Thrombocytogenesis by megakaryocyte; Interpretation by protoplatelet hypothesis

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 87, Issue 5, 2011, Pages 254-273

  Kosaki, Goro ^a   Kambayashi, Junichi ^b  

^a OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^b Otsuka Maryland Medicinal Labs   (United States)

Author keywords

Cytoplasmic fragmentation model; Megakaryocyte; Platelet production; Proplatelet; Protoplatelet

Indexed keywords

BIOLOGICAL MODEL; CELL DIFFERENTIATION; CENTRIOLE; CYTOLOGY; HUMAN; MEGAKARYOCYTE; METABOLISM; POLYPLOIDY; REVIEW; THROMBOCYTE; ULTRASTRUCTURE;

BLOOD PLATELETS; CELL DIFFERENTIATION; CENTRIOLES; HUMANS; MEGAKARYOCYTES; MODELS, BIOLOGICAL; POLYPLOIDY;

EID: 79957571972     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.87.254     Document Type: Review

References (70)

1. Wright, J.H. (1906) Die Entstehung der Blutplättchen. Virchows Arch. 186, 55-63.
2. Bessis, M. (1956) Cytology of the Blood and Bloodforming Organs. Grune & Stratton, New York.
3. Yamada, E. (1957) The fine structure of the megakaryocyte in the mouse spleen. Acta Anat. (Basel) 28, 267-290.
4. Kosaki, G., Tanaka, K. and Inoshita, K. (1973) Electron microscopic observations on megakaryocyte differentiation and platelet production. Acta Haematol. Jpn. 36, 383-384 (in Japanese).
5. Kosaki, G., Inoshita, K. and Okuma, H. (1974) Electron microscopic studies on human thrombocytogenesis. In Platelets, Thrombosis and Inhibitors (eds. Didisheim, P., Shimamoto, T. and Yamazaki, H.). Schattauer, Stuttgart, pp. 97-102.
6. Kosaki, G. and Fujimoto, T. (1979) Morphology of blood platelets, megakaryocytes differentiation and platelet release. In Nippon-Ketsuekigaku-Zensho (New Edition), vol. 11 Hemorrhagic diathesis (ed. The Publication Committee). Maruzen, Tokyo, pp. 1-55 (in Japanese).
7. Behnke, O. (1968) An electron microscope study of the megacaryocyte of the rat bone marrow. I. The development of the demarcation membrane system and the platelet surface coat. J. Ultrastruct. Res. 24, 412-433.
8. Behnke, O. (1969) An electron microscope study of the rat megacaryocyte. II Some aspects of platelet release and microtubules. J. Ultrastruct. Res. 26, 111-129.
9. Becker, R.P. and De Bruyn, P.P.H. (1976) The transmural passage of blood cells into myeloid sinusoids and the entry of platelets into the sinusoidal circulation; a scanning electron microscopic investigation. Am. J. Anat. 145, 183-206.
10. Muto, M. (1976) A scanning and transmission electron microscopic study on rat bone marrow sinuses and transmural migration of blood cells. Arch. Histol. Jpn. 39, 51-66.
11. Thiéry, J.P. and Bessis, M. (1956) Mecanisme de la plaquettogenese. Etude "in vitro" par la microcinematographie. Rev. Hematol. (Paris) 11, 162- 174.
12. Albrecht, M. (1957) Studien zur Thrombocytenbildung an Megakaryocyten in menschlichen Knochenmarkkulturen. Acta Haematol. 17, 160- 168.
13. Radley, J.M. and Scurfield, G. (1980) The mechanism of platelet release. Blood 56, 996-999.
14. Italiano, J.E. Jr., Lecine, P., Shivdasani, R.A. and Hartwig, J.H. (1999) Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes. J. Cell Biol. 147, 1299-1312.
15. Wright, J.H. (1910) The histogenesis of the blood platelets. J. Morphol. 21, 263-278.
16. Kinosita, R. and Ohno, S. (1961) Biodynamics of thrombopoiesis. In Blood Platelets (eds. Johnson, S.A., Monto, R.W., Rebuck, J.W. and Horn, R.C.). Little Brown, Boston, pp. 611-616.
