Investigations of human platelet-type 12-lipoxygenase: Role of lipoxygenase products in platelet activation

Journal of Lipid Research

Volumn 53, Issue 12, 2012, Pages 2546-2559

  Ikei, Kenneth N ^a   Yeung, Jennifer ^b   Apopa, Patrick L ^b   Ceja, Jesús ^a   Vesci, Joanne ^b   Holman, Theodore R ^a   Holinstat, Michael ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Eicosanoids; Fatty acid oxidation; Thrombin; Thrombosis

Indexed keywords

12 HYDROPEROXY 8,10,14 ICOSATRIENOIC ACID; ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONIC ACID; DIHOMO GAMMA LINOLENIC ACID; EICOSADIENOIC ACID; ESSENTIAL FATTY ACID; ICOSAPENTAENOIC ACID; INTEGRIN; LINOLEIC ACID; LINOLENIC ACID; PROTEIN ALPHAIIBBETA3; RAP1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BLOOD CLOT RETRACTION; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME METABOLISM; ENZYME RELEASE; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; METABOLIC REGULATION; NORMAL HUMAN; PRIORITY JOURNAL; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION;

ARACHIDONATE 12-LIPOXYGENASE; FATTY ACIDS, ESSENTIAL; HUMANS; OXIDATION-REDUCTION; PLATELET ACTIVATION; SUBSTRATE SPECIFICITY;

EID: 84869061348     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M026385     Document Type: Article

References (66)

