Road blocks in making platelets for transfusion

Journal of Thrombosis and Haemostasis

Volumn 13, Issue S1, 2015, Pages S55-S62

  Thon, J N ^a,b,c   Medvetz, D A ^a,b   Karlsson, S M ^c   Italiano, J E ^a,b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Platelet BioGenesis   (United States)

Author keywords

Biomedical engineering; Bioreactors; Hematopoietic stem cells; Megakaryocytes; Platelets

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN LIKE 5; BETA TUBULIN; CD135 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; GRANULOCYTE COLONY STIMULATING FACTOR; HLA A ANTIGEN; HLA ANTIGEN CLASS 2; HLA B ANTIGEN; HLA C ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 11; INTERLEUKIN 3; INTERLEUKIN 6; INTERLEUKIN 9; LEUKOSIALIN; LOW DENSITY LIPOPROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PHALLOIDIN; PLATELET DERIVED GROWTH FACTOR BB; SEROTONIN; SOMATOMEDIN B; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1; THROMBOCYTE FACTOR 4; THROMBOPOIETIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VON WILLEBRAND FACTOR;

ALLOIMMUNITY; ANTIGEN EXPRESSION; BACTERIUM CONTAMINATION; BLOOD STORAGE; CELL DIFFERENTIATION; CELL MATURATION; CLINICAL EFFECTIVENESS; EMBRYONIC STEM CELL; EX VIVO STUDY; GRAFT REJECTION; HEMATOLOGIC MALIGNANCY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IN VIVO STUDY; INFECTION RISK; MEGAKARYOCYTE; MINOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; OUTCOME ASSESSMENT; PATIENT SAFETY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RISK ASSESSMENT; SHELF LIFE; STEM CELL; THROMBOCYTE TRANSFUSION; THROMBOCYTOPOIESIS; UMBILICAL CORD BLOOD STEM CELL; BIOREACTOR; CELL CULTURE; CULTURE TECHNIQUE; DEVICES; GENE EXPRESSION REGULATION; GENETICS; NUCLEAR REPROGRAMMING; PHENOTYPE; PHYSIOLOGY; STEM CELL NICHE; THROMBOCYTE;

BIOREACTORS; BLOOD PLATELETS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CELLULAR REPROGRAMMING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MEGAKARYOCYTES; PHENOTYPE; PLATELET TRANSFUSION; STEM CELL NICHE; THROMBOPOIESIS;

EID: 84931375133     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12942     Document Type: Review

References (76)

