Low molecular weight catalytic metalloporphyrin antioxidant AEOL 10150 protects lungs from fractionated radiation

Free Radical Research

Volumn 41, Issue 11, 2007, Pages 1273-1282

  Rabbani, Zahid N ^a   Salahuddin, Fawzia K ^a   Yarmolenko, Pavel ^a   Batinic Haberle, Ines ^a   Thrasher, Bradley A ^a   Gauter Fleckenstein, Benjamin ^a,b   Dewhirst, Mark W ^a   Anscher, Mitchell S ^a   Vujaskovic, Zeljko ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Hypoxia; Oxidative stress; Pulmonary toxicity; Radiation; Superoxide dismutase metalloporphyrin mimetic

Indexed keywords

3 NITROTYROSINE; AEOL 10150; ANTIOXIDANT; CD31 ANTIGEN; MANGANESE TETRAKIS(N,N DIETHYLIMIDAZOLIUM 2 YL)PORPHYRIN; METALLOPORPHYRIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DOSE RESPONSE; DRUG MEGADOSE; FEMALE; HISTOPATHOLOGY; HYPOXEMIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LONG TERM EXPOSURE; LOW DRUG DOSE; LUNG INJURY; NONHUMAN; OXIDATIVE STRESS; RADIATION DOSE FRACTIONATION; RADIATION EXPOSURE; RADIATION INJURY; RADIATION PROTECTION; RAT;

ANIMALS; ANTIOXIDANTS; CATALYSIS; CYTOPROTECTION; DOSE FRACTIONATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; FEMALE; LUNG; LUNG DISEASES; METALLOPORPHYRINS; MODELS, BIOLOGICAL; MOLECULAR WEIGHT; RADIATION INJURIES, EXPERIMENTAL; RANDOM ALLOCATION; RATS; RATS, INBRED F344;

ANIMALIA; RATTUS;

EID: 36048939654     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715760701689550     Document Type: Article

References (63)

