Complex and context dependent regulation of hematopoiesis by tgf-β superfamily signaling

Annals of the New York Academy of Sciences

Volumn 1176, Issue , 2009, Pages 55-69

  Söderberg, Sofie Singbrant ^a   Karlsson, Göran ^a   Karlsson, Stefan ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

BMP; Conditional knock out; Hematopoiesis; Hematopoietic stem cell; TGF

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; ENDOGLIN; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

CELL LINEAGE; CELL PROLIFERATION; CONFERENCE PAPER; HEMATOPOIESIS; HUMAN; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 70349833632     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2009.04569.x     Document Type: Conference Paper

References (107)

1. Akala, O.O. & M.F. Clarke. 2006. Hematopoietic stem cell self-renewal. Curr. Opin. Genet. Dev. 16: 496-501.
2. Blank, U., G. Karlsson & S. Karlsson. 2008. Signaling pathways governing stem-cell fate. Blood 111: 492-503.
3. Kawabata, M., T. Imamura & K. Miyazono. 1998. Signal transduction by bone morphogenetic proteins. Cytokine Growth Factor Rev. 9: 49-61. (Pubitemid 28280536)
4. Shi, Y. & J. Massague. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
5. ten Dijke, P. & C.S. Hill. 2004. New insights into TGF-beta-Smad signalling. Trends Biochem. Sci. 29: 265-273.
6. Goumans, M.J. et al. 2002. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. Embo J. 21: 1743-1753.
7. Derynck, R. & Y.E. Zhang. 2003. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-584.
8. Fonsatti, E. et al. 2001. Endoglin: An accessory component of the TGF-beta-binding receptor-complex with diagnostic, prognostic, and bioimmunothera-peutic potential in human malignancies. J. Cell Phys-iol. 188: 1-7.
9. Lebrin, F. et al. 2004. Endoglin promotes endothe-lial cell proliferation and TGF-beta/ALK1 signal transduction. Embo J. 23: 4018-4028.
10. Massague, J., J. Seoane & D. Wotton. 2005. Smad transcription factors. Genes Dev. 19: 2783-2810.
11. Guo, X. & X.F. Wang. 2009. Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res. 19(1): 71-88.
12. Kimura, N. et al. 2000. BMP2-induced apoptosis is mediated by activation of the TAK1-p38 kinase pathway that is negatively regulated by Smad6. J. Biol. Chem. 275: 17647-17652.
13. Ruscetti, F.W., S. Akel & S.H. Bartelmez. 2005. Au-tocrine transforming growth factor-beta regulation of hematopoiesis: many outcomes that depend on the context. Oncogene 24: 5751-5763.
14. Larsson, J. & S. Karlsson. 2005. The role of Smad signaling in hematopoiesis. Oncogene 24: 5676-5692.
15. Fortunel, N.O., A. Hatzfeld & J.A. Hatzfeld. 2000. Transforming growth factor-beta: pleiotropic role in the regulation of hematopoiesis. Blood 96: 2022-2036.
16. Lu, L. et al. 1993. Comparative effects of suppressive cytokines on isolated single CD34(3+) stem/progenitor cells from human bone marrow and umbilical cord blood plated with and without serum. Exp. Hematol. 21: 1442-1446.
17. Batard, P. et al. 2000. TGF-(beta)1 maintains hematopoietic immaturity by a reversible negative control of cell cycle and induces CD34 antigen up-modulation. J. Cell Sci. 113(Pt 3): 383-390.
18. Sitnicka, E. et al. 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.
19. Keller, J.R. et al. 1990. Transforming growth factor beta directly regulates primitive murine hematopoi-etic cell proliferation. Blood 75: 596-602.
20. Jacobsen, S.E. et al. 1991. Bidirectional effects of transforming growth factor beta (TGF-beta) on colony-stimulating factor-induced human myelopoiesis in vitro: differential effects of distinct TGF-beta isoforms. Blood 78: 2239-2247.
21. Ruscetti, F.W. & S.H. Bartelmez. 2001. Transforming growth factor beta, pleiotropic regulator of hematopoietic stem cells: potential physiological and clinical relevance. Int. J. Hematol. 74: 18-25.
22. Weekx, S.F. et al. 1999. Developmentally regulated responsiveness to transforming growth factor-beta is correlated with functional differences between human adult and fetal primitive hematopoietic progenitor cells. Leukemia 13: 1266-1272.
