Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression

Journal of Experimental Medicine

Volumn 201, Issue 10, 2005, Pages 1603-1614

  Wang, Lisheng ^a   Menendez, Pablo ^a   Shojaei, Farbod ^a,b   Li, Li ^a   Mazurier, Frederick ^c   Dick, John E ^c   Cerdan, Chantal ^a   Levac, Krysta ^a   Bhatia, Mickie ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CD45 ANTIGEN; HOX PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CLONOGENIC ASSAY; COLONY FORMING UNIT; EMBRYO DEVELOPMENT; GENE CLUSTER; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SOMATIC CELL;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; EMBRYO; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 19344361972     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20041888     Document Type: Article

References (60)

1. Siena, S., M. Bregni, B. Brando, N. Belli, F. Ravagnam, L. Gandola, A.C. Stern, P.M. Lansdorp, G. Bonadonna, and A.M. Gianni. 1991. Flow cytometry for clinical estimation of circulating hematopoietic progenitors for autologous transplantation in cancer patients. Blood. 77: 400-409.
2. Heimfeld, S. 2003. HLA-identical stem cell transplantation: is there an optimal CD34 cell dose? Bone Marrow Transplant. 31:839-845.
3. Wang, L., L. Li, F. Shojaei, P. Menendez, T. Martin, A. Rouleau, and M. Bhatia. 2004. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity. 21:31-41.
4. Wang, J.C., C. Dorrell, C.Y. Ito, T. Inamitsu, G. Guenechea, O.I. Gan, and J.E. Dick. 2001. Normal and leukemic human stem cells assayed in immune-deficient mice. In Hematopoiesis: A Developmental Approach. L.I. Zon, editor. Oxford University Press, New York. 99-118.
5. Perrault, C., N. Ajzenberg, P. Legendre, G. Rastegar-Lari, D. Meyer, J.A. Lopez, and D. Baruch. 1999. Modulation by heparin of the interaction α the Al domain of von Willebrand factor with glycoprotein Ib. Blood. 94:4186-4194.
6. Wang, J., T. Kimura, R. Asada, S. Harada, S. Yokota, Y. Kawamoto, Y. Fujimura, T. Tsuji, S. Ikehara, and Y. Sonoda. 2003. SCID-repopulating cell activity of human cord blood-derived CD34-cells assured by intra-bone marrow injection. Blood. 101:2924-2931.
7. Yahata, T., K. Ando, T. Sato, H. Miyatake, Y. Nakamura, Y. Muguruma, S. Kato, and T. Hotta. 2003. A highly sensitive strategy for SCID-repopulating cell assay by direct injection of primitive human hematopoietic cells into NOD/SCID mice bone marrow. Blood. 101:2905-2913.
8. Mazurier, F., M. Doedens, O.I. Gan, and J.E. Dick. 2003. Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat. Med. 9:959-963.
9. Lapidot, T. 2001. Mechanism of human stem cell migration and repopulation of NOD/SCID and B2mnull NOD/SCID mice. The role of SDF-1/CXCR4 interactions. Ann. N. Y. Acad. Sci. 938:83-95.
10. Plett, P.A., S.M. Frankovitz, and C.M. Orschell. 2003. Distribution of marrow repopulating cells between bone marrow and spleen early after transplantation. Blood. 102:2285-2291.
11. Jetmore, A., P.A. Plett, X. Tong, P.M. Wolber, R. Breese, R. Abonour, C.M. Orschell-Traycoff, and E.F. Srour. 2002. Homing efficiency, cell cycle kinetics, and survival of quiescent and cycling human CD34(+) cells transplanted into conditioned NOD/SCID recipients. Blood. 99:1585-1593.
12. Zannettino, A.C., H.J. Buhring, S. Niutta, S.M. Watt, M.A. Benton, and P.J. Simmons. 1998. The sialomucin CD164 (MGC-24v) is an adhesive glycoprotein expressed by human hematopoietic progenitors and bone marrow stromal cells that serves as a potent negative regulator of hematopoiesis. Blood. 92:2613-2628.
13. Ke, X., L. Jia, H. Jing, Y. Liu, Y. Zhang, and C. Di. 2002. Effects of novel human chemokine-like factor 1 (CKLF1) on bone marrow hematopoietic stem cell/progenitor cell in vitro. Zhonghua Xue Ye Xue Za Zhi. 23:301-303.
