Identification of Tyr504 as an Alternative Tyrosyl Radical Site in Human Prostaglandin H Synthase-2

Biochemistry

Volumn 43, Issue 6, 2004, Pages 1560-1568

  Rogge, Corina E ^a   Liu, Wen ^a   Wu, Gang ^a,b   Wang, Lee Ho ^a   Kulmacz, Richard J ^a   Tsai, Ah Lim ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE; ENZYME INHIBITION; HYDROGEN; LIPIDS; ORGANIC ACIDS; PROTEINS;

HYDROGEN ABSTRACTION; MUTANTS;

BIOCHEMISTRY;

ARACHIDONIC ACID; HEMOPROTEIN; HYDROGEN; MUTANT PROTEIN; NIMESULIDE; PEROXIDASE; PHENYLALANINE; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE 2; PROSTAGLANDIN SYNTHASE INHIBITOR; RECOMBINANT PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; ELECTRONICS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENE MUTATION; HUMAN; MOUSE; NONHUMAN; PEROXIDATION; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REACTION ANALYSIS; RESIDUE ANALYSIS; RING OPENING; RING ROTATION; SIGNAL TRANSDUCTION; SPECIES DIFFERENTIATION; STRUCTURE ANALYSIS; TIME;

BINDING, COMPETITIVE; CATALYSIS; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; CYCLOOXYGENASE INHIBITORS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FREE RADICALS; HUMANS; IMMUNOBLOTTING; ISOENZYMES; KINETICS; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; PEROXIDASES; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PROTEIN BINDING; RECOMBINANT PROTEINS; SULFONAMIDES; TYROSINE;

OVIS;

EID: 1042265206     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035717o     Document Type: Article

References (50)