23. Fan, X. et al. 2002. Transient disruption of autocrine TGF-beta signaling leads to enhanced survival and proliferation potential in single primitive human hemopoietic progenitor cells. J. Immunol. 168: 755-762.
24. Goey, H. et al. 1989. Inhibition of early murine hemopoietic progenitor cell proliferation after in vivo locoregional administration of transforming growth factor-beta 1. J. Immunol. 143: 877-880.
25. Kim, S.J. & J. Letterio. 2003. Transforming growth factor-beta signaling in normal and malignant hematopoiesis. Leukemia 17: 1731-1737.
26. Langer, J.C. et al. 2004. Quantitative trait analysis reveals transforming growth factor-beta2 as a positive regulator of early hematopoietic progenitor and stem cell function. J. Exp. Med. 199: 5-14.
27. Massague, J., S.W. Blain & R.S. Lo. 2000. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103: 295-309.
28. Cheng, T. et al. 2001. Transforming growth factor beta 1 mediates cell-cycle arrest of primitive hematopoietic cells independent of p21(Cip1/Waf1) or p27(Kip1). Blood 98: 3643-3649.
29. Scandura, J.M. et al. 2004. Transforming growth factor beta-induced cell cycle arrest of human hematopoietic cells requires p57KIP2 up-regulation. Proc. Natl. Acad. Sci. USA 101: 15231-15236.
30. Yamazaki, S. et al. 2008. TGF-{beta} as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood. 113: 1208.
31. Jacobsen, F.W., T. Stokke & S.E. Jacobsen. 1995. Transforming growth factor-beta potently inhibits the viability-promoting activity of stem cell factor and other cytokines and induces apoptosis of primitive murine hematopoietic progenitor cells. Blood 86: 2957-2966.
32. Jacobsen, S.E. et al. 1991. Transforming growth factor-beta trans-modulates the expression of colony stimulating factor receptors on murine hematopoi-etic progenitor cell lines. Blood 77: 1706-1716.
33. Dubois, C.M. et al. 1990. Transforming growth factor beta is a potent inhibitor of interleukin 1 (IL-1) receptor expression: proposed mechanism of inhibition of IL-1 action. J. Exp. Med. 172: 737-744.
34. Dubois, C.M. et al. 1994. Transforming growth factor-beta regulates c-kit message stability and cell-surface protein expression in hematopoietic progenitors. Blood 83: 3138-3145.
35. Kulkarni, A.B. et al. 1993. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA 90: 770-774.
36. Dickson, M.C. et al. 1995. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121: 1845-1854.
37. Letterio, J.J. et al. 1994. Maternal rescue of transforming growth factor-beta 1 null mice. Science 264: 1936-1938.
38. Shull, M.M. et al. 1992. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359: 693-699.
39. Yaswen, L. et al. 1996. Autoimmune manifestations in the transforming growth factor-beta 1 knockout mouse. Blood 87: 1439-1445.
40. Letterio, J.J. et al. 1996. Autoimmunity associated with TGF-beta1-deficiency in mice is dependent on MHC class II antigen expression. J. Clin. Invest. 98: 2109-2119.
41. Gorelik, L. & R.A. Flavell. 2000. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12: 171-181.
42. Oshima, M., H. Oshima & M.M. Taketo. 1996. TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev. Biol. 179: 297-302.
43. Larsson, J. et al. 2001. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. Embo J. 20: 1663-1673.
44. Park, C. et al. 2004. A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 131: 2749-2762.
45. Larsson, J. et al. 2003. TGF-beta signaling-deficient hematopoietic stem cells have normal self-renewal and regenerative ability in vivo despite increased proliferative capacity in vitro. Blood 102: 3129-3135.
46. Leveen, P. et al. 2002. Induced disruption of the transforming growth factor beta type II receptor gene in mice causes a lethal inflammatory disorder that is transplantable. Blood 100: 560-568.
47. Larsson, J. et al. 2005. Quiescence of hematopoietic stem cells and maintenance of the stem cell pool is not dependent on TGF-beta signaling in vivo. Exp. Hematol. 33: 592-596.
48. Blank, U. et al. 2006. Smad7 promotes self-renewal of hematopoietic stem cells. Blood 108: 4246-4254.
