Structural analysis of resting mouse platelets by 3D-EM reveals an unexpected variation in α-granule shape

References

• White JG. Electron microscopic studies of platelet secretion. Prog Hemost Thromb 1974;2:49–98.
   PubMedGoogle Scholar
• White JG. Current concepts of platelet structure. Am J Clin Pathol 1979;71:363–378.
   PubMed Web of Science ®Google Scholar
• King SM, Reed GL. Development of platelet secretory granules. Semin Cell Dev Biol 2002;13:293–302.
   PubMed Web of Science ®Google Scholar
• Yadav S, Storrie B. The cellular basis of platelet secretion: emerging structure/function relationships. Platelets 2017;28:108–118.
   PubMed Web of Science ®Google Scholar
• Pokrovskaya ID, Yadav S, Rao A, McBride E, Kamykowski JA, Zhang G, et al. 3D ultrastructural analysis of α-granule, dense granule, mitochondria and canalicular system arrangement in resting human platelets. Res Practice Thromb Haemost 2020; 4:472–485.
   Web of Science ®Google Scholar
• Pokrovskaya ID, Joshi S, Tobin M, Desai R, Aronova MA, Kamykowski JA, et al.. SNARE-dependent membrane fusion initiates α-granule matrix decondensation in mouse platelets. Blood Adv 2018;2(21):2947–2958.
   PubMed Web of Science ®Google Scholar
• Jonnalagadda D, Izu LT, Whiteheart SW. Platelet secretion is kinetically heterogeneous in an agonist-responsive manner. Blood 2012;184:5209–5218.
   Web of Science ®Google Scholar
• Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discovery 2007;6:273–286.
   PubMed Web of Science ®Google Scholar
• Sehgal S, Storrie B. Evidence that differential packaging of the major platelet granule protein von Willebrand factor and fibrinogen can support differential release. J Thromb Haemos 2007;5:2009–2016.
   PubMed Web of Science ®Google Scholar
• Italiano JE Jr, Richardson JL, Patel-Hett S,Battinelli E, Zaslavsky A, Short S, et al. Angiogenesis is regulated by a novel mechanism: pro-and antiangiogenic proteins are organized into separate platelet alpha-granules and differentially released. Blood 2008; 111:1227–1233.
   PubMed Web of Science ®Google Scholar
• Kamykowski J, Carlton P, Sehgal S, Storrie B. Quantitative immunofluorescence mapping reveals little functional co-clustering of proteins within platelet α-granules. Blood 2011;118:1370–1373.
   PubMed Web of Science ®Google Scholar
• Battinelli EM, Thon JN, Okazaki R, Peters CG, Vijey P, Wilkie AR, et al.. Megakaryotes package contents into separate α-granules that are differentially distributed in platelets. Blood Adv 2019; 3:3092–3098.
   PubMed Web of Science ®Google Scholar
• Wang R, Stone RL, Jason TJ,  Rochat RH, Nick AM, Vinod Vijayan K. Electron cryotomography reveals ultrastructural alterations in platelets from patients with ovarian cancer. Proc Natl Acad Sci USA 2015; 112:14266–14273.
   PubMed Web of Science ®Google Scholar
• Pokrovskaya ID, Aronova MA, Kamykowski JA,  Prince AA, Hoyne JD, Calco GN, et al. STEM tomography reveals that the canalicular system and α-granules remain separate compartments during early secretion stages in blood platelets. J Thromb Haemost 2016; 14:572–584.
   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;120(26):2538–2549.
   Web of Science ®Google Scholar
• Yadav S, Williamson JK, Aronova MA, Prince AA, Pokrovskaya ID, Leapman RD, Storrie B. Golgi proteins in circulating human platelets are distributed across non-stacked, scattered structures. Platelets 2017;28:400–408.
   PubMed Web of Science ®Google Scholar
• McBride EL, Rao A, Zhang G, Hoyne JD, Calco GN, Kuo BC, et al. Comparison of 3D cellular imaging techniques based on scanned electron probes: serial block face SEM vs. axial bright-field STEM tomography. J Struct Biol 2018; 202:216–228.
   PubMed Web of Science ®Google Scholar
• Joshi S, Banerjee M, Zhang J, Kesaraju A, Pokrovskaya ID, Storrie B, Whiteheart SW. Alterations in platelet secretion differentially affect thrombosis and hemostasis. Blood Adv 2018;2(17):2187–2198.
   PubMed Web of Science ®Google Scholar
• Pokrovskaya ID, Tobin M, Desai R, Joshi S, Kamykowski JA, Zhang G. et al. Canalicular system reorganization during mouse platelet activation as revealed by 3D ultrastructural analysis. Platelets 2020 Jan; 31: 1–8. doi: https://doi.org/10.1080/09537104.2020.1719993. [ Epub ahead of print].
   PubMed Web of Science ®Google Scholar
• Schmitt A, Guichard J, Mass JM, Debili N, Cramer EM. Of mice and men: comparisonof the ultrastructure of megakaryocytes and platelets. Exp Hematol 2001;29:1295–1302.
   PubMed Web of Science ®Google Scholar
• White JG. An overview of platelet structural physiology. Scanning Microsc 1987;1:1677–1700.
   PubMedGoogle Scholar
• van Nispen Tot Pannerden H, de Haas F, Gerts W,  Posthuma G, van Dijk, Heijnen H for HFGFG. The platelet interior revisited: electron tomography reveals tubular alpha-granule subtypes. Blood 2010; 118:1147–1156.
   Web of Science ®Google Scholar
• Barrios M, Rodr.guez-Acosta A, Gil A, Salazar AM, Taylor P, S.nchez EE, Arocha-Piñango GL, Guerrero B. Comparative hemostatic parameters in BALB/c, C57BL/6 and C3H/He mice. Thromb Res 2009;2:338–343.
   Web of Science ®Google Scholar
• Frojmovic MM, Milton JG. Human platelet size, shape and related functions in health and disease. Physiol Rev 1982;62:185–261.
   PubMed Web of Science ®Google Scholar
• Nunnari J. Mitochondria: in sickness and in health. Cell 2012;148:1145–1159.
   PubMed Web of Science ®Google Scholar
• Labba K, Murley A, Nunnari J. Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol 2014;30:357–391.
   PubMed Web of Science ®Google Scholar