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PMID: 19798694 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

GATA3 in development and cancer differentiation: cells GATA have it!

Journal of cellular physiology ·Vol. 222 ·No. 1 ·2010-01-00 ·Pages 42-9

Chou J, Provot S, Werb Z

Abstract

There is increasing evidence that the numerous mechanisms that regulate cell differentiation during normal development are also involved in tumorigenesis. In breast cancer, differentiation markers expressed by the primary tumor are routinely profiled to guide clinical decisions. Indeed, numerous studies have shown that the differentiation profile correlates with the metastatic potential of tumors. The transcription factor GATA3 has emerged recently as a strong predictor of clinical outcome in human luminal breast cancer. In the mammary gland, GATA3 is required for luminal epithelial cell differentiation and commitment, and its expression is progressively lost during luminal breast cancer progression as cancer cells acquire a stem cell-like phenotype. Importantly, expression of GATA3 in GATA3-negative, undifferentiated breast carcinoma cells is sufficient to induce tumor differentiation and inhibits tumor dissemination in a mouse model. These findings demonstrate the exquisite ability of a differentiation factor to affect malignant properties, and raise the possibility that GATA3 or its downstream genes could be used in treating luminal breast cancer. This review highlights our recent understanding of GATA3 in both normal mammary development and tumor differentiation.

MeSH Terms
Animals Breast Neoplasms/pathology Cell Differentiation Embryonic Development Female GATA3 Transcription Factor/metabolism Humans Neoplasm Metastasis/pathology Organ Specificity
Chemicals
GATA3 Transcription Factor
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Chou Jonathan
Department of Anatomy, University of California, San Francisco, California 94143-0452, USA.
Provot Sylvain
Werb Zena
References (87)
87 references, click to expand
  1. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy.
    J Exp Med. 2001 Mar 19;193(6):727-40 PMID: 11257139
  2. Transcription factor GATA-3 is essential for lens development.
    Dev Dyn. 2009 Sep;238(9):2280-91 PMID: 19623612
  3. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis.
    Dev Cell. 2008 Jun;14(6):818-29 PMID: 18539112
  4. GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model.
    Cancer Cell. 2008 Feb;13(2):141-52 PMID: 18242514
  5. Macrophages regulate the angiogenic switch in a mouse model of breast cancer.
    Cancer Res. 2006 Dec 1;66(23):11238-46 PMID: 17114237
  6. Inflammation and cancer.
    Nature. 2002 Dec 19-26;420(6917):860-7 PMID: 12490959
  7. Endogenous human microRNAs that suppress breast cancer metastasis.
    Nature. 2008 Jan 10;451(7175):147-52 PMID: 18185580
  8. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer.
    Nature. 2007 Oct 11;449(7163):682-8 PMID: 17898713
  9. CDK inhibitor p18(INK4c) is a downstream target of GATA3 and restrains mammary luminal progenitor cell proliferation and tumorigenesis.
    Cancer Cell. 2009 May 5;15(5):389-401 PMID: 19411068
  10. Expression of the Gata3 transcription factor in the acoustic ganglion of the developing avian inner ear.
    J Comp Neurol. 2009 Oct 20;516(6):507-18 PMID: 19673002
  11. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis.
    Nat Genet. 1995 Sep;11(1):40-4 PMID: 7550312
  12. The epithelial-mesenchymal transition generates cells with properties of stem cells.
    Cell. 2008 May 16;133(4):704-15 PMID: 18485877
  13. ID genes mediate tumor reinitiation during breast cancer lung metastasis.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19506-11 PMID: 18048329
  14. GATA-3 is expressed in association with estrogen receptor in breast cancer.
    Int J Cancer. 1999 Apr 20;84(2):122-8 PMID: 10096242
  15. Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism.
