28
Views
0
CrossRef citations to date
0
Altmetric
Special Reports

Extracellular superoxide dismutase for the treatment of inflammatory skin diseases

&
Pages 609-616 | Published online: 10 Jan 2014

References

  • Cotran RS, Kumar V, Collins T, Robbins SL. Robbins Pathologic Basis of Disease. Saunders, Philadelphia, PA, USA (1999).
  • Cork MJ, Robinson DA, Vasilopoulos Y et al. New perspectives on epidermal barrier dysfunction in atopic dermatitis: gene-environment interactions. J. Allergy Clin. Immunol. 118(1), 3–21, quiz 22–23 (2006).
  • Homey B, Alenius H, Muller A et al. CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat. Med. 8(2), 157–165 (2002).
  • Leung DY, Bieber T. Atopic dermatitis. Lancet 361(9352), 151–160 (2003).
  • Stamatas GN, Morello AP 3rd, Mays DA. Early Inflammatory Processes in the Skin. Curr. Mol. Med. 2013, 27 (2013).
  • Campbell JJ, Butcher EC. Chemokines in tissue-specific and microenvironment-specific lymphocyte homing. Curr. opin. immunol. 12(3), 336–341 (2000).
  • Reiss Y, Proudfoot AE, Power CA, Campbell JJ, Butcher EC.. CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J. Exp. Med. 194(10), 1541–1547 (2001).
  • Pierard-Franchimont C, Pierard GE. [Etanercept (Enbrel) for the treatment of moderate to severe plaque type psoriasis]. Rev. Med. Liege 61(3), 201–205 (2006).
  • Martin P, Gomez M, Lamana A et al. The leukocyte activation antigen CD69 limits allergic asthma and skin contact hypersensitivity. J. Allergy Clin. Immunol. 126(2), 355–365, 365, e351–353 (2010).
  • Peiser M. Role of Th17 cells in skin inflammation of allergic contact dermatits. Clin. Dev. Immunol. 2013, 261037 (2013).
  • Elias PM, Arbiser J, Brown BE et al. Epidermal vascular endothelial growth factor production is required for permeability barrier homeostasis, dermal angiogenesis, and the development of epidermal hyperplasia: implications for the pathogenesis of psoriasis. Am. J. Pathol. 173(3), 689–699 (2008).
  • Heidenreich R, Rocken M, Ghoreschi K. Angiogenesis drives psoriasis pathogenesis. Int. J. Exp. Pathol. 90(3), 232–248 (2009).
  • Campanati A, Goteri G, Simonetti O et al. Angiogenesis in psoriatic skin and its modifications after administration of etanercept: videocapillaroscopic, histological and immunohistochemical evaluation. Int. J. Immunopathol. Pharmacol. 22(2), 371–377 (2009).
  • Costa C, Incio J, Soares R. Angiogenesis and chronic inflammation: cause or consequence? Angiogenesis 10(3), 149–166 (2007).
  • Mor F, Quintana FJ, Cohen IR. Angiogenesis-inflammation cross-talk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. J. Immunol. 172(7), 4618–4623 (2004).
  • Schonthaler HB, Huggenberger R, Wculek SK, Detmar M, Wagner EF. Systemic anti-VEGF treatment strongly reduces skin inflammation in a mouse model of psoriasis. Proc. Natl Acad. Sci. USA 106(50), 21264–21269 (2009).
  • Canavese M, Altruda F, Ruzicka T, Schauber J. Vascular endothelial growth factor (VEGF) in the pathogenesis of psoriasis--a possible target for novel therapies? J. Dermatol. Sci. 58(3), 171–176 (2010).
  • Halin C, Fahrngruber H, Meingassner JG et al. Inhibition of chronic and acute skin inflammation by treatment with a vascular endothelial growth factor receptor tyrosine kinase inhibitor. Am. J. Pathol. 173(1), 265–277 (2008).
  • Barnes PJ, Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 336(15), 1066–1071 (1997).
  • Szabo C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6(8), 662–680 (2007).
