Pre-existent asymmetry in the human cyclooxygenase-2 sequence homodimer

Journal of Biological Chemistry

Volumn 288, Issue 40, 2013, Pages 28641-28655

  Dong, Liang ^a   Sharma, Narayan P ^a   Jurban, Brice J ^a   Smith, William L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; HETERO DIMERS; HOMODIMERS;

BIOCHEMISTRY; BIOLOGY;

BIOMOLECULES;

ACETYLSALICYLIC ACID; APOENZYME; CYCLOOXYGENASE 2; HEME; HETERODIMER; HOMODIMER;

ACETYLATION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME SUBUNIT; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROCESSING;

ARACHIDONIC ACID; CYCLOOXYGENASE (COX) PATHWAY; DRUG ACTION; EICOSANOID; PROTEIN CONFORMATION;

ACETYLATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ARACHIDONIC ACID; ASPIRIN; CYCLOOXYGENASE 2; CYCLOOXYGENASE INHIBITORS; FLURBIPROFEN; GUANIDINE; HEME; HUMANS; INDOMETHACIN; KINETICS; MODELS, BIOLOGICAL; MUTANT PROTEINS; MUTATION; NAPROXEN; OXYGEN; PALMITIC ACID; PEROXIDASE; PROTEIN MULTIMERIZATION; PYRAZOLES; SUBSTRATE SPECIFICITY; SULFONAMIDES;

EID: 84885107035     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.505503     Document Type: Article

References (70)

