Developments in the production of platelets from stem cells (Review)
- Authors:
- Jie Yang
- Jianfeng Luan
- Yanfei Shen
- Baoan Chen
-
Affiliations: Department of Hematology and Oncology, School of Medicine, Zhongda Hospital, Southeast University, Nanjing, Jiangsu 210009, P.R. China, Jinling Hospital Department of Blood Transfusion, School of Medicine, Nanjing University, Nanjing, Jiangsu 210002, P.R. China, Medical School, School of Chemistry and Chemical Engineering, Southeast University, Nanjing, Jiangsu 210009, P.R. China - Published online on: November 3, 2020 https://doi.org/10.3892/mmr.2020.11645
- Article Number: 7
-
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Wang B and Zheng J: Platelet generation in vivo and in vitro. Springerplus. 5:7872016. View Article : Google Scholar : PubMed/NCBI | |
Lu SJ, Li F, Yin H, Feng Q, Kimbrel EA, Hahm E, Thon JN, Wang W, Italiano JE, Cho J and Lanza R: Platelets generated from human embryonic stem cells are functional in vitro and in the microcirculation of living mice. Cell Res. 21:530–545. 2011. View Article : Google Scholar : PubMed/NCBI | |
Golebiewska EM and Poole AW: Platelet secretion: From haemostasis to wound healing and beyond. Blood Rev. 29:153–162. 2015. View Article : Google Scholar : PubMed/NCBI | |
Franco AT, Corken A and Ware J: Platelets at the interface of thrombosis, inflammation, and cancer. Blood. 126:582–588. 2015. View Article : Google Scholar : PubMed/NCBI | |
Nachmias VT and Yoshida KI: The cytoskeleton of the blood platelet: A Dynamic Structure. Advances Mol Cell Biol. 2:181–211. 1988. View Article : Google Scholar | |
Nurhayati RW, Ojima Y and Taya M: Recent developments in ex vivo platelet production. Cytotechnology. 68:2211–2221. 2016. View Article : Google Scholar : PubMed/NCBI | |
Saluk J, Bijak M, Ponczek MB and Wachowicz B: The formation, metabolism and the evolution of blood platelets. Postepy Hig Med Dosw (Online). 68:384–391. 2014.(In Polish). View Article : Google Scholar : PubMed/NCBI | |
Sim X, Poncz M, Gadue P and French DL: Understanding platelet generation from megakaryocytes: Implications for in vitro-derived platelets. Blood. 127:1227–1233. 2016. View Article : Google Scholar : PubMed/NCBI | |
Stasi R: How to approach thrombocytopenia. Hematology Am Soc Hematol Educ Program. 2012:191–197. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gollomp K, Lambert MP and Poncz M: Current status of blood ‘pharming’: Megakaryoctye transfusions as a source of platelets. Curr Opin Hematol. 24:565–571. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ellingson KD, Sapiano MRP, Haass KA, Savinkina AA, Baker ML, Chung KW, Henry RA, Berger JJ, Kuehnert MJ and Basavaraju SV: Continued decline in blood collection and transfusion in the United States-2015. Transfusion. 57 (Suppl 2):S1588–S1598. 2017. View Article : Google Scholar | |
Estcourt LJ: Why has demand for platelet components increased? A review. Transfus Med. 24:260–268. 2014. View Article : Google Scholar : PubMed/NCBI | |
Baigger A, Blasczyk R and Figueiredo C: Towards the manufacture of megakaryocytes and platelets for clinical application. Transfus Med Hemother. 44:165–173. 2017. View Article : Google Scholar : PubMed/NCBI | |
