Metalloporphyrin antioxidants ameliorate normal tissue radiation damage in rat brain

International Journal of Radiation Biology

Volumn 86, Issue 2, 2010, Pages 145-163

  Pearlstein, Robert D ^a,b   Higuchi, Yoshinori ^b,c   Moldovan, Maria ^b   Johnson, Kwame ^a   Fukuda, Shiro ^a   Gridley, Daila S ^b   Crapo, James D ^d   Warner, David S ^a   Slater, James M ^b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

Antioxidant; Normal tissue complication probability; Pre conditioning; Radioprotection

Indexed keywords

ANTIOXIDANT; HEME OXYGENASE 1; MANGANESE MESO TETRAKIS (DIETHYL 2-5 IMIDAZOLE) PORPHYRIN; METALLOPORPHYRIN; RADIOPROTECTIVE AGENT; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTOMA CELL; BLOOD BRAIN BARRIER; CELL CULTURE; CELL SURVIVAL; CLONOGENESIS; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; ENDOTHELIUM CELL; ENZYME ACTIVITY; GLIOMA CELL; HEMISPHERE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LATERAL BRAIN VENTRICLE; MALE; MOLECULAR WEIGHT; NERVOUS TISSUE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN EXPRESSION; RADIATION DOSE; RADIATION INJURY; RADIATION NECROSIS; RADIOSENSITIVITY; RAT; TUMOR CELL; UPREGULATION;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN INJURIES; CELL LINE, TUMOR; CELLS, CULTURED; DNA BREAKS, DOUBLE-STRANDED; HEME OXYGENASE (DECYCLIZING); HUMANS; MALE; METALLOPORPHYRINS; NEUROGLIA; NEURONS; RADIATION INJURIES, EXPERIMENTAL; RADIATION TOLERANCE; RADIATION-PROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE;

RATTUS;

EID: 77249094039     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.3109/09553000903419965     Document Type: Article

References (56)

