Scalable generation of universal platelets from human induced pluripotent stem cells

Stem Cell Reports

Volumn 3, Issue 5, 2014, Pages 817-831

  Feng, Qiang ^a   Shabrani, Namrata ^b   Thon, Jonathan N ^c,d   Huo, Hongguang ^a   Thiel, Austin ^a   Machlus, Kellie R ^c,d   Kim, Kyungho ^b   Brooks, Julie ^a   Li, Feng ^a   Luo, Chenmei ^a   Kimbrel, Erin A ^a   Wang, Jiwu ^f   Kim, Kwang Soo ^g   Italiano, Joseph ^c,d,e   Cho, Jaehyung ^b   Lu, Shi Jiang ^a   Lanza, Robert ^a  

^a Medical and Scientific Development Advanced Cell Technology   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f Allele Biotechnology and Pharmaceuticals Inc   (United States)

^g MCLEAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 MICROGLOBULIN; HLA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; LEUKOSIALIN;

ANIMAL CELL; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CRYOPRESERVATION; FILOPODIUM; HUMAN; HUMAN CELL; LAMELLIPODIUM; MACROPHAGE ACTIVATION; MALE; MEGAKARYOCYTE; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; THROMBOCYTE; THROMBOCYTE AGGREGATION; THROMBOCYTE TRANSFUSION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CULTURE TECHNIQUE; CYTOLOGY; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GENE INACTIVATION; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; PROCEDURES; REPRODUCIBILITY; SCID MOUSE; ULTRASTRUCTURE; XENOGRAFT;

ANIMALIA;

ANIMALS; ANTIGENS, CD31; ANTIGENS, CD34; ANTIGENS, CD43; BETA 2-MICROGLOBULIN; BLOOD PLATELETS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; GENE KNOCKOUT TECHNIQUES; HLA ANTIGENS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MEGAKARYOCYTES; MICE, INBRED NOD; MICE, SCID; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; PLATELET TRANSFUSION; REPRODUCIBILITY OF RESULTS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84922534997     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.09.010     Document Type: Article

References (46)

