Kinetic and structural investigations of the allosteric site in human epithelial 15-lipoxygenase-2

Biochemistry

Volumn 48, Issue 36, 2009, Pages 8721-8730

  Wecksler, Aaron T ^a   Kenyon, Victor ^a   Garcia, Natalie K ^a   Deschamps, Joshua D ^a,c   Van Der Donk, Wilfred A ^b   Holman, Theodore R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c KaloBios Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

15-LIPOXYGENASE; ALLOSTERIC EFFECT; ALLOSTERIC EFFECTORS; ALLOSTERIC REGULATION; ALLOSTERIC SITE; CELLULAR BIOLOGY; FEED-BACK LOOP; HIGH TEMPERATURE; HISTIDINE RESIDUES; HOMOLOGY MODELS; HYDROGEN ATOM ABSTRACTION; HYDROGEN BONDINGS; ISOTOPE EFFECT; LIPOXYGENASES; LOW TEMPERATURES; PH DEPENDENCE; PRODUCT DISTRIBUTIONS; PROSTATE CANCERS; RATE-DETERMINING STEP; STRUCTURAL INVESTIGATION; SUBSTRATE SPECIFICITY; TITRATION CURVES; TUNNELING MECHANISM;

ABSTRACTING; ATOMS; CARBOXYLATION; CYTOLOGY; HYDROGEN; HYDROGEN BONDS; ISOTOPES; PH EFFECTS;

SUBSTRATES;

13 HYDROXYOCTADECADIENOIC ACID; 15 LIPOXYGENASE 2; ARACHIDONATE 15 LIPOXYGENASE; ARACHIDONIC ACID; CARBOXYLIC ACID; CARCINOGEN; CORIOLIC ACID; FATTY ACID; HISTIDINE; HYDROGEN; LANTHANUM; LINOLEIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DIFFUSION; ENZYME BINDING; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STRUCTURE; EPITHELIUM; HIGH TEMPERATURE; HUMAN; HYDROGEN BOND; ISOTOPE ANALYSIS; LOW TEMPERATURE; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTON TRANSPORT; STRUCTURAL HOMOLOGY; TITRIMETRY;

ALLOSTERIC SITE; ARACHIDONATE 15-LIPOXYGENASE; ARACHIDONIC ACID; BINDING, COMPETITIVE; DEUTERIUM EXCHANGE MEASUREMENT; EPITHELIAL CELLS; HISTIDINE; HUMANS; ISOENZYMES; KINETICS; MALE; MODELS, MOLECULAR; PROSTATE; PROTEIN BINDING; SOLVENTS; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; TANDEM MASS SPECTROMETRY;

EID: 70249112246     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9009242     Document Type: Article

References (62)

