Oxyferryl heme and not tyrosyl radical is the likely culprit in prostaglandin H synthase-1 peroxidase inactivation

Biochemistry

Volumn 46, Issue 2, 2007, Pages 534-542

  Wu, Gang ^a,b   Rogge, Corina E ^a   Wang, Jinn Shyan ^c   Kulmacz, Richard J ^a   Palmer, Graham ^b   Tsai, Ah Lim ^a,d  

^a UNIVERSITY OF TEXAS   (United States)

^b RICE UNIVERSITY   (United States)

^c FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; ELECTRON TRANSFER; PEROXIDASE REACTIONS; PORPHYRIN RADICALS;

ALCOHOLS; CATALYSIS; ELECTRON TRANSITIONS; HYDROGEN PEROXIDE; OXIDATION; PROTEINS;

ENZYME KINETICS;

15 HYDROPEROXYARACHIDONIC ACID; ALCOHOL; ETHYL HYDROGEN PEROXIDE; HEME; HEMOPROTEIN; HYDROGEN PEROXIDE; LIPID HYDROPEROXIDE; OXIDIZING AGENT; OXYFERRYL HEME; OXYGEN RADICAL; PEROXIDASE; PEROXY RADICAL; PORPHYRIN DERIVATIVE; PORPHYRIN RADICAL; PROSTAGLANDIN G2; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE H 1; PROTOPORPHYRIN; RADICAL; SINGLET OXYGEN; TYROSINE; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; COMPUTER MODEL; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME KINETICS; ENZYME MECHANISM; NONHUMAN; PRIORITY JOURNAL; RADICAL REACTION;

ANIMALS; CYCLOOXYGENASE INHIBITORS; ELECTRON SPIN RESONANCE SPECTROSCOPY; FREE RADICALS; HEME; KINETICS; LEUKOTRIENES; LIPID PEROXIDES; MALE; MODELS, BIOLOGICAL; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; SHEEP; TYROSINE;

EID: 33846255027     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061859h     Document Type: Article

References (34)

