Transcriptional regulation of fetal to adult hemoglobin switching: New therapeutic opportunities

Blood

Volumn 117, Issue 15, 2011, Pages 3945-3953

  Wilber, Andrew ^a   Nienhuis, Arthur W ^b   Persons, Derek A ^b  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ALPHA GLOBIN; AZACITIDINE; DEOXYRIBONUCLEASE I; GAMMA GLOBIN; HEMOGLOBIN; HEMOGLOBIN F; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; KRUPPEL LIKE FACTOR; LENTIVIRUS VECTOR; PROTEIN ARGININE METHYLTRANSFERASE; SHORT HAIRPIN RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCL11A; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR NF E2; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR SOX6; UNCLASSIFIED DRUG;

BETA THALASSEMIA; DISEASE SEVERITY; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVE SITE; EPIGENETICS; ERYTHROID CELL; ERYTHROLEUKEMIA CELL; ERYTHROPOIESIS; GENE EXPRESSION; GENE INTERACTION; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE SWITCHING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC LINKAGE; HEMATOPOIETIC STEM CELL; HEMOGLOBIN BLOOD LEVEL; HEMOGLOBIN SWITCHING; HEMOGLOBIN SYNTHESIS; HETEROZYGOTE; HISTONE MODIFICATION; HISTONE UBIQUITINATION; HOMOZYGOTE; HOUSEKEEPING GENE; HUMAN; INTRON; LEUKEMOGENESIS; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE TRAIT LOCUS; REVIEW; RNA INTERFERENCE; SICKLE CELL ANEMIA; SINGLE NUCLEOTIDE POLYMORPHISM; SUMOYLATION; THALASSEMIA; TRANSCRIPTION REGULATION; TRANSGENE; UPREGULATION; VIRAL GENE DELIVERY SYSTEM;

EID: 79954568538     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-11-316893     Document Type: Review

References (100)

1. Korber E. Uber Differengen des Blufarstoffs. Inaugural dissertation. Universität Dorpat. 1866.
2. von Kruger F. Z. Biol. 1888;24:318.
3. Brinkman R, Wildschut A, Wittermans A. On the occurrence of two kinds of haemoglobin in normal human blood. J Physiol. 1934;80(4):377-387.
4. Garner C, Tatu. T, Game L, et al. A candidate gene study of F cell levels in sibling pairs using a joint linkage and association analysis. Gene Screen. 2000;1(1):9-14.
5. Thein SL, Sampietro M, Rohde K, et al. Detection of a major gene for heterocellular hereditary persistence of fetal hemoglobin after accounting for genetic modifiers. Am J Hum Genet. 1994;54(2):214-228. (Pubitemid 24046333)
6. Menzel S, Garner C, Gut I, et al. A QTL influencing F cell production maps to a gene encoding a zinc-finger protein on chromosome 2p15. Nat Genet. 2007;39(10):1197-1199. (Pubitemid 47482679)
7. Donze D, Townes TM, Bieker JJ. Role of erythroid Kruppel-like factor in human gamma-to beta-globin gene switching. J Biol Chem. 1995;270(4):1955-1959.
8. 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(13):3434-3442. (Pubitemid 34760575)
9. Lauer J, Shen CK, Maniatis T. The chromosomal arrangement of human alpha-like globin genes: sequence homology and alpha-globin gene deletions. Cell. 1980;20(1):119-130. (Pubitemid 10117306)
10. Efstratiadis A, Posakony JW, Maniatis T, et al. The structure and evolution of the human betaglobin gene family. Cell. 1980;21(3):653-668. (Pubitemid 10022874)
11. Maniatis T, Fritsch EF, Lauer J, Lawn RM. The molecular genetics of human hemoglobins. Annu Rev Genet. 1980;14:145-178.
