Hematopoietic stem cell: Self-renewal versus differentiation

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 2, Issue 6, 2010, Pages 640-653

  Seita, Jun ^a   Weissman, Irving L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA;

CYTOKINE; MEMBRANE ANTIGEN;

ANIMAL; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION PROFILING; GENETICS; HEMATOPOIETIC STEM CELL; HUMAN; METABOLISM; MOUSE; REVIEW;

ANIMALS; ANTIGENS, SURFACE; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION PROFILING; HEMATOPOIETIC STEM CELLS; HUMANS; MICE;

EID: 78751582939     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.86     Document Type: Review

References (143)

1. Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993, 81:2844-2853.
2. Rossi DJ, Seita J, Czechowicz A, Bhattacharya D, Bryder D, Weissman IL. Hematopoietic stem cell quiescence attenuates DNA damage response and permits DNA damage accumulation during aging. Cell Cycle 2007, 6:2371-2376.
3. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
4. Weissman I. Stem cell research: paths to cancer therapies and regenerative medicine. JAMA 2005, 294:1359-1366.
5. Becker AJ, Mc CE, Till JE. Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 1963, 197:452-454.
6. Siminovitch L, McCulloch EA, Till JE. The distribution of colony-forming cells among spleen colonies. J Cell Physiol 1963, 62:327-336.
7. Till JE, Mc CE. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 1961, 14:213-222.
8. Wu AM, Till JE, Siminovitch L,McCulloch EA. Cytological evidence for a relationship between normal hemotopoietic colony-forming cells and cells of the lymphoid system. J Exp Med 1968, 127:455-464.
9. Na Nakorn T, Traver D, Weissman IL, Akashi K. Myeloerythroid-restricted progenitors are sufficient to confer radioprotection and provide the majority of day 8 CFU-S. J Clin Invest. 2002, Jun; 109(12):1579-85.
10. Muller-Sieburg CE, Whitlock CA, Weissman IL. Isolation of two early B lymphocyte progenitors from mouse marrow: a committed pre-pre-B cell and a clonogenic Thy-1-lo hematopoietic stem cell. Cell 1986, 44:653-662.
11. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science 1988, 241:58-62.
12. Uchida N, Weissman IL. Searching for hematopoietic stem cells: evidence that Thy-1.1lo Lin- Sca-1+ cells are the only stem cells in C57BL/Ka-Thy-1.1 bone marrow. J Exp Med 1992, 175:175-184.
13. Ikuta K, Weissman IL. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci U S A 1992, 89:1502-1506.
14. Smith LG, Weissman IL, Heimfeld S. Clonal analysis of hematopoietic stem-cell differentiation in vivo. Proc Natl Acad Sci U S A 1991, 88:2788-2792.
15. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994, 1:661-673.
16. OsawaM,Hanada K,HamadaH,NakauchiH. Longterm lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996, 273:242-245.
17. Uchida N, Tsukamoto A, He D, Friera AM, Scollay R, Weissman IL. High doses of purified stem cells cause early hematopoietic recovery in syngeneic and allogeneic hosts. J Clin Invest 1998, 101:961-966.
18. Christensen JL, Weissman IL. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci U S A 2001, 98:14541-14546.
19. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
20. Adolfsson J, Mansson R, Buza-Vidas N, Hultquist A, Liuba K, Jensen CT, et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythromegakaryocytic potential a revised road map for adult blood lineage commitment. Cell 2005, 121:295-306.
21. Arinobu Y, Mizuno S, Chong Y, Shigematsu H, Iino T, Iwasaki H, et al. Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 2007, 1:416-427.
22. Forsberg EC, Serwold T, Kogan S, Weissman IL, Passegue E. New evidence supporting megakaryocyteerythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell 2006, 126:415-426.
23. Serwold T, Ehrlich LI, Weissman IL. Reductive isolation from bone marrow and blood implicates common lymphoid progenitors as the major source of thymopoiesis. Blood 2009, 113:807-815.