Whitaker B, Rajbhandary S, Kleinman S, Harris A and Kamani N: Trends in United States blood collection and transfusion: Results from the 2013 AABB Blood Collection, Utilization, and patient blood management survey. Transfusion. 56:2173–2183. 2016. View Article : Google Scholar : PubMed/NCBI | |
Thon JN, Medvetz DA, Karlsson SM and Italiano JE Jr: Road blocks in making platelets for transfusion. J Thromb Haemost. 13 (Suppl 1):S55–S62. 2015. View Article : Google Scholar : PubMed/NCBI | |
Reems JA, Pineault N and Sun S: In vitro megakaryocyte production and platelet biogenesis: state of the art. Transfus Med Rev. 24:33–43. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lambert MP, Sullivan SK, Fuentes R, French DL and Poncz M: Challenges and promises for the development of donor-independent platelet transfusions. Blood. 121:3319–3324. 2013. View Article : Google Scholar : PubMed/NCBI | |
Fujiyama S, Hori N, Sato T, Enosawa S, Murata M and Kobayashi E: Development of an ex vivo xenogeneic bone environment producing human platelet-like cells. PLoS One. 15:e02305072020. View Article : Google Scholar : PubMed/NCBI | |
Brand A: Alloimmune platelet refractoriness: Incidence declines, unsolved problems persist. Transfusion. 41:724–726. 2001. View Article : Google Scholar : PubMed/NCBI | |
Avanzi MP and Mitchell WB: Ex vivo production of platelets from stem cells. Br J Haematol. 165:237–247. 2014. View Article : Google Scholar : PubMed/NCBI | |
Sugimoto N and Eto K: Platelet production from induced pluripotent stem cells. J Thromb Haemost. 15:1717–1727. 2017. View Article : Google Scholar : PubMed/NCBI | |
Nakamura-Ishizu A, Matsumura T, Stumpf PS, Umemoto T, Takizawa H, Takihara Y, O'Neil A, Majeed Abba, MacArthur BD and Suda T: Thrombopoietin metabolically primes hematopoietic stem cells to megakaryocyte-lineage differentiation. Cell Rep. 25:1772–1785 e6. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen Z, Wang Z and Gu Z: Bioinspired and biomimetic nanomedicines. Acc Chem Res. 52:1255–1264. 2019.PubMed/NCBI | |
Morishima N and Nakanishi K: Proplatelet formation in megakaryocytes is associated with endoplasmic reticulum stress. Genes Cells. 21:798–806. 2016. View Article : Google Scholar : PubMed/NCBI | |
Borst S, Sim X, Poncz M, French DL and Gadue P: Induced pluripotent stem cell-derived megakaryocytes and platelets for disease modeling and future clinical applications. Arterioscler Thromb Vasc Biol. 37:2007–2013. 2017. View Article : Google Scholar : PubMed/NCBI | |
Smith BW and Murphy GJ: Stem cells, megakaryocytes, and platelets. Curr Opin Hematol. 21:430–437. 2014. View Article : Google Scholar : PubMed/NCBI | |
Pineault N, Robert A, Cortin V and Boyer L: Ex vivo differentiation of cord blood stem cells into megakaryocytes and platelets. Methods Mol Biol. 946:205–224. 2013. View Article : Google Scholar : PubMed/NCBI | |
Gertz JM, McLean KC and Bouchard BA: Endocytosed factor V is trafficked to CD42b+ proplatelet extensions during differentiation of human umbilical cord blood-derived megakaryocytes. J Cell Physiol. 233:8691–8700. 2018. View Article : Google Scholar : PubMed/NCBI | |
van den Oudenrijn S, von dem Borne AE and 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. 28:1054–1061. 2000. View Article : Google Scholar : PubMed/NCBI | |
Nurhayati RW, Ojima Y and Taya M: BMS-777607 promotes megakaryocytic differentiation and induces polyploidization in the CHRF-288-11 cells. Hum Cell. 28:65–72. 2015. View Article : Google Scholar : PubMed/NCBI | |
