Pharmacologic induction of fetal hemoglobin production

Hematology/Oncology Clinics of North America

Volumn 24, Issue 6, 2010, Pages 1131-1144

  Atweh, George ^a   Fathallah, Hassana ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Fetal hemoglobin expression; Gene regulation; Globin; Sickle cell; Thalassemia

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; 6 (1,3 DIOXO 1H,3H BENZO[DE]ISOQUINOLIN 2 YL) N HYDROXYHEXANAMIDE; APICIDIN; AZACITIDINE; BETA GLOBIN; BUTYRIC ACID; DELTA GLOBIN; DNA METHYLTRANSFERASE INHIBITOR; EPSILON GLOBIN; ERYTHROPOIETIN; GAMMA GLOBIN; HEMOGLOBIN; HEMOGLOBIN A; HEMOGLOBIN A2; HEMOGLOBIN F; HISTONE DEACETYLASE INHIBITOR; HYDROXYUREA; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE;

DRUG MECHANISM; ERYTHROCYTE; ERYTHROPOIESIS; GENE CONTROL; GENE EXPRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ADULT; AZACITIDINE; DNA METHYLATION; ENZYME INHIBITORS; FETAL HEMOGLOBIN; GAMMA-GLOBINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMOGLOBINOPATHIES; HUMANS;

EID: 78249266598     PISSN: 08898588     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hoc.2010.08.001     Document Type: Review

References (100)

1. Rochette J., Craig J.E., Thein S.L. Fetal hemoglobin levels in adults. Blood Rev 1994, 8:213-224.
2. Bailey K., Morris J.S., Thomas P., et al. Fetal haemoglobin and early manifestations of homozygous sickle cell disease. Arch Dis Child 1992, 67:517-520.
3. Stevens M.C., Hayes R.J., Vaidya S., et al. Fetal hemoglobin and clinical severity of homozygous sickle cell disease in early childhood. J Pediatr 1981, 98:37-41.
4. Bollekens J.A., Forget B.G. Delta beta thalassemia and hereditary persistence of fetal hemoglobin. Hematol Oncol Clin North Am 1991, 5:399-422.
5. Serjeant G.R. Natural history and determinants of clinical severity of sickle cell disease. Curr Opin Hematol 1995, 2:103-108.
6. Perrine R.P., Pembrey M.E., John P., et al. Natural history of sickle cell anemia in Saudi Arabs. A study of 270 subjects. Ann Intern Med 1978, 88:1-6.
7. Kar B.C., Satapathy R.K., Kulozik A.E., et al. Sickle cell disease in Orissa State, India. Lancet 1986, 2:1198-1201.
8. Platt O.S., Thorington B.D., Brambilla D.J., et al. Pain in sickle cell disease. Rates and risk factors. N Engl J Med 1991, 325:11-16.
9. Castro O., Brambilla D.J., Thorington B., et al. The acute chest syndrome in sickle cell disease: incidence and risk factors. The cooperative study of sickle cell disease. Blood 1994, 84:643-649.
10. Platt O.S., Brambilla D.J., Rosse W.F., et al. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med 1994, 330:1639-1644.
11. Goodwin A.J., McInerney J.M., Glander M.A., et al. 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.
12. Martin D.I., Orkin S.H. Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1. Genes Dev 1990, 4:1886-1898.
13. Ney P.A., Sorrentino B.P., Lowrey C.H., et al. Inducibility of the HS II enhancer depends on binding of an erythroid specific nuclear protein. Nucleic Acids Res 1990, 18:6011-6017.
14. Im H., Grass J.A., Johnson K.D., et al. Chromatin domain activation via GATA-1 utilization of a small subset of dispersed GATA motifs within a broad chromosomal region. Proc Natl Acad Sci U S A 2005, 102:17065-17070.
15. Zhou D., Pawlik K.M., Ren J., et al. Differential binding of erythroid Krupple-like factor to embryonic/fetal globin gene promoters during development. J Biol Chem 2006, 281:16052-16057.
16. Forrester W.C., Takegawa S., Papayannopoulou T., et al. Evidence for a locus activation region: the formation of developmentally stable hypersensitive sites in globin-expressing hybrids. Nucleic Acids Res 1987, 15:10159-10177.
17. Grosveld F., van Assendelft G.B., Greaves D.R., et al. Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell 1987, 51:975-985.