1. Lee EJ, Godara P, Haylock D. Biomanufacture of human platelets for transfusion: rationale and approaches. Exp Hematol 2014; 42: 332-46.
2. Lambert MP, Sullivan SK, Fuentes R, French DL, Poncz M. Challenges and promises for the development of donor-independent platelet transfusions. Blood 2013; 121: 3319-24.
3. Services DoHaH. 2011 National Blood Collection and Utilization Report. The 2011 national blood collection and utilization survey report Washington, DC: DHHS, 2013.
4. Bergmeier W, Burger PC, Piffath CL, Hoffmeister KM, Hartwig JH, Nieswandt B, Wagner DD. Metalloproteinase inhibitors improve the recovery and hemostatic function of in vitro-aged or -injured mouse platelets. Blood 2003; 102: 4229-35.
5. Nishikii H, Eto K, Tamura N, Hattori K, Heissig B, Kanaji T, Sawaguchi A, Goto S, Ware J, Nakauchi H. Metalloproteinase regulation improves in vitro generation of efficacious platelets from mouse embryonic stem cells. J Exp Med 2008; 205: 1917-27.
6. Blood Collection and Transfusion Market: A Global Perspective - 2014. Marketing Research Bureau, 2014.
7. Rumjantseva V, Hoffmeister KM. Novel and unexpected clearance mechanisms for cold platelets. Transfus Apheres Sci 2010; 42: 63-70.
8. Whitaker BI, Schlump K, Schulman J, Green J. Report of the US Department of Health and Human Services. The 2009 National Blood Collection and Utilization Survey Report. Washington, DC: US Department of Health and Human Services, Office of the Assistant Secretary for Health, 2011.
9. DiCarlo AL, Poncz M, Cassatt DR, Shah JR, Czarniecki CW, Maidment BW. Medical countermeasures for platelet regeneration after radiation exposure. Report of a workshop and guided discussion sponsored by the National Institute of Allergy and Infectious Diseases, Bethesda, MD, March 22-23, 2010. Radiat Res 2011; 176: e0001-15.
10. Schiffer CA. Diagnosis and management of refractoriness to platelet transfusion. Blood Rev 2001; 15: 175-80.
11. Long MW, Williams N, Ebbe S. Immature megakaryocytes in the mouse: physical characteristics, cell cycle status, and in vitro responsiveness to thrombopoietic stimulatory factor. Blood 1982; 59: 569-75.
12. Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993; 81: 2844-53.
13. Ebbe S. Biology of megakaryocytes. Prog Hemostasis Thromb 1976; 3: 211-29.
14. Zimmet J, Ravid K. Polyploidy: occurrence in nature, mechanisms, and significance for the megakaryocyte-platelet system. Exp Hematol 2000; 28: 3-16.
15. Merico V, Zuccotti M, Carpi D, Baev D, Mulas F, Sacchi L, Bellazzi R, Pastorelli R, Redi CA, Moratti R, Garagna S, Balduini A. The genomic and proteomic blueprint of mouse megakaryocytes derived from embryonic stem cells. J Thromb Haemost 2012; 10: 907-15.
16. Kaushansky A, Kaushansky K. Systems biology of megakaryocytes. Adv Exp Med Biol 2014; 844: 59-84.
17. Machlus KR, Thon JN, Italiano JE Jr. Interpreting the developmental dance of the megakaryocyte: a review of the cellular and molecular processes mediating platelet formation. Br J Haematol 2014; 165: 227-36.
18. Thon JN, Italiano JE. Platelets: production, morphology and ultrastructure. Handb Exp Pharmacol 2012: 3-22.
19. Matsunaga T, Tanaka I, Kobune M, Kawano Y, Tanaka M, Kuribayashi K, Iyama S, Sato T, Sato Y, Takimoto R, Takayama T, Kato J, Ninomiya T, Hamada H, Niitsu Y. Ex vivo large-scale generation of human platelets from cord blood CD34+ cells. Stem Cells 2006; 24: 2877-87.
20. Nakamura S, Takayama N, Hirata S, Seo H, Endo H, Ochi K, Fujita K, Koike T, Harimoto K, Dohda T, Watanabe A, Okita K, Takahashi N, Sawaguchi A, Yamanaka S, Nakauchi H, Nishimura S, Eto K. Expandable megakaryocyte cell lines enable clinically applicable generation of platelets from human induced pluripotent stem cells. Cell Stem Cell 2014; 14: 535-48.