Six KR, Sicot G, Devloo R, Feys HB, Baruch D and Compernolle V: A comparison of haematopoietic stem cells from umbilical cord blood and peripheral blood for platelet production in a microfluidic device. Vox Sang. 114:330–339. 2019. View Article : Google Scholar : PubMed/NCBI | |
Choi ES, Nichol JL, Hokom MM, Hornkohl AC and Hunt P: Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional. Blood. 85:402–413. 1995. View Article : Google Scholar : PubMed/NCBI | |
Veljkovic DK, Rivard GE, Diamandis M, Blavignac J, Cramer-Borde EM and Hayward CP: Increased expression of urokinase plasminogen activator in Quebec platelet disorder is linked to megakaryocyte differentiation. Blood. 113:1535–1542. 2009. View Article : Google Scholar : PubMed/NCBI | |
Cohen KS, Cheng S, Larson MG, Cupples LA, McCabe EL, Wang YA, Ngwa JS, Martin RP, Klein RJ, Hashmi B, et al: Circulating CD34(+) progenitor cell frequency is associated with clinical and genetic factors. Blood. 121:e50–e56. 2013. View Article : Google Scholar : PubMed/NCBI | |
Pecci A, Malara A, Badalucco S, Bozzi V, Torti M, Balduini CL and Balduini A: Megakaryocytes of patients with MYH9-related thrombocytopenia present an altered proplatelet formation. Thromb Haemost. 102:90–96. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ivetic N, Nazi I, Karim N, Clare R, Smith JW, Moore JC, Hope KJ, Kelton JG and Arnold DM: Producing megakaryocytes from a human peripheral blood source. Transfusion. 56:1066–1074. 2016. View Article : Google Scholar : PubMed/NCBI | |
Orban M, Goedel A, Haas J, Sandrock-Lang K, Gartner F, Jung CB, Zieger B, Parrotta E, Kurnik K, Sinnecker D, et al: Functional comparison of induced pluripotent stem cell- and blood-derived GPIIbIIIa deficient platelets. PLoS One. 10:e01159782015. View Article : Google Scholar : PubMed/NCBI | |
Sinnecker D, Goedel A, Laugwitz KL and Moretti A: Induced pluripotent stem cell-derived cardiomyocytes: A versatile tool for arrhythmia research. Circ Res. 112:961–968. 2013. View Article : Google Scholar : PubMed/NCBI | |
Heazlewood SY, Nilsson SK, Cartledge K, Be CL, Vinson A, Gel M and Haylock DN: Progress in bio-manufacture of platelets for transfusion. Platelets. 28:649–656. 2017. View Article : Google Scholar : PubMed/NCBI | |
Feng Q, Shabrani N, Thon JN, Huo H, Thiel A, Machlus KR, Kim K, Brooks J, Li F, Luo C, et al: Scalable generation of universal platelets from human induced pluripotent stem cells. Stem Cell Reports. 3:817–831. 2014. View Article : Google Scholar : PubMed/NCBI | |
Börger AK, Eicke D, Wolf C, Gras C, Aufderbeck S, Schulze K, Engels L, Eiz-Vesper B, Schambach A, Guzman CA, et al: Generation of HLA-Universal iPSC-derived megakaryocytes and platelets for survival under refractoriness conditions. Mol Med. 22:274–285. 2016. View Article : Google Scholar : PubMed/NCBI | |
Gaur M, Kamata T, Wang S, Moran B, Shattil SJ and Leavitt AD: Megakaryocytes derived from human embryonic stem cells: A genetically tractable system to study megakaryocytopoiesis and integrin function. J Thromb Haemost. 4:436–442. 2006. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, Liu C, Wang H, Wu D, Su P, Wang M, Guo J, Zhao S, Dong S, Zhou W, et al: Thrombopoietin knock-in augments platelet generation from human embryonic stem cells. Stem Cell Res Ther. 9:1942018. View Article : Google Scholar : PubMed/NCBI | |
