Mechanism for fetal hemoglobin induction by histone deacetylase inhibitors involves γ-globin activation by CREB1 and ATF-2

Blood

Volumn 108, Issue 10, 2006, Pages 3590-3599

  Sangerman, Jose ^b   Moo, Seung Lee ^b   Yao, Xiao ^b   Oteng, Eugene ^b   Hsiao, Cheng Hui ^b   Li, Wei ^b   Zein, Sima ^b   Ofori Acquah, Solomon F ^b   Pace, Betty S ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BUTYRIC ACID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA; GAMMA GLOBIN; HEMOGLOBIN; HISTONE DEACETYLASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; TRICHOSTATIN A;

ACETYLATION; ARTICLE; CONTROLLED STUDY; GENE INDUCTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 33751293605     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-01-023713     Document Type: Article

References (81)

1. Nagata Y, Todokoro K. JNK and p38 activation and ERK inhibition are required for environmental stress-induced erythroid differentiation and apoptosis. Blood. 1999;94:853-863.
2. Chin H, Wakao H, Miyajima A, Miyasaka N, Miura O. Erythropoietin induces tyrosine phosphorylation of the interleukin-3 receptor beta subunit (betaIL3) and recruitment of Stat5 to possible Stat5-docking sites in betaIL3. Blood. 1997;8:4327-4336.
3. Jacob-Helber SM, Ryan JJ, Sawyer S. JNK and p38 are activated by erythropoietin (EPO) but are not induced in apoptosis following EPO withdrawal in EPO-dependent HCD57 cells. Blood. 2000;96;933-940.
4. Dean JL, Brook M, Clark AR, Saklatvala J. p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes. J Biol Chem. 1999;274:264-269.
5. Steinbrech DS, Mehrara BJ, Saadeh PB, et al. VEGF expression in an osteoblast-like cell line is regulated by a hypoxia response mechanism. Am J Physiol Cell Physiol. 2000;278:C853-C860.
6. Nagata Y, Takahashi N, Davis RJ, Todokoro K. Activation of p38 MAP kinase and JNK but not ERK is required for erythropoietin-induced erythroid differentiation. Blood. 1998;92:1859-1869.
7. Tamura K, Sudo T, Senftleben U, Dadak AM, Johnson R, Karin M. Requirement for p38alpha in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell. 2000;102:221-231.
8. Yamashita T, Wakao H, Miyajima A, Asano S. Differentiation inducers modulate cytokine signaling pathways in a murine erythroleukemia cell line. Cancer Res. 1998;58:556-561.
9. Boosalis MS, Bandyopadhyay R, Bresnick EH, et al. Short-chain fatty acid derivatives stimulate cell proliferation and induce STAT-5 activation. Blood. 2001;97:3259-3267.
10. Pace BS, Qian X, Sangerman J, et al. p38 MAP kinase is required for fetal hemoglobin induction by butyrate and trichostatin. Exp Hematol. 2003;11:1089-1096.
11. Witt O, Sand K, Pekrum A. Butyrate-induced erythroid differentiation of human K562 leukemia cells involves inhibition of ERK and activation of p38 MAP kinase pathways. Blood. 2000;95:2391-2396.
12. Perrine SP, Ginder GD, Faller DV, et al. A short-term trial of butyrate to stimulate fetal-globin-gene expression in the beta-globin disorders. N Engl J Med. 1993;328:81-86.
13. Perrine SP, Olivieri NF, Faller DV, Vichinsky EP, Dover GJ, Ginder GD. Butyrate derivatives: new agents for stimulating fetal globin production in the beta-globin disorders. Am J Pediatr Hematol Oncol. 1994;16:67-71.
14. Weinberg RS, Ji X, Sutton M, et al. Butyrate increases the efficiency of translation of gamma-globin mRNA. Blood. 2005;105:1807-1809.
15. Witt O, Monkemeyer S, Ronndahl B, Reinhardt D, Kanbach K, Pekrun A. Induction of fetal hemoglobin expression by the histone deacetylase inhibitor apicidin. Blood. 2003;101:2001-2007.
16. Johnson J, Hunter R, McElveen R, Qian XH, Baliga BS, Pace BS. Fetal hemoglobin induction by the histone deacetylase inhibitor, scriptaid. Cell Mol Biol. 2005;51:229-238.
