Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells

Journal of Experimental Medicine

Volumn 189, Issue 7, 1999, Pages 1139-1147

  Bhatia, Mickie ^a,b   Bonnet, Dominique ^c,d,e   Wu, Dongmei ^a,b   Murdoch, Barbara ^c,d   Wrana, Jeff ^c,d   Gallacher, Lisa ^a,b   Dick, John E ^c,d  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e Laboratory of Molecular and Cellular Biology of Hematopoiesis   (United States)

Author keywords

Bone morphogenetic proteins; Ex vivo; Hematopoiesis; Stem cells; Xenotransplantation

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CLONAL ANERGY; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC SYSTEM; HUMAN; HUMAN CELL; MESONEPHROS; PRIORITY JOURNAL; PROTEIN SYNTHESIS REGULATION; SIGNAL TRANSDUCTION; STEM CELL; XENOTRANSPLANTATION;

ACTIVIN RECEPTORS; ADULT; ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL SURVIVAL; CELLS, CULTURED; CHIMERA; FETAL BLOOD; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; INFANT, NEWBORN; MICE; MICE, INBRED NOD; MICE, SCID; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 0033526067     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.7.1139     Document Type: Article

References (42)

1. Metcalf, D. 1993. Hematopoietic regulators: redundancy or subtlety? Blood. 82:3515-3523.
2. Metcalf, D. 1998. Lineage commitment and maturation in hematopoietic cells: the case for extrinsic regulation. Blood. 92:345-347.
3. Ogawa, M. 1993. Differentiation and proliferation of hematopoietic stem cells. Blood. 81:2844-2853.
4. Huber, T.L., and L.I. Zon. 1998. Transcriptional regulation of blood formation during Xenopus development. Semin. Immunol. 10:103-109.
5. Choi, K., M. Kennedy, A. Kazarov, J.C. Papadimitriou, and G. Keller. 1998. A common precursor for hematopoietic and endothelial cells. Development (Camb.). 125:725-732.
6. Yoder, M.C., V.E. Papaioannou, P.P. Breitfeld, and D.A. Williams. 1994. Murine yolk sac endoderm- and mesoderm-derived cell lines support in vitro growth and differentiation of hematopoietic cells. Blood. 83:2436-2443.
7. Rollins-Smith, L.A., and P. Blair. 1990. Contribution of ventral blood island mesoderm to hematopoiesis in postmetamorphic and metamorphosis-inhibited Xenopus laevis. Dev. Biol. 142:178-183.
8. Palis, J., K.E. McGrath, and P.D. Kingsley. 1995. Initiation of hematopoiesis and vasculogenesis in murine yolk sac explants. Blood. 86:156-163.
9. Kelley, C., K. Yee, R. Harland, and L.I. Zon. 1994. Ventral expression of GATA-1 and GATA-2 in the Xenopus embryo defines induction of hematopoietic mesoderm. Dev. Biol. 165:193-205.
10. Medvinsky, A., and E. Dzierzak. 1996. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell. 86:897-906.
11. Yoder, M.C., K. Hiatt, P. Dutt, P. Mukherjee, D.M. Bodine, and D. Orlic. 1997. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity. 7:335-344.
12. Kishimoto, Y., K.H. Lee, L. Zon, M. Hammerschmidt, and S. Schulte-Merker. 1997. The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development (Camb.). 124:4457-4466.
13. Maeno, M., P.E. Mead, C. Kelley, R.H. Xu, H.F. Kung, A. Suzuki, N. Ueno, and L.I. Zon. 1996. The role of BMP-4 and GATA-2 in the induction and differentiation of hematopoietic mesoderm in Xenopus laevis. Blood. 88:1965-1972.
14. Winnier, G., M. Blessing, P.A. Labosky, and B.L. Hogan. 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9:2105-2116.
15. Mishina, Y., A. Suzuki, N. Ueno, and R.R. Behringer. 1995. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9:3027-3037.
16. Sitnicka, E., F.W. Ruscetti, G.V. Priestley, N.S. Wolf, and S.H. Bartelmez. 1996. Transforming growth factor beta 1 directly and reversibly inhibits the initial cell divisions of long-term repopulating hematopoietic stem cells. Blood. 88:82-88.
17. + haemopoietic progenitor cells. Br. J. Haematol. 99:951-958.
18. + peripheral blood progenitors and increases the number of transduced progenitors. Exp. Hematol. 26:374-381.
