Early and late administration of MnTE-2-PyP5+ in mitigation and treatment of radiation-induced lung damage

Free Radical Biology and Medicine

Volumn 48, Issue 8, 2010, Pages 1034-1043

  Gauter Fleckenstein, Benjamin ^a,b   Fleckenstein, Katharina ^a,b   Owzar, Kouros ^a   Jiang, Chen ^a   Rebouças, Júlio S ^a   Batinic Haberle, Ines ^a   Vujaskovic, Zeljko ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Free radicals; Lung injury; Manganese porphyrin; MnTE 2 PyP5+; Oxidative stress; Radiation; Radioprotector

Indexed keywords

8 HYDROXYGUANINE; ENDOTHELIN 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MANGANESE TETRAKIS(N ETHYLPYRIDINIUM 2 YL)PORPHYRIN; PORPHYRIN DERIVATIVE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BODY WEIGHT; BREATHING RATE; CONTROLLED STUDY; EARLY INTERVENTION; FEMALE; HISTOPATHOLOGY; LUNG INJURY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RADIATION INJURY; RADIATION PROTECTION; RAT; SIGNAL TRANSDUCTION; THERAPY DELAY;

ANIMALS; ANTIOXIDANTS; FEMALE; METALLOPORPHYRINS; RADIATION PNEUMONITIS; RADIATION-PROTECTIVE AGENTS; RATS; RATS, INBRED F344; RESPIRATION; TIME FACTORS;

ANIMALIA; RATTUS;

EID: 77950520455     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.01.020     Document Type: Article

References (85)

