Regio- and stereo-chemical oxidation of linoleic acid by human myoglobin and hydrogen peroxide: Tyr103 affects rate and product distribution

Biochemical Journal

Volumn 381, Issue 2, 2004, Pages 365-372

  Rayner, Benjamin S ^a,b   Stocker, Roland ^b   Lay, Peter A ^c   Witting, Paul K ^a,b  

^a Department of Microbiology and Infectious Diseases   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Ischaemia reperfusion injury; Lipid peroxidation; Myoglobin; Peroxidase activity

Indexed keywords

AMINO ACIDS; ELECTRONS; HYDROGEN BONDS; HYDROGEN PEROXIDE; OXIDATION; PROTEINS;

STEADY-STATE ANALYSIS; WILD-TYPE PROTEINS;

BIOCHEMISTRY;

HYDROGEN PEROXIDE; LINOLEIC ACID; MYOGLOBIN; STEARIC ACID DERIVATIVE; TYROSINE;

ARTICLE; CHEMICAL REACTION; ENZYME ACTIVITY; LIPID OXIDATION; OXIDATION KINETICS; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; STEADY STATE; STEREOCHEMISTRY; WILD TYPE;

ANIMALS; HUMANS; HYDROGEN PEROXIDE; LINOLEIC ACID; LIPID PEROXIDATION; MYOGLOBIN; OXIDATION-REDUCTION; PHENYLALANINE; RECOMBINANT PROTEINS; STEREOISOMERISM; TYROSINE; WHALES;

EID: 3242746585     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031924     Document Type: Article

References (47)

