Experimental Hematology
Volume 36, Issue 5 , Pages 624-641 , May 2008

Retinoic acid receptor γ activates receptor tyrosine kinase Tie1 gene transcription through transcription factor GATA4 in F9 stem cells

  • Dan Su
  • ,
  • Lorraine J. Gudas

      Affiliations

    • Corresponding Author InformationOffprint requests to: Lorraine J. Gudas, Ph.D., Department of Pharmacology, Weill Cornell Medical College, 1300 York Avenue, New York, NY 10065

Received 9 October 2007 ,Revised 19 December 2007 ,Accepted 31 December 2007.

References 

  1. Gudas LJ. Retinoids, retinoid-responsive genes, cell differentiation, and cancer. Cell Growth Differ. 1992;3:655–662
  2. Strickland S, Smith KK, Marotti KR. Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell. 1980;21:347–355
  3. Germain P, Chambon P, Eichele G, et al. International Union of Pharmacology. LXIII. Retinoid X receptors. Pharmacol Rev. 2006;58:760–772
  4. Olefsky JM. Nuclear receptor minireview series. J Biol Chem. 2001;276:36863–36864
  5. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J. 1996;10:940–954
  6. Mongan NP, Gudas LJ. Diverse actions of retinoid receptors in cancer prevention and treatment. Differentiation. 2007;75:853–870
  7. Mark M, Ghyselinck NB, Chambon P. Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu Rev Pharmacol Toxicol. 2006;46:451–480
  8. Hu L, Gudas LJ. Cyclic AMP analogs and retinoic acid influence the expression of retinoic acid receptor alpha, beta, and gamma mRNAs in F9 teratocarcinoma cells. Mol Cell Biol. 1990;10:391–396
  9. Zhuang Y, Faria TN, Chambon P, Gudas LJ. Identification and characterization of retinoic acid receptor beta2 target genes in F9 teratocarcinoma cells. Mol Cancer Res. 2003;1:619–630
  10. Faria TN, Mendelsohn C, Chambon P, Gudas LJ. The targeted disruption of both alleles of RARbeta(2) in F9 cells results in the loss of retinoic acid-associated growth arrest. J Biol Chem. 1999;274:26783–26788
  11. Boylan JF, Lufkin T, Achkar CC, Taneja R, Chambon P, Gudas LJ. Targeted disruption of retinoic acid receptor alpha (RAR alpha) and RAR gamma results in receptor-specific alterations in retinoic acid-mediated differentiation and retinoic acid metabolism. Mol Cell Biol. 1995;15:843–851
  12. Boylan JF, Lohnes D, Taneja R, Chambon P, Gudas LJ. Loss of retinoic acid receptor gamma function in F9 cells by gene disruption results in aberrant Hoxa-1 expression and differentiation upon retinoic acid treatment. Proc Natl Acad Sci U S A. 1993;90:9601–9605
  13. Taneja R, Bouillet P, Boylan JF, et al. Reexpression of retinoic acid receptor (RAR) gamma or overexpression of RAR alpha or RAR beta in RAR gamma-null F9 cells reveals a partial functional redundancy between the three RAR types. Proc Natl Acad Sci U S A. 1995;92:7854–7858
  14. Taneja R, Roy B, Plassat JL, et al. Cell-type and promoter-context dependent retinoic acid receptor (RAR) redundancies for RAR beta 2 and Hoxa-1 activation in F9 and P19 cells can be artefactually generated by gene knockouts. Proc Natl Acad Sci U S A. 1996;93:6197–6202
  15. Chiba H, Clifford J, Metzger D, Chambon P. Specific and redundant functions of retinoid X Receptor/Retinoic acid receptor heterodimers in differentiation, proliferation, and apoptosis of F9 embryonal carcinoma cells. J Cell Biol. 1997;139:735–747
  16. Chiba H, Clifford J, Metzger D, Chambon P. Distinct retinoid X receptor-retinoic acid receptor heterodimers are differentially involved in the control of expression of retinoid target genes in F9 embryonal carcinoma cells. Mol Cell Biol. 1997;17:3013–3020
  17. Su D, Gudas LJ. Gene expression profiling elucidates a specific role for RARgamma in the retinoic acid induced differentiation of F9 teratocarcinoma stem cells. Biochem Pharmacol. 2008;75:1129–1160