1. Fleckenstein K., Zgonjanin L., Chen L., Rabbani Z., Jackson I.L., Thrasher B., Kirkpatrick J., Foster W.M., Vujaskovic Z. Temporal onset of hypoxia and oxidative stress after pulmonary irradiation. Int. J. Radiat. Oncol. Biol. Phys. 2007, 68:196-204.
2. Vujaskovic Z., Anscher M.S., Feng Q.F., Rabbani Z.N., Amin K., Samulski T.S., Dewhirst M.W., Haroon Z.A. Radiation-induced hypoxia may perpetuate late normal tissue injury. Int. J. Radiat. Oncol. Biol. Phys. 2001, 50:851-855.
3. Mikkelsen R.B., Wardman P. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 2003, 22:5734-5754.
4. Leach J.K., Van Tuyle G., Lin P.S., Schmidt-Ullrich R., Mikkelsen R.B. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res. 2001, 61:3894-3901.
5. Pearce L.L., Epperly M.W., Greenberger J.S., Pitt B.R., Peterson J. Identification of respiratory complexes I and III as mitochondrial sites of damage following exposure to ionizing radiation and nitric oxide. Nitric Oxide 2001, 5:128-136.
6. Zorov D.B., Filburn C.R., Klotz L.O., Zweier J.L., Sollott S.J. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med. 2000, 192:1001-1014.
7. Li F., Sonveaux P., Rabbani Z.N., Liu S., Yan B., Huang Q., Vujaskovic Z., Dewhirst M.W., Li C.Y. Regulation of HIF-1alpha stability through S-nitrosylation. Mol. Cell 2007, 26:63-74.
8. Moeller B.J., Cao Y., Li C.Y., Dewhirst M.W. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 2004, 5:429-441.
9. Tse H.M., Milton M.J., Piganelli J.D. 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 Radic. Biol. Med. 2004, 36:233-247.
10. 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.
11. Rabbani Z.N., Batinic-Haberle I., Anscher M.S., Huang J., Day B.J., Alexander E., Dewhirst M.W., Vujaskovic Z. 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.
12. Rabbani Z.N., Salahuddin F.K., Yarmolenko P., Batinic-Haberle I., Thrasher B.A., Gauter-Fleckenstein B., Dewhirst M.W., Anscher M.S., Vujaskovic Z. Low molecular weight catalytic metalloporphyrin antioxidant AEOL 10150 protects lungs from fractionated radiation. Free Radic. Res. 2007, 41:1273-1282.
13. Vujaskovic Z., Batinic-Haberle I., Rabbani Z.N., Feng Q.F., Kang S.K., Spasojevic I., Samulski T.V., Fridovich I., Dewhirst M.W., Anscher M.S. 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.
14. Vujaskovic Z., Batinic-Haberle I., Rabbani Z.N., Spasojevic I., Samulski T.V., Fridovich I., Dewhirst M.W., Anscher M.S. Effects of metalloporphyrin catalytic antioxidant AEOL 10113 on radiation-induced lung injury. Free Radic. Biol. Med. 2002, 33:S239.
15. Moulder J.E., Cohen E.P. Future strategies for mitigation and treatment of chronic radiation-induced normal tissue injury. Semin. Radiat. Oncol. 2007, 17:141-148.
16. Zhao W., Diz D.I., Robbins M.E. Oxidative damage pathways in relation to normal tissue injury. Br. J. Radiol. 2007, 80(Spec. Issue 1):S23-S31.
17. Robbins M.E., Zhao W. Chronic oxidative stress and radiation-induced late normal tissue injury: a review. Int. J. Radiat. Biol. 2004, 80:251-259.
18. Batinic-Haberle I. Manganese porphyrins and related compounds as mimics of superoxide dismutase. Methods Enzymol. 2002, 349:223-233.
19. Batinic-Haberle I., Benov L., Spasojevic I., Fridovich I. The ortho effect makes manganese(III) meso-tetrakis(N-methylpyridinium-2-yl)porphyrin a powerful and potentially useful superoxide dismutase mimic. J. Biol. Chem. 1998, 273:24521-24528.
20. Salvemini D., Wang Z.Q., Zweier J.L., Samouilov A., Macarthur H., Misko T.P., Currie M.G., Cuzzocrea S., Sikorski J.A., Riley D.P. A nonpeptidyl mimic of superoxide dismutase with therapeutic activity in rats. Science 1999, 286:304-306.
21. Baker K., Marcus C.B., Huffman K., Kruk H., Malfroy B., Doctrow S.R. Synthetic combined superoxide dismutase/catalase mimetics are protective as a delayed treatment in a rat stroke model: a key role for reactive oxygen species in ischemic brain injury. J. Pharmacol. Exp. Ther. 1998, 284:215-221.