Matsubara Y, Ono Y, Suzuki H, Arai F, Suda T, Murata M and Ikeda Y: OP9 bone marrow stroma cells differentiate into megakaryocytes and platelets. PLoS One. 8:e581232013. View Article : Google Scholar : PubMed/NCBI | |
Ono-Uruga Y, Tozawa K, Horiuchi T, Murata M, Okamoto S, Ikeda Y, Suda T and Matsubara Y: Human adipose tissue-derived stromal cells can differentiate into megakaryocytes and platelets by secreting endogenous thrombopoietin. J Thromb Haemost. 14:1285–1297. 2016. View Article : Google Scholar : PubMed/NCBI | |
Tozawa K, Ono-Uruga Y, Yazawa M, Mori T, Murata M, Okamoto S, Ikeda Y and Matsubara Y: Megakaryocytes and platelets from a novel human adipose tissue-derived mesenchymal stem cell line. Blood. 133:633–643. 2019. View Article : Google Scholar : PubMed/NCBI | |
McArthur K, Chappaz S and Kile BT: Apoptosis in megakaryocytes and platelets: The life and death of a lineage. Blood. 131:605–610. 2018. View Article : Google Scholar : PubMed/NCBI | |
Guo T, Wang X, Qu Y, Yin Y, Jing T and Zhang Q: Megakaryopoiesis and platelet production: Insight into hematopoietic stem cell proliferation and differentiation. Stem Cell Investig. 2:32015.PubMed/NCBI | |
Pope NJ and Bresnick EH: Differential coregulator requirements for function of the hematopoietic transcription factor GATA-1 at endogenous loci. Nucleic Acids Res. 38:2190–2200. 2010. View Article : Google Scholar : PubMed/NCBI | |
Orkin SH, Shivdasani RA, Fujiwara Y and McDevitt MA: Transcription factor GATA-1 in megakaryocyte development. Stem Cells. 16 (Suppl 2):S79–S83. 1998. View Article : Google Scholar | |
Wang X, Crispino JD, Letting DL, Nakazawa M, Poncz M and Blobel GA: Control of megakaryocyte-specific gene expression by GATA-1 and FOG-1: Role of Ets transcription factors. EMBO J. 21:5525–5234. 2002. View Article : Google Scholar | |
Gao Z, Huang Z, Olivey HE, Gurbuxani S, Crispino JD and Svensson EC: FOG-1-mediated recruitment of NuRD is required for cell lineage re-enforcement during haematopoiesis. EMBO J. 29:457–468. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lejon S, Thong SY, Murthy A, AlQarni S, Murzina NV, Blobel GA, Laue ED and Mackay JP: Insights into association of the NuRD complex with FOG-1 from the crystal structure of an RbAp48.FOG-1 complex. J Biol Chem. 286:1196–1203. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hart A, Melet F, Grossfeld P, Chien K, Jones C, Tunnacliffe A, Favier R and Bernstein A: Fli-1 is required for murine vascular and megakaryocytic development and is hemizygously deleted in patients with thrombocytopenia. Immunity. 13:167–177. 2000. View Article : Google Scholar : PubMed/NCBI | |
Starck J, Weiss-Gayet M, Gonnet C, Guyot B, Vicat JM and Morle F: Inducible Fli-1 gene deletion in adult mice modifies several myeloid lineage commitment decisions and accelerates proliferation arrest and terminal erythrocytic differentiation. Blood. 116:4795–4805. 2010. View Article : Google Scholar : PubMed/NCBI | |
Deutsch VR and Tomer A: Advances in megakaryocytopoiesis and thrombopoiesis: From bench to bedside. Br J Haematol. 161:778–793. 2013. View Article : Google Scholar : PubMed/NCBI | |
Eisbacher M, Holmes ML, Newton A, Hogg PJ, Khachigian LM, Crossley M and Chong BH: Protein-protein interaction between Fli-1 and GATA-1 mediates synergistic expression of megakaryocyte-specific genes through cooperative DNA binding. Mol Cell Biol. 23:3427–3441. 2003. View Article : Google Scholar : PubMed/NCBI | |
