Csf3r mutations in mice confer a strong clonal HSC advantage via activation of Stat5

Journal of Clinical Investigation

Volumn 118, Issue 3, 2008, Pages 946-955

  Liu, Fulu ^a   Kunter, Ghada ^a   Krem, Maxwell M ^a   Eades, William C ^a   Cain, Jennifer A ^a   Tomasson, Michael H ^a   Hennighausen, Lothar ^b   Link, Daniel C ^a,c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c Division of Oncology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE COLONY STIMULATING FACTOR RECEPTOR; STAT5 PROTEIN; STAT5A PROTEIN; STAT5B PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GENE MUTATION; LEUKEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STEM CELL;

ANIMALS; CELL PROLIFERATION; GRANULOCYTE COLONY-STIMULATING FACTOR; HEMATOPOIETIC STEM CELLS; MICE; MICE, INBRED C57BL; MUTATION; NEUTROPENIA; RECEPTORS, GRANULOCYTE COLONY-STIMULATING FACTOR; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR;

EID: 40549121259     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI32704     Document Type: Article

References (62)

1. Bonnet, D., and Dick, J.E. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3:730-737.
2. Catlin, S.N., Guttorp, P., and Abkowitz, J.L. 2005. The kinetics of clonal dominance in myeloproliferative disorders. Blood. 106:2688-2692.
3. Jamieson, C.H., et al. 2004. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med. 351:657-667.
4. Kustikova, O.S., et al. 2007. Retroviral vector insertion sites associated with dominant hematopoietic clones mark "stemness" pathways. Blood. 109:1897-1907.
5. Kostmann, R. 1956. Infantile genetic agranulocytosis: a new recessive lethal disease in man. Acta Paediatr. 105:1-78.
6. Welte, K., Zeidler, C., and Dale, D.C. 2006. Severe congenital neutropenia. Semin. Hematol. 43:189-195.
7. Donadieu, J., et al. 2005. Analysis of risk factors for myelodysplasias, leukemias and death from infection among patients with congenital neutropenia. Experience of the French Severe Chronic Neutropenia Study Group. Haematologica. 90:45-53.
8. Rosenberg, P.S., et al. 2006. The incidence of leukemia and mortality from sepsis in patients with severe congenital neutropenia receiving long-term G-CSF therapy. Blood. 107:4628-4635.
9. Dale, D.C., et al. 1993. A randomized controlled phase III trial of recombinant human granulocyte colony-stimulating factor (filgrastim) for treatment of severe chronic neutropenia. Blood. 81:2496-2502.
10. Germeshausen, M., Ballmaier, M., and Welte, K. 2007. Incidence of CSF3R mutations in severe congenital neutropenia and relevance for leukemogenesis: Results of a long-term survey. Blood. 109:93-99.
11. Dong, F., et al. 1995. Mutations in the gene for the granulocyte colony-stimulating-factor receptor in patients with acute myeloid leukemia preceded by severe congenital neutropenia. N. Engl. J. Med. 333:487-493.
12. Hermans, M.H., et al. 1999. Sustained receptor activation and hyperproliferation in response to granulocyte colony-stimulating factor (G-CSF) in mice with a severe congenital neutropenia/acute myeloid leukemia-derived mutation in the G- CSF receptor gene. J. Exp. Med. 189:683-692.
13. Hunter, M.G., and Avalos, B.R. 2000. Granulocyte colony-stimulating factor receptor mutations in severe congenital neutropenia transforming to acute myelogenous leukemia confer resistance to apoptosis and enhance cell survival. Blood. 95:2132-2137.
14. Hermans, M.H., et al. 1998. Perturbed granulopoiesis in mice with a targeted mutation in the granulocyte colony-stimulating factor receptor gene associated with severe chronic neutropenia. Blood. 92:32-39.
15. McLemore, M.L., Poursine-Laurent, J., and Link, D.C. 1998. Increased granulocyte colony-stimulating factor responsiveness but normal resting granulopoiesis in mice carrying a targeted granulocyte colony-stimulating factor receptor mutation derived from a patient with severe congenital neutropenia. J. Clin. Invest. 102:483-492.
