Structural and Molecular Properties of Platelet Membrane Systems

  • Neville Crawford


Our understanding about the chemical composition and functional properties of platelet membrane systems has been advancing very rapidly at both the morphological and molecular levels over the last ten years or so. This is well emphasized by the fact that in certain areas of membrane biochemistry the use of the platelet as a model cell for probing the more general aspects of membrane structure and behavior, as also for studying drug transport and disease-related membrane defects, has resulted in a popularity rating for the platelet almost equal to that enjoyed earlier by the red cell. Although both the red cell and the platelet are anucleate cells, in some respects the platelet with its highly interactive surface membrane, its mitochondria, internal membranes, and lysosomes and storage organelles more reflects the behavioral and metabolic activities of other cells in the body than does the red cell with its high level of functional specialization. Since the platelet circulates as a poised and potentially highly reactive cell, responding rapidly to external stimuli, and is also most sensitive to even minor biochemical changes in the surrounding milieu, considerably more attention has been focused on the plasma membrane and its constituents and properties than on the various intracellular membrane systems that are equally well developed for functional needs. These latter membrane elements include not only endoplasmic-reticulumlike (ER) structures often referred to as dense tubular membrane system (DTS), but also include the boundary membranes of the many different granular organelles residing within the cytoplasmic matrix (mitochondria, lysosomes, α-granules, dense body granules, etc.).


Surface Membrane Membrane Fraction Human Platelet Intracellular Membrane Platelet Membrane 
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  1. Akkerman, J. W. N., Ebberink, R. H. M., Lips, J. P. M., and Christiaens, C. M. L., 1980, Rapid separation of cytosol and particle fractions of human platelets by digitonin-induced cell damage, Br. J. Haematol 44:291–300.PubMedCrossRefGoogle Scholar
  2. Baenziger, N. L., and Majerus, P. W., 1974, Isolation of human platelets and platelet surface membranes. Methods Enzymol. 31:149–156.PubMedCrossRefGoogle Scholar
  3. Barber, A. J., and Jamieson, G. A., 1970, Isolation and characterization of plasma membranes from human blood platelets, J. Biol Chem. 245:6357–6362.PubMedGoogle Scholar
  4. Barber, A. J., and Jamieson, G. A., 1971a, Platelet collagen adhesion characterization of collagen glucosyltransferase of plasma membranes of human blood platelets, Biochim. Biophys. Acta 252:533–545.PubMedCrossRefGoogle Scholar
  5. Barber, A. J., and Jamieson, G. A., 1971b, Characterization of membrane-bound collagen galactosyltransferase of human blood platelets,Biochim. Biophys. Acta 252:546–552.PubMedCrossRefGoogle Scholar
  6. Barber, A. J., Pepper, D. S., and Jamieson, G. A., 1971, A comparison of methods for platelet lysis and the isolation of platelet membranes,Thromb. Diathes. Haemorrh. 26:38.Google Scholar
  7. Behnke, O., 1965, Further studies on microtubules: A marginal bundle in human and rat thrombocytes, J. Ultrastruct. Res. 13:469–477.PubMedCrossRefGoogle Scholar
  8. Behnke, O., 1967, Electron microscopic observations on the membrane systems of the rat blood platelet, Anat. Ree. 158:121–138.CrossRefGoogle Scholar