18. Kollias G., Wrighton N., Hurst J., et al. Regulated expression of human A gamma-, beta-, and hybrid gamma beta-globin genes in transgenic mice: manipulation of the developmental expression patterns. Cell 1986, 46:89-94.
19. Navas P.A., Peterson K.R., Li Q., et al. Developmental specificity of the interaction between the locus control region and embryonic or fetal globin genes in transgenic mice with an HS3 core deletion. Mol Cell Biol 1998, 18:4188-4196.
20. Miller I.J., Bieker J.J. A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Kruppel family of nuclear proteins. Mol Cell Biol 1993, 13:2776-2786.
21. Jackson D.A., McDowell J.C., Dean A. Beta-globin locus control region HS2 and HS3 interact structurally and functionally. Nucleic Acids Res 2003, 31:1180-1190.
22. Enver T., Raich N., Ebens A.J., et al. Developmental regulation of human fetal-to-adult globin gene switching in transgenic mice. Nature 1990, 344:309-313.
23. Strouboulis J., Dillon N., Grosveld F. Developmental regulation of a complete 70-kb human beta-globin locus in transgenic mice. Genes Dev 1992, 6:1857-1864.
24. Townes T.M., Behringer R.R. Human globin locus activation region (LAR): role in temporal control. Trends Genet 1990, 6:219-223.
25. Forrester W.C., Epner E., Driscoll M.C., et al. A deletion of the human beta-globin locus activation region causes a major alteration in chromatin structure and replication across the entire beta-globin locus. Genes Dev 1990, 4:1637-1649.
26. Bender M.A., Bulger M., Close J., et al. Beta-globin gene switching and DNase I sensitivity of the endogenous beta-globin locus in mice do not require the locus control region. Mol Cell 2000, 5:387-393.
27. Arcasoy M.O., Romana M., Fabry M.E., et al. High levels of human gamma-globin gene expression in adult mice carrying a transgene of deletion-type hereditary persistence of fetal hemoglobin. Mol Cell Biol 1997, 17:2076-2089.
28. Drissen R., Palstra R.J., Gillemans N., et al. The active spatial organization of the beta-globin locus requires the transcription factor EKLF. Genes Dev 2004, 18:2485-2490.
29. Kooren J., Palstra R.J., Klous P., et al. Beta-globin active chromatin Hub formation in differentiating erythroid cells and in p45 NF-E2 knock-out mice. J Biol Chem 2007, 282:16544-16552.
30. Layon M.E., Ackley C.J., West R.J., et al. Expression of GATA-1 in a non-hematopoietic cell line induces beta-globin locus control region chromatin structure remodeling and an erythroid pattern of gene expression. J Mol Biol 2007, 366(3):737-744.
31. Asano H., Li X.S., Stamatoyannopoulos G. FKLF-2: a novel Kruppel-like transcriptional factor that activates globin and other erythroid lineage genes. Blood 2000, 95:3578-3584.
32. Zhou W., Clouston D.R., Wang X., et al. Induction of human fetal globin gene expression by a novel erythroid factor, NF-E4. Mol Cell Biol 2000, 20:7662-7672.
33. Zhou W., Zhao Q., Sutton R., et al. The role of p22 NF-E4 in human globin gene switching. J Biol Chem 2004, 279:26227-26232.
34. Song S.H., Hou C., Dean A. A positive role for NLI/Ldb1 in long-range beta-globin locus control region function. Mol Cell 2007, 28:810-822.
35. Ley T.J., DeSimone J., Anagnou N.P., et al. 5-azacytidine selectively increases gamma-globin synthesis in a patient with beta+ thalassemia. N Engl J Med 1982, 307:1469-1475.
36. Ley T.J., DeSimone J., Noguchi C.T., et al. 5-Azacytidine increases gamma-globin synthesis and reduces the proportion of dense cells in patients with sickle cell anemia. Blood 1983, 62:370-380.
37. Fucharoen S., Siritanaratkul N., Winichagoon P., et al. Hydroxyurea increases hemoglobin F levels and improves the effectiveness of erythropoiesis in beta-thalassemia/hemoglobin E disease. Blood 1996, 87:887-892.
38. Charache S., Dover G.J., Moore R.D., et al. Hydroxyurea: effects on hemoglobin F production in patients with sickle cell anemia. Blood 1992, 79:2555-2565.