21. Choi ES, Nichol JL, Hokom MM, Hornkohl AC, Hunt P. Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional. Blood 1995; 85: 402-13.
22. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282: 1145-7.
23. Chapman AR, Scala CC. Evaluating the first-in-human clinical trial of a human embryonic stem cell-based therapy. Kennedy Inst Ethics J 2012; 22: 243-61.
24. Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM, Mickunas E, Gay R, Klimanskaya I, Lanza R. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 2012; 379: 713-20.
25. Lu SJ, Li F, Yin H, Feng Q, Kimbrel EA, Hahm E, Thon JN, Wang W, Italiano JE, Cho J, Lanza R. Platelets generated from human embryonic stem cells are functional in vitro and in the microcirculation of living mice. Cell Res 2011; 21: 530-45.
26. Pick M, Azzola L, Osborne E, Stanley EG, Elefanty AG. Generation of megakaryocytic progenitors from human embryonic stem cells in a feeder- and serum-free medium. PLoS ONE 2013; 8: e55530.
27. Takayama N, Nishikii H, Usui J, Tsukui H, Sawaguchi A, Hiroyama T, Eto K, Nakauchi H. Generation of functional platelets from human embryonic stem cells in vitro via ES-sacs, VEGF-promoted structures that concentrate hematopoietic progenitors. Blood 2008; 111: 5298-306.
28. Cairo MS, Wagner JE. Placental and/or umbilical cord blood: an alternative source of hematopoietic stem cells for transplantation. Blood 1997; 90: 4665-78.
29. Wolf SM, Kahn JP, Wagner JE. Using preimplantation genetic diagnosis to create a stem cell donor: issues, guidelines & limits. J Law Med Ethics 2003; 31: 327-39.
30. Takayama N, Nishimura S, Nakamura S, Shimizu T, Ohnishi R, Endo H, Yamaguchi T, Otsu M, Nishimura K, Nakanishi M, Sawaguchi A, Nagai R, Takahashi K, Yamanaka S, Nakauchi H, Eto K. Transient activation of c-MYC expression is critical for efficient platelet generation from human induced pluripotent stem cells. J Exp Med 2010; 207: 2817-30.
31. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-76.
32. Riolobos L, Hirata RK, Turtle CJ, Wang PR, Gornalusse GG, Zavajlevski M, Riddell SR, Russell DW. HLA engineering of human pluripotent stem cells. Mol Ther 2013; 21: 1232-41.
33. Taylor CJ, Peacock S, Chaudhry AN, Bradley JA, Bolton EM. Generating an iPSC bank for HLA-matched tissue transplantation based on known donor and recipient HLA types. Cell Stem Cell 2012; 11: 147-52.
34. Feng Q, Shabrani N, Thon JN, Huo H, Thiel A, Machlus KR, Kim K, Brooks J, Li F, Luo C, Kimbrel EA, Wang J, Kim KS, Italiano J, Cho J, Lu SJ, Lanza R. Scalable generation of universal platelets from human induced pluripotent stem cells. Stem Cell Reports 2014; 3: 817-31.
35. Hod E, Schwartz J. Platelet transfusion refractoriness. Br J Haematol 2008; 142: 348-60.
36. Slichter SJ. Platelet transfusion therapy. Hematol Oncol Clin North Am 2007; 21: 697-729, vii.
37. Lund TC, Boitano AE, Delaney CS, Shpall EJ, Wagner JE. Advances in umbilical cord blood manipulation-from niche to bedside. Nat Rev Clin Oncol 2015; 12: 163-74.
38. Rauch C, Feifel E, Amann EM, Spotl HP, Schennach H, Pfaller W, Gstraunthaler G. Alternatives to the use of fetal bovine serum: human platelet lysates as a serum substitute in cell culture media. Altex 2011; 28: 305-16.
39. Avanzi MP, Mitchell WB. Ex vivo production of platelets from stem cells. Br J Haematol 2014; 165: 237-47.
40. Reems JA, Pineault N, Sun S. In vitro megakaryocyte production and platelet biogenesis: state of the art. Transfus Med Rev 2010; 24: 33-43.