  9. Behnke, O., 1970, Microtubules in disc shaped blood cells, Int. Res. Exp. Pathol. 9:1–92.Google Scholar
  10. Behnke, O., and Zelander, T., 1966, Substructure in negatively stained microtubules of mammalian blood platelets,Exp. Cell Res. 43:236–247.PubMedCrossRefGoogle Scholar
  11. Bennett, H. S., 1963, Morphological aspects of extracellular polysaccharides,J. Histochem. Cytochem. 11:14–23.CrossRefGoogle Scholar
  12. Bhattacharyya, B., and Wolff, J., 1976, Polymerization of membrane tubulin, Nature (London) 264:576–578.CrossRefGoogle Scholar
  13. Brodie, G. N., Baenziger, N. L., Chase, L. R., and Majerus, P. W., 1972, The effects of thrombin on adenyl cyclase activity and a membrane protein from human platelets, J. Clin. Invest. 51:81–87.PubMedCrossRefGoogle Scholar
  14. Broekman, M. J., Westmorland, M. P., and Cohen, P., 1974, An improved method for isolating a granules and mitochondria from human platelets, J. Cell Biol. 60:507–513.PubMedCrossRefGoogle Scholar
  15. Carey, F., Menashi, S., and Crawford, N., 1982, Localization of cyclooxygenase and thromboxane synthetase in human platelet intracellular membranes, Biochem. J. 204:847–851.PubMedGoogle Scholar
  16. Casde, A. G., and Crawford, N., 1976, Phosphorylation of platelet microtubule proteins by an endogenous protein kinase,Biochem. Soc. Trans. 4:691–693.Google Scholar
  17. Castle, A. G., and Crawford, N., 1977, The isolation and characterization of platelet microtubule proteins, Biochim. Biophys. Acta 494:76–91.PubMedGoogle Scholar
  18. Clemetson, K. J., Capitanio, A., and Lüscher, E. F., 1979, High resolution two dimensional gel electrophoresis of the proteins and glycoproteins of human blood platelets and platelet membranes, Biochim. Biophys. Acta 553:11–24.PubMedCrossRefGoogle Scholar
  19. Cohen, I., and De Vries, A., 1973, Platelet contractile regulation in an isometric system, Nature (London) 246:36–37.CrossRefGoogle Scholar
  20. Cohen, I., and Lüscher, E. F., 1975, The blood platelet contractile system, Haemostasis 4:125–243.Google Scholar
  21. Coleman, R., and Finean, J. B., 1966, Preparation and properties of isolated plasma membranes from guinea-pig tissues, Biochim. Biophys. Acta 125:197–203.Google Scholar
  22. Crawford, N., 1976, Platelet microfilaments and microtubules, in: Platelets in Biology and Pathology (J. L. Gordon, ed.) Elsevier/North Holland, Biomedical Press, Amsterdam, pp. 121–157.Google Scholar
  23. Crawford, N., Amos, L. A., and Castle, A. G., 1980, Platelet microtubule subunit proteins: Assembly and disassembly factors in platelets, in: Cellular Response Mechanisms and their Biological Significance (A. Rotman, F. A. Meyer, C. Gitler and A. Sulberberg, eds.), John Wiley & Sons, Ltd., New York, pp. 177–178.Google Scholar
  24. Cutler, L. S., Feinstein, M. B., and Christian, C. P., 1980, Cytochemical localization of oubain-sensitive K-dependent p nitrophenyl phosphatase (transport ATPase) in human blood platelets, J. Histochem. Cytochem. 28:1183–1188.PubMedCrossRefGoogle Scholar
  25. Day, H. J., Holmsen, H., and Hovig, T., 1969, Subcellular particles of human platelets, Scand. J. Haematol, (suppl. 7.1): 1–35.Google Scholar
  26. De Duve, C., 1963–64, The separation and characterization of subcellular particles, Harvey Lec. 59:49–87.Google Scholar
  27. De Duve, C., 1964, Principles of tissue fractionation, J. Theor. Biol. 6:33–39.PubMedCrossRefGoogle Scholar