39. Olivieri N.F., Freedman M.H., Perrine S.P., et al. Trial of recombinant human erythropoietin: three patients with thalassemia intermedia. Blood 1992, 80:3258-3260.
40. Nagel R.L., Vichinsky E., Shah M., et al. F reticulocyte response in sickle cell anemia treated with recombinant human erythropoietin: a double-blind study. Blood 1993, 81:9-14.
41. Atweh G.F., Sutton M., Nassif I., et al. Sustained induction of fetal hemoglobin by pulse butyrate therapy in sickle cell disease. Blood 1999, 93:1790-1797.
42. Perrine S.P., Ginder G.D., Faller D.V., 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.
43. Mavilio F., Giampaolo A., Care A., et al. Molecular mechanisms of human hemoglobin switching: selective undermethylation and expression of globin genes in embryonic, fetal, and adult erythroblasts. Proc Natl Acad Sci U S A 1983, 80:6907-6911.
44. van der Ploeg L.H., Flavell R.A. DNA methylation in the human gamma delta beta-globin locus in erythroid and nonerythroid tissues. Cell 1980, 19:947-958.
45. Kaminskas E., Farrell A.T., Wang Y.C., et al. FDA drug approval summary: azacitidine (5-azacytidine, Vidaza) for injectable suspension. Oncologist 2005, 10:176-182.
46. Silverman L.R., Demakos E.P., Peterson B.L., et al. Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: a study of the cancer and leukemia group B. J Clin Oncol 2002, 20:2429-2440.
47. DeSimone J., Heller P., Hall L., et al. 5-Azacytidine stimulates fetal hemoglobin synthesis in anemic baboons. Proc Natl Acad Sci U S A 1982, 79:4428-4431.
48. DeSimone J., Heller P., Schimenti J.C., et al. Fetal hemoglobin production in adult baboons by 5-azacytidine or by phenylhydrazine-induced hemolysis is associated with hypomethylation of globin gene DNA. Prog Clin Biol Res 1983, 134:489-500.
49. Charache S., Dover G., Smith K., et al. Treatment of sickle cell anemia with 5-azacytidine results in increased fetal hemoglobin production and is associated with nonrandom hypomethylation of DNA around the gamma-delta-beta-globin gene complex. Proc Natl Acad Sci U S A 1983, 80:4842-4846.
50. Lowrey C.H., Nienhuis A.W. Brief report: treatment with azacitidine of patients with end-stage beta-thalassemia. N Engl J Med 1993, 329:845-848.
51. Carr B.I., Rahbar S., Asmeron Y., et al. Carcinogenicity and haemoglobin synthesis induction by cytidine analogues. Br J Cancer 1988, 57:395-402.
52. DeSimone J., Koshy M., Dorn L., et al. Maintenance of elevated fetal hemoglobin levels by decitabine during dose interval treatment of sickle cell anemia. Blood 2002, 99:3905-3908.
53. Koshy M., Dorn L., Bressler L., et al. 2-deoxy 5-azacytidine and fetal hemoglobin induction in sickle cell anemia. Blood 2000, 96:2379-2384.
54. Saunthararajah Y., Hillery C.A., Lavelle D., et al. Effects of 5-aza-2'-deoxycytidine on fetal hemoglobin levels, red cell adhesion, and hematopoietic differentiation in patients with sickle cell disease. Blood 2003, 102:3865-3870.
55. Yang A.S., Estecio M.R., Garcia-Manero G., et al. Comment on " Chromosomal instability and tumors promoted by DNA hypomethylation" and " Induction of tumors in nice by genomic hypomethylation" Science 2003, 302:1153. [author reply 1153].
56. Belinsky S.A., Klinge D.M., Stidley C.A., et al. Inhibition of DNA methylation and histone deacetylation prevents murine lung cancer. Cancer Res 2003, 63:7089-7093.
57. Laird P.W., Jackson-Grusby L., Fazeli A., et al. Suppression of intestinal neoplasia by DNA hypomethylation. Cell 1995, 81:197-205.
58. Humphries R.K., Dover G., Young N.S., et al. 5-Azacytidine acts directly on both erythroid precursors and progenitors to increase production of fetal hemoglobin. J Clin Invest 1985, 75:547-557.
