Neuroprotective efficacy from a lipophilic redox-modulating Mn(III) N-hexylpyridylporphyrin, MnTnHex-2-PyP: Rodent models of ischemic stroke and subarachnoid hemorrhage

Journal of Pharmacology and Experimental Therapeutics

Volumn 338, Issue 3, 2011, Pages 906-916

  Sheng, Huaxin ^a   Spasojevic, Ivan ^a   Tse, Hubert M ^b   Jung, Jin Yong ^a   Hong, Jun ^c   Zhang, Zhiquan ^a   Piganelli, Jon D ^b   Batinic Haberle, Ines ^a   Warner, David S ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c Tangshan Gongren Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MANGANESE MESO TETRAKIS(N HEXYLPYRIDINIUM 2 YL)PORPHYRIN; NEUROPROTECTIVE AGENT; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CEREBRAL ARTERY; ARTICLE; BRAIN FUNCTION; BRAIN INFARCTION SIZE; BRAIN INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; DNA BINDING; DRUG ACCUMULATION; DRUG BRAIN LEVEL; DRUG EFFICACY; INTERNAL CAROTID ARTERY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUBARACHNOID HEMORRHAGE; VASOCONSTRICTION;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CYTOKINES; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; INFARCTION, MIDDLE CEREBRAL ARTERY; INTERLEUKIN-6; LASER-DOPPLER FLOWMETRY; MALE; METALLOPORPHYRINS; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; NF-KAPPA B; RATS; RATS, WISTAR; REPERFUSION INJURY; STROKE; STRUCTURE-ACTIVITY RELATIONSHIP; SUBARACHNOID HEMORRHAGE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80051669546     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.110.176701     Document Type: Article

References (52)

1. Aladag MA, Turkoz Y, Sahna E, Parlakpinar H, and Gul M (2003) The attenuation of vasospasm by using a sod mimetic after experimental subarachnoidal haemorrhage in rats. Acta Neurochir (Wien) 145:673-677. (Pubitemid 37094011)
2. Alvarez B, Demicheli V, Durán R, Trujillo M, Cerveñansky C, Freeman BA, and Radi R (2004) Inactivation of human Cu,Zn superoxide dismutase by peroxynitrite and formation of histidinyl radical. Free Radic Biol Med 37:813-822. (Pubitemid 39078553)
3. 5+) a powerful and potentially useful superoxide dismutase mimic. J Biol Chem 273:24521-24528.
4. Batinić-Haberle I, Cuzzocrea S, Rebouças JS, Ferrer-Sueta G, Mazzon E, Di Paola R, Radi R, Spasojević I, Benov L, and Salvemini D (2009a) Pure MnTBAP selectively scavenges peroxynitrite over superoxide: comparison of pure and commercial MnTBAP samples to MnTE-2-PyP in two models of oxidative stress injury, an SOD-specific Escherichia coli model and carrageenan-induced pleurisy. Free Radic Biol Med 46:192-201.
5. Batinić-Haberle I, Ndengele MM, Cuzzocrea S, Rebouças JS, Spasojević I, and Salvemini D (2009b) Lipophilicity is a critical parameter that dominates the efficacy of metalloporphyrins in blocking the development of morphine antinociceptive tolerance through peroxynitrite-mediated pathways. Free Radic Biol Med 46:212-219.
6. Batinić-Haberle I, Rajic Z, Tovmasyan A, Reboucas JS, Ye X, Leong KW, Dewhirst MW, Vujaskovic Z, Benov L, and Spasojevic I (2011a) Diverse functions of cationic Mn(III) substituted N-pyridylporphyrins, known as SOD mimics. Free Radic Biol Med doi:10.1016/j.freeradbiomed.2011.04.046.
7. Batinić-Haberle I, Reboucas JS, Benov L, and Spasojevic I (2011b) Chemistry, biology and medical effects of water soluble metallopophyrins, in Handbook of Porphyrin Science (Kadish KM, Smith K, Guillard R eds) pp 291-393, World Scientific, Singapore.
