Experimental Hematology
Volume 37, Issue 8 , Pages 889-900 , August 2009

Role of STAT3 and GATA-1 interactions in γ-globin gene expression

  • Xiao Yao

      Affiliations

    • Department of Molecular and Cell Biology, University of Texas at Dallas, Richardson, Tex., USA
  • ,
  • Sirisha Kodeboyina

      Affiliations

    • Department of Molecular and Cell Biology, University of Texas at Dallas, Richardson, Tex., USA
  • ,
  • Li Liu

      Affiliations

    • Department of Molecular and Cell Biology, University of Texas at Dallas, Richardson, Tex., USA
  • ,
  • James Dzandu

      Affiliations

    • Department of Molecular and Cell Biology, University of Texas at Dallas, Richardson, Tex., USA
  • ,
  • Jose Sangerman

      Affiliations

    • Department of Pediatrics, Yale University, New Haven, Conn., USA
  • ,
  • Solomon F. Ofori-Acquah

      Affiliations

    • Department of Pediatrics, Emory University, Atlanta, Ga., USA
  • ,
  • Betty S. Pace

      Affiliations

    • Department of Molecular and Cell Biology, University of Texas at Dallas, Richardson, Tex., USA
    • Corresponding Author InformationOffprint requests to: Betty S. Pace, M.D., Department of Molecular and Cell Biology, University of Texas at Dallas, FO 3.1, 800 West Campbell Road, Richardson, TX 75080

Received 14 September 2008 ,Revised 6 April 2009 ,Accepted 8 May 2009.

