Impact of electrostatics in redox modulation of oxidative stress by Mn porphyrins: Protection of SOD-deficient Escherichia coli via alternative mechanism where Mn porphyrin acts as a Mn carrier

Free Radical Biology and Medicine

Volumn 45, Issue 2, 2008, Pages 201-210

  Rebouças, Júlio S ^a   DeFreitas Silva, Gilson ^b   Spasojević, Ivan ^a   Idemori, Ynara M ^b   Benov, Ludmil ^c   Batinić Haberle, Ines ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c KUWAIT UNIVERSITY   (Kuwait)

Author keywords

Electrostatics; Escherichia coli; Mn porphyrins; Mn transport; Redox modulators; SOD mimics

Indexed keywords

MANGANESE; MANGANESE MESO TETRAKIS(4 CARBOXYLATOPHENYL)PROPHYRIN; MANGANESE MESO TETRAKIS(4 SULFONATOPHENYL)PROPHYRIN; PORPHYRIN; SUPEROXIDE DISMUTASE;

ARTICLE; ELECTRICITY; ESCHERICHIA COLI; OXIDATIVE STRESS; PRIORITY JOURNAL; ULTRAVIOLET RADIATION;

ANIMALS; BIOMIMETICS; FREE RADICAL SCAVENGERS; MANGANESE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PORPHYRINS; STATIC ELECTRICITY; STRUCTURE-ACTIVITY RELATIONSHIP; SUPEROXIDE DISMUTASE;

ESCHERICHIA COLI;

EID: 44649184942     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.04.009     Document Type: Article

References (59)