1. Solomon, E. I., J. Zhou, F. Neese, and E. G. Pavel. 1997. New insights from spectroscopy into the structure/function relationships of lipoxygenases. Chem. Biol. 4: 795-808. (Pubitemid 28000620)
2. Serhan, C. N. 1994. Lipoxin biosynthesis and its impact in inflammatory and vascular events. Biochim. Biophys. Acta. 1212: 1-25. (Pubitemid 24123884)
3. Nakano, H., T. Inoue, N. Kawasaki, H. Miyataka, H. Matsumoto, T. Taguchi, N. Inagaki, H. Nagai, and T. Satoh. 2000. Synthesis and biological activities of novel antiallergic agents with 5-lipoxygenase inhibiting action. Bioorg. Med. Chem. 8: 373-380. (Pubitemid 30122778)
4. Ghosh, J., and C. E. Myers. 1998. Inhibition of arachidonate 5-lipoxygenase triggers massive apoptosis in human prostate cancer cells. Proc. Natl. Acad. Sci. USA. 95: 13182-13187. (Pubitemid 28509545)
5. Steele, V. E., C. A. Holmes, E. T. Hawk, L. Kopelovich, R. A. Lubet, J. A. Crowell, C. C. Sigman, and G. J. Kelloff. 1999. Lipoxygenase inhibitors as potential cancer chemopreventives. Cancer Epidemiol. Biomarkers Prev. 8: 467-483. (Pubitemid 29230553)
6. Hussain, H., L. P. Shornick, V. R. Shannon, J. D. Wilson, C. D. Funk, A. P. Pentland, and M. J. Holtzman. 1994. Epidermis contains platelet-type 12-lipoxygenase that is overexpressed in germinal layer keratinocytes in psoriasis. Am. J. Physiol. 266: C243-C253. (Pubitemid 24058306)
7. Quintana, L. F., B. Guzman, S. Collado, J. Claria, and E. Poch. 2006. A coding polymorphism in the 12-lipoxygenase gene is associated to essential hypertension and urinary 12(S)-HETE. Kidney Int. 69: 526-530. (Pubitemid 43164445)
8. Zink, M. H., C. L. Oltman, T. Lu, P. V. Katakam, T. L. Kaduce, H. Lee, K. C. Dellsperger, A. A. Spector, P. R. Myers, and N. L. Weintraub. 2001. 12-lipoxygenase in porcine coronary microcirculation: implications for coronary vasoregulation. Am. J. Physiol. Heart Circ. Physiol. 280: H693-H704.
9. Fonlupt, P., M. Croset, and M. Lagarde. 1991. 12-HETE inhibits the binding of PGH2/TXA2 receptor ligands in human platelets. Thromb. Res. 63: 239-248.
10. Nyby, M. D., M. Sasaki, Y. Ideguchi, H. E. Wynne, M. T. Hori, M. E. Berger, M. S. Golub, A. S. Brickman, and M. L. Tuck. 1996. Platelet lipoxygenase inhibitors attenuate thrombin- and thromboxane mimetic-induced intracellular calcium mobilization and platelet aggregation. J. Pharmacol. Exp. Ther. 278: 503-509. (Pubitemid 27167012)
11. Olas, B., B. Wachowicz, A. Stochmal, and W. Oleszek. 2005. Inhibition of blood platelet adhesion and secretion by different phenolics from Yucca schidigera Roezl. bark. Nutrition. 21: 199-206. (Pubitemid 40255730)
12. Yeung, J., P. L. Apopa, J. Vesci, V. Kenyon, G. Rai, A. Jadhav, A. Simeonov, T. R. Holman, D. J. Maloney, O. Boutaud, et al. 2012. Protein kinase C regulation of 12-lipoxygenase-mediated human platelet activation. Mol. Pharmacol. 81: 420-430.
13. Ma, K., C. S. Nunemaker, R. Wu, S. K. Chakrabarti, D. A. Taylor- Fishwick, and J. L. Nadler. 2010. 12-Lipoxygenase products reduce insulin secretion and {beta}-cell viability in human islets. J. Clin. Endocrinol. Metab. 95: 887-893.
14. Tohjima, T., N. Honda, K. Mochizuki, J. Kinoshita, K. Watanabe, T. Arisaka, R. Kawamori, M. Nakamura, Y. Kurahashi, T. Yoshimoto, et al. 1998. Decreased activity of arachidonate 12-lipoxygenase in platelets of Japanese patients with non-insulin-dependent diabetes mellitus. Metabolism. 47: 257-263. (Pubitemid 28108770)
15. Connolly, J. M., and D. P. Rose. 1998. Enhanced angiogenesis and growth of 12-lipoxygenase gene-transfected MCF-7 human breast cancer cells in athymic nude mice. Cancer Lett. 132: 107-112. (Pubitemid 28535191)
16. Natarajan, R., and J. Nadler. 1998. Role of lipoxygenases in breast cancer. Front. Biosci. 3: E81-E88.