24. Karsunky H, Inlay MA, Serwold T, Bhattacharya D, Weissman IL. Flk2+ common lymphoid progenitors possess equivalent differentiation potential for the B and T lineages. Blood 2008, 111:5562-5570.
25. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997, 91:661-672.
26. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000, 404:193-197.
27. Pronk CJ, Rossi DJ,Mansson R, Attema JL,Norddahl GL, Chan CK, et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell 2007, 1:428-44
28. Traver D, Akashi K, Manz M, Merad M, Miyamoto T, Engleman EG, et al. Development of CD8alphapositive dendritic cells from a common myeloid progenitor. Science 2000, 290:2152-2154.
29. Manz MG, Traver D, Akashi K,Merad M, Miyamoto T, Engleman EG, et al. Dendritic cell development from common myeloid progenitors. Ann N Y Acad Sci 2001, 938:167-173; discussion 173-174.
30. Manz MG, Traver D, Miyamoto T, Weissman IL, Akashi K. Dendritic cell potentials of early lymphoid and myeloid progenitors. Blood 2001, 97:3333-3341.
31. Baum CM,Weissman IL, Tsukamoto AS, Buckle AM, Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A 1992, 89:2804-2808.
32. McCune JM, Namikawa R, Kaneshima H, Shultz LD, Lieberman M, Weissman IL. The SCID-hu mouse: murine model for the analysis of human hematolymphoid differentiation and function. Science 1988, 241:1632-1639.
33. Civin CI, Strauss LC, Brovall C, Fackler MJ, Schwartz JF, Shaper JH. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J Immunol 1984, 133:157-165.
34. DiGiusto D, Chen S, Combs J,Webb S, Namikawa R, Tsukamoto A, et al. Human fetal bone marrow early progenitors for T, B, and myeloid cells are found exclusively in the population expressing high levels of CD34. Blood 1994, 84:421-432.
35. Krause DS, Fackler MJ, Civin CI, May WS. CD34: structure, biology, and clinical utility. Blood 1996, 87:1-13.
36. Hao QL, Thiemann FT, Petersen D, Smogorzewska EM, Crooks GM. Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progenitor population. Blood 1996, 88:3306-3313.
37. Huang S, Terstappen LW. Lymphoid and myeloid differentiation of single human CD34+, HLA-DR+, CD38- hematopoietic stem cells. Blood 1994, 83:1515-1526.
38. Miller JS, McCullar V, Punzel M, Lemischka IR, Moore KA. Single adult human CD34(+)/Lin-/CD38(-) progenitors give rise to natural killer cells, B-lineage cells, dendritic cells, and myeloid cells. Blood 1999, 93:96-106.
39. Uchida N, Sutton RE, Friera AM, He D, Reitsma MJ, Chang WC, et al. HIV, but not murine leukemia virus, vectors mediate high efficiency gene transfer into freshly isolated G0/G1 human hematopoietic stem cells. Proc Natl Acad Sci U S A 1998, 95:11939-11944.
40. Petzer AL, Hogge DE, Landsdorp PM, Reid DS, Eaves CJ. Self-renewal of primitive human hematopoietic cells (long-term-culture-initiating cells) in vitro and their expansion in defined medium. Proc Natl Acad Sci U S A 1996, 93:1470-1474.
41. Bhatia M, Wang JC, Kapp U, Bonnet D, Dick JE. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A 1997, 94:5320-5325.
42. Larochelle A, Vormoor J, Hanenberg H, Wang JC, Bhatia M, Lapidot T, et al. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat Med 1996, 2:1329-1337.
43. MichalletM, Philip T, Philip I, Godinot H, Sebban C, Salles G, et al. Transplantation with selected autologous peripheral blood CD34+Thy1+ hematopoietic stem cells (HSCs) in multiple myeloma: impact of HSC dose on engraftment, safety, and immune reconstitution. Exp Hematol 2000, 28:858-870.
