PL EN


Preferences help
enabled [disable] Abstract
Number of results
2004 | 51 | 3 | 789-803
Article title

Nitric oxide and platelet energy metabolism.

Content
Title variants
Languages of publication
EN
Abstracts
EN
This study was undertaken to determine whether nitric oxide (NO) can affect platelet responses through the inhibition of energy production. It was found that NO donors: S-nitroso-N-acetylpenicyllamine, SNAP, (5-50 μM) and sodium nitroprusside, SNP, (5-100 μM) inhibited collagen- and ADP-induced aggregation of porcine platelets. The corresponding IC50 values for SNAP and SNP varied from 5 to 30 μM and from 9 to 75 μM, respectively. Collagen- and thrombin-induced platelet secretion was inhibited by SNAP (IC50 = 50 μM) and by SNP (IC50 = 100 μM). SNAP (20-100 μM), SNP (10-200 μM) and collagen (20 μg/ml) stimulated glycolysis in intact platelets. The degree of glycolysis stimulation exerted by NO donors was similar to that produced by respiratory chain inhibitors (cyanide and antimycin A) or uncouplers (2,4-dinitrophenol). Neither the NO donors nor the respiratory chain blockers affected glycolysis in platelet homogenate. SNAP (20-100 μM) and SNP (50-200 μM) inhibited oxygen consumption by platelets. The effect of SNP and SNAP on glycolysis and respiration was not reduced by 1H-[1,2,4]oxadiazolo-[4,3-a]quinoxalin-1-one, a selective inhibitor of NO-stimulated guanylate cyclase. SNAP (5-100 μM) and SNP (10-300 μM) inhibited the activity of platelet cytochrome oxidase and had no effect on NADH:ubiquinone oxidoreductase and succinate dehydrogenase. Blocking of the mitochondrial energy production by antimycin A slightly affected collagen-evoked aggregation and strongly inhibited platelet secretion. The results indicate that: 1) in porcine platelets NO is able to diminish mitochondrial energy production through the inhibition of cytochrome oxidase, 2) the inhibitory effect of NO on platelet secretion (but not aggregation) can be attributed to the reduction of mitochondrial energy production.
Publisher

Year
Volume
51
Issue
3
Pages
789-803
Physical description
Dates
published
2004
received
2003-11-13
revised
2004-03-22
accepted
2004-04-05
Contributors
  • Department of Physical Chemistry, Medical University of Białystok, Białystok, Poland
  • Department of Physical Chemistry, Medical University of Białystok, Białystok, Poland
author
  • Department of Physical Chemistry, Medical University of Białystok, Białystok, Poland
  • Department of Pediatric Laboratory Diagnostics, Medical University of Białystok, Białystok, Poland
References
  • Akahori M, Uedono Y, Yamagami K, Takeyama N, Kitazawa Y. (1995) Hypoxia alters the energy metabolism and aggregation of washed human platelets. Haematologia.; 26: 191-8.
  • Akkerman JWN. (1978) Regulation of carbohydrate metabolism in platelets. Thromb Haemost.; 39: 712-24.
  • Akkerman JWN, Holmsen H. (1981) Interrelationships among platelet responses: studies on the burst in proton liberation, lactate production, and oxygen uptake during platelet aggregation and Ca2+ secretion. Blood.; 57: 956-65.
  • Akkerman JWN, Gorter G, Sixma JJ. (1978) Regulation of glycolytic flux in human platelets. Biochim Biophys Acta.; 541: 241-50.
  • Beghetti M, Sparling C, Stephens D. (2003) Inhaled NO inhibits platelet aggregation and elevates plasma but not intraplatelet cGMP in healthy human volunteers. Am J Physiol Heart Circ Physiol.; 285: H637-42.
  • Berkels R, Bertsch A, Zuther T, Dhein S, Stockklauser K, Rosen P, Rosen R. (1997) Evidence for a NO synhase in porcine platelets which is stimulated during activation/aggregation. Eur J Haematol.; 58: 307-13.