Vo KK, Jarocha DJ, Lyde RB, Hayes V, Thom CS, Sullivan SK, French DL and Poncz M: FLI1 level during megakaryopoiesis affects thrombopoiesis and platelet biology. Blood. 129:3486–3494. 2017. View Article : Google Scholar : PubMed/NCBI | |
Okada Y, Nagai R, Matsuura E, Hoshika Y, Nakata E, Nagura H, Watanabe A, Komatsu N and Doi T: Suppression of RUNX1 by siRNA in megakaryocytic UT-7/GM cells. Nucleic Acids Symp Ser (Oxf). 261–262. 2006. View Article : Google Scholar : PubMed/NCBI | |
Mata J, Curado S, Ephrussi A and Rørth P: Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell. 101:511–522. 2000. View Article : Google Scholar : PubMed/NCBI | |
Butcher L, Ahluwalia M, Ord T, Johnston J, Morris RH, Kiss-Toth E, Ord T and Erusalimsky JD: Evidence for a role of TRIB3 in the regulation of megakaryocytopoiesis. Sci Rep. 7:66842017. View Article : Google Scholar : PubMed/NCBI | |
Gotoh A, Miyazawa K, Ohyashiki K, Tauchi T, Boswell HS, Broxmeyer HE and Toyama K: Tyrosine phosphorylation and activation of focal adhesion kinase (p125FAK) by BCR-ABL oncoprotein. Exp Hematol. 23:1153–1159. 1995.PubMed/NCBI | |
Gotoh T, Niino Y, Tokuda M, Hatase O, Nakamura S, Matsuda M and Hattori S: Activation of R-Ras by Ras-guanine nucleotide-releasing factor. J Biol Chem. 272:18602–18607. 1997. View Article : Google Scholar : PubMed/NCBI | |
Ortiz-Rivero S, Baquero C, Hernandez-Cano L, Roldan-Etcheverry JJ, Gutierrez-Herrero S, Fernandez-Infante C, Martin-Granado V, Anguita E, de Pereda JM, Porras A and Guerrero C: C3G, through its GEF activity, induces megakaryocytic differentiation and proplatelet formation. Cell Commun Signal. 16:1012018. View Article : Google Scholar : PubMed/NCBI | |
Sullenbarger B, Bahng JH, Gruner R, Kotov N and Lasky LC: Prolonged continuous in vitro human platelet production using three-dimensional scaffolds. Exp Hematol. 37:101–110. 2009. View Article : Google Scholar : PubMed/NCBI | |
Malara A, Currao M, Gruppi C, Celesti G, Viarengo G, Buracchi C, Laghi L, Kaplan DL and Balduini A: Megakaryocytes contribute to the bone marrow-matrix environment by expressing fibronectin, type IV collagen, and laminin. Stem Cells. 32:926–937. 2014. View Article : Google Scholar : PubMed/NCBI | |
Abbonante V, Di Buduo CA, Gruppi C, De Maria C, Spedden E, De Acutis A, Staii C, Raspanti M, Vozzi G, Kaplan DL, et al: A new path to platelet production through matrix sensing. Haematologica. 102:1150–1160. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tozzi L, Laurent PA, Di Buduo CA, Mu X, Massaro A, Bretherton R, Stoppel W, Kaplan DL and Balduini A: Multi-channel silk sponge mimicking bone marrow vascular niche for platelet production. Biomaterials. 178:122–133. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ito Y, Nakamura S, Sugimoto N, Shigemori T, Kato Y, Ohno M, Sakuma S, Ito K, Kumon H, Hirose H, et al: Turbulence activates platelet biogenesis to enable clinical scale ex vivo production. Cell. 174:636–648 e18. 2018. View Article : Google Scholar : PubMed/NCBI | |
Jiang HJ, Yu Z, Ding N, Yang M, Zhang L, Fan XM, Zhou Y, Zou Q, Hou J, Zheng J, et al: The role of AGK in thrombocytopoiesis and possible therapeutic strategies. Blood. 136:119–129. 2020. View Article : Google Scholar : PubMed/NCBI | |
