Pharmaceutical Research

, Volume 30, Issue 11, pp 2718–2728 | Cite as

Superoxide Dismutase Administration, A Potential Therapy Against Oxidative Stress Related Diseases: Several Routes of Supplementation and Proposal of an Original Mechanism of Action

  • Julie Carillon
  • Jean-Max Rouanet
  • Jean-Paul Cristol
  • Richard Brion
Expert Review

ABSTRACT

Oxidative stress, involved in many diseases, is defined as an impaired balance between reactive oxygen species (ROS) production and antioxidant defences. Antioxidant enzymes such as superoxide dismutase (SOD) play a key role in diminishing oxidative stress. Thus, the removal of ROS by exogenous SODs could be an effective preventive strategy against various diseases. The poor bioavailability of exogenous SODs has been criticized. However, improvements in SOD formulation may overcome this limitation and boost interest in its therapeutic properties. Here, we provide a review of animal and human studies about SODs supplementation in order to evaluate their therapeutic value. Protective effects have been observed against irradiation, carcinogenesis, apoptosis and neurodegeneration. SODs administration has also been reported to alleviate inflammatory, infectious, respiratory, metabolic and cardiovascular diseases and genitourinary and fertility disorders, raising the question of its mechanism of action in these diverse situations. Some authors have shown an increase in endogenous antioxidant enzymes after exogenous SODs administration. The induction of endogenous antioxidant defence and, consequently, a decrease in oxidative stress, could explain all the effects observed. Further investigations need to be carried out to test the hypothesis that SODs supplementation acts by inducing an endogenous antioxidant defence.

