The plasma membrane redox system in human platelet functions and platelet-leukocyte interactions

 

 Buy Article Permissions and Reprints

Summary

The plasma membrane electron transport is crucial for blood coagulation and thrombosis, since reactive oxygen species and thiol changes, generated by plasma membrane redox reactions, modulate activation of platelets, as well as their interaction with leukocytes. Several antioxidants are linked to this system; thus, platelets are also able to counterbalance radical production and to regulate thrombus growth. Aim of this review is to give an update on the plasma membrane redox system in platelets, as well as on its role in platelet functions and leukocyte-platelet crosstalk.

• References

• 1 Del Principe D, Mancuso G, Menichelli A. et al. Production of hydrogen peroxide in phagocyting human platelets: an electron microscopic cytochemical demonstration. Biol Cell 1980; 38: 135-140.
  PubMedGoogle Scholar
• 2 Finazzi-Agrò A, Menichelli A, Persiani M. et al. Hydrogen peroxide release from human blood platelets. Biochim Biophys Acta 1982; 718: 21-25.
  CrossrefPubMedGoogle Scholar
• 3 Bakdash N, Williams MS. Spatially distinct production of reactive oxygen species regulates platelet activation. Free Radic Biol Med 2008; 45: 158-166.
  CrossrefPubMedGoogle Scholar
• 4 Del Principe D, Mancuso G, Menichelli A. et al. Oxygen consumption in platelets of newborn infants before and after stimulation by thrombin. Thromb Haemost 1976; 35: 712-716.
  Article in Thieme ConnectPubMedGoogle Scholar
• 5 Krötz F, Sohn HY, Pohl U. Reactive oxygen species: players in the platelet game. Arterioscler Thromb Vasc Biol 2004; 24: 1988-1996.
  CrossrefPubMedGoogle Scholar
• 6 Freedman JE. Oxidative Stress and Platelets. Arterioscler Thromb Vasc Biol 2008; 28: 11-16.
  CrossrefPubMedGoogle Scholar
• 7 Berridge MV, Tan AS. High-capacity redox control at the plasma membrane of mammalian cells: trans-membrane, cell surface, and serum NADH-oxidases. Antioxid Redox Signal 2000; 2: 231-242.
  CrossrefPubMedGoogle Scholar
• 8 VanDuijn MM, Van der Zee J, Van den Broek PJ. The ascorbate-driven reduction of extracellular ascorbate free radical by the erythrocyte is an electrogenic process. FEBS Lett 2001; 491: 67-70.
  CrossrefPubMedGoogle Scholar
• 9 Arroyo A, Kagan VE, Tyurin VA. et al. NADH and NADPH-dependent reduction of coenzyme Q at the plasma membrane. Antioxid Redox Signal 2000; 2: 251-262.
  CrossrefPubMedGoogle Scholar
• 10 Ly JD, Lawen A. Transplasma membrane electron transport: enzymes involved and biological function. Redox Rep 2003; 8: 3-21.
  CrossrefPubMedGoogle Scholar
• 11 Geiszt M, Leto TL. The Nox family of NAD(P)H oxidases: host defense and beyond. J Biol Chem 2004; 279: 51715-51718.
  CrossrefPubMedGoogle Scholar
• 12 Cave AC, Brewer AC, Narayanapanicker A. et al. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 2006; 8: 691-728.
  CrossrefPubMedGoogle Scholar
• 13 O’Donnell VB, Smith GC, Jones OT. Involvement of phenyl radicals in iodonium inhibition of flavoenzymes. Mol Pharmacol 1994; 46: 778-785.
  PubMedGoogle Scholar
• 14 Heumüller S, Wind S, Barbosa-Sicard E. et al. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 2008; 51: 211-217.
  CrossrefPubMedGoogle Scholar
• 15 Seno T, Inoue N, Gao D. et al. Involvement of NADH/NADPH oxidase in human platelet ROS production. Thromb Res 2001; 103: 399-409.
  CrossrefPubMedGoogle Scholar
• 16 Zielinski T, Wachowicz B, Saluk-Juszczak J. et al. The generation of superoxide anion in blood platelets in response to different forms of Proteus mirabilis lipopolysaccharide: effects of staurosporin, wortmannin, and indomethacin. Thromb Res 2001; 103: 149-155.
  CrossrefPubMedGoogle Scholar
• 17 White JG. Platelets are covercytes, not phagocytes: uptake of bacteria involves channels of the open canalicular system. Platelets 2005; 16: 121-131.
  CrossrefPubMedGoogle Scholar
• 18 Krötz F, Sohn HY, Gloe T. et al. NAD(P)H oxidase-dependent platelet superoxide anion release increases platelet recruitment. Blood 2002; 100: 917-924.