1. Schneider, C., Pratt, D. A., Porter, N. A., and Brash, A. R. (2007) Control of oxygenation in lipoxygenase and cyclooxygenase catalysis. Chem. Biol. 14, 473-488
2. Rouzer, C. A., and Marnett, L. J. (2009) Cyclooxygenases: structural and functional insights. J. Lipid Res. 50, S29-S34
3. Tsai, A. L., and Kulmacz, R. J. (2010) Prostaglandin H synthase: resolved and unresolved mechanistic issues. Arch. Biochem. Biophys. 493, 103-124
4. Smith, W. L., Urade, Y., and Jakobsson, P. J. (2011) Enzymes of the cyclooxygenase pathways of prostanoid biosynthesis. Chem. Rev. 111, 5821-5865
5. Duggan, K. C., Walters, M. J., Musee, J., Harp, J. M., Kiefer, J. R., Oates, J. A., and Marnett, L. J. (2010) Molecular basis for cyclooxygenase inhibition by the non-steroidal anti-inflammatory drug naproxen. J. Biol. Chem. 285, 34950-34959
6. Patrono, C., García Rodríguez, L. A., Landolfi, R., and Baigent, C. (2005) Low-dose aspirin for the prevention of atherothrombosis. N. Engl. J. Med. 353, 2373-2383
7. Grosser, T., Fries, S., and FitzGerald, G. A. (2006) Biological basis for the cardiovascular consequences of COX-2 inhibition: therapeutic challenges and opportunities. J. Clin. Invest. 116, 4-15
8. Nakanishi, M., Montrose, D. C., Clark, P., Nambiar, P. R., Belinsky, G. S., Claffey, K. P., Xu, D., and Rosenberg, D. W. (2008) Genetic deletion of mPGES-1 suppresses intestinal tumorigenesis. Cancer Res. 68, 3251-3259
9. Uddin, M. J., Crews, B. C., Blobaum, A. L., Kingsley, P. J., Gorden, D. L., McIntyre, J. O., Matrisian, L. M., Subbaramaiah, K., Dannenberg, A. J., Piston, D. W., and Marnett, L. J. (2010) Selective visualization of cyclooxygenase-2 in inflammation and cancer by targeted fluorescent imaging agents. Cancer Res. 70, 3618-3627
10. Fischer, S. M., Hawk, E. T., and Lubet, R. A. (2011) Coxibs and other nonsteroidal anti-inflammatory drugs in animal models of cancer chemoprevention. Cancer Prevention Research 4, 1728-1735
11. Taketo, M. M. (2012) Roles of stromal microenvironment in colon cancer progression. J. Biochem. 151, 477-481
12. Renda, G., Tacconelli, S., Capone, M. L., Sacchetta, D., Santarelli, F., Sciulli, M. G., Zimarino, M., Grana, M., D'Amelio, E., Zurro, M., Price, T. S., Patrono, C., De Caterina, R., and Patrignani, P. (2006) Celecoxib, ibuprofen, and the antiplatelet effect of aspirin in patients with osteoarthritis and ischemic heart disease. Clin. Pharmacol. Ther. 80, 264-274
13. Grosser, T., Yu, Y., and Fitzgerald, G. A. (2010) Emotion recollected in tranquility: Lessons learned from the COX-2 saga. Annu. Rev. Med. 61, 17-33
14. Trelle, S., Reichenbach, S., Wandel, S., Hildebrand, P., Tschannen, B., Villiger, P. M., Egger, M., and Jüni, P. (2011) Cardiovascular safety of non-steroidal anti-inflammatory drugs: network meta-analysis. BMJ 342, c7086
15. Yu, Y., Ricciotti, E., Scalia, R., Tang, S. Y., Grant, G., Yu, Z., Landesberg, G., Crichton, I., Wu, W., Pure, E., Funk, C. D., and FitzGerald, G. A. (2012) Vascular COX-2 modulates blood pressure and thrombosis in mice. Sci. Transl. Med. 4, 132ra154
16. Xiao, G., Chen, W., and Kulmacz, R. J. (1998) Comparison of structural stabilities of prostaglandin H synthase-1 and-2. J. Biol. Chem. 273, 6801-6811
17. Yuan, C., Rieke, C. J., Rimon, G., Wingerd, B. A., and Smith, W. L. (2006) Partnering between monomers of cyclooxygenase-2 homodimers. Proc. Natl. Acad. Sci. U.S.A. 103, 6142-6147
18. Yuan, C., Sidhu, R. S., Kuklev, D. V., Kado, Y., Wada, M., Song, I., and Smith, W. L. (2009) Cyclooxygenase allosterism, fatty acid-mediated cross-talk between monomers of cyclooxygenase homodimers. J. Biol. Chem. 284, 10046-10055
19. Kulmacz, R. J., and Lands, W. E. (1984) ProstaglandinHsynthase. Stoichiometry of heme cofactor. J. Biol. Chem. 259, 6358-6363
20. Kulmacz, R. J., and Lands, W. E. (1985) Stoichiometry and kinetics of the interaction of prostaglandin H synthase with anti-inflammatory agents. J. Biol. Chem. 260, 12572-12578
21. Prusakiewicz, J. J., Duggan, K. C., Rouzer, C. A., and Marnett, L. J. (2009) Differential sensitivity and mechanism of inhibition of COX-2 oxygenation of arachidonic acid and 2-arachidonoylglycerol by ibuprofen and mefenamic acid. Biochemistry 48, 7353-7355
22. Rimon, G., Sidhu, R. S., Lauver, D. A., Lee, J. Y., Sharma, N. P., Yuan, C., Frieler, R. A., Trievel, R. C., Lucchesi, B. R., and Smith, W. L. (2010) Coxibs interfere with the action of aspirin by binding tightly to one monomer of cyclooxygenase-1. Proc. Natl. Acad. Sci. U.S.A. 107, 28-33