KEY WORDS

bioavailability endogenous antioxidant defence formulation inflammation 

ABBREVIATIONS

AAPH

Hydrochloride 2,2′-azobis-2-amidinopropane

AIDS

Acquired immunodeficiency syndrome

ARE

Antioxidant response element

CAT

Catalase

Cu/Zn-SOD

Copper/zinc-superoxide dismutase

DIVEMA

Divinyl ether and maleic anhydride

DNA

Deoxyribonucleic acid

EC-SOD

Extracellular-superoxide dismutase

Fe-SOD

Iron-superoxide dismutase

FIV

Feline immunodeficiency virus

GPx

Glutathione peroxidase

H2O2

Hydrogen peroxide

HIV

Human immunodeficiency virus

HO°

Hydroxyl radical

Mn-SOD

Manganese-superoxide dismutase

Nrf2

Transcription factor nuclear-factor-E2-related factor

O2°-

Superoxide anion radical

PEG

Pegylated

PMA

Phorbol 12-myristate 13-acetate

ROS

Reactive oxygen species

SOD

Superoxide dismutase

REFERENCES

  1. 1.
    Davies KJA. Oxidative stress: the paradox of aerobic life. Biochem Soc Symp. 1995;61:1–31.PubMedGoogle Scholar
  2. 2.
    Rhee SG. Cell signaling : H2O2, a necessary evil for cell signaling. Science. 2006;312(5782):1882–3.PubMedGoogle Scholar
  3. 3.
    Griendling KK, Alexander RW. Oxidative stress and cardiovascular disease. Circulation. 1997;96(10):3264–5.PubMedGoogle Scholar
  4. 4.
    McCord JM. The evolution of free radicals and oxidative stress. Am J Med. 2000;108:652–9.PubMedGoogle Scholar
  5. 5.
    Fridovich I. Superoxide radical and superoxide dismutases. Annu Rev Biochem. 1995;64:97–112.PubMedGoogle Scholar
  6. 6.
    Hassan HM, Scandalios JG. Superoxide dismutases in aerobic organism. In: Alscher RG, Cumming JR, editors. Stress Responses in Plants: Adaptation and Acclimation Mechanisms. New York: Wiley-Liss; 1990. p. 175–99.Google Scholar
  7. 7.
    Nordmann R, Ribière C. Superoxyde dismutases : rôle biologique; espoir thérapeutique ? Cah Nutr Diét. 1991;26(6):398–402.Google Scholar
  8. 8.
    Beyer W, Imlay J, Fridovich I. Superoxide dismutases. Prog Nucleic Acid Res Mol Biol. 1991;40:221–53.PubMedGoogle Scholar
  9. 9.
    Faraci FM, Didion SP. Vascular protection: superoxide dismutase isoforms in the vessel wall. Arterioscler Thromb Vasc Biol. 2004;24:1367–73.PubMedGoogle Scholar
  10. 10.
    Scandalios JG. Molecular genetics of superoxide dismutase in plants. In: Scandalios JG, editor. Oxidative stress and molecular biology of antioxidant defences. Cold Spring Harbor; 1997. P. 527–68.Google Scholar
  11. 11.
    Muchova J, Sustrova M, Garaiova I, Liptakova A, Blazicek P, Kvasnicka P, et al. Influence of age on activities of antioxidant enzymes and lipid peroxidation products in erythrocytes and neutrophils of down syndrome patients. Free Radic Biol Med. 2001;31(4):499–508.PubMedGoogle Scholar
  12. 12.
    Perluigi M, Butterfield A. Oxidative stress and down syndrome: a route toward Alzheimer-like dementia. Curr Gerontol Geriatr Res. 2012;2012:724904.PubMedGoogle Scholar
  13. 13.
    Edeas MA, Emerit I, Khalfoun Y, Lazizi Y, Cernjavski L, Levy A, et al. Clastogenic factors in plasma of HIV-1 infected patients activate HIV-1 replication in vitro:inhibition by superoxide dismutase. Free Radic Biol Med. 1997;23(4):571–8.PubMedGoogle Scholar
  14. 14.
    Epperly MW, Liggitt D, Greenberger JS. Systemic intravenous (IV) as well as local administration of manganese superoxide dismutase-plasmid/liposome (MnSOD-PL) displays no detectable toxicity while offering protection from irradiation-induced damage. Int J Radiat Oncol Biol Phys. 2005;63(2):S487–8.Google Scholar
  15. 15.
    Greenberger JS, Smith T, Schlesselman JJ, Epperly M. In a mouse model intravenous administration of Mn SOD-PL protects against whole body irradiation. Int J Radiat Oncol Biol Phys. 2007;69(3):S619.Google Scholar
  16. 16.
    Greenberger JS, Hricisak L, Epperly MW. In a model of irradiation retreatment of the lung (stimulating radiotherapy for lung cancer local recurrence), normal lung tolerance is increased by administration of manganese SOD-PL. Int J Radiat Oncol Biol Phys. 2005;63(2):S475–6.Google Scholar