12. Tiemeier DC, Tilghman SM, Polsky FI, et al. A comparison of two cloned mouse beta-globin genes and their surrounding and intervening sequences. Cell. 1978;14(2):237-245. (Pubitemid 8369825)
13. Higgs DR, Vickers MA, Wilkie AO, et al. A review of the molecular genetics of the human alphaglobin gene cluster. Blood. 1989;73(5):1081-1104. (Pubitemid 19107407)
14. Stamatoyannopoulos G. Control of globin gene expression during development and erythroid differentiation. Exp Hematol. 2005;33(3):259-271. (Pubitemid 40261307)
15. Weatherall DJ. Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat Rev Genet. 2001;2(4):245-255. (Pubitemid 33674773)
16. Higgs DR, Weatherall DJ. The alpha thalassaemias. Cell Mol Life Sci. 2009;66:1154-1162.
17. Dover GJ, Boyer SH. Quantitation of hemoglobins within individual red cells: asynchronous biosynthesis of fetal and adult hemoglobin during erythroid maturation in normal subjects. Blood. 1980;56(6):1082-1091. (Pubitemid 11205065)
18. Thorpe SJ, Thein SL, Sampietro M, et al. Immunochemical estimation of haemoglobin types in red blood cells by FACS analysis. Br J Haematol. 1994;87(1):125-132. (Pubitemid 24207010)
19. Wheeler JT, Krevans JR. The homozygous state of persistent fetal hemoglobin and the interaction of persistent fetal hemoglobin with thalassemia. Bull Johns Hopkins Hosp. 1961;109:217-233.
20. Fessas P, Stamatoyannopoulos G, Karaklis A. Observations on the hereditary persistence of fetal hemoglobin. Iatriki. 1962;1:487.
21. Weatherall DJ. The thalassaemias. BMJ. 1997;314(7095):1675-1678. (Pubitemid 27232041)
22. Gazouli M, Katsantoni E, Kosteas T, Anagnou NP. Persistent fetal gamma-globin expression in adult transgenic mice following deletion of two silencer elements located 3' to the human Agammaglobin gene. Mol Med. 2009;15(11):415-424.
23. Katsantoni EZ, Langeveld A, Wai AW, et al. Persistent gamma-globin expression in adult transgenic mice is mediated by HPFH-2, HPFH-3 and HPFH-6 breakpoint sequences. Blood. 2003;102(9):3412-3419. (Pubitemid 37314784)
24. Pembrey ME, Wood WG, Weatherall DJ, Perrine RP. Fetal haemoglobin production and the sickle gene in the oases of Eastern Saudi Arabia. Br J Haematol. 1978;40(3):415-429. (Pubitemid 9027677)
25. Nienhuis AW, Stamatoyannopoulos G. Hemoglobin switching. Cell. 1978;15(1):307-315.
26. Nienhuis AW, Anderson WF. Hemoglobin switching in sheep and goats: change in functional globin messenger RNAin reticulocytes and bone marrow cells. Proc Natl Acad Sci U S A. 1972;69(8):2184-2188.
27. De Simone J, Heller P, Adams JG. Hemopoietic stress and fetal hemoglobin synthesis: comparative studies in vivo and in vitro. Blood. 1979;54(5):1176- 1181. (Pubitemid 10197562)
28. Papayannopoulou T, Nakamoto B, Buckley J, et al. Erythroid progenitors circulating in the blood of adult individuals produce fetal hemoglobin in culture. Science. 1978;199(4335):1349-1350. (Pubitemid 8292507)
29. Fabry ME, Suzuka SM, Weinberg RS, et al. Second generation knockout sickle mice: the effect of Hb F. Blood. 2001;97(2):410-418. (Pubitemid 32063176)
30. Chada K, Magram J, Costantini F. An embryonic pattern of expression of a human fetal globin gene in transgenic mice. Nature. 1986;319(6055):685-689. (Pubitemid 16119456)
31. Magram J, Chada K, Costantini F. Developmental regulation of a cloned adult beta-globin gene in transgenic mice. Nature. 1985;315(6017):338-340. (Pubitemid 15044627)
32. Behringer RR, Ryan TM, Palmiter RD, Brinster RL, Townes TM. Human gamma-to betaglobin gene switching in transgenic mice. Genes Dev. 1990;4(3):380-389.
33. Kollias G, Wrighton N, Hurst J, Grosveld F. 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(1):89-94. (Pubitemid 16027828)
34. Peterson KR, Clegg CH, Huxley C, et al. Transgenic mice containing a 248-kb yeast artificial chromosome carrying the human beta-globin locus display proper developmental control of human globin genes. Proc Natl Acad Sci U S A. 1993;90(16):7593-7597. (Pubitemid 23249996)
35. Gaensler KM, Kitamura M, Kan YW. Germ-line transmission and developmental regulation of a 150-kb yeast artificial chromosome containing the human beta-globin locus in transgenic mice. Proc Natl Acad Sci U S A. 1993;90(23):11381-11385. (Pubitemid 23354433)
36. Tuan D, London IM. Mapping of DNase I-hypersensitive sites in the upstream DNA of human embryonic epsilon-globin gene in K562 leukemia cells. Proc Natl Acad Sci U S A. 1984;81(9):2718-2722. (Pubitemid 14109330)
37. Grosveld F, van Assendelft GB, Greaves DR, Kollias G. Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell. 1987;51(6):975-985.
