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Hamostaseologie 1996; 16(02): 88-96
DOI: 10.1055/s-0038-1656644
Übersichtsarbeiten/Review Articles
Schattauer GmbH

Evolution of Cellular Haemostasis

The Stem Cell-Megakaryocyte-Blood Platelet System
W. Schneider
1   Klinik für Hämatologie, Onkologie und klinische Immunologie, Heinrich-Heine-Universität Düsseldorf
,
N. Gattermann
1   Klinik für Hämatologie, Onkologie und klinische Immunologie, Heinrich-Heine-Universität Düsseldorf
› Author Affiliations
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Publication History

Publication Date:
23 July 2018 (online)

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Summary

Haemostasis in primitive organisms relies on simple mechanisms of wound re-pair. During evolution, haemostasis developed in parallel with rising metabolic activity, more complex circulatory systems, and increasing size of organisms. Thrombocytes are first found in lower vertebrates. However, these cells are nucleated and derive directly from haematopoietic progenitor cells, without an interposed megakaryocyte system. Megakaryocytes are an evolutionary innovation in mammalians and human beings. Their unique system of proliferation and differentiation provided the basis for an enormous increase in the production of the haemostatically active elements, the platelets. In contrast to nucleated thrombocytes, these fragments of megakaryocyte cytoplasm have improved haemostatic functions and show favourable rheologic features that facilitate their interaction with the vessel wall. The megakaryocyte system is susceptible to a variety of regulatory factors, in particular thrombopoietin and other haematopoietic and inflammatory cytokines. On the one hand, this enables the stem cell -megakaryocyte - platelet system to adapt its platelet production to increased haemostatic demand. On the other hand, acute or chronic overstimulation of megakaryocytopoiesis by infection, inflammation or malignant disease, can cause severe thromboembolic or thrombohaemorrhagic complications. Because these problems usually manifest themselves relatively late in life, namely after reproductive ages, they could not be eliminated during evolution.

Keywords

Nucleated thrombocytes - blood platelets - megakaryocytopoiesis - adhesion molecules - stem cells
 