23. Sharma, N. P., Dong, L., Yuan, C., Noon, K. R., and Smith, W. L. (2010) Asymmetric acetylation of the cyclooxygenase-2 homodimer by aspirin and its effects on the oxygenation of arachidonic, eicosapentaenoic, and docosahexaenoic acids. Mol. Pharmacol. 77, 979-986
24. Dong, L., Vecchio, A. J., Sharma, N. P., Jurban, B. J., Malkowski, M. G., and Smith, W. L. (2011) Human cyclooxygenase-2 is a sequence homodimer that functions as a conformational heterodimer. J. Biol. Chem. 286, 19035-19046
25. Duggan, K. C., Hermanson, D. J., Musee, J., Prusakiewicz, J. J., Scheib, J. L., Carter, B. D., Banerjee, S., Oates, J. A., and Marnett, L. J. (2011) (R)-Profens are substrate-selective inhibitors of endocannabinoid oxygenation by COX-2. Nat. Chem. Biol. 7, 803-809
26. Mbonye, U. R., Yuan, C., Harris, C. E., Sidhu, R. S., Song, I., Arakawa, T., and Smith, W. L. (2008) Two distinct pathways for cyclooxygenase-2 protein degradation. J. Biol. Chem. 283, 8611-8623
27. Mbonye, U. R., Wada, M., Rieke, C. J., Tang, H.-Y., Dewitt, D. L., and Smith, W. L. (2006) The 19-amino acid cassette of cyclooxygenase-2 mediates entry of the protein into the endoplasmic reticulum-associated degradation system. J. Biol. Chem. 281, 35770-35778
28. Zou, H., Yuan, C., Dong, L., Sidhu, R. S., Hong, Y. H., Kuklev, D. V., and Smith, W. L. (2012) Human cyclooxygenase-1 activity and its responses to COX inhibitors are allosterically regulated by nonsubstrate fatty acids. J. Lipid Res. 53, 1336-1347
29. Liu, J., Seibold, S. A., Rieke, C. J., Song, I., Cukier, R. I., and Smith, W. L. (2007) Prostaglandin endoperoxide H synthases: Peroxidase hydroperoxide specificity and cyclooxygenase activation. J. Biol. Chem. 282, 18233-18244
30. Song, I., Ball, T. M., and Smith, W. L. (2001) Different suicide inactivation processes for the peroxidase and cyclooxygenase activities of prostaglandin endoperoxide H synthase-1. Biochem. Biophys. Res. Commun. 289, 869-875
31. Rieke, C. J., Mulichak, A. M., Garavito, R. M., and Smith, W. L. (1999) The role of arginine 120 of human prostaglandin endoperoxide H synthase-2 in the interaction with fatty acid substrates and inhibitors. J. Biol. Chem. 274, 17109-17114
32. Rouzer, C. A., and Marnett, L. J. (2008) Non-redundant functions of cyclooxygenases: Oxygenation of endocannabinoids. J. Biol. Chem. 283, 8065-8069
33. Vecchio, A. J., and Malkowski, M. G. (2011) The structure of NS-398 bound to cyclooxygenase-2. J. Struct. Biol. 176, 254-258
34. Rome, L. H., and Lands, W. E. (1975) Structural requirements for timedependent inhibition of prostaglandin biosynthesis by anti-inflammatory drugs. Proc. Natl. Acad. Sci. U.S.A. 72, 4863-4865
35. Holtzman, M. J., Zhang, V., Hussain, H., Roswit, W. T., and Wilson, J. D. (1994) Prostaglandin H synthase and lipoxygenase gene families in the epithelial cell barrier. Ann. N.Y. Acad. Sci. 744, 58-77
36. Lecomte, M., Laneuville, O., Ji, C., DeWitt, D. L., and Smith, W. L. (1994) Acetylation of human prostaglandin endoperoxide synthase-2 (cyclooxygenase-2) by aspirin. J. Biol. Chem. 269, 13207-13215
37. 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 prostaglandinHsynthase-2. Biochemistry 36, 1836-1845
38. 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
39. Malkowski, M. G., Ginell, S. L., Smith, W. L., and Garavito, R. M. (2000) The x-ray crystal structure of prostaglandin endoperoxide H synthase-1 complexed with arachidonic acid. Science 289, 1933-1937
40. 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
41. 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-linolenic acid with prostaglandin endoperoxide H synthases. J. Biol. Chem. 276, 10358-10365
42. Vecchio, A. J., and Malkowski, M. G. (2011) The structural basis of endocannabinoid oxygenation by cyclooxygenase-2. J. Biol. Chem. 286, 20736-20745
43. Vecchio, A. J., Simmons, D. M., and Malkowski, M. G. (2010) Structural basis of fatty acid substrate binding to cyclooxygenase-2. J. Biol. Chem. 285, 22152-22163
44. Bhattacharyya, D. K., Lecomte, M., Rieke, C. J., Garavito, M., and Smith, W. L. (1996) Involvement of arginine 120, glutamate 524, and tyrosine 355 in the binding of arachidonate and 2-phenylpropionic acid inhibitors to the cyclooxygenase active site of ovine prostaglandin endoperoxide H synthase-1. J. Biol. Chem. 271, 2179-2184
45. Koljak, R., Järving, I., Kurg, R., Boeglin, W. E., Varvas, K., Valmsen, K., Ustav, M., Brash, A. R., and Samel, N. (2001) The basis of prostaglandin synthesis in coral. Molecular cloning and expression of a cyclooxygenase from the arctic soft coral Gersemia fruticosa. J. Biol. Chem. 276, 7033-7040
