Top

Published in:

01-01-2011 | Progress in Hematology

Red blood cell production from immortalized progenitor cell line

Authors: Yukio Nakamura, Takashi Hiroyama, Kenichi Miharada, Ryo Kurita

Published in: International Journal of Hematology | Issue 1/2011

Abstract

The supply of transfusable red blood cells (RBCs) is not sufficient in many countries. If immortalized erythroid progenitor cell lines able to produce transfusable RBCs in vitro were established, they would be valuable resources. However, such cell lines have not been established. We have developed a robust method to establish immortalized erythroid progenitor cell lines following the induction of hematopoietic differentiation of mouse embryonic stem (ES) cells and have established many immortalized erythroid progenitor cell lines so far. Although their precise characteristics varied among cell lines, each of these lines could differentiate in vitro into more mature erythroid cells, including enucleated RBCs. Following transplantation of these erythroid cells into mice suffering from acute anemia, the cells proliferated transiently, subsequently differentiated into functional RBCs, and significantly ameliorated the acute anemia. Considering the number of human ES cell lines that have been established so far and the number of induced pluripotent stem cell lines that will be established in future, the intensive testing of a number of these lines for establishing immortalized erythroid progenitor cell lines may allow the establishment of such cell lines similar to the mouse erythroid progenitor cell lines.

Neildez-Nguyen TM, Wajcman H, Marden MC, Bensidhoum M, Moncollin V, Giarratana MC, Kobari L, Thierry D, Douay L. Human erythroid cells produced ex vivo at large scale differentiate into red blood cells in vivo. Nat Biotechnol. 2002;20:467–72.CrossRefPubMed

Giarratana MC, Kobari L, Lapillonne H, Chalmers D, Kiger L, Cynober T, et al. Ex vivo generation of fully mature human red blood cells from hematopoietic stem cells. Nat Biotechnol. 2005;23:69–74.CrossRefPubMed

Miharada K, Hiroyama T, Sudo K, Nagasawa T, Nakamura Y. Efficient enucleation of erythroblasts differentiated in vitro from hematopoietic stem and progenitor cells. Nat Biotechnol. 2006;24:1255–6.CrossRefPubMed

Lee JC, Gimm JA, Lo AJ, Koury MJ, Krauss SW, Mohandas N, et al. Mechanism of protein sorting during erythroblast enucleation: role of cytoskeletal connectivity. Blood. 2004;103:1912–9.CrossRefPubMed

Kingsley PD, Malik J, Fantauzzo KA, Palis J. Yolk sac-derived primitive erythroblasts enucleate during mammalian embryogenesis. Blood. 2004;104:19–25.CrossRefPubMed

Ohneda O, Bautch VL. Murine endothelial cells support fetal liver erythropoiesis and myelopoiesis via distinct interactions. Brit J Haematol. 1997;98:798–808.CrossRef

Yanai N, Sato Y, Obinata M. A new type-II membrane protein in erythropoietic organs enhances erythropoiesis. Leukemia. 1997;11:484–5.PubMed

Hanspal M, Smockova Y, Uong Q. Molecular identification and functional characterization of a novel protein that mediates the attachment of erythroblasts to macrophages. Blood. 1998;92:2940–50.PubMed

Iavarone A, King ER, Dai XM, Leone G, Stanley ER, Lasorella A. Retinoblastoma promotes definitive erythropoiesis by repressing Id2 in fetal liver macrophages. Nature. 2004;432:1040–5.CrossRefPubMed

10.

Spike BT, Dirlam A, Dibling BC, Marvin J, Williams BO, Jacks T, et al. The Rb tumor suppressor is required for stress erythropoiesis. EMBO J. 2004;23:4319–29.CrossRefPubMed

11.

Yoshida H, Kawane K, Koike M, Mori Y, Uchiyama Y, Nagata S. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature. 2005;437:754–8.CrossRefPubMed

12.

Hebiguchi M, Hirokawa M, Guo YM, Saito K, Wakui H, Komatsuda A, et al. Dynamics of human erythroblast enucleation. Int J Hematol. 2008;88:498–507.CrossRefPubMed

13.

Keller G, Kennedy M, Papayannopoulou T, Wiles MV. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol Cell Biol. 1993;13:473–86.PubMed

14.

Nakano T, Kodama H, Honjo T. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science. 1994;265:1098–101.CrossRefPubMed

15.

Nakano T, Kodama H, Honjo T. In vitro development of primitive and definitive erythrocytes from different precursors. Science. 1996;272:722–4.CrossRefPubMed

16.

Carotta S, Pilat S, Mairhofer A, Schmidt U, Dolznig H, Steinlein P, et al. Directed differentiation and mass cultivation of pure erythroid progenitors from mouse embryonic stem cells. Blood. 2004;104:1873–80.CrossRefPubMed

17.

Li F, Lu S, Vida L, Thomson JA, Honig GR. Bone morphogenetic protein 4 induces efficient hematopoietic differentiation of rhesus monkey embryonic stem cells in vitro. Blood. 2001;98:335–42.CrossRefPubMed

18.