  CrossrefPubMedGoogle Scholar
• 19 Begonja AJ, Gambaryan S, Geiger J. et al. Platelet NAD(P)H-oxidase-generated ROS production regulates alphaIIbbeta3-integrin activation independent of the NO/cGMP pathway. Blood 2005; 106: 2757-2760.
  CrossrefPubMedGoogle Scholar
• 20 Carnevale R, Pignatelli P, Lenti L. et al. LDL are oxidatively modified by platelets via GP91(phox) and accumulate in human monocytes. FASEB J 2007; 21: 927-934.
  CrossrefPubMedGoogle Scholar
• 21 Chlopicki S, Olszanecki R, Janiszewski M. et al. Functional role of NADPH oxidase in activation of platelets. Antioxid Redox Signal 2004; 6: 691-698.
  CrossrefPubMedGoogle Scholar
• 22 Peter AD, Morrè DJ, Morrè DM. A light-responsive and periodic NADH oxidase activity of the cell surface of tetrahymena and of human buffy coat cells. Antioxid Redox Signal 2000; 2: 289-300.
  CrossrefPubMedGoogle Scholar
• 23 Morré DJ, Morré DM. Cell surface NADH oxidases (ECTO-NOX proteins) with roles in cancer, cellular time-keeping, growth, aging and neurodegenerative diseases. Free Radic Res 2003; 37: 795-808.
  CrossrefPubMedGoogle Scholar
• 24 Morré DJ, Chueh PJ, Lawler J. et al. The sulfonylurea-inhibited NADH oxidase activity of HeLa cell plasma membranes has properties of a protein disulfidethiol oxidoreductase with protein disulfidethiol interchange activity. J Bioenerg Biomembr 1998; 30: 477-487.
  CrossrefPubMedGoogle Scholar
• 25 Irani K, Pham Y, Coleman LD. et al. Priming of platelet α_IIbβ₃ by oxidants is associated with tyrosine phosphorylation of β3. Arterioscler Thromb Vasc Biol 1998; 18: 1698-1706.
  CrossrefPubMedGoogle Scholar
• 26 Lahav J, Jurk K, Hess O. et al. Sustained integrin ligation involves extracellular free sulfhydryls and enzymatically catalyzed disulfide exchange. Blood 2002; 100: 2472-2478.
  CrossrefPubMedGoogle Scholar
• 27 Essex DW, Li M, Feinman RD. et al. Platelet surface glutathione reductase-like activity. Blood 2004; 104: 1383-1385.
  CrossrefPubMedGoogle Scholar
• 28 Chen K, Lin Y, Detwiler TC. Protein disulfide isomerase activity is released by activated platelets. Blood 1992; 79: 2226-2228.
  PubMedGoogle Scholar
• 29 Essex DW, Chen K, Swiatkowska M. Localization of protein disulfide isomerase to the external surface of the platelet plasma membrane. Blood 1995; 86: 2168-2173.
  PubMedGoogle Scholar
• 30 Jordan PA, Stevens JM, Hubbard GP. et al. A role for the thiol isomerase protein ERP5 in platelet function. Blood 2005; 105: 1500-1507.
  CrossrefPubMedGoogle Scholar
• 31 Lahav J, Gofer-Dadosh N, Luboshitz J. et al. Protein disulfide isomerase mediates integrin-dependent adhesion. FEBS Lett 2000; 475: 89-92.
  CrossrefPubMedGoogle Scholar
• 32 Lahav J, Wijnen EM, Hess O. et al. Enzymatically catalyzed disulfide exchange is required for platelet adhesion to collagen via integrin alpha2beta1. Blood 2003; 102: 2085-2092.
  CrossrefPubMedGoogle Scholar
• 33 Manickam N, Sun X, Li M. et al. Protein disulphide isomerase in platelet function. Br J Haematol 2008; 140: 223-229.
  PubMedGoogle Scholar
• 34 Janiszewski M, Lopes LR, Carmo AO. et al. Regulation of NAD(P)H oxidase by associated protein disulfide isomerase in vascular smooth muscle cells. J Biol Chem 2005; 280: 40813-40819.
  CrossrefPubMedGoogle Scholar
• 35 Lyles MM, Gilbert HF. Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: dependence of the rate on the composition of the redox buffer. Biochemistry 1991; 30: 613-619.
  CrossrefPubMedGoogle Scholar
• 36 Savini I, Catani MV, Arnone R. et al. Translational control of the ascorbic acid transporter SVCT2 in human platelets. Free Radic Biol Med 2007; 42: 608-616.
  CrossrefPubMedGoogle Scholar
• 37 Takajo Y, Ikeda H, Haramaki N. et al. Augmented oxidative stress of platelets in chronic smokers. Mechanisms of impaired platelet-derived nitric oxide bioactivity and augmented platelet aggregability. J Am Coll Cardiol 2001; 38: 1320-1327.
