Platelet demand modulates the type of intravascular protrusion of megakaryocytes in bone marrow

Thrombosis and Haemostasis

Volumn 112, Issue 4, 2014, Pages 743-756

  Kowata, Shugo ^a   Isogai, Sumio ^a   Murai, Kazunori ^a   Ito, Shigeki ^a   Tohyama, Koujiro ^a   Ema, Masatsugu ^b   Hitomi, Jiro ^a   Ishida, Yoji ^a  

^a IWATE MEDICAL UNIVERSITY   (Japan)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Megakaryocyte; Proplatelet; Thick protrusion; Thrombopoiesis

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GLYCOPROTEIN IB; ANTITHROMBOCYTIC AGENT; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELLULAR PARAMETERS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; INTRAVASCULAR PROTRUSION; MEGAKARYOCYTE; MICROSCOPY; MOUSE; NONHUMAN; PROPLATELET; SCANNING ELECTRON MICROSCOPY; THROMBOCYTE; THROMBOCYTE ADHESION; THROMBOCYTE COUNT; THROMBOCYTE RELEASE REACTION; THROMBOCYTE STRUCTURE; THROMBOCYTOPENIA; THROMBOCYTOPOIESIS; TRANSMISSION ELECTRON MICROSCOPY; TWO PHOTON INTRAVITAL MICROSCOPY; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; CYTOLOGY; ENDOPLASMIC RETICULUM; IMMUNOLOGY; METABOLISM; MICROTUBULE; PHOTON; PHYSIOLOGY; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; BLOOD PLATELETS; BONE MARROW; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULES; PHOTONS; PLATELET AGGREGATION INHIBITORS; PLATELET COUNT; STEM CELLS; THROMBOCYTOPENIA; THROMBOPOIESIS;

EID: 84908541408     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH14-02-0123     Document Type: Article

References (49)

