Structure and function of the open canalicular system – the platelet’s specialized internal membrane network

References

• Behnke O. Electron microscopic observations on the membrane systems of the rat blood platelet. Anat Rec 1967;158(2):121–137.
   PubMedGoogle Scholar
• White JG. The transfer of thorium particles from plasma to platelets and platelet granules. Am J Pathol 1968;53(4):567–575.
   PubMed Web of Science ®Google Scholar
• Escolar G, White JG. The platelet open canalicular system: A final common pathway. Blood Cells 1991;17(3):467–485. discussion 86-95.
   PubMedGoogle Scholar
• Escolar G, Leistikow E, White JG. The fate of the open canalicular system in surface and suspension-activated platelets. Blood 1989;74(6):1983–1988.
   PubMed Web of Science ®Google Scholar
• White JG, Krumwiede M. Further studies of the secretory pathway in thrombin-stimulated human platelets. Blood 1987;69(4):1196–1203.
   PubMed Web of Science ®Google Scholar
• Behnke O. 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 1968;24(5):412–433.
   Google Scholar
• Eckly A, Heijnen H, Pertuy F, Geerts W, Proamer F, Rinckel J-Y, et al. Biogenesis of the demarcation membrane system (DMS) in megakaryocytes. Blood 2014;123(6):921–930.
   PubMed Web of Science ®Google Scholar
• Schulze H, Korpal M, Hurov J, Kim SW, Zhang J, Cantley LC, et al. Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood 2006;107(10):3868–3875.
   PubMed Web of Science ®Google Scholar
• Mahaut-Smith MP, Thomas D, Higham AB, Usher-Smith JA, Hussain JF, Martinez-Pinna J, et al. Properties of the demarcation membrane system in living rat megakaryocytes. Biophys J 2003;84(4):2646–2654.
   PubMed Web of Science ®Google Scholar
• Radley JM, Haller CJ. The demarcation membrane system of the megakaryocyte: A misnomer? Blood 1982;60(1):213–219.
   PubMed Web of Science ®Google Scholar
• Junt T, Schulze H, Chen Z, Massberg S, Goerge T, Krueger A, et al. Dynamic visualization of thrombopoiesis within bone marrow. Science 2007;317(5845):1767–1770.
   PubMed Web of Science ®Google Scholar
• Thon JN, Macleod H, Begonja AJ, Zhu J, Lee K-C, Mogilner A, et al. Microtubule and cortical forces determine platelet size during vascular platelet production. Nat Commun 2012;3:852.
   PubMed Web of Science ®Google Scholar
• Patel SR, Richardson JL, Schulze H, Kahle E, Galjart N, Drabek K, et al. Differential roles of microtubule assembly and sliding in proplatelet formation by megakaryocytes. Blood 2005;106(13):4076–4085.
   PubMed Web of Science ®Google Scholar
• Rojnuckarin P, Kaushansky K. Actin reorganization and proplatelet formation in murine megakaryocytes: The role of protein kinase calpha. Blood 2001;97(1):154–161.
   PubMed Web of Science ®Google Scholar
• Choi E, Nichol J, Hokom M, Hornkohl A, Hunt P. Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional. Blood 1995;85(2):402–413.
   PubMed Web of Science ®Google Scholar
• Kosaki G. Platelet production by megakaryocytes: Protoplatelet theory justifies cytoplasmic fragmentation model. Int J Hematol 2008;88(3):255–267.
   PubMed Web of Science ®Google Scholar
• White JG, Krumwiede MD, Escolar G. Glycoprotein Ib is homogeneously distributed on external and internal membranes of resting platelets. Am J Pathol 1999;155(6):2127–2134.
   PubMed Web of Science ®Google Scholar
• Cramer EM, Savidge GF, Vainchenker W, Berndt MC, Pidard D, Caen JP, et al. Alpha-granule pool of glycoprotein IIb-IIIa in normal and pathologic platelets and megakaryocytes. Blood 1990;75(6):1220–1227.
   PubMed Web of Science ®Google Scholar
• van Nispen tot Pannerden H, de Haas F, Geerts W, Posthuma G, van Dijk S, Heijnen HF. The platelet interior revisited: Electron tomography reveals tubular alpha-granule subtypes. Blood 2010;116(7):1147–1156.
   PubMed Web of Science ®Google Scholar
• Mountford JK, Petitjean C, Putra HW, McCafferty JA, Setiabakti NM, Lee H, et al. The class II PI 3-kinase, PI3KC2alpha, links platelet internal membrane structure to shear-dependent adhesive function. Nat Commun 2015;6:6535.