49. Karlsson, G. et al. 2007. Smad4 is critical for self-renewal of hematopoietic stem cells. J. Exp. Med. 204: 467-474.
50. Chadwick, K. et al. 2005. Smad7 alters cell fate decisions of human hematopoietic repopulating cells. Blood 105: 1905-1915.
51. He, W. et al. 2006. Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFbeta pathway. Cell 125: 929-941.
52. Nishita, M. et al. 2000. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403: 781-785.
53. Edlund, S. et al. 2005. Interaction between Smad7 and beta-catenin: importance for transforming growth factor beta-induced apoptosis. Mol. Cell Biol. 25: 1475-1488.
54. Blokzijl, A. et al. 2003. Cross-talk between the Notch and TGF-beta signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J. Cell Biol. 163: 723-728.
55. Wolfraim, L.A. et al. 2004. Loss of Smad3 in acute T-cell lymphoblastic leukemia. N. Engl. J. Med. 351: 552-559.
56. Li, D.Y. et al. 1999. Defective angiogenesis in mice lacking endoglin. Science 284: 1534-1537.
57. Bourdeau, A., D.J. Dumont & M. Letarte. 1999. A murine model of hereditary hemorrhagic telangiec-tasia. J. Clin. Invest. 104: 1343-1351.
58. Arthur, H.M. et al. 2000. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev. Biol. 217: 42-53.
59. McAllister, K.A. et al. 1994. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat. Genet. 8: 345-351.
60. Chen, C.Z. et al. 2002. Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 99: 15468-15473.
61. Chen, C.Z. et al. 2003. The endoglin(positive) sca-1(positive) rhodamine(low) phenotype defines a near-homogeneous population of long-term repopulating hematopoietic stem cells. Immunity 19: 525-533.
62. Rokhlin, O.W. et al. 1995. Differential expression of endoglin on fetal and adult hematopoietic cells in human bone marrow. J. Immunol. 154: 4456-4465.
63. Buhring, H.J. et al. 1991. Endoglin is expressed on a subpopulation of immature erythroid cells of normal human bone marrow. Leukemia 5: 841-847.
64. Pierelli, L. et al. 2000. CD34+/CD105 +cells are enriched in primitive circulating progenitors resid- ing in the G0 phase of the cell cycle and contain all bone marrow and cord blood CD34+/CD38low/-precursors. Br. J. Haematol. 108: 610-620.
65. Lastres, P. et al. 1992. Regulated expression on human macrophages of endoglin, an Arg-Gly-Asp-containing surface antigen. Eur. J. Immunol. 22: 393-397.
66. Schmidt-Weber, C.B. et al. 2005. TGF-{beta} signaling of human T cells is modulated by the ancillary TGF-{beta} receptor endoglin. Int. Immunol. 17: 921-930.
67. Perlingeiro, R.C. 2007. Endoglin is required for he-mangioblast and early hematopoietic development. Development 134: 3041-3048.
68. Cho, S.K. et al. 2001. Expression and function of CD105 during the onset of hematopoiesis from Flk1(+) precursors. Blood 98: 3635-3642.
69. Moody, J.L. et al. 2007. Endoglin is not critical for hematopoietic stem cell engraftment and reconstitution but regulates adult erythroid development. Stem Cells 25: 2809-2819.
70. Johansson, B.M. & M.V. Wiles. 1995. Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoi-etic development. Mol. Cell Biol. 15: 141-151.
71. Pearson, S. et al. 2008. The stepwise specification of embryonic stem cells to hematopoietic fate is driven by sequential exposure to Bmp4, activin A, bFGF and VEGF. Development 135: 1525-1535.
72. Shav-Tal, Y. & D. Zipori. 2002. The role of activin a in regulation of hemopoiesis. Stem Cells 20: 493-500.
73. Maguer-Satta, V. et al. 2001. Expression of FLRG, a novel activin A ligand, is regulated by TGF-beta and during hematopoiesis [corrected]. Exp. Hematol. 29: 301-308.
74. Utsugisawa, T. et al. 2006. A road map toward defin-ing the role of Smad signaling in hematopoietic stem cells. Stem Cells 24: 1128-1136.
75. Shoham, T. et al. 2003. The mesenchymal stroma negatively regulates B cell lymphopoiesis through the expression of activin A. Ann. N. Y. Acad. Sci. 996: 245-260.
76. Maguer-Satta, V. et al. 2003. Regulation of human erythropoiesis by activin A, BMP2, and BMP4, members of the TGFbeta family. Exp. Cell Res. 282: 110-120.