22. Goldstein S., Samuni A., Hideg K., Merenyi G. Structure-activity relationship of cyclic nitroxides as SOD mimics and scavengers of nitrogen dioxide and carbonate radicals. J. Phys. Chem. A 2006, 110:3679-3685.
23. Batinic-Haberle, I.; Reboucas, J. S.; Spasojevich, I. Superoxide Dismutase Mimics: Chemistry, Pharmacology and Therapeutic Potential. Antioxid. Redox. Signal. 2010 Jan 22. doi:10.1089/ars.2009.2876.
24. Murphy M.P. Targeting lipophilic cations to mitochondria. Biochim. Biophys. Acta 2008, 1777:1028-1031.
25. Munroe W., Kingsley C., Durazo A., Gralla E.B., Imlay J.A., Srinivasan C., Valentine J.S. Only one of a wide assortment of manganese-containing SOD mimicking compounds rescues the slow aerobic growth phenotypes of both Escherichia coli and Saccharomyces cerevisiae strains lacking superoxide dismutase enzymes. J. Inorg. Biochem. 2007, 101:1875-1882.
26. Pollard J.M., Reboucas J.S., Durazo A., Kos I., Fike F., Panni M., Gralla E.B., Valentine J.S., Batinic-Haberle I., Gatti R.A. Radioprotective effects of manganese-containing superoxide dismutase mimics on ataxia telangiectasia cells. Free Radic. Biol. Med. 2009, 47:250-260.
27. Langan A.R., Khan M.A., Yeung I.W., Van Dyk J., Hill R.P. Partial volume rat lung irradiation: the protective/mitigating effects of Eukarion-189, a superoxide dismutase-catalase mimetic. Radiother. Oncol. 2006, 79:231-238.
28. Lee J.H., Park J.W. A manganese porphyrin complex is a novel radiation protector. Free Radic. Biol. Med. 2004, 37:272-283.
29. 5+, targets mouse heart mitochondria. Free Radic. Biol. Med. 2007, 42:1193-1200.
30. Ferrer-Sueta G., Hannibal L., Batinic-Haberle I., Radi R. Reduction of manganese porphyrins by flavoenzymes and submitochondrial particles: a catalytic cycle for the reduction of peroxynitrite. Free Radic. Biol. Med. 2006, 41:503-512.
31. Ferrer-Sueta G., Vitturi D., Batinic-Haberle I., Fridovich I., Goldstein S., Czapski G., Radi R. Reactions of manganese porphyrins with peroxynitrite and carbonate radical anion. J. Biol. Chem. 2003, 278:27432-27438.
32. Uozaki H., Fukayama M., Nakagawa K., Ishikawa T., Misawa S., Doi M., Maekawa K. The pathology of multi-organ involvement: two autopsy cases from the Tokai-mura criticality accident. BJR Suppl. 2005, 27:13-16.
33. Baranov A.E., Selidovkin G.D., Butturini A., Gale R.P. Hematopoietic recovery after 10-Gy acute total body radiation. Blood 1994, 83:596-599.
34. Perez C.A., Bauer M., Edelstein S., Gillespie B.W., Birch R. Impact of tumor control on survival in carcinoma of the lung treated with irradiation. Int. J. Radiat. Oncol. Biol. Phys. 1986, 12:539-547.
35. Perez C.A., Stanley K., Rubin P., Kramer S., Brady L., Perez-Tamayo R., Brown G.S., Concannon J., Rotman M., Seydel H.G. A prospective randomized study of various irradiation doses and fractionation schedules in the treatment of inoperable non-oat-cell carcinoma of the lung: preliminary report by the Radiation Therapy Oncology Group. Cancer 1980, 45:2744-2753.
36. Saunders M., Dische S., Barrett A., Harvey A., Griffiths G., Palmar M. Continuous, hyperfractionated, accelerated radiotherapy (CHART) versus conventional radiotherapy in non-small cell lung cancer: mature data from the randomised multicentre trial. CHART Steering Committee. Radiother. Oncol. 1999, 52:137-148.
37. Willner J., Baier K., Caragiani E., Tschammler A., Flentje M. Dose, volume, and tumor control prediction in primary radiotherapy of non-small-cell lung cancer. Int. J. Radiat. Oncol. Biol. Phys. 2002, 52:382-389.
38. Wurschmidt F., Bunemann H., Bunemann C., Beck-Bornholdt H.P., Heilmann H.P. Inoperable non-small cell lung cancer: a retrospective analysis of 427 patients treated with high-dose radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 1994, 28:583-588.
39. Fleckenstein K., Gauter-Fleckenstein B., Jackson I.L., Rabbani Z., Anscher M., Vujaskovic Z. Using biological markers to predict risk of radiation injury. Semin. Radiat. Oncol. 2007, 17:89-98.
40. •? dismutation. J. Chem. Soc. Dalton Trans. 2002, 2689-2696.