1. Kaushansky K. Determinants of platelet number and regulation of thrombopoiesis. Hematology Am Soc Hematol Educ Program 2009; 147-152.
2. Aster RH. Pooling of platelets in the spleen: role in the pathogenesis of “hypersplenic” thrombocytopenia. J Clin Invest 1966; 45: 645-657.
3. Harker LA, Finch CA. Thrombokinetics in man. J Clin Invest 1969; 48: 963-974.
4. Becker RP, De Bruyn PP. 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 1976; 145: 183-205.
5. Italiano JE Jr, Lecine P, Shivdasani RA, et al. Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes. J Cell Biol 1999; 147: 1299-1312.
6. Thon JN, Montalvo A, Patel-Hett S, et al. Cytoskeletal mechanics of proplatelet maturation and platelet release. J Cell Biol 2010; 191: 861-874.
7. Thon JN, Macleod H, Begonja AJ, et al. Microtubule and cortical forces determine platelet size during vascular platelet production. Nat Commun 2012; 3: 852.
8. Handagama PJ, Feldman BF, Jain NC, et al. Circulating proplatelets: isolation and quantitation in healthy rats and in rats with induced acute blood loss. Am J Vet Res 1987; 48: 962-965.
9. Zucker-Franklin D, Philipp CS. Platelet production in the pulmonary capillary bed: new ultrastructural evidence for an old concept. Am J Pathol 2000; 157: 69-74.
10. Yamada E. The fine structure of the megakaryocyte in the mouse spleen. Acta Anat 1957; 29: 267-290.
11. Behnke O. An electron microscope study of the rat megakaryocyte. II. Some aspects of platelet release and microtubules. J Ultrastruct Res 1969; 26: 111-129.
12. Kosaki G. In vivo platelet production from mature megakaryocytes: does platelet release occur via proplatelets? Int J Hematol 2005; 81: 208-219.
13. Behnke O. Microtubules in disk-shaped blood cells. Int Rev Exp Pathol 1970; 9: 1-92.
14. White JG, Rao GH. Microtubule coils versus the surface membrane cytoskeleton in maintenance and restoration of platelet discoid shape. Am J Pathol 1998; 152: 597-609.
15. Radley JM, Scurfield G. The mechanism of platelet release. Blood 1980; 56: 996-999.
16. Muto M. A scanning and transmission electron microscopic study on rat bone marrow sinuses and transmural migration of blood cells. Arch Histol Jpn 1976; 39: 51-66.
17. Richardson JL, Shivdasani RA, Boers C, et al. Mechanisms of organelle transport and capture along proplatelets during platelet production. Blood 2005; 106: 4066-4075.
18. Patel SR, Richardson JL, Schulze H, et al. Differential roles of microtubule assembly and sliding in proplatelet formation by megakaryocytes. Blood 2005; 106: 4076-4085.
19. Radley JM, Haller CJ. The demarcation membrane system of the megakaryocyte: a misnomer? Blood 1982; 60: 213-219.
20. Schulze H, Korpal M, Hurov J, et al. Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood 2006; 107: 3868-3875.
21. Junt T, Schulze H, Chen Z, et al. Dynamic visualization of thrombopoiesis within bone marrow. Science 2007; 317: 1767-1770.
22. Wright JH. Die Entstehung der Blutplättchen. Virchows Arch 1906; 186: 55-63.
23. Breton-Gorius J, Reyes F. Ultrastructure of human bone marrow cell maturation. Int Rev Cytol 1976; 46: 251-321.
24. Lichtman MA, Chamberlain JK, Simon W, et al. The parasinusoidal location of megakaryocytes in marrow: a determinant of platelet release and a physiologic version of vascular invasion and metastasis. Trans Assoc Am Physicians 1977; 90: 313-323.
25. Okabe M, Ikawa M, Kominami K, et al. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 1997; 407: 313-319.
26. Ema M, Takahashi S, Rossant J. Deletion of the selection cassette, but not cisacting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors. Blood 2006; 107: 111-117.
27. Lo Celso C, Lin CP, Scadden DT. In vivo imaging of transplanted hematopoietic stem and progenitor cells in mouse calvarium bone marrow. Nat Protoc 2011; 6: 1-14.
28. Isogai S, Horiguchi M, Hitomi J. The para-aortic ridge plays a key role in the formation of the renal, adrenal and gonadal vascular systems. J Anat 2010; 216: 656-670.
29. Takaku T, Malide D, Young NS, et al. Hematopoiesis in 3 dimensions: human and murine bone marrow architecture visualized by confocal microscopy. Blood 2010; 116: 41-45.
30. Levin J, Levin FC, Metcalf D. The effects of acute thrombocytopenia on megakaryocyte-CFC and granulocyte-macrophage-CFC in mice: studies of bone marrow and spleen. Blood 1980; 56: 274-283.
31. Kienast J, Schmitz G. Flow cytometric analysis of thiazole orange uptake by platelets: a diagnostic aid in the evaluation of thrombocytopenic disorders. Blood 1990; 75: 116-121.
32. Zucker-Franklin D. Megakaryocyte and platelet structure in thrombocytopoiesis: the effect of cytokines. Stem Cells 1996; 14 (Suppl 1): 1-17.
33. White JG, Krumwiede MD, Escolar G. Glycoprotein Ib is homogeneously distributed on external and internal membranes of resting platelets. Am J Pathol 1999; 155: 2127-2134.
34. Strassel C, Eckly A, Léon C, et al. Intrinsic impaired proplatelet formation and microtubule coil assembly of megakaryocytes in a mouse model of Bernard-Soulier syndrome. Haematologica 2009; 94: 800-810.
35. White JG. Platelet structure. In: Platelets. 3rd ed. Oxford, Elsevier 2013; pp. 117-144.
36. Leader A, Pereg D, Lishner M. Are platelet volume indices of clinical use? A multidisciplinary review. Ann Med 2012; 44: 805-816.
37. Tong M, Seth P, Penington DG. Proplatelets and stress platelets. Blood 1987; 69: 522-528.
38. Radley JM, Hartshorn MA. Megakaryocyte fragments and the microtubule coil. Blood Cells 1987; 12: 603-614.
39. Ascoff L. Ueber capillare embolie von riesenkernhaltigen zellen. Arch Pathol Anat Phys 1893; 134: 11-14.
40. Levine RF, Eldor A, Shoff PK, et al. Circulating megakaryocytes: delivery of large numbers of intact, mature megakaryocytes to the lungs. Eur J Haematol 1993; 51: 233-246.
41. Zhang L, Orban M, Lorenz M, et al. A novel role of sphingosine 1-phosphate receptor S1pr1 in mouse thrombopoiesis. J Exp Med 2012; 209: 2165-2181.
42. Behnke O, Forer A. From megakaryocytes to platelets: platelet morphogenesis takes place in the bloodstream. Eur J Haematol 1998; 61: 3-23.
43. Weyrich AS, Zimmerman GA. Platelets in lung biology. Annu Rev Physiol 2013; 75: 569-591.
44. Kuter DJ, Bussel JB, Lyons RM, et al. Efficacy of romiplostim in patients with chronic immune thrombocytopenic purpura: a double-blind randomised controlled trial. Lancet 2008; 371: 395-403.
45. Emmons RV, Reid DM, Cohen RL, et al. Human thrombopoietin levels are high when thrombocytopenia is due to megakaryocyte deficiency and low when due to increased platelet destruction. Blood 1996; 87: 4068-4071.
46. Nagasawa T, Hasegawa Y, Shimizu S, et al. Serum thrombopoietin level is mainly regulated by megakaryocyte mass rather than platelet mass in human subjects. Br J Haematol 1998; 101: 242-244.
47. Ito T, Ishida Y, Kashiwagi R, et al. Recombinant human c-Mpl ligand is not a direct stimulator of proplatelet formation in mature human megakaryocytes. Br J Haematol 1996; 94: 387-390.
48. Ishida Y, Ito T, Kuriya S. Effects of c-mpl ligand on cytoplasmic maturation of murine megakaryocytes and on platelet production. J Histochem Cytochem 1998; 46: 49-57.
49. Chang Y, Auradé F, Larbret F, et al. Proplatelet formation is regulated by the Rho/ROCK pathway. Blood 2007; 109: 4229-4236.