44. Negrin RS, Atkinson K, Leemhuis T, Hanania E, Juttner C, Tierney K, et al. Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with metastatic breast cancer. Biol Blood Marrow Transplant 2000, 6:262-271.
45. Vose JM, Bierman PJ, Lynch JC, Atkinson K, Juttner C, Hanania CE, et al. Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with recurrent indolent non-Hodgkin's lymphoma. Biol Blood Marrow Transplant 2001, 7:680-687.
46. Guenechea G, Gan OI, Dorrell C, Dick JE. Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nat Immunol 2001, 2:75-82.
47. Mazurier F, Gan OI, McKenzie JL, Doedens M, Dick JE. Lentivector-mediated clonal tracking reveals intrinsic heterogeneity in the human hematopoietic stem cell compartment and culture-induced stem cell impairment. Blood 2004, 103:545-552.
48. McKenzie JL, Gan OI, Doedens M, Wang JC, Dick JE. Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment. Nat Immunol 2006, 7:1225-1233.
49. Majeti R, Park CY, Weissman IL. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 2007, 1:635-645.
50. Fritsch G, Buchinger P, Printz D, Fink FM, Mann G, Peters C, et al. Rapid discrimination of early CD34+ myeloid progenitors using CD45-RA analysis. Blood 1993, 81:2301-2309.
51. Galy A, Travis M, Cen D, Chen B. Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 1995, 3:459-473.
52. Kimura T, Sakabe H, Tanimukai S, Abe T, Urata Y, Yasukawa K, et al. Simultaneous activation of signals through gp130, c-kit, and interleukin-3 receptorpromotes a trilineage blood cell production in the absence of terminally acting lineage-specific factors. Blood 1997, 90:4767-4778.
53. Manz MG, Miyamoto T, Akashi K, Weissman IL. Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci U S A 2002, 99:11872-11877.
54. Russell ES. Analysis of pleiotropism at the W-locus in the mouse; relationship between the effects of W and Wv substitution on hair pigmentation and on erythrocytes. Genetics 1949, 34:708-723.
55. Sarvella PA, Russell LB. Steel, a new dominant gene in the mouse. J Hered 1956, 47:123-128.
56. Bernstein SE, Russell ES, Keighley G. Two hereditary mouse anemias deficient in response to erythropoietin. Ann N Y Acad Sci 1968, 149:475-485.
57. Ebbe S, Phalen E, Stohlman F, Jr. Abnormalities of megakaryocytes in S1-S1d mice. Blood 1973, 42:865-871.
58. Ebbe S, Phalen E, Stohlman F, Jr. Abnormalities of megakaryocytes in W-WV mice. Blood 1973, 42:857-864.
59. Ruscetti FW, Boggs DR, Torok BJ, Boggs SS. Reduced blood and marrow neutrophils and granulocytic colony-forming cells in S1/S1d mice. Proc Soc Exp Biol Med 1976, 152:398-402.
60. Kitamura Y, Go S. Decreased production of mast cells in S1/S1d anemic mice. Blood 1979, 53:492-497.
61. Kitamura Y, Go S, Hatanaka K. Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood 1978, 52:447-452.
62. Geissler EN, Russell ES. Analysis of the hematopoietic effects of new dominant spotting (W) mutations of the mouse. II. Effects on mast cell development. Exp Hematol 1983, 11:461-466.
63. Fujita J, Onoue H, Ebi Y, Nakayama H, Kanakura Y. In vitro duplication and in vivo cure of mast-cell deficiency of Sl/Sld mutant mice by cloned 3T3 fibroblasts. Proc Natl Acad Sci U S A 1989, 86:2888-2891.
64. Mayer TC, Green MC. An experimental analysis of the pigment defect caused by mutations at the W and S1 loci in mice. Dev Biol 1968, 18:62-75.
65. Russell ES, Bernstein SE. Proof of whole-cell implant in therapy ofW-series anemia. Arch Biochem Biophys 1968, 125:594-597.