17. Albrecht, M. (1969) Untersuchungen zur Thrombozytenbildung an Megakaryozyten in vitro. In Der Thrombozyt (ed. Marx, R.). Lehmanns, München, pp. 44-51.
18. Junt, T., Schulze, H., Chen, Z., Massburg, S., George, T., Krueger, A., Wagner, D.D., Graf, T., Italiano, J.E. Jr., Shivdasani, R.A. and von Andrian, U.H. (2007) Dynamic visualization of thrombopoiesis within bone marrow. Science 317 (5845), 1767-1770.
19. Richardson, J.L., Shivdasani, R.A., Boers, C., Hartwig, J.H. and Italiano, J.E. Jr. (2005) Mechanisms of organelle transport and capture along proplatelets during platelet production. Blood 106, 4066-4075.
20. Zucker-Franklin, D. and Petursson, S. (1984) Thrombocytopoiesis: analysis by membrane tracer and freeze-fracture studies on fresh human and cultured mouse megakaryocytes in vitro. J. Cell Biol. 99, 390-402.
21. Straneva, J.E., Goheen, M.P., Hui, S.L., Bruno, E. and Hoffman, R. (1986) Terminal cytoplasmic maturation of human megakaryocytes in vitro. Exp. Hematol. 14, 919-929.
22. Falcieri, E., Bassini, A., Pierpaoli, S., Luchetti, F., Zamai, L., Vitale, M., Guidotti, L. and Zauli, G. (2000) Ultrastructural characterization of maturation, platelet release, and senescence of human cultured megakaryocytes. Anat. Rec. 258, 90-99.
23. Kosaki, G. (2008) Platelet production by megakaryocytes: protoplatelet theory justifies cytoplasmic fragmentation model. Int. J. Hematol. 88, 255- 267.
24. Kosaki, G. (2003) Ultrastructural characterization of in vivo platelet release from megakaryocytes. Does it occur via proplatelets? Proposal of a new concept "protoplatelet". Jpn. J. Thromb. Hemost. 14, 495-506 (in Japanese).
25. Kosaki, G. (2005) In vivo platelet production from mature megakaryocytes: does platelet release occur via proplatelets? Int. J. Hematol. 81, 208-219.
26. Bessis, M. (1973) The thrombocytic series. In Living Cells, Their Ultrastructure (ed. Bessis M.). Springer, Berlin, p. 370.
27. Nagata, Y., Muro, Y. and Todokoro, K. (1997) Thrombopoietin-induced polyploidization of bone marrow megakaryocytes is due to a unique regulatory mechanism in late mitosis. J. Cell Biol. 139, 449-457.
28. Vitrat, N., Cohen-Solal, K., Pique, C., Le Couedic, J.P., Norol, F., Larsen, A.K., Katz, A., Vainchenker, W. and Debili, N. (1998) Endomitosis of human megakaryocytes are due to abortive mitosis. Blood 91, 3711-3723.
29. Bassini, A., Pierpaoli, S., Falcieri, E., Vitale, M., Guidotti, L., Capitani, S. and Zauli, G. (1999) Selective modulation of the cyclin B/CDK1 and cyclin D/CDK4 complexes during in vitro human megakaryocyte development. Br. J. Haematol. 104, 820-828.
30. Oakley, C.E. and Oakley, B.R. (1989) Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338, 662-664.
31. Dictenberg, J.B., Zimmerman, W., Sparks, C.A., Young, A., Vidair, C., Zheng, Y., Carrington, W., Fay, F.S. and Doxsey, S.J. (1998) Pericentrin and γ-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J. Cell Biol. 141, 163-174.
32. Patel, S.R., Richardson, J.L., Schulze, H., Kahle, E., Galjart, N., Drabek, K., Shivdasani, R.A., Hartwig, J.H. and Italiano, J.E. Jr. (2005) Differential roles of microtubule assembly and sliding in proplatelet formation by megakaryocytes. Blood 106, 4076-4085.
33. Mori, Y., Akedo, H., Tanigaki, Y., Tanaka, K. and Okada, M. (1979) Ciliogenesis in tissue-cultured cells by the increased density of cell population. Exp. Cell Res. 120, 435-439.