1. Batinić-Haberle I., Benov L., Spasojević I., Hambright P., Crumbliss A.L., and Fridovich I. The relationship between redox potentials, proton dissociation constants of pyrrolic nitrogens, and in vitro and in vivo superoxide dismutase activities of manganese(III) and iron(III) cationic and anionic porphyrins. Inorg. Chem. 38 (1999) 4011-4022
2. {radical dot}- dismutation. Mn(III) methoxyethylpyridyl- and methoxyethylimidazolylporphyrins. J. Chem. Soc., Dalton Trans. (2004) 1696-1702
3. {radical dot}- dismutation. J. Chem. Soc., Dalton Trans. (2002) 2689-2696
4. Batinić-Haberle I., Spasojević I., Stevens R.D., Bondurant B., Okado-Matsumoto A., Fridovich I., Vujasković Ž., and Dewhirst M.W. New PEG-ylated Mn(III) porphyrins approaching catalytic activity of SOD enzyme. Dalton Trans. (2006) 617-624
5. {radical dot}- dismutation by superoxide dismutase mimics. J. Biol. Chem. 278 (2003) 6831-6837
6. Ferrer-Sueta G., Vitturi D., Batinić-Haberle I., Fridovich I., Goldstein S., Czapski G., and Radi R. Reactions of manganese porphyrins with peroxynitrite and carbonate radical anion. J. Biol. Chem. 278 (2003) 27432-27438
7. Ferrer-Sueta G., Batinić-Haberle I., Spasojević I., and Fridovich I. Peroxynitrite scavanging by manganese(III) meso-tetrakis-(N-methylpyridyl)porphyrins. Chem. Res. Toxicol. 12 (1999) 442-449
8. Szabó C., Ischiropoulos H., and Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6 (2007) 662-680
9. Szabó C., Mabley J.G., Moeller S.M., Shimanovich R., Pacher P., Virag L., Soriano V.G., van Duzer J.H., Williams W., Salzman A.L., and Groves J.T. Pathogenic role of peroxynitrite in the development of diabetes and diabetic vascular complications: studies with FP15, a novel potent peroxynitrite decomposition catalyst. Mol. Med. 8 (2002) 571-580
10. Aviv I., and Gross V. Corrole-Based Applications. Chem. Commun. (2007) 1987-1999
11. {radical dot}-, TGF-β and VEGF production by macrophages. Free Radic. Res. 41 (2007) 8-14
12. Zhao Y., Chaiswing L., Oberley T.D., Batinić-Haberle I., St. Clair W., Epstein C.J., and St. Clair D.K. A mechanism-based antioxidant approach for the reduction of skin carcinogenesis. Cancer Res. 65 (2005) 1401-1405
13. Moeller B.J., Cao Y., Li C.Y., and Dewhirst M.W. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: Role of oxygenation, free radicals and stress granules. Cancer Cell 5 (2004) 429-441
14. Tse H., Milton M.J., and 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. 36 (2004) 233-247
15. Gauter-Fleckenstein B., Fleckenstein K., Owzar K., Jian C., Batinić-Haberle I., and Vujasković Ž. Comparison of two Mn porphyrin-based mimics of superoxide-dismutase (SOD) in pulmonary radioprotection. Free Radic. Biol. Med. 44 (2008) 982-989
16. Piganelli J.D., Flores S.C., Cruz C., Koepp J., Young R., Bradley B., Kachadourian R., Batinić-Haberle I., and Haskins K. A metalloporphyrin superoxide dismutase mimetic (SOD mimetic) inhibits autoimune diabetes. Diabetes 51 (2002) 347-355
17. Benov L., and Batinić-Haberle I. A manganese porphyrin SOD mimic suppresses oxidative stress and extends the life span of streptozotocin-diabetic rats. Free Radic. Res. 38 (2005) 81-88
18. Aslan M., Ryan T.M., Adler B., Townes T.M., Parks D.A., Thompson J.A., Tousson A., Gladwin M.T., Tarpey M.M., Patel R.P., Batinić-Haberle I., White C.R., and Freeman B.A. Oxygen radical inhibition of nitric-oxide dependent vascular function in sickle cell disease. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 15215-15220
19. Csont T., Viappiani S., Sawicka J., Slee S., Altarejos J.Y., Batinić-Haberle I., and Schulz R. The involvement of superoxide and iNOS-derived NO in cardiac dysfunction induced by pro-inflammatory cytokines. J. Mol. Cell. Cardiol. 39 (2005) 833-840
20. Saba H., Batinić-Haberle I., Munusamy S., Mitchell T., Lichti C., Megyesi J., and MacMillan-Crow L.A. Manganese porphyrin reduces renal injury and mitochondrial damage during ischemia/reperfusion. Free Radic. Biol. Med. 42 (2007) 1571-1578