1. Stone, HB, Coleman, CN, Anscher, MS and McBride, WH. (2003) Effects of radiation on normal tissue: Consequences and mechanisms. Lancet Oncol, 4, pp. 529-536.
2. Stone, HB, McBride, WH and Coleman, CN (2002) Modifying normal tissue damage postirradiation. Report of a workshop sponsored by the Radiation Research Program. Radiat Res, 157, pp. 204-223.
3. Riley, PA. (1994) Free radicals in biology: Oxidative stress and the effects of ionizing radiation. Int J Radiat Biol, 65, pp. 27-33.
4. Rubin, P., Finkelstein, J. and Shapiro, D. (1992) Molecular biology mechanisms in the radiation induction of pulmonary injury syndromes: interrelationship between the alveolar macrophage and the septal fibroblast. Int J Radiat Oncol Biol Phys, 24, pp. 93-101.
5. Rubin, P., Johnston, CJ, Williams, JP, McDonald, S. and Finkelstein, JN. (1995) A perpetual cascade of cytokines postirradiation leads to pulmonary fibrosis. Int J Radiat Oncol Biol Phys, 33, pp. 99-109.
6. Crystal, RG. (1991) Oxidants and respiratory tract epithelial injury: pathogenesis and strategies for therapeutic intervention. Am J Med, 91, pp. 39S-44S.
7. Kang, SK, Rabbani, ZN, Folz, RJ, Golson, ML, Huang, H., Samulski, TS, Dewhirst, MW, Anscher, MS and Vujaskovic, Z. (2003) Overexpression of extracellular superoxide dismutase protects mice from radiation-induced lung injury. Int J Radiat Oncol Biol Phys, 57, pp. 1056-1066.
8. Mikkelsen, RB and Wardman, P. (2003) Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene, 22, pp. 5734-5754.
9. Fleckenstein, K., Zgonjanin, L., Chen, L., Rabbani, Z., Jackson, IL, Thrasher, B., Kirkpatrick, J., Foster, WM and Vujaskovic, Z. (2007) Temporal onset of hypoxia and oxidative stress after pulmonary irradiation. Int J Radiat Oncol Biol Phys, 68, pp. 196-204.
10. Rabbani, ZN, Batinic-Haberle, I., Anscher, MS, Huang, J., Day, BJ, Alexander, E., Dewhirst, MW and Vujaskovic, Z. (2007) 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, 67, pp. 573-580.
11. Rabbani, ZN, Anscher, MS, Folz, RJ, Archer, E., Huang, H., Chen, L., Golson, ML, Samulski, TS, Dewhirst, MW and Vujaskovic, Z. (2005) Overexpression of extracellular superoxide dismutase reduces acute radiation induced lung toxicity. BMC Cancer, 5, p. 59.
12. Batinic-Haberle, I., Spasojevic, I., Stevens, RD, Hambright, P., Neta, P., Okado-Matsumoto, A. and Fridovich, I. (2004) New class of potent catalysts of O2.-dismutation. Mn(III) ortho-methoxyethylpyridyl- and di-ortho-methoxyethylimidazolylporphyrins. Dalton Trans, 11, pp. 1696-1702.
13. Sheng, H., Enghild, JJ, Bowler, R., Patel, M., Batinic-Haberle, I., Calvi, CL, Day, BJ, Pearlstein, RD, Crapo, JD and Warner, DS. (2002) Effects of metalloporphyrin catalytic antioxidants in experimental brain ischemia. Free Rad Biol Med, 33, pp. 947-961.
14. Ashcroft, T., Simpson, JM and Timbrell, V. (1988) Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol, 41, pp. 467-470.
15. Vujaskovic, Z., Anscher, MS, Feng, QF, Rabbani, ZN, Amin, K., Samulski, TS, Dewhirst, MW and Haroon, ZA. (2001) Radiation-induced hypoxia may perpetuate late normal tissue injury. Int J Radiat Oncol Biol Phys, 50, pp. 851-855.
16. Anscher, MS, Thrasher, B., Rabbani, Z., Teicher, B. and Vujaskovic, Z. (2006) Antitransforming growth factor-beta antibody 1D11 ameliorates normal tissue damage caused by high-dose radiation. Int J Radiat Oncol Biol Phys, 65, pp. 876-881.
17. Moeller, BJ, Cao, Y., Dewhirst, MW and Li, CY. (2004) Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: Role of reoxygenation, free radicals, and stress granules. Cancer Cell, 5, pp. 429-441.
18. Beckman, JS. (2001) -OONO: Rebounding from nitric oxide. Circ Res, 89, pp. 295-297.
19. Beckman, JS, Beckman, TW, Chen, J., Marshall, PA and Freeman, BA. (1990) Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA, 87, pp. 1620-1624.
20. Beckman, JS and Koppenol, WH. (1996) Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am J Physiol, 271, pp. C1424-C1437.
21. Pryor, WA and Squadrito, GL. (1995) The chemistry of peroxynitrite: A product from the reaction of nitric oxide with superoxide. Am J Physiol, 268, pp. L699-L722.
22. Zhu, X., Heunks, LM, Versteeg, EM, van der Heijden, HF, Ennen, L., van Kuppevelt, TH, Vina, J. and Dekhuijzen, PN. (2005) Hypoxia-induced dysfunction of rat diaphragm: Role of peroxynitrite. Am J Physiol Lung Cell Mol Physiol, 288, pp. L16-L26.
