Activated platelets contribute to oxidized low-density lipoproteins and dysfunctional high-density lipoproteins through a phospholipase A2-dependent mechanism

FASEB Journal

Volumn 26, Issue 2, 2012, Pages 927-937

  Blache, Denis ^a   Gautier, Thomas ^a   Tietge, Uwe J F ^b   Lagrost, Laurent ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Oxidative stress; Thrombosis

Indexed keywords

FATTY ACID; HIGH DENSITY LIPOPROTEIN; LEPTIN; LY 311727; LYSOPHOSPHATIDYLCHOLINE; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHOLIPASE A2; PHOSPHOLIPASE INHIBITOR; TICLOPIDINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BLOOD CLOTTING TIME; FEMALE; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; OXIDATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; RAT; THROMBOCYTE; THROMBOSIS;

ANIMALS; ATHEROSCLEROSIS; BLOOD PLATELETS; ENZYME INHIBITORS; FEMALE; GROUP II PHOSPHOLIPASES A2; HUMANS; INDOLES; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; PLATELET ACTIVATION; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; TICLOPIDINE;

MUS;

EID: 84856515327     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-191593     Document Type: Article

References (63)

1. Boyanovsky, B. B., and Webb, N. R. (2009) Biology of secretory phospholipase A2. Cardiovasc. Drugs Ther. 23, 61-72
2. Burke, J. E., and Dennis, E. A. (2009) Phospholipase A2 biochemistry. Cardiovasc. Drugs Ther. 23, 49-59
3. Arbibe, L., Koumanov, K., Vial, D., Rougeot, C., Faure, G., Havet, N., Longacre, S., Vargaftig, B. B., Bereziat, G., Voelker, D. R., Wolf, C., and Touqui, L. (1998) Generation of lysophospholipids from surfactant in acute lung injury is mediated by type-II phospholipase A2 and inhibited by a direct surfactant protein A-phospholipase A2 protein interaction. J. Clin. Invest. 102, 1152-1160 (Pubitemid 28436275)
4. 2 in normal and atherosclerotic arteries - activity of the isolated enzyme on low-density lipoproteins. Arterioscler. Thomb. Vasc. Biol. 17, 300-309
5. Oorni, K., and Kovanen, P. T. (2009) Lipoprotein modification by secretory phospholipase A(2) enzymes contributes to the initiation and progression of atherosclerosis. Curr. Opin. Lipidol. 20, 421-427
6. Garces, F., Lopez, F., Nino, C., Fernandez, A., Chacin, L., Hurt-Camejo, E., Camejo, G., and Apitz-Castro, R. (2010) High plasma phospholipase A2 activity, inflammation markers, and LDL alterations in obesity with or without type 2 diabetes. Obesity 18, 2023-2029
7. Leinonen, E. S., Hiukka, A., Hurt-Camejo, E., Wiklund, O., Sarna, S. S., Mattson, H. L., Westerbacka, J., Salonen, R. M., Salonen, J. T., and Taskinen, M. R. (2004) Low-grade inflammation, endothelial activation and carotid intima-media thickness in type 2 diabetes. J. Intern. Med. 256, 119-127 (Pubitemid 38998258)
8. Mattsson, N., Magnussen, C. G., Ronnemaa, T., Mallat, Z., Benessiano, J., Jula, A., Taittonen, L., Kahonen, M., Juonala, M., Viikari, J. S., and Raitakari, O. T. (2010) Metabolic syndrome and carotid intima-media thickness in young adults: roles of apolipoprotein B, apolipoprotein A-I, C-reactive protein, and secretory phospholipase A2: the cardiovascular risk in young Finns study. Arterioscler. Thromb. Vasc. Biol. 30, 1861-1866