  • Born GVR. (1963) Quantitative investigation into aggregation of blood platelets. J Physiol.; 168: 78-95.
  • Borutaite V, Matthias A, Harris H, Moncada S, Brown GC. (2001) Reversible inhibition of cellular respiration by nitric oxide in vascular inflammation. Am J Physiol Heart Circ Physiol.; 281: H2256-60.
  • Brown GC. (1999) Nitric oxide and mitochondrial respiration. Biochim Biophys Acta.; 1411: 351-69.
  • Brown GC. (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta.; 1504: 46-57.
  • Chrono-Log Diagnostic Protocol. (1987) Manual for testing with the whole-blood aggregometer model 550. Chrono-Log Corp. Havertown, PA, USA.
  • Clementi E. Brown GC, Feelishc, and Moncada S. (1998) Persistent inhibition of cell respiration by nitric oxide: Crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci USA.; 95: 7631-6.
  • Geng Y, Hansson GK, Holme E. (1992) Interferon-gamma and tumor necrosis factor synergize to induce nitric oxide production and inhibit mitochondrial respiration in vascular smooth muscle cells. Circ Res.; 71: 1268-76.
  • Gordge MP, Hothersall JS, Noronha-Dutra AA. (1998) Evidence for a cyclic GMP-independent mechanism in the anti-platelet action of S-nitrosoglutathione. Br J Pharmacol.; 124: 141-8.
  • Guppy M, Whisson ME, Sabaratnam R, Withers P, Brand K. (1990) Alternative fuels for platelet storage: a metabolic study. Vox Sang.; 59: 146-52.
  • Guppy M, Abas L, Arthur PG, Whisson ME. (1995) The Pasteur effect in human platelets: implications for storage and metabolic control. Br J Haematol.; 91: 752-7.
  • Gutmann I, Wahlefeld AW. (1985) L-(+)Lactate determination with lactate dehydrogenase and NAD. In Methods of Enzymatic Analysis. Bergmeyer HU, ed, pp 1464-8. VCH Velagsgesellschaft mbH. Weiheim.
  • Holmsen H. (1981) Biochemistry of the platelet: energy metabolism. in Haemostasis and Thrombosis: Basic Principles and Clinical Practice. Colman RW, Hirsh J, Marder VJ, Salzman EW, eds, pp 431-43, JB Lippincott Comp. Philadelphia.
  • Holmsen H, Dangelmaier CA. (1989) Measurement of secretion of serotonin. Methods Enzymol.; 169: 195-205.
  • Holmsen H, Kaplan KL, Dangelmaier CA. (1982) Differential energy requirements for platelet responses. Biochem J.; 208: 9-18.
  • Hooper DC, Ohnishi ST, Kean R, Numagami Y, Dietzschold B, Koprowski H. (1995) Local nitric oxide production in viral and autoimmune diseases of the central nervous system. Proc Natl Acad Sci USA.; 92: 5312-6.
  • King TE. (1967) Preparation of succinate dehydrogenase and reconstitution of succinate oxidase. Methods Enzymol.; 10: 322-31.
  • Lantoine F, Brunet A, Bedioui F, Devynck J, Devynck MA. (1995) Direct measurement of nitric oxide production in platelets: relationship with cytosolic Ca2+ concentration. Biochem Biophys Res Commun.; 215: 842-8.
  • Lenaz G. (1988) Quinone specificity of complex I. Biochim Biophys Acta.; 1364: 207-21
  • Malinski T, Bailey F, Zhang ZG, Chopp M. (1993) Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. JCereb Blood Flow Metab.; 13: 355-8.
  • Moncada S, Palmer RMJ, Higgs EA. (1991) Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev.; 43: 109-42.
  • Morimoto T, Ogihara S. (1996) ATP is required in platelet serotonin exocytosis for protein phosphorylation and priming of secretory vesicles docked on the plasma membrane. J Cell Sci.; 109: 113-8.
