Developmental differences of in vitro cultured murine bone marrow- and fetal liver-derived megakaryocytes

References

• Noetzli LJ, French SL, Machlus KR. New insights into the differentiation of megakaryocytes from hematopoietic progenitors. Arterioscler Thromb Vasc Biol 2019;39(7):1288–1300. 10.1161/ATVBAHA.119.312129.
   PubMed Web of Science ®Google Scholar
• Notta F, Zandi S, Takayama N, Dobson S, Gan OI, Wilson G, Kaufmann KB, McLeod J, Laurenti E, Dunant CF, et al. Distinct routes of lineage development reshape the human blood hierarchy across ontogeny. Science 2016;351(6269):aab2116. 10.1126/science.aab2116.
   PubMed Web of Science ®Google Scholar
• de Sauvage FJ, Hass PE, Spencer SD, Malloy BE, Gurney AL, Spencer SA, Darbonne WC, Henzel WJ, Wong SC, Kuang W-J, et al. Stimulation of megakaryocytopoiesis and thrombopoiesis by the c-Mpl ligand. Nature 1994;369(6481):533–538. 10.1038/369533a0.
   PubMed Web of Science ®Google Scholar
• Kaushansky K, Lok S, Holly RD, Broudy VC, Lin N, Bailey MC, Forstrom JW, Buddle MM, Oort PJ, Hagen FS Promotion of megakaryocyte progenitor expansion and differentiation by the c-Mpl ligand thrombopoietin. Nature 1994;369(6481):568–571. 10.1038/369568a0.
   PubMed Web of Science ®Google Scholar
• van Den Oudenrijn S, Von Dem Borne AE, de Haas M. Differences in megakaryocyte expansion potential between CD34(+) stem cells derived from cord blood, peripheral blood, and bone marrow from adults and children. Exp Hematol 2000;28(9):1054–1061. 10.1016/S0301-472X(00)00517-8.
   PubMed Web of Science ®Google Scholar
• Schipper LF, Brand A, Reniers N, Melief CJJ, Willemze R, Fibbe WE. Differential maturation of megakaryocyte progenitor cells from cord blood and mobilized peripheral blood. Exp Hematol 2003;31(4):324–330. 10.1016/S0301-472X(03)00004-3.
   PubMed Web of Science ®Google Scholar
• Mattia G, Vulcano F, Milazzo L, Barca A, Macioce G, Giampaolo A, Hassan HJ . Different ploidy levels of megakaryocytes generated from peripheral or cord blood CD34+ cells are correlated with different levels of platelet release. Blood 2002;99(3):888–897. 10.1182/blood.V99.3.888.
   PubMed Web of Science ®Google Scholar
• De Bruyn C, Delforge A, Martiat P, Bron D. Ex vivo expansion of megakaryocyte progenitor cells: cord blood versus mobilized peripheral blood. Stem Cells Dev 2005;14(4):415–424. 10.1089/scd.2005.14.415.
   PubMed Web of Science ®Google Scholar
• Miyazaki R, Ogata H, Iguchi T, Sogo S, Kushida T, Ito T, Inaba M, Ikehara S, Kobayashi Y. Comparative analyses of megakaryocytes derived from cord blood and bone marrow. Br J Haematol 2000;108(3):602–609. 10.1046/j.1365-2141.2000.01854.x.
   PubMed Web of Science ®Google Scholar
• Vijey P, Posorske B, Machlus KR. In vitro culture of murine megakaryocytes from fetal liver-derived hematopoietic stem cells. Platelets 2018;29(6):583–588. 10.1080/09537104.2018.1492107.
   PubMed Web of Science ®Google Scholar
• Schulze H. Culture of murine megakaryocytes and platelets from fetal liver and bone marrow. Methods Mol Biol 2012;788:193–203.
   PubMedGoogle Scholar
• Begonja AJ, Pluthero FG, Suphamungmee W, Giannini S, Christensen H, Leung R, Lo RW, Nakamura F, Lehman W, Plomann M, et al. FlnA binding to PACSIN2 F-BAR domain regulates membrane tubulation in megakaryocytes and platelets. Blood 2015;126(1):80–88. 10.1182/blood-2014-07-587600.
   PubMed Web of Science ®Google Scholar
• Jurak Begonja A, Hoffmeister KM, Hartwig JH, Falet H. FlnA-null megakaryocytes prematurely release large and fragile platelets that circulate poorly. Blood 2011;118(8):2285–2295. 10.1182/blood-2011-04-348482.