9. Kugiyama, K., Ota, Y., Takazoe, K., Moriyama, Y., Kawano, H., Miyao, Y., Sakamoto, T., Soejima, H., Ogawa, H., Doi, H., Sugiyama, S., and Yasue, H. (1999) Circulating levels of secretory type II phospholipase A(2) predict coronary events in patients with coronary artery disease. Circulation 100, 1280-1284 (Pubitemid 29440119)
10. Mallat, Z., Benessiano, J., Simon, T., Ederhy, S., Sebella-Arguelles, C., Cohen, A., Huart, V., Wareham, N. J., Luben, R., Khaw, K. T., Tedgui, A., and Boekholdt, S. M. (2007) Circulating secretory phospholipase A2 activity and risk of incident coronary events in healthy men and women: the EPIC-Norfolk study. Arterioscler. Thromb. Vasc. Biol. 27, 1177-1183 (Pubitemid 46641976)
11. Davi, G., and Patrono, C. (2007) Platelet activation and atherothrombosis. N. Engl. J. Med. 357, 2482-2494
12. Gawaz, M., Langer, H., and May, A. E. (2005) Platelets in inflammation and atherogenesis. J. Clin. Invest. 115, 3378-3384 (Pubitemid 43121822)
13. Rauch, U., Osende, J. I., Fuster, V., Badimon, J. J., Fayad, Z., and Chesebro, J. H. (2001) Thrombus formation on atherosclerotic plaques: pathogenesis and clinical consequences. Ann. Intern. Med. 134, 224-238 (Pubitemid 32113325)
14. Singh, U., and Jialal, I. (2006) Oxidative stress and atherosclerosis. Pathophysiology 13, 129-142
15. Fogelman, A. M., Shechter, I., Seager, J., Hokom, M., Child, J. S., and Edwards, P. A. (1980) Malondialdehyde alteration of low density lipoproteins leads to cholesteryl ester accumulation in human monocyte-macrophages. Proc. Natl. Acad. Sci. U. S. A. 77, 2214-2218 (Pubitemid 10089629)
16. Aviram, M., Dankner, G., and Brook, J. G. (1990) Platelet secretory products increase low density lipoprotein oxidation, enhance its uptake by macrophages, and reduce its fluidity. Arteriosclerosis 10, 559-563 (Pubitemid 20220579)
17. Krotz, F., Sohn, H. Y., and Pohl, U. (2004) Reactive oxygen species: players in the platelet game. Arterioscler. Thromb. Vasc. Biol. 24, 1988-1996 (Pubitemid 39482420)
18. Huo, Y., Schober, A., Forlow, S. B., Smith, D. F., Hyman, M. C., Jung, S., Littman, D. R., Weber, C., and Ley, K. (2003) Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat. Med. 9, 61-67 (Pubitemid 36098261)
19. Massberg, S., Brand, K., Gruner, S., Page, S., Muller, E., Muller, I., Bergmeier, W., Richter, T., Lorenz, M., Konrad, I., Nieswandt, B., and Gawaz, M. (2002) A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J. Exp. Med. 196, 887-896
20. Jawien, J., Csanyi, G., Gajda, M., Mateuszuk, L., Lomnicka, M., Korbut, R., and Chlopicki, S. (2007) Ticlopidine attenuates progression of atherosclerosis in apolipoprotein E and low density lipoprotein receptor double knockout mice. Eur. J. Pharmacol. 556, 129-135 (Pubitemid 46074012)
21. Carnevale, R., Pignatelli, P., Lenti, L., Buchetti, B., Sanguigni, V., Di Santo, S., and Violi, F. (2007) LDL are oxidatively modified by platelets via GP91(phox) and accumulate in human monocytes. FASEB J. 21, 927-934 (Pubitemid 46348265)
22. Tietge, U. J., Maugeais, C., Cain, W., Grass, D., Glick, J. M., De Beer, F. C., and Rader, D. J. (2000) Overexpression of secretory phospholipase A(2) causes rapid catabolism and altered tissue uptake of high density lipoprotein cholesteryl ester and apolipoprotein A-I. J. Biol. Chem. 275, 10077-10084 (Pubitemid 30202058)