  17. 17.
    Rabbani Z, Jackson I, Zhang X, Xu P, Vujaskovic Z. Subcutaneous administration of bovine superoxide dismutase protects lungs from radiation induced lung injury. Int J Radiat Oncol Biol Phys. 2010;78(3):S39–40.Google Scholar
  18. 18.
    Epperly MW, Kagan VE, Sikora CA, Gretton JE, Defilippi SJ, Bar-Sagi D, et al. Manganese superoxide dismutase-plasmid/liposome (MnSOD-PL) administration protects mice from esophagitis associated with fractionated radiation. Int J Cancer. 2001;96:221–31.PubMedGoogle Scholar
  19. 19.
    Nie Y, Epperly M, Shen H, Greenberger JS. Intraesophageal administration of MnSOD-PL pre-irradiation results in increased engraftment of bone marrow progenitors of esophageal stem cells. Int J Radiat Oncol Biol Phys. 2007;69(3):S41–2.Google Scholar
  20. 20.
    Escribano A, Garcia-Grande A, Montanes P, Miralles L, Garcia A. Aerosol orgotein (Ontosein) for the prevention of radiotherapy-induced adverse effects in head and neck cancer patients : a feasibility study. Neoplasma. 2002;49(3):201–8.PubMedGoogle Scholar
  21. 21.
    Valencia J, Velilla C, Urpegui A, Alvarez I, Llorens MA, Coronel P, et al. The efficacy of orgotein in the treatment of acute toxicity due to radiotherapy on head and neck tumors. Tumori. 2002;88(5):385–9.PubMedGoogle Scholar
  22. 22.
    Epperly MW, Carpenter M, Agarwal A, Mitra P, Nie S, Greenberger JS. Intraoral manganese superoxide dismutase-plasmid/liposome (MnSOD-PL) radioprotective gene therapy decreases ionizing irradiation-induced murine mucosal cell cycling and apoptosis. In Vivo. 2004;18(4):401–10.PubMedGoogle Scholar
  23. 23.
    Esco R, Valencia J, Coronel P, Carceller JA, Gimeno M, Bascon N. Efficacy of orgotein in prevention of late side effects of pelvic irradiation : a randomized study. Int J Radiat Oncol Biol Phys. 2004;60(4):1211–9.PubMedGoogle Scholar
  24. 24.
    Kadrnka F. Results of a multicenter orgotein study in radiation induced and interstitial cystitis. Eur J Rheumatol Inflamm. 1981;4(2):237–43.PubMedGoogle Scholar
  25. 25.
    Maier U, Zechner O. Therapy of radiation injuries of the bladder with orgotein (Peroxinom). J Urol Nephrol. 1988;81(5):305–8.Google Scholar
  26. 26.
    Menander-Huber KB, Edsmyr F, Huber W. Orgotein (superoxide dismutase): a drug for the amelioration of radiation-induced side effects. A double-blind, placebo-controlled study in patients with bladder tumors. Urol Res. 1978;6(4):255–7.PubMedGoogle Scholar
  27. 27.
    Sanchiz F, Milla A, Artola N, Julia JC, Moya LM, Pedro A, et al. Prevention of radioinduced cystitis by orgotein : a randomized study. Anticancer Res. 1996;16(4A):2025–8.PubMedGoogle Scholar
  28. 28.
    Delanian S, Martin M, Bravard A, Luccioni C, Lefaix JL. Cu/Zn superoxide dismutase modulates phenotypic changes in cultured fibroblasts from human skin with chronic radiotherapy damage. Radiother Oncol. 2001;58:325–31.PubMedGoogle Scholar
  29. 29.
    Lefaix JL, Delanian S, Leplat JJ, Tricaud Y, Martin M, Nimrod A, et al. Successful treatment of radiation-induced fibrosis using Cu/Zn SOD and Mn SOD: an experimental study. Int J Radiat Oncol Biol Phys. 1996;35(2):305–12.PubMedGoogle Scholar
  30. 30.
    Campana F, Zervoudis S, Perdereau B, Gez E, Fourquet A, Badiu C, et al. Topical superoxide dismutase reduces post-irradiation breast cancer fibrosis. J Cell Mol Med. 2004;8(1):109–16.PubMedGoogle Scholar
  31. 31.
    Delenian S, Baillet F, Huart J, Lefaix JL, Maulard C, Housset M. Successful treatment of radiation-induced fibrosis using liposomal Cu/Zn superoxide-dismutase- Clinical-Trial. Radiother Oncol. 1994;32(1):12–20.Google Scholar
  32. 32.
    Takehara Y, Yamaoka K, Sato EF, Yoshioka T, Utsumi K. DNA damage by various forms of active oxygens and its inhibition by different scavengers using plasmid DNA. Physiol Chem Phy Med. 1994;26(3):215–26.Google Scholar