46. Mancini, J. A., Riendeau, D., Falgueyret, J. P., Vickers, P. J., and O'Neill, G. P. (1995) Arginine 120 of prostaglandin G/H synthase-1 is required for the inhibition by nonsteroidal anti-inflammatory drugs containing a carboxylic acid moiety. J. Biol. Chem. 270, 29372-29377
47. Vecchio, A. J., Orlando, B. J., Nandagiri, R., and Malkowski, M. G. (2012) Investigating substrate promiscuity in cyclooxygenase-2: The role of arg-120 and residues lining the hydrophobic groove. J. Biol. Chem. 287, 24619-24630
48. Gierse, J. K., Zhang, Y., Hood, W. F., Walker, M. C., Trigg, J. S., Maziasz, T. J., Koboldt, C. M., Muhammad, J. L., Zweifel, B. S., Masferrer, J. L., Isakson, P. C., and Seibert, K. (2005) Valdecoxib: assessment of cyclooxygenase-2 potency and selectivity. J. Pharmacol. Exp. Ther. 312, 1206-1212
49. Uddin, M. J., Crews, B. C., Ghebreselasie, K., Huda, I., Kingsley, P. J., Ansari, M. S., Tantawy, M. N., Reese, J., and Marnett, L. J. (2011) Fluorinated COX-2 inhibitors as agents in PET imaging of inflammation and cancer. Cancer Prevention Research 4, 1536-1545
50. Prusakiewicz, J. J., Felts, A. S., Mackenzie, B. S., and Marnett, L. J. (2004) Molecular basis of the time-dependent inhibition of cyclooxygenases by indomethacin. Biochemistry 43, 15439-15445
51. Simmons, D. L., Botting, R. M., and Hla, T. (2004) Cyclooxygenase isozymes: The biology of prostaglandin synthesis and inhibition. Pharmacol. Rev. 56, 387-437
52. Otto, J. C., DeWitt, D. L., and Smith, W. L. (1993) N-Glycosylation of prostaglandin endoperoxide synthases-1 and-2 and their orientations in the endoplasmic reticulum. J. Biol. Chem. 268, 18234-18242
53. Otto, J. C., and Smith, W. L. (1994) The orientation of prostaglandin endoperoxide synthases-1 and-2 in the endoplasmic reticulum. J. Biol. Chem. 269, 19868-19875
54. Wada, M., Saunders, T. L., Morrow, J., Milne, G. L., Walker, K. P., Dey, S. K., Brock, T. G., Opp, M. R., Aronoff, D. M., and Smith, W. L. (2009) Two pathways for cyclooxygenase-2 protein degradation in vivo. J. Biol. Chem. 284, 30742-30753
55. Brown, J. (2006) Breaking symmetry in protein dimers: designs and functions. Protein Sci. 15, 1-13
56. Swapna, L. S., Srikeerthana, K., and Srinivasan, N. (2012) Extent of structural asymmetry in homodimeric proteins: prevalence and relevance. PLoS One 7, e36688
57. Guo, Q., Chang, S., Diekman, L., Xiao, G., and Kulmacz, R. J. (1997) Comparison of prostaglandin H synthase isoform structures using limited proteolytic digestion. Arch. Biochem. Biophys. 344, 150-158
58. Chen, Y. N., and Marnett, L. J. (1989) Heme prosthetic group required for acetylation of prostaglandinHsynthase by aspirin. FASEB J. 3, 2294-2297
59. Kulmacz, R. J. (1989) Topography of prostaglandin H synthase. Antiinflammatory agents and the protease-sensitive arginine 253 region. J. Biol. Chem. 264, 14136-14144
60. Seydoux, F., Malhotra, O. P., and Bernhard, S. A. (1974) Half-site reactivity. CRC Crit. Rev. Biochem. 2, 227-257
61. Godoy-Ruiz, R., Krejcirikova, A., Gallagher, D. T., and Tugarinov, V. (2011) Solution NMR evidence for symmetry in functionally or crystallographically asymmetric homodimers. J. Am. Chem. Soc. 133, 19578-19581
62. Sidhu, R. S., Lee, J. Y., Yuan, C., and Smith, W. L. (2010) Comparison of cyclooxygenase-1 crystal structures: cross-talk between monomers comprising cyclooxygenase-1 homodimers. Biochemistry 49, 7069-7079
63. 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
64. 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
65. DeWitt, D. L., el-Harith, E. A., Kraemer, S. A., Andrews, M. J., Yao, E. F., Armstrong, R. L., and Smith, W. L. (1990) The aspirin and heme-binding sites of ovine and murine prostaglandin endoperoxide synthases. J. Biol. Chem. 265, 5192-5198
66. Shimokawa, T., and Smith, W. L. (1992) Prostaglandin endoperoxide synthase: The aspirin acetylation region. J. Biol. Chem. 267, 12387-12392
67. Schneider, C., Boeglin, W. E., Prusakiewicz, J. J., Rowlinson, S. W., Marnett, L. J., Samel, N., and Brash, A. R. (2002) Control of prostaglandin stereochemistry at the 15-carbon by cyclooxygenases-1 and-2. A critical role for serine 530 and valine 349. J. Biol. Chem. 277, 478-485; Correction (2002) J. Biol. Chem. 277, 13354
68. 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
69. Zhen, Y., Mills, D. A., Hoganson, G. W., Lucas, R., Shi, W., Babcock, G. T., and Ferguson-Miller, S. (1999) in Frontiers of Cellular Bioenergetics: Molecular Biology, Biochemistry, and Physiopathology (Papa, S., Guerrieri, F., and Tager, J. M., eds) pp. 157-178, Plenum Publishing Corp., New York
70. 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