17. Balif BA, Blenis J. Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ. 2001;12:397-408.
18. Garrington TP, Johnson GL. Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr Opin Cell Biol. 1999;11:211-218.
19. Uddin S, Ah-Kang J, Ulaszek J, Mahmud D, Wickrema A. Differentiation stage-specific activation of p38 mitogen-activated protein kinase isoforms in primary human erythroid cells. Proc Natl Acad Sci U S A. 2004;101:147-152.
20. Eckert RL, Efimova T, Balasubramanian S, Crish JF, Bone F, Dashti S. p38 mitogen-activated protein kinases on the body surface - a function for p38 delta. J Invest Dermatol. 2003;120:823-828.
21. Chen Z, Gibson TB, Robinson F, et al. MAP kinases. Chem Rev. 2001;101:2449-2476.
22. Huang HM, Chang TW, Liu JC. Basic fibroblast growth factor antagonizes activin A-mediated growth inhibition and hemoglobin synthesis in K562 cells by activating ERK1/2 and deactivating p38 MAP kinase. Biochem Biophys Res Commun. 2004;320:1247-1252.
23. Dalby KN, Morrice N, Caldwell FB, Avruch J, Cohen P. Identification of regulatory phosphorylation sites in mitogen-activated protein kinase (MAPK)-activated protein kinase-1a/p90rsk that are inducible by MAPK. J Biol Chem. 1998;273:1496-1505.
24. Meng W, Swenson LL, Fitzgibbon MJ, et al. Structure of mitogen-activated protein kinase-activated protein (MAPKAP) kinase 2 suggests a bifunctional switch that couples kinase activation with nuclear export. J Biol Chem. 2002;277:37401-37405.
25. New L, Jiang Y, Zhao M, et al. PRAK, a novel protein kinase regulated by the p38 MAP kinase. EMBO J. 1998;17:3371-3384.
26. Krebs FC, Goodenow MM, Wigdahl B. Neuroglial ATF/CREB factors interact with the human immunodeficiency virus type 1 long terminal repeat. J Neurovirol. 1997;3(suppl 1):S28-S32.
27. Foulkes NS, Laoide BM, Schlotter F, Sassone-Corsi P. Transcriptional antagonist cAMP-responsive element modulator (CREM) down-regulates c-fos cAMP-induced expression. Proc Natl Acad Sci U S A. 1991;88:5448-5452.
28. Yoshida M, Horinouchi S, Beppu T. Trichostatin A and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function. Bioessays. 1995;17:423-430.
29. Monneret C. Histone deacetylase inhibitors. Eur J Med Chem. 2005;40:1-13.
30. Huo X, Zhang J. Important roles of reversible acetylation in the function of hematopoietic transcription factors. J Cell Mol Med. 2005;9:103-112.
31. Lam AL, Pazin DE, Sullivan BA. Control of gene expression and assembly of chromosomal subdomains by chromatin regulators with antagonistic functions. Chromosoma. 2005;114:242-251.
32. Pace BS, Chen XR, Thompson A, Goodman SR. Butyrate-inducible elements in the human gamma-globin promoter. Exp Hematol. 2000;28:283-293.
33. Smith RD, Malley JD, Schechter AN. Quantitative analysis of globin gene induction in single human erythroleukemic cells. Nucleic Acids Res. 2000;28:4998-5004.
34. Fibach E, Burke LP, Schechter AN, Noguchi CT, Rodgers GP. Hydroxyurea increases fetal hemoglobin in cultured erythroid cells derived from normal individuals and patients with sickle cell anemia or beta-thalassemia. Blood. 1993;81:1630-1635.
35. Sassone-Corsi P, Ransone LJ, Verma IM. Cross-talk in signal transduction: TPA-inducible factor jun/AP-1 activates cAMP-responsive enhancer elements. Oncogene. 1990;5:427-431.
36. Park JI, Strock CJ, Ball DW, Nelkin BD. The Ras/Raf/MEK/extracellular signal-regulated kinase pathway induces autocrine-paracrine growth inhibition via the leukemia inhibitory factor/JAK/STAT pathway. Mol Cell Biol. 2003;23:543-545.
37. Chung KC, Kim SM, Rhang S, Lau LF, Gomes I, Ahn YS. Expression of immediate early gene pip92 during anisomycin-induced cell death is mediated by the JNK- and p38-dependent activation of Elk1. Eur J Biochem. 2000;267:4676-4684.