  33. 33.
    Vouldoukis I, Conti M, Krauss P, Kamaté C, Blasquez S, Tefit M, et al. Supplementation with Gliadin-combined plant superoxide dismutase extract promotes antioxidant defences and protects against oxidative stress. Phytother Res. 2004;18(12):957–62.PubMedGoogle Scholar
  34. 34.
    Prost M. Utilisation de générateur de radicaux libres dans le domaine des dosages biologiques. FR Patent. 1989;2:642. 526.Google Scholar
  35. 35.
    Stocker P, Lesgards JF, Vidal N, Chalier F, Prost M. ESR study of a biological assay on whole blood: antioxidant efficiency of various vitamins. Biochim Biophys Acta. 2003;1621(1):1–8.PubMedGoogle Scholar
  36. 36.
    Notin C, Vallon L, Desbordes F, Leleu C. Oral supplementation with superoxide dismutase in Standardbred trotters in training: a double-blind placebo-controlled study. Eq Vet J. 2010;42(38):375–81.Google Scholar
  37. 37.
    Leskova GF. Protective effect of different form superoxide dismutase on the plasma membrane phospholipid composition of hepatocyte and adipocyte and on the blood lipoprotein composition in hemorrhagic shock in cats. Vopr Med Khim. 1999;45(5):389–97.PubMedGoogle Scholar
  38. 38.
    Regnault C, Roch-Arveiller M, Tissot M, Sarfati G, Giroud JP, Postaire E, et al. Effect of encapsulation on the anti-inflammatory properties of superoxide dismutase after oral administration. Clin Chim Acta. 1995;240:117–27.PubMedGoogle Scholar
  39. 39.
    Jadot G, Michelson AM, Puget K. Anti-inflammatory activity of superoxide dismutases inhibition of carrageenan induced edema in rats. Free Rad Res Comms. 1985;1(6):395–403.Google Scholar
  40. 40.
    Jadot G, Michelson AM, Puget K, Baret A. Anti-inflammatory activity of superoxide dismutase inhibition of Adriamycin induced edema in rats. Free Rad Res Comms. 1986;2(2):19–26.Google Scholar
  41. 41.
    Vaille A, Jadot G, Elizagaray A. Anti-inflammatory activity of various superoxide dismutases on polyarthritis in the Lewis rat. Biochem Pharmacol. 1990;39(2):247–55.PubMedGoogle Scholar
  42. 42.
    Gammer W, Broback LG. Clinical comparison of orgotein and methylprednisolone acetate in the treatment of osteoarthrosis of the knee joint. Scand J Rheumatol. 1984;13(2):108–12.PubMedGoogle Scholar
  43. 43.
    Goebel KM, Storck U, Neurath F. Intrasynovial orgotein therapy in rheumatoid arthritis. Lancet. 1981;1(8228):1015–7.PubMedGoogle Scholar
  44. 44.
    Lund-Olesen K, Menander-Huber KB. Intra-articular orgotein therapy in osteoarthritis of the knee. A double-blind, placebo-controlled trial. Arzneimittelforschung. 1983;33(8):1199–203.PubMedGoogle Scholar
  45. 45.
    Mazieres B, Masquelier AM, Capron MH. A French controlled multicenter study of intra-articular orgotein versus intraarticular corticosteroids in the treatment of knee osteoarthritis : a one-year followup. J Rheumatol Suppl. 1991;27:134–7.PubMedGoogle Scholar
  46. 46.
    McIlwain H, Silverfield JC, Cheatum DE, Poiley J, Taborn J, Ignaczak T, et al. Intra-articular orgotein in osteoarthritis of the knee : a placebo-controlled efficacy, safety, and dosage comparison. Am J Med. 1989;87(3):295–300.PubMedGoogle Scholar
  47. 47.
    Terlizzi N, Bonali C, Tamburrino V, Numo R. Evaluation of the efficacy of orgotein in a series of patients with hydrarthrosis of the knee. Minerva Med. 1986;77(21):947–51.PubMedGoogle Scholar
  48. 48.
    Talke M. Intra-articular therapy with superoxide dismutase (orgotein) or cortisone in rheumatoid and arthritic inflammatory finger joint lesions. Handchir Mikrochir Plast Chir. 1984;16(1):59–63.PubMedGoogle Scholar
  49. 49.
    Muller U, Moll G. Treatment of epicondylitis with locally injected orgotein (double blind study). J Rheumatol. 1983;42(1):21–4.Google Scholar
  50. 50.
    Lin Y, Pape HD, Friedrich R. Use of superoxide dismutase (SOD) in patients with temporomandibular joint dysfunction- a preliminary study. Int J Oral Maxillafac Surg. 1994;23(6 Pt 2):428–9.Google Scholar