38. Forrester WC, Novak U, Gelinas R, Groudine M. Molecular analysis of the human beta-globin locus activation region. Proc Natl Acad Sci U S A. 1989;86(14):5439-5443. (Pubitemid 19185564)
39. Bank A. Regulation of human fetal hemoglobin: new players, new complexities. Blood. 2006;107(2):435-443. (Pubitemid 43076362)
40. Wijgerde M, Grosveld F, Fraser P. Transcription complex stability and chromatin dynamics in vivo. Nature. 1995;377(6546):209-213.
41. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell. 2002;10(6):1453-1465. (Pubitemid 36050885)
42. Fraser P, Pruzina S, Antoniou M, Grosveld F. Each hypersensitive site of the human beta-globin locus control region confers a different developmental pattern of expression on the globin genes. Genes Dev. 1993;7(1):106-113. (Pubitemid 23071204)
43. Townes TM, Lingrel JB, Chen HY, Brinster RL, Palmiter RD. Erythroid-specific expression of human beta-globin genes in transgenic mice. EMBO J. 1985;4(7):1715-1723.
44. Enver T, Raich N, Ebens AJ, et al. Developmental regulation of human fetal-to-adult globin gene switching in transgenic mice. Nature. 1990;344(6264):309-313.
45. Dillon N, Grosveld F. Human gamma-globin genes silenced independently of other genes in the beta-globin locus. Nature. 1991;350(6315):252-254. (Pubitemid 21912213)
46. Zhu X, Ling J, Zhang L, Pi W, Wu M, Tuan D. A facilitated tracking and transcription mechanism of long-range enhancer function. Nucleic Acids Res. 2007;35(16):5532-5544. (Pubitemid 47423926)
47. Thein SL, Menzel S, Lathrop M, Garner C. Control of fetal hemoglobin: new insights emerging from genomics and clinical implications. Hum Mol Genet. 2009;18(R2):R216-R223.
48. Lettre G, Sankaran VG, Bezerra MA, et al. DNA polymorphisms at the BCL11A, HBS1L-MYB, and beta-globin loci associate with fetal hemoglobin levels and pain crises in sickle cell disease. Proc Natl Acad Sci USA. 2008;105(33):11869-11874.
49. Uda M, Galanello R, Sanna S, et al. Genomewide association study shows BCL11A associated with persistent fetal hemoglobin and amelioration of the phenotype of beta-thalassemia. Proc Nat Acad Sci U S A. 2008;105(5):1620-1625. (Pubitemid 351346564)
50. Chakalova L, Osborne CS, Dai YF, et al. The Corfu deltabeta thalassemia deletion disrupts gamma-globin gene silencing and reveals posttranscriptional regulation of HbF expression. Blood. 2005;105(5):2154-2160. (Pubitemid 40731807)
51. Calzolari R, McMorrow T, Yannoutsos N, Langeveld A, Grosveld F. Deletion of a region that is a candidate for the difference between the deletion forms of hereditary persistence of fetal hemoglobin and deltabeta-thalassemia affects betabut not gamma-globin gene expression. EMBO J. 1999;18(4):949-958. (Pubitemid 29082274)
52. Bank A, O'Neill D, Lopez R, et al. Role of intergenic human gamma-delta-globin sequences in human hemoglobin switching and reactivation of fetal hemoglobin in adult erythroid cells. Ann N Y Acad Sci. 2005;1054:48-54. (Pubitemid 43031010)
53. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008;132(4):631-644. (Pubitemid 351260057)
54. Dzierzak E, Speck NA. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol. 2008;9(2):129-136.
55. Wilson NK, Foster SD, Wang X, et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell. 2010;7(4):532-544.
56. Hager GL, McNally JG, Misteli T. Transcription dynamics. Mol Cell. 2009;35(6):741-753.
57. Hoogenkamp M, Lichtinger M, Krysinska H, et al. Early chromatin unfolding by RUNX1: a molecular explanation for differential requirements during specification versus maintenance of the hematopoietic gene expression program. Blood. 2009;114(2):299-309.