41. Ru YX, Zhao SX, Dong SX, Yang YQ, Eyden B. On the maturation of megakaryocytes: a review with original observations on human in vivo cells emphasizing morphology and ultrastructure. Ultrastruct Pathol 2015; 39: 79-87.
42. Liu ZJ, Hoffmeister KM, Hu Z, Mager DE, Ait-Oudhia S, Debrincat MA, Pleines I, Josefsson EC, Kile BT, Italiano J Jr, Ramsey H, Grozovsky R, Veng-Pedersen P, Chavda C, Sola-Visner M. Expansion of the neonatal platelet mass is achieved via an extension of platelet lifespan. Blood 2014; 123: 3381-9.
43. Larson MK, Watson SP. A product of their environment: do megakaryocytes rely on extracellular cues for proplatelet formation? Platelets 2006; 17: 435-40.
44. Takahashi R, Sekine N, Nakatake T. Influence of monoclonal antiplatelet glycoprotein antibodies on in vitro human megakaryocyte colony formation and proplatelet formation. Blood 1999; 93: 1951-8.
45. Shin JW, Swift J, Spinler KR, Discher DE. Myosin-II inhibition and soft 2D matrix maximize multinucleation and cellular projections typical of platelet-producing megakaryocytes. Proc Natl Acad Sci USA 2011; 108: 11458-63.
46. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, Jin DK, Dias S, Zhang F, Hartman TE, Hackett NR, Crystal RG, Witte L, Hicklin DJ, Bohlen P, Eaton D, Lyden D, de Sauvage F, Rafii S. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 2004; 10: 64-71.
47. Fujimoto TT, Kohata S, Suzuki H, Miyazaki H, Fujimura K. Production of functional platelets by differentiated embryonic stem (ES) cells in vitro. Blood 2003; 102: 4044-51.
48. Dunois-Larde C, Capron C, Fichelson S, Bauer T, Cramer-Borde E, Baruch D. Exposure of human megakaryocytes to high shear rates accelerates platelet production. Blood 2009; 114: 1875-83.
49. Thon JN, Montalvo A, Patel-Hett S, Devine MT, Richardson JL, Ehrlicher A, Larson MK, Hoffmeister K, Hartwig JH, Italiano JE Jr. Cytoskeletal mechanics of proplatelet maturation and platelet release. J Cell Biol 2011; 191: 861-74.
50. Liu ZJ, Sola-Visner M. Neonatal and adult megakaryopoiesis. Curr Opin Hematol 2011; 18: 330-7.
51. Klusmann JH, Godinho FJ, Heitmann K, Maroz A, Koch ML, Reinhardt D, Orkin SH, Li Z. Developmental stage-specific interplay of GATA1 and IGF signaling in fetal megakaryopoiesis and leukemogenesis. Genes Dev 2010; 24: 1659-72.
52. 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: 1238-49 e5.
53. Fuentes R, Wang Y, Hirsch J, Wang C, Rauova L, Worthen GS, Kowalska MA, Poncz M. Infusion of mature megakaryocytes into mice yields functional platelets. J Clin Investig 2010; 120: 3917-22.
54. Ono Y, Wang Y, Suzuki H, Okamoto S, Ikeda Y, Murata M, Poncz M, Matsubara Y. Induction of functional platelets from mouse and human fibroblasts by p45NF-E2/Maf. Blood 2012; 120: 3812-21.
55. Chen TW, Hwang SM, Chu IM, Hsu SC, Hsieh TB, Yao CL. Characterization and transplantation of induced megakaryocytes from hematopoietic stem cells for rapid platelet recovery by a two-step serum-free procedure. Exp Hematol 2009; 37: 1330-9 e5.
56. Paquette RL, Dergham ST, Karpf E, Wang HJ, Slamon DJ, Souza L, Glaspy JA. Ex vivo expanded unselected peripheral blood: progenitor cells reduce posttransplantation neutropenia, thrombocytopenia, and anemia in patients with breast cancer. Blood 2000; 96: 2385-90.
57. Bertolini F, Battaglia M, Pedrazzoli P, Da Prada GA, Lanza A, Soligo D, Caneva L, Sarina B, Murphy S, Thomas T, della Cuna GR. Megakaryocytic progenitors can be generated ex vivo and safely administered to autologous peripheral blood progenitor cell transplant recipients. Blood 1997; 89: 2679-88.