  51. 51.
    Jadot G, Michelson AM. Comparative anti inflammatory activity of different superoxide dismutases and liposomal SOD in ischemia. Free Rad Res Comms. 1986;3(6):389–94.Google Scholar
  52. 52.
    Stone WC, Bjorling DE, Southard JH, Galbreath EJ, Lindsay WA. Evaluation of intestinal villus height in rats after ischemia and reperfusion by administration of superoxide-dismutase, polyethylene glycol-conjugated SOD, and 2,21-aminosteroids. Am J Vet Res. 1992;53(11):2153–6.PubMedGoogle Scholar
  53. 53.
    Segui J, Gironella M, Sans M, Granell S, Gil F, Gimeno M, et al. Superoxide dismutase ameliorates TNBS-induced colitis by reducing oxidative stress, adhesion molecule expression, and leukocyte recruitment into the inflamed intestine. J Leukocyte Biol. 2004;76(3):537–44.PubMedGoogle Scholar
  54. 54.
    Watterlot L, Rochat T, Sokol H, Cherbuy C, Bouloufa I, Lefèvre F, et al. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. Int J Food Microbiol. 2010;144:35–41.PubMedGoogle Scholar
  55. 55.
    Okada F, Shionoya H, Kobayashi M, Kobayashi T, Tazawa H, Onuma K, et al. Prevention of inflammation-mediated acquisition of metastatic properties of benign mouse fibrosarcoma cells by administration of an orally available superoxide dismutase. Brit J Cancer. 2006;94:854–62.PubMedGoogle Scholar
  56. 56.
    Webb CB, Lehman TL, McCord KW. Effects of an oral superoxide enzyme supplementation on indices of oxidative stress, proviral load, and CD4:CD8 ratios in asymptomatic FIV-infected cats. J Feline Med Surg. 2008;10:423–30.PubMedGoogle Scholar
  57. 57.
    Wengenack TM, Curran GL, Poduslo JF. Postischemic, systemic administration of polyamine-modified superoxide dismutase reduces hippocampal CA1 neurodegeneration in rat global cerebral ischemia. Brain Res. 1997;754:46–54.PubMedGoogle Scholar
  58. 58.
    Nakajima S, Ohsawa I, Nagata K, Ohta S, Ohno M, Ijichi T, et al. Oral supplementation with melon superoxide dismutase extract promotes antioxidant defences in the brain and prevents stress-induced impairment of spatial memory. Behav Brain Res. 2009;200(1):15–21.PubMedGoogle Scholar
  59. 59.
    Hamm RJ, Temple MD, Pike BR, Ellis EF. The effect of postinjury administration of polyethylene glycol-conjugated superoxide dismutase (Pegorgotein, Dismutec®) or lidocaine on behavioural function following fluid-percussion brain injury in rats. J Neurotraum. 1996;13(6):325–32.Google Scholar
  60. 60.
    Milesi MA, Lacan D, Brosse H, Desor D, Notin C. Effect of an oral supplementation with a proprietary melon juice concentrate (Extramel®) on stress and fatigue in healthy people: a pilot, double-blind, placebo-controlled clinical trial. Nutr J. 2009;8:40.PubMedGoogle Scholar
  61. 61.
    Décordé K, Agne A, Lacan D, Ramos J, Fouret G, Ventura E, et al. Preventive effect of a melon extract rich in superoxide scavenging activity on abdominal and liver fat and adipokine imbalance in high-fat-fed hamsters. J Agric Food Chem. 2009;57:6461–7.PubMedGoogle Scholar
  62. 62.
    Décordé K, Ventura E, Lacan D, Ramos J, Cristol JP, Rouanet JM. An SOD rich melon extract Extramel® prevents aortic lipids and liver steatosis in diet-induced model of atherosclerosis. Nut Metab Card Dis. 2010;20:301–7.Google Scholar
  63. 63.
    Laursen JB, Rajagopalan S, Galis Z, Tarpey M, Freeman BA, Harrison DG. Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation. 1997;95(3):588–93.PubMedGoogle Scholar
  64. 64.
    Nakazono K, Watanabe N, Matsuno K, Sasaki J, Sato T, Inoue M. Does superoxide underlie the pathogenesis of hypertension. PNAS. 1991;88(22):10045–8.PubMedGoogle Scholar
  65. 65.
    Crapo JD, DeLong DM, Sjostrom K, Hasler GR, Drew RT. The failure of aerosolized superoxide dismutase to modify pulmonary oxygen toxicity. Am Rev Respir Dis. 1977;115:1027–33.PubMedGoogle Scholar
  66. 66.