8. Batinić-Haberle I, Rebouças JS, and Spasojević I (2010a) Superoxide dismutase mimics: chemistry, pharmacology, and therapeutic potential. Antioxid Redox Signal 13:877-918.
9. .-. dismutation. J Chem Soc Dalton Trans 2689-2696.
10. .- dismutation. Mn(III) ortho-methoxyethylpyridyl- and di-ortho-methoxyethylimidazolylporphyrins. Dalton Trans 1696-1702.
11. Batinic-Haberle I, Spasojevic I, Tse HM, Tovmasyan A, Rajic Z, St Clair DK, Vujaskovic Z, Dewhirst MW and Piganelli JD (2010b) Design of Mn porphyrins for treating oxidative stress injuries and their redox-based regulation of cellular transcriptional activities. Amino Acids doi:10.1007/s00726-010-0603-6.
12. DeFreitas-Silva G, Rebouças JS, Spasojević I, Benov L, Idemori YM, and Batinić-Haberle I (2008) SOD-like activity of Mn(II) β-octabromo-meso-tetrakis(N-methylpyridinium-3-yl)porphyrin equals that of the enzyme itself. Arch Biochem Biophys 477:105-112.
13. Dogan S, Unal M, Ozturk N, Yargicoglu P, Spasojevic I, Batinc-Haberle I, and Aslan M (2011) Manganese porphyrin reduces retinal injury induced by ocular hypertension. Exp Eye Res doi:10.1016/j.exer.2011.05.008.
14. Goldstein S, Fridovich I, and Czapski G (2006) Kinetic properties of Cu,Zn-superoxide dismutase as a function of metal content-order restored. Free Radic Biol Med 41:937-941. (Pubitemid 44247545)
15. Hall ED, Pazara KE, Braughler JM, Linseman KL, and Jacobsen EJ (1990) Nonsteroidal lazaroid U78517F in models of focal and global ischemia. Stroke 21:III83-III87.
16. Jaramillo MD, Briejl MM, and Tome ME (2010) Manganese porphyrin glutathionylates the p65 subunit of NF-κB to potentiate glucocorticoid-induced apoptosis in lymphoma. Free Radic Biol Med 49:S63.
17. Kamii H, Kato I, Kinouchi H, Chan PH, Epstein CJ, Akabane A, Okamoto H, and Yoshimoto T (1999) Amelioration of vasospasm after subarachnoid hemorrhage in transgenic mice overexpressing CuZn-superoxide dismutase. Stroke 30:867-871; discussion 872.
18. Kos I, Rebouças JS, DeFreitas-Silva G, Salvemini D, Vujaskovic Z, Dewhirst MW, Spasojević I, and Batinić-Haberle I (2009) Lipophilicity of potent porphyrin-based antioxidants: comparison of ortho and meta isomers of Mn(III) N- alkylpyridylporphyrins. Free Radic Biol Med 47:72-78.
19. Kramer AH and Fletcher JJ (2010) Statins in the management of patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Neurocrit Care 12:285-296.
20. Liang LP, Huang J, Fulton R, Day BJ, and Patel M (2007) An orally active catalytic metalloporphyrin protects against 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine neurotoxicity in vivo. J Neurosci 27:4326-4333. (Pubitemid 46640723)
21. Longa EZ, Weinstein PR, Carlson S, and Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84-91. (Pubitemid 19040218)
22. Mackensen GB, Patel M, Sheng H, Calvi CL, Batinic-Haberle I, Day BJ, Liang LP, Fridovich I, Crapo JD, Pearlstein RD, et al. (2001) Neuroprotection from delayed postischemic administration of a metalloporphyrin catalytic antioxidant. J Neurosci 21:4582-4592. (Pubitemid 32565617)
23. Marshall JW, Duffin KJ, Green AR, and Ridley RM (2003) NXY-059, a free radical-trapping agent, substantially lessens the functional disability resulting from cerebral ischemia in a primate species. Stroke 32:190-198. (Pubitemid 32063845)
24. McGirt MJ, Lynch JR, Parra A, Sheng H, Pearlstein RD, Laskowitz DT, Pelligrino DA, and Warner DS (2002) Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke 33:2950-2956. (Pubitemid 35462871)
25. Niizuma K, Endo H, and Chan PH (2009) Oxidative stress and mitochondrial dysfunction as determinants of ischemic neuronal death and survival. J Neurochem 109(Suppl 1):133-138.