   PubMed Web of Science ®Google Scholar
• White JG. Interaction of membrane systems in blood platelets. Am J Pathol 1972;66(2):295–312.
   PubMed Web of Science ®Google Scholar
• Ebbeling L, Robertson C, McNicol A, Gerrard JM. Rapid ultrastructural changes in the dense tubular system following platelet activation. Blood 1992;80(3):718–723.
   PubMed Web of Science ®Google Scholar
• Zucker-Franklin D, Benson KA, Myers KM. Absence of a surface-connected canalicular system in bovine platelets. Blood 1985;65(1):241–244.
   PubMed Web of Science ®Google Scholar
• Gader AG, Ghumlas AK, Hussain MF, Haidari AA, White JG. The ultrastructure of camel blood platelets: A comparative study with human, bovine, and equine cells. Platelets 2008;19(1):51–58.
   PubMed Web of Science ®Google Scholar
• Segura D, Monreal L, Perez-Pujol S, Pino M, Ordinas A, Brugues R, et al. Assessment of platelet function in horses: Ultrastructure, flow cytometry, and perfusion techniques. J Vet Intern Med 2006;20(3):581–588.
   PubMed Web of Science ®Google Scholar
• Kudo S, Onai H, Ogawa R. Response of blood cells to hemorrahagic shock in the dog. J Anesth 1987;1(1):51–61.
   PubMedGoogle Scholar
• Liu LP, Shan CW, Liu XH, Xiao HC, Yang SQ. Effect of procainamide on ultrastructure of blood platelet in rabbits. Acta Pharmacol 1998;19(4):376–379.
   Google Scholar
• Daimon T, Mizuhira V, Uchida K. Fine structural distribution of the surface-connected canalicular system in frog thrombocytes. Cell Tissue Res 1979;201(3):431–439.
   PubMed Web of Science ®Google Scholar
• Ferguson H. The ultrastructure of plaice (Pleuronectes platessa) leucocytes. J Fish Biol 1976;8(2):139–142.
   Web of Science ®Google Scholar
• Daimon T, Uchida K. Electron microscopic and cytochemical observations on the membrane systems of the chicken thrombocyte. J Anat 1978;125(Pt 1):11–21.
   PubMedGoogle Scholar
• Choi W, Karim ZA, Whiteheart SW. Protein expression in platelets from six species that differ in their open canalicular system. Platelets 2010;21(3):167–175.
   PubMed Web of Science ®Google Scholar
• Harrison P, Wilbourn B, Debili N, Vainchenker W, Breton-Gorius J, Lawrie AS, et al. Uptake of plasma fibrinogen into the alpha granules of human megakaryocytes and platelets. J Clin Investig 1989;84(4):1320–1324.
   PubMed Web of Science ®Google Scholar
• Escolar G, Lopez-Vilchez I, Diaz-Ricart M, White JG, Galan AM. Internalization of tissue factor by platelets. Thromb Res 2008;122(Suppl 1):S37–41.
   PubMedGoogle Scholar
• Fogelson AL, Wang NT. Platelet dense-granule centralization and the persistence of ADP secretion. Am J Physiol 1996;270(3 Pt 2):H1131–40.
   PubMed Web of Science ®Google Scholar
• Feng D, Crane K, Rozenvayn N, Dvorak AM, Flaumenhaft R. Subcellular distribution of 3 functional platelet SNARE proteins: Human cellubrevin, SNAP-23, and syntaxin 2. Blood 2002;99(11):4006.
   PubMed Web of Science ®Google Scholar
• Flaumenhaft R. Molecular basis of platelet granule secretion. Arterioscler Thromb Vasc Biol 2003;23(7):1152–1160.
   PubMed Web of Science ®Google Scholar
• Flaumenhaft R, Croce K, Chen E, Furie B, Furie BC. Proteins of the exocytotic core complex mediate platelet alpha-granule secretion. Roles Vesicle-Associated Membrane Protein, SNAP-23, Syntaxin 4 J Biol Chem 1999;274(4):2492–2501.
   Google Scholar
• Polgár J, Chung S-H, Reed GL. Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood 2002;100(3):1081.
   PubMed Web of Science ®Google Scholar
• White JG, Escolar G. The blood platelet open canalicular system: A two-way street. Eur J Cell Biol 1991;56(2):233–242.