    Immunity. 1998 Nov;9(5):745-55 PMID: 9846495
  16. GATA factor transgenes under GATA-1 locus control rescue germline GATA-1 mutant deficiencies.
    Blood. 2000 Aug 1;96(3):910-6 PMID: 10910904
  17. A GATA-1-regulated microRNA locus essential for erythropoiesis.
    Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3333-8 PMID: 18303114
  18. Transcription factor GATA-3 regulates the transcriptional activity of dopamine beta-hydroxylase by interacting with Sp1 and AP4.
    Neurochem Res. 2008 Sep;33(9):1821-31 PMID: 18338249
  19. GATA-3 expression in breast cancer has a strong association with estrogen receptor but lacks independent prognostic value.
    Cancer Epidemiol Biomarkers Prev. 2008 Feb;17(2):365-73 PMID: 18268121
  20. Cooperation of Gata3, c-Myc and Notch in malignant transformation of double positive thymocytes.
    Mol Immunol. 2008 Jun;45(11):3085-95 PMID: 18471881
  21. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages.
    Cancer Cell. 2009 Aug 4;16(2):91-102 PMID: 19647220
  22. Genes that mediate breast cancer metastasis to lung.
    Nature. 2005 Jul 28;436(7050):518-24 PMID: 16049480
  23. Repeated observation of breast tumor subtypes in independent gene expression data sets.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8418-23 PMID: 12829800
  24. Identification of GATA3 as a breast cancer prognostic marker by global gene expression meta-analysis.
    Cancer Res. 2005 Dec 15;65(24):11259-64 PMID: 16357129
  25. T helper cell differentiation: on again, off again.
    Curr Opin Immunol. 2002 Jun;14(3):366-72 PMID: 11973136
  26. Identification of selective inhibitors of cancer stem cells by high-throughput screening.
    Cell. 2009 Aug 21;138(4):645-659 PMID: 19682730
  27. miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2.
    Blood. 2009 Feb 19;113(8):1794-804 PMID: 18849488
  28. Expression of the transcription factor GATA3 in the postnatal mouse central nervous system.
    Neurosci Res. 2008 Aug;61(4):420-8 PMID: 18554735
  29. A role for microRNAs in maintenance of mouse mammary epithelial progenitor cells.
    Genes Dev. 2007 Dec 15;21(24):3238-43 PMID: 18079172
  30. Mutation of GATA3 in human breast tumors.
    Oncogene. 2004 Oct 7;23(46):7669-78 PMID: 15361840
  31. Associations between gene expressions in breast cancer and patient survival.
    Hum Genet. 2002 Oct;111(4-5):411-20 PMID: 12384785
  32. GATA3 haplo-insufficiency causes human HDR syndrome.
    Nature. 2000 Jul 27;406(6794):419-22 PMID: 10935639
  33. GATA3 inhibits breast cancer growth and pulmonary breast cancer metastasis.
    Oncogene. 2009 Jul 23;28(29):2634-42 PMID: 19483726
  34. Molecular portraits of human breast tumours.
    Nature. 2000 Aug 17;406(6797):747-52 PMID: 10963602
  35. Lipid defect underlies selective skin barrier impairment of an epidermal-specific deletion of Gata-3.
    J Cell Biol. 2006 Nov 20;175(4):661-70 PMID: 17116754
  36. Regulation of Th2 differentiation and Il4 locus accessibility.
    Annu Rev Immunol. 2006;24:607-56 PMID: 16551261
  37. Importin alpha: a multipurpose nuclear-transport receptor.
    Trends Cell Biol. 2004 Sep;14(9):505-14 PMID: 15350979
  38. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system.
    Nat Genet. 2000 Jun;25(2):209-12 PMID: 10835639
  39. Suppression of GATA-3 nuclear import and phosphorylation: a novel mechanism of corticosteroid action in allergic disease.