58. Shpall EJ, Quinones R, Giller R, Zeng C, Baron AE, Jones RB, Bearman SI, Nieto Y, Freed B, Madinger N, Hogan CJ, Slat-Vasquez V, Russell P, Blunk B, Schissel D, Hild E, Malcolm J, Ward W, McNiece IK. Transplantation of ex vivo expanded cord blood. Biol Blood Marrow Transplant 2002; 8: 368-76.
59. Thon JN, Montalvo A, Patel-Hett S, Devine MT, Richardson JL, Ehrlicher A, Larson MK, Hoffmeister K, Hartwig JH, Italiano JE Jr. Cytoskeletal mechanics of proplatelet maturation and platelet release. J Cell Biol 2010; 191: 861-74.
60. Xi J, Zhu H, Liu D, Nan X, Zheng W, Liu K, Shi W, Chen L, Lv Y, Yan F, Li Y, Xie X, Wang Y, Yue W, Xu X, Wei X, Zhu J, Huang X, Pei X. Infusion of megakaryocytic progenitor products generated from cord blood hematopoietic stem/progenitor cells: results of the phase 1 study. PLoS ONE 2013; 8: e54941.
61. Thon JN, Italiano JE. Platelet formation. Semin Hematol 2010; 47: 220-6.
62. Ahmed RP, Ashraf M, Buccini S, Shujia J, Haider H. Cardiac tumorigenic potential of induced pluripotent stem cells in an immunocompetent host with myocardial infarction. Regen Med 2011; 6: 171-8.
63. Monzen S, Osuda K, Miyazaki Y, Hayashi N, Takahashi K, Kashiwakura I. Radiation sensitivities in the terminal stages of megakaryocytic maturation and platelet production. Radiat Res 2009; 172: 314-20.
64. Ebbe S. Regulation of murine megakaryocyte size and ploidy by non-platelet-dependent mechanisms in radiation-induced megakaryocytopenia. Radiat Res 1991; 127: 278-84.
65. Ebbe S, Phalen E, Yee T. Postirradiation thrombocytopoiesis: suppression, recovery, compensatory states, and macromegakaryocytosis. Prog Clin Biol Res 1986; 215: 71-89.
66. Thon JN, Mazutis L, Wu S, Sylman JL, Ehrlicher A, Machlus KR, Feng Q, Lu S, Lanza R, Neeves KB, Weitz DA, Italiano JE Jr. Platelet bioreactor-on-a-chip. Blood 2014; 124: 1857-67.
67. Jiang J, Woulfe DS, Papoutsakis ET. Shear enhances thrombopoiesis and formation of microparticles that induce megakaryocytic differentiation of stem cells. Blood 2014; 124: 2094-103.
68. Junt T, Schulze H, Chen Z, Massberg S, Goerge T, Krueger A, Wagner DD, Graf T, Italiano JE Jr, Shivdasani RA, von Andrian UH. Dynamic visualization of thrombopoiesis within bone marrow. Science 2007; 317: 1767-70.
69. Tangelder GJ, Slaaf DW, Arts T, Reneman RS. Wall shear rate in arterioles in vivo: least estimates from platelet velocity profiles. Am J Physiol 1988; 254: H1059-64.
70. Looney MR, Thornton EE, Sen D, Lamm WJ, Glenny RW, Krummel MF. Stabilized imaging of immune surveillance in the mouse lung. Nat Methods 2011; 8: 91-6.
71. Gold M, Chan V, Turcr C, DeFranco A. Membrane Ig crosslinking regulates phosphatidylinositol-3-kinase in B lymphocytes. J Immunol 1992; 148: 2012-22.
72. Lane WJ, Dias S, Hattori K, Heissig B, Choy M, Rabbany SY, Wood J, Moore MA, Rafii S. Stromal-derived factor 1-induced megakaryocyte migration and platelet production is dependent on matrix metalloproteinases. Blood 2000; 96: 4152-9.
73. Zhang L, Urtz N, Gaertner F, Legate KR, Petzold T, Lorenz M, Mazharian A, Watson SP, Massberg S. Sphingosine kinase 2 (Sphk2) regulates platelet biogenesis by providing intracellular sphingosine 1-phosphate (S1P). Blood 2013; 122: 791-802.
74. Pallotta I, Lovett M, Kaplan DL, Balduini A. Three-dimensional system for the in vitro study of megakaryocytes and functional platelet production using silk-based vascular tubes. Tissue Eng Part C Methods 2011; 17: 1223-32.
75. Sullenbarger B, Bahng JH, Gruner R, Kotov N, Lasky LC. Prolonged continuous in vitro human platelet production using three-dimensional scaffolds. Exp Hematol 2009; 37: 101-10.
76. Diamond SL, Purvis J, Chatterjee M, Flamm MH. Systems biology of platelet-vessel wall interactions. Front Physiol 2013; 4: 229.