1. Chanprasert, S., Geddis, A.E., Barroga, C., Fox, N.E., and Kaushansky, K. (2006). Thrombopoietin (TPO) induces c-myc expression through a PI3K- and MAPK-dependent pathway that is not mediated by Akt, PKCzeta or mTOR in TPO-dependent cell lines and primary megakaryocytes. Cell. Signal. 18, 1212-1218.
2. Choi, E.S., Nichol, J.L., Hokom, M.M., Hornkohl, A.C., and Hunt, P. (1995). Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional. Blood 85, 402-413.
3. Choi, K.D., Vodyanik, M., and Slukvin, I.I. (2011). Hematopoietic differentiation and production of mature myeloid cells from human pluripotent stem cells. Nat. Protoc. 6, 296-313.
4. D'Urso, C.M., Wang, Z.G., Cao, Y., Tatake, R., Zeff, R.A., and Ferrone, S. (1991). Lack of HLA class I antigen expression by cultured melanoma cells FO-1 due to a defect in B2m gene expression. J. Clin. Invest. 87, 284-292.
5. Gerecht-Nir, S., Ziskind, A., Cohen, S., and Itskovitz-Eldor, J. (2003). Human embryonic stem cells as an in vitro model for human vascular development and the induction of vascular differentiation. Laboratory investigation; a journal of technical methods and pathology 83, 1811-1820.
6. Gras, C., Schulze, K., Goudeva, L., Guzman, C.A., Blasczyk, R., and Figueiredo, C. (2013). HLA-universal platelet transfusions prevent platelet refractoriness in a mouse model. Hum. Gene Ther. 24, 1018-1028.
7. Guo, Y., Niu, C., Breslin, P., Tang, M., Zhang, S., Wei, W., Kini, A.R., Paner, G.P., Alkan, S., Morris, S.W., et al. (2009). c-Myc-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Blood 114, 2097-2106.
8. Hod, E., and Schwartz, J. (2008). Platelet transfusion refractoriness. Br. J. Haematol. 142, 348-360.
9. Hu, Z., and Yang, Y.G. (2012). Full reconstitution of human platelets in humanized mice after macrophage depletion. Blood 120, 1713-1716.
10. Israels, S.J. (2013). Platelet function in the newborn. In Platelets, A.D. Michelson, ed. (San Diego: Elsevier Academic Press), pp. 503-516.
11. Israels, S.J., and Rand, M.L. (2013). What we have learned from inherited platelet disorders. Pediatr. Blood Cancer 60 (Suppl 1), S2-S7.
12. Israels, S.J., Rand, M.L., and Michelson, A.D. (2003). Neonatal platelet function. Semin. Thromb. Hemost. 29, 363-372.
13. Junt, T., Schulze, H., Chen, Z., Massberg, S., Goerge, T., Krueger, A., Wagner, D.D., Graf, T., Italiano, J.E., Jr., Shivdasani, R.A., and von Andrian, U.H. (2007). Dynamic visualization of thrombopoiesis within bone marrow. Science 317, 1767-1770.
14. Kaufman, R.M., Airo, R., Pollack, S., and Crosby, W.H. (1965). Circulating megakaryocytes and platelet release in the lung. Blood 26, 720-731.
15. Kennedy, M., Awong, G., Sturgeon, C.M., Ditadi, A., LaMotte- Mohs, R., Zúñiga-Pflücker, J.C., and Keller, G. (2012). T lymphocyte potential marks the emergence of definitive hematopoietic progenitors in human pluripotent stem cell differentiation cultures. Cell Reports 2, 1722-1735.
16. Klimanskaya, I., Chung, Y., Becker, S., Lu, S.J., and Lanza, R. (2007). Derivation of human embryonic stem cells from single blastomeres. Nat. Protoc. 2, 1963-1972.
17. Klimchenko, O., Mori, M., Distefano, A., Langlois, T., Larbret, F., Lecluse, Y., Feraud, O., Vainchenker, W., Norol, F., and Debili, N. (2009). A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood 114, 1506-1517.
18. Long, M.W. (1998). Megakaryocyte differentiation events. Semin. Hematol. 35, 192-199.
19. Lu, S.J., Feng, Q., Caballero, S., Chen, Y., Moore, M.A., Grant, M.B., and Lanza, R. (2007). Generation of functional hemangioblasts from human embryonic stem cells. Nat. Methods 4, 501-509.
20. Lu, S.J., Li, F., Yin, H., Feng, Q., Kimbrel, E.A., Hahm, E., Thon, J.N., Wang, W., Italiano, J.E., Cho, J., and Lanza, R. (2011). Platelets generated from human embryonic stem cells are functional in vitro and in the microcirculation of living mice. Cell Res. 21, 530-545.
21. Lu, S.J., Kelley, T., Feng, Q., Chen, A., Reuveny, S., Lanza, R., and Oh, S.K. (2013). 3D microcarrier system for efficient differentiation of human pluripotent stem cells into hematopoietic cells without feeders and serum [corrected]. Regen. Med. 8, 413-424.
22. Matsunaga, T., Tanaka, I., Kobune, M., Kawano, Y., Tanaka, M., Kuribayashi, K., Iyama, S., Sato, T., Sato, Y., Takimoto, R., et al. (2006). Ex vivo large-scale generation of human platelets from cord blood CD34+ cells. Stem Cells 24, 2877-2887.
23. Mei, Y., Saha, K., Bogatyrev, S.R., Yang, J., Hook, A.L., Kalcioglu, Z.I., Cho, S.W., Mitalipova, M., Pyzocha, N., Rojas, F., et al. (2010). Combinatorial development of biomaterials for clonal growth of human pluripotent stem cells. Nat. Mater. 9, 768-778.