26. Parra A, McGirt MJ, Sheng H, Laskowitz DT, Pearlstein RD, and Warner DS (2002) Mouse model of subarachnoid hemorrhage associated cerebral vasospasm: methodological analysis. Neurol Res 24:510-516. (Pubitemid 34742689)
27. Pollard JM, Reboucas JS, Durazo A, Kos I, Fike F, Panni M, Gralla EB, Valentine JS, Batinic-Haberle I, and Gatti RA (2009) Radioprotective effects of manganese-containing superoxide dismutase mimics on ataxia-telangiectasia cells. Free Radic Biol Med 47:250-260.
28. Rebouças JS, Spasojević I, and Batinić-Haberle I (2008) Quality of potent Mn porphyrin-based SOD mimics and peroxynitrite scavengers for pre-clinical mechanistic/therapeutic purposes. J Pharm Biomed Anal 48:1046-1049.
29. Ross AD, Sheng H, Warner DS, Piantadosi CA, Batinic-Haberle I, Day BJ, and Crapo JD (2002) Hemodynamic effects of metalloporphyrin catalytic antioxidants: structure-activity relationships and species specificity. Free Radic Biol Med 33:1657-1669. (Pubitemid 35462006)
30. 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 Radic Biol Med 42:1571-1578. (Pubitemid 46591998)
31. Sakai H, Sheng H, Yates RB, Ishida K, Pearlstein RD, and Warner DS (2007) Isoflurane provides long-term protection against focal cerebral ischemia in the rat. Anesthesiology 106:92-99; discussion 98-110.
32. Sheng H, Batinc-Haberle I, and Warner DS (2002a) Catalytic antioxidants as novel pharmacologic approaches to treatment of ischemic brain injury. Drug News Perspect 15:654-665. (Pubitemid 36152054)
33. Sheng H, Enghild JJ, Bowler R, Patel M, Batinić-Haberle I, Calvi CL, Day BJ, Pearlstein RD, Crapo JD, and Warner DS (2002b) Effects of metalloporphyrin catalytic antioxidants in experimental brain ischemia. Free Radic Biol Med 33:947-961. (Pubitemid 35284033)
34. Sheng H, Reynolds JD, Auten RL, Demchenko IT, Piantadosi CA, Stamler JS, and Warner DS (2011) Pharmacologically augmented S-nitrosylated hemoglobin improves recovery from murine subarachnoid hemorrhage. Stroke 42:471-476.
35. Sheng H, Yang W, Fukuda S, Tse HM, Paschen W, Johnson K, Batinic-Haberle I, Crapo JD, Pearlstein RD, Piganelli J, et al. (2009) Long-term neuroprotection from a potent redox-modulating metalloporphyrin in the rat. Free Radic Biol Med 47:917-923.
36. Shuaib A, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, Diener HC, Ashwood T, Wasiewski WW, Emeribe U, et al. (2007) NXY-059 for the treatment of acute ischemic stroke. N Engl J Med 357:562-571. (Pubitemid 47236281)
37. Spasojevic I, Batinic-Haberle I, and Fridovich I (2000) Nitrosylation of manganese(II) tetrakis(N-ethylpyridinium-2-yl)porphyrin: a simple and sensitive spectrophotometric assay for nitric oxide. Nitric Oxide 4:526-533.