  • Nishimura I, Minakami S. (1975) Effect of hydrogen ions concentration on energy metabolism in pig platelets Biochim Biophys Acta.; 396: 1-10.
  • Niu X, Arthur P, Abas L, Whisson M, Guppy M. (1996) Carbohydrate metabolism in human platelets in a low glucose medium under aerobic conditions. Biochim Biophys Acta.; 1291: 97-106.
  • Oddis CV, Finke MS. (1995) Cytokine-stimulated nitric oxide production inhibits mitochondrial activity in cardiac myocytes. Biochem Biophys Res Commun.; 213: 1002-9.
  • Radomski MW, Zakar T, Salas E. (1996) Nitric oxide in platelets. Methods Enzymol.; 269: 88-107.
  • Ragan CI, Wilson MT, Derley-Usmar VM, Lowe PN. (1987) Mitochondria: a Practical Approach. Darley-Usmar VM, Rickewood D, Wilson MT. eds, pp 79-112. IRL Press Oxford.
  • Riddell DR, Owen JS. (1999) Nitric oxide and platelet aggregation. Vitam Horm.; 57: 25-48.
  • Schmidt HH, Lohmann SM, Walter U. (1993) The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochim Biophys Acta.; 1178: 153-75.
  • Singh RJ, Hogg N, Kalyanaraman B. (1996) Mechanism of nitric oxide release from S-nitrosothiols. J Biol Chem.; 271: 18596-603.
  • Smith L. (1955) Cytochrome c oxidase. In Methods of Biochemical Analysis, vol. 2, pp 427-9. Glick D. Wiley (Interscience), New York.
  • Smith L, Conrad H. (1961) A study of the kinetics of the oxidation of cytochrome c by cytochrome oxidase. Arch Biochem Biophys.; 63: 403-13.
  • Sogo N, Magid KS, Shaw CA, Weeb DJ, Megson IL. (2000) Inhibition of human platelet aggregation by nitric oxide donors drugs: relative contribution of cGMP-independent mechanisms. Biochem Biophys Res Commun.; 279: 412-19.
  • Stone JR, Marletta MA. (1996) Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide. Biochemistry.; 35: 1093-9.
  • Szabo C. (1996) Physiological and pathophysiological roles of nitric oxide in the central nervous system. Brain Res Bull.; 41: 131- 41.
  • Titheradge MA. (1999) Nitric oxide in septic shock. Biochim Biophys Acta.; 1411: 437-55.
  • Verhoeven AJM, Mommersteeg ME, Akkerman JWN. (1984) Metabolic energy is required in human platelets at any stage during optical aggregation and secretion. Biochim Biophys Acta.; 800: 242-50.
  • Waldmann R, Walter U. (1989) Cyclic nucleotide elevating vasodilators inhibit platelet aggregation at an early step of the activation cascade. Eur J Pharmacol.; 159: 317-20.
  • Wang GR, Zhu Y, Halushka PV, Lincoln TM, Mendelsohn ME. (1998) Mechanism of platelet inhibition by nitric oxide: in vivo phosphorylation of thromboxane receptor by cyclic GMP-dependent protein kinase. Proc Natl Acad Sci USA.; 95: 4888-93.
  • Welter R, Yu L, Yu CA. (1996) The effect of nitric oxide on electron transport complexes. Arch Biochem Biophys.; 331: 9-14.
  • Yamamoto T, Bing RJ. (2000), Nitric oxide donors. Proc Soc Exp Biol Med.; 225: 200-6.
  • Zhou Q, Hellermann GR, Solomonson LP. (1995) Nitric oxide release from resting human platelets. Thromb Res.; 77: 87-96.
Document Type
Publication order reference
Identifiers
YADDA identifier
bwmeta1.element.bwnjournal-article-abpv51i3p789kz
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.