1. Abbasoglu SD, Erbil Y, Eren T, Giris M, Barbaros U, Yucel R, Olgac V, Uysal M, Toker G. 2006. The effect of heme oxygenase-1 induction by octreotide on radiation enteritis. Peptides 27:1570-1576.
2. Ahmad AS, Zhuang H, Dore S. 2006. Heme oxygenase-1 protects brain from acute excitotoxicity. Neuroscience 141:1703-1708.
3. Alam J, Shibahara S, Smith A. 1989. Transcriptional activation of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. Journal Biological Chemistry 264: 6371-6375
4. Batinic-Haberle I. 2002. Manganese porphyrins and related compounds as mimics of superoxide dismutase. Methods Enzymology 349:223-233.
5. Bauer M, Bauer I. 2002. Heme oxygenase-1: Redox regulation and role in the hepatic response to oxidative stress. Antioxidants and Redox Signaling 4:749-758.
6. Berberat PO, Dambrauskas Z, Gulbinas A, Giese T, Giese N, Kunzli B, Autschbach F, Meuer S, Buchler MW, Friess H. 2005. Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clinical Cancer Research 11:3790-3798.
7. Burger PC, Mahaley MS, Dudka L, Vogel FS. 1979. The morphologic effects of radiation administered therapeutically for intracranial gliomas. Cancer 44:1256-1272.
8. Camphausen K, Citrin D, Krishna MC, Mitchell JB. 2005. Implications for tumor control during protection of normal tissues with antioxidants. Journal Clinical Oncology 23: 5455-5457.
9. Chen K, Gunter K, Maines MD. 2000. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. Journal Neurochemistry 75:304-313.
10. Choi AM, Alam J. 1996. Heme oxygenase-1: Function, regulation, and implication of a novel stress-inducible protein in oxidantinduced lung injury. American Journal Respiratory Cell Molecular Biology 15:9-19.
11. Datta PK, Moulder JE, Fish BL, Cohen EP, Lianos EA. 2001. Induction of heme oxygenase 1 in radiation nephropathy: Role of angiotensin II. Radiation Research 155:734-739.
12. DeGraff WG, Krishna MC, Kaufman D, Mitchell JB. 1992. Nitroxide-mediated protection against X-ray-and neocarzinostatin-induced DNA damage. Free Radical Biology & Medicine 13:479-487.
13. Emerson MR, Samson FE, Pazdernik TL. 2000. Effects of hypoxia preconditioning on expression of metallothionein-1,2 and heme oxygenase-1 before and after kainic acid-induced seizures. Cell Molecular Biology (Noisy-le-grand) 46:619-626.
14. Ewing P, Wilke A, Eissner G, Holler E, Andreesen R, Gerbitz A. 2005. Expression of heme oxygenase-1 protects endothelial cells from irradiation-induced apoptosis. Endothelium 12: 113-119.
15. Giris M, Erbil Y, Oztezcan S, Olgac V, Barbaros U, Deveci U, Kirgiz B, Uysal M, Toker GA. 2006. The effect of heme oxygenase-1 induction by glutamine on radiation-induced intestinal damage: The effect of heme oxygenase-1 on radiation enteritis. American Journal Surgery 191:503-509.
16. Gray B, Carmichael AJ. 1992. Kinetics of superoxide scavenging by dismutase enzymes and manganese mimics determined by electron spin resonance. Biochemistry Journal 281:795-802.
17. Guo X, Shin VY, Cho CH. 2001. Modulation of heme oxygenase in tissue injury and its implication in protection against gastrointestinal diseases. Life Science 69:3113-3119.
18. Kennedy AS, Archambeau JO, Archambeau MH, Holshouser B, Thomas J, Moyers M, Hinshaw D Jr, Slater JM. 2005. Magnetic resonance imaging as a monitor of changes in the irradiated rat brain. An aid to determining the time course of events in a histologic study. Investigational Radiology 30:214-220.
19. Jirak D, Namestkova K, Herynek V, Liscak R, Vymazal J, Mares V, Sykova E, Hajek M. 2007. Lesion evolution after gamma knife irradiation observed by magnetic resonance imaging. International Journal Radiation Biololgy 83:237-244.
20. Kondziolka D, Lunsford D, Classen D, Maitz AH, Flickinger JC. 1992. Radiobiology of radiosurgery: Part I. The normal rat brain model. Neurosurgery 31:271-279.
21. Lee BI, Chan PH, Kim GW. 2005a. Metalloporphyrin-based superoxide dismutase mimic attenuates the nuclear translocation of apoptosis-inducing factor and the subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. Stroke 36:2712-2717.
22. Lee JH, Lee YM, Park JW. 2005b. Regulation of ionizing radiationinduced apoptosis by a manganese porphyrin complex. Biochemical and Biophysical Research Communications 334: 298-305.
23. Lee JH, Park JW. 2004. A manganese porphyrin complex is a novel radiation protector. Free Radical Biology &Medicine 37: 272-283.
24. Li YQ, Chen P, Haimovitz-Friedman A, Reilly RM, Wong CS. 2003. Endothelial apoptosis initiates acute blood-brain barrier disruption after ionizing radiation. Cancer Research 63: 5950-5956.
25. Liang LP, Huang J, Fulton R, Day BJ, Patel M. 2007. An orally active catalytic metalloporphyrin protects against 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine neurotoxicity in vivo. Journal Neuroscience 27:4326-4333.
26. Luo X, Kim DW, Crapo JD, Pearlstein R, Slater JM, Gridley DS. 2005. Differential modification of tumor and normal cell response to radiation by a metalloporphyrin antioxidant. 52nd Annual Meeting of the Radiation Research Society. Denver, CO, USA.
27. Mackensen GB, Patel M, Sheng H, Calvi CL, Batinic-Haberle I, Day BJ, Liang LP, Fridovich I, Crapo JD, Pearlstein RD, Warner DS. 2001. Neuroprotection from delayed postischemic administration of a metalloporphyrin catalytic antioxidant. Journal Neuroscience 21:4582-4592.
28. Makinde AY, Luo-Owen X, Rizvi A, Crapo JD, Pearlstein RD, Slater JM, Gridley DS. 2009. Effect of a metalloporphyrin antioxidant (Mn TE-2-PyP) on the response of a mouse prostate tumor model to radiation. Anticancer Research 29: 139-150.