17. Harats, D., A. Shaish, J. George, M. Mulkins, H. Kurihara, H. Levkovitz, and E. Sigal. 2000. Overexpression of 15-lipoxygenase in vascular endothelium accelerates early atherosclerosis in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 20: 2100-2105.
18. Kamitani, H., M. Geller, and T. Eling. 1998. Expression of 15-lipoxygenase by human colorectal carcinoma Caco-2 cells during apoptosis and cell differentiation. J. Biol. Chem. 273: 21569-21577. (Pubitemid 28405326)
19. Chen, X-S., A. R. Brash, and C. D. Funk. 1993. Purification and characterization of recombinant histidine-tagged human platelet 12-lipoxygenase expressed in a baculovirus/insect cell system. Eur. J. Biochem. 214: 845-852. (Pubitemid 23188162)
20. Boeglin, W. E., R. B. Kim, and A. R. Brash. 1998. A 12R-lipoxygenase in human skin: mechanistic evidence, molecular cloning, and expression. Proc. Natl. Acad. Sci. USA. 95: 6744-6749. (Pubitemid 28278051)
21. Holinstat, M., O. Boutaud, P. L. Apopa, J. Vesci, M. Bala, J. A. Oates, and H. E. Hamm. 2011. Protease-activated receptor signaling in platelets activates cytosolic phospholipase A2alpha differently for cyclooxygenase-1 and 12-lipoxygenase catalysis. Arterioscler. Thromb. Vasc. Biol. 31: 435-442.
22. Morgan, L. T., C. P. Thomas, H. Kuhn, and V. B. O'Donnell. 2010. Thrombin-activated human platelets acutely generate oxidized docosahexaenoic-acid-containing phospholipids via 12-lipoxygenase. Biochem. J. 431: 141-148.
23. Thomas, C. P., L. T. Morgan, B. H. Maskrey, R. C. Murphy, H. Kuhn, S. L. Hazen, A. H. Goodall, H. A. Hamali, P. W. Collins, and V. B. O'Donnell. 2010. Phospholipid-esterified eicosanoids are generated in agonist-activated human platelets and enhance tissue factor-dependent thrombin generation. J. Biol. Chem. 285: 6891-6903.
24. Yeung, J., and M. Holinstat. 2011. 12-lipoxygenase: a potential target for novel anti-platelet therapeutics. Cardiovasc. Hematol. Agents Med. Chem. 9: 154-164.
25. Burke, J. E., and E. A. Dennis. 2009. Phospholipase A2 biochemistry. Cardiovasc. Drugs Ther. 23: 49-59.
26. Barre, D. E., and B. J. Holub. 1992. The effect of borage oil consumption on the composition of individual phospholipids in human platelets. Lipids. 27: 315-320.
27. Johnson, M. M., D. D. Swan, M. E. Surette, J. Stegner, T. Chilton, A. N. Fonteh, and F. H. Chilton. 1997. Dietary supplementation with gamma-linolenic acid alters fatty acid content and eicosanoid production in healthy humans. J. Nutr. 127: 1435-1444. (Pubitemid 27323451)
28. Kris-Etherton, P., S. R. Daniels, R. H. Eckel, M. Engler, B. V. Howard, R. M. Krauss, A. H. Lichtenstein, F. Sacks, S. St Jeor, M. Stampfer, et al. 2001. Summary of the scientific conference on dietary fatty acids and cardiovascular health: conference summary from the nutrition committee of the American Heart Association. Circulation. 103: 1034-1039. (Pubitemid 32183813)
29. Simopoulos, A. P. 2006. Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biomed. Pharmacother. 60: 502-507. (Pubitemid 44635081)
30. Kapoor, R., and Y. S. Huang. 2006. Gamma linolenic acid: an antiinflammatory omega-6 fatty acid. Curr. Pharm. Biotechnol. 7: 531-534. (Pubitemid 46017544)
31. Segraves, E. N., and T. R. Holman. 2003. Kinetic investigations of the rate-limiting step in human 12- and 15-lipoxygenase. Biochemistry. 42: 5236-5243. (Pubitemid 36560419)
32. Wecksler, A. T., C. Jacquot, W. A. van der Donk, and T. R. Holman. 2009. Mechanistic investigations of human reticulocyte 15- and platelet 12-lipoxygenases with arachidonic acid. Biochemistry. 48: 6259-6267.
33. Amagata, T., S. Whitman, T. A. Johnson, C. C. Stessman, C. P. Loo, E. Lobkovsky, J. Clardy, P. Crews, and T. R. Holman. 2003. Exploring sponge-derived terpenoids for their potency and selectivity against 12-human, 15-human, and 15-soybean lipoxygenases. J. Nat. Prod. 66: 230-235. (Pubitemid 36278235)