References 

  1. Stamatoyannopoulos G, Grosveld F. Hemoglobin switching. In:  Stamatoyannopoulos G,  Majerus PW,  Perlmutter RM,  Varmus H editor. The Molecular Basis of Blood Disease. 3rd ed. Philadelphia, PA: WB Saunders; 2000;p. 135–182
  2. Morrison JC, Whybrew WD, Bucovaz ET, Wiser WL. Fluctuation of fetal hemoglobin in sickle-cell anemia. Am J Obstet Gynecol. 1976;125:1085–1088
  3. Resar LM, Segal JB, Fitzpatric LK, Friedmann A, Brusilow SW, Dover GJ. Induction of fetal hemoglobin synthesis in children with sickle cell anemia on low-dose oral sodium phenylbutyrate therapy. J Pediatr Hematol Oncol. 2002;24:737–741
  4. Ware RE, Eggleston B, Redding-Lallinger R, et al. Predictors of fetal hemoglobin response in children with sickle cell anemia receiving hydroxyurea therapy. Blood. 2002;99:10–14
  5. Li Q, Peterson KR, Fang X, Stamatoyannopoulos G. Locus control regions. Blood. 2002;100:3077–3086
  6. Walters M, Martin DI. Functional erythroid promoters created by interaction of the transcription factor GATA-1 with CACCC and AP-1/NFE-2 elements. Proc Natl Acad Sci U S A. 1992;89:10444–10448
  7. Goodwin AJ, McInerney JM, Glander MA, Pomerantz O, Lowrey CH. In vivo formation of a human beta-globin locus control region core element requires binding sites for multiple factors including GATA-1, NF-E2, erythroid Kruppel-like factor, and Sp1. J Biol Chem. 2001;276:26883–26892
  8. Foley HA, Ofori-Acquah SF, Yoshimura A, Critz S, Baliga BS, Pace BS. Stat3 beta inhibits gamma-globin gene expression in erythroid cells. J Biol Chem. 2002;277:16211–16219
  9. Mantovani R, Superti-Furga G, Gilman J, Ottolenghi S. The deletion of the distal CCAAT box region of the A gamma-globin gene in black HPFH abolishes the binding of the erythroid specific protein NFE3 and of the CCAAT displacement protein. Nucleic Acids Res. 1989;17:6681–6691
  10. Asano H, Li XS, Stamatoyannopoulos G. FKLF, a novel Kruppel-like factor that activates human embryonic and fetal beta-like globin genes. Mol Cell Biol. 1999;19:3571–3579
  11. Asano H, Li XS, Stamatoyannopoulos G. FKLF-2: a novel Kruppel-like transcriptional factor that activates globin and other erythroid lineage genes. Blood. 2000;95:3578–3584
  12. Bose F, Fugazza C, Casalgrandi M, et al. Functional interaction of CP2 with GATA-1 in the regulation of erythroid promoters. Mol Cell Biol. 2006;26:3942–3954
  13. Tanabe O, Katsuoka F, Campbell AD, et al. An embryonic/fetal beta-type globin gene repressor contains a nuclear receptor TR2/TR4 heterodimer. EMBO J. 2002;21:3434–3442
  14. Caldenhoven E, van Dijk TB, Solari R, et al. STAT3beta, a splice variant of transcription factor STAT3, is a dominant negative regulator of transcription. J Biol Chem. 1996;271:13221–13227
  15. Schaefer TS, Sanders LK, Nathans D. Cooperative transcriptional activity of Jun and Stat3 beta, a short form of Stat3. Proc Natl Acad Sci U S A. 1995;92:9097–9101
  16. Yoo JY, Huso DL, Nathans D, Desiderio S. Specific ablation of Stat3beta distorts the pattern of Stat3-responsive gene expression and impairs recovery from endotoxic shock. Cell. 2002;108:331–344
  17. Ezoe S, Matsumura I, Gale K, et al. GATA transcription factors inhibit cytokine-dependent growth and survival of a hematopoietic cell line through the inhibition of STAT3 activity. J Biol Chem. 2005;280:13163–13170
  18. Ikonomi P, Noguchi CT, Miller W, Kassahun H, Hardison R, Schechter AN. Levels of GATA-1/GATA-2 transcription factors modulate expression of embryonic and fetal hemoglobins. Gene. 2000;261:277–287
  19. Taga T, Kishimoto T. gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol. 1997;15:797–819
  20. Rose-John S. Coordination of interleukin-6 biology by membrane bound and soluble receptors. Adv Exp Med Biol. 2001;495:145–151
  21. Schindler C, Darnell JE. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu Rev Biochem. 1995;64:621–651
  22. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. Interleukin-6-type cytokine signaling through the gp130/Jak/STAT pathway. Biochem J. 1998;334(Pt 2):297–314
  23. Stancato LF, David M, Carter-Su C, Larner AC, Pratt WB. Preassociation of STAT1 with STAT2 and STAT3 in separate signaling complexes prior to cytokine stimulation. J Biol Chem. 1996;271:4134–4137
  24. Sehgal PB. Plasma membrane rafts and chaperones in cytokine/STAT signaling. Acta Biochim Pol. 2003;50:583–594
  25. Gerhartz C, Heesel B, Sasse J, et al. Differential activation of acute phase response factor/STAT3 and STAT1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130, I: definition of a novel phosphotyrosine motif mediating STAT1 activation. J Biol Chem. 1006;271:12991–12998.
  26. Tajima S, Tsuji K, Ebihara Y, et al. Analysis of IL-6 receptor and gp130 expressions and proliferative capability of human CD34+ cells. J Exp Med. 1996;184:1357–1364
  27. Chung YJ, Park B, Kang YJ, Kim TM, Eaves CJ, Oh IH. Unique effects of STAT3 on the early phase of hematopoietic stem cell regeneration. Blood. 2006;108:1208–1215