1. Vane, J. R., Bakhle, Y. S., and Botting, R. M. (1998) Cyclooxygenases 1 and 2. Annu. Rev. Pharmacol. Toxicol. 38, 97-120.
2. Capdevila, J. H., Falck, J. R., and Estabrook, R. W. (1992) Cytochrome P450 and the arachidonate cascade. FASEB J. 6, 731-736.
3. Haeggstrom, J. Z., and Wetterholm, A. (2002) Enzymes and receptors in the leukotriene cascade. Cell. Mol. Life Sci. 59, 742-753.
4. Yamamoto, S. (1992) Mammalian lipoxygenases: molecular structures and functions. Biochim. Biophys. Acta 1128, 117-131.
5. Solomon, E. I., Zhou, J., Neese, F., and Pavel, E. G. (1997) New insights from spectroscopy into the structure/function relationships of lipoxygenases. Chem. Biol. 4, 795-808.
6. Serhan, C. N. (1994) Lipoxin biosynthesis and its impact in inflammatory and vascular events. Biochim. Biophys. Acta 1212, 1-25.
7. Nakano, H., Inoue, T., Kawasaki, N., Miyataka, H., Matsumoto, H., Taguchi, T., Inagaki, N., Nagai, H., and Satoh, T. (2000) Synthesis and biological activities of novel antiallergic agents with 5-lipoxygenase inhibiting action. Bioorg. Med. Chem. 8, 373-380.
8. Hussain, H., Shornick, L. P., Shannon, V. R., Wilson, J. D., Funk, C. D., Pentland, A. P., and Holtzman, M. J. (1994) Epidermis contains platelet-type 12-lipoxygenase that is overexpressed in germinal layer keratinocytes in psoriasis. Am. J. Physiol. 266, C243-253.
9. Harats, D., Shaish, A., George, J., Mulkins, M., Kurihara, H., Levkovitz, H., and Sigal, E. (2000) Overexpression of 15-lipoxygenase in vascular endothelium accelerates early atherosclerosis in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 20, 2100-2105.
10. Steele, V. E., Holmes, C. A., Hawk, E. T., Kopelovich, L., Lubet, R. A., Crowell, J. A., Sigman, C. C., and Kellof, G. J. (1999) Lipoxygenase inhibitors as potential cancer chemopreventives. Cancer Epidemiol., Biomarkers Prevention 8, 467-483. (Pubitemid 29230553)
11. Falgueyret, J. P., Denis, D., Macdonald, D., Hutchinson, J. H., and Riendeau, D. (1995) Characterization of the arachidonate and ATP binding sites of human 5-lipoxygenase using photoaffinity labeling and enzyme immobilization. Biochemistry 34, 13603-13611.
12. Hogaboom, G. K., Cook, M., Newton, J. F., Varrichio, A., Shorr, R. G., Sarau, H. M., and Crooke, S. T. (1986) Purification, characterization, and structural properties of a single protein from rat basophilic leukemia (RBL-1) cells possessing 5-lipoxygenase and leukotriene A4 synthetase activities. Mol. Pharmacol. 30, 510-519.
13. Rouzer, C. A., and Samuelsson, B. (1986) The importance of hydroperoxide activation for the detection and assay of mammalian 5-lipoxygenase. FEBS Lett. 204, 293-296.
14. Shimizu, T., Izumi, T., Seyama, Y., Tadokoro, K., Radmark, O., and Samuelsson, B. (1986) Characterization of leukotriene A4 synthase from murine mast cells: evidence for its identity to arachidonate 5-lipoxygenase. Proc. Natl. Acad. Sci. U. S. A. 83, 4175-4179.
15. Mogul, R., Johansen, E., and Holman, T. R. (2000) Oleyl sulfate reveals allosteric inhibition of soybean lipoxygenase-1 and human 15-lipoxygenase. Biochemistry 39, 4801-4807. (Pubitemid 30225345)
16. Ruddat, V. C., Whitman, S., Holman, T. R., and Bernasconi, C. F. (2003) Stopped-flow kinetic investigations of the activation of soybean lipoxygenase-1 and the influence of inhibitors on the allosteric site. Biochemistry 42, 4172-4178. (Pubitemid 36418310)
17. Shappell, S. B., Manning, S., Boeglin, W. E., Guan, Y. F., Roberts, R. L., Davis, L., Olson, S. J., Jack, G. S., Coffey, C. S., Wheeler, T. M., Breyer, M. D., and Brash, A. R. (2001) Alterations in lipoxygenase and cyclooxygenase-2 catalytic activity and mRNA expression in prostate carcinoma. Neoplasia 3, 287-303. (Pubitemid 32801879)
18. Butler, R. M., S., H., Tindall, D. J., and Young, C. Y. (2000) Nonapoptotic cell death associated with S-phase arrest of prostate cancer cells via the peroxisome proliferator-activated receptor gamma ligand, 15-deoxy-delta12,14-prostaglandin J2. Cell Growth Differ. 11, 49-61.
19. Hsi, L. C., Wilson, L., Nixon, J., and Eling, T. E. (2001) 15-Lipoxygenase-1 metabolites down-regulate peroxisome proliferator-activated receptor gamma via the MAPK signaling pathway. J. Biol. Chem. 276, 34545-34552.
20. Wecksler, A. T., Kenyon, V., Deschamps, J. D., and Holman, T. R. (2008) Substrate specificity changes for human reticulocyte and epithelial 15-lipoxygenases reveal allosteric product regulation. Biochemistry 47, 7364-7375. (Pubitemid 351991015)