66. Jarboe DL, Huff TF. The mast cell-committed progenitor. II. W/Wv mice do not make mast cell-committed progenitors and S1/S1d fibroblasts do not support development of normal mast cell-committed progenitors. J Immunol 1989, 142:2418-2423.
67. Nocka K,Majumder S, Chabot B, Ray P, Cervone M, Bernstein A, et al. Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice-evidence for an impaired c-kit kinase in mutant mice. Genes Dev 1989, 3:816-826.
68. Reith AD, Rottapel R, Giddens E, Brady C, Forrester L, Bernstein A. W mutant mice with mild or severe developmental defects contain distinct point mutations in the kinase domain of the c-kit receptor. Genes Dev 1990, 4:390-400.
69. Zsebo KM, Williams DA, Geissler EN, Broudy VC, Martin FH, Atkins HL, et al. Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 1990, 63:213-224.
70. Whitlock CA, Tidmarsh GF, Muller-Sieburg C, Weissman IL. Bone marrow stromal cell lines with lymphopoietic activity express high levels of a pre-B neoplasia-associated molecule. Cell 1987, 48:1009-1021.
71. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003, 425:836-841.
72. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846.
73. Adolfsson J, Borge OJ, Bryder D, Theilgaard-Monch K, Astrand-Grundstrom I, Sitnicka E, et al. Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity. Immunity 2001, 15:659-669.
74. Buza-Vidas N, Antonchuk J, Qian H, Mansson R, Luc S, Zandi S, et al. Cytokines regulate postnatal hematopoietic stem cell expansion: opposing roles of thrombopoietin and LNK. Genes Dev 2006, 20:2018-2023.
75. Kimura S, Roberts AW, Metcalf D, Alexander WS. Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc Natl Acad Sci U S A 1998, 95:1195-1200.
76. Solar GP, Kerr WG, Zeigler FC, Hess D, Donahue C, de Sauvage FJ, et al. Role of c-mpl in early hematopoiesis. Blood 1998, 92:4-10.
77. Yang L, Bryder D, Adolfsson J, Nygren J, Mansson R, Sigvardsson M, et al. Identification of Lin(-)Sca1(+)kit(+) CD34(+)Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 2005, 105:2717-2723.
78. Terskikh AV, Miyamoto T, Chang C, Diatchenko L, Weissman IL. Gene expression analysis of purified hematopoietic stem cells and committed progenitors. Blood 2003, 102:94-101.
79. Seita J, Ema H, Ooehara J, Yamazaki S, Tadokoro Y, Yamasaki A, et al. Lnk negatively regulates selfrenewal of hematopoietic stem cells by modifying thrombopoietin-mediated signal transduction. Proc Natl Acad Sci U S A 2007, 104:2349-2354
80. Takaki S, Sauer K, Iritani BM, Chien S, Ebihara Y, Tsuji K, et al. Control of B cell production by the adaptor protein lnk. Definition Of a conserved family of signal-modulating proteins. Immunity 2000, 13:599-609.
81. Tong W, Zhang J, Lodish HF. Lnk inhibits erythropoiesis and Epo-dependent JAK2 activation and downstream signaling pathways. Blood 2005, 105:4604-4612.
82. Velazquez L, Cheng AM, Fleming HE, Furlonger C, Vesely S, Bernstein A, et al. Cytokine signaling and hematopoietic homeostasis are disrupted in Lnkdeficient mice. J Exp Med 2002, 195:1599-1611.
83. Ema H, Sudo K, Seita J, Matsubara A, Morita Y, Osawa M, et al. Quantification of self-renewal capacity in single hematopoietic stem cells from normal and Lnk-deficient mice. Dev Cell 2005, 8:907-914.
84. de Sauvage FJ, Carver-Moore K, Luoh SM, Ryan A, Dowd M, Eaton DL, et al. Physiological regulation of early and late stages of megakaryocytopoiesis by thrombopoietin. J Exp Med 1996, 183:651-656.
