Homocysteine decreases platelet NO level via protein kinase C activation

Nitric Oxide - Biology and Chemistry

Volumn 20, Issue 2, 2009, Pages 104-113

  Signorello, Maria Grazia ^a   Segantin, Alessia ^a   Passalacqua, Mario ^a   Leoncini, Giuliana ^a  

^a UNIVERSITY OF GENOA   (Italy)

Author keywords

Homocysteine; Human platelets; NADPH oxidase; Nitric oxide; Nitric oxide synthase; Protein kinase C

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 3 NITROTYROSINE; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HOMOCYSTEINE; NITRIC OXIDE; PHOSPHOLIPASE C GAMMA2; PLECKSTRIN; PROTEIN KINASE C; PROTEIN P47; PROTEIN P47 PHOX; PROTEIN P67; PROTEIN P67 PHOX; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; UNCLASSIFIED DRUG;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; IMMUNODETECTION; IMMUNOFLUORESCENCE MICROSCOPY; NORMAL HUMAN; PRIORITY JOURNAL; THROMBOCYTE;

ANALYSIS OF VARIANCE; BLOOD PLATELETS; CITRULLINE; CYCLIC GMP; ENZYME ACTIVATION; ENZYME INHIBITORS; HOMOCYSTEINE; HUMANS; MICROSCOPY, FLUORESCENCE; NADPH OXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTEIN KINASE C; SUPEROXIDES; TYROSINE;

EID: 59049085356     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.niox.2008.11.005     Document Type: Article

References (64)