1. Smith, W. L., and Dewitt, D. L. (1996) Prostaglandin endoperoxide H synthases-1 and -2. Adv. Immunol. 62, 167-215.
2. Herschman, H. R. (1996) Prostaglandin synthase 2, Biochim. Biophys. Acta 1299, 125-140.
3. Smith, W. L., Eling, T. E., Kulmacz, R. J., Marnett, L. J., and Tsai, A.-L. (1992) Tyrosyl radicals and their role in hydroperoxide-dependent activation and inactivation of prostaglandin endoperoxide synthase, Biochemistry 31, 3-7.
4. 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.
5. 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.
6. Tsai, A.-L., Kulmacz, R. J., and Palmer, G. (1995) Spectroscopic evidence for reaction of prostaglandin H synthase-1 tyrosyl radical with arachidonic acid, J. Biol. Chem. 270, 10503-10508.
7. Malkowski, M. G., Ginell, S. L., Smith, W. L., and Garavito, R. M. (2000) The productive conformation of arachidonic acid bound to prostaglandin synthase, Science 289, 1933-1937.
8. Tsai, A.-L., and Kulmacz, R. J. (2000) Tyrosyl radicals in prostaglandin H synthase-1 and -2, Prost. Lipid Med. 62, 231-254.
9. 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.
10. 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 (erratum: Lassmann, G., Odenwaller, R., Curtis, J. F., DeGray, J. A., Mason, R. P., Marnett, L. J., and Eling, T. E. (1992) J. Biol. Chem. 267 (9), 6449).
11. 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 (erratum: Lassmann, G., Odenwaller, R., Curtis, J. F., DeGray, J. A., Mason, R. P., Marnett, L. J., and Eling, T. E. (1992) J. Biol. Chem. 267 (9), 6449).
12. 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.
13. 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.
14. Kulmacz, R. J., Ren, Y., Tsai, A.-L., and Palmer, G. (1990) Prostaglandin H synthase: spectroscopic studies of the interaction with hydroperoxides and with indomethacin, Biochemistry 29, 8760-8771.
15. Xiao, G., Tsai, A.-L., Palmer, G., Boyar, W. C., Marshall, P. J., and Kulmacz, R. J. (1997) Analysis of hydroperoxide-induced tyrosyl radicals and lipoxygenase activity in aspirin-treated human prostaglandin H synthase-2, Biochemistry 36, 1836-1845.
16. 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.
17. Dorlet, P., Seibold, S. A., Babcock, G. T., Gerfen, G. J., Smith, W. L., Tsai, A.-L., and Un, S. (2002) High-field EPR study of tyrosyl radicals in prostaglandin H(2) synthase-1, Biochemistry 41, 6107-6114.
18. 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.
19. 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.
20. Barry, B. A., el-Deeb, M. K., Sandusky, P. O., and Babcock, G. T. (1990) Tyrosine radicals in photosystem II and related model compounds. Characterization by isotopic labeling and EPR spectroscopy, J. Biol. Chem. 265, 20139-20143.
21. Onuchic, J. N., Beratan, D. N., Winkler, J. R., and Gray, H. B. (1992) Pathway analysis of protein electron-transfer reactions, Annu. Rev. Biophys. Biomol. Struct. 21, 349-377.
22. Beratan, D. N., and Onuchic, J. N. (1996) The protein bridge between redox centers, in Protein Electron Transfer (Bendall, D. S., Ed.) pp 23-41, BIOS Science Publishers Ltd., Oxford.
23. Kurumbail, R. G., Stevens, A. M., Gierse, J. K., McDonald, J. J., Stegeman, R. A., Pak, J. Y., Gildehaus, D., Miyashiro, J. M., Penning, T. D., Seibert, K., Isakson, P. C., and Stallings, W. C. (1996) Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents, Nature 384, 644-648.
24. Guo, Q., Wang, L. H., Ruan, K. H., and Kulmacz, R. J. (1996) Role of Va1509 in time-dependent inhibition of human prostaglandin H synthase-2 cyclooxygenase activity by isoform-selective agents, J. Biol. Chem. 271, 19134-19139.
25. Bambai, B., Rogge, C. E., Stec, B., and Kulmacz, R. J. (2004) Role of Asn382 and Thr383 in activation and inactivation of human prostaglandin H synthase cyclooxygenase catalysis, J. Biol. Chem. (manuscript in press).
26. Kulmacz, R. J., and Lands, W. (1987) Cyclo-oxygenase: measurement, purification and properties in Prostaglandins and Related Substances: A Practical Approach (McDonald-Gibson, R. G., Nigam, S., and Slater, T. F., Eds.) pp. 209-227 IRL Press, Washington, DC.
27. Smith, W. L., and Lands, W. E. (1972) Oxygenation of unsaturated fatty acids by soybean lipoxygenase, J. Biol. Chem. 247, 1038-1047.
28. 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.