34. McNiven, M.A., Wang, M. and Porter, K.R. (1984) Microtubule polarity and the direction of pigment transport reverse simultaneously in surgically severed melanophore arms. Cell 37, 753-765.
35. Moskwin-Tarkhanov, M.I. and Onishchenko, G.E. (1978) Centrioles in megakaryocytes of mouse bone marrow. Tsitologiia 20, 1436-1437.
36. Behnke, O. (1970) Microtubules in disk-shaped blood cells. Int. Rev. Exp. Pathol. 9, 1-92.
37. Jiang, F., Jia, Y. and Cohen, I. (2002) Fibronectinand protein kinase C-mediated activation of ERK/MAPK are essential for proplatelet-like formation. Blood 99, 3579-3584.
38. Patel-Hett, S., Richardson, J.L., Schulze, H., Drabek, K., Isaac, N.A., Hoffmeister, K., Shivdasani, R.A., Bulinski, J.C., Galjart, N., Hartwig, J.H. and Italiano, J.E. Jr. (2008) Visualization of microtubule growth in living platelets reveals a dynamic marginal band with multiple microtubules. Blood 111, 4605-4616.
39. Lewis, S.A., Gu, W. and Cowan, N.J. (1987) Free intermingling of mammalian β-tubulin isotypes among functionally distinct microtubules. Cell 49, 539-548.
40. Radley, J.M. and Haller, C.J. (1982) The demarcation membrane system of the megakaryocyte: a misnomer? Blood 60, 213-219.
41. Haller, C.J. and Radley, J.M. (1983) Time-lapse cinemicrography and scanning electron microscopy of platelet formation by megakaryocytes. Blood Cells 9, 407-418.
42. Shaklai, M. and Tavassoli, M. (1978) Demarcation membrane system in rat megakaryocyte and the mechanism of platelet formation: a membrane reorganization process. J. Ultrastruct. Res. 62, 270-285.
43. Tavassoli, M. (1979) Fusion-fission reorganization of membrane: a developing membrane model for thrombocytogenesis in megakaryocytes. Blood Cells 5, 89-99.
44. Mahaut-Smith, M.P., Thomas, D., Higham, A.B., Usher-Smith, J.A., Hussain, J.F., Martinez-Pinna, J., Skepper, J.N. and Mason, M.J. (2003) Properties of the demarcation membrane system in living rat megakaryocytes. Biophys. J. 84, 2646-2654.
45. Schulze, H., Korpal, M., Hurov, J., Kim, S.W., Zhang, J., Cantley, L.C., Graf, T. and Shivdasani, R.A. (2006) Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood 107, 3868-3875.
46. Radley, J.M., Hartshorn, M.A. and Green, S.L. (1987) The response of megakaryocytes with processes to thrombin. Thromb. Haemost. 58, 732-736.
47. Eldor, A., Levine, R.F., Caine, Y.G., HyAm, E. and Vlodavsky, I. (1986) Megakaryocyte interaction with the subendothelial extracellular matrix. Prog. Clin. Biol. Res. 215, 399-404.
48. Maximow, A. (1927) Megakaryocyten. In Handbuch der mikroskopischen Anatomie des Menschen. 2ter Band, 1terTeil (ed. Moellendorff, W.). Julius Springer, Berlin, pp. 405-409.
49. Cramer, E.M., Norol, F., Guichard, J., Breton-Goruis, J. and Vainchenker, W. (1997) Ultrastructure of platelet formation by human megakaryocytes cultured with the Mpl ligand. Blood 89, 2336-2346.
50. Flaumenhaft, R., Dilks, J.R., Richardson, J., Alden, E., Patel-Hett, S.R., Battinelli, E., Klement, G.L., Sola-Visner, M. and Italiano, J.E. Jr. (2009) Megakaryocyte-derived microparticles: direct visualization and distinction from platelet-derived microparticles. Blood 113, 1112-1121.
51. Radley, J.M. and Hartshorn, M.A. (1987) Megakaryocyte fragments and the microtubule coil. Blood Cells 12, 603-610.
52. Handagama, P.J., Feldman, B.F., Jain, N.C., Farver, T.B. and Kono, C.S. (1987) Circulating proplatelets: isolation and quantitation in healthy rats and in rats with induced acute blood loss. Am. J. Vet. Res. 48, 962-965.