24. Nakamura, S., Takayama, N., Hirata, S., Seo, H., Endo, H., Ochi, K., Fujita, K., Koike, T., Harimoto, K., Dohda, T., et al. (2014). Expandable megakaryocyte cell lines enable clinically applicable generation of platelets from human induced pluripotent stem cells. Cell Stem Cell 14, 535-548.
25. Nishikawa, S.I., Nishikawa, S., Hirashima, M., Matsuyoshi, N., and Kodama, H. (1998). Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 125, 1747-1757.
26. Nishikii, H., Eto, K., Tamura, N., Hattori, K., Heissig, B., Kanaji, T., Sawaguchi, A., Goto, S., Ware, J., and Nakauchi, H. (2008). Metalloproteinase regulation improves in vitro generation of efficacious platelets from mouse embryonic stem cells. J. Exp. Med. 205, 1917-1927.
27. Oberlin, E., Tavian, M., Blazsek, I., and Péault, B. (2002). Bloodforming potential of vascular endothelium in the human embryo. Development 129, 4147-4157.
28. Ono, Y., Wang, Y., Suzuki, H., Okamoto, S., Ikeda, Y., Murata, M., Poncz, M., and Matsubara, Y. (2012). Induction of functional platelets from mouse and human fibroblasts by p45NF-E2/Maf. Blood 120, 3812-3821.
29. Panzer, S., and Jilma, P. (2011). Methods for testing platelet function for transfusion medicine. Vox Sang. 101, 1-9.
30. Pick, M., Azzola, L., Osborne, E., Stanley, E.G., and Elefanty, A.G. (2013). Generation of megakaryocytic progenitors from human embryonic stem cells in a feeder- and serum-free medium. PLoS ONE 8, e55530.
31. Pineault, N., Boucher, J.F., Cayer, M.P., Palmqvist, L., Boyer, L., Lemieux, R., and Proulx, C. (2008). Characterization of the effects and potential mechanisms leading to increased megakaryocytic differentiation under mild hyperthermia. Stem Cells Dev. 17, 483-493.
32. Proulx, C., Dupuis, N., St-Amour, I., Boyer, L., and Lemieux, R. (2004). Increased megakaryopoiesis in cultures of CD34-enriched cord blood cells maintained at 39 degrees C. Biotechnol. Bioeng. 88, 675-680.
33. Reems, J.A., Pineault, N., and Sun, S. (2010). In vitro megakaryocyte production and platelet biogenesis: state of the art. Transfus. Med. Rev. 24, 33-43.
34. Robert, A., Boyer, L., and Pineault, N. (2011). Glycoprotein Iba receptor instability is associated with loss of quality in platelets produced in culture. Stem Cells Dev. 20, 379-390.
35. Robert, A., Cortin, V., Garnier, A., and Pineault, N. (2012). Megakaryocyte and platelet production from human cord blood stem cells. Methods Mol. Biol. 788, 219-247.
36. Rodin, S., Domogatskaya, A., Ström, S., Hansson, E.M., Chien, K.R., Inzunza, J., Hovatta, O., and Tryggvason, K. (2010). Long-term selfrenewal of human pluripotent stem cells on human recombinant laminin-511. Nat. Biotechnol. 28, 611-615.
37. Salvagiotto, G., Burton, S., Daigh, C.A., Rajesh, D., Slukvin, I.I., and Seay, N.J. (2011). A defined, feeder-free, serum-free system to generate in vitro hematopoietic progenitors and differentiated blood cells from hESCs and hiPSCs. PLoS ONE 6, e17829.
38. Schiffer, C.A. (2001). Diagnosis and management of refractoriness to platelet transfusion. Blood Rev. 15, 175-180.
39. Sone, M., Itoh, H., Yamashita, J., Yurugi-Kobayashi, T., Suzuki, Y., Kondo, Y., Nonoguchi, A., Sawada, N., Yamahara, K., Miyashita, K., et al. (2003). Different differentiation kinetics of vascular progenitor cells in primate and mouse embryonic stem cells. Circulation 107, 2085-2088.
40. Takayama, N., Nishikii, H., Usui, J., Tsukui, H., Sawaguchi, A., Hiroyama, T., Eto, K., and Nakauchi, H. (2008). Generation of functional platelets from human embryonic stem cells in vitro via ESsacs, VEGF-promoted structures that concentrate hematopoietic progenitors. Blood 111, 5298-5306.
41. Takayama, N., Nishimura, S., Nakamura, S., Shimizu, T., Ohnishi, R., Endo, H., Yamaguchi, T., Otsu, M., Nishimura, K., Nakanishi, M., et al. (2010). Transient activation of c-MYC expression is critical for efficient platelet generation from human induced pluripotent stem cells. J. Exp. Med. 207, 2817-2830.
42. Thompson, A., Zhao, Z., Ladd, D., Zimmet, J., and Ravid, K. (1996). A new transgenic mouse model for the study of cell cycle control in megakaryocytes. Stem Cells 14 (Suppl 1), 181-187.
43. Thon, J.N., Macleod, H., Begonja, A.J., Zhu, J., Lee, K.C., Mogilner, A., Hartwig, J.H., and Italiano, J.E., Jr. (2012). Microtubule and cortical forces determine platelet size during vascular platelet production. Nat. Commun. 3, 852.
44. Thon, J.N., Mazutis, L., Wu, S., Sylman, J.L., Ehrlicher, A., Machlus, K.R., Feng, Q., Lu, S., Lanza, R., Neeves, K.B., et al. (2014). Platelet bioreactor-on-a-chip. Blood. Published online July 21, 2014. blood-2014-05-574913.
45. Vodyanik, M.A., Thomson, J.A., and Slukvin, I.I. (2006). Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood 108, 2095-2105.
46. Warren, L., Ni, Y., Wang, J., and Guo, X. (2012). Feeder-free derivation of human induced pluripotent stem cells with messenger RNA. Sci. Rep. 2, 657.