29. Kulmacz, R. J. (1986) Prostaglandin H synthase and hydroperoxides: peroxidase reaction and inactivation kinetics, Arch. Biochem. Biophys. 249, 273-285.
30. Hsi, L. C., Hoganson, C. W., Babcock, G. T., and Smith, W. L. (1994) Characterization of a tyrosyl radical in prostaglandin endoperoxide synthase-2, Biochem. Biophys. Res. Commun. 202, 1592-1598.
31. Tsai, A.-L., Palmer, G., Wu, G., Peng, S., Okeley, N. M., van der Donk, W. A., and Kulmacz, R. J. (2002) Structural characterization of arachidonyl radicals formed by aspirin-treated prostaglandin H synthase-2, J. Biol. Chem. 277, 38311-38321.
32. Sjoberg, B. M., Reichard, P., Graslund, A., and Ehrenberg, A. (1978) The tyrosine free-radical in ribonucleotide reductase from Escherichia-coli, J. Biol. Chem. 253, 6863-6865.
33. Ivancich, A., Jouve, H. M., Sartor, B., and Gaillard, J. (1997) EPR investigation of compound I in Proteus mirabilis and bovine liver catalases: Formation of porphyrin and tyrosyl radical intermediates, Biochemistry 36, 9356-9364.
34. Debus, R. J., Barry, B. A., Sithole, I., Babcock, G. T., and McIntosh, L. (1988) Directed mutagenesis indicates that the donor to P-680+ in photosystem-II Is tyrosine-161 of the D1 polypeptide, Biochemistry 27, 9071-9074.
35. Debus, R. J., Barry, B. A., Babcock, G. T., and McIntosh, L. (1988) Site-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. U.S.A. 85, 427-30.
36. Rogers, M. S., and Dooley, D. M. (2003) Copper-tyrosyl radical enzymes, Curr. Opin. Chem. Biol. 7, 189-196.
37. Chouchane, S., Girotto, S., Yu, S., and Magliozzo, R. S. (2002) Identification and characterization of tyrosyl radical formation in Mycobacterium tuberculosis catalase-peroxidase (KatG), J. Biol. Chem. 277, 42633-42638.
38. Ryle, M. J., Liu, A., Muthukumaran, R. B., Ho, R. Y. N., Koehntop, K. D., McCracken, J., Que, L. Jr., and Hausinger, R. P. (2003) O2- and alpha-ketoglutarate-dependent tyrosyl radical formation in TauD, an alpha-keto acid-dependent non-heme iron dioxygenase, Biochemistry 42, 1854-1862.
39. Svistunenko, D. A., Dunne, J., Fryer, M., Nicholls, P., Reeder, B. J., Wilson, M. T., Bigotti, M. G., Cutruzzola, F., and Cooper, C. E. (2002) Comparative study of tyrosine radicals in hemoglobin and myoglobins treated with hydrogen peroxide, Biophys. J. 83, 2845-2855.
40. Seibold, S. A., Cerda, J. F., Mulichak, A. M., Song, I., Garavito, R. M., Arakawa, T., Smith, W. L., and Babcock, G. T. (2000) Peroxidase activity in prostaglandin endoperoxide H synthase-1 occurs with a neutral histidine proximal heme ligand, Biochemistry 39, 6616-6624.
41. Kozak, K. R., Prusakiewicz, J. J., Rowlinson, S. W., Schneider, C., and Marnett, L. J. (2001) Amino acid determinants in cyclooxygenase-2 oxygenation of the endocannabinoid 2-arachidonylglycerol, J. Biol. Chem. 276, 30072-30077.
42. Rowlinson, S. W., Kiefer, J. R., Prusakiewicz, J. J., Pawlitz, J. L., Kozak, K. R., Kalgutkar, A. S., Stallings, W. C., Kurumbail, R. G., and Marnett, L. J. (2003) A novel mechanism of cyclooxygenase-2 inhibition involving interactions with Ser-530 and Tyr-385. J. Biol. Chem. 278, 45763-45769.
43. Smith, W. L., and Lands, W. E. Y. (1972) Oxygenation of polyunsaturated fatty acids during prostaglandin biosynthesis by sheep vesicular gland, Biochemistry 11, 3276-3285.
44. Barnett, J., Chow, J., Ives, D., Chiou, M., MacKenzie, R., Osen, E., Nguyen, B., Tsing, S., Bach, C., Freire, J., Chan, H., Sigal, E., and Ramesha, C. (1994) Purification, characterization and selective inhibition of human prostraglandin G/H synthase 1 and 2 expressed in the baculovirus system, Biochim. Biophys. Acta 1209, 130-139.
45. 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.
46. Stubbe, J. (1990) Ribonucleotide Reductases: Amazing and Confusing, J. Biol. Chem. 265, 5329-5332.
47. Nordlund, P., and Eklund, H. (1993) Structure and Function of the Escherichia coli ribonucleotide reductase protein R2, J. Mol. Biol. 232, 123-164.
48. Uhlin, U., and Eklund, H. (1994) The structure of ribonucleotide reductase R1, Nature 370, 533-539.
49. Licht, S., Gerfen, G. J., and Stubbe, J. (1996) Thiyl Radicals in Ribonucleotide Reductases, Science 271, 477-481.
50. Tommos, C., Hoganson, C. W., Valentin, M. D., Lydakis-Simantiris, N., Dorlet, P., Westphal, K., Chu, H. A., McCracken, J., and Babcock, G. T. (1998) Manganese and tyrosyl radical function in photosynthetic oxygen evolution, Curr. Opin. Chem. Biol. 2, 244-252.