34. Chen, X. S., and C. D. Funk. 1993. Structure-function properties of human platelet 12-lipoxygenase: chimeric enzyme and in vitro mutagenesis studies. FASEB J. 7: 694-701.
35. Murphy, R. C., R. M. Barkley, K. Zemski Berry, J. Hankin, K. Harrison, C. Johnson, J. Krank, A. McAnoy, C. Uhlson, and S. Zarini. 2005. Electrospray ionization and tandem mass spectrometry of eicosanoids. Anal. Biochem. 346: 1-42. (Pubitemid 41456623)
36. Graff, G., L. A. Anderson, and L. W. Jaques. 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. (Pubitemid 20215872)
37. Hoye, T. R., C. S. Jeffrey, and F. Shao. 2007. Mosher ester analysis for the determination of absolute configuration of stereogenic (chiral) carbinol carbons. Nat. Protoc. 2: 2451-2458.
38. Holinstat, M., B. Voss, M. L. Bilodeau, J. N. McLaughlin, J. Cleator, and H. E. Hamm. 2006. PAR4, but not PAR1, signals human platelet aggregation via Ca2+ mobilization and synergistic P2Y12 receptor activation. J. Biol. Chem. 281: 26665-26674. (Pubitemid 44401875)
39. Holinstat, M., A. M. Preininger, S. B. Milne, W. J. Hudson, H. A. Brown, and H. E. Hamm. 2009. Irreversible platelet activation requires protease-activated receptor 1-mediated signaling to phosphatidylinositol phosphates. Mol. Pharmacol. 76: 301-313.
40. van Triest, M., J. de Rooij, and J. L. Bos. 2001. Measurement of GTP-bound Ras-like GTPases by activation-specific probes. Methods Enzymol. 333: 343-348.
41. Gong, H., B. Shen, P. Flevaris, C. Chow, S. C. Lam, T. A. Voyno-Yasenetskaya, T. Kozasa, and X. Du. 2010. G protein subunit Galpha13 binds to integrin alphaIIbbeta3 and mediates integrin "outside-in" signaling. Science. 327: 340-343.
42. Ivanov, I., D. Heydeck, K. Hofheinz, J. Roffeis, V. B. O'Donnell, H. Kuhn, and M. Walther. 2010. Molecular enzymology of lipoxygenases. Arch. Biochem. Biophys. 503: 161-174.
43. Knapp, M. J., F. P. Seebeck, and J. P. Klinman. 2001. Steric control of oxygenation regiochemistry in soybean lipoxygenase-1. J. Am. Chem. Soc. 123: 2931-2932. (Pubitemid 32910739)
44. Gomolka, B., E. Siegert, K. Blossey, W. H. Schunck, M. Rothe, and K. H. Weylandt. 2011. Analysis of omega-3 and omega-6 fatty acid-derived lipid metabolite formation in human and mouse blood samples. Prostaglandins Other Lipid Mediat. 94: 81-87.
45. Harper, C. R., M. J. Edwards, A. P. DeFilippis, and T. A. Jacobson. 2006. Flaxseed oil increases the plasma concentrations of cardioprotective (n-3) fatty acids in humans. J. Nutr. 136: 83-87. (Pubitemid 43156489)
46. Holy, E. W., M. Forestier, E. K. Richter, A. Akhmedov, F. Leiber, G. G. Camici, P. Mocharla, T. F. Luscher, J. H. Beer, and F. C. Tanner. 2011. Dietary alpha-linolenic acid inhibits arterial thrombus formation, tissue factor expression, and platelet activation. Arterioscler. Thromb. Vasc. Biol. 31: 1772-1780.
47. Siess, W., F. L. Siegel, and E. G. Lapetina. 1984. Dihomogammalinolenic acid, but not eicosapentaenoic acid, activates washed human platelets. Biochim. Biophys. Acta. 801: 265-276. (Pubitemid 14007750)
48. Flevaris, P., A. Stojanovic, H. Gong, A. Chishti, E. Welch, and X. Du. 2007. A molecular switch that controls cell spreading and retraction. J. Cell Biol. 179: 553-565. (Pubitemid 350074797)
49. von Schacky, C., and P. C. Weber. 1985. Metabolism and effects on platelet function of the purified eicosapentaenoic and docosahexaenoic acids in humans. J. Clin. Invest. 76: 2446-2450.
50. Bergstroem, S., H. Danielsson, D. Klenberg, and B. Samuelsson. 1964. The enzymatic conversion of essential fatty acids into prostaglandins. J. Biol. Chem. 239: PC4006-PC4008.