    Freeman BA, Turrens JF, Mirza Z, Crapo JD, Young SL. Modulation of oxidant lung injury by using liposome-entrapped superoxide dismutase and catalase. Fed Proc. 1985;44:2591–5.PubMedGoogle Scholar
  67. 67.
    Padmanabhan RV, Gudapaty R, Liener IE, Schwartz BA, Hoidal JR. Protection against pulmonary oxygen toxicity in rats by the intratracheal administration of liposome-encapsulated superoxide dismutase or catalase. Am Rev Respir Dis. 1985;132:164–7.PubMedGoogle Scholar
  68. 68.
    Simonson SG, Welty-Wolf KE, Huang YC, Taylor DE, Kantrow SP, Carraway MS, et al. Aerosolized manganese SOD decreases hyperoxic pulmonary injury in primates. I: physiology and biochemistry. J Appl Physiol. 1997;83:550–8.PubMedGoogle Scholar
  69. 69.
    Turrens JF, Crapo JD, Freeman BA. Protection against oxygen toxicity by intravenous injection of liposome-entrapped catalase and superoxide dismutase. J Clin Invest. 1984;73:87–95.PubMedGoogle Scholar
  70. 70.
    Welty-Wolf KE, Simonson SG, Huang YC, Kantrow SP, Carraway MS, Chang LY, et al. Aerosolized manganese SOD decreases hyperoxic pulmonary injury in primates. II: morphometric analysis. J Appl Physiol. 1997;83:559–68.PubMedGoogle Scholar
  71. 71.
    White CW, Jackson JH, Abuchowski A, Kazo GM, Mimmack RF, Berger EM, et al. Polyethylene glycol-attached antioxidant enzymes decrease pulmonary oxygen toxicity in rats. J Appl Physiol. 1989;66:584–90.PubMedGoogle Scholar
  72. 72.
    Assa’ad AH, Ballard ET, Sebastian KD, Loven DP, Boivin GP, Lierl MB. Effect of superoxide dismutase on a rabbit model of chronic allergic asthma. Ann Allergy Asthma Immunol. 1998;80:215–24.PubMedGoogle Scholar
  73. 73.
    Tanaka K, Tanaka Y, Miyazaki Y, Namba T, Sato K, Aoshiba K, et al. Therapeutic effect of lecithinized superoxide dismutase on pulmonary emphysema. J Pharmacol Exp Ther. 2011;338(3):810–8.PubMedGoogle Scholar
  74. 74.
    Rosenfeld WN, Davis JM, Parton L, Richter SE, Price A, Flaster E, et al. Safety and pharmacokinetics of recombinant human superoxide dismutase administered intratracheally to premature neonates with respiratory distress syndrome. Pediatrics. 1996;97(6):811–7.PubMedGoogle Scholar
  75. 75.
    Cocchia N, Pasolini MP, Mancini R, Petrazzuoto O, Cristofaro I, Rosapane I, et al. Effect of sod (superoxide dismutase) protein supplementation in semen extenders on mobility, viability, acrosome status and ERK (extracellular signal-regulated kinase) protein phosphorylation of chilled stallion spermatozoa. Theriogenology. 2011;75:1201–10.PubMedGoogle Scholar
  76. 76.
    Bartsch G, Menader-Huber KB, Huber W, Marberger H. Orgotein, a new drug for the treatment of Peyronie’s disease. Eur J Rheumatol Inflamm. 1981;4(2):250–9.PubMedGoogle Scholar
  77. 77.
    Gustafson H, Johansson B, Edsmyr F. Peyronie’s disease : experience of local treatment with Orgotein. Eur Urol. 1981;7(6):346–8.PubMedGoogle Scholar
  78. 78.
    Ludwig G. Evaluation of conservative therapeutic approaches to Peyronie’s disease (fibrotic induration of the penis). Urol Int. 1991;47(4):236–9.PubMedGoogle Scholar
  79. 79.
    Primus G. Orgotein in the treatment of plastic induration of the penis (Peyronie’s disease). Int Urol Nephrol. 1993;25(2):169–72.PubMedGoogle Scholar
  80. 80.
    Vouldoukis I, Lacan D, Kamaté C, Coste P, Calenda A, Mazier D, et al. Antioxidant and anti inflammatory properties of a cucumis melo L.C. extract rich in superoxide dismutase activity. J Ethnopharmacol. 2004;94:67–75.PubMedGoogle Scholar
  81. 81.
    Swart PJ, Hirano T, Kuipers ME, Ito Y, Smith C, Hashida M, et al. Targeting of superoxide dismutase to the liver results in anti-inflammatory effects in rats with fibrotic livers. J Hepatol. 1999;31:1034–43.PubMedGoogle Scholar
  82. 82.
    Huber W, Menander-Huber KB, Saifer MG, Williams LD. Bioavailability of superoxide dismutase: implications for the anti-inflammatory action mechanism of orgotein. Agents Actions. 1980;7:185–95.PubMedGoogle Scholar
  83. 83.