21. Wu T.J., Khoo N.H., Zhou F., Day B.J., and Parks D.A. Decreased hepatic ischemia-reperfusion injury by manganese-porphyrin complexes. Free Radic. Res. 41 (2007) 127-134
22. Sompol P., Ittarat W., Tangpong J., Chen Y., Doubinskaia I., Batinić-Haberle I., Abdul H.M., Butterfield A., and St. Clair D.K. A neuronal model of Alzheimer's disease: an insight into the mechanisms of oxidative stress-mediated mitochondrial injury. Neuroscience 153 (2008) 120-130
23. Sheng H., Spasojević I., Warner D.S., and Batinić-Haberle I. Mouse spinal cord compression injury is ameliorated by intrathecal manganese(III) porphyrin. Neurosci. Lett. 366 (2004) 220-225
24. Okado-Matsumoto A., Batinić-Haberle I., and Fridovich I. Complementation of SOD deficient Escherichia coli by manganese porphyrin mimics of superoxide dismutase. Free Radic. Biol. Med. 37 (2004) 401-410
25. Rebouças J.S., Spasojević I., Tjahjono D.H., Richaud A., Mendez F., Benov L., and Batinić-Haberle I. Redox modulation of oxidative stress by Mn porphyrin-based therapeutics: the effect of charge distribution. Dalton Trans. (2008) 1233-1242
26. Spasojević I., and Batinić-Haberle I. Manganese(III) complexes with porphyrins and related compounds as scavengers of superoxide. Inorg. Chim. Acta 317 (2001) 230-242
27. Rebouças J.S., Spasojević I., and Batinić-Haberle I. Pure manganese(III) 5,10,15,20-tetrakis(4-benzoic acid)porphyrin (MnTBAP) is not a superoxide dismutase mimic in aqueous systems: a case of structure-activity relationship as a watchdog mechanism in experimental therapeutics and biology. J. Biol. Inorg. Chem. 13 (2008) 289-302
28. Vance C.K., and Miller A.F. A simple proposal that can explain the inactivity of metal-substituted superoxide dismutases. J. Am. Chem. Soc. 120 (1998) 461-467
29. Ellerby R.M., Cabelli D.E., Graden J.A., and Valentine J.S. Copper-zinc superoxide dismutase: why not pH-dependent?. J. Am. Chem. Soc. 118 (1996) 6556-6561
30. Goldstein S., Fridovich I., and Czapski G. Kinetic properties of Cu,Zn-superoxide dismutase as a function of metal content-order restored. Free Radic. Biol. Med. 41 (2006) 937-941
31. Lahaye D., Muthukumaran K., Hung C.H., Gryko D., Rebouças J.S., Spasojević I., Batinić-Haberle I., and Lindsey J.S. Design and synthesis of manganese porphyrins with tailored lipophilicity: investigation of redox properties and superoxide dismutase activity. Bioorg. Med. Chem. 15 (2007) 7066-7086
32. Dolphin D., Traylor T.G., and Xie L.Y. Polyhaloporphyrins: unusual ligands for metals and metal-catalyzed oxidations. Acc. Chem. Res. 30 (1997) 251-259
33. Ou Z., Shao J., D'Souza F., Tagliatesta P., and Kadish K.M. β-Pyrrole brominated meso-tetraphenylporphyrins: synthesis, spectral and electrochemical properties. J. Porphyrins Phthalocyanines 8 (2004) 201-214
34. do Nascimento E., Silva G.d.e.F., Caetano F.A., Fernandes M.A.M., da Silva D.C., de Carvalho M.E.M.D., Pernaut J.M., Rebouças J.S., and Idemori Y.M. Partially and fully β-brominated Mn-porphyrins in P450 biomimetic systems: effects of the degree of bromination on electrochemical and catalytic properties. J. Inorg. Biochem. 99 (2005) 1193-1204
35. Rebouças J.S., Carvalho M.E.M.D., and Idemori Y.M. Perhalogenated 2-pyridylporphyrin complexes: synthesis, self-coordinating aggregation properties, and catalytic studies. J. Porphyrins Phthalocyanines 6 (2002) 50-57
36. Batinić-Haberle I., Liochev S.I., Spasojević I., and Fridovich I. A potent superoxide dismutase mimic: manganese β-octabromo-meso-tetrakis-(N-methylpyridinium-4-yl) porphyrin. Arch. Biochem. Biophys. 343 (1997) 225-233
37. Batinić-Haberle I., Benov L., and Fridovich I. An anionic impurity in preparations of cytochrome c interferes with assays of cationic catalysts of the dismutation of the superoxide anion radical. Anal. Biochem. 275 (1999) 267
38. Waud W.R., Brady F.O., Wiley R.D., and Rajagopalan K.V. A new purification procedure for bovine milk xanthine oxidase: effect of proteolysis on the subunit structure. Arch. Biochem. Biophys. 169 (1975) 695-701