23. Grass, D. S., Felkner, R. H., Chiang, M. Y., Wallace, R. E., Nevalainen, T. J., Bennett, C. F., and Swanson, M. E. (1996) Expression of human group II PLA2 in transgenic mice results in epidermal hyperplasia in the absence of inflammatory infiltrate. J. Clin. Invest. 97, 2233-2241 (Pubitemid 26165712)
24. Bodary, P. F., Gu, S., Shen, Y., Hasty, A. H., Buckler, J. M., and Eitzman, D. T. (2005) Recombinant leptin promotes atherosclerosis and thrombosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 25, e119-e122
25. Blache, D. (1995) Involvement of hydrogen and lipid peroxides in the acute tobacco smoking-induced platelet hyperactivity. Am. J. Physiol. 268, H679-H685
26. Blache, D., Devaux, S., Joubert, O., Loreau, N., Schneider, M., Durand, P., Prost, M., Gaume, V., Adrian, M., Laurant, P., and Berthelot, A. (2006) Long-term moderate magnesium-deficient diet shows relationships between blood pressure, inflammation and oxidant stress defense in aging rats. Free Radic. Biol. Med. 41, 277-284 (Pubitemid 43949467)
27. Kurz, K. D., Main, B. W., and Sandusky, G. E. (1990) Rat model of arterial thrombosis induced by ferric chloride. Thromb. Res. 60, 269-280
28. Hatch, F. T. (1968) Practical methods for plasma lipoprotein analysis. Adv. Lipid Res. 6, 1-68
29. Gesquière, L., Loreau, N., and Blache, D. (1997) Impaired cellular cholesterol efflux by oxysterol-enriched high density lipoproteins. Free Radic. Biol. Med. 23, 541-547 (Pubitemid 27287337)
30. Basu, S. K., Goldstein, J. L., Anderson, R. G. W., and Brown, M. S. (1976) Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 73, 3178-3182
31. El-Saadani, M., Esterbauer, H., El-Sayed, M., Goher, M., Nassar, A. Y., and Jürgens, G. (1989) A spectrophotometric assay for lipid peroxides in serum lipoproteins using a commercially available reagent. J. Lipid Res. 30, 627-630 (Pubitemid 19107750)
32. Blache, D., Rodriguez, C., and Davignon, J. (1995) Pro-oxidant effects of 7-hydroperoxycholest-5-en-3β-ol on the copper-initiated oxidation of low density lipoprotein. FEBS Lett. 357, 135-139
33. Blache, D., Durand, P., Girodon, F., Gesquière, L., and Loreau, N. (1998) Determination of sterols, oxysterols and fatty acids of phospholipids in cells and lipoproteins: a one sample method. J. Am. Oil Chem. Soc. 75, 107-113 (Pubitemid 128607965)
34. Polette, A., and Blache, D. (1992) Effect of vitamin E on acute iron load-potentiated aggregation, secretion, calcium uptake and thromboxane biosynthesis in rat platelets. Atherosclerosis 96, 171-179
35. Steinbrecher, U. P., Witztum, J. L., Parthasarathy, S., and Steinberg, D. (1987) Decrease in reactive amino groups during oxidation or endothelial cell modificaiton of LDL. Correlation with changes in receptor-mediated catabolism. Arteriosclerosis 7, 135-143 (Pubitemid 17061134)
36. Gesquière, L., Loreau, N., Minnich, A., Davignon, J., and Blache, D. (1999) Oxidative stress leads to cholesterol accumulation in vascular smooth muscle cells. Free Radic. Biol. Med. 27, 134-145 (Pubitemid 29353094)