21. Nordlund, P., and Reichard, P. (2006) Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681-706.
22. Reichard, P. (2002) Ribonucleotide reductases: the evolution of allosteric regulation. Arch. Biochem. Biophys. 397, 149-155.
23. Guichardant, M., Thevenon, C., Pageaux, J. F., and Lagarde, M. (1997) Basal concentrations of free and esterified monohydroxylated fatty acids in human blood platelets. Clin. Chem. 43, 2403-2407.
24. Wecksler, A. T., Jacquot, C., van der Donk, W. A., and Holman, T. R. (2009) Mechanistic investigations of human reticulocyte 15- and platelet 12-lipoxygenases with arachidonic acid. Biochemistry 48, 6259-6267.
25. Lewis, E., Johnson, E., and Holman, T. (1999) Large competitive kinetic isotope effects in human 15-lipoxygenase catalysis measured by a novel HPLC method. J. Am. Chem. Soc. 121, 1395-1396.
26. Jacquot, C., Wecksler, A. T., McGinley, C. M., Segraves, E. N., Holman, T. R., and van der Donk, W. A. (2008) Isotope sensitive branching and kinetic isotope effects in the reaction of deuterated arachidonic acids with human 12- and 15-lipoxygenases. Biochemistry 47, 7295-7303. (Pubitemid 351956378)
27. Peng, S., Okeley, N. M., Tsai, A. L., Wu, G., Kulmacz, R. J., and van der Donk, W. A. (2002) Synthesis of isotopically labeled arachidonic acids to probe the reaction mechanism of prostaglandin H synthase. J. Am. Chem. Soc. 124, 10785-10796.
28. Peng, S., McGinley, C. M., and van der Donk, W. A. (2004) Synthesis of site-specifically labeled arachidonic acids as mechanistic probes for prostaglandin H synthase. Org. Lett. 6, 349-352.
29. Deschamps, J. D., Gautschi, J. T., Whitman, S., Johnson, T. A., Gassner, N. C., Crews, P., and Holman, T. R. (2007) Discovery of platelet-type 12-human lipoxygenase selective inhibitors by high-throughput screening of structurally diverse libraries. Bioorg. Med. Chem. 15, 6900-6908.
30. Glickman, M. H., and Klinman, J. P. (1995) Nature of rate-limiting steps in the soybean lipoxygenase-1 reaction. Biochemistry 34, 14077-14092.
31. Rickert, K. W., and Klinman, J. P. (1999) Nature of hydrogen transfer in soybean lipoxygenase 1: separation of primary and secondary isotope effects. Biochemistry 38, 12218-12228. (Pubitemid 129516190)
32. Segraves, E. N., and Holman, T. R. (2003) Kinetic investigations of the rate-limiting step in human 12- and 15-lipoxygenase. Biochemistry 42, 5236-5243.
33. Glickman, M. H., and Klinman, J. P. (1996) Lipoxygenase reaction mechanism: demonstration that hydrogen abstraction from substrate precedes dioxygen binding during catalytic turnover. Biochemistry 35, 12882-12892.
34. Jacquot, C., Peng, S., and van der Donk, W. A. (2008) Kinetic isotope effects in the oxidation of arachidonic acid by soybean lipoxygenase-1. Bioorg. Med. Chem. Lett. 18, 5959-5962.
35. Kenyon, V., Chorny, I., Carvajal, W. J., Holman, T. R., and Jacobson, M. P. (2006) Novel human lipoxygenase inhibitors discovered using virtual screening with homology models. J. Med. Chem. 49, 1356-1563.
36. Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., Repasky, M. P., Knoll, E. H., Shelley, M., Perry, J. K., Shaw, D. E., Francis, P., and Shenkin, P. S. (2004) Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem. 47, 1739-1749.
37. Halgren, T. A., Murphy, R. B., Friesner, R. A., Beard, H. S., Frye, L. L., Pollard, W. T., and Banks, J. L. (2004) Glide: A new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J. Med. Chem. 47, 1750-1759.
38. Eldridge, M. D., Murray, C. W., Auton, T. R., Paolini, G. V., and Mee, R. P. (1997) Empirical scoring functions: I. The development of a fast empirical scoring function to estimate the binding affinity of ligands in receptor complexes. J. Comput. Aided Mol. Des. 11, 425-445.
39. Deschamps, J. D., Kenyon, V. A., and Holman, T. R. (2006) Baicalein is a potent in vitro inhibitor against both reticulocyte 15-human and platelet 12-human lipoxygenases. Bioorg. Med. Chem. 14, 4295-4301.
40. Klinman, J. P. (2006) The role of tunneling in enzyme catalysis of C-H activation. Biochim. Biophys. Acta 1757, 981-987.
41. Knapp, M. J., and Klinman, J. P. (2002) Environmentally coupled hydrogen tunneling. Linking catalysis to dynamics. Eur. J. Biochem. 269, 3113-3121.
42. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) Temperature- dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics. J. Am. Chem. Soc. 124, 3865-3874.
43. Edwards, S. J., Soudackov, A. V., and Hammes-Schiffer, S. (2009) Analysis of kinetic isotope effects for proton-coupled electron transfer reactions. J. Phys. Chem. A xxx.
44. Kiefer, P. M., and Hynes, J. T. (2004) Kinetic isotope effects for nonadiabatic proton transfer reactions in a polar environment. 1. Interpretation of tunneling kinetic isotopic effects. J. Phys. Chem. A 108, 11793-11808.
45. Tomchick, D. R., Phan, P., Cymborowski, M., Minor, W., and Holman, T. R. (2001) Structural and functional characterization of second-coordination sphere mutants of soybean lipoxygenase-1. Biochemistry 40, 7509-7517. (Pubitemid 32578015)
46. Zhang, Z., Harms, E., and Van Etten, R. L. (1994) Asp129 of low molecular weight protein tyrosine phosphatase is involved in leaving group protonation. J. Biol. Chem. 269, 25947-25950.
47. Mejillano, M. R., Shivanna, B. D., and Himes, R. H. (1996) Studies on the nocodazole-induced GTPase activity of tubulin. Arch. Biochem. Biophys. 336, 130-138.
48. Schneck, J. L., Villa, J. P., McDevitt, P., McQueney, M. S., Thrall, S. H., and Meek, T. D. (2008) Chemical mechanism of a cysteine protease, cathepsin C, as revealed by integration of both steady-state and pre-steady-state solvent kinetic isotope effects. Biochemistry 47, 8697-8710.
49. Quinn, D. M., Sutton, L. D. (1991) Enzyme Mechanism from Isotope Effects , CRC Press, Boca Raton, Fl.
50. Relyea, H. A., Vrtis, J. M., Woodyer, R., Rimkus, S. A., and van der Donk, W. A. (2005) Inhibition and pH dependence of phosphite dehydrogenase. Biochemistry 44, 6640-6649.
51. Bowers, P. M., and Klevit, R. E. (2000) Hydrogen bond geometry and 2H/1H fractionation in proteins. J. Am. Chem. Soc. 122, 1030-1033.
52. Lin, J., Westler, W. M., Cleland, W. W., Markley, J. L., and Frey, P. A. (1998) Fractionation factors and activation energies for exchange of the low barrier hydrogen bonding proton in peptidyl trifluoromethyl ketone complexes of chymotrypsin. Proc. Natl. Acad. Sci. U.S.A. 95, 14664-14668.
53. Kreevoy, M. M., and Liang, T. M. (2002) Structures and isotopic fractionation factors of complexes, A1HA2. J. Am. Chem. Soc. 102, 3315-3322.
54. Cosgrove, M. S., Loh, S. N., Ha, J. H., and Levy, H. R. (2002) The catalytic mechanism of glucose 6-phosphate dehydrogenases: assignment and 1H NMR spectroscopy pH titration of the catalytic histidine residue in the 109 kDa Leuconostoc mesenteroides enzyme. Biochemistry 41, 6939-6945.
55. Segal, I. H. (1993) Enzyme Kinetics: Behavior and Analysis of Equilibrium and Steady-State Enzyme Systems , John Wiley & Sons, Inc., New York.
56. Mogul, R., and Holman, T. R. (2001) Inhibition studies of soybean and human 15-lipoxygenases with long-chain alkenyl sulfate substrates. Biochemistry 40, 4391-4397. (Pubitemid 32319584)
57. Thuresson, E. D., Lakkides, K. M., and Smith, W. L. (2000) Different catalytically competent arrangements of arachidonic acid within the cyclooxygenase active site of prostaglandin endoperoxide H synthase-1 lead to the formation of different oxygenated products. J. Biol. Chem. 275, 8501-8507.
58. Di Venere, A., Salucci, M. L., van Zadelhoff, G., Veldink, G., Mei, G., Rosato, N., Finazzi-Agro, A., and Maccarrone, M. (2003) Structure-to-function relationship of mini-lipoxygenase, a 60-kDa fragment of soybean lipoxygenase-1 with lower stability but higher enzymatic activity. J. Biol. Chem. 278, 18281-18288.
59. Shappell, S. B. B., W., E., Olson, S. J., Kasper, S., and Brash, A. R. (1999) 15-lipoxygenase-2 (15-LOX-2) is expressed in benign prostatic epithelium and reduced in prostate adenocarcinoma. J. Am. Pathol. 155, 235-245.
60. Tang, D. G., Bhatia, B., Tang, S., and Schneider-Broussard, R. (2007) 15-lipoxygenase 2 (15-LOX2) is a functional tumor suppressor that regulates human prostate epithelial cell differentiation, senescence, and growth (size). Prostaglandins Other Lipid Mediat 82, 135-146.
61. Hsi, L. C., Wilson, L. C., and Eling, T. E. (2002) Opposing effects of 15-lipoxygenase-1 and -2 metabolites on MAPK signaling in prostate. Alteration in peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 277, 40549-40556.
62. Schewe, T. (2002) 15-lipoxygenase-1: a prooxidant enzyme. Biol. Chem. 383, 365-374.