  CrossrefPubMedGoogle Scholar
• 38 McVeigh GE, Hamilton P, Wilson M. et al. Platelet nitric oxide and superoxide release during the development of nitrate tolerance: effect of supplemental ascorbate. Circulation 2002; 106: 208-213.
  CrossrefPubMedGoogle Scholar
• 39 Wells WW, Xu DP, Yang YF. et al. Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J Biol Chem 1990; 265: 15361-15364.
  PubMedGoogle Scholar
• 40 Freedman JE, Farhat JH, Loscalzo J. et al. alpha-tocopherol inhibits aggregation of human platelets by a protein kinase C-dependent mechanism. Circulation 1996; 94: 2434-2440.
  CrossrefPubMedGoogle Scholar
• 41 Liu M, Wallmon A, Olsson-Mortlock C. et al. Mixed tocopherols inhibit platelet aggregation in humans: potential mechanisms. Am J Clin Nutr 2003; 77: 700-706.
  CrossrefPubMedGoogle Scholar
• 42 Taccone-Gallucci M, Lubrano R, Del Principe D. et al. Platelet lipid peroxidation in haemodialysis patients: effects of vitamin E supplementation. Nephrol Dial Transplant 1989; 4: 975-978.
  CrossrefPubMedGoogle Scholar
• 43 Blache D. Involvement of hydrogen and lipid peroxides in acute tobacco smoking-induced platelet hyperactivity. Am J Physiol 1995; 268: H679-H685.
  PubMedGoogle Scholar
• 44 Del Principe D, Menichelli A, De Matteis W. et al. Hydrogen peroxide is an intermediate in the platelet activation cascade triggered by collagen, but not by thrombin. Thromb Res 1991; 62: 365-375.
  CrossrefPubMedGoogle Scholar
• 45 Rosado JA, Nunez AM, Lopez JJ. et al. Intracellular Ca2+ homeostasis and aggregation in platelets are impaired by ethanol through the generation of H2O2 and oxidation of sulphydryl groups. Arch Biochem Biophys 2006; 452: 9-16.
  CrossrefPubMedGoogle Scholar
• 46 May AE, Seizer P, Gawaz M. Platelets: inflammatory firebugs of vascular walls. Arterioscler Thromb Vasc Biol 2008; 28: s5-s10.
  CrossrefPubMedGoogle Scholar
• 47 Cerletti C, Evangelista V, de Gaetano G. P-selectin-beta 2-integrin cross-talk: a molecular mechanism for polymorphonuclear leukocyte recruitment at the site of vascular damage. Thromb Haemost 1999; 82: 787-793.
  Article in Thieme ConnectPubMedGoogle Scholar
• 48 Williams LA, Martin-Padura I, Dejana E. et al. Identification and characterisation of human Junctional Adhesion Molecule (JAM). Mol Immunol 1999; 36: 1175-1188.
  CrossrefPubMedGoogle Scholar
• 49 Lösche W, Dressel M, Krause S. et al. Contact-induced modulation of neutrophil elastase secretion and phagocytic activity by platelets. Blood Coagul Fibrinolysis 1996; 7: 210-213.
  CrossrefPubMedGoogle Scholar
• 50 Li N, Hu H, Lindqvist M. et al. Platelet-leukocyte cross talk in whole blood. Arterioscler Thromb Vasc Biol 2000; 20: 2702-2708.
  CrossrefPubMedGoogle Scholar
• 51 Langer HF, Gawaz M. Platelet-vessel wall interactions in atherosclerotic disease. Thromb Haemost 2008; 99: 480-486.
  Article in Thieme ConnectPubMedGoogle Scholar
• 52 Del Principe D, Menichelli A, Di Giulio S. et al. Stimulated platelets release factor(s) affecting the in vitro response of human polymorphonuclear cells. J Leukoc Biol 1990; 48: 7-14.
  CrossrefPubMedGoogle Scholar
• 53 Jancinová V, Drábiková K, Nosál’ R. et al. Inhibition of FMLP-stimulated neutrophil chemiluminescence by blood platelets increased in the presence of the serotonin-liberating drug chloroquine. Thromb Res 2003; 109: 293-298.
  CrossrefPubMedGoogle Scholar
• 54 Del Principe D, Frega G, Palumbo G. Platelet-leukocyte interactions: platelets possess an antioxidant armamentarium. Thromb Haemost 2003; 90: 759-760.
  Article in Thieme ConnectPubMedGoogle Scholar
• 55 Janiszewski M, Carmo AO, Pedro MA. et al. Platelet-derived exosomes of septic individuals possess proapoptotic NAD(P)H oxidase activity: a novel vascular redox pathway. Crit Care Med 2004; 32: 818-825.