23. Heunks, LM, Machiels, HA, de Abreu, R., Zhu, XP, van der Heijden, HF and Dekhuijzen, PN. (2001) Free radicals in hypoxic rat diaphragm contractility: No role for xanthine oxidase. Am J Physiol Lung Cell Mol Physiol, 281, pp. L1402-L1412.
24. Mohanraj, P., Merola, AJ, Wright, VP and Clanton, TL. (1998) Antioxidants protect rat diaphragmatic muscle function under hypoxic conditions. J Appl Physiol, 84, pp. 1960-1966.
25. Cernanec, JM, Weinberg, JB, Batinic-Haberle, I., Guilak, F. and Fermor, B. (2007) Influence of oxygen tension on interleukin 1-induced peroxynitrite formation and matrix turnover in articular cartilage. J Rheumatol, 34, pp. 401-407.
26. Saba, H., Batinic-Haberle, I., Munusamy, S., Mitchell, T., Lichti, C., Megyesi, J. and MacMillan-Crow, LA. (2007) Manganese porphyrin reduces renal injury and mitochondrial damage during ischemia/reperfusion. Free Rad Biol Med, 42, pp. 1571-1578.
27. Saleh, D., Barnes, PJ and Giaid, A. (1997) Increased production of the potent oxidant peroxynitrite in the lungs of patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med, 155, pp. 1763-1769.
28. Inghilleri, S., Morbini, P., Oggionni, T., Barni, S. and Fenoglio, C. (2006) In situ assessment of oxidant and nitrogenic stress in bleomycin pulmonary fibrosis. Histochem Cell Biol, 125, pp. 661-669.
29. Worthington, J., Robson, T., Murray, M., O'Rourke, M., Keilty, G. and Hirst, DG. (2000) Modification of vascular tone using iNOS under the control of a radiation-inducible promoter. Gene Ther, 7, pp. 1126-1131.
30. Quintero, M., Brennan, PA, Thomas, GJ and Moncada, S. (2006) Nitric oxide is a factor in the stabilization of hypoxia-inducible factor-1alpha in cancer: Role of free radical formation. Cancer Res, 66, pp. 770-774.
31. Chandel, NS, Mathieu, CE, Schumacker, PT, Maltepe, E., Goldwasser, E. and Simon, MC. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA, 95, pp. 11715-11720.
32. 2 sensing. J Biol Chem, 275, pp. 25130-25138.
33. Mateo, J., García-Lecea, M., Cadenas, S., Hernández, C. and Moncada, S. (2003) Regulation of hypoxia-inducible factor-1α by nitric oxide through mitochondria-dependent and -independent pathways. Biochem J, 376, pp. 537-544.
34. Wellman, TL, Jenkins, J., Penar, PL, Tranmer, B., Zahr, R. and Lounsbury, KM. (2004) Nitric oxide and reactive oxygen species exert opposing effects on the stability of hypoxia-inducible factor-1alpha (HIF-1alpha) in explants of human pial arteries. FASEB J, 18, pp. 379-381.
35. Semenza, GL. (2002) Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol, 64, pp. 993-998.
36. Haroon, ZA, Raleigh, JA, Greenberg, CS and Dewhirst, MW. (2000) Early wound healing exhibits cytokine surge without evidence of hypoxia. Ann Surg, 231, pp. 137-147.
37. Schmidt-Ullrich, RK, Dent, P., Mikkelsen, RB, Valerie, K. and Grant, S. (2000) Signal transduction and cellular radiation responses. Radiat Res, 153, pp. 245-257.
38. Li, YQ, Ballinger, JR, Nordal, RA, Su, ZF and Wong, CS. (2001) Hypoxia in radiation-induced blood-spinal cord barrier breakdown. Cancer Res, 61, pp. 3348-3354.
39. Garg, AK and Aggarwal, BB. (2002) Reactive oxygen intermediates in TNF signaling. Molec Immunol, 39, pp. 509-517.
40. Zhang, Y. and Chen, F. (2004) Reactive oxygen species (ROS), troublemakers between nuclear factor-κB (NF-κB) and c-Jun NH2-terminal Kinase (JNK). Cancer Res, 64, pp. 1902-1905.
41. Tse, HM, Milton, MJ and Piganelli, JD. (2004) Mechanistic analysis of the immunomodulatory effects of a catalytic antioxidant on antigen-presenting cells: Implication for their use in targeting oxidation-reduction reactions in innate immunity. Free Rad Biol Med, 36, pp. 233-247.
42. Zhao, Y., Clair, D. St., Clair, W. St., Chaiswing, L., Oberley, TD, Batinic-Haberle, I. and Epstein, CJ. (2005) A mechanism-based antioxidant approach for the reduction of skin carcinogenesis. Cancer Res, 65, pp. 1401-1405.
43. Smith, KR, Uyeminami, DL, Kodavanti, UP, Crapo, JD, Chang, LY and Pinkerton, KE. (2002) Inhibition of tobacco smoke-induced lung inflammation by a catalytic antioxidant. Free Rad Biol Med, 33, pp. 1106-1114.
44. Batinic-Haberle, I. (2002) Manganese porphyrins and related compounds as mimics of superoxide dismutase. Methods Enzymol, 349, pp. 223-233.