Kaushansky K, Broudy VC, Lin N, Jorgensen MJ, McCarty J, Fox N, Zucker-Franklin D and Lofton-Day C: Thrombopoietin, the Mp1 ligand, is essential for full megakaryocyte development. Proc Natl Acad Sci USA. 92:3234–3238. 1995. View Article : Google Scholar : PubMed/NCBI | |
Panuganti S, Schlinker AC, Lindholm PF, Papoutsakis ET and Miller WM: Three-stage ex vivo expansion of high-ploidy megakaryocytic cells: Toward large-scale platelet production. Tissue Eng Part A. 19:998–1014. 2013. View Article : Google Scholar : PubMed/NCBI | |
Chang Y, Bluteau D, Debili N and Vainchenker W: From hematopoietic stem cells to platelets. J Thromb Haemost. 5 (Suppl 1):S318–S327. 2007. View Article : Google Scholar | |
Behrens K and Alexander WS: Cytokine control of megakaryopoiesis. Growth Factors. 36:89–103. 2018. View Article : Google Scholar : PubMed/NCBI | |
Fielder PJ, Gurney AL, Stefanich E, Marian M, Moore MW, Carver-Moore K and de Sauvage FJ: Regulation of thrombopoietin levels by c-mpl-mediated binding to platelets. Blood. 87:2154–2161. 1996. View Article : Google Scholar : PubMed/NCBI | |
He X, Chen Z, Jiang Y, Qiu X and Zhao X: Different mutations of the human c-mpl gene indicate distinct haematopoietic diseases. J Hematol Oncol. 6:112013. View Article : Google Scholar : PubMed/NCBI | |
Di Buduo CA, Currao M, Pecci A, Kaplan DL, Balduini CL and Balduini A: Revealing eltrombopag's promotion of human megakaryopoiesis through AKT/ERK-dependent pathway activation. Haematologica. 101:1479–1488. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wong RSM, Saleh MN, Khelif A, Salama A, Portella MSO, Burgess P and Bussel JB: Safety and efficacy of long-term treatment of chronic/persistent ITP with eltrombopag: Final results of the EXTEND study. Blood. 130:2527–2536. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gill H, Leung GM, Lopes D and Kwong YL: The thrombopoietin mimetics eltrombopag and romiplostim in the treatment of refractory aplastic anaemia. Br J Haematol. 176:991–994. 2017. View Article : Google Scholar : PubMed/NCBI | |
Fischer JC and Uhrberg M: Prevention of leukemia relapse by donor activating KIR2DS1. N Engl J Med. 367:2054–2055. 2012. View Article : Google Scholar : PubMed/NCBI | |
Al-Samkari H, Grace RF and Kuter DJ: The role of romiplostim for pediatric patients with immune thrombocytopenia. Ther Adv Hematol. 11:20406207209129922020. View Article : Google Scholar : PubMed/NCBI | |
Al-Samkari H, Parnes AD, Goodarzi K, Weitzman JI, Connors JM and Kuter DJ: A multicenter study of romiplostim for chemotherapy-induced thrombocytopenia in solid tumors and hematologic malignancies. Haematologica. Jun 4–2020.(Epub ahead of print). doi.org/10.3324/haematol.2020.251900. View Article : Google Scholar | |
Kuter DJ, Arnold DM, Rodeghiero F, Janssens A, Selleslag D, Bird R, Newland A, Mayer J, Wang K and Olie R: Safety and efficacy of self-administered romiplostim in patients with immune thrombocytopenia: Results of an integrated database of five clinical trials. Am J Hematol. 95:643–651. 2020. View Article : Google Scholar : PubMed/NCBI | |
Hosokawa K, Yamazaki H, Tanabe M, Imi T, Sugimori N and Nakao S: High-dose romiplostim accelerates hematologic recovery in patients with aplastic anemia refractory to eltrombopag. Leukemia. Jul 3–2020.(Epub ahead of print). doi org/10.1038/s41375-020-0950-6. |