Experimental Hematology
Volume 38, Issue 6 , Pages 489-503.e1 , June 2010

Dynamic regulation of Gata1 expression during the maturation of conventional dendritic cells

  • Gergely T. Kozma

      Affiliations

    • Department of Hematology, Oncology and Molecular Medicine, Istituto Superiore di Sanità, Rome, Italy
    • Drs. Kozma and Martelli contributed equally to this work.
    • ,
  • Fabrizio Martelli

      Affiliations

    • Department of Hematology, Oncology and Molecular Medicine, Istituto Superiore di Sanità, Rome, Italy
    • Drs. Kozma and Martelli contributed equally to this work.
    • ,
  • Maria Verrucci

      Affiliations

    • Department of Hematology, Oncology and Molecular Medicine, Istituto Superiore di Sanità, Rome, Italy
    • ,
  • Laura Gutiérrez

      Affiliations

    • Cell Biology, Erasmus University Medical Center Rotterdam, The Netherlands
    • ,
  • Giovanni Migliaccio

      Affiliations

    • Department of Cellular Biology and Neurosciences, Istituto Superiore di Sanità, Rome, Italy
    • ,
  • Massimo Sanchez

      Affiliations

    • Department of Cellular Biology and Neurosciences, Istituto Superiore di Sanità, Rome, Italy
    • ,
  • Elena Alfani

      Affiliations

    • Department of Cellular Biology and Neurosciences, Istituto Superiore di Sanità, Rome, Italy
    • ,
  • Sjaak Philipsen

      Affiliations

    • Cell Biology, Erasmus University Medical Center Rotterdam, The Netherlands
    • ,
  • Anna Rita Migliaccio

      Affiliations

    • Department of Hematology, Oncology and Molecular Medicine, Istituto Superiore di Sanità, Rome, Italy
    • Department of Medicine, Mount Sinai School of Medicine and Myeloproliferative Disease Research Consortium, New York, NY., USA
    • Corresponding Author InformationOffprint requests to: Anna Rita Migliaccio, Ph.D., Department of Medicine, Mount Sinai School of Medicine, One Gustave L Levy Place, Box #1079, New York, NY 10029

Received 25 June 2009 ,Revised 8 March 2010 ,Accepted 9 March 2010.