39. Batinić-Haberle I., Benov L., Spasojević I., and Fridovich I. The ortho effect makes manganese(III) meso-tetrakis(N-methylpyridinium-2-yl)porphyrin (MnTM-2-PyP) a powerful and potentially useful superoxide dismutase mimic. J. Biol. Chem. 273 (1998) 24521-24528
40. Kachadourian R., Flaherty M.M., Crumbliss A.L., Patel M., and Day B.J. Synthesis and in vitro antioxidant properties of manganese(III) β-octabromo-meso-tetrakis(4-carboxyphenyl)porphyrin. J. Inorg. Biochem. 95 (2003) 240-248
41. Richards R.A., Hammons K., Joe M., and Miskelly G.M. Observation of a stable water-soluble lithium porphyrin. Inorg. Chem. 35 (1996) 1940-1944
42. 8 as homogeneous and supported reagents toward hydrogen peroxide and sodium hypochlorite. Turk. J. Chem. 25 (2001) 215-222
43. 3+-octabromo-tetrakis(4-sulfophenyl)porphine on linoleate hydroperoxide and its analytical application. Talanta 71 (2007) 456-461
44. Tabata M., Nishimoto J., Ogata A., Kusano T., and Nahar N. Metalation of water-soluble octabromoporphyrin with lithium(I), cadmium(I), and mercury(II). Bull. Chem. Soc. Jpn. 69 (1996) 673-677
45. Tabata M., Sun H., and Nishimoto J. Trace analysis of lithium with a water-soluble porphyrin. J. Inclusion Phenom. Mol. Recognit. Chem. 32 (1998) 267-281
46. Spasojević I., Batinić-Haberle I., Stevens R.D., Hambright P., Thorpe A.N., Grodkowski J., Neta P., and Fridovich I. Manganese(III) biliverdin IX dimethyl ester: a powerful catalytic scavenger of superoxide employing the Mn(III)/Mn(IV) redox couple. Inorg. Chem. 40 (2001) 726-739
47. Bielski B.H.J., Cabelli D.E., Arudi R.L., and Ross A.B. Reactivity of hydroperoxyl/superoxide radicals in aqueous solution. J. Phys. Chem. Ref. Data 14 (1985) 1041-1100
48. Riley D.P. Functional mimics of superoxide dismutase enzymes as therapeutic agents. Chem. Rev. 99 (1999) 2573-2587
49. Imlay J.A., and Linn S. Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. J. Bacteriol. 169 (1987) 2967-2976
50. do Nascimento E. Manganese porphyrins derived from meso-tetrakis(4-carboxyphenyl)porphyrin in biomimetic systems: effects of the degree of bromination on chemical, electrochemical, and catalytic properties, Ph.D. Dissertation (2004), Universidade Federal de Minas Gerais, Belo Horizonte
51. Hambright P. Chemistry of water soluble porphyrins. In: Kadish K.M., Smith K.M., and Guilard R. (Eds). The porphyrin handbook vol. 2 (2000), Academic Press, New York 129-210
52. Getzoff E.D., Tainer J.A., Weiner P.K., Kollman P.A., Richardson J.S., and Richardson D.C. Electrostatic recognition between superoxide and copper, zinc superoxide-dismutase. Nature 306 (1983) 287-290
53. Zhou H.X., Wong K.Y., and Vijayakumar M. Design of fast enzymes by optimizing interaction potential in active site. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 12372-12377
54. Al-Maghrebi M., Fridovich I., and Benov L. Manganese supplementation relieves the phenotypic deficits seen in superoxide-dismutase-null Escherichia coli. Arch. Biochem. Biophys. 402 (2002) 104-109
55. Fisher A.E.O., Lau G., and Naughton D.P. Lipophilic ionophore complexes as superoxide dismutase mimetics. Biochem. Biophys. Res. Commun. 329 (2005) 930-933
56. Archibald F.S., and Fridovich I. The scavenging of superoxide radical by manganous complexes in vitro. Arch. Biochem. Biophys. 214 (1982) 452-463
57. Ferrer-Sueta G., Hannibal L., Batinić-Haberle I., and Radi R. Reduction of manganese porphyrins by flavoenzymes and submitochondrial particles and the catalytic redox cycle of peroxynitrite. Free Radic. Biol. Med. 41 (2006) 503-512
58. Ventateshrao S., Yin J., Jarzecki A.A., Schultz P.G., and Spiro T.G. Porphyrin distortion during affinity maturation of a ferrochelatase antibody, monitored by resonance Raman spectroscopy. J. Am. Chem. Soc. 126 (2004) 16361-16367
59. - disproportionation. Inorg. Chem. 41 (2002) 5874-5881