   PubMed Web of Science ®Google Scholar
• White JG. The secretory pathway of bovine platelets. Blood 1987;69(3):878–885.
   PubMed Web of Science ®Google Scholar
• Sage SO, Pugh N, Farndale RW, Harper AG. Pericellular Ca(2+) recycling potentiates thrombin-evoked Ca(2+) signals in human platelets. Physiol Rep 2013;1(5):e00085.
   PubMedGoogle Scholar
• Hourdille P, Heilmann E, Combrie R, Winckler J, Clemetson KJ, Nurden AT. Thrombin induces a rapid redistribution of glycoprotein Ib-IX complexes within the membrane systems of activated human platelets. Blood 1990;76(8):1503–1513.
   PubMed Web of Science ®Google Scholar
• Hartwig JH. The platelet: Form and function. Semin Hematol 2006;43(1 Suppl 1):S94–100.
   PubMed Web of Science ®Google Scholar
• Blair P, Platelet FR. α-granules: Basic biology and clinical correlates. Blood Rev 2009;23(4):177–189.
   PubMed Web of Science ®Google Scholar
• Grouse LH, Rao GH, Weiss DJ, Perman V, White JG. Surface-activated bovine platelets do not spread, they unfold. Am J Pathol 1990;136(2):399–408.
   PubMed Web of Science ®Google Scholar
• Maldonado JE, Gilchrist GS, Brigden LP, Bowie EJ. Ultrastructure of platelets in Bernard-Soulier syndrome. Mayo Clin Proc 1975;50(7):402–406.
   PubMed Web of Science ®Google Scholar
• Savoia A, Kunishima S, de Rocco D, Zieger B, Rand ML, Pujol-Moix N, et al. Spectrum of the mutations in Bernard-Soulier syndrome. Hum Mutat 2014;35(9):1033–1045.
   PubMed Web of Science ®Google Scholar
• Jantunen E. Inherited giant platelet disorders. Eur J Haematol 1994;53(4):191–196.
   PubMed Web of Science ®Google Scholar
• White JG. Giant platelet disorders. Haematologica 2002;87:85–92.
   Google Scholar
• Ludwig J, Hashimoto E, McGill DB, Van Heerden JA. Classification of hepatic venous outflow obstruction: ambiguous terminology of the Budd-Chiari syndrome. Mayo Clin Proc 1990;65(1):51–55.
   PubMed Web of Science ®Google Scholar
• Dayal S, Pati HP, Pande GK, Sharma P, Saraya AK. Platelet ultra-structure study in Budd-Chiari syndrome. Eur J Haematol 1995;55(5):294–301.
   PubMed Web of Science ®Google Scholar
• White JG, Keel S, Reyes M, Burris SM. Alpha–delta platelet storage pool deficiency in three generations. Platelets 2007;18(1):1–10.
   PubMed Web of Science ®Google Scholar
• Grgurevich S, Krishnan R, White MM, Jennings LK. Role of in vitro cholesterol depletion in mediating human platelet aggregation. J Thromb Haemost 2003;1(3):576–586.
   PubMed Web of Science ®Google Scholar
• Osman S, Taylor KA, Allcock N, Rainbow RD, Mahaut-Smith MP. Detachment of surface membrane invagination systems by cationic amphiphilic drugs. Sci Rep 2016;6:18536.
   PubMed Web of Science ®Google Scholar
• Valet C, Chicanne G, Severac C, Chaussade C, Whitehead MA, Cabou C, et al. Essential role of class II PI3K-C2alpha in platelet membrane morphology. Blood 2015;126(9):1128–1137.
   PubMed Web of Science ®Google Scholar
• Eckly A, Rinckel JY, Proamer F, Ulas N, Joshi S, Whiteheart SW, et al. Respective contributions of single and compound granule fusion to secretion by activated platelets. Blood 2016;128(21):2538–2549.
   PubMed Web of Science ®Google Scholar
• Merchan-Perez A, Rodriguez JR, Alonso-Nanclares L, Schertel A, Counting Synapses DJ. Using FIB/SEM microscopy: A true revolution for ultrastructural volume reconstruction. Front Neuroanat 2009;3:18.
   PubMed Web of Science ®Google Scholar
• Bennett AE, Narayan K, Shi D, Hartnell LM, Gousset K, He H, et al. Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages. PLoS Pathog 2009;5(9):e1000591.
   PubMed Web of Science ®Google Scholar