  28. Feinberg, H., 1982, Platelet membrane proteins, in: Membrane Abnormalities and Disease, Volume 1 (M. Tao, ed.), C.R.C. Press, Boca Raton, Florida, pp. 91–129.Google Scholar
  29. French, P. C., Holmsen, H., and Stormorken, H., 1970, Adenine nucleotide metabolism of blood plateletsVII ATPases: Subcellular localization and behavior during the thrombin platelet interaction, Biochim. Biophys. Acta 206:438–448.PubMedGoogle Scholar
  30. George, J. N., 1978, Platelet behavior and aging in the circulation, in: Blood Platelets in Transfusion Therapy (T. J. Greenwalt and G. A. Jamieson, eds.), Alan R. Liss Inc., New York, pp. 39–64.Google Scholar
  31. George, J. N., and Lewis, P. C., 1978, Studies on platelet membranes III. Membrane glycoprotein loss from circulating platelets in rabbits: Inhibition by aspirin-dipyridamole and acceleration by thrombin, J. Lab. Clin. Med. 91:301–306.PubMedGoogle Scholar
  32. George, J. N., Lewis, P. C., and Sears, D. A., 1976, Studies in platelet plasma membranes II. Characterization of surface proteins of rabbit platelets in vitro and during circulation in vivo using diazotized 125I diiodosulfanilic acid as a label,J. Lab. Clin. Med. 88:247–260.PubMedGoogle Scholar
  33. George, J. N., Thoi, L. L., and Morgan, R. K., 1981, Quantitative analysis of platelet membrane glycoproteins: Effect of platelet washing procedures and isolation of platelet density subpopulations, Thromb. Res. 23:69–77.PubMedCrossRefGoogle Scholar
  34. Gerrard, J. M., White, J. G., and Rao, G. M. R., 1974, Effects of the ionophore A23187 on blood platelets 2. Influence on ultrastructure,Am. J. Pathol. 77:151–166.PubMedGoogle Scholar
  35. Gerrard, J. M., White, J. G., Rao, G. M. R., and Townsend, D., 1976, Localization of platelet prostaglandin production in the platelet dense tubular system. Am. J. Pathol. 83:283–294.PubMedGoogle Scholar
  36. Gerrard, J. M., White, J. G., and Peterson, D. A., 1978a, The platelet dense tubular system: Its relationship to prostaglandin synthesis and calcium flux, Thromb. Haemostasis 40:224–231.Google Scholar
  37. Gerrard, J. M., Butler, A. M., Graff, G., Stoddard, S. F., and White, J. G., 1978b, Prostaglandin endoperoxides promote calcium release from a platelet membrane preparation. Prostaglandins Leukotrienes Med. 1:373–385.Google Scholar
  38. Greenberg, J. H., Fletcher, A. P., and Jamieson, G. A., 1973, The presence of glycogen synthase in preparations of platelet plasma membranes,Thromb. Diathes. Haemorrh. 30:307–314.Google Scholar
  39. Griffith, L. M., and Pollard, T. D., 1982, The interaction of actin filaments with microtubules and microtubule associated with proteins, J. Biol. Chem. 257:9143–9151.PubMedGoogle Scholar
  40. Guccione, M. A., Packham, M. A., Kinlough-Rathbone, R. L., and Mustard, J. F., 1971, Reactions of 14C ADP and 14c ATP with washed platelets from rabbits, Blood 37:542–551.PubMedGoogle Scholar
  41. Hack, N., Carey, F., and Crawford, N., 1984, The inhibition of platelet cyclooxygenase by aspirin is associated with the acetylation of a 72kDa polypeptide in the intracellular membranes, Biochem. J. 223:105–111.PubMedGoogle Scholar
  42. Marker, L. A., 1971, Thrombokinetics, in: The Platelet (K. M. Brinkhaus, R. W. Shermer, and F. K. Mostofi, eds.), Williams and Wilkins, Baltimore, Maryland, pp. 13–25.Google Scholar
  43. Harris, H., 1981, Regulation of motile activity in platelets, Platelets in Biology and Pathology, Vol. 2 (J. L. Gordon, ed.), Elsevier-North Holland, Amsterdam, pp. 473–500.Google Scholar