38. Computational Biology and Informatics Laboratory, School of Medicine, University of Pennsylvania. TESS: Transcription Element Search System. http://www.cbil.upenn.edu/cgi-bin/tess/tess. Accessed December 10, 2005.
39. National Center for Biotechnology Information. Single Nucleotide Polymorphism. http://www.ncbi.nlm.nih.gov/SNP. Accessed.
40. Persengiev SP, Green MR. The role of ATF/CREB family members in cell growth, survival and apoptosis. Apoptosis. 2003;8:225-228.
41. Richards JP, Bachinger HP, Goodman RH, Brennan RG. Analysis of the structural properties of cAMP-responsive element-binding protein (CREB) and phosphorylated CREB. J Biol Chem. 1996;271:13716-13723.
42. Xu J, Zimmer D. Differential regulation of A gamma and G gamma fetal hemoglobin mRNA levels by hydroxyurea and butyrate. Exp Hematol. 1998;26:265-272.
43. Ao H, Ko SW, Zhuo M. CREB activity maintains the survival of cingulate cortical pyramidal neurons in the adult mouse brain. Mol Pain. 2006;2:15-18.
44. Walton M, Woodgate AM, Muravlev A, Xu R, During MJ, Dragunow M. CREB phosphorylation promotes nerve cell survival. J Neurochem. 1999;73:1836-1842.
45. Pissard S, Beuzard Y. A potential regulatory region for the expression of fetal hemoglobin in sickle cell disease. Blood. 1994;84:331-338.
46. Powars D, Hiti A. Sickle cell anemia: beta s gene cluster haplotypes as genetic markers for severe disease expression. Am J Dis Child. 1993;147:1197-1202.
47. Stamatoyannopoulos G, Grosveld F. Hemoglobin switching. In: Stamatoyannopoulos G, Majerus PW, Permutter RM, Varmus H, eds. The Molecular Basis of Blood Diseases. Philadelphia, PA: Saunders Press; 2001:135-185.
48. Bacolla A, Ulrich MJ, Larson JE, Ley TJ, Wells RD. An intramolecular triplex in the human gamma-globin 5′-flanking region is altered by point mutations associated with hereditary persistence of fetal hemoglobin. J Biol Chem. 1995;270:24556-24563.
49. Efremov DG, Dimovski AJ, Huisman TH. The -158 (C-T) promoter mutation is responsible for the increased transcription of the 3′ gamma gene in the Atlanta type of hereditary persistence of fetal hemoglobin. Blood. 1998;83:3350-3355.
50. Poillon WN, Kim BC, Castro O. Intracellular hemoglobin S polymerization and the clinical severity of sickle cell anemia. Blood. 1998;91:1777-1783.
51. Rahmani M, Reese E, Dai Y, et al. Cotreatment with suberanoylanilide hydroxamic acid and 17-allylamino 17-demethoxygeldanamycin synergistically induces apoptosis in Bcr-Abl+ cells sensitive and resistant to STI571 (imatinib mesylate) in association with down-regulation of Bcr-Abl, abrogation of signal transducer and activator of transcription 5 activity, and Bax conformational change. Mol Pharmacol. 2005;67:1166-1176.
52. Hsiao CH, Li W, Lou TF, Baliga BS, Pace BS. Fetal hemoglobin induction by histone deacetylase inhibitors involves generation of reactive oxygen species. Exp Hematol. 2006;34:264-273.
53. Witt O, Monkemeyer S, Kanbach K, Pekrun A. Induction of fetal hemoglobin synthesis by valproate: modulation of MAP kinase pathways. Am J Hematol. 2002;71:45-46.
54. Candido EP, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 1978;14:105-113.
55. de Haan JB, Gevers W, Parker MI. Effects of sodium butyrate on the synthesis and methylation of DNA in normal cells and their transformed counterparts. Cancer Res. 1986;46:713-716.
56. Kunkel TA, Katarzyna B, McClary J. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 1991;204:125-139.
57. Archer SY, Meng S, Shei A, Hodin RA. p21(WAF1) is required for butyrate-mediated growth inhibition of human colon cancer cells. Proc Natl Acad Sci U S A. 1998;95:6791-6796.
58. Pellizzaro C, Coradini D, Daniotti A, Abolafio G, Daidone MG. Modulation of cell cycle-related protein expression by sodium butyrate in human non-small cell lung cancer cell lines. Int J Cancer. 2001;91:654-657.