  • Ferretti G, Bacchetti T, Campanati A, Simonetti O, Liberati G, Offidani A. Correlation between lipoprotein(a) and lipid peroxidation in psoriasis: role of the enzyme paraoxonase-1. Br. J. Dermatol. 166(1), 204–207 (2012).
  • Filipe P, Morliere P, Silva JN et al. Plasma lipoproteins as mediators of the oxidative stress induced by UV light in human skin: a review of biochemical and biophysical studies on mechanisms of apolipoprotein alteration, lipid peroxidation, and associated skin cell responses. Oxid. Med. Cell. Longev. 2013, 285825 (2013).
  • Tekin NS, Tekin IO, Barut F, Sipahi EY. Accumulation of oxidized low-density lipoprotein in psoriatic skin and changes of plasma lipid levels in psoriatic patients. Mediators Inflamm. 2007, 78454 (2007).
  • 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 120(5), 649–661 (2005).
  • Naik E, Dixit VM. Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J. Exp. Med. 208(3), 417–420 (2011).
  • Bulua AC, Simon A, Maddipati R et al. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J. Exp. Med. 208(3), 519–533 (2011).
  • Nakahira K, Haspel JA, Rathinam VA et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12(3), 222–230 (2011).
  • Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 469(7329), 221–225 (2011).
  • Niwa Y. Lipid peroxides and superoxide dismutase (SOD) induction in skin inflammatory diseases, and treatment with SOD preparations. Dermatologica 179(Suppl. 1), 101–106 (1989).
  • Kim Y, Kim BH, Lee H et al. Regulation of skin inflammation and angiogenesis by EC-SOD via HIF-1alpha and NF-kappaB pathways. Free Radic. Biol. Med. 51(11), 1985–1995 (2012).
  • Kwon MJ, Han J, Kim BH, Lee YS, Kim TY. 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(4), 297–313 (2012).
  • Kim BH, Na KM, Oh I et al. Kurarinone regulates immune responses through regulation of the JAK/STAT and TCR-mediated signaling pathways. Biochem. Pharmacol. 85(8), 1134–1144 (2013).
  • Hayashi D, Sugaya H, Ohkoshi T et al. Vitamin E improves biochemical indices associated with symptoms of atopic dermatitis-like inflammation in NC/Nga mice. J. Nutr. Sci. Vitaminol. (Tokyo) 58(3), 161–168 (2012).
  • Sunitha K, Hemshekhar M, Thushara RM et al. N-Acetylcysteine amide: a derivative to fulfill the promises of N-Acetylcysteine. Free Radic. Res. 47(5), 357–367 (2013).
  • Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic. Biol. Med. 51(5), 1000–1013 (2011).
  • Hur SJ, Kang SH, Jung HS et al. Review of natural products actions on cytokines in inflammatory bowel disease. Nutr. Res. 32(11), 801–816 (2012).
  • Fridovich I. Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 64, 97–112 (1995).
  • Zelko IN, Mariani TJ, Folz RJ. 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(3), 337–349 (2002).
  • Na K, Kim KE, Park ST, Kim TY. EC-SOD suppresses contact hypersensitivity in mouse skin by impairing Langerhans cell migration. J. Invest. Dermatol. 127(8), 1930–1937 (2007).
  • Ha HY, Kim Y, Ryoo ZY, Kim TY. Inhibition of the TPA-induced cutaneous inflammation and hyperplasia by EC-SOD. Biochem. Biophys. Res. Commun. 348(2), 450–458 (2006).
  • Lee YS, Cheon IS, Kim BH, Kwon MJ, Lee HW, Kim TY. Loss of extracellular superoxide dismutase induces severe IL-23-mediated skin inflammation in mice. J. Invest. Dermatol. 133(3), 732–741 (2013).
  • Kwon MJ, Kim B, Lee YS, Kim TY. Role of superoxide dismutase 3 in skin inflammation. J. Dermatol. Sci. 67(2), 81–87 (2012).
  • Laurila JP, Laatikainen LE, Castellone MD, Laukkanen MO. SOD3 reduces inflammatory cell migration by regulating adhesion molecule and cytokine expression. PLoS ONE 4(6), e5786 (2009).