14. Besta, F., S. Massberg, K. Brand, E. Muller, S. Page, S. Gruner, M. Lorenz, K. Sadoul, W. Kolanus, E. Lengyel, and M. Gawaz. 2002. Role of beta(3)-endonexin in the regulation of NF-kappaB-dependent expression of urokinase-type plasminogen activator receptor. J. Cell Sci. 115:3879-3888.
15. Xu, Y.X., B.R. Talari, N. Janakiraman, R.A. Chapman, and S.C. Gautam. 1999. Growth factors: production of monocyte chemotactic protein-1 (MCP-1/JE) by bone marrow stromal cells: effect on the migration and proliferation of hematopoietic progenitor cells. Hematology. 4:345-356.
16. Babic, I., A. Schallhorn, P.P. Lindberg, and F.R. Jink. 2000. SHPS-1 induces aggregation of Ba/F3 pro-B cells via an interaction with CD47. J. Immunol. 164:3652-3658.
17. Ruppert, M., S. Aigner, M. Hubbe, H. Yagita, and P. Altevogt. 1995. The L1 adhesion molecule is a cellular ligand for VLA-5. J. Cell Biol. 131:1881-1891.
18. Hayward, C.P., G.E. Rivard, W.H. Kane, J. Drouin, S. Zheng, J.C. Moore, and J.G. Kelton. 1996. An autosomal dominant, qualitative platelet disorder associated with multimerin deficiency, abnormalities in platelet factor V. thrombospondin, von Willebrand factor, and fibrinogen and an epinephrine aggregation defect. Blood. 87:4967-4978.
19. Gerotziafas, G.T., I. Elalamy, C. Lecrubier, J. Lebrazi, M. Mirshahi, F. Potevin, T. Lecompte, and M.M. Samama. 2001. The role of platelet factor 4 in platelet aggregation induced by the antibodies implicated in heparin-induced thrombocytopenia. Blood Coagul. Fibrinolysis. 12:511-520.
20. Friedman, A.D. 2002. Runx1, c-Myb, and C/EBPalpha couple differentiation to proliferation or growth arrest during hematopoiesis. J. Cell. Biochem. 86:624-629.
21. Araki, T., and J. Milbrandt. 2000. Ninjurin2, a novel homophilic adhesion molecule, is expressed in mature sensory and enteric neurons and promotes neurite outgrowth. J. Neurosci. 20:187-195.
22. Araki, T., D.B. Zimonjic, N.C. Popescu, and J. Milbrandt. 1997. Mechanism of homophilic binding mediated by ninjurin, a novel widely expressed adhesion molecule. J. Biol. Chem. 272:21373-21380.
23. Brinck, J., and P. Heldin. 1999. Expression of recombinant hyaluronan synthase (HAS) isoforms in CHO cells reduces cell migration and cell surface CD44. Exp. Cell Res. 252:342-351.
24. Kollet, O., I. Petit, J. Kahn, S. Samira, A. Dar, A. Peled, V. Deutsch, M. Gunetti, W. Piacibello, A. Nagler, and T. Lapidot. 2002. Human CD34(+)CXCR4(-) sorted cells harbor intracellular CXCR4, which can be functionally expressed and provide NOD/SCID repopulation. Blood. 100:2778-2786.
25. Peled, A., I. Petit, O. Kollet, M. Magid, T. Ponomaryov, T. Byk, A. Nagler, H. Ben-Hur, A. Many, L. Shultz, et al. 1999. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science. 283:845-848.
26. Higuchi, Y., A. Yasui, K. Matsuura, and S. Yamamoto. 2002. CD156 transgenic mice. Different responses between inflammatory types. Pathobiology. 70:47-54.
27. Boissy, P., T.R. Lenhard, T. Kirkegaard, J.J. Peschon, R.A. Black, J.M. Delaisse, and M. del Carmen Ovejero. 2003. An assessment of ADAMs in bone cells: absence of TACE activity prevents osteoclast recruitment and the formation of the marrow cavity in developing long bones. FEBS Lett. 553:257-261.