77. Urist, M.R. 1965. Bone: formation by autoinduction. Science 150: 893-899.
78. Hogan, B.L. 1996. Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6: 432-438.
79. Wozney, J.M. 2002. Overview of bone morpho-genetic proteins. Spine 27: S2-S8.
80. Sadlon, T.J., I.D. Lewis & R.J. D'Andrea. 2004. BMP4: its role in development of the hematopoietic system and potential as a hematopoietic growth factor. Stem Cells 22: 457-474.
81. Snyder, A., S.T. Fraser & M.H. Baron. 2004. Bone morphogenetic proteins in vertebrate hematopoi-etic development. J. Cell Biochem. 93: 224-232.
82. Gupta, S. et al. 2006. BMP signaling restricts hemato-vascular development from lateral meso-derm during somitogenesis. Development 133: 2177-2187.
83. Maeno, M. et al. 1996. The role of BMP-4 and GATA-2 in the induction and differentiation of hematopoietic mesoderm in Xenopus laevis. Blood 88: 1965-1972.
84. Huber, T.L. et al. 1998. Cooperative effects of growth factors involved in the induction of hematopoietic mesoderm. Blood 92: 4128-4137.
85. Winnier, G. et al. 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9: 2105-2116.
86. Mishina, Y. et al. 1995. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9: 3027-3037. (Pubitemid 26018138)
87. Chadwick, K. et al. 2003. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102: 906-915.
88. Bhatia, M. et al. 1999. Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells. J. Exp. Med. 189: 1139-1148.
89. Zhang, H. & A. Bradley. 1996. Mice deficient for BMP2 are nonviable and have defects in am-nion/chorion and cardiac development. Development 122: 2977-2986.
90. Beppu, H. et al. 2000. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev. Biol. 221: 249-258.
91. Dale, L. et al. 1992. Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development. Development 115: 573-585.
92. Yang, X. et al. 1999. Angiogenesis defects and mes-enchymal apoptosis in mice lacking SMAD5. Development 126: 1571-1580.
93. Chang, H. et al. 1999. Smad5 knockout mice die at mid-gestation due to multiple embryonic and ex-traembryonic defects. Development 126: 1631-1642.
94. Tremblay, K.D., N.R. Dunn & E.J. Robertson. 2001. Mouse embryos lacking Smad1 signals dis- play defects in extra-embryonic tissues and germ cell formation. Development 128: 3609-3621.
95. Liu, B. et al. 2003. Disruption of Smad5 gene leads to enhanced proliferation of high-proliferative potential precursors during embryonic hematopoiesis. Blood 101: 124-133.
96. McReynolds, L.J. et al. 2007. Smad1 and Smad5 differentially regulate embryonic hematopoiesis. Blood 110: 3881-3890.
97. Zhang, J. et al. 2003. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425: 836-841.
98. Bhardwaj, G. et al. 2001. Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat. Immunol. 2: 172-180.
99. Fuchs, O. et al. 2002. Inhibition of Smad5 in human hematopoietic progenitors blocks erythroid differentiation induced by BMP4. Blood Cells Mol. Dis. 28: 221-233.
100. Detmer, K. & A.N. Walker. 2002. Bone morphogenetic proteins act synergistically with haematopoietic cytokines in the differentiation of haematopoietic progenitors. Cytokine 17: 36-42.
101. Lenox, L.E., J.M. Perry & R.F. Paulson. 2005. BMP4 and Madh5 regulate the erythroid response to acute anemia. Blood 105: 2741-2748.
102. Li, W. et al. 2001. Characterization of the DNA-binding property of Smad5. Biochem. Biophys. Res. Commun. 286: 1163-1169.
103. Bruno, E. et al. 1998. The Smad5 gene is involved in the intracellular signaling pathways that mediate the inhibitory effects of transforming growth factor-beta on human hematopoiesis. Blood 91: 1917-1923.
104. Singbrant, S. et al. 2006. Smad5 is dispensable for adult murine hematopoiesis. Blood 108: 3707-3712.
105. Arnold, S.J. et al. 2006. Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo. Dev. Biol. 296: 104-118.
106. Adolfsson, J. et al. 2005. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121: 295-306.
107. Weissman, I.L. & J.A. Shizuru. 2008. The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoim-mune diseases. Blood 112: 3543-3553.