References 

  1. Watts C. Capture and processing of exogenous antigens for presentation on MHC molecules. Annu Rev Immunol. 1997;15:821–850
  2. Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol. 2002;2:151–161
  3. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med. 1997;185:1101–1111
  4. Theofilopoulos AN, Baccala R, Beutler B, Kono DH. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol. 2005;23:307–336
  5. Asselin-Paturel C, Boonstra A, Dalod M, et al. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat Immunol. 2001;2:1144–1150
  6. Inaba K, Inaba M, Deguchi M, et al. Granulocytes, macrophages, and dendritic cells arise from a common major histocompatibility complex class II-negative progenitor in mouse bone marrow. Proc Natl Acad Sci U S A. 1993;90:3038–3042
  7. Wu L, Liu YJ. Development of dendritic-cell lineages. Immunity. 2007;26:741–750
  8. Cella M, Engering A, Pinet V, Pieters J, Lanzavecchia A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature. 1997;388:782–787
  9. Maldonado-Lopez R, De Smedt T, Michel P, et al. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J Exp Med. 1999;189:587–592
  10. Mason DW, Pugh CW, Webb M. The rat mixed lymphocyte reaction: roles of a dendritic cell in intestinal lymph and T-cell subsets defined by monoclonal antibodies. Immunology. 1981;44:75–87
  11. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 1994;179:1109–1118
  12. Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med. 1995;182:389–400
  13. Randolph GJ, Angeli V, Swartz MA. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol. 2005;5:617–628
  14. Kroczek RA, Mages HW, Hutloff A. Emerging paradigms of T-cell co-stimulation. Curr Opin Immunol. 2004;16:321–327
  15. Riley JL, Mao M, Kobayashi S, et al. Modulation of TCR-induced transcriptional profiles by ligation of CD28, ICOS, and CTLA-4 receptors. Proc Natl Acad Sci U S A. 2002;99:11790–11795
  16. Witsch EJ, Peiser M, Hutloff A, et al. ICOS and CD28 reversely regulate IL-10 on re-activation of human effector T cells with mature dendritic cells. Eur J Immunol. 2002;32:2680–2686
  17. Tureci O, Bian H, Nestle FO, et al. Cascades of transcriptional induction during dendritic cell maturation revealed by genome-wide expression analysis. FASEB J. 2003;17:836–847
  18. Fujii S, Liu K, Smith C, Bonito AJ, Steinman RM. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J Exp Med. 2004;199:1607–1618
  19. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene. 2002;21:3368–3376
  20. Gutierrez L, Nikolic T, van Dijk TB, et al. Gata1 regulates dendritic-cell development and survival. Blood. 2007;110:1933–1941
  21. Tanaka H, Matsumura I, Nakajima K, et al. GATA-1 blocks IL-6-induced macrophage differentiation and apoptosis through the sustained expression of cyclin D1 and bcl-2 in a murine myeloid cell line M1. Blood. 2000;95:1264–1273
  22. Bakri Y, Sarrazin S, Mayer UP, et al. Balance of MafB and PU.1 specifies alternative macrophage or dendritic cell fate. Blood. 2005;105:2707–2716
  23. Arinobu Y, Mizuno S, Chong Y, 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
  24. Chen JY, You YK, Chen JC, Huang TC, Kuo CM. Organization and promoter analysis of the zebrafish (Danio rerio) interferon gene. DNA Cell Biol. 2005;24:641–650
  25. Sundrud MS, Vancompernolle SE, Eger KA, et al. Transcription factor GATA-1 potently represses the expression of the HIV-1 coreceptor CCR5 in human T cells and dendritic cells. Blood. 2005;106:3440–3448
  26. Triantis V, Moulin V, Looman MW, Hartgers FC, Janssen RA, Adema GJ. Molecular characterization of the murine homologue of the DC-derived protein DC-SCRIPT. J Leukoc Biol. 2006;79:1083–1091
  27. McKimmie CS, Fraser AR, Hansell C, et al. Hemopoietic cell expression of the chemokine decoy receptor D6 is dynamic and regulated by GATA1. J Immunol. 2008;181:8171–8181
  28. Göbel F, Taschner S, Jurkin J, et al. Reciprocal role of GATA-1 and vitamin D receptor in human myeloid dendritic cell differentiation. Blood. 2009;114:3813–3821
  29. McDevitt MA, Shivdasani RA, Fujiwara Y, Yang H, Orkin SH. A “knockdown” mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc Natl Acad Sci U S A. 1997;94:6781–6785
  30. Takahashi S, Onodera K, Motohashi H, et al. Arrest in primitive erythroid cell development caused by promoter-specific disruption of the GATA-1 gene. J Biol Chem. 1997;272:12611–12615