28. Bennin, D.A., A.S. Don, T. Brake, J.L. McKenzie, H. Rosenbaum, L. Ortiz, A.A. DePaoli-Roach, and M.C. Horne. 2002. Cyclin G2 associates with protein phosphatase 2A catalytic and regulatory B′ subunits in active complexes and induces nuclear aberrations and a G1/S phase cell cycle arrest. J. Biol. Chem. 277:27449-27467.
29. Iwabuchi, K., B. Li, H.F. Massa, B.J. Trask, T. Date, and S. Fields. 1998. Stimulation of p53-mediated transcriptional activation by the p53-binding proteins, 53BP1 and 53BP2. J. Biol. Chem. 273:26061-26068.
30. Cheng, T., N. Rodrigues, H. Shen, Y. Yang, D. Dombkowski, M. Sykes, and D.T. Scadden, 2000. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science. 287:1804-1808.
31. Hatada, I., H. Ohashi, Y. Fukushima, Y. Kaneko, M. Inoue, Y. Komoto, A. Okada, S. Ohishi, A. Nabetani, H. Morisaki, et al. 1996. An imprinted gene p57KIP2 is mutated in Beckwith-Wiedemann syndrome. Nat. Genet. 14:171-173.
32. Satoh, Y., I. Matsumura, H. Tanaka, S. Ezoe, H. Sugahara, M. Mizuki, H. Shibayama, E. Ishiko, J. Ishiko, K. Nakajima, and Y. Kanakura. 2004. Roles for c-Myc in self-renewal of hematopoietic stem cells. J. Biol. Chem. 279:24986-24993.
33. Hart, S.M., and L. Foroni. 2002. Core binding factor genes and human leukemia. Haematologica. 87:1307-1323.
34. Ernst, P., J.K. Fisher, W. Avery, S. Wade, D. Foy, and S.J. Korsmeyer. 2004. Definitive hematopoiesis requires the mixed-lineage leukemia gene. Dev. Cell. 6:437-443.
35. Warren, A.J., W.H. Colledge, M.B. Carlton, M.J. Evans, A.J. Smith, and T.H. Rabbitts. 1994. The oncogenic cysteine-rich LIM domain protein rbtn2 is essential tor erythroid development. Cell. 78:45-57.
36. Douglas, K.R., M.L. Brinkmeier, J.A. Kennell, P. Eswara, T.A. Harrison, A.I. Patrianakos, B.S. Sprecher, M.A. Potok, R.H. Lyons Jr., O.A. MacDougald, and S.A. Camper. 2001. Identification of members of the Wnt signaling pathway in the embryonic pituitary gland. Mamm. Genome. 12:843-851.
37. Murdoch, B., K. Chadwick, M. Martin, F. Shojaei, K.V. Shah, L. Gallacher, R.T. Moon, and M. Bhatia. 2003. Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc. Natl. Acad. Sci. USA. 100:3422-3427.
38. Oelgeschlager, M., R. Janknecht, J. Krieg, S. Schreck, and B. Luscher. 1996. Interaction of the co-activator CBP with Myb proteins: effects on Myb-specific transactivation and on the cooperativity with NF-M. EMBO J. 15:2771-2780.
39. Kyba, M., R.C. Perlingeiro, and G.Q. Daley. 2002. HOXB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell. 109:29-37.
40. Menendez P., W.L. Chadwick, L. Li, and M. Bhatia. 2004. Retroviral transduction of hematopoietic cells differentiated from human embryonic stem cell derived CD45negPFV hemogenic precursors. Mol. Ther. 11:1109-1120.
41. Milsom, M.D., R. Duxbury, D. Gagen, R.K. Humphries, M. Schmidt, C. von-Kalle, and L.J. Fairbairn. 2005. Overexpression of HOXB4 confers a myelo-erythroid differentiation delay in vitro. Leukemia. 19:148-153.
42. Schiedlmeier, B., H. Klump, E. Will, G. Arman-Kalcek, Z. Li, Z. Wang, A. Rimek, J. Friel, C. Baum, and W. Ostertag. 2003. High-level ectopic HOXB4 expression confers a profound in vivo competitive growth advantage on human cord blood CD34+ cells, but impairs lymphomyeloid differentiation. Blood. 101:1759-1768.