41. Ashcroft T., Simpson J.M., Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J. Clin. Pathol. 1988, 41:467-470.
42. Hsu S.M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 1981, 29:577-580.
43. Agresti A. Categorical Data Analysis 1990, Wiley, New York.
44. Hajek J., Sidak Z., Pranab K. Theory of Rank Tests 1999, Academic Press, San Diego.
45. Pinheiro J.C., Bates D.M. Mixed-Effects Models in S and S-PLUS 2000, Springer, New York.
46. R: a Language and Environment for Statistical Computing 2007, R Development Core Team, R Foundation for Statistical Computing, Vienna.
47. Fischer-Nielsen A., Jeding I.B., Loft S. Radiation-induced formation of 8-hydroxy-2?-deoxyguanosine and its prevention by scavengers. Carcinogenesis 1994, 15:1609-1612.
48. Withers H.R., Peters L.J, Kogelnik H.S. The pathobiology of late effects in irradiation. Radiation Biology in Cancer Research 1980, 439-448. Raven Press, New York. R.E. Meyn, H.R. Withers (Eds.).
49. Bentzen S.M. Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat. Rev. Cancer 2006, 6:702-713.
50. Trott K.R., Herrmann T., Kasper M. Target cells in radiation pneumopathy. Int. J. Radiat. Oncol. Biol. Phys. 2004, 58:463-469.
51. Pena L.A., Fuks Z., Kolesnick R. Stress-induced apoptosis and the sphingomyelin pathway. Biochem. Pharmacol. 1997, 53:615-621.
52. Moosavi H., McDonald S., Rubin P., Cooper R., Stuard I.D., Penney D. Early radiation dose-response in lung: an ultrastructural study. Int. J. Radiat. Oncol. Biol. Phys. 1977, 2:921-931.
53. Travis E.L. The sequence of histological changes in mouse lungs after single doses of X-rays. Int. J. Radiat. Oncol. Biol. Phys. 1980, 6:345-347.
54. Jurmann M.J., Dammenhayn L., Schaefers H.J., Haverich A. Pulmonary reperfusion injury: evidence for oxygen-derived free radical mediated damage and effects of different free radical scavengers. Eur. J. Cardiothorac. Surg. 1990, 4:665-670.
55. Trachootham D., Lu W., Ogasawara M.A., Nilsa R.D., Huang P. Redox regulation of cell survival. Antioxid. Redox. Signaling 2008, 10:1343-1374.
56. Finkelstein J.N., Johnston C.J., Baggs R., Rubin P. Early alterations in extracellular matrix and transforming growth factor beta gene expression in mouse lung indicative of late radiation fibrosis. Int. J. Radiat. Oncol. Biol. Phys. 1994, 28:621-631.
57. Johnston C.J., Piedboeuf B., Rubin P., Williams J.P., Baggs R., Finkelstein J.N. Early and persistent alterations in the expression of interleukin-1 alpha, interleukin-1 beta and tumor necrosis factor alpha mRNA levels in fibrosis-resistant and sensitive mice after thoracic irradiation. Radiat. Res. 1996, 145:762-767.
58. Robbins M.E., Diz D.I. Pathogenic role of the renin-angiotensin system in modulating radiation-induced late effects. Int. J. Radiat. Oncol. Biol. Phys. 2006, 64:6-12.
59. Rubin P., Johnston C.J., Williams J.P., McDonald S., Finkelstein J.N. A perpetual cascade of cytokines postirradiation leads to pulmonary fibrosis. Int. J. Radiat. Oncol. Biol. Phys. 1995, 33:99-109.
60. Greenberger J.S. Radioprotection. In Vivo 2009, 23:323-336.
61. Zhao W., Robbins M.E. Inflammation and chronic oxidative stress in radiation-induced late normal tissue injury: therapeutic implications. Curr. Med. Chem. 2009, 16:130-143.
62. Cohen E.P., Fish B.L., Moulder J.E. Successful brief captopril treatment in experimental radiation nephropathy. J. Lab. Clin. Med. 1997, 129:536-547.
63. Molteni A., Moulder J.E., Cohen E.F., Ward W.F., Fish B.L., Taylor J.M., Wolfe L.F., Brizio-Molteni L., Veno P. Control of radiation-induced pneumopathy and lung fibrosis by angiotensin-converting enzyme inhibitors and an angiotensin II type 1 receptor blocker. Int. J. Radiat. Biol. 2000, 76:523-532.
64. Ward W.F., Kim Y.T., Molteni A., Solliday N.H. Radiation-induced pulmonary endothelial dysfunction in rats: modification by an inhibitor of angiotensin converting enzyme. Int. J. Radiat. Oncol. Biol. Phys. 1988, 15:135-140.