  28. Peters M, Müller A, Rose-John S. Interleukin-6 and soluble interleukin-6 receptor: direct stimulation of gp130 and hematopoiesis. Blood. 1998;92:3495–3504
  29. Sangerman J, Lee MS, Yao X, et al. Mechanism for fetal hemoglobin induction by histone deacetylase inhibitors involves gamma-globin activation by CREB1 and ATF-2. Blood. 2006;108:3590–3599
  30. Andrews NC, Faller DV. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 1991;19:2499
  31. Watts HJ, Yeung D, Parkes H. Real-time detection and quantification of DNA hybridization by an optical biosensor. Anal Chem. 1995;67:4283–4289
  32. Biet E, Sun J, Dutreix M. Conserved sequence preference in DNA binding among recombination proteins: an effect of ssDNA secondary structure. Nucleic Acids Res. 1999;27:596–600
  33. Zhang X, Darnell JE. Functional importance of Stat3 tetramerization in activation of the alpha 2-macroglobulin gene. J Biol Chem. 2001;276:33576–33581
  34. Ferry AE, Baliga BS, Monteiro C, Pace BS. Globin gene silencing in primary erythroid cultures, an inhibitory role for interleukin-6. J Biol Chem. 1997;272:20030–20037
  35. Amrolia PJ, Cunningham JM, Ney P, Nienhuis AW, Jane SM. Identification of two novel regulatory elements within the 5′-untranslated region of the human A gamma-globin gene. J Biol Chem. 1995;270:12892–12898
  36. Li Q, Clegg C, Peterson K, Shaw S, Raich N, Stamatoyannopoulos G. Binary transgenic mouse model for studying the trans control of globin gene switching: evidence that GATA-1 is an in vivo repressor of human epsilon gene expression. Proc Natl Acad Sci U S A. 1997;94:2444–2448
  37. Kirito K, Uchida M, Takatoku M, et al. A novel function of Stat1 and Stat3 proteins in erythropoietin-induced erythroid differentiation of a human leukemia cell line. Blood. 1998;92:462–471
  38. Jelkmann W, Bohlius J, Hallek M, Sytkowski AJ. The erythropoietin receptor in normal and cancer tissues. Crit Rev Oncol Hematol. 2008;67:39–61
  39. Socolovsky M, Fallon AE, Wang S, Brugnara C, Lodish HF. Fetal anemia and apoptosis of red cell progenitors in Stat5a-/-5b-/- mice: a direct role for Stat5 in Bcl-X (L) induction. Cell. 1999;98:181–191
  40. Welch JJ, Watts JA, Vakoc CR, et al. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood. 2004;15:3136–3147
  41. Weiss MJ, Orkin SH. Transcription factor GATA-1 permits survival and maturation of erythroid precursors by preventing apoptosis. Proc Natl Acad Sci U S A. 1995;10:9623–9627
  42. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene. 2002;21:3368–3376
  43. Grosveld F, Rodriguez P, Meier N, et al. Isolation and characterization of hematopoietic transcription factor complexes by in vivo biotinylation tagging and mass spectrometry. Ann N Y Acad Sci. 2005;1054:55–60
  44. Trainor CD, Ghirlando R, Simpson MA. GATA zinc finger interactions modulate DNA binding and transactivation. J Biol Chem. 2000;275:28157–28166
  45. Trainor CD, Omichinski JG, Vandergon TL, Gronenborn AM, Clore GM, Felsenfeld G. A palindromic regulatory site within vertebrate GATA-1 promoters requires both zinc fingers of the GATA-1 DNA-binding domain for high-affinity interaction. Mol Cell Biol. 1996;16:2238–2247
  46. Magis W, Martin DI. HMG-I binds to GATA motifs: implications for an HPFH syndrome. Biochem Biophys Res Commun. 1995;214:927–933
  47. Zhiyi Chen H-YL, Basran Raveen K, et al. A T-to-G transversion at nucleotide –567 upstream of HBG2 in a GATA-1 binding motif is associated with elevated hemoglobin F. Mol Cell Biol. 2008;28:4386–4393
  48. Harju-Baker S, Costa FC, Fedosyuk H, Neades R, Peterson KR. Silencing of Agamma-globin gene expression during adult definitive erythropoiesis mediated by GATA-1-FOG-1-Mi2 complex binding at the -566 GATA site. Mol Cell Biol. 2008;28:3101–3113
  49. Duan Z, Stamatoyannopoulos G, Li Q. Role of NF-Y in in vivo regulation of the gamma-globin gene. Mol Cell Biol. 2001;21:3083–3095
  50. Zhang P, Zhang X, Iwama A, et al. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood. 2000;96:2641–2648
  51. Stopka T, Amanatullah DF, Papetti M, Skoultchi AI. PU.1 inhibits the erythroid program by binding to GATA-1 on DNA and creating a repressive chromatin structure. EMBO J. 2005;24:3712–3723
  52. Tsai SF, Strauss E, Orkin SH. Functional analysis and in vivo footprinting implicate the erythroid transcription factor GATA-1 as a positive regulator of its own promoter. Genes Dev. 1991;5:919–931
  53. Tsang AP, Visvader JE, Turner CA, et al. FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell. 1997;90:109–119
  54. Newton A, Mackay J, Crossley M. The N-terminal zinc finger of the erythroid transcription factor GATA-1 binds GATC motifs in DNA. J Biol Chem. 2001;276:35794–35801
  55. 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

PII: S0301-472X(09)00160-X

doi: 10.1016/j.exphem.2009.05.004

Experimental Hematology
Volume 37, Issue 8 , Pages 889-900 , August 2009