1. Wittenberg, B. A. and Wittenberg, J. B. (1989) Transport of oxygen in muscle. Annu. Rev. Physiol. 51, 857-878
2. Qiu, Y., Sutton, L. and Riggs, A. F. (1998) Identification of myoglobin in human smooth muscle. J. Biol. Chem. 273, 23426-23432
3. Lloyd-Raven, E. and Mauk, A. G. (2000) Myoglobin. In Advances in Inorganic Chemistry: Heme-Fe Proteins, vol. 51 (Sykes, A. G., ed.), pp. 1-49, Academic Press, London
4. Hogg, N., Rice-Evans, C., Darley-Usmar, V., Wilson M. T., Paganga, G. and Bourne, L. (1994) The role of lipid hydroperoxides in the myoglobin-dependent oxidation of LDL. Arch. Biochem. Biophys. 314, 39-44
5. 2: involvement of α-tocopheroxyl and phosphatidylcholine alkoxyl radicals. Chem. Res. Toxicol. 12, 1173-1181
6. Irwin, J. A., Ostdal, H. and Davies, M. J. (1999) Myoglobin-induced oxidative damage: evidence for radical transfer from oxidized myoglobin to other proteins and antioxidants. Arch. Biochem. Biophys. 362, 94-104
7. George, P. and Irvine, D. H. (1954) Free radical production in oxidation-reduction reactions of peroxidase, catalase and metmyoglobin. Br. J. Radiol. 27, 131-137
8. Allentoff, A. J., Bolton, J. L., Wilkis, A., Thompson, J. A. and Ortiz de Montellano, P. R. (1992) Heterolytic versus homolytic peroxide bond cleavage by sperm whale myoglobin and myoglobin mutants. J. Am. Chem. Soc. 114, 9744-9749
9. 2-mediated cross-linking of sperm whale myoglobin. J. Biol. Chem. 263, 17880-17886
10. Davies, M. J. (1991) Identification of a globin free radical in equine myoglobin treated with peroxides. Biochim. Biophys. Acta 1077, 86-90
11. DeGray, J. A., Gunther, M. R., Tschirret-Guth, R., Ortiz de Montellano, P. R. and Mason, R. P. (1997) Peroxidation of a specific tryptophan of metmyoglobin by hydrogen peroxide. J. Biol. Chem. 272, 2359-2362
12. 2: involvement of a thiyl radical produced at cysteine 110. J. Biol. Chem. 275, 20391-20398
13. Catalano, C. E. and Ortiz de Montellano, P. R. (1987) Oxene transfer, electron abstraction, and co-oxidation in the epoxidation of stilbene and 7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene by hemoglobin. Biochemistry 26, 8373-8380
14. Rao, S. I., Wilks, A., Hamberg, M. and Ortiz de Montellano, P. R. (1994) The lipoxygenase activity of myoglobin: oxidation of linoleic acid by the ferryl oxygen rather than protein radical. J. Biol. Chem. 269, 7210-7216
15. Witting, P. K., Mauk, A. G., Douglas, D. J. and Stocker, R. (2001) Reaction of human myoglobin and peroxynitrite: characterizing biomarkers for myoglobin-derived oxidative stress. Biochem. Biophys. Res. Commun. 286, 352-356
16. Kanner, J. and Harel, S. (1985) Initiation of membranal lipid peroxidation by activated metmyoglobin and methemoglobin. Arch. Biochem. Biophys. 237, 314-321
17. Galaris, D., Eddy, L., Arduini, A., Cadenas, E. and Hochstein, P. (1989) Mechanisms of reoxygenation injury in myocardial infarction: implications of a myoglobin redox cycle. Biochem. Biophys. Res. Commun. 160, 1162-1168
18. Hatley, M. E., Srinivasan, S., Reilly, K. B., Bolick, D. T. and Hedrick, C. C. (2003) Increased production of 12/15 lipoxygenase eicosanoids accelerates monocyte/endothelial interactions in diabetic db/db mice. J. Biol. Chem. 278, 25369-25375
19. Kuhn, H., Belkner, J., Zaiss, S., Fahrenklemper, T. and Wohlfeil, S. (1994) Involvement of 15-lipoxygenase in early stages of atherogenesis. J. Exp. Med. 179, 1903-1911
20. Baer, A. N., Costello, P. B. and Green, F. A. (1991) Stereospecificity of the hydroxyeicosatetraenoic and hydroxyoctadecadienoic acids produced by cultured bovine endothelial cells. Biochim. Biophys. Acta. 1085, 45-52
21. 2. Biochemistry 41, 11495-11503
22. Buettner, G. R. (1990) Use of ascorbate as test for catalytic metals in simple buffers. Methods Enzymol. 186, 125-127
23. Zoller, M. J. and Smith, M. (1987) Oligonucleotide-directed mutagenesis: a simple method using two oligonucleotide primers and a single-stranded DNA template. Methods Enzymol. 154, 329-350
24. Hubbard, S. R., Hendrickson, W. A., Lambright, D. G. and Boxer, S. G. (1990) X-ray crystal structure of a recombinant human myoglobin mutant at 2.8 Å resolution. J. Mol. Biol. 213, 215-218