  31. Onodera K, Takahashi S, Nishimura S, et al. GATA-1 transcription is controlled by distinct regulatory mechanisms during primitive and definitive erythropoiesis. Proc Natl Acad Sci U S A. 1997;94:4487–4492
  32. Takahashi S, Shimizu R, Suwabe N, et al. GATA factor transgenes under GATA-1 locus control rescue germline GATA-1 mutant deficiencies. Blood. 2000;96:910–916
  33. Yu C, Cantor AB, Yang H, et al. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J Exp Med. 2002;195:1387–1395
  34. Shimizu R, Kuroha T, Ohneda O, et al. Leukemogenesis caused by incapacitated GATA-1 function. Mol Cell Biol. 2004;24:10814–10825
  35. Pan X, Ohneda O, Ohneda K, et al. Graded levels of GATA-1 expression modulate survival, proliferation, and differentiation of erythroid progenitors. J Biol Chem. 2005;280:22385–22394
  36. Ito E, Toki T, Ishihara H, et al. Erythroid transcription factor GATA-1 is abundantly transcribed in mouse testis. Nature. 1993;362:466–468
  37. Nishimura S, Takahashi S, Kuroha T, et al. A GATA box in the GATA-1 gene hematopoietic enhancer is a critical element in the network of GATA factors and sites that regulate this gene. Cell Biol. 2000;20:713–723
  38. Vyas P, Ault K, Jackson CW, Orkin SH, Shivdasani RA. Consequences of GATA-1 deficiency in megakaryocytes and platelets. Blood. 1999;93:2867–2875
  39. Vyas P, McDevitt MA, Cantor AB, Katz SG, Fujiwara Y, Orkin SH. Different sequence requirements for expression in erythroid and megakaryocytic cells within a regulatory element upstream of the GATA-1 gene. Development. 1999;126:2799–2811
  40. Migliaccio AR, Rana RA, Sanchez M, et al. GATA-1 as a regulator of mast cell differentiation revealed by the phenotype of the GATA-1low mouse mutant. J Exp Med. 2003;197:281–296
  41. Hirasawa R, Shimizu R, Takahashi S, et al. Essential and instructive roles of GATA factors in eosinophil development. J Exp Med. 2002;195:1379–1386
  42. Abe K, Shimizu R, Pan X, Hamada H, Yoshikawa H, Yamamoto M. Stem cells of GATA1-related leukemia undergo pernicious changes after 5-fluorouracil treatment. Exp Hematol. 2009;37:435–445
  43. Kobayashi E, Shimizu R, Kikuchi Y, Takahashi S, Yamamoto M. Loss of the Gata1 gene IE exon leads to variant transcript expression and the production of a GATA1 protein lacking the N-terminal domain. J Biol Chem. 2010;285:773–783
  44. Martelli F, Ghinassi B, Panetta B, et al. Variegation of the phenotype induced by the Gata1low mutation in mice of different genetic backgrounds. Blood. 2005;106:4102–4113
  45. Varricchio L, Mancini A, Migliaccio AR. Pathological interactions between hemopoietic stem cells and their niche revealed by mouse models of primary myelofibrosis. Expert Review Hematology. 2009;2:315–334
  46. Skoda RC, Tsai SF, Orkin SH, Leder P. Expression of c-MYC under the control of GATA-1 regulatory sequences causes erythroleukemia in transgenic mice. J Exp Med. 1995;181:1603–1613
  47. Montoya M, Schiavoni G, Mattei F, et al. Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood. 2002;99:3263–3271
  48. Follows GA, Tagoh H, Lefevre P, Hodge D, Morgan GJ, Bonifer C. Epigenetic consequences of AML1-ETO action at the human c-FMS locus. EMBO J. 2003;22:2798–2809
  49. Guyot B, Murai K, Fujiwara Y, et al. Characterization of a megakaryocyte-specific enhancer of the key hemopoietic transcription factor GATA1. J Biol Chem. 2006;281:13733–13742
  50. Menges M, Baumeister T, Rössner S, et al. IL-4 supports the generation of a dendritic cell subset from murine bone marrow with altered endocytosis capacity. J Leukoc Biol. 2005;77:535–543
  51. Shia WJ, Pattenden SG, Workman JL. Histone H4 lysine 16 acetylation breaks the genome's silence. Genome Biol. 2006;7:217–217
  52. Plath K, Fang J, Mlynarczyk-Evans SK, et al. Role of histone H3 lysine 27 methylation in X inactivation. Science. 2003;300:131–135
  53. Suzuki M, Moriguchi T, Ohneda K, Yamamoto M. Differential contribution of the Gata1 gene hematopoietic enhancer to erythroid differentiation. Mol Cell Biol. 2009;29:1163–1175
  54. Stamatoyannopoulos G, Grosveld F. Hemoglobin switching. In: Stamatoyannopoulos G and MAJERUS pw, ADS. The molecular basis of blood disease. Philadelphia: Saunders; 2001;p. 135–182
  55. Stamatoyannopoulos G. Control of globin gene expression during development and erythroid differentiation. Exp Hematol. 2005;33:259–271

PII: S0301-472X(10)00083-4

doi: 10.1016/j.exphem.2010.03.006

Experimental Hematology
Volume 38, Issue 6 , Pages 489-503.e1 , June 2010

Article Tools

* Image Usage & Resolution