  • Corsini E, Galbiati V, Nikitovic D, Tsatsakis AM. Role of oxidative stress in chemical allergens induced skin cells activation. Food Chem. Toxicol. 6915(13), 00147–00146 (2013).
  • Turunen P, Puhakka HL, Heikura T et al. Extracellular superoxide dismutase with vaccinia virus anti-inflammatory protein 35K or tissue inhibitor of metalloproteinase-1: Combination gene therapy in the treatment of vein graft stenosis in rabbits. Hum. Gene Ther. 17(4), 405–414 (2006).
  • Iida S, Chu Y, Francis J et al. Gene transfer of extracellular superoxide dismutase improves endothelial function in rats with heart failure. Am. J. Physiol. Heart Circ. Physiol. 289(2), H525–H532 (2005).
  • Ohta H, Adachi T, Hirano K. Internalization of human extracellular-superoxide dismutase by bovine aortic endothelial cells. Free Radic. Biol. Med. 16(4), 501–507 (1994).
  • Zhao J, Gao P, Xiao W et al. A novel human derived cell-penetrating peptide in drug delivery. Mol. Biol. Rep. 38(4), 2649–2656 (2011).
  • Petersen SV, Thogersen IB, Valnickova Z et al. The concentration of extracellular superoxide dismutase in plasma is maintained by LRP-mediated endocytosis. Free Radic. Biol. Med. 49(5), 894–899 (2010).
  • Chu Y, Piper R, Richardson S, Watanabe Y, Patel P, Heistad DD. Endocytosis of extracellular superoxide dismutase into endothelial cells: role of the heparin-binding domain. Arterioscler. Thromb. Vasc. Biol. 26(9), 1985–1990 (2006).
  • Carlsson LM, Marklund SL, Edlund T. The rat extracellular superoxide dismutase dimer is converted to a tetramer by the exchange of a single amino acid. Proc. Natl Acad. Sci. USA 93(11), 5219–5222 (1996).
  • Edlund A, Edlund T, Hjalmarsson K et al. A non-glycosylated extracellular superoxide dismutase variant. Biochem. J. 288(Pt 2), 451–456 (1992).
  • Oury TD, Crapo JD, Valnickova Z, Enghild JJ. Human extracellular superoxide dismutase is a tetramer composed of two disulphide-linked dimers: a simplified, high-yield purification of extracellular superoxide dismutase. Biochem. J. 317(Pt 1), 51–57 (1996).
  • Petersen SV, Oury TD, Valnickova Z et al. The dual nature of human extracellular superoxide dismutase: one sequence and two structures. Proc. Natl Acad. Sci. USA 100(24), 13875–13880 (2003).
  • Olsen DA, Petersen SV, Oury TD et al. The intracellular proteolytic processing of extracellular superoxide dismutase (EC-SOD) is a two-step event. J. Biol. Chem. 279(21), 22152–22157 (2004).
  • Bowler RP, Nicks M, Olsen DA et al. Furin proteolytically processes the heparin-binding region of extracellular superoxide dismutase. J. Biol. Chem. 277(19), 16505–16511 (2002).
  • Enghild JJ, Thogersen IB, Oury TD, Valnickova Z, Hojrup P, Crapo JD. The heparin-binding domain of extracellular superoxide dismutase is proteolytically processed intracellularly during biosynthesis. J. Biol. Chem. 274(21), 14818–14822 (1999).
  • Gottfredsen RH, Tran SM, Larsen UG et al. The C-terminal proteolytic processing of extracellular superoxide dismutase is redox regulated. Free Radic. Biol. Med. 52(1), 191–197 (2012).
  • Oshikawa J, Urao N, Kim HW et al. Extracellular SOD-derived H2O2 promotes VEGF signaling in caveolae/lipid rafts and post-ischemic angiogenesis in mice. PLoS ONE 5(4), e10189 (2010).
  • Petersen SV, Kristensen T, Petersen JS et al. The folding of human active and inactive extracellular superoxide dismutases is an intracellular event. J. Biol. Chem. 283(22), 15031–15036 (2008).