65. Ward W.F., Molteni A., Ts'ao C.H., Hinz J.M. Captopril reduces collagen and mast cell accumulation in irradiated rat lung. Int. J. Radiat. Oncol. Biol. Phys. 1990, 19:1405-1409.
66. Ward W.F., Molteni A., Ts'ao C.H., Kim Y.T., Hinz J.M. Radiation pneumotoxicity in rats: modification by inhibitors of angiotensin converting enzyme. Int. J. Radiat. Oncol. Biol. Phys. 1992, 22:623-625.
67. Delanian S., Porcher R., Rudant J., Lefaix J.L. Kinetics of response to long-term treatment combining pentoxifylline and tocopherol in patients with superficial radiation-induced fibrosis. J. Clin. Oncol. 2005, 23:8570-8579.
68. Brush J., Lipnick S.L., Phillips T., Sitko J., McDonald J.T., McBride W.H. Molecular mechanisms of late normal tissue injury. Semin. Radiat. Oncol. 2007, 17:121-130.
69. Denham J.W., Hauer-Jensen M. The radiotherapeutic injury-a complex 'wound'. Radiother. Oncol. 2002, 63:129-145.
70. Cragg P.A., Drysdale D.B. Interaction of hypoxia and hypercapnia on ventilation, tidal volume and respiratory frequency in the anaesthetized rat. J. Physiol. 1983, 341:477-493.
71. James P.E., Grinberg O.Y., Swartz H.M. Superoxide production by phagocytosing macrophages in relation to the intracellular distribution of oxygen. J. Leukocyte Biol. 1998, 64:78-84.
72. 2 in phagocyte-induced hypermetabolism and pulmonary injury. J. Appl. Physiol. 1995, 78:112-116.
73. Jacono F.J., Peng Y.J., Nethery D., Faress J.A., Lee Z., Kern J.A., Prabhakar N.R. Acute lung injury augments hypoxic ventilatory response in the absence of systemic hypoxemia. J. Appl. Physiol. 2006, 101:1795-1802.
74. Wang X., Wang B.R., Duan X.L., Zhang P., Ding Y.Q., Jia Y., Jiao X.Y., Ju G. Strong expression of interleukin-1 receptor type I in the rat carotid body. J. Histochem. Cytochem. 2002, 50:1677-1684.
75. Wang X., Zhang X.J., Xu Z., Li X., Li G.L., Ju G., Wang B.R. Morphological evidence for existence of IL-6 receptor alpha in the glomus cells of rat carotid body. Anat. Rec. A Discoveries Mol. Cell. Evol. Biol. 2006, 288:292-296.
76. Agapito M.T., Sanz-Alfayate G., Gomez-Nino A., Gonzalez C., Obeso A. General redox environment and carotid body chemoreceptor function. Am. J. Physiol. Cell Physiol. 2009, 296:C620-631.
77. Csont T., Viappiani S., Sawicka J., Slee S., Altarejos J.Y., Batinic-Haberle I., Schulz R. The involvement of superoxide and iNOS-derived NO in cardiac dysfunction induced by pro-inflammatory cytokines. J. Mol. Cell. Cardiol. 2005, 39:833-840.
78. Piganelli J.D., Flores S.C., Cruz C., Koepp J., Batinic-Haberle I., Crapo J., Day B., Kachadourian R., Young R., Bradley B., Haskins K. A metalloporphyrin-based superoxide dismutase mimic inhibits adoptive transfer of autoimmune diabetes by a diabetogenic T-cell clone. Diabetes 2002, 51:347-355.
79. •?, TGF-beta, and VEGF production by macrophages. Free Radic. Res. 2007, 41:8-14.
80. 5+, in plasma and major organs of B6C3F1 mice. Free Radic. Biol. Med. 2008, 45:943-949.
81. Moeller B.J., Batinic-Haberle I., Spasojevic I., Rabbani Z.N., Anscher M.S., Vujaskovic Z., Dewhirst M.W. A manganese porphyrin superoxide dismutase mimetic enhances tumor radioresponsiveness. Int. J. Radiat. Oncol. Biol. Phys. 2005, 63:545-552.
82. Ye X., Fels D., Dedeugd C., Dewhirst M.W., Leong K., Batinic-Haberle I. The in vitro cytotoxic effects of Mn(III) alkylpyridylporphyrin/ascorbate system on four tumor cell lines. Free Radic. Biol. Med. 2009, 47(Spec. Issue 1):136-158.
83. 5+, via suppression of oxidative stress in a mouse model of breast tumor. Free Radic. Biol. Med. 2009, 47:992-1004.
84. Jaramillo M.C., Frye J.B., Crapo J.D., Briehl M.M., Tome M.E. Increased manganese superoxide dismutase expression or treatment with manganese porphyrin potentiates dexamethasone-induced apoptosis in lymphoma cells. Cancer Res. 2009, 69:5450-5457.
85. Zhao Y., Chaiswing L., Oberley T.D., Batinic-Haberle I., St Clair W., Epstein C.J., St Clair D. A mechanism-based antioxidant approach for the reduction of skin carcinogenesis. Cancer Res. 2005, 65:1401-1405.