59. Lallemand F, Courilleau D, Sabbah M, Redeuilh G, Mester J. Direct inhibition of the expression of cyclin D1 gene by sodium butyrate. Biochem Biophys Res Commun. 1996;229:163-169.
60. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 1997;389:349-352.
61. Radhakrishnan I, Perez-Alvarado GC, Parker D, Dyson HJ, Montminy MR, Wright PE. Structural analyses of CREB-CBP transcriptional activator-coactivator complexes by NMR spectroscopy: implications for mapping the boundaries of structural domains. Mol Biol. 1999;287:859-865.
62. Johannessen M, Delghandi MP, Moens U. What turns CREB on? Cell Signal. 2004;16:1211-1227.
63. van Dam H, Duyndam M, Rottier R, et al. Heterodimer formation of cJun and ATF-2 is responsible for induction of c-jun by the 243 amino acid adenovirus E1A protein. EMBO J. 1993;12:479-487.
64. Quinn PG. Mechanisms of basal and kinase-inducible transcription activation by CREB. Proc Nucleic Acid Res Mol Biol. 2002;72:269-305.
65. Davis S, Vanhoutte P, Pages C, Cabouche J, Larouche S. The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci. 2000;20:4563-4572.
66. Rosenberg D, Groussin L, Jullian E, Perlemoine K, Bertagna X, Bertherat J. Role of the PKA-regulated transcription factor CREB in development and tumorigenesis of endocrine tissues. Ann N Y Acad Sci. 2002;968:65-74.
67. Inoue A, Kuroyanagi Y, Terui K, Moi P, Ikuta T. Negative regulation of gamma-globin gene expression by cyclic AMP-dependent pathway in erythroid cells. Exp Hematol. 2004;32:244-253.
68. Adler V, Polotskaya A, Kim J, et al. Dose rate and mode of exposure are key factors in JNK activation by UV irradiation. Carcinogenesis. 1996;17:2073-2076.
69. Tsukiyama T, Wu C. Chromatin remodeling and transcription. Curr Opin Genet Dev. 1997;7:182-191.
70. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 1997;389:349-352.
71. McCaffrey PG, Newsome DA, Fibach E, Yoshida M, Su MS. Induction of gamma-globin by histone deacetylase inhibitors. Blood. 1997;90:2075-2083.
72. Ikuta T, Kan YW, Swerdlow PS, Faller DV, Perrine SP. Alterations in protein-DNA interactions in the gamma-globin gene promoter in response to butyrate therapy. Blood. 1998;92:2924-2933.
73. Hodny Z, Li R, Barath P, Nelson BD. Sp1 and chromatin environment are important contributors to the formation of repressive chromatin structures on the transfected human adenine nucleotide translocase-2 promoter. Biochem J. 2000;346:93-97.
74. Nakano K, Mizuno T, Sowa Y, et al. Butyrate activates the WAF1/Cip1 gene promoter through Sp1 sites in a p53-negative human colon cancer cell line. J Biol Chem. 1997;272:22199-22206.
75. Sowa Y, Orita T, Minamikawa S, et al. Histone deacetylase inhibitor activates the WAF1/Cip1 gene promoter through the Sp1 sites. Biochem Biophys Res Commun. 1997;241:142-150.
76. Doetzlhofer A, Rotheneder H, Lagger G, et al. Histone deacetylase 1 can repress transcription by binding to Sp1. Mol Cell Biol. 1999;19:5504-5511.
77. Walker GE, Wilson EM, Powell D, Oh Y. Butyrate, a histone deacetylase inhibitor, activates the human IGF binding protein-3 promoter in breast cancer cells: molecular mechanism involves a Sp1/Sp3 multiprotein complex. Endocrinology. 2001;142:3817-3827.
78. 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.
79. Ofori-Acquah SF, Lalloz MR, Layton DM. Nucleotide variation regulates the level of enhancement by hypersensitive site 2 of the beta-globin locus control region. Blood Cells Mol Dis. 2001;27:803-811.
80. Washburn BK, Esposito RE. Identification of the Sin3-binding site in Ume6 defines a two-step process for conversion of Ume6 from a transcriptional repressor to an activator in yeast. Mol Cell Biol. 2001;21:2057-2069.
81. Fazzio TG, Kooperberg C, Goldmark JP, et al. Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression. Mol Cell Biol. 2001;21:6450-6460.