  18. Korhonen J, Lahtinen I, Halmekyto M, et al. Endothelial-specific gene expression directed by the tie gene promoter in vivo. Blood. 1995;86:1828–1835
  19. Puri MC, Rossant J, Alitalo K, Bernstein A, Partanen J. The receptor tyrosine kinase TIE is required for integrity and survival of vascular endothelial cells. EMBO J. 1995;14:5884–5891
  20. Armstrong E, Korhonen J, Silvennoinen O, Cleveland JL, Lieberman MA, Alitalo R. Expression of tie receptor tyrosine kinase in leukemia cell lines. Leukemia. 1993;7:1585–1591
  21. Partanen J, Makela TP, Alitalo R, Lehvaslaiho H, Alitalo K. Putative tyrosine kinases expressed in K-562 human leukemia cells. Proc Natl Acad Sci U S A. 1990;87:8913–8917
  22. Hashiyama M, Iwama A, Ohshiro K, et al. Predominant expression of a receptor tyrosine kinase, TIE, in hematopoietic stem cells and B cells. Blood. 1996;87:93–101
  23. Iwama A, Hamaguchi I, Hashiyama M, Murayama Y, Yasunaga K, Suda T. Molecular cloning and characterization of mouse TIE and TEK receptor tyrosine kinase genes and their expression in hematopoietic stem cells. Biochem Biophys Res Commun. 1993;195:301–309
  24. Eklund L, Olsen BR. Tie receptors and their angiopoietin ligands are context-dependent regulators of vascular remodeling. Exp Cell Res. 2006;312:630–641
  25. Suri C, Jones PF, Patan S, et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 1996;87:1171–1180
  26. Sato TN, Tozawa Y, Deutsch U, et al. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature. 1995;376:70–74
  27. Dumont DJ, Gradwohl G, Fong GH, et al. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 1994;8:1897–1909
  28. Puri MC, Bernstein A. Requirement for the TIE family of receptor tyrosine kinases in adult but not fetal hematopoiesis. Proc Natl Acad Sci U S A. 2003;100:12753–12758
  29. Kontos CD, Cha EH, York JD, Peters KG. The endothelial receptor tyrosine kinase Tie1 activates phosphatidylinositol 3-kinase and Akt to inhibit apoptosis. Mol Cell Biol. 2002;22:1704–1713
  30. Kim I, Kim HG, So JN, Kim JH, Kwak HJ, Koh GY. Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3′-Kinase/Akt signal transduction pathway. Circ Res. 2000;86:24–29
  31. Porat RM, Grunewald M, Globerman A, et al. Specific induction of tie1 promoter by disturbed flow in atherosclerosis-prone vascular niches and flow-obstructing pathologies. Circ Res. 2004;94:394–401
  32. Korhonen J, Partanen J, Armstrong E, et al. Enhanced expression of the tie receptor tyrosine kinase in endothelial cells during neovascularization. Blood. 1992;80:2548–2555
  33. Hatva E, Kaipainen A, Mentula P, et al. Expression of endothelial cell-specific receptor tyrosine kinases and growth factors in human brain tumors. Am J Pathol. 1995;146:368–378
  34. Kaipainen A, Vlaykova T, Hatva E, et al. Enhanced expression of the tie receptor tyrosine kinase messenger RNA in the vascular endothelium of metastatic melanomas. Cancer Res. 1994;54:6571–6577
  35. Dumont DJ, Fong GH, Puri MC, Gradwohl G, Alitalo K, Breitman ML. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev Dyn. 1995;203:80–92
  36. De Palma M, Venneri MA, Galli R, et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell. 2005;8:211–226
  37. De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med. 2003;9:789–795
  38. Yue X, Favot P, Dunn TL, Cassady AI, Hume DA. Expression of mRNA encoding the macrophage colony-stimulating factor receptor (c-fms) is controlled by a constitutive promoter and tissue-specific transcription elongation. Mol Cell Biol. 1993;13:3191–3201
  39. Avivi A, Skorecki K, Yayon A, Givol D. Promoter region of the murine fibroblast growth factor receptor 2 (bek/KGFR) gene. Oncogene. 1992;7:1957–1962