  • Petersen SV, Valnickova Z, Oury TD, Crapo JD, Chr Nielsen N, Enghild JJ. The subunit composition of human extracellular superoxide dismutase (EC-SOD) regulates enzymatic activity. BMC Biochem. 8, 19 (2007).
  • Ryu K, Kim YH, Kim Y, Lee JS, Jeon B, Kim TY. Increased yield of high-purity and active tetrameric recombinant human EC-SOD by solid phase refolding. J. Microbiol. Biotechnol. 18(10), 1648–1654 (2008).
  • Chen HL, Yen CC, Tsai TC et al. Production and characterization of human extracellular superoxide dismutase in the methylotrophic yeast Pichia pastoris. J. Agric. Food Chem. 54(21), 8041–8047 (2006).
  • Bae JY, Koo BK, Ryu HB et al. Cu/Zn incorporation during purification of soluble human EC-SOD from E. coli stabilizes proper disulfide bond formation. Appl. Biochem. Biotechnol. 169(5), 1633–1647 (2013).
  • Son YJ, Bae JY, Chong SH et al. Expression, high cell density culture and purification of recombinant EC-SOD in Escherichia coli. Appl. Biochem. Biotechnol. 162(6), 1585–1598 (2010).
  • Zhu XQ, Li SX, He HJ, Yuan QS. On-column refolding of an insoluble His6-tagged recombinant EC-SOD overexpressed in Escherichia coli. Acta Biochim. Biophys. Sin. (Shanghai) 37(4), 265–269 (2005).
  • Ahl IM, Lindberg MJ, Tibell LA. Coexpression of yeast copper chaperone (yCCS) and CuZn-superoxide dismutases in Escherichia coli yields protein with high copper contents. Protein Expr. Purif. 37(2), 311–319 (2004).
  • Hartman JR, Geller T, Yavin Z et al. High-level expression of enzymatically active human Cu/Zn superoxide dismutase in Escherichia coli. Proc. Natl Acad. Sci. USA 83(19), 7142–7146 (1986).
  • Yen CC, Lai YW, Chen HL et al. Aerosolized human extracellular superoxide dismutase prevents hyperoxia-induced lung injury. PLoS ONE 6(10), e26870 (2011).
  • Nakaoka R, Tabata Y, Yamaoka T, Ikada Y. Prolongation of the serum half-life period of superoxide dismutase by poly(ethylene glycol) modification. J. Control. Release 46(3), 253–261 (1997).
  • Kaipel M, Wagner A, Wassermann E et al. Increased biological half-life of aerosolized liposomal recombinant human Cu/Zn superoxide dismutase in pigs. J. Aerosol. Med. Pulm. Drug Deliv. 21(3), 281–290 (2008).
  • Cuzzocrea S, Mazzon E, Dugo L et al. Protective effects of a new stable, highly active SOD mimetic, M40401 in splanchnic artery occlusion and reperfusion. Br. J. Pharmacol. 132(1), 19–29 (2001).
  • Doctrow SR, Lopez A, Schock AM et al. A synthetic superoxide dismutase/catalase mimetic EUK-207 mitigates radiation dermatitis and promotes wound healing in irradiated rat skin. J. Invest. Dermatol. 2012(29), 410 (2012).
  • Perveen S, Patel H, Arif A, Younis S, Codipilly CN, Ahmed M. Role of EC-SOD overexpression in preserving pulmonary angiogenesis inhibited by oxidative stress. PLoS ONE 7(12), e51945 (2012).
  • Tibell L, Hjalmarsson K, Edlund T, Skogman G, Engstrom A, Marklund SL. Expression of human extracellular superoxide dismutase in Chinese hamster ovary cells and characterization of the product. Proc. Natl Acad. Sci. USA 84(19), 6634–6638 (1987).
  • Benov LT, Beyer WF Jr, Stevens RD, Fridovich I. Purification and characterization of the Cu, Zn SOD from Escherichia coli. Free Radic. Biol. Med. 21(1), 117–121 (1996).
  • Djalali M, Abtahi H, Sadeghi MR et al. A new method for the purification of Cu-Zn superoxide dismutase from human erythrocytes. Iranian J. Publ. Health. 3(4), 58–66 (2005).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.