   PubMed Web of Science ®Google Scholar
• Thon JN, Devine MT, Begonja AJ, Tibbitts J, Italiano JE. High-content live-cell imaging assay used to establish mechanism of trastuzumab emtansine (T-DM1)-mediated inhibition of platelet production. Blood 2012;120(10):1975–1984. 10.1182/blood-2012-04-420968.
   PubMed Web of Science ®Google Scholar
• Begonja AJ, Gambaryan S, Schulze H, Patel-Hett S, Italiano JE Jr., Hartwig JH, Walter U . Differential roles of cAMP and cGMP in megakaryocyte maturation and platelet biogenesis. Exp Hematol 2013;41(1):91–101 e4. 10.1016/j.exphem.2012.09.001.
   PubMed Web of Science ®Google Scholar
• Bertovic I, Kurelic R, Milosevic I, Bender M, Krauss M, Haucke V, Jurak Begonja A . Vps34 derived phosphatidylinositol 3-monophosphate modulates megakaryocyte maturation and proplatelet production through late endosomes/lysosomes. J Thromb Haemost 2020;18(7):1756–1772. 10.1111/jth.14764.
   PubMed Web of Science ®Google Scholar
• Slayton WB, Wainman DA, Li XM, Hu Z, Jotwani A, Cogle CR, Walker D, Fisher RC, Wingard JR, Scott EW, et al. Developmental differences in megakaryocyte maturation are determined by the microenvironment. Stem Cells 2005;23(9):1400–1408. 10.1634/stemcells.2004-0373.
   PubMed Web of Science ®Google Scholar
• Palazzo A, Bluteau O, Messaoudi K, Marangoni F, Chang Y, Souquere S, Pierron G, Lapierre V, Zheng Y, Vainchenker W, et al. The cell division control protein 42-Src family kinase-neural Wiskott-Aldrich syndrome protein pathway regulates human proplatelet formation. J Thromb Haemost 2016;14(12):2524–2535. 10.1111/jth.13519.
   PubMed Web of Science ®Google Scholar
• Elagib KE, Lu C-H, Mosoyan G, Khalil S, Zasadzinska E, Foltz DR, Balogh P, Gru AA, Fuchs DA, Rimsza LM, et al. Neonatal expression of RNA-binding protein IGF2BP3 regulates the human fetal-adult megakaryocyte transition. J Clin Invest 2017;127(6):2365–2377. 10.1172/JCI88936.
   PubMed Web of Science ®Google Scholar
• Mazharian A, Watson SP, Severin S. Critical role for ERK1/2 in bone marrow and fetal liver–derived primary megakaryocyte differentiation, motility, and proplatelet formation. Exp Hematol 2009;37(10):1238–49 e5. 10.1016/j.exphem.2009.07.006.
   PubMed Web of Science ®Google Scholar
• Strassel C, Eckly A, Leon C, Moog S, Cazenave J-P, Gachet C, Lanza F . Hirudin and heparin enable efficient megakaryocyte differentiation of mouse bone marrow progenitors. Exp Cell Res 2012;318(1):25–32. 10.1016/j.yexcr.2011.10.003.
   PubMed Web of Science ®Google Scholar
• Mikkola HKA, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH. Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 2003;101(2):508–516. 10.1182/blood-2002-06-1699.
   PubMed Web of Science ®Google Scholar
• Gekas C, Graf T. CD41 expression marks myeloid-biased adult hematopoietic stem cells and increases with age. Blood 2013;121(22):4463–4472. 10.1182/blood-2012-09-457929.
   PubMed Web of Science ®Google Scholar
• Lepage A, Leboeuf M, Cazenave J-P, de La Salle C, Lanza F, Uzan G. The αIIbβ3 integrin and GPIb-V-IX complex identify distinct stages in the maturation of CD34+cord blood cells to megakaryocytes. Blood 2000;96(13):4169–4177. 10.1182/blood.V96.13.4169.
   PubMed Web of Science ®Google Scholar
• Ghalloussi D, Dhenge A, Bergmeier W. New insights into cytoskeletal remodeling during platelet production. J Thromb Haemost 2019;17(9):1430–1439. 10.1111/jth.14544.
   PubMed Web of Science ®Google Scholar
• Tomer A. Human marrow megakaryocyte differentiation: multiparameter correlative analysis identifies von Willebrand factor as a sensitive and distinctive marker for early (2N and 4N) megakaryocytes. Blood 2004;104(9):2722–2727. 10.1182/blood-2004-02-0769.
   PubMed Web of Science ®Google Scholar
• Eckly A, Heijnen H, Pertuy F, Geerts W, Proamer F, Rinckel J-Y, Léon C, Lanza F, Gachet C . Biogenesis of the demarcation membrane system (DMS) in megakaryocytes. Blood 2014;123(6):921–930. 10.1182/blood-2013-03-492330.