37. Gesquière, L., Loreau, N., and Blache, D. (2000) Role of the cyclic AMP-dependent pathway in free radical-induced cholesterol accumulation in vascular smooth muscle cells. Free Radic. Biol. Med. 29, 181-190
38. Rosenblat, M., Belinky, P., Vaya, J., Levy, R., Hayek, T., Coleman, R., Merchav, S., and Aviram, M. (1999) Macrophage enrichment with the isoflavan glabridin inhibits NADPH oxidase-induced cell-mediated oxidation of low density lipoprotein. A possible role for protein kinase C. J. Biol. Chem. 274, 13790-13799
39. Witztum, J. L., and Steinberg, D. (1991) Role of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 88, 1785-1792
40. Kennedy, B. P., Payette, P., Mudgett, J., Vadas, P., Pruzanski, W., Kwan, M., Tang, C., Rancourt, D. E., and Cromlish, W. A. (1995) A natural disruption of the secretory group II phospholipase A2 gene in inbred mouse strains. J. Biol. Chem. 270, 22378-22385
41. Porela, P., Pulkki, K., Voipio-Pulkki, L. M., Pettersson, K., Leppanen, V., and Nevalainen, T. J. (2000) Level of circulating phospholipase A2 in prediction of the prognosis of patients with suspected myocardial infarction. Basic Res. Cardiol. 95, 413-417
42. Koenig, W., Vossen, C. Y., Mallat, Z., Brenner, H., Benessiano, J., and Rothenbacher, D. (2009) Association between type II secretory phospholipase A2 plasma concentrations and activity and cardiovascular events in patients with coronary heart disease. Eur. Heart J. 30, 2742-2748
43. Van der Giet, M., Tölle, M., Pratico, D., Lufft, V., Schuchardt, M., Hörl, M. P., Zidek, W., and Tietge, U. J. (2010) Increased type IIA secretory phospholipase A2 expression contributes to oxidative stress in end-stage renal disease. J. Mol. Med. 88, 75-83
44. Kugiyama, K., Ota, Y., Sugiyama, S., Kawano, H., Doi, H., Soejima, H., Miyamoto, S., Ogawa, H., Takazoe, K., and Yasue, H. (2000) Prognostic value of plasma levels of secretory type II phospholipase A2 in patients with unstable angina pectoris. Am. J. Cardiol. 86, 718-722
45. Rosengren, B., Peilot, H., Umaerus, M., Jonsson-Rylander, A. C., Mattsson-Hulten, L., Hallberg, C., Cronet, P., Rodriguez-Lee, M., and Hurt-Camejo, E. (2006) Secretory phospholipase A2 group V: lesion distribution, activation by arterial proteoglycans, and induction in aorta by a Western diet. Arterioscler. Thromb. Vasc. Biol. 26, 1579-1585 (Pubitemid 44288986)
46. Sato, H., Kato, R., Isogai, Y., Saka, G., Ohtsuki, M., Taketomi, Y., Yamamoto, K., Tsutsumi, K., Yamada, J., Masuda, S., Ishikawa, Y., Ishii, T., Kobayashi, T., Ikeda, K., Taguchi, R., Hatakeyama, S., Hara, S., Kudo, I., Itabe, H., and Murakami, M. (2008) Analyses of group III secreted phospholipase A2 transgenic mice reveal potential participation of this enzyme in plasma lipoprotein modification, macrophage foam cell formation, and atherosclerosis. J. Biol. Chem. 283, 33483-33497
47. Magrioti, V., and Kokotos, G. (2010) Phospholipase A2 inhibitors as potential therapeutic agents for the treatment of inflammatory diseases. Expert Opin. Ther. Pat. 20, 1-18
48. Rosenson, R. S., Hislop, C., McConnell, D., Elliott, M., Stasiv, Y., Wang, N., and Waters, D. D. (2009) Effects of 1-H-indole-3-glyoxamide (A-002) on concentration of secretory phospholipase A2 (PLASMA study): a phase II double-blind, randomised, placebo-controlled trial. Lancet 373, 649-658