  • REFERENCES

  • 1 Basch RS, Kouri YH, Karpatkin S. Expression of CD4 by human megakaryocytes. Proc Natl Acad Sci USA 1990; 87: 8085-9
    CrossrefPubMedGoogle Scholar
  • 2 Belamarich FA. Hemostasis in animals other than mammals: the role of cells. Progr Haemostas Thrombos 1976; 3: 191-209
    PubMedGoogle Scholar
  • 3 Belamarich FA, Stiller RA, Shepro D. The release reaction: is it a common mechanism in all types of hemostatic cells?. Ser Haemat 1973; 6: 418-28
    PubMedGoogle Scholar
  • 4 Berger G, Massé JM, Cramer EM. Alpha-granule membrane mirrors the platelet plasma membrane and contains the glycoproteins Ib, IX, and V. Blood 1996; 87: 1385-95
    CrossrefPubMedGoogle Scholar
  • 5 Briddell RA, Brandt JE, Straneva JE. et al. Characterizeation of the human burst forming unit-megakaryocyte. Blood 1989; 74: 145-51
    PubMedGoogle Scholar
  • 6 Broudy VC, Lin N, Kaushansky K. Throm-bopoietin (c-mpl ligand) acts synergistically with erythropoietin and stem cell factor to enhance murine megakaryocyte colony growth and increases megakaryocyte poly-poloidy in vitro. Blood 1994; 84 (Suppl. 01) 330a (1304)
    PubMedGoogle Scholar
  • 7 Burstein SA, Breton-Gorius J. Megakaryo-poiesis and platelet formation. In: Williams Hematology. Fifth Edition. Beutler E, Licht-man MA, Coller BS. et al. (eds). New York: McGraw-Hill; 1995: 1149-61
    Google Scholar
  • 8 Campbell NA. Biology Bd Redwood City. California: Benjamin/Cummings Publishing; 1990: 36-50
    Google Scholar
  • 9 Campbell NA. Water and the fitness of the environment. In: Biology Redwood City. California: Benjamin/Cummings Publishing Comp., Inc; 1990: 36-50
    Google Scholar
  • 10 Dolzhanskiy A, Basch RS, Karpatkin S. Development of human megakaryocytes: I. Hematopoietic progenitors (CD34+ bone marrow cells) are enriched with megakaryocytes expressing CD4. Blood 1996; 87: 1353-60
    PubMedGoogle Scholar
  • 11 Duke WW. The relation of blood platelets to haemorrhagic disease. JAMA 1910; 55: 1185-92
    CrossrefPubMedGoogle Scholar
  • 12 Eigenthaler M, Ullrich H, Geiger J. et al. Defective nitrovasodilator-stimulated protein phosphorylation and calcium regulation in cGMP-dependent protein kinase-defi-cient human platelets of chronic myelocytic leukemia. J Biol Chem 1993; 268: 13526-31
    PubMedGoogle Scholar
  • 13 Feinendegen LE, Odartchenko N, Cotties H. et al. Kinetics of megakaryocyte proliferation. Proc Soc Exper Biol Med 1962; 111: 177-82
    CrossrefPubMedGoogle Scholar
  • 14 Foster D, Sprecher C, Grant F. et al. Human thrombopoietin: gene structure, cDNA sequence, expression and chromosomal localization. Proc Natl Acad Sci USA 1994; 91: 13023-7
    CrossrefPubMedGoogle Scholar
  • 15 Geiger J, Nolte C, Walter U. Regulation of calcium mobilization and entry in human platelets by endothelium-derived factors. Am J Physiol 1994; 267: C236-44
    CrossrefPubMedGoogle Scholar
  • 16 George IN, El-Harake ME, Aster RH. Thrombocytopenia due to enhanced platelet destruction by immunologic mechanisms. In: Williams Hematology, Fifth Edition. Beutler E, Lichtman MA, Coller BS. et al. (eds). New York: St. Louis, San Francisco: Mcgraw-Hill; 1995: 1315-55
    Google Scholar
  • 17 Gewirtz AM, Boghosian-Sell L, Catani L. et al. Expression of Fc gamma RH and CD4 receptors by normal human megakaryocytes. Exp Hematol 1992; 20: 512-6
    PubMedGoogle Scholar
  • 18 Gewirtz AM, Poncz M. Megakaryocytopoie-sis and platelet production. In: Hematology. Basic Principles and Practice. Hoffman R, Benz EJ, Shattil SJ. et al. (eds). New York: Churchill Livingstone; 1991: 1148-57
    Google Scholar
  • 19 Hancock V, Martin JF, Lelchuk R. The relationship between human megakaryocyte nuclear DNA content and gene expression. Br J Haematol 1993; 85: 692-7
    CrossrefPubMedGoogle Scholar
  • 20 Harker L, Slichter S. The bleeding time as a screening test for evaluation of platelet function. N Engl J Med 1972; 287: 155-9
