212
Views
10
CrossRef citations to date
0
Altmetric
ORIGINAL ARTICLE

Subcutaneous administration of bovine superoxide dismutase protects lungs from radiation-induced lung injury

, , &
Pages 1259-1268 | Received 21 May 2015, Accepted 23 Jun 2015, Published online: 23 Jul 2015

References

  • Tyldesley S, Boyd C, Schulze K, Walker H, Mackillop WJ. Estimating the need for radiotherapy for lung cancer: an evidence-based, epidemiologic approach. Int J Radiat Oncol Biol Phys 2001;49:973–985.
  • Marks LB, Bentzen SM, Deasy JO, Kong FM, Bradley JD, Vogelius IS, et al. Radiation dose-volume effects in the lung. Int J Radiat Oncol Biol Phys 2010;76:S70–76.
  • Fleckenstein K, Zgonjanin L, Chen L, Rabbani Z, Jackson IL, Thrasher B, et al. Temporal onset of hypoxia and oxidative stress after pulmonary irradiation. Int J Radiat Oncol Biol Phys 2007;68:196–204.
  • Schaue D, Kachikwu EL, McBride WH. Cytokines in radiobiological responses: a review. Radiat Res 2012;178: 505–523.
  • Vujaskovic Z, Anscher MS, Feng QF, Rabbani ZN, Amin K, Samulski TS, et al. Radiation-induced hypoxia may perpetuate late normal tissue injury. Int J Radiat Oncol Biol Phys 2001;50:851–855.
  • Ibuki Y, Goto R. Ionizing radiation-induced macrophage activation: augmentation of nitric oxide production and its significance. Cell Mol Biol (Noisy-le-grand) 2004;50 Online Pub:OL617–626.
  • Carillon J, Rouanet JM, Cristol JP, Brion R. Superoxide dismutase administration, a potential therapy against oxidative stress related diseases: several routes of supplementation and proposal of an original mechanism of action. Pharm Res 2013;30:2718–2728.
  • Miriyala S, Spasojevic I, Tovmasyan A, Salvemini D, Vujaskovic Z, St Clair D, et al. Manganese superoxide dismutase, MnSOD and its mimics. Biochim Biophys Acta 2012;1822:794–814.
  • Noor R, Mittal S, Iqbal J. Superoxide dismutase–applications and relevance to human diseases. Med Sci Monit 2002;8:RA210–215.
  • 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 2002;33: 337–349.
  • Delanian 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;32:12–20.
  • Delanian S, Balla-Mekias S, Lefaix JL. Striking regression of chronic radiotherapy damage in a clinical trial of combined pentoxifylline and tocopherol. J Clin Oncol 1999;17: 3283–3290.
  • 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;35:305–312.
  • Breuer R, Tochner Z, Conner MW, Nimrod A, Gorecki M, Or R, Slavin S. Superoxide dismutase inhibits radiation- induced lung injury in hamsters. Lung 1992;170:19–29.
  • Kang SK, Rabbani ZN, Folz RJ, Golson ML, Huang H, Yu D, et al. Overexpression of extracellular superoxide dismutase protects mice from radiation-induced lung injury. Int J Radiat Oncol Biol Phys 2003;57:1056–1066.
  • Machtay M, Scherpereel A, Santiago J, Lee J, McDonough J, Kinniry P, et al. Systemic polyethylene glycol-modified (PEGylated) superoxide dismutase and catalase mixture attenuates radiation pulmonary fibrosis in the C57/bl6 mouse. Radiother Oncol 2006;81:196–205.
  • Malaker K, Das RM. Effect of superoxide dismutase on early radiation injury of lungs in the rat. Mol Cell Biochem 1988;84:141–145.
  • Rabbani ZN, Anscher MS, Folz RJ, Archer E, Huang H, Chen L, et al. Overexpression of extracellular superoxide dismutase reduces acute radiation induced lung toxicity. BMC Cancer 2005;5:59.
  • Carpenter M, Epperly MW, Agarwal A, Nie S, Hricisak L, Niu Y, Greenberger JS. Inhalation delivery of manganese superoxide dismutase-plasmid/liposomes protects the murine lung from irradiation damage. Gene Ther 2005;12:685–693.