53. Tong, M., Seth, P. and Penington, D.G. (1987) Proplatelets and stress platelets. Blood 69, 522- 528.
54. Zucker-Franklin, D. and Philipp, C.S. (2000) Platelet production in the pulmonary capillary bed: new ultrastructural evidence for an old concept. Am. J. Pathol. 157, 69-74.
55. Leven, R.M. and Tablin, F. (1992) Extracellular matrix stimulation of guinea pig megakaryocyte proplatelet formation in vitro is mediated through the vitronectin receptor. Exp. Hematol. 20, 1316- 1322.
56. Larson, M.K. and Watson, S.P. (2006) Regulationof proplatelet formation and platelet release by integrin αIIbβ3. Blood 108, 1509-1514.
57. Rojnuckarin, P. and Kaushansky, K. (2001) Actin reorganization and proplatelet formation in murine megakaryocytes: the role of protein kinase Cα. Blood 97, 154-161.
58. Lecine, P., Italiano, J.E. Jr., Kim, S.W., Villeval, J.L. and Shivdasani, R.A. (2000) Hematopoieticspecific β1-tubulin participates in a pathway of platelet biogenesis dependent on the transcription factor NF-E2. Blood 96, 1366-1373.
59. Hartwig, J. and Italiano, J. Jr. (2003) The birth of the platelet. J. Thromb. Haemost. 1, 1580-1586.
60. Schulze, H., Korpal, M., Bergmeier, W., Italiano, J.E. Jr., Wahl, S.M. and Shivdasani, R.A. (2004) Interactions between the megakaryocyte/plateletspecific β1 tubulin and the secretory leucocyte protease inhibitor SLPI suggest a role for regulated proteolysis in platelet functions. Blood 104, 3949- 3957.
61. Lichtman, M.A., Chamberlain, J.K., Simon, W. and Santillo, P.A. (1978) Parasinusoidal location of megakaryocytes in marrow: a determinant of platelet release. Am. J. Hematol. 4, 303-312.
62. Kojima, H., Kozuma, Y. and Nagasawa, T. (2006) Mechanism of platelet production from megakaryocytes -role of proplatelet formation-. Jpn. J. Thromb. Hemost. 17, 261-271 (in Japanese).
63. Schwer, H.D., Lecine, P., Tiwari, S., Italiano, J.E. Jr., Hartwig, J.H. and Shivdasani, R.A. (2001) A lineage-restricted and divergent β-tubulin isoform is essential for the biogenesis, structure and function of blood platelets. Curr. Biol. 11, 579- 586.
64. Italiano, J.E. Jr., Bergmeier, W., Tiwari, S., Falet, H., Hartwig, J.H., Hoffmeister, K.M., André, P., Wagner, D.D. and Shivdasani, R.A. (2003) Mechanisms and implications of platelet discoid shape. Blood 101, 4789-4796.
65. Stenberg, P.E., McDonald, T.P. and Jackson, C.W. (1995) Disruption of microtubules in vivo by vincristine induces large membrane complexes and other cytoplasmic abnormalities in megakaryocytes and platelets of normal rats like those in human and Wistar Furth rat hereditary macrothrombocytopenias. J. Cell. Physiol. 162, 86-102.
66. Ihzumi, T., Hattori, A., Sanada, M. and Muto, M. (1977) Megakaryocyte and platelet formation: A scanning electron microscope study in mouse spleen. Arch. Histol. Jpn. 40, 305-320.
67. Radley, J.M., Rogerson, J., Ellis, S.L. and Hasthorpe, S. (1991) Megakaryocyte maturation in long-term marrow culture. Exp. Hematol. 19, 1075-1078.
68. Choi, E.S., Nichol, J.L., Hokom, M.M., Hornkohl, A.C. and Hunt, P. (1995) Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional. Blood 85, 402-413.
69. Howell, W.H. and Donahue, D.D. (1937) The production of blood platelets in the lungs. J. Exp. Med. 65, 177-203.
70. Dunois-Lardé, E., Capron, C., Fichelson, S., Bauer, T., Cramer-Bordé, E. and Baruch, D. (2009) Exposure of human megakaryocytes to high shear rates accelerates platelet production. Blood 114, 1875-1883.