1. Wall R.T., Harlan J.M., Harker L.A., and Striker G.E. Homocysteine-induced endothelial cell injury in vitro: a model for the study of vascular injury. Thromb. Res. 18 (1980) 113-121
2. Silverman M.D., Tumuluri R.J., Davis M., Lopez G., Rosenbaum J.T., and Lelkes P.I. Homocysteine upregulates vascular cell adhesion molecule-1 expression in cultured human aortic endothelial cells and enhances monocyte adhesion. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 587-592
3. Koga T., Claycombe K., and Meydani M. Homocysteine increases monocyte and T-cell adhesion to human aortic endothelial cells. Atherosclerosis 161 (2002) 365-374
4. Wang J., Dudman N.P., and Wilcken D.E. Effects of homocysteine and related compounds on prostacyclin production by cultured human vascular endothelial cells. Thromb. Haemost. 70 (1993) 1047-1052
5. Mujumdar V.S., Aru G.M., and Tyagi S.C. Induction of oxidative stress by homocyst(e)ine impairs endothelial function. J. Cell. Biochem. 82 (2001) 491-500
6. Weiss N., Keller C., Hoffmann U., and Loscalzo J. Endothelial dysfunction and atherothrombosis in mild hyperhomocysteinaemia. Vasc. Med. 7 (2002) 227-239
7. Leoncini G., Bruzzese D., and Signorello M.G. A role for PLCgamma2 in platelet activation by homocysteine. J. Cell. Biochem. 100 (2007) 1255-1265
8. Signorello M.G., Pascale R., and Leoncini G. Effect of homocysteine on arachidonic acid release in human platelets. Eur. J. Clin. Invest. 32 (2002) 279-284
9. Leoncini G., Bruzzese D., and Signorello M.G. Activation of p38 MAPKinase/cPLA2 pathway in homocysteine-treated platelets. J. Thromb. Haemost. 4 (2006) 209-216
10. Leslie C.C. Properties and regulation of cytosolic phospholipase A2. J. Biol. Chem. 272 (1997) 16709-16712
11. Paine E., Palmantier R., Akiyama S.K., Olden K., and Roberts J.D. Arachidonic acid activates mitogen-activated protein (MAP) kinase-activated protein kinase 2 and mediates adhesion of a human breast carcinoma cell line to collagen type IV through a p38 MAP kinase-dependent pathway. J. Biol. Chem. 275 (2000) 11284-11290
12. Muthalif M.M., Benter I.F., Karzoun N., Fatima S., Harper J., Uddin M.R., and Malik K.U. 20-Hydroxyeicosatetraenoic acid mediates calcium/calmodulin-dependent protein kinase II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. Proc. Natl. Acad. Sci. USA 95 (1998) 12701-12706
13. Colasanti M., Persichini T., Cavalieri E., Fabrizi C., Mariotto S., Menegazzi M., Lauro G.M., and Suzuki H. Rapid inactivation of NOS-I by lipopolysaccharide plus interferon-gamma-induced tyrosine phosphorylation. J. Biol. Chem. 274 (1999) 9915-9917
14. Komeima K., Hayashi Y., Naito Y., and Watanabe Y. Inhibition of neuronal nitric-oxide synthase by calcium/ calmodulin-dependent protein kinase IIalpha through Ser847 phosphorylation in NG108-15 neuronal cells. J. Biol. Chem. 275 (2000) 28139-28143
15. Palomba L., Bianchi M., Persichini T., Magnani M., Colasanti M., and Cantoni O. Downregulation of nitric oxide formation by cytosolic phospholipase A2-released arachidonic acid. Free Radic. Biol. Med. 36 (2004) 319-329
16. Mayer B., and Hemmeus B. Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem. Sci. 22 (1997) 477-481
17. Radomski M., Palmer R., and Moncada S. Comparative pharmacology of endothelium-derived relaxing factor, nitric oxide and prostacyclin in platelets. Br. J. Pharmacol. 92 (1987) 181-187
18. Radomski M., Palmer R., and Moncada S. An l-arginine/nitric oxide pathway present in human platelets regulates aggregation. Proc. Natl. Acad. Sci. USA 87 (1990) 5193-5197
19. Muruganandam A., and Mutus B. Isolation of nitric oxide synthase from human platelets. Biochim. Biophys. Acta 1200 (1994) 1-6
20. Michell B.J., Chen Z.P., Tiganis T., Stapleton D., Katsis F., Power D.A., Sim A.T., and Kemp B.E. Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J. Biol. Chem. 276 (2001) 17625-17628
21. Upchurch Jr. G.R., Welch G.N., Fabian A.J., Freedman J.E., Johnson J.L., Keaney Jr. J.F., and Loscalzo J. Homocyst(e)ine decreases bioavailable nitric oxide by a mechanism involving glutathione peroxidase. J. Biol. Chem. 272 (1997) 17012-17017
22. Li N., Yi F.X., Rute E., Zhang D.X., Slocum G.R., and Zou A.P. Effects of homocysteine on intracellular nitric oxide and superoxide levels in the renal arterial endothelium. Am. J. Physiol. Heart Circ. Physiol. 283 (2002) H1237-H1243
23. Zhang X., Li H., Jin H., Ebin Z., Brodsky S., and Goligorsky M.S. Effects of homocysteine on endothelial nitric oxide production. Am. J. Physiol. Renal. Physiol. 279 (2000) F671-F678