59. Jane S.M., Gumucio D.L., Ney P.A., et al. Methylation-enhanced binding of Sp1 to the stage selector element of the human gamma-globin gene promoter may regulate development specificity of expression. Mol Cell Biol 1993, 13:3272-3281.
60. Sengupta P.K., Lavelle D., DeSimone J. Increased binding of Sp1 to the gamma-globin gene promoter upon site-specific cytosine methylation. Am J Hematol 1994, 46:169-172.
61. Lavelle D.E. The molecular mechanism of fetal hemoglobin reactivation. Semin Hematol 2004, 41:3-10.
62. Letvin N.L., Linch D.C., Beardsley G.P., et al. Augmentation of fetal-hemoglobin production in anemic monkeys by hydroxyurea. N Engl J Med 1984, 310:869-873.
63. Stamatoyannopoulos G. Control of globin gene expression during development and erythroid differentiation. Exp Hematol 2005, 33:259-271.
64. Mabaera R., Greene M.R., Richardson C.A., et al. Neither DNA hypomethylation nor changes in the kinetics of erythroid differentiation explain 5-azacytidine's ability to induce human fetal hemoglobin. Blood 2008, 111:411-420.
65. Fathallah H., Weinberg R.S., Galperin Y., et al. Role of epigenetic modifications in normal globin gene regulation and butyrate-mediated induction of fetal hemoglobin. Blood 2007, 110:3391-3397.
66. Yin W., Barkess G., Fang X., et al. Histone acetylation at the human {beta}-globin locus changes with developmental age. Blood 2007, 110(12):4101-4107.
67. Cao H., Stamatoyannopoulos G., Jung M. Induction of human gamma globin gene expression by histone deacetylase inhibitors. Blood 2004, 103:701-709.
68. Pace B.S., Qian X.H., Sangerman J., et al. p38 MAP kinase activation mediates gamma-globin gene induction in erythroid progenitors. Exp Hematol 2003, 31:1089-1096.
69. Cao H. Pharmacological induction of fetal hemoglobin synthesis using histone deacetylase inhibitors. Hematology 2004, 9:223-233.
70. Witt O., Monkemeyer S., Ronndahl G., et al. Induction of fetal hemoglobin expression by the histone deacetylase inhibitor apicidin. Blood 2003, 101:2001-2007.
71. Ginder G.D., Whitters M.J., Pohlman J.K. Activation of a chicken embryonic globin gene in adult erythroid cells by 5-azacytidine and sodium butyrate. Proc Natl Acad Sci U S A 1984, 81:3954-3958.
72. Bard H., Prosmanne J. Relative rates of fetal hemoglobin and adult hemoglobin synthesis in cord blood of infants of insulin-dependent diabetic mothers. Pediatrics 1985, 75:1143-1147.
73. Perrine S.P., Greene M.F., Faller D.V. Delay in the fetal globin switch in infants of diabetic mothers. N Engl J Med 1985, 312:334-338.
74. Constantoulakis P., Knitter G., Stamatoyannopoulos G. On the induction of fetal hemoglobin by butyrates: in vivo and in vitro studies with sodium butyrate and comparison of combination treatments with 5-AzaC and AraC. Blood 1989, 74:1963-1971.
75. Perrine S.P., Rudolph A., Faller D.V., et al. Butyrate infusions in the ovine fetus delay the biologic clock for globin gene switching. Proc Natl Acad Sci U S A 1988, 85:8540-8542.
76. Sher G.D., Ginder G.D., Little J., et al. Extended therapy with intravenous arginine butyrate in patients with beta-hemoglobinopathies. N Engl J Med 1995, 332:1606-1610.
77. Perrine S.P., Yang Y.M., Piga A., et al. Butyrate + EPO in beta thalassemia intermedia: interim findings of a phase II trial. Blood 2002, 100:47a.
78. Collins A.F., Pearson H.A., Giardina P., et al. Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: a clinical trial. Blood 1995, 85:43-49.
79. Reich S., Buhrer C., Henze G., et al. Oral isobutyramide reduces transfusion requirements in some patients with homozygous beta-thalassemia. Blood 2000, 96:3357-3363.
80. Ikuta T., Kan Y.W., Swerdlow P.S., et al. Alterations in protein-DNA interactions in the gamma-globin gene promoter in response to butyrate therapy. Blood 1998, 92:2924-2933.