  • Epperly MW, Defilippi S, Sikora C, Gretton J, Kalend A, Greenberger JS. Intratracheal injection of manganese superoxide dismutase (MnSOD) plasmid/liposomes protects normal lung but not orthotopic tumors from irradiation. Gene Ther 2000;7:1011–1018.
  • Epperly MW, Travis EL, Sikora C, Greenberger JS. Manganese [correction of Magnesium] superoxide dismutase (MnSOD) plasmid/liposome pulmonary radioprotective gene therapy: modulation of irradiation-induced mRNA for IL-I, TNF-alpha, and TGF-beta correlates with delay of organizing alveolitis/fibrosis. Biol Blood Marrow Transplant 1999;5:204–214.
  • Gauter-Fleckenstein B, Fleckenstein K, Owzar K, Jiang C, Batinic-Haberle I, Vujaskovic Z. Comparison of two Mn porphyrin-based mimics of superoxide dismutase in pulmonary radioprotection. Free Radic Biol Med 2008;44:982–989.
  • Gauter-Fleckenstein B, Fleckenstein K, Owzar K, Jiang C, Reboucas JS, Batinic-Haberle I, Vujaskovic Z. Early and late administration of MnTE-2-PyP5 + in mitigation and treatment of radiation-induced lung damage. Free Radic Biol Med 2010;48:1034–1043.
  • Rabbani ZN, Batinic-Haberle I, Anscher MS, Huang J, Day BJ, Alexander E, et al. Long-term administration of a small molecular weight catalytic metalloporphyrin antioxidant, AEOL 10150, protects lungs from radiation-induced injury. Int J Radiat Oncol Biol Phys 2007;67:573–580.
  • Gauter-Fleckenstein B, Reboucas JS, Fleckenstein K, Tovmasyan A, Owzar K, Jiang C, et al. Robust rat pulmonary radioprotection by a lipophilic Mn N-alkylpyridylporphyrin, MnTnHex-2-PyP(5+). Redox Biol 2014;2:400–410.
  • Muscoli C, Cuzzocrea S, Riley DP, Zweier JL, Thiemermann C, Wang ZQ, Salvemini D. On the selectivity of superoxide dismutase mimetics and its importance in pharmacological studies. Br J Pharmacol 2003;140:445–460.
  • Regnault C, Soursac M, Roch-Arveiller M, Postaire E, Hazebroucq G. Pharmacokinetics of superoxide dismutase in rats after oral administration. Biopharm Drug Dispos 1996; 17:165–174.
  • Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 1988;41:467–470.
  • Zhang Y, Zhang X, Rabbani ZN, Jackson IL, Vujaskovic Z. Oxidative stress mediates radiation lung injury by inducing apoptosis. Int J Radiat Oncol Biol Phys 2012;83:740–748.
  • Kimura M, Rabbani ZN, Zodda AR, Yan H, Jackson IL, Polascik TJ, et al. Role of oxidative stress in a rat model of radiation-induced erectile dysfunction. J Sex Med 2012;9: 1535–1549.
  • Rabbani ZN, Mi J, Zhang Y, Delong M, Jackson IL, Fleckenstein K, et al. Hypoxia inducible factor 1alpha signaling in fractionated radiation-induced lung injury: role of oxidative stress and tissue hypoxia. Radiat Res 2010;173: 165–174.
  • Rabbani ZN, Salahuddin FK, Yarmolenko P, Batinic-Haberle I, Thrasher BA, Gauter-Fleckenstein B, et al. Low molecular weight catalytic metalloporphyrin antioxidant AEOL 10150 protects lungs from fractionated radiation. Free Radic Res 2007;41:1273–1282.
  • Bentzen SM. Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat Rev Cancer 2006;6:702–713.
  • Jackson IL, Zhang X, Hadley C, Rabbani ZN, Zhang Y, Marks S, Vujaskovic Z. Temporal expression of hypoxia- regulated genes is associated with early changes in redox status in irradiated lung. Free Radic Biol Med 2012;53: 337–346.
  • Vujaskovic Z, Batinic-Haberle I, Rabbani ZN, Feng QF, Kang SK, Spasojevic I, et al. A small molecular weight catalytic metalloporphyrin antioxidant with superoxide dismutase (SOD) mimetic properties protects lungs from radiation- induced injury. Free Radic Biol Med 2002;33:857–863.
  • Mahmood J, Jelveh S, Zaidi A, Doctrow SR, Hill RP. Mitigation of radiation-induced lung injury with EUK-207 and genistein: effects in adolescent rats. Radiat Res 2013;179:125–134.
