GATA-3 regulates hematopoietic stem cell maintenance and cell-cycle entry

Blood

Volumn 119, Issue 10, 2012, Pages 2242-2251

  Ku, Chia Jui ^a   Hosoya, Tomonori ^a   Maillard, Ivan ^a   Engel, James Douglas ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUOROURACIL; TRANSCRIPTION FACTOR GATA 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW SUPPRESSION; CELL ASSAY; CELL COUNT; CELL CYCLE REGULATION; CELL POPULATION; CELL PROLIFERATION; CELL QUIESCENCE; CELL REGENERATION; CONTROLLED STUDY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL MAINTENANCE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; TH2 CELL; TRANSGENIC MOUSE;

EID: 84858047776     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-07-366070     Document Type: Article

References (58)

1. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273(5272):242-245. (Pubitemid 26285891)
2. Adolfsson J, Borge OJ, Bryder D, 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(4):659-669. (Pubitemid 33016450)
3. 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(7):1109-1121. (Pubitemid 40884400)
4. Cheshier SH, Morrison SJ, Liao X, Weissman IL. In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci U S A. 1999;96(6):3120-3125. (Pubitemid 29148854)
5. Wilson A, Laurenti E, Oser G, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 2008;135(6):1118-1129.
6. Orford KW, Scadden DT. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet. 2008;9(2):115-128.
7. Hock H, Hamblen MJ, Rooke HM, et al. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature. 2004;431(7011):1002-1007. (Pubitemid 39434423)
8. Lacorazza HD, Yamada T, Liu Y, et al. The transcription factor MEF/ELF4 regulates the quiescence of primitive hematopoietic cells. Cancer Cell. 2006;9(3):175-187. (Pubitemid 43357944)
9. Miyamoto K, Araki KY, Naka K, et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell. 2007;1(1):101-112. (Pubitemid 46865800)
10. Khandanpour C, Sharif-Askari E, Vassen L, et al. Evidence that growth factor independence 1b regulates dormancy and peripheral blood mobilization of hematopoietic stem cells. Blood. 2010; 116(24):5149-5161.
11. Min IM, Pietramaggiori G, Kim FS, Passegue E, Stevenson KE, Wagers AJ. The transcription factor EGR1 controls both the proliferation and localization of hematopoietic stem cells. Cell Stem Cell. 2008;2(4):380-391. (Pubitemid 351455239)
12. Santaguida M, Schepers K, King B, et al. JunB protects against myeloid malignancies by limiting hematopoietic stem cell proliferation and differentiation without affecting self-renewal. Cancer Cell. 2009;15(4):341-352.
13. Laurenti E, Varnum-Finney B, Wilson A, et al. Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity. Cell Stem Cell. 2008;3(6):611-624.
14. Fujiwara T, O'Geen H, Keles S, et al. Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol Cell. 2009;36(4):667-681.
15. Yu M, Riva L, Xie H, et al. Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell. 2009;36(4):682-695.
16. Zhang Y, Wu W, Cheng Y, et al. Primary sequence and epigenetic determinants of in vivo occupancy of genomic DNA by GATA1. Nucleic Acids Res. 2009;37(21):7024-7038.
17. Wei G, Abraham BJ, Yagi R, et al. Genome-wide analyses of transcription factor GATA3-mediated gene regulation in distinct T cell types. Immunity. 2011;35(2):299-311.
18. Attema JL, Papathanasiou P, Forsberg EC, Xu J, Smale ST, Weissman IL. Epigenetic characterization of hematopoietic stem cell differentiation using miniChIP and bisulfite sequencing analysis. Proc Natl Acad Sci U S A. 2007;104(30):12371-12376. (Pubitemid 47206144)
19. Månsson R, Hultquist A, Luc S, et al. Molecular evidence for hierarchical transcriptional lineage priming in fetal and adult stem cells and multipotent progenitors. Immunity. 2007;26(4):407-419. (Pubitemid 46603001)
20. Kent DG, Copley MR, Benz C, et al. Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential. Blood. 2009;113(25):6342-6350.
21. Zhong JF, Zhao Y, Sutton S, et al. Gene expression profile of murine long-term reconstituting vs. short-term reconstituting hematopoietic stem cells. Proc Natl Acad Sci U S A. 2005;102(7): 2448-2453. (Pubitemid 40279396)
22. Tsai FY, Keller G, Kuo FC, et al. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature. 1994;371(6494):221-226. (Pubitemid 24293019)
23. Ting CN, Olson MC, Barton KP, Leiden JM. Transcription factor GATA-3 is required for development of the T-cell lineage. Nature. 1996; 384(6608):474-478.
24. Tsai FY, Orkin SH. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood. 1997;89(10):3636-3643. (Pubitemid 27227086)
25. Ling KW, Ottersbach K, van Hamburg JP, et al. GATA-2 plays two functionally distinct roles during the ontogeny of hematopoietic stem cells. J Exp Med. 2004;200(7):871-882. (Pubitemid 39362923)
26. Rodrigues NP, Janzen V, Forkert R, et al. Haploinsufficiency of GATA-2 perturbs adult hematopoietic stem-cell homeostasis. Blood. 2005;106(2): 477-484. (Pubitemid 40981241)
27. Hosoya T, Maillard I, Engel JD. From the cradle to the grave: activities of GATA-3 throughout T-cell development and differentiation. Immunol Rev. 2010;238(1):110-125.