38. Spasojević I, Chen Y, Noel TJ, Fan P, Zhang L, Rebouças JS, St Clair DK, and Batinić-Haberle I (2008a) Pharmacokinetics of the potent redox-modulating manganese porphyrin, MnTE-2-PyP(5+), in plasma and major organs of B6C3F1 mice. Free Radic Biol Med 45:943-949.
39. Spasojević I, Chen Y, Noel TJ, Yu Y, Cole MP, Zhang L, Zhao Y, St Clair DK, and Batinić-Haberle I (2007) Mn porphyrin-based superoxide dismutase (SOD) mimic, MnIIITE-2-PyP5+, targets mouse heart mitochondria. Free Radic Biol Med 42:1193-1200.
40. Spasojevic I, Kos I, Benov LT, Rajic Z, Fels D, Dedeugd C, Ye X, Vujaskovic Z, Reboucas JS, Leong KW, et al. (2011) Bioavailability of metalloporphyrin-based SOD mimics is greatly influenced by a single charge residing on a Mn site. Free Radic Res 45:188-200.
41. Spasojevic I, Sheng H, Warner DS, and Batinic-Haberle I (2008b) Metalloporphyrins are versatile and powerful therapeutics: biometrics of SOD, peroxyredoxin, and P450, at the Second World Conference on Magic Bullets (Ehrlich II); 2008 Oct 3-5; Nurnberg, Germany.
42. Spasojevic I, Tovmasyan A, Rajic Z, Salvemini D, St. Clair D, Valentine JS, Vujaskovic Z, Gralla EB and Batinic-Haberle I (2010) Accumulation of porphyrin-based SOD mimics in mitochondria is proportional to their lipophilicity. S. cerevisiae study of ortho Mn(III) N- alkylpyridylporphyrins. Free Radic Biol Med 49:S199.
43. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, and Sharp FR (1990) A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10:290-293. (Pubitemid 20096202)
44. The RANTTAS Investigators (1996) A randomized trial of tirilazad mesylate in patients with acute stroke (RANTTAS). Stroke 27:1453-1458.
45. Trujillo M, Clippe A, Manta B, Ferrer-Sueta G, Smeets A, Declercq JP, Knoops B, and Radi R (2007) Pre-steady state kinetic characterization of human peroxiredoxin 5: taking advantage of Trp84 fluorescence increase upon oxidation. Arch Biochem Biophys 467:95-106. (Pubitemid 47625297)
46. 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 Radic Biol Med 36:233-247. (Pubitemid 38117241)
47. Vance CK and Miller AF (1998) A simple proposal that can explain the inactivity of metal-substituted superoxide dismutases. J Am Chem Soc 120:461-467. (Pubitemid 28067812)
48. Warner DS, Ludwig PS, Pearlstein R, and Brinkhous AD (1995) Halothane reduces focal ischemic injury in the rat when brain temperature is controlled. Anesthesiology 82:1237-1245; discussion 27A.
49. Warner DS, Sheng H, and Batinić-Haberle I (2004) Oxidants, antioxidants and the ischemic brain. J Exp Biol 207:3221-3231. (Pubitemid 39275296)
50. Yokoo N, Sheng H, Mixco J, Homi HM, Pearlstein RD, and Warner DS (2004) Intraischemic nitrous oxide alters neither neurologic nor histologic outcome: a comparison with dizocilpine. Anesth Analg 99:896-903, table of contents. (Pubitemid 39100386)
51. Zhang H, Joseph J, Gurney M, Becker D, and Kalyanaraman B (2002) Bicarbonate enhances peroxidase activity of Cu,Zn-superoxide dismutase. Role of carbonate anion radical and scavenging of carbonate anion radical by metalloporphyrin antioxidant enzyme mimetics. J Biol Chem 277:1013-1020. (Pubitemid 34968846)
52. Zhou ML, Shi JX, Hang CH, Cheng HL, Qi XP, Mao L, Chen KF, and Yin HX (2007) Potential contribution of nuclear factor-κB to cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits. J Cereb Blood Flow Metab 27:1583-1592. (Pubitemid 47301442)