16. Guba, S.C., Sartor, C.A., Hutchinson, R., Boxer, L.A., and Emerson, S.G. 1994. Granulocyte colony-stimulating factor (G-CSF) production and G-CSF receptor structure in patients with congenital neutropenia. Blood. 83:1486-1492.
17. Kiel, M.J., et al. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 121:1109-1121.
18. Nozaki, I., et al. 2005. Small proline-rich proteins 2 are noncoordinately upregulated by IL-6/STAT3 signaling after bile duct ligation. Lab. Invest. 85:109-123.
19. Kelly, J.A., et al. 2003. Stat5 synergizes with T cell receptor/antigen stimulation in the development of lymphoblastic lymphoma. J. Exp. Med. 198:79-89.
20. Miccoli, M.C., Vaccarelli, G., Lanave, C., Cribiu, E.P., and Ciccarese, S. 2005. Comparative analyses of sheep and human TRG joining regions: evolution of J genes in Bovidae is driven by sequence conservation in their promoters for germline transcription. Gene. 355:67-78.
21. Mizuki, M., et al. 2003. Suppression of myeloid transcription factors and induction of STAT response genes by AML-specific Flt3 mutations. Blood. 101:3164-3173.
22. Giraud, S., Hurlstone, A., Avril, S., and Coqueret, O. 2004. Implication of BRG1 and cdk9 in the STAT3-mediated activation of the p21waf1 gene. Oncogene. 23:7391-7398.
23. Takahashi, S., Harigae, H., Kaku, M., Sasaki, T., and Licht, J.D. 2004. Flt3 mutation activates p21WAF1/CIP1 gene expression through the action of STAT5. Biochem. Biophys. Res. Commun. 316:85-92.
24. Mitchell, T.J., Whittaker, S.J., and John, S. 2003. Dysregulated expression of COOH-terminally truncated Stat5 and loss of IL2-inducible Stat5-dependent gene expression in Sezary Syndrome. Cancer Res. 63:9048-9054.
25. Krebs, D.L., and Hilton, D.J. 2001. SOCS proteins: negative regulators of cytokine signaling. Stem Cells. 19:378-387.
26. Irish, J.M., et al. 2004. Single cell profiling of potentiated phospho-protein networks in cancer cells. Cell. 118:217-228.
27. McLemore, M.L., et al. 2001. STAT-3 activation is required for normal G-CSF-dependent proliferation and granulocytic differentiation. Immunity. 14:193-204.
28. Yao, Z., et al. 2006. Stat5a/b are essential for normal lymphoid development and differentiation. Proc. Natl. Acad. Sci. U. S. A. 103:1000-1005.
29. Li, G., et al. 2007. STAT5 requires the N-domain to maintain hematopoietic stem cell repopulating function and appropriate lymphoid-myeloid lineage output. Exp. Hematol. 35:1684.
30. Bernard, T., Gale, R.E., and Linch, D.C. 1996. Analysis of granulocyte colony stimulating factor receptor isoforms, polymorphisms and mutations in normal haemopoietic cells and acute myeloid leukaemia blasts. Br. J. Haematol. 93:527-533.
31. Carapeti, M., et al. 1997. Rarity of dominant-negative mutations of the G-CSF receptor in patients with blast crisis of chronic myeloid leukemia or de novo acute leukemia. Leukemia. 11:1005-1008.
32. Glimm, H., Oh, I.H., and Eaves, C.J. 2000. Human hematopoietic stem cells stimulated to proliferate in vitro lose engraftment potential during their S/G(2)/M transit and do not reenter G(0). Blood. 96:4185-4193.
33. Passegue, E., Wagers, A.J., Giuriato, S., Anderson, W.C., and Weissman, I.L. 2005. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 202:1599-1611.
34. Cheng, T., et al. 2000. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science. 287:1804-1808.
35. Zhang, J., et al. 2006. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature. 441:518-522.
36. Yilmaz, O.H., et al. 2006. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature. 441:475-482.
37. Kato, Y., et al. 2005. Selective activation of STAT5 unveils its role in stem cell self-renewal in normal and leukemic hematopoiesis. J. Exp. Med. 202:169-179.