85. Suri C, Jones PF, Patan S, Bartunkova S,Maisonpierre PC, Davis S, et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996, 87:1171-1180.
86. Mach N, Lantz CS, Galli SJ, Reznikoff G, Mihm M, Small C, et al. Involvement of interleukin-3 in delayed-type hypersensitivity. Blood 1998, 91: 778-783.
87. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994, 368:339-342.
88. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992, 359:693-699.
89. Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 1995, 121:1845-1854.
90. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, et al. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 1997, 124:2659-2670.
91. KaartinenV,Voncken JW, Shuler C, WarburtonD, Bu D, Heisterkamp N, et al. Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 1995, 11:415-421.
92. Gurney AL, Carver-Moore K, de Sauvage FJ, Moore MW. Thrombocytopenia in c-mpl-deficient mice. Science 1994, 265:1445-1447.
93. Dumont DJ, Gradwohl G, Fong GH, Puri MC, Gertsenstein M, Auerbach A, et al.Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev 1994, 8:1897-1909.
94. Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M, et al. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 1995, 376:70-74.
95. Ichihara M, Hara T, Takagi M, Cho LC, Gorman DM, Miyajima A. Impaired interleukin-3 (IL-3) response of the A/J mouse is caused by a branch point deletion in the IL-3 receptor alpha subunit gene. EMBO J 1995, 14:939-950.
96. Nishinakamura R, Miyajima A, Mee PJ, Tybulewicz VL, Murray R. Hematopoiesis in mice lacking the entire granulocyte-macrophage colony-stimulating factor/interleukin-3/interleukin-5 functions. Blood 1996, 88:2458-2464.
97. Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, et al. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci U S A 1996, 93:407-411.
98. Nandurkar HH, Robb L, Tarlinton D, Barnett L, Kontgen F, Begley CG. Adultmicewith targetedmutation of the interleukin-11 receptor (IL11Ra) display normal hematopoiesis. Blood 1997, 90:2148-2159.
99. Larsson J, Goumans MJ, Sjostrand LJ, van Rooijen MA, Ward D, Leveen P, et al. Abnormal angiogenesis but intact hematopoietic potential in TGFbeta type I receptor-deficient mice. EMBO J 2001, 20:1663-1673.
100. Oshima M, Oshima H, Taketo MM. TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol 1996, 179:297-302.
101. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, et al. Wnt proteins are lipidmodified and can act as stem cell growth factors. Nature 2003, 423:448-452.
102. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, et al. A role for Wnt signalling in selfrenewal of haematopoietic stem cells. Nature 2003, 423:409-414.
103. Kirstetter P, Anderson K, Porse BT, Jacobsen SE, Nerlov C. Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 2006, 7:1048-1056.
104. Scheller M, Huelsken J, Rosenbauer F, Taketo MM, Birchmeier W, Tenen DG, et al. Hematopoietic stem cell and multilineage defects generated by constitutive beta-catenin activation. Nat Immunol 2006, 7:1037-1047.
105. CobasM,Wilson A, Ernst B,Mancini SJ,MacDonald HR, Kemler R, et al. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 2004, 199:221-229.
106. Jeannet G, Scheller M, Scarpellino L, Duboux S, Gardiol N, Back J, et al. Long-term, multilineage hematopoiesis occurs in the combined absence of beta-catenin and gamma-catenin. Blood 2008, 111:142-149.
107. Koch U, Wilson A, Cobas M, Kemler R, Macdonald HR, Radtke F. Simultaneous loss of beta- and gamma-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 2008, 111:160-164.
108. Zhao C, Blum J, Chen A, Kwon HY, Jung SH, Cook JM, et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 2007, 12:528-541.
109. Batard P, Monier MN, Fortunel N, Ducos K, Sansilvestri-Morel P, Phan T, et al. TGF-(beta)1maintains hematopoietic immaturity by a reversible negative control of cell cycle and induces CD34 antigen up-modulation. J Cell Sci 2000, 113:383-390.