19. Hatzfeld, J., M.L. Li, E.L. Brown, H. Sookdeo, J.P. Levesque, T. O'Toole, C. Gurney, S.C. Clark, and A. Hatzfeld. 1991. Release of early human hematopoietic progenitors from quiescence by antisense transforming growth factor β1 or Rb oligonucleotides. J. Exp. Med. 174:925-929.
20. Hatzfeld, J., P. Batard, A.A. Cardoso, M.L. Li, B. Panterne, P. Sansilvestri, M. Ginsbourg, J.P. Levesque, and A. Hatzfeld. 1994. Purification and release from quiescence of umbilical cord blood early progenitors reveal their potential to engraft adults. Blood Cells. 20:430-435.
21. Massague, J. 1998. TGF-beta signal transduction. Annu. Rev. Biochem. 67:753-791.
22. Whitman, M. 1998. Smads and early developmental signaling by the TGFβ superfamily. Genes Dev. 12:2445-2462.
23. Wiles, M.V., and B.M. Johansson. 1997. Analysis of factors controlling primary germ layer formation and early hematopoiesis using embryonic stem cell in vitro differentiation. Leukemia. 11(Suppl. 3):454-456.
24. Harland, R.M. 1994. The transforming growth factor beta family and induction of the vertebrate mesoderm: bone morphogenetic proteins are ventral inducers. Prof. Natl. Acad. Sci. USA. 91:10243-10246.
25. Attisano, L., and J.L. Wrana. 1998. Mads and Smads in TGF beta signalling. Curr. Opin. Cell Biol. 10:188-194.
26. Wrana, J., and T. Pawson. 1997. Signal transduction. Mad about SMADs. Nature. 388:28-29.
27. Wrana, J.L., and L. Attisano. 1996. MAD-related proteins in TGF-beta signalling. Trends Genet. 12:493-496.
28. Zhou, S., P. Buckhaults, L. Zawel, F. Bunz, G. Riggins, J. Le Dai, S.E. Kern, K.W. Kinzler, and B. Vogelstein. 1998. Targeted deletion of Smad4 shows it is required for transforming growth factor beta and activin signaling in colorectal cancer cells. Proc. Natl. Acad. Sci. USA. 95:2412-2416.
29. Chen, X., E. Weisberg, V. Fridmacher, M. Watanabe, G. Naco, and M. Whitman. 1997. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature. 389:85-89.
30. Hoodless, P.A., and J.L. Wrana. 1998. Mechanism and function of signaling by the TGF beta superfamily. Curr. Top. Microbiol. Immunol. 228:235-272.
31. Zavadil, J., J. Brezinova, P. Svoboda, Z. Zemanova, and K. Michalova. 1997. Smad5, a tumor suppressor candidate at 5q31.1, is hemizygously lost and not mutated in the retained allele in human leukemia cell line HL60. Leukemia. 11:1187-1192.
32. Zon, L.I. 1995. Developmental biology of hematopoiesis. Blood. 86:2876-2891.
33. Mead, P.E., I.H. Brivanlou, C.M. Kelley, and L.I. Zon. 1996. BMP-4-responsive regulation of dorsal-ventral patterning by the homeobox protein Mix.1. Nature. 382:357-360.
34. Bhatia, M., J.C.Y. Wang, U. Kapp, D. Bonnet, and J.E. Dick. 1997. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Prof. Natl. Acad. Sci. USA. 94:5320-5325.
35. Larochelle, A., J. Vormoor, H. Hanenberg, J.C. Wang, M. Bhatia, T. Lapidot, T. Moritz, B. Murdoch, X.L. Xiao, I. Kato, et al. 1996. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat. Med. 2:1329-1337.
36. Lapidot, T., F. Pflumio, M. Doedens, B. Murdoch, D.E. Williams, and J.E. Dick. 1992. Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in scid mice. Science. 255:1137-1141.
37. Dick, J.E. 1996. Normal and leukemic human stem cells assayed in SCID mice. Semin. Immunol. 8:197-206.
38. 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.
39. Vormoor, J., T. Lapidot, F. Pflumio, G. Risdon, B. Patterson, H.E. Broxmeyer, and J.E. Dick. 1993. High-level multilineage engraftment of human cord blood cells in SCID mice. J. Hematother. 2:215-216.
40. Dewulf, N., K. Verschueren, O. Lonnoy, A. Moren, S. Grimsby, K. Vande Spiegle, K. Miyazono, D. Huylebroeck, and P. Ten Dijke. 1995. Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology. 136: 2652-2663.
41. Kanatsu, M., and S.I. Nishikawa. 1996. In vitro analysis of epiblast tissue potency for hematopoietic cell differentiation. Development (Camb.). 122:823-830.
42. Williams, D.A. 1993. Ex vivo expansion of hematopoietic stem and progenitor cells - robbing Peter to pay Paul? Blood. 81:3169-3172.