38. Zhang, S., et al. 2000. Essential role of signal transducer and activator of transcription (Stat)5a but not Stat5b for Flt3-dependent signaling. J. Exp. Med. 192:719-728.
39. Bunting, K.D., et al. 2002. Reduced lymphomyeloid repopulating activity from adult bone marrow and fetal liver of mice lacking expression of STAT5. Blood. 99:479-487.
40. Schuringa, J.J., Chung, K.Y., Morrone, G., and Moore, M.A.S. 2004. Constitutive activation of STAT5A promotes human hematopoietic stem cell self-renewal and erythroid differentiation. J. Exp. Med. 200:623-635.
41. Moriggl, R., et al. 2005. Stat5 tetramer formation is associated with leukemogenesis. Cancer Cell. 7:87-99.
42. Hayakawa, F., et al. 2000. Tandem-duplicated Flt3 constitutively activates STAT5 and MAP kinase and introduces autonomous cell growth in IL-3-dependent cell lines. Oncogene. 19:624-631.
43. Schwaller, J., et al. 2000. Stat5 Is Essential for the Myelo- and Lymphoproliferative Disease Induced by TEL/JAK2. Mol. Cell. 6:693.
44. Hoelbl, A., et al. 2006. Clarifying the role of Stat5 in lymphoid development and Abelson-induced transformation. Blood. 107:4898-4906.
45. Schepers, H., et al. 2007. STAT5 is required for long-term maintenance of normal and leukemic human stem/progenitor cells. Blood. 110:2880.
46. Iwama, A., et al. 2004. Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity. 21:843-851.
47. Antonchuk, J., Sauvageau, G., and Humphries, R.K. 2002. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell. 109:39-45.
48. Lacorazza, H.D., et al. 2006. The transcription factor MEF/ELF4 regulates the quiescence of primitive hematopoietic cells. Cancer Cell. 9:175-187.
49. Arai, F., et al. 2004. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 118:149-161.
50. Reya, T., et al. 2003. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 423:409-414.
51. Zhang, P., et al. 2004. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity. 21:853-863.
52. Yuan, Y., Shen, H., Franklin, D.S., Scadden, D.T., and Cheng, T. 2004. In vivo self-renewing divisions of haematopoietic stem cells are increased in the absence of the early G1-phase inhibitor, p18INK4C. Nat. Cell Biol. 6:436-442.
53. Duncan, A.W., et al. 2005. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 6:314-322.
54. Hock, H., et al. 2004. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature. 431:1002-1007.
55. Zeng, H., Yucel, R., Kosan, C., Klein-Hitpass, L., and Moroy, T. 2004. Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells. EMBO J. 23:4116-4125.
56. Zhu, J., Zhang, Y., Joe, G.J., Pompetti, R., and Emerson, S.G. 2005. NF-Ya activates multiple hematopoietic stem cell (HSC) regulatory genes and promotes HSC self-renewal. Proc. Natl. Acad. Sci. U. S. A. 102:11728-11733.
57. Adam, M., et al. 2006. Targeting PIM kinases impairs survival of hematopoietic cells transformed by kinase inhibitor-sensitive and kinase inhibitor-resistant forms of Fms-like tyrosine kinase 3 and BCR/ABL. Cancer Res. 66:3828.
58. Jeha, S., et al. 2000. Spontaneous remission of granulocyte colony-stimulating factor-associated leukemia in a child with severe congenital neutropenia. Blood. 96:3647-3649.
59. Cui, Y., et al. 2004. Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol. Cell. Biol. 24:8037.
60. Richards, M.K., Liu, F., Iwasaki, H., Akashi, K., and Link, D.C. 2003. Pivotal role of granulocyte colony-stimulating factor in the development of progenitors in the common myeloid pathway. Blood. 102:3562-3568.
61. Jacob, J., Haug, J.S., Raptis, S., and Link, D.C. 1998. Specific signals generated by the cytoplasmic domain of the granulocyte colony-stimulating factor (G-CSF) receptor are not required for G-CSF-dependent granulocytic differentiation. Blood. 92:353.
62. Cain, J.A., et al. 2007. Myeloproliferative disease induced by TEL-PDGFRB displays dynamic range sensitivity to Stat5 gene dosage. Blood. 109:3906.