amine Attenuates Glutamate-Induced Oxidative Stress and Inflammation in the Brain vol.32, pp.1, 2017, https://doi.org/10.1007/s12640-017-9717-x
  3. Extracellular reactive oxygen species are generated by a plasma membrane oxidative phosphorylation system vol.112, 2017, https://doi.org/10.1016/j.freeradbiomed.2017.08.016
  4. Extracellular superoxide dismutase ameliorates house dust mite-induced atopic dermatitis-like skin inflammation and inhibits mast cell activation in mice vol.25, pp.8, 2016, https://doi.org/10.1111/exd.13028
  5. Inhibitory effects of superoxide dismutase 3 on Propionibacterium acnes-induced skin inflammation vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-22132-z