49. Blache, D., Durand, P., Prost, M., and Loreau, N. (2002) (+)-Catechin inhibits platelet hyperactivity induced by an acute iron load in vivo. Free Radic. Biol. Med. 33, 1670-1680 (Pubitemid 35462007)
50. Gesquiere, L., Cho, W., and Subbaiah, P. V. (2002) Role of group IIa and group V secretory phospholipases A(2) in the metabolism of lipoproteins. Substrate specificities of the enzymes and the regulation of their activities by sphingomyelin. Biochemistry 41, 4911-4920 (Pubitemid 34298658)
51. Singer, A. G., Ghomashchi, F., Le Calvez, C., Bollinger, J., Bezzine, S., Rouault, M., Sadilek, M., Nguyen, E., Lazdunski, M., Lambeau, G., and Gelb, M. H. (2002) Interfacial kinetic and binding properties of the complete set of human and mouse groups I, II, V, X, and XII secreted phospholipases A2. J. Biol. Chem. 277, 48535-48549 (Pubitemid 35470814)
52. 2. Biochim. Biophys. Acta Lipids Lipid Metab. 1214, 88-96
53. Korotaeva, A. A., Samoilova, E. V., Piksina, G. F., and Prokazova, N. V. (2010) Oxidized phosphatidylcholine stimulates activity of secretory phospholipase A2 group IIA and abolishes sphingomyelin-induced inhibition of the enzyme. Prostaglandins Other Lipid Mediat. 91, 38-41
54. Hurt-Camejo, E., and Camejo, G. (1997) Potential involvement of type II phospholipase A2 in atherosclerosis. Atherosclerosis 132, 1-8 55.
55. Jaross, W., Eckey, R., and Menschikowski, M. (2002) Biological effects of secretory phospholipase A(2) group IIA on lipoproteins and in atherogenesis. Eur. J. Clin. Invest. 32, 383-393
56. Berliner, J. A., Territo, M., Navab, M., Andalibi, A., Parhami, F., Liao, F., Kim, J., Estworthy, S., Lusis, A. J., and Fogelman, A. M. (1992) Minimally modified lipoproteins in diabetes. Diabetes 41, 74-76
57. 2. Arterioscler. Thomb. Vasc. Biol. 19, 1284-1290
58. 2 in atherosclerosis-2. Potential involvement of biologically active oxidized phospholipids. Arterioscler. Thomb. Vasc. Biol. 19, 1291-1298
59. Ansell, B. J., Fonarow, G. C., and Fogelman, A. M. (2007) The paradox of dysfunctional high-density lipoprotein. Curr. Opin. Lipidol. 18, 427-434 (Pubitemid 47051922)
60. Tietge, U. J., Maugeais, C., Cain, W., and Rader, D. J. (2003) Acute inflammation increases selective uptake of HDL cholesteryl esters into adrenals of mice overexpressing human sPLA2. Am. J. Physiol. Endocrinol. Metab. 285, E403-E411 (Pubitemid 36899715)
61. Zusman, R. M., Chesebro, J. H., Comerota, A., Hartmann, J. R., Massin, E. K., Raps, E., and Wolf, P. A. (1999) Antiplatelet therapy in the prevention of ischemic vascular events: literature review and evidence-based guidelines for drug selection. Clin. Cardiol. 22, 559-573 (Pubitemid 29416183)
62. Corsonello, A., Malara, A., De Domenico, D., Perticone, F., Valenti, A., Buemi, M., Ientile, R., and Corica, F. (2004) Identifying pathways involved in leptin-dependent aggregation of human platelets. Int. J. Obes. Relat. Metab. Disord. 28, 979-984 (Pubitemid 38998702)
63. Leite, J. O., Vaishnav, U., Puglisi, M., Fraser, H., Trias, J., and Fernandez, M. L. (2009) A-002 (Varespladib), a phospholipase A2 inhibitor, reduces atherosclerosis in guinea pigs. BMC Cardiovasc. Disord. 9, 7