    Oyen WJ, Boerman OC, Storm G, van Bloois L, Koenders EB, Claessens RAMJ, et al. Detecting infection and inflammation with technetium-99m-labeled stealth® liposomes. J Nucl Med. 1996;37:1392–7.PubMedGoogle Scholar
  84. 84.
    Takakura Y, Masuda S, Tokuda H, Nishikawa M, Hashida M. Targeted delivery of superoxide dismutase to macrophages via mannose receptor-mediated mechanism. Biochem Pharmacol. 1994;47(5):853–8.PubMedGoogle Scholar
  85. 85.
    Giri SN, Misra HP. Fate of superoxide dismutase in mice following oral route of administration. Med Biol. 1984;62:285–9.PubMedGoogle Scholar
  86. 86.
    Zidenberg-cherr S, Keen CL, Lonnerdal B, Hurley LS. Dietary superoxide dismutase does not affect tissue levels. Am J Clin Nutr. 1983;37:5–7.PubMedGoogle Scholar
  87. 87.
    Greenwald RA. Superoxide dismutase and catalase as therapeutic agents for human diseases. A critical Review. Free Radic Biol Med. 1990;8:201–9.PubMedGoogle Scholar
  88. 88.
    Corvo ML, Boerman OC, Oyen WJG, Bloois LV, Cruz MEM, Crommelin DJA, et al. Intravenous administration of superoxide dismutase entrapped in long circulating liposomes II. In vivo fate in a rat model of adjuvant arthritis. Biochim Biophys Acta. 1999;1419:325–34.PubMedGoogle Scholar
  89. 89.
    Corvo ML, Boerman OC, Oyen WJG, Jorge JCS, Cruz MEM, Crommelin DJA, et al. Subcutaneous administration of superoxide dismutase entrapped in long circulating liposomes: In vivo fate and therapeutic activity in an inflammation model. Parmaceut Res. 2000;17(5):600–6.Google Scholar
  90. 90.
    Jubeh TT, Antler S, Haupt S, Barenholz Y, Rubinstein A. Local prevention of oxidative stress in the intestinal epithelium of the rat by adhesive liposomes of superoxide dismutase and tempamine. Molecular Pharmaceut. 2005;2(1):2–11.Google Scholar
  91. 91.
    Jubeh TT, Nadler-Milbauer M, Barenholz Y, Rubinstein A. Local treatment of experimental colitis in the rat by negatively charged liposomes of catalase, TMN and SOD. J Drug Target. 2006;14(3):155–63.PubMedGoogle Scholar
  92. 92.
    Clarke MB, Wright R, Irwin D, Bose S, Van Rheen Z, Birari R, et al. Sustained lung activity of a novel chimeric protein, SOD2/3, after intratracheal administration. Free Radic Biol Med. 2010;49:2032–9.PubMedGoogle Scholar
  93. 93.
    Arangoa MA, Campanero MA, Renedo MJ, Ponchel G, Irache JM. Gliadin nanoparticles as carriers for the oral administration of lipophilic drugs. Relationships between bioadhesion and pharmacokinetics. Pharmaceut Res. 2001;18(11):1521–7.Google Scholar
  94. 94.
    Dugas B. Glisodin®: A nutraceutical product that promote the oral delivery of superoxide dismutase. Free Radic Biol Med. 2002;33:S64.Google Scholar
  95. 95.
    Carillon J, Fouret G, Feillet-Coudray C, Lacan D, Cristol JP, Rouanet JM. Short-term assessment of toxicological aspects, oxidative and inflammatory response to dietary melon superoxide dismutase in rats. Food Chem Tox. 2013;55:323–8.Google Scholar
  96. 96.
    Regnault C, Soursac M, Roch-arveiller M, Postaire E, Hazebroucq G. Pharmacokinetics of superoxide dismutase in rats after oral administration. Biopharm Drug Disposition. 1996;17:165–74.Google Scholar
  97. 97.
    Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: How are they linked? Free Radic Biol Med. 2010;49(11):1603–16.PubMedGoogle Scholar
  98. 98.
    Lallès JP, Lacan D, David JC. A melon pulp concentrate rich in superoxide dismutase reduces stress proteins along the gastrointestinal tract of pigs. Nutrition. 2011;27:358–63.PubMedGoogle Scholar
  99. 99.
    Vozenin-Brotons MC, Sivan V, Gault N, Renard C, Geffrotin C, Delanian S, et al. Antifibrotic action of Cu/Zn SOD is mediated by TGF-β1 repression and phenotypic reversion of myofibroblasts. Free Radic Biol Med. 2001;30(1):30–42.PubMedGoogle Scholar
  100. 100.
    Nelson SK, Bose SK, Grunwald GK, Myhill P, McCord JM. The induction of human superoxide dismutase and catalase in vivo : A fundamentally new approach to antioxidant therapy. Free Radic Biol Med. 2006;40:341–7.PubMedGoogle Scholar