    PLoS Med. 2009 May 12;6(5):e1000076 PMID: 19436703
  40. Purification and unique properties of mammary epithelial stem cells.
    Nature. 2006 Feb 23;439(7079):993-7 PMID: 16395311
  41. A link between RNA metabolism and silencing affecting Arabidopsis development.
    Dev Cell. 2008 Jun;14(6):854-66 PMID: 18486559
  42. Mast cell lineage diversion of T lineage precursors by the essential T cell transcription factor GATA-3.
    Nat Immunol. 2007 Aug;8(8):845-55 PMID: 17603486
  43. Characterization of GATA3 mutations in the hypoparathyroidism, deafness, and renal dysplasia (HDR) syndrome.
    J Biol Chem. 2004 May 21;279(21):22624-34 PMID: 14985365
  44. Human GATA-3 trans-activation, DNA-binding, and nuclear localization activities are organized into distinct structural domains.
    Mol Cell Biol. 1994 Mar;14(3):2201-12 PMID: 8114750
  45. Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis.
    Dev Dyn. 2006 Dec;235(12):3404-12 PMID: 17039550
  46. The function role of GATA-3 in Th1 and Th2 differentiation.
    Immunol Res. 2003;28(1):25-37 PMID: 12947222
  47. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch.
    Immunity. 2007 Jul;27(1):89-99 PMID: 17658279
  48. Friend of GATA-1 represses GATA-3-dependent activity in CD4+ T cells.
    J Exp Med. 2001 Nov 19;194(10):1461-71 PMID: 11714753
  49. Physical and functional interaction between GATA-3 and Smad3 allows TGF-beta regulation of GATA target genes.
    Curr Biol. 2002 Jan 8;12(1):35-45 PMID: 11790301
  50. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers.
    Nat Med. 2009 Aug;15(8):907-13 PMID: 19648928
  51. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies.
    J Pathol. 2002 Mar;196(3):254-65 PMID: 11857487
  52. Stem cells and breast cancer: A field in transit.
    Nat Rev Cancer. 2003 Nov;3(11):832-44 PMID: 14668814
  53. Gata3 acts downstream of beta-catenin signaling to prevent ectopic metanephric kidney induction.
    PLoS Genet. 2008 Dec;4(12):e1000316 PMID: 19112489
  54. Notch directly regulates Gata3 expression during T helper 2 cell differentiation.
    Immunity. 2007 Jul;27(1):100-10 PMID: 17658278
  55. Scratching the surface of skin development.
    Nature. 2007 Feb 22;445(7130):834-42 PMID: 17314969
  56. GATA-3: an unexpected regulator of cell lineage determination in skin.
    Genes Dev. 2003 Sep 1;17(17):2108-22 PMID: 12923059
  57. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions.
    Nat Rev Cancer. 2008 Oct;8(10):755-68 PMID: 18784658
  58. Structure and specificity of GATA proteins in Th2 development.
    Mol Cell Biol. 2001 Apr;21(8):2716-25 PMID: 11283251
  59. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland.
    Cell. 2006 Dec 1;127(5):1041-55 PMID: 17129787
  60. GATA3 protein as a MUC1 transcriptional regulator in breast cancer cells.
    Breast Cancer Res. 2006;8(6):R64 PMID: 17078870
  61. Trophic macrophages in development and disease.
    Nat Rev Immunol. 2009 Apr;9(4):259-70 PMID: 19282852
  62. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors.
    Nature. 2009 Jun 4;459(7247):708-11 PMID: 19396158
  63. GATA3 and the T-cell lineage: essential functions before and after T-helper-2-cell differentiation.
    Nat Rev Immunol. 2009 Feb;9(2):125-35 PMID: 19151747
  64. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases.
    Am J Pathol. 2003 Nov;163(5):2113-26 PMID: 14578209
  65. Transcriptome and phenotypic analysis reveals Gata3-dependent signalling pathways in murine hair follicles.
    Development. 2007 Jan;134(2):261-72 PMID: 17151017
  66. Metastasis: from dissemination to organ-specific colonization.
    Nat Rev Cancer. 2009 Apr;9(4):274-84 PMID: 19308067
  67. Patterning mechanisms of branched organs.
    Science. 2008 Dec 5;322(5907):1506-9 PMID: 19056977
  68. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10869-74 PMID: 11553815
  69. T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes.
    Nat Immunol. 2002 Jul;3(7):643-51 PMID: 12055628
  70. Essential role of GATA3 for the maintenance of type 2 helper T (Th2) cytokine production and chromatin remodeling at the Th2 cytokine gene loci.
