Role of Tyr348 in Tyr385 radical dynamics and cyclooxygenase inhibitor interactions in prostaglandin H synthase-2

Biochemistry

Volumn 45, Issue 2, 2006, Pages 523-532

  Rogge, Corina E ^a   Ho, Bryant ^a   Liu, Wen ^a   Kulmacz, Richard J ^a   Tsai, Ah Lim ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CHEMICAL REACTIONS; ENZYMES; HYDROGEN; HYDROGEN BONDS; ORGANIC ACIDS;

ARACHIDONIC ACID; CYCLOOXYGENASE INHIBITOR INTERACTIONS; PROSTAGLANDIN H SYNTHASE-2; TIME-DEPENDENT INHIBITORY ACTION;

ENZYME KINETICS;

ACETYLSALICYLIC ACID; ARACHIDONIC ACID; DICLOFENAC; HYDROGEN; ISOPROTEIN; NIMESULIDE; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE INHIBITOR; TYROSINE;

ARTICLE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; HUMAN; HYDROGEN BOND; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; WILD TYPE;

AMINO ACID SUBSTITUTION; ASPIRIN; BINDING SITES; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; ELECTRON SPIN RESONANCE SPECTROSCOPY; FREE RADICALS; HUMANS; HYDROGEN BONDING; ISOENZYMES; MUTATION; PEROXIDASES; PHENYLALANINE; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; SULFONAMIDES; THERMODYNAMICS; TYROSINE;

EID: 30744465930     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051235w     Document Type: Article

References (49)