  44. Harris, G. L., and Crawford, N., 1973, Isolation of pig platelet membranes and granules: Distribution and validity of marker enzymes, Biochim. Biophys. Acta 291:701–709.PubMedCrossRefGoogle Scholar
  45. Haslam, R. J., 1973, Interactions of the pharmacological receptors of blood platelets with adenylate cyclase, Ser. Hematol. 6:333–350.Google Scholar
  46. Hovig, T., 1968, The ultrastructure of platelets in normal and abnormal states, Ser. Hematol. 1:13–64.Google Scholar
  47. Käser-Glanzmann, R., George, J. N., Jakabova, M., and Lüscher, E. F., 1977, Stimulation of calcium uptake into platelet membrane vesicles by cAMP and protein kinase, Biochim. Biophys. Acta 466:429–440.PubMedCrossRefGoogle Scholar
  48. Käser-Glanzmann, R., Goerge, J. N., Jakabova, M., and Lüscher, E. F., 1978, Further characterization of the calcium accumulating vesicles from human blood platelets, Biochim. Biophys. Acta 512:1–12.PubMedCrossRefGoogle Scholar
  49. Kaulen, H. D., and Gross, R., 1973, Metabolic properties of human platelet membranes, 1. Characterization of platelet membranes prepared by sucrose and Ficoll Density gradients, Thromb. Diathes. Haemorrh. 30:307–314.Google Scholar
  50. Kinoshita, T., Nachman, R. L., and Minick, R., 1979, Isolation of human platelet membranes with polylysine beads, J. Cell Biol. 82:688–696.PubMedCrossRefGoogle Scholar
  51. Koteliansky, V. E., Gneushev, G. N., and Muszbek, L., 1983, Identification and isolation of vinculin from platelets, Thromb. Haemostasis 50:188.Google Scholar
  52. Lagarde, M., Bryon, P. A., Guichardant, M., and Dechauanne, M., 1980, A simple and efficient method for platelet isolation from their plasma, Thromb. Res. 17:581–587.PubMedCrossRefGoogle Scholar
  53. Lagarde, M., Menashi, S., and Crawford, N., 1981, Localization of phospholipase A2 and diglyceride lipase activities in human platelet intracellular membranes, Febs Lett. 124:23–26.PubMedCrossRefGoogle Scholar
  54. Lagarde, M., Authi, K. S., and Crawford, N., 1982a, Fatty acid specificity of human platelet membrane phospholipase A2 and diacylglycerol lipase, Biochem. Soc. Trans. 10:241–243.Google Scholar
  55. Lagarde, M., Guichardant, M., Menashi, S., and Crawford, N., 1982b, The phospholipid and fatty acid; composition of human platelet surface and intracellular membranes isolated by high voltage free flow electrophoresis,J. Biol. Chem. 256:3100–3104.Google Scholar
  56. Lagarde, M., Croset, M., Authi, K. S., and Crawford, N., 1984, Subcellular localization and some properties of lipoxygenase activity in human blood platelets, Biochem. J. 222:495–500.PubMedGoogle Scholar
  57. Mangenstem, E., and Stark, G., 1975 Morphometric analysis of platelet ultrastructure in normal and experimental conditions, in: Platelets: Recent Advances in Basic Research and Clinical Aspects (O.N. Ulutin and J. Verrier Jones, eds.), Excerpta Medica, Amsterdam, pp. 37–42.Google Scholar
  58. Mannuci, P. M., 1972, Methods for the preparation of wasted platelet suspension.Adv. Exp. Med. Biol. 34:57–78.Google Scholar
  59. Marcus, A. J., Zucker-Franklin, D., Safier, L. B., and Ullman, M. L., 1966, Studies on human platelet granules and membranes, J. Clin. Invest. 45:14–21.PubMedCrossRefGoogle Scholar
  60. Martin, J. F., Trowbridge, E. A., Salmon, G. L., and Slater, D. N., 1982, The relationship between platelet and megakaryocyte volumes, Thromb. Res. 28:447–459.PubMedCrossRefGoogle Scholar