1. Rouzer, C. A., and Marnett, L. J. (2003) Mechanism of free radical oxygenation of polyunsaturated fatty acids by cyclooxygenases, Chem. Rev. 103, 2239-2304.
2. Tsai, A.-L., and Kulmacz, R. J. (2000) Tyrosyl radicals in prostaglandin H synthase-1 and -2, Prostaglandins Leukotrienes Med. 62, 231-254.
3. Lambeir, A. M., Markey, C. M., Dunford, H. B., and Marnett, L. J. (1985) Spectral properties of the higher oxidation states of prostaglandin H synthase, J. Biol. Chem. 260, 14894-14896.
4. Dietz, R., Nastainczyk, W., and Ruf, H. H. (1988) Higher oxidation states of prostaglandin H synthase. Rapid electronic spectroscopy detected two spectral intermediates during the peroxidase reaction with prostaglandin G2, Eur. J. Biochem. 171, 321-328.
5. Shimokawa, T., Kulmacz, R. J., DeWitt, D. L., and Smith, W. L. (1990) Tyrosine 385 of prostaglandin endoperoxide synthase is required for cyclooxygenase catalysis, J. Biol. Chem. 265, 20073-20076.
6. Tsai, A.-L., Hsi, L. C., Kulmacz, R. J., Palmer, G., and Smith, W. L. (1994) Characterization of the tyrosyl radicals in ovine prostaglandin H synthase-1 by isotope replacement and site-directed mutagenesis, J. Biol. Chem. 269, 5085-5091.
7. Markey, C. M., Alward, A., Weller, P. E., and Marnett, L. J. (1987) Quantitative studies of hydroperoxide reduction by prostaglandin-H synthase: Reducing substrate-specificity and the relationship of peroxidase to cyclooxygenase activities, J. Biol. Chem. 262, 6266-6279.
8. Marshall, P. J., Kulmacz, R. J., and Lands, W. E. M. (1987) Constraints on prostaglandin biosynthesis in tissues, J. Biol. Chem. 262, 3510-3517.
9. Wu, G., Wei, C., Kulmacz, R. J., Osawa, Y., and Tsai, A.-L. (1999) A mechanistic study of self-inactivation of the peroxidase activity in prostaglandin H synthase-1, J. Biol. Chem. 274, 9231-9237.
10. Wu, G., Kulmacz, R. J., and Tsai, A. L. (2003) Cyclooxygenase inactivation kinetics during reaction of prostaglandin H synthase-1 with peroxide, Biochemistry 42, 13772-13777.
11. Tsai, A.-L., Wei, C., Baek, H. K., Kulmacz, R. J., and Van Wart, H. E. (1997) Comparison of peroxidase reaction mechanisms of prostaglandin H synthase-1 containing heme and mangano protoporphyrin IX, J. Biol. Chem. 272, 8885-8894.
12. Tsai, A.-L., Wu, G., Palmer, G., Bambai, B., Koehn, J. A., Marshall, P. J., and Kulmacz, R. J. (1999) Rapid kinetics of tyrosyl radical formation and heme redox state changes in prostaglandin H synthase-1 and -2, J. Biol. Chem. 274, 21695-21700.
13. Hecker, M., Ullrich, V., Fischer, C., and Meese, C. O. (1987) Identification of novel arachidonic acid metabolites formed by prostaglandin H synthase, Eur. J. Biochem. 169, 113-123.
14. Kulmacz, R. J., and Lands, W. E. (1983) Requirements for hydroperoxide by the cyclooxygenase and peroxidase activities of prostaglandin H synthase, Prostaglandins 25, 531-540.
15. Odenwaller, R., Maddipati, K. R., and Marnett, L. J. (1992) Detection of a higher oxidation state of manganese-prostaglandin endoperoxide synthase, J. Biol. Chem. 267, 13863-13869.
16. Strieder, S., Schaible, K., Scherer, H. J., Dietz, R., and Ruf, H. H. (1992) Prostaglandin endoperoxide synthase substituted with manganese protoporphyrin IX. Formation of a higher oxidation state and its relation to cyclooxygenase reaction, J. Biol. Chem. 267, 13870-13878.
17. Kulmacz, R. J., Palmer, G., Wei, C., and Tsai, A.-L. (1994) Reaction and free radical kinetics of prostaglandin H synthase with manganese protoporphyrin IX as the prosthetic group, Biochemistry 33, 5428-5439.
18. Mizuno, K., Yamamoto, S., and Lands, W. E. (1982) Effects of non-steroidal anti-inflammatory drugs on fatty acid cyclooxygenase and prostaglandin hydroperoxidase activities, Prostaglandins 23, 743-757.
19. Graff, G., Anderson, L. A., and Jaques, L. W. (1990) Preparation and purification of soybean lipoxygenase-derived unsaturated hydroperoxy and hydroxy fatty acids and determination of molar absorptivities of hydroxy fatty acids, Anal. Biochem. 188, 38-47.
20. Kulmacz, R. J., and Lands, W. (1987) in Prostaglandins and Related Substances: A Practical Approach (Benedetto, C., McDonald-Gibson, R. G., Nigam, S., and Slater, T. F., Eds.) pp 209-227, IRL Press, Washington, DC.
21. Tsai, A.-L., Wu, G., and Kulmacz, R. J. (1997) Stoichiometry of the interaction of prostaglandin H synthase with substrates, Biochemistry 36, 13085-13094.
22. Tsai, A.-L., Berka, V., Kulmacz, R. J., Wu, G., and Palmer, G. (1998) An improved sample packing device for rapid freeze-trap electron paramagnetic resonance spectroscopy kinetic measurements, Anal. Biochem. 264, 165-171.
23. Tsai, A.-L., Palmer, G., and Kulmacz, R. J. (1992) Prostaglandin H synthase. Kinetics of tyrosyl radical formation and of cyclooxygenase catalysis, J. Biol. Chem. 267, 17753-17759.
24. Wu, G., Vuletich, J. L., Kulmacz, R. J., Osawa, Y., and Tsai, A.-L. (2001) Peroxidase self-inactivation in prostaglandin H synthase-1 pretreated with cyclooxygenase inhibitors or substituted with mangano protoporphyrin IX, J. Biol. Chem. 276, 19879-19888.
25. DeGray, J. A., Lassmann, G., Curtis, J. F., Kennedy, T. A., Marnett, L. J., Eling, T. E., and Mason, R. P. (1992) Spectral analysis of the protein-derived tyrosyl radicals from prostaglandin H synthase, J. Biol. Chem. 267, 23583-23588.
26. Shi, W., Hoganson, C. W., Espe, M., Bender, C. J., Babcock, G. T., Palmer, G., Kulmacz, R. J., and Tsai, A.-L. (2000) Electron paramagnetic resonance and electron nuclear double resonance spectroscopic identification and characterization of the tyrosyl radicals in prostaglandin H synthase-1, Biochemistry 39, 4112-4121.
27. Koshkin, V., and Dunford, H. B. (1999) Coupling of the peroxidase and cyclooxygenase reactions of prostaglandin H synthase, Biochim. Biophys. Acta 1430, 341-348,
28. Kulmacz, R. J., van der Donk, W. A., and Tsai, A.-L. (2003) Comparison of the properties of prostaglandin H synthase-1 and -2, Prog. Lipid Res. 42, 377-404.
29. Tsai, A.-L., Palmer, G., Xiao, G., Swinney, D. C., and Kulmacz, R. J. (1998) Structural characterization of arachidonyl radicals formed by prostaglandin H synthase-2 and prostaglandin H synthase-1 reconstituted with mangano protoporphyrin IX, J. Biol. Chem. 273, 3888-3894.
30. Hemler, M. E., Graff, G., and Lands, W. E. (1978) Accelerative autoactivation of prostaglandin biosynthesis by PGG2, Biochem. Biophys. Res. Commun. 85, 1325-1331.
31. Rogge, C. E., Liu, W., Wu, G., Wang, L. H., Kulmacz, R. J., and Tsai, A. L. (2004) Identification of Tyr504 as an alternative tyrosyl radical site in human prostaglandin H synthase-2, Biochemistry 43, 1560-1568.
32. Lassmann, G., Odenwaller, R., Curtis, J. F., DeGray, J. A., Mason, R. P., Marnett, L. J., and Eling, T. E. (1991) Electron spin resonance investigation of tyrosyl radicals of prostaglandin H synthase. Relation to enzyme catalysis, J. Biol. Chem. 266, 20045-20055 [(1992) 267 (9), 6449 (erratum)].
33. Lambeir, A. M., Markey, C. M., Dunford, H. B., and Marnett, L. J. (1987) Spectral properties of the higher oxidation states of prostaglandin H synthase, Adv. Prostaglandin, Thromboxane, Leukotriene Res. 17A, 25-28.
34. Dix, T. A., and Marnett, L. J. (1985) Conversion of linoleic acid hydroperoxide to hydroxy, keto, epoxyhydroxy, and trihydroxy fatty acids by hematin, J. Biol. Chem. 260, 5351-5357.