110. Garbe A, Spyridonidis A, Mobest D, Schmoor C, Mertelsmann R, Henschler R. Transforming growth factor-beta 1 delays formation of granulocytemacrophage colony-forming cells, but spares more primitive progenitors during ex vivo expansion of CD34+ haemopoietic progenitor cells. Br J Haematol 1997, 99:951-958.
111. Sitnicka E, Ruscetti FW, Priestley GV, Wolf NS, Bartelmez SH. Transforming growth factor beta 1 directly and reversibly inhibits the initial cell divisions of long-term repopulating hematopoietic stem cells. Blood 1996, 88:82-88.
112. Fortunel N, Batard P, Hatzfeld A, Monier MN, Panterne B, Lebkowski J, et al. High proliferative potential-quiescent cells: a working model to study primitive quiescent hematopoietic cells. J Cell Sci 1998, 111:1867-1875.
113. Hatzfeld J, Li ML, Brown EL, Sookdeo H, Levesque JP, O'Toole T, et al. Release of early human hematopoietic progenitors from quiescence by antisense transforming growth factor beta 1 or Rb oligonucleotides. J Exp Med 1991, 174:925-929.
114. Soma T, Yu JM, Dunbar CE. Maintenance of murine long-term repopulating stem cells in ex vivo culture is affected by modulation of transforming growth factorbeta but not macrophage inflammatory protein-1 alpha activities. Blood 1996, 87:4561-4567.
115. Cheng T, Shen H, Rodrigues N, Stier S, Scadden DT. Transforming growth factor beta 1 mediates cellcycle arrest of primitive hematopoietic cells independent of p21(Cip1/Waf1) or p27(Kip1). Blood 2001, 98:3643-3649.
116. Dao MA, Hwa J, Nolta JA. Molecular mechanism of transforming growth factor beta-mediated cell-cycle modulation in primary human CD34(+) progenitors. Blood 2002, 99:499-506.
117. Dao MA, Taylor N, Nolta JA. Reduction in levels of the cyclin-dependent kinase inhibitor p27(kip-1) coupled with transforming growth factor beta neutralization induces cell-cycle entry and increases retroviral transduction of primitive human hematopoietic cells. Proc Natl Acad Sci U S A 1998, 95:13006-13011.
118. Dubois CM, Ruscetti FW, Palaszynski EW, Falk LA, Oppenheim JJ, Keller JR. 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 1990, 172:737-744.
119. Dubois CM, Ruscetti FW, Stankova J, Keller JR. Transforming growth factor-beta regulates c-kit message stability and cell-surface protein expression in hematopoietic progenitors. Blood 1994, 83:3138-3145.
120. Ducos K, Panterne B, Fortunel N, Hatzfeld A,Monier MN, Hatzfeld J. p21(cip1) mRNA is controlled by endogenous transforming growth factor-beta1 in quiescent human hematopoietic stem/progenitor cells. J Cell Physiol 2000, 184:80-85.
121. Jacobsen SE, Keller JR, Ruscetti FW, Kondaiah P, Roberts AB, Falk LA. Bidirectional effects of transforming growth factor beta (TGF-beta) on colonystimulating factor-induced human myelopoiesis in vitro: differential effects of distinct TGF-beta isoforms. Blood 1991, 78:2239-2247.
122. Jacobsen SE, Ruscetti FW, Dubois CM, Lee J, Boone TC,Keller JR. Transforming growth factor-beta transmodulates the expression of colony stimulating factor receptors on murine hematopoietic progenitor cell lines. Blood 1991, 77:1706-1716.
123. Sansilvestri P, Cardoso AA, Batard P, Panterne B, Hatzfeld A, Lim B, et al. Early CD34high cells can be separated into KIThigh cells in which transforming growth factor-beta (TGF-beta) downmodulates c-kit and KITlow cells in which anti-TGF-beta upmodulates c-kit. Blood 1995, 86:1729-1735.