43. Burt, R.K., L. Verda, D.A. Kim, Y. Oyama, K. Luo, and C. Link. 2004. Embryonic stem cells as an alternate marrow donor source: engraftment without graft-versus-host disease. J. Exp. Med. 199:895-904.
44. Kim, J.H., J.M. Auerbach, J.A. Rodriguez-Gomez, I. Velasco, D. Gavin, N. Lumelsky, S.H. Lee, J. Nguyen, R. Sanchez-Pernaute, K. Bankiewicz, and R. McKay. 2002. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature. 418:50-56.
45. Lumelsky, N., O. Blondel, P. Laeng, I. Velasco, R. Ravin, and R. McKay. 2001. Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science. 292:1389-1394.
46. Rideout, W.M. III, K. Eggan, and R. Jaenisch. 2001. Nuclear cloning and epigenetic reprogramming of the genome. Science. 293:1093-1098.
47. Davidson, A.J., P. Ernst, Y. Wang, M.P. Dekens, P.D. Kingsley, J. Palis, S.J. Korsmeyer, G.Q. Daley, and L.I. Zon. 2003. cdx4 Mutants fail to specify blood progenitors and can be rescued by multiple HOX genes. Nature. 425:300-306.
48. Yuan, Y., H. Shen, D.S. Franklin, D.T. Scadden, and T. Cheng. 2004. In vivo self-renewing divisions of haematopoietic stem cells are increased in the absence of the early G1-phase inhibitor, p181NK4C. Nat. Cell Biol. 6:436-442.
49. Thomson, J.A., J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, and J.M. Jones. 1998. Embryonic stem cell lines derived from human blastocysts. Science. 282:1145-1147.
50. Xu, C., M.S. Inokuma, J. Denham, K. Golds, P. Kundu, J.D. Gold, and M.K. Carpenter. 2001. Feeder-free growth of undifferentiated human embryonic stem cells. Nat. Biotechnol. 19:971-974.
51. Chadwick, K., L. Wang, L. Li, P. Menendez, B. Murdoch, A. Rouleau, and M. Bhatia. 2003. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood. 102:906-915.
52. Bhatia, M., D. Bonnet, U. Kapp, J.C. Wang, B. Murdoch, and J.E. Dick. 1997. Quantitative analysis reveals expansion of human hematopoietic repopulating cells after short-term ex vivo culture. J. Exp. Med. 186:619-624.
53. Eaves, C., C. Miller, E. Conneally, J. Audet, R. Oostendorp, J. Cashman, P. Zandstra, S. Rose-John, J. Piret, and A. Eaves. 1999. Introduction to stem cell biology in vitro. Threshold to the future. Ann. NY Acad. Sci. 872:1-8.
54. Bhatia, M., D. Bonnet, B. Murdoch, O.I. Gan, and J.E. Dick. 1998. A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat. Med. 4:1038-1045.
55. Antonchuk, J., G. Sauvageau, and R.K. Humphries. 2002. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell. 109: 39-45.
56. Brun, A.C., X. Fan, J.M. Bjomsson, R.K. Humphries, and S. Karlsson. 2003. Enforced adenoviral vector-mediated expression of HOXB4 in human umbilical cord blood CD34+ cells promotes myeloid differentiation but not proliferation. Mol. Ther. 8:618-628.
57. Giannola, D.M., W.D. Shlomchik, M. Jegathesan, D. Liebowitz, C.S. Abrams, T. Kadesch, A. Dancis, and S.G. Emerson. 2000. Hematopoietic expression of HOXB4 is regulated in normal and leukemic stem cells through transcriptional activation of the HOXB4 promoter by upstream stimulating factor (USF)-1 and USF-2. J. Exp. Med. 192: 1479-1490.
58. Wiznerowicz, M., A.Z. Fong, R.G. Hawley, and A. Mackiewicz. 1998. Development of a double-copy bicistronic retroviral vector for human gene therapy. Adv. Exp. Med. Biol. 451:441-447.
59. Chadwick, K.S.F., L. Gallagher, M. Bhatia. 2005. Smad7 alters cell fate decisions of human hematopoietic repopulating cells. Blood. 105:1905-1915.
60. Livak, K.J., and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25:402-408.