    J Biol Chem. 2004 Jun 25;279(26):26983-90 PMID: 15087456
  71. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  72. PU.1 expression delineates heterogeneity in primary Th2 cells.
    Immunity. 2005 Jun;22(6):693-703 PMID: 15963784
  73. Classification of breast cancer using genetic algorithms and tissue microarrays.
    Clin Cancer Res. 2006 Nov 1;12(21):6459-68 PMID: 17085660
  74. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis.
    Cell. 2009 Jun 12;137(6):1032-46 PMID: 19524507
  75. Generation of a functional mammary gland from a single stem cell.
    Nature. 2006 Jan 5;439(7072):84-8 PMID: 16397499
  76. Ras-ERK MAPK cascade regulates GATA3 stability and Th2 differentiation through ubiquitin-proteasome pathway.
    J Biol Chem. 2005 Aug 19;280(33):29409-19 PMID: 15975924
  77. Hormonal and local control of mammary branching morphogenesis.
    Differentiation. 2006 Sep;74(7):365-81 PMID: 16916375
  78. Regulation of IL-4 gene expression by distal regulatory elements and GATA-3 at the chromatin level.
    Immunity. 2001 Apr;14(4):447-59 PMID: 11336690
  79. Function of GATA transcription factors in preadipocyte-adipocyte transition.
    Science. 2000 Oct 6;290(5489):134-8 PMID: 11021798
  80. Micromanagers of malignancy: role of microRNAs in regulating metastasis.
    Trends Genet. 2008 Sep;24(9):448-56 PMID: 18674843
  81. Regulation of Th2 cytokine genes by p38 MAPK-mediated phosphorylation of GATA-3.
    J Immunol. 2007 Feb 15;178(4):2491-8 PMID: 17277157
  82. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation.
    Nat Cell Biol. 2007 Feb;9(2):201-9 PMID: 17187062
  83. Crystal structures of multiple GATA zinc fingers bound to DNA reveal new insights into DNA recognition and self-association by GATA.
    J Mol Biol. 2008 Sep 19;381(5):1292-306 PMID: 18621058
  84. Gata3 participates in a complex transcriptional feedback network to regulate sympathoadrenal differentiation.
    Development. 2006 Oct;133(19):3871-81 PMID: 16943277
  85. Cutting edge: the differential involvement of the N-finger of GATA-3 in chromatin remodeling and transactivation during Th2 development.
    J Immunol. 2002 Oct 15;169(8):4103-7 PMID: 12370337
  86. Knock-in mutation of transcription factor GATA-3 into the GATA-1 locus: partial rescue of GATA-1 loss of function in erythroid cells.
    Dev Biol. 1998 Apr 15;196(2):218-27 PMID: 9576834
  87. GATA-3 - not just for Th2 cells anymore.
    Cell Mol Immunol. 2007 Feb;4(1):15-29 PMID: 17349208
Article Info
Journal
Journal of cellular physiology
Abbr.
J Cell Physiol
ISSN
1097-4652
Published
2010-01-00
Pages
42-9
Language
English
Region
United States
NLM ID
0050222
PMCID
PMC2915440
Subset
IM
Grants
NIEHS NIH HHS · U01 ES012801-010001 · United States
NCI NIH HHS · R01 CA129523-04 · United States
NIEHS NIH HHS · ES012801 · United States
NCI NIH HHS · CA129523 · United States
NIEHS NIH HHS · U01 ES012801 · United States
NCI NIH HHS · R01 CA129523 · United States
NCI NIH HHS · R01 CA057621 · United States
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