    CrossrefPubMedGoogle Scholar
  • 21 Harker LA, Hunt P, Marzec UM. et al. Regulation of platelet production and function by megakaryocyte growth and development factor in nonhuman primates. Blood 1996; 87: 1833-44
    PubMedGoogle Scholar
  • 22 Hawkey CM. Comparative Mammalian Hematology. London: Heineman; 1974
    Google Scholar
  • 23 Heemskerk JW, Feijge MA, Sage SO. et al. Indirect regulation of Ca2+ entry by cAMP-dependent and cGMP-dependent protein kinases and phospholipase C in rat platelets. Eur J Biochem 1994; 223: 543-51
    CrossrefPubMedGoogle Scholar
  • 24 Hegyi E, Nakazawa M, Debili N. et al. Developmental changes in human megakaryocyte ploidy. Exp Hematol 1991; 19: 87-94
    PubMedGoogle Scholar
  • 25 Hirama T, Koeffler HP. Role of the cyclin-dependent kinase inhibitors in the development of cancer. Blood 1995; 86: 841-54
    PubMedGoogle Scholar
  • 26 Jackson CW. Megakaryocyte endomitosis: a review. Intern J Cell Cloning 1990; 8: 224-6
    PubMedGoogle Scholar
  • 27 Jandl JH. Blood. Textbook of Hematology. Bd Boston/Toronto: Little, Brown and Company; 1987: 40
    Google Scholar
  • 28 Janzarik H, Morgenstern E. The nucleated thrombocytoid cells. I. Electron microscopic studies on chicken blood cells. Thromb Haemost 1979; 41: 608-21
    Article in Thieme ConnectPubMedGoogle Scholar
  • 29 Johnson GR, Barker DC. Erythroid progenitor cells and stimulating factors during murine embryonic and fetal development. Exp Hematol 1985; 13: 200-8
    PubMedGoogle Scholar
  • 30 Kaushansky K, Lok S, Holly RD. et al. Promotion of megakaryocyte progenitor expansion and differentiation by the c-Mpl ligand thrombopoietin. Nature 1994; 369: 568-71
    CrossrefPubMedGoogle Scholar
  • 31 Kelemen E. Specific thrombopoietin cloned and sequenced - with personal retrospect and clinical prospects. Leukemia 1995; 9: 1-2
    PubMedGoogle Scholar
  • 32 Kelemen E, Cserhati I, Tanos B. Demonstration and some properties of human thrombopoietin in thrombocythemic sera. Acta Haematol 1958; 20: 350
    CrossrefPubMedGoogle Scholar
  • 33 Kouri YH, Borkowsky W, Nardi M. et al. Human megakaryocytes have a CD4 molecule capable of binding human immunodeficiency virus-1. Blood 1993; 81: 2664-70
    PubMedGoogle Scholar
  • 34 Krause DS, Fackler MJ, Civin CI. et al. CD34: Structure, biology, and clinical utility. Blood 1996; 87: 1-13
    PubMedGoogle Scholar
  • 35 Kristensen SD, Bath PMW, Martin JF. The bleeding time is inversely related to megakaryocyte nuclear DNA content and size in man. Thromb Haemost 1988; 59: 357-9
    Article in Thieme ConnectPubMedGoogle Scholar
  • 36 Lefkovits J, Topol EJ. Platelet glycoprotein Ilb/IIIa receptor inhibitors in ischemic heart disease. Curr Opin Cardiol 1995; 10: 420-6
    CrossrefPubMedGoogle Scholar
  • 37 Lok S, Kaushansky K, Holly R. et al. Cloning and expression of murine thrombopoietin cDNA and stimulation of platelet production in vivo. Nature 1994; 369: 565-8
    CrossrefPubMedGoogle Scholar
  • 38 Metcalf D. Thrombopoietin - at last. Nature 1994; 369: 519-20
    CrossrefPubMedGoogle Scholar
  • 39 Michelson AD, Benoit SE, Furman MI. et al. The platelet surface expression of glycoprotein V is regulated by two independent mechanisms: proteolysis and a reversible cy-toskeletal-mediated redistribution to the surface-connected canalicular system. Blood 1996; 87: 1396-408
    PubMedGoogle Scholar
  • 40 Mouthon MA, Bernard O, Mitjavila MT. et al. Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood 1993; 81: 647-55
    PubMedGoogle Scholar
  • 41 Nagahisa H, Nagata Y, Ohnuki T. et al. Bone marrow stromal cells produce thrombopoietin and stimulate megakaryocyte growth and maturation but suppress proplatelet formation. Blood 1996; 87: 1309-16
    PubMedGoogle Scholar