124. Scandura JM, Boccuni P, Massague J, Nimer SD. Transforming growth factor beta-induced cell cycle arrest of human hematopoietic cells requires p57KIP2 up-regulation. Proc Natl Acad Sci U S A 2004, 101:15231-15236.
125. Yamazaki S, Iwama A, Takayanagi S, Eto K, Ema H, Nakauchi H. TGF-beta as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood 2009, 113:1250-1256.
126. Larsson J, Blank U, Helgadottir H, Bjornsson JM, Ehinger M, Goumans MJ, et al. TGF-beta signalingdeficient hematopoietic stem cells have normal selfrenewal and regenerative ability in vivo despite increased proliferative capacity in vitro. Blood 2003, 102:3129-3135.
127. Dumont DJ, Yamaguchi TP, Conlon RA, Rossant J, Breitman ML. tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene 1992, 7:1471-1480.
128. Iwama A, Hamaguchi I, Hashiyama M, Murayama Y, Yasunaga K, Suda T. Molecular cloning and characterization of mouse TIE and TEK receptor tyrosine kinase genes and their expression in hematopoietic stem cells. Biochem Biophys Res Commun 1993, 195:301-309.
129. Sato TN, Qin Y, Kozak CA, Audus KL. Tie-1 and tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system. Proc Natl Acad Sci U S A 1993, 90:9355-9358.
130. Puri MC, Bernstein A. Requirement for the TIE family of receptor tyrosine kinases in adult but not fetal hematopoiesis. Proc Natl Acad Sci U S A 2003, 100:12753-12758.
131. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004, 118:149-161.
132. Park IK, He Y, Lin F, Laerum OD, Tian Q, Bumgarner R, et al. Differential gene expression profiling of adult murine hematopoietic stem cells. Blood 2002, 99:488-498.
133. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR. A stem cell molecular signature. Science 2002, 298:601-604.
134. Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, et al. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood 2003, 101:383-389.
135. Forsberg EC, Prohaska SS, Katzman S, Heffner GC, Stuart JM, Weissman IL. Differential expression of novel potential regulators in hematopoietic stem cells. PLoS Genet 2005, 1:e28.
136. Rossi DJ, Bryder D, Zahn JM, Ahlenius H, Sonu R, Wagers AJ, et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci U S A 2005, 102:9194-9199.
137. Ramos CA, Bowman TA, Boles NC, Merchant AA, Zheng Y, Parra I, et al. Evidence for diversity in transcriptional profiles of single hematopoietic stem cells. PLoS Genet 2006, 2:e159.
138. Chambers SM, Boles NC, Lin KY, Tierney MP, Bowman TV, Bradfute SB, et al. Hematopoietic fingerprints: an expression database of stem cells and their progeny. Cell Stem Cell 2007, 1:578-591.
139. Yashiro Y, Bannai H, Minowa T, Yabiku T, Miyano S, Osawa M, et al. Transcriptional profiling of hematopoietic stem cells by high-throughput sequencing. Int J Hematol 2009, 89:24-33.
140. Ooi AG, Karsunky H, Majeti R, Butz S, Vestweber D, Ishida T, et al. The adhesion molecule esam1 is a novel hematopoietic stem cell marker. Stem Cells 2009, 27:653-661.
141. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL. The aging of hematopoietic stem cells. Nat Med 1996, 2:1011-1016.
142. Miranda-Saavedra D, De S, Trotter MW, Teichmann SA, Gottgens B. BloodExpress: a database of gene expression in mouse haematopoiesis. Nucleic Acids Res 2009, 37:D873-D879.
143. Majeti R, Becker MW, Tian Q, Lee TL, Yan X, Liu R, et al. Dysregulated gene expression networks in human acute myelogenous leukemia stem cells. Proc Natl Acad Sci U S A 2009, 106:3396-3401.