  61. Martin, J. F., Slater, D. N., and Trowbridge, E. A., 1983, Abnormal intrapulmonary platelet production. A possible cause of vascular and lung disease. Lancet 1:793–796.PubMedCrossRefGoogle Scholar
  62. McKean, M. L., Smith, J. B., and Silver, M., 1983, Phospholipid biosynthesis in human platelets. Formation of phosphatidyl choline from 1-acyl lysophosphatidyl choline by acyl-CoA I acyl snglycero-3-phosphocholine transferase, J. Biol. Chem. 257:11278–11283.Google Scholar
  63. Menashi, S., Harwood, R., and Grant, M. E., 1976, Native collagen is not a substrate for collagen glucosyl transferase of platelets, Nature (London) 246(5587):670–672.CrossRefGoogle Scholar
  64. Menashi, S., Weintroub, H., and Crawford, N., 1981, Characterization of human platelet surface and intracellular membranes isolated by free flow electrophoresis, J. Biol. Chem. 256:4095–4101.PubMedGoogle Scholar
  65. Menashi, S., Authi, K. S., Carey, F., and Crawford, N., 1984, Characterization of the calcium-sequestering process associated with human platelet intracellular membranes isolated by free-flow electrophoresis, Biochem. J. 222:413–417.PubMedGoogle Scholar
  66. Minter, B. F., and Crawford, N., 1967, The subcellular distribution of serotonin in blood platelets before and after incubation with serotonin, Biochem. J. 105:22–23.Google Scholar
  67. Minter, B. F., and Crawford, N., 1974, Subcellular distribution of reserpine and 5-hydroxytryptamine in blood platelets after treatment with reserpine in vitro and in vivo, Biochem. Pharmacol. 23:351–367.;CrossRefGoogle Scholar
  68. Moake, J. L., Ahmed, K., Bachur, N. R., and Gutfreund, D. E., 1970, Mg2+ dependent (Na+,K +)-stimulated ATPase of human platelets: Properties and inhibition by ADP, Biochim. Biophys. Acta 211:337–344.CrossRefGoogle Scholar
  69. Morrissey, J. H., 1981, A silver stain for proteins in Polyacrylamide gels. A modified procedure with enhanced uniform sensitivity. Anal. Biochem. 117:307–310.PubMedCrossRefGoogle Scholar
  70. O'Farrell, P. H., 1975, High resolution two-dimensional electrophoresis of proteins, J. Biol. Chem. 250:4007–4021.PubMedGoogle Scholar
  71. Paulus, J. M., 1975, Platelet size in man. Blood 46:321–336.PubMedGoogle Scholar
  72. Pennington, D. G., 1981, Formation of platelets, in: Research Monographs in Cell and Tissue Physiology, Volume 5, Platelets in Biology and Pathology—2 (J. L. Gordon, ed.), Elsevier/North Holland Biomedical Press, Amsterdam, pp. 19–41.Google Scholar
  73. Pennington, D. G., and Streatfield, K., 1975, Heterogeneity of megakaryocytes and platelets, Ser. Hematol. 8:22–48.Google Scholar
  74. Pennington, D. G., Streatfield, D. G. K., and Weste, S., 1974, Megakaryocyte ploidy and ultrastructure in stimulated thrombopoiesis, in: Platelets—Production, Function, Transfusion and Storage (M. Baldini and S. Ebbe, eds.), Grune and Stratton, New York, pp. 115–130.Google Scholar
  75. Rittenhouse-Simmons, S., and Deykin, D., 1976, Isolation of membranes from normal and thrombin-treated gel filtered platelets using a lectin marker, Biochim. Biophys. Acta 426:688–674.PubMedCrossRefGoogle Scholar
  76. Roth, G. T., and Majerus, P. W., 1975, The mechanism of the effect of aspirin on human platelets. 1. Acetylation of a particulate fraction protein,J. Clin. Invest. 56:624–632.PubMedCrossRefGoogle Scholar
  77. Roth, G. T., Stanford, N., and Majerus, P. W., 1975, Acetylation of prostaglandin synthase by aspirin, Proc. Natl. Acad. Sei. U.S.A. 72(8):3073–3076.CrossRefGoogle Scholar