  101. 101.
    Skarpanska-Stejnborn A, Pilaczynska-Szczesniak L, Basta P, Deskur-Smielecka E, Woitas-Slubowska D, Adach Z. Effects of oral supplementation with plant superoxide dismutase extract on selected redox parameters and an inflammatory marker in a 2,000-m rowing-ergometer test. Int J Sport Nutr Exerc Metab. 2011;21(2):124–34.PubMedGoogle Scholar
  102. 102.
    Izumi M, McDonald MC, Sharpe MA, Chatteriee PK, Thiemermann C. Superoxide dismutase mimetics with catalase activity reduce the organ injury in hemorrhagic shock. Shock. 2002;18(3):230–5.PubMedGoogle Scholar
  103. 103.
    Gonzalez PK, Zhuang J, Doctrow SR, Malfroy B, Benson PF, Menconi MJ, et al. EUK-8, a synthetic superoxide dismutase and catalase mimetic, ameliorates acute lung injury in endotoxemic swine. J Pharmacol Exp Ther. 1995;275:798–806.PubMedGoogle Scholar
  104. 104.
    Yang H, Roberts LJ, Shi MJ, Zhou LC, Ballard BR, Richardson A, et al. Retardation of atherosclerosis by overexpression of catalase or both Cu/Zn-superoxide dismutase and catalase in mice lacking apolipoprotein E. Circ Res. 2004;95(11):1075–81.PubMedGoogle Scholar
  105. 105.
    Chan K, Kan YW. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci USA. 1999;96(22):12731–6.PubMedGoogle Scholar
  106. 106.
    Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA. 2001;98(8):4611–6.PubMedGoogle Scholar
  107. 107.
    Juurlink BHJ. Dietary Nrf2 activators inhibit atherogenic processes. Atherosclerosis. 2012;225(1):29–33.PubMedGoogle Scholar
  108. 108.
    Li W, Khor TO, Xu C, Shen G, Jeong WS, Yu S, et al. Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis. Biochem Pharmacol. 2008;76(11):1485–9.PubMedGoogle Scholar
  109. 109.
    Negi G, Kumar A, Joshi RP, Sharma SS. Oxidative stress and Nrf2 in the pathophysiology of diabetic neuropathy: old perspective with a new angle. Biochem Biophys Res Commun. 2011;408:1–5.PubMedGoogle Scholar
  110. 110.
    Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol. 2003;43:233–60.PubMedGoogle Scholar
  111. 111.
    Pedruzzi LM, Stockler-Pinto MB, Leite MJ, Mafra D. Nrf2ekeap1 system versus NF-kB: The good and the evil in chronic kidney disease? Biochimie. 2012;94(12):2461–6.PubMedGoogle Scholar
  112. 112.
    Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, et al. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA. 2001;98(6):3410–5.PubMedGoogle Scholar
  113. 113.
    Enwonwu CO, Sanders C. Nutrition: impact on oral and systemic health. Compend Contin Educ Dent. 2001;22:12–8.PubMedGoogle Scholar
  114. 114.
    Germano C. SOD/gliadin: the ultimate defense against disease and aging. In: Twins Streams. Kensington Publishing Corp.; 2001.pp 121–35.Google Scholar
  115. 115.
    Baret A, Jadot G, Michelson AM. Pharmacokinetics and anti-inflammatory properties in the rat of superoxide dismutase (CuSODs and MnSOD) from various species. Biochem Pharmacol. 1984;33(17):2755–60.PubMedGoogle Scholar
  116. 116.
    Jadot G. Anti-inflammatory activity of superoxide dismutases studies on adjuvant induced polyarthritis in rats. Free Rad Res Comms. 1985;2(2):27–42.Google Scholar
  117. 117.
    Michelson AM, Puget K, Jadot G. Anti-inflammatory activity of superoxide dismutases comparison of enzymes from different sources in different models in rats mechanism of action. Free Rad Res Comms. 1986;2(2):43–56.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Julie Carillon
    • 1
  • Jean-Max Rouanet
    • 1
  • Jean-Paul Cristol
    • 1
    • 2
  • Richard Brion
    • 3
  1. 1.Nutrition & Métabolisme, UMR 204 NutriPass Prévention des Malnutritions et des Pathologies AssociéesUniversité Montpellier 1-2MontpellierFrance
  2. 2.Département de Biochimie Centre Hospitalier Universitaire MontpellierUniversité Montpellier 1MontpellierFrance
  3. 3.Centre CAPIO-BAYARD, Service de CardiologieVilleurbanneFrance

Personalised recommendations