  • 42 Niewiarowski S, Varma KG. Biochemistry and physiology of secreted platelet proteins. In: Hemostasis and Thrombosis. Basic Principles and Clinical Practice. Colman EW, Hirsh J, Marder VJ. et al. (eds). Philadelphia, Toronto: JB Lippincott Comp; 1982: 421-30
    Google Scholar
  • 43 Nishihira H, Toy oda Y, Miyazaki H. et al. Growth of macroscopic human megakaryocyte colonies from cord blood in culture with recombinant human thrombopoietin (c-mpl ligand) and the effects of gestational age on frequency of colonies. Br J Haematol 1996; 92: 23-8
    CrossrefPubMedGoogle Scholar
  • 44 Novitzky TJ. Endotoxins and their detection with the limulus amebocyte lysate test. In: Progress in Clinical and Biological Research. New York: Alan R Liss, Inc; 1982
    Google Scholar
  • 45 Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993; 81: 2844-53
    CrossrefPubMedGoogle Scholar
  • 46 Orkin SH. GATA-binding transcription factors in hematopoietic cells. Blood 1992; 80: 575-81
    PubMedGoogle Scholar
  • 47 O'Brien JR, Etherington M, Jamieson S. et al. Stressed template bleeding time and other platelet function tests in myocardial infarction. Lancet 1973; 1: 694-6
    PubMedGoogle Scholar
  • 48 Paulus JM, Grosdent JC, Prenant M. et al. Factors regulating megakaryocyte progenitor commitment to polyploidization. C R Acad Sci Iii 1995; 381-6
    PubMedGoogle Scholar
  • 49 Sauvage de F, Hass P, Spencer S. et al. Stimulation of megakaryocytopoiesis and throm-bopoiesis by the c-Mpl ligand. Nature 1994; 369: 533-8
    CrossrefPubMedGoogle Scholar
  • 50 Savage B, Bottini E, Ruggeri ZM. Interaction of integrin alpha lib beta 3 with multiple fibrinogen domains during platelet adhesion. J Biol Chem 1995; 270: 28812-7
    CrossrefPubMedGoogle Scholar
  • 51 Schick BP. Clinical implications of basic research: Hope for treatment of thrombocytopenia. N Engl J Med 1994; 331: 875-6
    CrossrefPubMedGoogle Scholar
  • 52 Schneider W, Gattermann N. Megakaryocytes: Origin of bleeding and thrombotic disorders. Europ J Clin Invest 1994; 24: 16-20
    CrossrefPubMedGoogle Scholar
  • 53 Shimamoto T, Ohyashiki K, Ohyashiki JH. et al. The expression pattern of erythrocyte/ megakaryocyte-related transcription factors GATA-1 and the stem cell leukemia gene correlates with hematopoietic differentiation and is associated with outcome of acute myeloid leukemia. Blood 1995; 86: 3173-80
    PubMedGoogle Scholar
  • 54 Sieff CA, Williams DA. Hematopoiesis. In: Blood. Principles and Practice of Hematology. Handin RI, Lux SE, Stossel TP. (eds). Philadelphia: JB Lippincott Company; 1995: 171-224
    Google Scholar
  • 55 Subramaniam M, Frenette PS, Saffaripour S. et al. Defects in hemostasis in P-selectin deficient mice. Blood 1996; 87: 1238-42
    PubMedGoogle Scholar
  • 56 Visvader JE, Elefanty AG, Strasser A. et al. GATA-1 but not SCL induces megakaryocytic differentiation in an early myeloid line. EMBO 1992; 11: 4557
    CrossrefPubMedGoogle Scholar
  • 57 Wachowicz B. Binding of adenosine diphosphate to turkey thrombocytes. Haemostasis 1982; 11: 139-48
    PubMedGoogle Scholar
  • 58 Wachowicz B, Krajewski T. The released proteins from avian thrombocytes. Thromb Haemost 1979; 42: 1289-95
    Article in Thieme ConnectPubMedGoogle Scholar
  • 59 Wendling F, Maraskovsky E, Debili N. et al. c-Mpl ligand is a humoral regulator of megakaryocytopoiesis. nature 1994; 369: 571-4
    CrossrefPubMedGoogle Scholar
  • 60 Williams N. Is thrombopoietin interleukin 6?. Exp Hematol 1991; 19: 714-8
    PubMedGoogle Scholar
  • 61 Winkelmann M, Pfitzer P, Schneider W. Significance of polyploidy in megakaryocytes and other cells in health and tumor disease. Klin Wochenschr 1987; 65: 1115-31
    CrossrefPubMedGoogle Scholar
  • 62 Wright JH. The histogenesis of the blood platelets. J Morphol 1910; 21: 263
    CrossrefPubMedGoogle Scholar
  • 63 Zon L. l. Developmental biology of hematopoiesis. Blood 1995; 86: 2876-91
    PubMedGoogle Scholar