24. Jiang X., Yang F., Tan H., Liao D., Bryan Jr. R.M., Randhawa J.K., Rumbaut R.E., Durante W., Schafer A.I., Yang X., and Wang H. Hyperhomocystinemia impairs endothelial function and eNOS activity via PKC activation. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 2515-2521
25. Mutus B., Rabini R.A., Staffolani R., Ricciotti R., Fumelli P., Moretti N., Martarelli D., and Mazzanti L. Homocysteine-induced inhibition of nitric oxide production in platelets: a study on healthy and diabetic subjects. Diabetologia 44 (2001) 979-982
26. Leoncini G., Pascale R., and Signorello M.G. Effects of homocysteine on l-arginine transport and nitric oxide formation in human platelets. Eur. J. Clin. Invest. 33 (2003) 713-719
27. Jin L., Caldwell R.B., Li-Masters T., and Caldwell R.W. Homocysteine induces endothelial dysfunction via inhibition of arginine transport. J. Physiol. Pharmacol. 58 (2007) 191-206
28. Rotmann A., Simon A., Martiné U., Habermeier A., and Closs E.I. Activation of classical protein kinase C decreases transport via systems y+ and y+L. Am. J. Physiol. Cell Physiol. 292 (2007) C2259-C2268
29. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
30. Raiteri L., Stigliani S., Siri A., Passalacqua M., Melloni E., Raiteri M., and Bonanno G. Glycine taken up through GLYT1 and GLYT2 heterotransporters into glutamatergic axon terminals of mouse spinal cord elicits release of glutamate by homotransporter reversal and through anion channels. Biochem. Pharmacol. 69 (2005) 159-168
31. Freedman J.E., and Keaney Jr. J.F. Nitric oxide and superoxide detection in human platelets. Methods Enzymol. 301 (1999) 61-70
32. Nardi M., Feinmark S.J., Hu L., Li Z., and Karpatkin S. Complement-independent Ab-induced peroxide lysis of platelets requires 12-lipoxygenase and a platelet NADPH oxidase pathway. J. Clin. Invest. 113 (2004) 973-980
33. MacMillan-Crow L.A., Crow J.P., Kerby J.D., Beckman J.S., and Thompson J.A. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl. Acad. Sci. USA 93 (1996) 11853-11858
34. Cattaneo M. Hyperhomocysteinemia atherosclerosis and thrombosis. Thromb. Haemost. 81 (1999) 165-176
35. Medina M., Urdiales J.L., and Amores-Sanchez M.I. Roles of homocysteine in cell metabolism: old and new functions. Eur. J. Biochem. 268 (2001) 3871-3882
36. den Heijer M., Willems H.P., Blom H.J., Gerrits W.B., Cattaneo M., Eichinger S., Rosendaal F.R., and Bos G.M. Homocysteine lowering by B vitamins and the secondary prevention of deep vein thrombosis and pulmonary embolism: a randomized, placebo-controlled, double-blind trial. Blood 109 (2007) 139-144
37. Jamison R.L., Hartigan P., Kaufman J.S., Goldfarb D.S., Warren S.R., Guarino P.D., Gaziano J.M., and Veterans Affairs Site Investigators. Effect of homocysteine lowering on mortality and vascular disease in advanced chronic kidney disease and end-stage renal disease: a randomized controlled trial. JAMA 298 (2007) 1163-1170
38. Durand P., Prost M., and Blache D. Pro-thrombotic effects of a folic acid deficient diet in rat platelets and macrophages related to elevated homocysteine and decreased n-3 polyunsaturated fatty acids. Atherosclerosis 121 (1996) 231-243
39. Durand P., Lussier-Cacan S., and Blache D. Acute methionine load-induced hyperhomocysteinemia enhances platelet aggregation, thromboxane biosynthesis, and macrophage-derived tissue factor activity in rats. FASEB J. 11 (1997) 1157-1168
40. Coppola A., Davi G., De Stefano V., Mancini F.P., Cerbone A.M., and Di Minno G. Homocysteine, coagulation, platelet function, and thrombosis. Semin. Thromb. Hemost. 26 (2000) 243-254
41. Riba R., Nicolaou A., Troxler M., Homer-Vaniasinkam S., and Naseem K.M. Altered platelet reactivity in peripheral vascular disease complicated with elevated plasma homocysteine levels. Atherosclerosis 175 (2004) 69-75
42. Di Minno G., Davì G., Margaglione M., Cirillo F., Grandone E., Ciabattoni G., Catalano I., Strisciuglio P., Andria G., Patrono C., and Mancini M. Abnormally high thromboxane biosynthesis in homozygous homocystinuria. Evidence for platelet involvement and probucol-sensitive mechanism. J. Clin. Invest. 92 (1993) 1400-1406
43. Leoncini G., Pascale R., and Signorello M.G. Modulation of l-arginine transport and nitric oxide production by gabexate mesylate. Biochem. Pharmacol. 64 (2002) 277-283