81. Ikuta T., Ausenda S., Cappellini M.D. Mechanism for fetal globin gene expression: role of the soluble guanylate cyclase-cGMP-dependent protein kinase pathway. Proc Natl Acad Sci U S A 2001, 98:1847-1852.
82. McElveen R.L., Lou T.F., Reese K., et al. Erk pathway inhibitor U0126 induces gamma-globin expression in erythroid cells. Cell Mol Biol (Noisy-le-grand) 2005, 51:215-227.
83. Weinberg R.S., Ji X., Sutton M., et al. Butyrate increases the efficiency of translation of gamma-globin mRNA. Blood 2005, 105:1807-1809.
84. Rodgers G.P., Dover G.J., Noguchi C.T., et al. Hematologic responses of patients with sickle cell disease to treatment with hydroxyurea. N Engl J Med 1990, 322:1037-1045.
85. Platt O.S., Orkin S.H., Dover G., et al. Hydroxyurea enhances fetal hemoglobin production in sickle cell anemia. J Clin Invest 1984, 74:652-656.
86. Steinberg M.H., Lu Z.H., Barton F.B., et al. Fetal hemoglobin in sickle cell anemia: determinants of response to hydroxyurea. Multicenter Study of Hydroxyurea. Blood 1997, 89:1078-1088.
87. Charache S., Terrin M.L., Moore R.D., et al. Effect of hydroxyurea on the frequency of painful crises in sickle cell anemia. Investigators of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia. N Engl J Med 1995, 332:1317-1322.
88. Rigano P., Manfre L., La Galla R., et al. Clinical and hematological response to hydroxyurea in a patient with Hb Lepore/beta-thalassemia. Hemoglobin 1997, 21:219-226.
89. Cario H., Wegener M., Debatin K.M., et al. Treatment with hydroxyurea in thalassemia intermedia with paravertebral pseudotumors of extramedullary hematopoiesis. Ann Hematol 2002, 81:478-482.
90. de Paula E.V., Lima C.S., Arruda V.R., et al. Long-term hydroxyurea therapy in beta-thalassaemia patients. Eur J Haematol 2003, 70:151-155.
91. Hajjar F.M., Pearson H.A. Pharmacologic treatment of thalassemia intermedia with hydroxyurea. J Pediatr 1994, 125:490-492.
92. Zimmerman S.A., Schultz W.H., Davis J.S., et al. Sustained long-term hematologic efficacy of hydroxyurea at maximum tolerated dose in children with sickle cell disease. Blood 2004, 103:2039-2045.
93. Cokic V.P., Smith R.D., Beleslin-Cokic B.B., et al. Hydroxyurea induces fetal hemoglobin by the nitric oxide-dependent activation of soluble guanylyl cyclase. J Clin Invest 2003, 111:231-239.
94. Conran N., Oresco-Santos C., Acosta H.C., et al. Increased soluble guanylate cyclase activity in the red blood cells of sickle cell patients. Br J Haematol 2004, 124:547-554.
95. Nahavandi M., Tavakkoli F., Wyche M.Q., et al. Nitric oxide and cyclic GMP levels in sickle cell patients receiving hydroxyurea. Br J Haematol 2002, 119:855-857.
96. Cokic V.P., Andric S.A., Stojilkovic S.S., et al. Hydroxyurea nitrosylates and activates soluble guanylyl cyclase in human erythroid cells. Blood 2008, 111:1117-1123.
97. Keefer J.R., Schneidereith T.A., Mays A., et al. Role of cyclic nucleotides in fetal hemoglobin induction in cultured CD34+ cells. Exp Hematol 2006, 34:1151-1161.
98. Bailey L., Kuroyanagi Y., Franco-Penteado C.F., et al. Expression of the gamma-globin gene is sustained by the cAMP-dependent pathway in beta-thalassaemia. Br J Haematol 2007, 138:382-395.
99. Tang D.C., Zhu J., Liu W., et al. The hydroxyurea-induced small GTP-binding protein SAR modulates gamma-globin gene expression in human erythroid cells. Blood 2005, 106:3256-3263.
100. Powars D.R., Weiss J.N., Chan L.S., et al. Is there a threshold level of fetal hemoglobin that ameliorates morbidity in sickle cell anemia?. Blood 1984, 63:921-926.