   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(5–6):412–433. 10.1016/S0022-5320(68)80046-2.
   PubMedGoogle Scholar
• MacPherson GG. Development of megakaryocytes in bone marrow of the rat: an analysis by electron microscopy and high resolution autoradiography. Proc R Soc Lond B Biol Sci 1971;177(1047):265–274.
   PubMed Web of Science ®Google Scholar
• Bentfeld-Barker ME, Bainton DF. Ultrastructure of rat megakaryocytes after prolonged thrombocytopenia. J Ultrastruct Res 1977;61(2):201–214. 10.1016/S0022-5320(77)80087-7.
   PubMedGoogle Scholar
• Antkowiak A, Viaud J, Severin S, Zanoun M, Ceccato L, Chicanne G, Strassel C, Eckly A, Leon C, Gachet C, et al. Cdc42-dependent F-actin dynamics drive structuration of the demarcation membrane system in megakaryocytes. J Thromb Haemost 2016;14(6):1268–1284. 10.1111/jth.13318.
   PubMed Web of Science ®Google Scholar
• Woo AJ, Wieland K, Huang H, Akie TE, Piers T, Kim J, Cantor AB . Developmental differences in IFN signaling affect GATA1s-induced megakaryocyte hyperproliferation. J Clin Invest 2013;123(8):3292–3304. 10.1172/JCI40609.
   PubMed Web of Science ®Google Scholar
• Merico V, Zuccotti M, Carpi D, Baev D, Mulas F, Sacchi L, Bellazzi R, Pastorelli R, Redi CA, Moratti R . The genomic and proteomic blueprint of mouse megakaryocytes derived from embryonic stem cells. J Thromb Haemost 2012;10(5):907–915. 10.1111/j.1538-7836.2012.04673.x.
   PubMed Web of Science ®Google Scholar
• Elagib KE, Brock AT, Goldfarb AN. Megakaryocyte ontogeny: clinical and molecular significance. Exp Hematol 2018;61:1–9. 10.1016/j.exphem.2018.02.003.
   PubMed Web of Science ®Google Scholar
• Six KR, Sicot G, Devloo R, Feys HB, Baruch D, Compernolle V. A comparison of haematopoietic stem cells from umbilical cord blood and peripheral blood for platelet production in a microfluidic device. Vox Sang 2019;114(4):330–339. 10.1111/vox.12776.
   PubMed Web of Science ®Google Scholar
• Potts KS, Sargeant TJ, Markham JF, Shi W, Biben C, Josefsson EC, Whitehead LW, Rogers KL, Liakhovitskaia A, Smyth GK, et al. A lineage of diploid platelet-forming cells precedes polyploid megakaryocyte formation in the mouse embryo. Blood 2014;124(17):2725–2729. 10.1182/blood-2014-02-559468.
   PubMed Web of Science ®Google Scholar
• Potts KS, Farley A, Dawson CA, Rimes J, Biben C, de Graaf C, Potts MA, Stonehouse OJ, Carmagnac A, Gangatirkar P, et al. Membrane budding is a major mechanism of in vivo platelet biogenesis. J Exp Med 2020;217(9). 10.1084/jem.20191206.
   PubMed Web of Science ®Google Scholar
• Couban S, Simpson DR, Barnett MJ, Bredeson C, Hubesch L, Howson-Jan K, Shore TB, Walker IR, Browett P, Messner HA . A randomized multicenter comparison of bone marrow and peripheral blood in recipients of matched sibling allogeneic transplants for myeloid malignancies. Blood 2002;100(5):1525–1531. 10.1182/blood-2002-01-0048.
   PubMed Web of Science ®Google Scholar
• Sanz GF, Saavedra S, Planelles D, Senent L, Cervera J, Barragan E, Jiménez C, Larrea L, Martín G, Martínez J . Standardized, unrelated donor cord blood transplantation in adults with hematologic malignancies. Blood 2001;98(8):2332–2338. 10.1182/blood.V98.8.2332.
   PubMed Web of Science ®Google Scholar
• Liu ZJ, Italiano J Jr., Ferrer-Marin F, Gutti R, Bailey M, Poterjoy B, Rimsza L, Sola-Visner M . Developmental differences in megakaryocytopoiesis are associated with up-regulated TPO signaling through mTOR and elevated GATA-1 levels in neonatal megakaryocytes. Blood 2011;117(15):4106–4117. 10.1182/blood-2010-07-293092.