25. Gunther, M. R., Tschirret-Guth, R. A., Witkowska, H. E., Fann, Y. C., Barr, D. P., Ortiz De Montellano, P. R. and Mason, R. P. (1998) Site-specific spin trapping of tyrosine radicals in the oxidation of metmyoglobin by hydrogen peroxide. Biochem. J. 330, 1293-1299
26. Upston, J. M., Neuzil, J., Witting, P. K., Alleva, R. and Stocker, R. (1997) Oxidation of free fatty acids in low density lipoprotein by 15-lipoxygenase stimulates nonenzymic, α-tocopherol-mediated peroxidation of cholesteryl esters. J. Biol. Chem. 272, 30067-30074
27. Kuhn, H., Belkner, J., Suzuki, H. and Yamamoto, S. (1994) Oxidative modification of human lipoproteins by lipoxygenases of different positional specificities. J. Lipid Res. 35, 1749-1759
28. Mashima, R., Tilley, L., Siomos, M.-A., Papalexis, V., Raftery, M. J. and Stocker, R. (2002) Plasmodium falciparum histidine-rich protein-2 (PfHRP2) modulates the redox activity of ferri-protoporphyrin IX (FePPIX) J. Biol. Chem. 277, 14514-14520
29. Reeder, B. J. and Wilson, M. T. (1998) Mechanism of the reaction of myoglobin with the lipid hydroperoxide hydroperoxyoctadecadienoic acid. Biochem J. 330, 1317-1323
30. Hildebrand, D. P., Lim, K. T., Rosell, F. I., Twitchett, M. B., Wan, L. and Mauk, A. G. (1998) Spectroscopic and functional studies of a novel quadruple myoglobin variant with increased peroxidase activity. J. Inorg. Biochem. 70, 11-16
31. Dutton, P. L. (1978) Redox potentiometry: determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems. Methods Enzymol. 54, 411-135
32. Bard, A. J. and Faulkner, F. R. (1980) in Electrochemical Methods, Fundamentals and Applications, p. 195, J. Wiley & Sons Publishers, New York
33. 2: electron transfer between tyrosine 103 phenoxyl radical and cysteine 110 yields a protein-thiyl radical. J. Biol. Chem. 276, 16540-16547
34. Ikeda-Saito, M., Hori, H., Andersson, L. A., Prince, R. C., Pickering, I. J., George, G. N., Sanders, 2nd, C. R., Lutz, R. S., McKelvey, E. J. and Mattera, R. (1992) Coordination structure of the ferric heme iron in engineered distal histidine myoglobin mutants. J. Biol. Chem. 267, 22843-22852
35. Galaris, D., Sevanian, A., Cadenas, E. and Hochstein, P. (1990) Ferrylmyoglobin-catalyzed linoleic acid peroxidation. Arch. Biochem. Biophys. 281, 163-169
36. Nui, Q. J. and Mendenhall, G. D. (1992) Yields of singlet molecular oxygen from peroxyl radical termination. J. Am. Chem. Soc. 114, 165-172
37. Turner, J. J., Rice-Evans, C. A., Davies, M. J. and Newman, E. S. (1991) The formation of free radicals by cardiac myocytes under oxidative stress and the effects of electron-donating drugs. Biochem. J. 277, 833-837
38. Van Dyke, B. R., Saltman, P. and Armstrong, F. A. (1996) Control of myoglobin electron-transfer rates by the distal (nonbound) histidine residue. J. Am. Chem. Soc. 118, 3490-3492
39. Takano, T. (1977) Structure of myoglobin refined at 2.0 Å resolution: I. Crystallographic refinement of metmyoglobin obtained from sperm whale. J. Mol. Biol. 110, 537-568
40. Evans, S. V. and Brayer, G. D. (1990) High-resolution study of the three-dimensional structure of horse heart metmyoglobin. J. Mol. Biol. 213, 885-897
41. Moore, G. R., Pettigrew, G. W. and Rogers, N. K. (1986) Factors influencing redox potentials of electron transfer proteins. Proc. Natl. Acad. Sci. U.S.A. 83, 4998-4999
42. Moore, G. R. and Williams, R. J. P. (1977) Structural basis for the variation in redox potential of cytochromes. FEBS Lett. 79, 229-232
43. Farhangrazi, Z. S., Fossett, M. E., Powers, L. S. and Ellis, Jr, W. R. (1995) Variable-temperature spectroelectrochemical study of horseradish peroxidase. Biochemistry 34, 2866-2871
44. Iwase, H., Takatori, T., Sakurada, K., Nagao, M., Niijima, H., Matsuda, Y. and Kobayashi, M. (1998) Calcium is required for quasi-lipoxygenase activity of hemoproteins. Free Radical Biol. Med. 25, 943-952
45. Porter, N. A., Weber, B. A. and Smith, K. J. (1980) Autoxidation of polyunsatured fatty acids. Factors controlling the stereochemistry of product hydroperoxides. J. Am. Chem. Soc. 102, 5597-5601
46. Upston, J. M., Terentis, A. C., Morris, K., Keaney, Jr, J. F. and Stocker, R. (2002) Oxidized lipid accumulates in the presence of α-tocopherol in atherosclerosis. Biochem. J. 363, 753-760
47. 97, and F-helix swap mutants. Biochemistry 37, 12301-12319