44. Ogonowski A.A., Kaesemeyer W.H., Jin L., Ganapathy V., Leibach F.H., and Caldwell R.W. Effects of NO donors and synthase agonists on endothelial cell uptake of l-Arg and superoxide production. Am. J. Physiol. Cell Physiol. 278 (2000) C136-C143
45. Leoncini G., Maresca M., and Colao C. Oxidative metabolism of human platelets. Biochem. Int. 25 (1991) 647-655
46. Seno T., Inoue N., Gao D., Okuda M., Sumi Y., Matsui K., Yamada S., Hirata K.I., Kawashima S., Tawa R., Imajoh-Ohmi S., Sakurai H., and Yokoyama M. Involvement of NADH/NADPH oxidase in human platelet ROS production. Thromb. Res. 103 (2001) 399-409
47. Soulet C., Gendreau S., Missy K., Benard V., Plantavid M., and Payrastre B. Characterisation of Rac activation in thrombin- and collagen-stimulated human blood platelets. FEBS Lett. 507 (2001) 253-258
48. Krötz F., Sohn H.Y., Gloe T., Zahler S., Riexinger T., Schiele T.M., Becker B.F., Theisen K., Klauss V., and Pohl U. NAD(P)H oxidase-dependent platelet superoxide anion release increases platelet recruitment. Blood 100 (2002) 917-924
49. Pignatelli P., Sanguigni V., Lenti L., Ferro D., Finocchi A., Rossi P., and Violi F. Gp91phox-dependent expression of platelet CD40 ligand. Circulation 110 (2004) 1326-1329
50. Baggiolini M., Boulay F., Badwey J.A., and Curnutte J.T. Activation of neutrophil leukocytes: chemoattractant receptors and respiratory burst. FASEB J. 7 (1993) 1004-1010
51. Shiose A., and Sumimoto H. Arachidonic acid and phosphorylation synergistically induce a conformational change of p47phox to activate the phagocyte NADPH oxidase. J. Biol. Chem. 275 (2000) 13793-13801
52. Qualliotine-Mann D., Agwu D.E., Ellenburg M.D., McCall C.E., and McPhail L.C. Phosphatidic acid and diacylglycerol synergize in a cell-free system for activation of NADPH oxidase from human neutrophils. J. Biol. Chem. 268 (1993) 23843-23849
53. Inanami O., Johnson J.L., McAdara J.K., Benna J.E., Faust L.R., Newburger P.E., and Babior B.M. Activation of the leukocyte NADPH oxidase by phorbol ester requires the phosphorylation of p47PHOX on serine 303 or 304. J. Biol. Chem. 273 (1998) 9539-9543
54. Dang P.M., Morel F., Gougerot-Pocidalo M.A., and El Benna J. Phosphorylation of the NADPH oxidase component p67(PHOX) by ERK2 and P38MAPK: selectivity of phosphorylated sites and existence of an intramolecular regulatory domain in the tetratricopeptide-rich region. Biochemistry 42 (2003) 4520-4526
55. Dana R., Leto T.L., Malech H.L., and Levy R. Essential requirement of cytosolic phospholipase A2 for activation of the phagocyte NADPH oxidase. J. Biol. Chem. 273 (1998) 441-445
56. Fontayne A., Dang P.M., Gougerot-Pocidalo M.A., and El-Benna J. Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation. Biochemistry 41 (2002) 7743-7750
57. Alvarez-Maqueda M., El Bekay R., Monteseirin J., Alba G., Chacon P., Vega A., Santa Maria C., Tejedo J.R., Martin-Nieto J., Bedoya F.J., Pintado E., and Sobrino F. Homocysteine enhances superoxide anion release and NADPH oxidase assembly by human neutrophils. Effects on MAPK activation and neutrophils migration. Atherosclerosis 172 (2004) 229-238
58. Chen Z.P., Mitchelhill K.I., Michell B.J., Stapleton D., Rodriguez-Crespo I., Witters L.A., Power D.A., Ortiz de Montellano P.R., and Kemp B.E. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 443 (1999) 285-289
59. Hirata K., Kuroda R., Sakoda T., Katayama M., Inoue N., Suematsu M., Kawashima S., and Yokoyama M. Inhibition of endothelial nitric oxide synthase activity by protein kinase C. Hypertension 25 (1995) 180-185
60. Matsubara M., Hayashi N., Jing T., and Titani K. Regulation of endothelial nitric oxide synthase by protein kinase C. J. Biochem. 133 (2003) 773-781
61. Chianga T.M., Woo-Rasberrya V., and Coleb F. Role of platelet endothelial form of nitric oxide synthase in collagen-platelet interaction: regulation by phosphorylation. Biochim. Biophys. Acta 1592 (2002) 169-174
62. Gkaliagkousi E., Ritter J., and Ferro A. Platelet-derived nitric oxide signaling and regulation. Circ. Res. 101 (2007) 654-662
63. Zhang Q., Malik P., Pandey D., Gupta S., Jagnandan D., de Chantemele E.B., Banfi B., Marrero M.B., Rudic R.D., Stepp D.W., and Fulton D.J. Paradoxical activation of endothelial nitric oxide synthase by NADPH oxidase. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 1627-1633
64. Xu H., and Pritchard Jr. K.A. Targeted increases in endothelial cell superoxide anion production stimulate eNOS-dependent nitric oxide production, not uncoupled eNOS activity. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 1580-1581