45. Mackensen, GB, Patel, M., Sheng, H., Calvi, CL, Batinic-Haberle, I., Day, BJ, Liang, LP, Fridovich, I., Crapo, JD, Pearlstein, RD and Warner, DS. (2001) Neuroprotection from delayed postischemic administration of a metalloporphyrin catalytic antioxidant. J Neurosci, 21, pp. 4582-4592.
46. Spasojevic, I., Chen, Y., Noel, TJ, Cole, MP, Zhang, L., Zhao, Y., Clair, DK St. and Batinic-Haberle, I. (2007) Mn porphyrin-based superoxide dismutase (SOD) mimic, MnIIITE-2-PyP5+, targets mouse heart mitochondria. Free Rad Biol Med, 42, pp. 1193-1200.
47. Ferrer-Sueta, G., Hannibal, L., Batinic-Haberle, I. and Radi, R. (2006) Reduction of manganese porphyrins by flavoenzymes and submitochondrial particles: A catalytic cycle for the reduction of peroxynitrite. Free Rad Biol Med, 41, pp. 503-512.
48. Ferrer-Sueta, G., Vitturi, D., Batinic-Haberle, I., Fridovich, I., Goldstein, S., Czapski, G. and Radi, R. (2003) Reactions of manganese porphyrins with peroxynitrite and carbonate radical anion. J Biol Chem, 278, pp. 27432-27438.
49. Szabo, C., Ischiropoulos, H. and Radi, R. (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nature Rev, 6, pp. 662-680.
50. Wahl, SM, Hunt, DA, Wakefield, LM, McCartney-Francis, N., Wahl, LM, Roberts, AB and Sporn, MB. (1987) Transforming growth factor type beta induces monocyte chemotaxis and growth factor production. Proc Natl Acad Sci USA, 84, pp. 5788-5792.
51. Thannickal, VJ, Toews, GB, White, ES, Lynch 3rd, JP and Martinez, FJ. (2004) Mechanisms of pulmonary fibrosis. Ann Rev Med, 55, pp. 395-417.
52. Bellocq, A., Azoulay, E., Marullo, S., Flahault, A., Fouqueray, B., Philippe, C., Cadranel, J. and Baud, L. (1999) Reactive oxygen and nitrogen intermediates increase transforming growth factor-beta1 release from human epithelial alveolar cells through two different mechanisms. Am J Resp Cell Mol Biol, 21, pp. 128-136.
53. Barcellos-Hoff, MH and Dix, TA (1996) Redox-mediated activation of latent transforming growth factor-β1. Mol Endocrinol, 10, pp. 1077-1083.
54. Thannickal, VJ and Fanburg, BL. (1995) Activation of an H2O2-generating NADH oxidase in human lung fibroblasts by transforming growth factor beta 1. J Biol Chem, 270, pp. 30334-30338.
55. Petkau, A. (1978) Radiation protection by superoxide dismutase. Photochem Photobiol, 28, pp. 765-774.
56. Petkau, A. and Chelack, WS. (1984) Radioprotection by superoxide dismutase of macrophage progenitor cells from mouse bone marrow. Biochem Biophys Res Comm, 119, pp. 1089-1095.
57. Petkau, A., Chelack, WS and Pleskach, SD. (1978) Protection by superoxide dismutase of white blood cells in x-irradiated mice. Life Sci, 22, pp. 867-881.
58. Epperly, M., Bray, J., Kraeger, S., Greenberger, JS, Zwacka, R., Engelhardt, J. and Travis, E. (1998) Prevention of late effects of irradiation lung damage by manganese superoxide dismutase gene therapy. Gene Ther, 5, pp. 196-208.
59. Epperly, MW, Bray, JA, Krager, S., Berry, LM, Gooding, W., Greenberger, JS, Engelhardt, JF, Zwacka, R. and Travis, EL. (1999) Intratracheal injection of adenovirus containing the human MnSOD transgene protects athymic nude mice from irradiation-induced organizing alveolitis. Int J Radiat Oncol Biol Phys, 43, pp. 169-181.
60. Epperly, MW, Defilippi, S., Sikora, C., Gretton, J., Kalend, A. and Greenberger, JS. (2000) Intratracheal injection of manganese superoxide dismutase (MnSOD) plasmid/liposomes protects normal lung but not orthotopic tumors from irradiation. Gene Ther, 7, pp. 1011-1018.
61. Epperly, MW, Epstein, CJ, Travis, EL and Greenberger, JS. (2000) Decreased pulmonary radiation resistance of manganese superoxide dismutase (MnSOD)-deficient mice is corrected by human manganese superoxide dismutase-plasmid/liposome (SOD2-PL) intratracheal gene therapy. Radiat Res, 154, pp. 365-374.
62. Vujaskovic, Z., Batinic-Haberle, I., Rabbani, ZN, Feng, QF, Kang, SK, Spasojevic, I., Samulski, TV, Fridovich, I., Dewhirst, MW and Anscher, MS. (2002) A small molecular weight catalytic metalloporphyrin antioxidant with superoxide dismutase (SOD) mimetic properties protects lungs from radiation-induced injury. Free Rad Biol Med, 33, pp. 857-863.
63. Oury, TD, Thakker, K., Menache, M., Chang, LY, Crapo, JD and Day, BJ. (2001) Attenuation of bleomycin-induced pulmonary fibrosis by a catalytic antioxidant metalloporphyrin. Am J Resp Cell Mol Biol, 25, pp. 164-169.