51. Falardeau, P., M. Hamberg, and B. Samuelsson. 1976. Metabolism of 8,11,14-eicosatrienoic acid in human platelets. Biochim. Biophys. Acta. 441: 193-200.
52. Needleman, P., M. O. Whitaker, A. Wyche, K. Watters, H. Sprecher, and A. Raz. 1980. Manipulation of platelet aggregation by prostaglandins and their fatty acid precursors: pharmacological basis for a therapeutic approach. Prostaglandins. 19: 165-181. (Pubitemid 10095106)
53. Gan, Q. F., M. F. Browner, D. L. Sloane, and E. Sigal. 1996. Defining the arachidonic acid binding site of human 15-lipoxygenase. Molecular modeling and mutagenesis. J. Biol. Chem. 271: 25412-25418. (Pubitemid 26337913)
54. Rickert, K. W., and J. P. Klinman. 1999. Nature of hydrogen transfer in soybean lipoxygenase-1: separation of primary and secondary isotope effects. Biochemistry. 38: 12218-12228.
55. Guo, Y., W. Zhang, C. Giroux, Y. Cai, P. Ekambaram, A-K. Dilly, A. Hsu, S. Zhou, K. R. Maddipati, J. Liu, et al. 2011. Identification of the orphan G protein coupled receptor GPR31 as a receptor for 12(S) hydroxyeicosatetraenoic acid. J. Biol. Chem. 286: 33832-33840.
56. Zafiriou, M. P., R. Deva, R. Ciccoli, A. Siafaka-Kapadai, and S. Nigam. 2007. Biological role of hepoxilins: upregulation of phospholipid hydroperoxide glutathione peroxidase as a cellular response to oxidative stress? Prostaglandins Leukot. Essent. Fatty Acids. 77: 209-215. (Pubitemid 350148263)
57. Kernoff, P. B., A. L. Willis, K. J. Stone, J. A. Davies, and G. P. McNicol. 1977. Antithrombotic potential of dihomo-gamma-linolenic acid in man. BMJ. 2: 1441-1444. (Pubitemid 8230392)
58. Fan, Y. Y., and R. S. Chapkin. 1998. Importance of dietary gamma-linolenic acid in human health and nutrition. J. Nutr. 128: 1411-1414.
59. Surette, M. E., I. L. Koumenis, M. B. Edens, K. M. Tramposch, B. Clayton, D. Bowton, and F. H. Chilton. 2003. Inhibition of leukotriene biosynthesis by a novel dietary fatty acid formulation in patients with atopic asthma: a randomized, placebo-controlled, parallel-group, prospective trial. Clin. Ther. 25: 972-979. (Pubitemid 36459701)
60. Levin, G., K. L. Duffin, M. G. Obukowicz, S. L. Hummert, H. Fujiwara, P. Needleman, and A. Raz. 2002. Differential metabolism of dihomo-gamma-linolenic acid and arachidonic acid by cyclo-oxygenase-1 and cyclo-oxygenase-2: implications for cellular synthesis of prostaglandin E1 and prostaglandin E2. Biochem. J. 365: 489-496. (Pubitemid 36135320)
61. Takai, S., D. Jin, H. Kawashima, M. Kimura, A. Shiraishi-Tateishi, T. Tanaka, S. Kakutani, K. Tanaka, Y. Kiso, and M. Miyazaki. 2009. Anti-atherosclerotic effects of dihomo-gamma-linolenic acid in ApoE-deficient mice. J. Atheroscler. Thromb. 16: 480-489.
62. Willis, A. L., and D. L. Smith. 1989. Therapeutic impact of eicosanoids in atherosclerotic disease. Eicosanoids. 2: 69-99.
63. Aragona, P., C. Bucolo, R. Spinella, S. Giuffrida, and G. Ferreri. 2005. Systemic omega-6 essential fatty acid treatment and pge1 tear content in Sjogren's syndrome patients. Invest. Ophthalmol. Vis. Sci. 46: 4474-4479. (Pubitemid 44264541)
64. Laidlaw, M., and B. J. Holub. 2003. Effects of supplementation with fish oil-derived n-3 fatty acids and gamma-linolenic acid on circulating plasma lipids and fatty acid profiles in women. Am. J. Clin. Nutr. 77: 37-42. (Pubitemid 36015370)
65. Hurtado de Catalfo, G. E., and I. N. de Gomez Dumm. 1996. Spontaneously hypertensive rats: eicosa-8,11,14-trienoic acid metabolism and arachidonic acid biosynthesis. Biochem. Mol. Biol. Int. 40: 759-768.
66. Manku, M. S., M. Oka, and D. F. Horrobin. 1979. Differential regulation of the formation of prostaglandins and related substances from arachidonic acid and from dihomogammalinolenic acid. II. Effects of vitamin C. Prostaglandins Med. 3: 129-137.