  • Heckert EG, Karakoti AS, Seal S, Self WT. The role of cerium redox state in the SOD mimetic activity of nanoceria. Biomaterials 2008;29:2705–2709.
  • Diebold I, Petry A, Hess J, Gorlach A. The NADPH oxidase subunit NOX4 is a new target gene of the hypoxia-inducible factor-1. Mol Biol Cell 2010;21:2087–2096.
  • Martin M, Lefaix J, Delanian S. TGF-beta1 and radiation fibrosis: a master switch and a specific therapeutic target? Int J Radiat Oncol Biol Phys 2000;47:277–290.
  • Vujaskovic Z, Groen HJ. TGF-beta, radiation-induced pulmonary injury and lung cancer. Int J Radiat Biol 2000;76:511–516.
  • Jackson IL, Chen L, Batinic-Haberle I, Vujaskovic Z. Superoxide dismutase mimetic reduces hypoxia-induced O2*-, TGF-beta, and VEGF production by macrophages. Free Radic Res 2007;41:8–14.
  • Flechsig P, Dadrich M, Bickelhaupt S, Jenne J, Hauser K, Timke C, et al. LY2109761 attenuates radiation-induced pulmonary murine fibrosis via reversal of TGF-beta and BMP-associated proinflammatory and proangiogenic signals. Clin Cancer Res 2012;18:3616–3627.
  • Yan F, Wang Y, Wu X, Peshavariya HM, Dusting GJ, Zhang M, Jiang F. Nox4 and redox signaling mediate TGF-beta-induced endothelial cell apoptosis and phenotypic switch. Cell Death Dis 2014;5:e1010.
  • Ismail S, Sturrock A, Wu P, Cahill B, Norman K, Huecksteadt T, et al. NOX4 mediates hypoxia-induced proliferation of human pulmonary artery smooth muscle cells: the role of autocrine production of transforming growth factor-{beta}1 and insulin-like growth factor binding protein-3. Am J Physiol Lung Cell Mol Physiol 2009;296:L489–499.
  • Buttner C, Skupin A, Reimann T, Rieber EP, Unteregger G, Geyer P, Frank KH. Local production of interleukin-4 during radiation-induced pneumonitis and pulmonary fibrosis in rats: macrophages as a prominent source of interleukin-4. Am J Respir Cell Mol Biol 1997;17:315–325.
  • Epperly MW, Bray JA, Krager S, Berry LM, Gooding W, Engelhardt JF, Zwacka R, Travis EL, Greenberger JS. Intratracheal injection of adenovirus containing the human MnSOD transgene protects athymic nude mice from irradiation-induced organizing alveolitis. Int J Radiat Oncol Biol Phys 1999;43:169–181.
  • Hauser GJ, McIntosh JK, Travis WD, Rosenberg SA. Manipulation of oxygen radical-scavenging capacity in mice alters host sensitivity to tumor necrosis factor toxicity but does not interfere with its antitumor efficacy. Cancer Res 1990;50: 3503–3508.
  • Nielsen OS, Overgaard J, Overgaard M, Steenholdt S, Jakobsen A, Sell A. Orgotein in radiation treatment of bladder cancer. A report on allergic reactions and lack of radioprotective effect Acta Oncol 1987;26:101–104.
  • de Benito V, de Barrio M, de Lopez-Saez MP, Ordoqui E, Prieto-Garcia A, Sainza T, Baeza ML. Anaphylactic shock caused by impurities in orgotein preparations. Allergol Immunopathol (Madr) 2001;29:272–275.
  • Joral A, Boyano T, Mira J, Agud JL, Saiz F. Systemic anaphylaxis following parenteral orgotein administration. J Investig Allergol Clin Immunol 1993;3:103–104.
  • 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;60:1211–1219.
  • 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: 201–208.
  • 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;88:385–389.
  • Niwa Y, Somiya K, Michelson AM, Puget K. Effect of liposomal-encapsulated superoxide dismutase on active oxygen-related human disorders. A preliminary study. Free Radic Res Commun 1985;1:137–153.
  • Batinic-Haberle I, Reboucas JS, Spasojevic I. Superoxide dismutase mimics: chemistry, pharmacology, and therapeutic potential. Antioxid Redox Signal 2010;13:877–918.

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.