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. 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. 2+-protoporphyrin-IX intermediate during aspirin-treated prostaglandin H2 synthase II catalysis of arachidonic acid to 15-HETE, Biochemistry 36, 7527-7534.
5. Lu, G., Tsai, A. L., Van Wart, H. E., and Kulmacz, R. J. (1999) Comparison of the peroxidase reaction kinetics of prostaglandin H synthase-1 and -2, J. Biol. Chem. 274, 16162-16167.
6. 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.
7. 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.
8. 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.
9. Picot, D., Loll, P. J., and Garavito, R. M. (1994) The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1, Nature 367, 243-249.
10. Loll, P. J., Picot, D., and Garavito, R. M. (1995) The structural basis of aspirin activity inferred from the crystal structure of inactivated prostaglandin H2 synthase, Nat. Struct. Biol. 2, 637-643.
11. Loll, P. J., Picot, D., Ekabo, O., and Garavito, R. M. (1996) Synthesis and use of iodinated nonsteroidal antiinflammatory drug analogs as crystallographic probes of the prostaglandin H2 synthase cyclooxygenase active site, Biochemistry 35, 7330-7340.
12. 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.
13. Luong, C., Miller, A., Barnett, J., Chow, J., Ramesha, C., and Browner, M. F. (1996) Flexibility of the NSAID binding site in the structure of human cyclooxygenase-2, Nat. Struct. Biol. 3, 927-933.
14. 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.
15. Thuresson, E. D., Malkowski, M. G., Lakkides, K. M., Rieke, C. J., Mulichak, A. M., Ginell, S. L., Garavito, R. M., and Smith, W. L. (2001) Mutational and X-ray crystallographic analysis of the interaction of dihomo-γ-linolenic acid with prostaglandin endoperoxide H synthases, J. Biol. Chem. 276, 10358-10365.
16. Malkowski, M. G., Thuresson, E. D., Lakkides, K. M., Rieke, C. J., Micielli, R., Smith, W. L., and Garavito, R. M. (2001) Structure of eicosapentaenoic and linoleic acids in the cyclooxygenase site of prostaglandin endoperoxide H synthase-1, J. Biol. Chem. 276, 37547-37555.
17. Loll, P. J., Sharkey, C. T., O'Connor, S. J., Dooley, C. M., O'Brien, E., Devocelle, M., Nolan, K. B., Selinsky, B. S., and Fitzgerald, D. J. (2001) O-Acetylsalicylhydroxamic acid, a novel acetylating inhibitor of prostaglandin H2 synthase: Structural and functional characterization of enzyme-inhibitor interactions, Mol. Pharm. 60, 1407-1413.
18. Selinsky, B. S., Gupta, K., Sharkey, C. T., and Loll, P. J. (2001) Structural analysis of NSAID binding by prostaglandin H2 synthase: Time-dependent and time-independent inhibitors elicit identical enzyme conformations, Biochemistry 40, 5172-5180.
19. 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.
20. Gupta, K., Selinsky, B. S., Kaub, C. J., Katz, A. K., and Loll, P. J. (2004) The 2.0 Å resolution crystal structure of prostaglandin H2 synthase-1: Structural insights into an unusual peroxidase, J. Mol. Biol. 335, 503-518.
21. Jeffrey, G. A. (1997) An Introduction to Hydrogen Bonding, Oxford University Press, New York.
22. 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.
23. Wilson, J. C., Wu, G., Tsai, A. L., and Gerfen, G. J. (2005) Determination of the structural environment of the tyrosyl radical in prostaglandin H-2 synthase-1: A high-frequency ENDOR/EPR study, J. Am. Chem. Soc. 127, 1618-1619.
24. Hochgesang, G. P., Rowlinson, S. W., and Marnett, L. J. (2000) Tyrosine-385 is critical for acetylation of cyclooxygenase-2 by aspirin, J. Am. Chem. Soc. 122, 6514-6515.
25. 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.
26. Bambai, B., Rogge, C. E., Stec, B., and Kulmacz, R. J. (2004) Role of Asn-382 and Thr-383 in activation and inactivation of human prostaglandin H synthase cyclooxygenase catalysis, J. Biol. Chem. 279, 4084-4092.
27. 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.
28. 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.) IRL Press, Washington, DC.
29. Guo, Q., Wang, L. H., Ruan, K. H., and Kulmacz, R. J. (1996) Role of Val509 in time-dependent inhibition of human prostaglandin H synthase-2 cyclooxygenase activity by isoform-selective agents, J. Biol. Chem. 271, 19134-19139.
30. Callan, O. H., So, O. Y., and Swinney, D. C. (1996) The kinetic factors that determine the affinity and selectivity for slow binding inhibition of human prostaglandin H synthase-1 and -2 by indomethacin and flurbiprofen, J. Biol. Chem. 271, 3548-3554.
31. 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.
32. Capdevila, J. H., Morrow, J. D., Belosludtsev, Y. Y., Beauchamp, D. R., DuBois, R. N., and Falck, J. R. (1995) The catalytic outcomes of the constitutive and the mitogen inducible isoforms of prostaglandin H2 synthase are markedly affected by glutathione and glutathione peroxidase(s), Biochemistry 34, 3325-3337.
33. 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.
34. 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.
35. 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.
36. Bender, C. J., Sahlin, M., Babcock, G. T., Barry, B. A., Chandrashekar, T. K., Salowe, S. P., Stubbe, J., Lindstrom, B., Petersson, L., Ehrenberg, A., and Sjoberg, B. M. (1989) An ENDOR study of the tyrosyl free-radical in ribonucleotide reductase from Escherichia coli, J. Am. Chem. Soc. 111, 8076-8083.
37. Fessenden, R. W., and Schuler, R. H. (1963) Electron spin resonance studies of transient alkyl radicals, J. Chem. Phys. 39, 2147-2195.
38. 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.
39. Holtzman, M. J., Turk, J., and Shornick, L. P. (1992) Identification of a pharmacologically distinct prostaglandin H synthase in cultured epithelial cells, J. Biol. Chem. 267, 21438-21445.
40. Tsai, A.-L., and Kulmacz, R. J. (2000) Tyrosyl radicals in prostaglandin H synthase-1 and -2, Prostaglandins & Other Lipid Mediators 62, 231-254.
41. Un, S., Atta, M., Fontecave, M., and Rutherford, A. W. (1995) G-Values as a probe of the local protein environment: High-field EPR of tyrosyl radicals in ribonucleotide reductase and photosystem-II, J. Am. Chem. Soc. 117, 10713-10719.
42. 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.
43. Meade, E. A., Smith, W. L., and DeWitt, D. L. (1993) Differential inhibition of prostaglandin endoperoxide synthase (cyclooxygenase) isozymes by aspirin and other non-steroidal anti-inflammatory drugs, J. Biol. Chem. 268, 6610-6614.
44. Kulmacz, R. J., Palmer, G., and Tsai, A.-L. (1991) Prostaglandin H synthase: Perturbation of the tyrosyl radical as a probe of anticyclooxygenase agents, Mol. Pharm. 40, 833-837.
45. Lanzo, C. A., Sutin, J., Rowlinson, S., Talley, J., and Marnett, L. J. (2000) Fluorescence quenching analysis of the association and dissociation of a diarylheterocycle to cyclooxygenase-1 and cyclooxygenase-2: Dynamic basis of cyclooxygenase-2 selectivity, Biochemistry 39, 6228-6234.
46. So, O. Y., Scarafia, L. E., Mak, A. Y., Callan, O. H., and Swinney, D. C. (1998) The dynamics of prostaglandin H synthases. Studies with prostaglandin H synthase-2 Y355F unmask mechanisms of time-dependent inhibition and allosteric activation, J. Biol. Chem. 273, 5801-5807.
47. Ku, E. C., and Wasvary, J. M. (1973) Inhibition of prostaglandin synthetase by SU-21524, Fed. Proc. 32, 3302.
48. Rome, L. H., and Lands, W. E. (1975) Structural requirements for time-dependent inhibition of prostaglandin biosynthesis by anti-inflammatory drugs, Proc. Natl. Acad. Sci. U.S.A. 72, 4863-4865.
49. Smith, W. L., and Lands, W. E. (1972) Oxygenation of unsaturated fatty acids by soybean lipoxygenase, J. Biol. Chem. 247, 1038-1047.