28. Hosoya T, Kuroha T, Moriguchi T, et al. GATA-3 is required for early T lineage progenitor development. J Exp Med. 2009;206(13):2987-3000.
29. Buza-Vidas N, Duarte S, Luc S, Bouriez-Jones T, Woll PS, Jacobsen SE. GATA3 is redundant for maintenance and self-renewal of hematopoietic stem cells. Blood. 2011;118(5):1291-1293.
30. van Doorninck JH, van Der Wees J, Karis A, et al. GATA-3 is involved in the development of serotonergic neurons in the caudal raphe nuclei. J Neurosci. 1999;19(12):RC12.
31. Kurek D, Garinis GA, van Doorninck JH, van der Wees J, Grosveld FG. Transcriptome and phenotypic analysis reveals Gata3-dependent signalling pathways in murine hair follicles. Development. 2007;134(2):261-272.
32. Kühn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science. 1995; 269(5229):1427-1429.
33. Lim KC, Lakshmanan G, Crawford SE, Gu Y, Grosveld F, Engel JD. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat Genet. 2000;25(2):209-212. (Pubitemid 30394995)
34. Kaufman CK, Zhou P, Pasolli HA, et al. GATA-3: an unexpected regulator of cell lineage determination in skin. Genes Dev. 2003;17(17):2108-2122. (Pubitemid 37052291)
35. Essers MA, Offner S, Blanco-Bose WE, et al. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature. 2009;458(7240):904-908.
36. Maillard I, Koch U, Dumortier A, et al. Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. Cell Stem Cell. 2008;2(4):356-366. (Pubitemid 351455243)
37. Yang XO, Angkasekwinai P, Zhu J, et al. Requirement for the basic helix-loop-helix transcription factor Dec2 in initial TH2 lineage commitment. Nat Immunol. 2009;10(12):1260-1266.
38. Yamada T, Park CS, Mamonkin M, Lacorazza HD. Transcription factor ELF4 controls the proliferation and homing of CD8+ T cells via the Kruppel-like factors KLF4 and KLF2. Nat Immunol. 2009; 10(6):618-626.
39. Li L, Jothi R, Cui K, et al. Nuclear adaptor Ldb1 regulates a transcriptional program essential for the maintenance of hematopoietic stem cells. Nat Immunol. 2011;12(2):129-136.
40. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000; 404(6774):193-197. (Pubitemid 30154488)
41. Rumfelt LL, Zhou Y, Rowley BM, Shinton SA, Hardy RR. Lineage specification and plasticity in CD19- early B cell precursors. J Exp Med. 2006; 203(3):675-687.
42. Lai AY, Kondo M. Identification of a bone marrow precursor of the earliest thymocytes in adult mouse. Proc Natl Acad Sci U S A. 2007;104(15): 6311-6316. (Pubitemid 47186091)
43. George KM, Leonard MW, Roth ME, et al. Embryonic expression and cloning of the murine GATA-3 gene. Development. 1994;120(9):2673-2686. (Pubitemid 24268840)
44. Hernández-Hoyos G, Anderson MK, Wang C, Rothenberg EV, Alberola-Ila J. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity. 2003;19(1): 83-94. (Pubitemid 36859903)
45. Sambandam A, Maillard I, Zediak VP, et al. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol. 2005;6(7):663-670. (Pubitemid 41716739)
46. Maillard I, Schwarz BA, Sambandam A, et al. Notch-dependent T-lineage commitment occurs at extrathymic sites following bone marrow transplantation. Blood. 2006;107(9):3511-3519.
47. Pandolfi PP, Roth ME, Karis A, et al. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat Genet. 1995;11(1):40-44.
48. Purton LE, Scadden DT. Limiting factors in murine hematopoietic stem cell assays. Cell Stem Cell. 2007;1(3):263-270. (Pubitemid 47355335)
49. Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell. 2006;127(5):1041-1055. (Pubitemid 44792255)
50. Bradford GB, Williams B, Rossi R, Bertoncello I. Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol. 1997;25(5):445-453. (Pubitemid 27226863)
51. Hodgson GS, Bradley TR. Properties of haematopoietic stem cells surviving 5-fluorouracil treatment: evidence for a pre-CFU-S cell? Nature. 1979;281(5730):381-382. (Pubitemid 10228214)
52. Venezia TA, Merchant AA, Ramos CA, et al. Molecular signatures of proliferation and quiescence in hematopoietic stem cells. PLoS Biol. 2004; 2(10):e301.
53. Takahashi S, Shimizu R, Suwabe N, et al. GATA factor transgenes under GATA-1 locus control rescue germline GATA-1 mutant deficiencies. Blood. 2000;96(3):910-916. (Pubitemid 30616855)
54. Xu W, Kee BL. Growth factor independent 1B (Gfi1b) is an E2A target gene that modulates Gata3 in T-cell lymphomas. Blood. 2007;109(10): 4406-4414. (Pubitemid 46743410)
55. Yuan Y, Shen H, Franklin DS, Scadden DT, Cheng T. In vivo self-renewing divisions of haematopoietic stem cells are increased in the absence of the early G1-phase inhibitor, p18INK4C. Nat Cell Biol. 2004;6(5):436-442. (Pubitemid 38607504)
56. Hozumi K, Negishi N, Tsuchiya I, et al. Notch signaling is necessary for GATA3 function in the initiation of T cell development. Eur J Immunol. 2008;38(4):977-985.
57. Dykstra B, Kent D, Bowie M, et al. Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell. 2007;1(2): 218-229. (Pubitemid 47215588)
58. Challen GA, Boles NC, Chambers SM, Goodell MA. Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell Stem Cell. 2010;6(3):265-278.