   PubMed Web of Science ®Google Scholar
• Schwer HD, Lecine P, Tiwari S, Italiano JE Jr., Hartwig JH, Shivdasani RA. A lineage-restricted and divergent beta-tubulin isoform is essential for the biogenesis, structure and function of blood platelets. Curr Biol 2001;11(8):579–586. 10.1016/S0960-9822(01)00153-1.
   PubMed Web of Science ®Google Scholar
• Alexander WS, Roberts AW, Nicola NA, Li R, Metcalf D. Deficiencies in progenitor cells of multiple hematopoietic lineages and defective megakaryocytopoiesis in mice lacking the thrombopoietic receptor c-Mpl. Blood 1996;87(6):2162–2170. 10.1182/blood.V87.6.2162.bloodjournal8762162.
   PubMed Web of Science ®Google Scholar
• Qian H, Buza-Vidas N, Hyland CD, Jensen CT, Antonchuk J, Mansson R, Thoren LA, Ekblom M, Alexander WS, Jacobsen SEW . Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 2007;1(6):671–684. 10.1016/j.stem.2007.10.008.
   PubMed Web of Science ®Google Scholar
• Sparger KA, Ramsey H, Lorenz V, Liu ZJ, Feldman HA, Li N, Laforest T, Sola-Visner MC . Developmental differences between newborn and adult mice in response to romiplostim. Platelets 2018;29(4):365–372. 10.1080/09537104.2017.1316481.
   PubMed Web of Science ®Google Scholar
• Hu Z, Slayton WB, Rimsza LM, Bailey M, Sallmon H, Sola-Visner MC. Differences between newborn and adult mice in their response to immune thrombocytopenia. Neonatology 2010;98(1):100–108. 10.1159/000280413.
   PubMed Web of Science ®Google Scholar
• Kuwaki T, Hagiwara T, Yuki C, Kodama I, Kato T, Miyazaki H. Quantitative analysis of thrombopoietin receptors on human megakaryocytes. FEBS Lett 1998;427(1):46–50. 10.1016/S0014-5793(98)00391-3.
   PubMed Web of Science ®Google Scholar
• Aguilar A, Pertuy F, Eckly A, Strassel C, Collin D, Gachet C, Lanza F, Léon C . Importance of environmental stiffness for megakaryocyte differentiation and proplatelet formation. Blood 2016;128(16):2022–2032. 10.1182/blood-2016-02-699959.
   PubMed Web of Science ®Google Scholar
• Heib T, Gross C, Muller ML, Stegner D, Pleines I. Isolation of murine bone marrow by centrifugation or flushing for the analysis of hematopoietic cells - a comparative study. Platelets 2021;32(5):601–607. 10.1080/09537104.2020.1797323.
   PubMed Web of Science ®Google Scholar
• Kahr WH, Lo RW, Li L, Pluthero FG, Christensen H, Ni R, Vaezzadeh N, Hawkins CE, Weyrich AS, Di Paola J . Abnormal megakaryocyte development and platelet function in Nbeal2(-/-) mice. Blood 2013;122(19):3349–3358. 10.1182/blood-2013-04-499491.
   PubMed Web of Science ®Google Scholar
• Fidler TP, Campbell RA, Funari T, Dunne N, Balderas Angeles E, Middleton EA, Chaudhuri D, Weyrich AS, Abel ED . Deletion of GLUT1 and GLUT3 reveals multiple roles for glucose metabolism in platelet and megakaryocyte function. Cell Rep 2017;21(6):1705. 10.1016/j.celrep.2017.10.086.
   PubMed Web of Science ®Google Scholar
• van Dijk J, Bompard G, Cau J, Kunishima S, Rabeharivelo G, Mateos-Langerak J, Cazevieille C, Cavelier P, Boizet-Bonhoure B, Delsert C, et al. Microtubule polyglutamylation and acetylation drive microtubule dynamics critical for platelet formation. BMC Biol 2018;16(1):116. 10.1186/s12915-018-0584-6.
   PubMed Web of Science ®Google Scholar
• Khan AO, Slater A, Maclachlan A, Nicolson PLR, Pike JA, Reyat JS, Yule J, Stapley R, Rayes J, Thomas SG . Post-translational polymodification of beta1-tubulin regulates motor protein localisation in platelet production and function. Haematologica 2020; Online ahead of print. 10.3324/haematol.2020.270793.
   Web of Science ®Google Scholar
• Bornert A, Boscher J, Pertuy F, Eckly A, Stegner D, Strassel C, Gachet C, Lanza F, Léon C . Cytoskeletal-based mechanisms differently regulate in vivo and in vitro proplatelet formation. Haematologica 2020;106(5):1368–1380. 10.3324/haematol.2019.239111.
   Web of Science ®Google Scholar