  CrossrefPubMedGoogle Scholar
• 56 Stokes KY, Russell JM, Jennings MH. et al. Platelet-associated NAD(P)H oxidase contributes to the thrombogenic phenotype induced by hypercholesterolemia. Free Radic Biol Med 2007; 43: 22-30.
  CrossrefPubMedGoogle Scholar
• 57 Rodríguez-Alonso J, Montañez R, Rodríguez-Caso L. et al. Homocysteine is a potent modulator of plasma membrane electron transport systems. J Bioenerg Biomembr 2008; 40: 45-51.
  CrossrefPubMedGoogle Scholar
• 58 Wang JS, Lin HY, Cheng ML. et al. Chronic intermittent hypoxia modulates eosinophil- and neutrophil-platelet aggregation and inflammatory cytokine secretion caused by strenuous exercise in men. J Appl Physiol 2007; 103: 305-314.
  CrossrefPubMedGoogle Scholar
• 59 Pittaluga M, Parisi P, Sabatini S. et al. Cellular and biochemical parameters of exercise-induced oxidative stress: relationship with training levels. Free Radic Res 2006; 40: 607-614.
  CrossrefPubMedGoogle Scholar
• 60 Pignatelli P, Di Santo S, Buchetti B. et al. Polyphenols enhance platelet nitric oxide by inhibiting protein kinase C-dependent NADPH oxidase activation: effect on platelet recruitment. FASEB 2006; 20: 1082-1089.
  CrossrefPubMedGoogle Scholar
• 61 Raghavan SA, Sharma P, Dikshit M. Role of ascorbic acid in the modulation of inhibition of platelet aggregation by polymorphonuclear leukocytes. Thromb Res 2003; 110: 117-126.
  CrossrefPubMedGoogle Scholar
• 62 Mabile L, Bruckdorfer KR, Rice-Evans C. Moderate supplementation with natural alpha-tocopherol decreases platelet aggregation and low-density lipoprotein oxidation. Atherosclerosis 1999; 147: 177-185.
  CrossrefPubMedGoogle Scholar
• 63 Murohara T, Ikeda H, Otsuka Y. et al. Inhibition of platelet adherence to mononuclear cells by alpha-tocopherol: role of P-selectin. Circulation 2004; 110: 141-148.
  CrossrefPubMedGoogle Scholar
• 64 Wang JS, Lin HY, Cheng ML. et al. Chronic intermittent hypoxia modulates eosinophil- and neutrophil-platelet aggregation and inflammatory cytokine secretion caused by strenuous exercise in men. J Appl Physiol 2007; 103: 305-314.
  CrossrefPubMedGoogle Scholar
• 65 Amer J, Zelig O, Fibach E. Oxidative status of red blood cells, neutrophils, and platelets in paroxysmal nocturnal hemoglobinuria. Exp Hematol 2008; 36: 369-377.
  CrossrefPubMedGoogle Scholar
• 66 Amer J, Ghoti H, Rachmilewitz E. et al. Red blood cells, platelets and polymorphonuclear neutrophils of patients with sickle cell disease exhibit oxidative stress that can be ameliorated by antioxidants. Br J Haematol 2006; 132: 108-113.
  CrossrefPubMedGoogle Scholar
• 67 Morré DJ, Rodriguez-Aguilera JC, Navas P. et al. Redox modulation of the response of NADH oxidase activity of rat liver plasma membranes to cyclic AMP plus ATP. Mol Cell Biochem 1997; 173: 71-77.
  CrossrefPubMedGoogle Scholar
• 68 Preissner KT. From Molecules to Medicine: New Horizons in Vascular Biology and Thrombosis (Part II). Thromb Haemost 2008; 99: 465.
  Article in Thieme ConnectPubMedGoogle Scholar
• 69 Kannemeier C, Shibamiya A, Nakazawa F. et al. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. PNAS 2007; 104: 6388-6393.
  CrossrefPubMedGoogle Scholar
• 70 Nakazawa F, Kannemeier C, Shibamiya A. et al. Extracellular RNA is a natural cofactor for the (auto-)activation of fctor VII-activating protease (FSAP). Biochem J 2005; 385: 831-838.
  CrossrefPubMedGoogle Scholar
• 71 Bandziulis RJ, Swanson MS, Dreyfuss G. RNA-binding proteins as developmental regulators. Genes Dev 1989; 3: 431-437.
  CrossrefPubMedGoogle Scholar
• 72 Pagni M, Ioannidis V, Cerutti L. et al. MyHits: a new interactive resource for protein annotation and domain identification. Nucleic Acids Res 2004; 32 Web Server issue W332-335.
  CrossrefPubMedGoogle Scholar