29. Mitchell JB, DeGraff W, Kaufman D, Krishna MC, Samuni A, Finkelstein E, Ahn MS, Hahn SM, Gamson J, Russo A. 1991. Inhibition of oxygen-dependent radiation-induced damage by the nitroxide superoxide dismutase mimic, tempol. Archives of Biochemistry and Biophysics 289:62-70.
30. Moeller BJ, Batinic-Haberle I, Spasojevic I, Rabbani ZN, Anscher MS, Vujaskovic Z, Dewhirst MW. 2005. A manganese porphyrin superoxide dismutase mimetic enhances tumor radioresponsiveness. International Journal of Radiation Oncology Biology Physics 63:545-552.
31. Orrell RW. 2006. AEOL-10150 (Aeolus). Current Opinions Investigational Drugs 7:70-80.
32. Panahian N, Yoshiura M, Maines MD. 1999. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. Journal Neurochemistry 72:1187-1203.
33. Paris F, Foks Z, Kang A, Capodieci P, Juan G, Ehleiter D, Haimovitz-Friedman A, Cordon-Cardo C, Kolesnick R. 2001 Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 293:293-297.
34. Park SH, Hwang SK, Kang DH, Lee SH, Park J, Hwang JH, Hamm IS, Park YM. 2008. Gamma knife radiosurgery for multiple brain metastases from lung cancer. Journal of Clinical Neuroscience 16:626-629.
35. Patel M. 1998. Inhibition of neuronal apoptosis by a metalloporphyrin superoxide dismutase mimic. Journal Neurochemistry 71:1068-1074.
36. Pearlstein RD, Beirne JP, Massey GW, Warner DS. 1998. Neuroprotective effects of NMDA receptor glycine recognition site antagonism: Dependence on glycine concentration. Neurochemistry 70:2012-2019.
37. Pouratian N, Crowley RW, Sherman JH, Jagannathan J, Sheehan JP. 2009. Gamma Knife radiosurgery after radiation therapy as an adjunctive treatment for glioblastoma. Journal of Neurooncology 94:409-418.
38. Rabbani ZN, Batinic-Haberle I, Anscher MS, Huang J, Day BJ, Alexander E, Dewhirst MW, Vujaskovic Z. 2007. Long-term administration of a small molecular weight catalytic metalloporphyrin antioxidant, AEOL 10150, protects lungs from radiation-induced injury. International Journal of Radiation Oncology Biology Physics 67:573-580. (Pubitemid 46108330)
39. Rajesh A, Sagar R, Singh S, Kumar R, Sharma AK, Prasad J, Singh S, Gupta M, Sharma RK, Puri SC, Krishna B, Siddiqui MS, Lahiri SS, Tripathi RP, Qazi GN. 2007. Cytoprotective effect of Podophyllum hexandrum against gamma radiation is mediated via hemopoietic system stimulation and up-regulation of heme-oxygenase-1 and the prosurvival multidomain protein Bcl-2. Integrated Cancer Therapies 6: 54-65.
40. Risom L, Moller P, Vogel U, Kristjansen PE, Loft S. 2003. X-rayinduced oxidative stress: DNA damage and gene expression of HO-1, ERCC1 and OGG1 in mouse lung. Free Radical Research 37:957-966.
41. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. Journal of Biological Chemistry 273:5858-5868.
42. Ryter SW, Choi AM. 2002. Heme oxygenase-1: Molecular mechanisms of gene expression in oxygen-related stress. Antioxidants and Redox Signaling 4:625-632.
43. Salvemini D, Riley DP, Cuzzocrea S. 2002. SOD mimetics are coming of age. Nature Review Drug Discovery 1:367-374.
44. Sasaki H, Lin LR, Yokoyama T, Sevilla MD, Reddy VN, Giblin FJ. 1998. TEMPOL protects against lens DNA strand breaks and cataract in the X-rayed rabbit. Investigational Ophthalmology and Visual Sciences 39:544-552.
45. Schaaf GJ, Maas RF, de Groene EM, Fink-Gremmels J. 2002. Management of oxidative stress by heme oxygenase-1 in cisplatin-induced toxicity in renal tubular cells. Free Radical Research 36:835-843.
46. Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM. 2002. Quantitative detection of (125)IdU-induced DNA doublestrand breaks with gamma-H2AX antibody. Radiation Research 158:486-492.
47. Sheng H, Enghild JJ, Bowler R, Patel M, Batinic-Haberle I, Calvi CL, Day BJ, Pearlstein RD, Crapo JD, Warner DS. 2002. Effects of metalloporphyrin catalytic antioxidants in experimental brain ischemia. Free Radicals in Biology and Medicine 33:947-961.
48. Shimizu H, Takahashi T, Suzuki T, Yamasaki A, Fujiwara T, Odaka Y, Hirakawa M, Fujita H, Akagi R. 2000. Protective effect of heme oxygenase induction in ischemic acute renal failure. Critical Care Medicine 28:809-817.
49. Shinohara C, Gobbel GT, Lamborn KR, Tada E, Fike JR. 1997. Apoptosis in the subendma of young adult rats after single and fractionated doses of X-rays. Cancer Research 57:2694-2702.
50. Speit G, Dennog C, Eichhorn U, Rothfuss A, Kaina B. 2000. Induction of heme oxygenase-1 and adaptive protection against the induction of DNA damage after hyperbaric oxygen treatment. Carcinogenesis 21:1795-1799.
51. Takahashi T, Morita K, Akagi R, Sassa S. 2004. Heme oxygenase-1: A novel therapeutic target in oxidative tissue injuries. Current Medicine Chemistry 11:1545-1561.
52. Tofilon PJ, Fike JR. 2000. The radioresponse of the central nervous system: A dynamic process. Radiation Research 153: 357-370.
53. Tse HM, Milton MJ, 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 Radical Biology & Medicine 36:233-247.
54. Vujaskovic Z, Batinic-Haberle I, Rabbani ZN, Feng QF, Kang SK, Spasojevic I, Samulski TV, Fridovich I, Dewhirst MW, Anscher MS. 2002. A small molecular weight catalytic metalloporphyrin antioxidant with superoxide dismutase (SOD) mimetic properties protects lungs from radiation-induced injury. Free Radical Biology & Medicine 33:857-863.
55. Yao P, Nussler A, Liu L, Hao L, Song F, Schirmeier A, Nussler N. 2007. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. Journal of Hepatology 47: 253-261.
56. Yokoyama S, Mita S, Okabe A, Abe M, Ogawa M. 2001. Prediction of radiosensitivity in human esophageal squamous cell carcinomas with heme oxygenase-1: A clinicopathological and immunohistochemical study. Oncology Reports 8: 355-358.