  40. Chen-Konak L, Guetta-Shubin Y, Yahav H, et al. Transcriptional and post-translation regulation of the Tie1 receptor by fluid shear stress changes in vascular endothelial cells. FASEB J. 2003;17:2121–2123
  41. Boutet SC, Quertermous T, Fadel BM. Identification of an octamer element required for in vivo expression of the TIE1 gene in endothelial cells. Biochem J. 2001;360:23–29
  42. Evans T. Regulation of hematopoiesis by retinoid signaling. Exp Hematol. 2005;33:1055–1061
  43. Miano JM, Berk BC. Retinoids: versatile biological response modifiers of vascular smooth muscle phenotype. Circ Res. 2000;87:355–362
  44. Bohnsack BL, Lai L, Dolle P, Hirschi KK. Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Genes Dev. 2004;18:1345–1358
  45. Lai L, Bohnsack BL, Niederreither K, Hirschi KK. Retinoic acid regulates endothelial cell proliferation during vasculogenesis. Development. 2003;130:6465–6474
  46. Oikawa T, Okayasu I, Ashino H, Morita I, Murota S, Shudo K. Three novel synthetic retinoids, Re 80, Am 580 and Am 80, all exhibit anti-angiogenic activity in vivo. Eur J Pharmacol. 1993;249:113–116
  47. Majewski S, Szmurlo A, Marczak M, Jablonska S, Bollag W. Inhibition of tumor cell-induced angiogenesis by retinoids, 1,25-dihydroxyvitamin D3 and their combination. Cancer Lett. 1993;75:35–39
  48. Gaetano C, Catalano A, Illi B, et al. Retinoids induce fibroblast growth factor-2 production in endothelial cells via retinoic acid receptor alpha activation and stimulate angiogenesis in vitro and in vivo. Circ Res. 2001;88:E38–E47
  49. Lansink M, Koolwijk P, van Hinsbergh V, Kooistra T. Effect of steroid hormones and retinoids on the formation of capillary-like tubular structures of human microvascular endothelial cells in fibrin matrices is related to urokinase expression. Blood. 1998;92:927–938
  50. Saito A, Sugawara A, Uruno A, et al. All-trans retinoic acid induces in vitro angiogenesis via retinoic acid receptor: possible involvement of paracrine effects of endogenous vascular endothelial growth factor signaling. Endocrinology. 2007;148:1412–1423
  51. Purton LE, Dworkin S, Olsen GH, et al. RARgamma is critical for maintaining a balance between hematopoietic stem cell self-renewal and differentiation. J Exp Med. 2006;203:1283–1293
  52. Gaines P, Berliner N. Retinoids in myelopoiesis. J Biol Regul Homeost Agents. 2003;17:46–65
  53. Walkley CR, Olsen GH, Dworkin S, et al. A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell. 2007;129:1097–1110
  54. Suzuki T, Aizawa K, Matsumura T, Nagai R. Vascular implications of the Kruppel-like family of transcription factors. Arterioscler Thromb Vasc Biol. 2005;25:1135–1141
  55. Arceci RJ, King AA, Simon MC, Orkin SH, Wilson DB. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol. 1993;13:2235–2246
  56. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265–275
  57. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 1996;84:321–330
  58. North TE, de Bruijn MF, Stacy T, et al. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity. 2002;16:661–672
  59. Mayer W, Hemberger M, Frank HG, et al. Expression of the imprinted genes MEST/Mest in human and murine placenta suggests a role in angiogenesis. Dev Dyn. 2000;217:1–10
  60. Gillespie RF, Gudas LJ. Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARbeta(2), and Cyp26A1 in F9 embryonal carcinoma cells. J Mol Biol. 2007;372:298–316
  61. Gillespie RF, Gudas LJ. Retinoic acid receptor isotype specificity in F9 teratocarcinoma stem cells results from the differential recruitment of coregulators to retinoic response elements. J Biol Chem. 2007;282:33421–33434
  62. Loudig O, Maclean GA, Dore NL, Luu L, Petkovich M. Transcriptional co-operativity between distant retinoic acid response elements in regulation of Cyp26A1 inducibility. Biochem J. 2005;392:241–248