  78. Saba, S. R., Rodman, N. F., and Mason, R. G., 1969, Platelet ATPase activities II. ATPase activities of isolated platelet membrane fractions, Am. J. Pathol. 55:225.PubMedGoogle Scholar
  79. Salganicoff, L., Hebda, P. A., Yandrasitz, J., and Fukami, M. M., 1975, Subcellular fractionation of pig platelets, Biochim. Biophys. Acta 385:394–411.PubMedCrossRefGoogle Scholar
  80. Schliwa, M., and van Blerkon, J., 1981, Structural interaction of cytoskeletal components, J. Cell Biol. 90(l):222–235.PubMedCrossRefGoogle Scholar
  81. Siegel, A., and Lüscher, E. F., 1967, Non-identity of the a-granules of human blood platelets with typical lysosomes. Nature (London) 215:745–747.CrossRefGoogle Scholar
  82. Sixma, J. J., and Lips, J. P. M., 1978, Isolation of platelet membranes: A review,Thromb. Haemostasis 39:328–337.Google Scholar
  83. Sixma, J. J., and Schiphorst, M. E., 1980, Identification of ectoproteins of human platelets. Combination of radioactive labelling and two dimensional electrophoresis,Biochim. Biophys. Acta 603:70–83.PubMedCrossRefGoogle Scholar
  84. Slater, D. N., Trowbridge, E. A., and Martin, J. F., 1983, The megakaryocyte in thrombocytopaenia: A microscopic study which supports the theory that platelets are produced in the pulmonary circulation, Thromb. Res. 28:475–483.Google Scholar
  85. Smith, S. K., and Limbird, L. E., 1982, Evidence that human platelet a adrenergic receptors coupled to inhibition of adenylate cyclase are not associated with the subunit of adenylate cyclase ADP ribosylated by cholera toxin,J. Biol. Chem. 257:10471–10478.PubMedGoogle Scholar
  86. Statland, B. E., Heagen, B. M., and White, J. G., 1969, Uptake of calcium by platelet relaxing factor, Nature (London) 223:521–522.CrossRefGoogle Scholar
  87. Taylor, D. G., and Crawford, N., 1974a, The subfractionation of platelet membranes by zonal centrifugation: Identification of surface membranes, Febs Lett. 41:317–321.PubMedCrossRefGoogle Scholar
  88. Taylor, D. G., and Crawford, N., 1974b, The subcellular fractionation of pig blood platelets by zonal centrifugation, in:Methodological Developments in Biochemistry, Volume 4, Subcellular Studies (E. Reid, ed.), Longmans Press Ltd. Burnt Hill, Harlow, Essex, England, pp. 319–326.Google Scholar
  89. Trowbridge, E. A., Martin, J. F., and Slater, D. N., 1982, Evidence for a theory of physical fragmentation of megakaryocytes implying that all platelets are produced in the pulmonary circulation, Thromb. Res. 28:461–475.PubMedCrossRefGoogle Scholar
  90. White, J. G., 1971, Platelet morphology, in: The Circulating Platelet (S.A. Johnson, ed.). Academic Press, New York, pp. 45–121.Google Scholar
  91. White, J. G., 1972a, Interaction of membrane systems in blood platelets, Am. J. Pathol. 66:295–372.PubMedGoogle Scholar
  92. White, J. G., 1972b, Uptake of latex particles by human platelets. Phagocytosis or sequestration, Am. J. Pathol. 70:45–56.Google Scholar
  93. White, J. G., and Krivit, W., 1965, Fine structural localization of adenosine triphosphatase in human platelets and other blood cells, Blood 26:554–568.PubMedGoogle Scholar
  94. White, J. G., and Sank, J. J., 1984, Microtubule coils in spread blood platelets.Blood 64:470–478.PubMedGoogle Scholar

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© Plenum Press, New York 1985

Authors and Affiliations

  • Neville Crawford
    • 1
  1. 1.Department of Biochemistry, Institute of Basic Medical ScienceRoyal College of Surgeons of EnglandLondonEngland

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