Umeda K, Heike T, Yoshimoto M, Shiota M, Suemori H, Luo HY, et al. Development of primitive and definitive hematopoiesis from nonhuman primate embryonic stem cells in vitro. Development. 2004;131:1869–79.CrossRefPubMed

19.

Kurita R, Sasaki E, Yokoo T, Hiroyama T, Takasugi K, Imoto H, et al. Tal1/Scl gene transduction using a lentiviral vector stimulates highly efficient hematopoietic cell differentiation from common marmoset (Callithrix jacchus) embryonic stem cells. Stem Cells. 2006;24:2014–22.CrossRefPubMed

20.

Kaufman DS, Hanson ET, Lewis RL, Auerbach R, Thomson JA. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci USA. 2001;98:10716–21.CrossRefPubMed

21.

Chadwick K, Wang L, Li L, Menendez P, Murdoch B, Rouleau A, et al. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood. 2003;102:906–15.CrossRefPubMed

22.

Cerdan C, Rouleau A, Bhatia M. VEGF-A165 augments erythropoietic development from human embryonic stem cells. Blood. 2004;103:2504–12.CrossRefPubMed

23.

Vodyanik MA, Bork JA, Thomson JA, Slukvin II. Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood. 2005;105:617–26.CrossRefPubMed

24.

Wang L, Li L, Menendez P, Cerdan C, Bhatia M. Human embryonic stem cells maintained in the absence of mouse embryonic fibroblasts or conditioned media are capable of hematopoietic development. Blood. 2005;105:4598–603.CrossRefPubMed

25.

Olivier EN, Qiu C, Velho M, Hirsch RE, Bouhassira EE. Large-scale production of embryonic red blood cells from human embryonic stem cells. Exp Hematol. 2006;34:1635–42.CrossRefPubMed

26.

Hiroyama T, Miharada K, Aoki N, Fujioka T, Sudo K, Danjo I, et al. Long lasting in vitro hematopoiesis derived from primate embryonic stem cells. Exp Hematol. 2006;34:760–9.CrossRefPubMed

27.

Lu SJ, Feng Q, Park JS, Vida L, Lee BS, Strausbauch M, et al. Biologic properties and enucleation of red blood cells from human embryonic stem cells. Blood. 2008;112:4475–84.CrossRefPubMed

28.

Lansdorp PM. Role of telomerase in hematopoietic stem cells. Ann NY Acad Sci. 2005;1044:220–7.CrossRefPubMed

29.

Hiroyama T, Miharada K, Sudo K, Danjo I, Aoki N, Nakamura Y. Establishment of mouse embryonic stem cell-derived erythroid progenitor cell lines able to produce functional red blood cells. PLoS One. 2008;3:e1544.

30.

Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72.CrossRefPubMed

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.CrossRefPubMed

32.

Fujioka T, Shimizu N, Yoshino K, Miyoshi H, Nakamura Y. Establishment of induced pluripotent stem cells from human neonatal tissues. Hum Cell. 2010;23:113–8.CrossRefPubMed

33.

Vogel G. Ready or not? Human ES cells head toward the clinic. Science. 2005;308:1534–8.CrossRefPubMed

34.

Hentze H, Graichen R, Colman A. Cell therapy and the safety of embryonic stem cell-derived grafts. Trends Biotechnol. 2007;25:24–32.CrossRefPubMed

35.

Schuldiner M, Itskovitz-Eldor J, Benvenisty N. Selective ablation of human embryonic stem cells expressing a “suicide” gene. Stem Cells. 2003;21:257–65.CrossRefPubMed

36.

Drukker M, Benvenisty N. The immunogenicity of human embryonic stem-derived cells. Trends Biotechnol. 2004;22:136–41.CrossRefPubMed

37.

Boyd AS, Higashi Y, Wood KJ. Transplanting stem cells: potential targets for immune attack. Modulating the immune response against embryonic stem cell transplantation. Adv Drug Deliv Rev. 2005;57:1944–69.CrossRefPubMed

Title: Red blood cell production from immortalized progenitor cell line
Authors: Yukio Nakamura
Takashi Hiroyama
Kenichi Miharada
Ryo Kurita
Publication date: 01-01-2011
Publisher: Springer Japan
Published in: International Journal of Hematology / Issue 1/2011
Print ISSN: 0925-5710
Electronic ISSN: 1865-3774
DOI: https://doi.org/10.1007/s12185-010-0742-2

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2011

Guest editorial: the seven wonders of erythropoiesis

Flow cytometric analysis of de novo acute myeloid leukemia in childhood: report from the Japanese Pediatric Leukemia/Lymphoma Study Group

Down-regulating the expression of IL-3Rβ interfered with the proliferation, not differentiation in NB4 cells

Analysis of bacteremia/fungemia and pneumonia accompanying acute myelogenous leukemia from 1987 to 2001 in the Japan Adult Leukemia Study Group

The molecular basis of iron overload disorders and iron-linked anemias

Quality of long-term cryopreserved umbilical cord blood units for hematopoietic cell transplantation

Keynote webinar | Spotlight on antibody–drug conjugates in cancer