58. Dzierzak E. Opening act in a hematopoietic program. Blood. 2009;114(2):229-230.
59. Wozniak RJ, Bresnick EH. Epigenetic control of complex loci during erythropoiesis. Curr Top Dev Biol. 2008;82:55-83.
60. Ley TJ, De Simone J, Anagnou NP, et al. 5-Azacytidine selectively increases gamma-globin synthesis in a patient with beta + thalassemia. N Engl J Med. 1982;307(24):1469-1475. (Pubitemid 13238767)
61. Ley TJ, De Simone J, Noguchi CT, et al. 5-Azacytidine increases gamma-globin synthesis and reduces the proportion of dense cells in patients with sickle cell anemia. Blood. 1983;62(2):370-380. (Pubitemid 13036087)
62. Bradner JE, Mak R, Tanguturi SK, et al. Chemical genetic strategy identifies histone deacetylase 1 (HDAC1) and HDAC2 as therapeutic targets in sickle cell disease. Proc Natl Acad Sci U S A. 2010;107(28):12617-12622.
63. Chakalova L, Fraser P. Organization of transcription. Cold Spring Harb Perspect Biol. 2010;2(9):a000729.
64. Schoenfelder S, Sexton T, Chakalova L, et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet. 2010;42(1):53-61.
65. Yu M, Riva L, Xie H, et al. Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell. 2009;36(4):682-695.
66. Fujiwara T, O'Geen H, Keles S, et al. Discovering hematopoietic mechanisms through genomewide analysis of GATA factor chromatin occupancy. Mol Cell. 2009;36(4):667-681.
67. Kerenyi MA, Orkin SH. Networking erythropoiesis. J Exp Med. 2010;207(12):2537-2541.
68. Papayannopoulou T, Brice M, Stamatoyannopoulos G. Analysis of human hemoglobin switching in MEL x human fetal erythroid cell hybrids. Cell. 1986;46(3):469-476. (Pubitemid 16031682)
69. Qiu C, Olivier EN, Velho M, Bouhassira EE. Globin switches in yolk sac-like primitive and fetallike definitive red blood cells produced from human embryonic stem cells. Blood. 2008;111(4):2400-2408. (Pubitemid 351451453)
70. Wilber A, Tschulena U, Hargrove PW, et al. A zinc-finger transcriptional activator designed to interact with the gamma-globin gene promoters enhances fetal hemoglobin production in primary human adult erythroblasts. Blood. 2010;115(15):3033-3041.
71. Thein SL, Menzel S, Peng X, et al. Intergenic variants of HBS1L-MYB are responsible for a major quantitative trait locus on chromosome 6q23 influencing fetal hemoglobin levels in adults. Proc Natl Acad Sci U S A. 2007;104(27):11346-11351. (Pubitemid 47175143)
72. Wahlberg K, Jiang J, Rooks H, et al. The HBS1L-MYB intergenic interval associated with elevated HbF levels shows characteristics of a distal regulatory region in erythroid cells. Blood. 2009;114(6):1254-1262.
73. Galarneau G, Palmer CD, Sankaran VG, et al. Fine-mapping at three loci known to affect fetal hemoglobin levels explains additional genetic variation. Nat Genet. 2010;42(2):1049-1051.
74. Sankaran VG, Menne TF, Xu J, et al. Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science. 2008;322(5909):1839-1842.
75. Xu J, Sankaran VG, Ni M, et al. Transcriptional silencing of gamma-globin by BCL11A involves long-range interactions and cooperation with SOX6. Genes Dev. 2010;24(8):783-798.
76. Sankaran VG, Xu J, Ragoczy T, et al. Developmental and species-divergent globin switching are driven by BCL11A. Nature. 2009;460(7259):1093-1097.
77. Yi Z, Cohen-Barak O, Hagiwara N, et al. Sox6 directly silences epsilon globin expression in definitive erythropoiesis. PLoS Genet. 2006;2(2):e14.
78. Miller IJ, Bieker JJ. 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(5):2776-2786. (Pubitemid 23133950)
79. Perkins AC, Sharpe AH, Orkin SH. Lethal betathalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature. 1995;375(6529):318-322.