  63. Gudas LJ, Sporn MB, Roberts A. Cellular biology and biochemistry of the retinoids. In:  Sporn MB,  Roberts AB,  Goodman DS editor. The Retinoids: Biology, Chemistry, and Medicine. New York: Raven Press; 1994;p. 443–520
  64. Hummasti S, Tontonoz P. The peroxisome proliferator-activated receptor N-terminal domain controls isotype-selective gene expression and adipogenesis. Mol Endocrinol. 2006;20:1261–1275
  65. Hauksdottir H, Privalsky ML. DNA recognition by the aberrant retinoic acid receptors implicated in human acute promyelocytic leukemia. Cell Growth Differ. 2001;12:85–98
  66. Wang C, Song B. Cell-type-specific expression of the platelet-derived growth factor alpha receptor: a role for GATA-binding protein. Mol Cell Biol. 1996;16:712–723
  67. Murakami A, Thurlow J, Dickson C. Retinoic acid-regulated expression of fibroblast growth factor 3 requires the interaction between a novel transcription factor and GATA-4. J Biol Chem. 1999;274:17242–17248
  68. Murakami A, Shen H, Ishida S, Dickson C. SOX7 and GATA-4 are competitive activators of Fgf-3 transcription. J Biol Chem. 2004;279:28564–28573
  69. Bielinska M, Wilson DB. Regulation of J6 gene expression by transcription factor GATA-4. Biochem J. 1995;307(Pt 1):183–189
  70. Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F. The transcription factor GATA6 is essential for early extraembryonic development. Development. 1999;126:723–732
  71. Fujikura J, Yamato E, Yonemura S, et al. Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev. 2002;16:784–789
  72. Narita N, Bielinska M, Wilson DB. Cardiomyocyte differentiation by GATA-4-deficient embryonic stem cells. Development. 1997;124:3755–3764
  73. 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;127:1041–1055
  74. Futaki S, Hayashi Y, Emoto T, Weber CN, Sekiguchi K. Sox7 plays crucial roles in parietal endoderm differentiation in F9 embryonal carcinoma cells through regulating Gata-4 and Gata-6 expression. Mol Cell Biol. 2004;24:10492–10503
  75. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242–248
  76. Morrisey EE, Ip HS, Lu MM, Parmacek MS. GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev Biol. 1996;177:309–322
  77. Weiler-Guettler H, Yu K, Soff G, Gudas LJ, Rosenberg RD. Thrombomodulin gene regulation by cAMP and retinoic acid in F9 embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1992;89:2155–2159
  78. Hatzopoulos AK, Folkman J, Vasile E, Eiselen GK, Rosenberg RD. Isolation and characterization of endothelial progenitor cells from mouse embryos. Development. 1998;125:1457–1468
  79. Hong T, Grabel LB. Migration of F9 parietal endoderm cells is regulated by the ERK pathway. J Cell Biochem. 2006;97:1339–1349
  80. Takeda M, Kosaka M, Nishina Y, Sawada K, Matsumoto K, Nishimune Y. Teratocarcinoma F9 cells induced to differentiate with sodium butyrate produce both tissue-type and urokinase-type plasminogen activators. J Cell Biochem. 1992;49:284–289
  81. Niforas P, Chu MD, Bird P. A retinoic acid/cAMP-responsive enhancer containing a cAMP responsive element is required for the activation of the mouse thrombomodulin-encoding gene in differentiating F9 cells. Gene. 1996;176:139–147
  82. Oka T, Dai YS, Molkentin JD. Regulation of calcineurin through transcriptional induction of the calcineurin A beta promoter in vitro and in vivo. Mol Cell Biol. 2005;25:6649–6659
  83. Molkentin JD, Kalvakolanu DV, Markham BE. Transcription factor GATA-4 regulates cardiac muscle-specific expression of the alpha-myosin heavy-chain gene. Mol Cell Biol. 1994;14:4947–4957
  84. Mustapha Z, Pang L, Nattel S. Characterization of the cardiac KCNE1 gene promoter. Cardiovasc Res. 2007;73:82–91

PII: S0301-472X(08)00006-4

doi: 10.1016/j.exphem.2007.12.016

Experimental Hematology
Volume 36, Issue 5 , Pages 624-641 , May 2008