80. Nuez B, Michalovich D, Bygrave A, Ploemacher R, Grosveld F. Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature. 1995;375(6529):316-318.
81. Borg J, Papadopoulos P, Georgitsi M, et al. Haploinsufficiency for the erythroid transcription factor KLF1 causes hereditary persistence of fetal hemoglobin. Nat Genet. 2010;42(9):801-805.
82. Zhou D, Liu K, Sun CW, Pawlik KM, Townes TM. KLF1 regulates BCL11A expression and gamma-to beta-globin gene switching. Nat Genet. 2010;42(9):742-744.
83. Jiang J, Best S, Menzel S, et al. cMYB is involved in the regulation of fetal hemoglobin production in adults. Blood. 2006;108(3):1077-1083. (Pubitemid 44154648)
84. Bianchi E, Zini R, Salati S, et al. c-myb supports erythropoiesis through the transactivation of KLF1 and LM02 expression. Blood. 2010;116(22):e99-e110.
85. Tanabe O, McPhee D, Kobayashi S, et al. Embryonic and fetal beta-globin gene repression by the orphan nuclear receptors, TR2 and TR4. EMBO J. 2007;26(9):2295-2306. (Pubitemid 46685858)
86. Omori A, Tanabe O, Engel JD, Fukamizu A, Tanimoto K. Adult stage gamma-globin silencing is mediated by a promoter direct repeat element. Mol Cell Biol. 2005;25(9):3443-3451. (Pubitemid 40559553)
87. Collins FS, Mentherall JE, Yamakawa M, et al. A point mutation in the A gamma-globin gene promoter in Greek hereditary persistence of fetal haemoglobin. Nature. 1985;313(6000):325-326. (Pubitemid 15151991)
88. Berry M, Grosveld F, Dillon N. A single point mutation is the cause of the Greek form of hereditary persistence of fetal haemoglobin. Nature. 1992;358(6386):499-502.
89. Sagami I, Tsai SY, Wang H, Tsai MJ, O'Malley BW. Identification of two factors required for transcription of the ovalbumin gene. Mol Cell Biol. 1986;6(12):4259-4267. (Pubitemid 17217372)
90. Filipe A, Li Q, Deveaux S, et al. Regulation of embryonic/fetal globin genes by nuclear hormone receptors: a novel perspective on hemoglobin switching. EMBO J. 1999;18(3):687-697. (Pubitemid 29057253)
91. Aerbajinai W, Zhu J, Kumkhaek C, Chin K, Rodgers GP. SCF induces gamma-globin gene expression by regulating downstream transcription factor COUP-TFII. Blood. 2009;114(1):187-194.
92. Liberati C, Cera MR, Secco P, et al. Cooperation and competition between the binding of COUP-TFII and NF-Y on human epsilon-and gammaglobin gene promoters. J Biol Chem. 2001;276(45):41700-41709.
93. van Dijk TB, Gillemans N, Stein C, et al. Friend of Prmt1, a novel chromatin target of protein arginine methyltransferases. Mol Cell Biol. 2010;30:260-272.
94. van Dijk TB, Gillemans N, Pourfarzad F, et al. Fetal globin expression is regulated by Friend of Prmt1. Blood. 2010;116(20):4349-4352.
95. Jane SM, Nienhuis AW, Cunningham JM. Hemoglobin switching in man and chicken is mediated by a heteromeric complex between the ubiquitous transcription factor CP2 and a developmentally specific protein. EMBOJ. 1995;14(1):97-105.
96. Zhou W, Zhao Q, Sutton R, et al. The role of p22 NF-E4 in human globin gene switching. J Biol Chem. 2004;279(25):26227-26232. (Pubitemid 38798770)
97. Jane SM, Gumucio DL, Ney PA, Cunningham JM, Nienhuis AW. 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(6):3272-3281. (Pubitemid 23157265)
98. Wilber A, Hargrove PW, Kim YS, et al. Therapeutic levels of fetal hemoglobin production in erythroid progeny of beta-thalassemic CD34+ cells following lentiviral vector-mediated gene transfer. Blood. 2011;117(10):2817- 2826.
99. Wu H, Yang WP, Barbas CF III. Building zinc fingers by selection: toward a therapeutic application. Proc Natl Acad Sci U S A. 1995;92(2):344-348.
100. Bauer DE, Orkin SH. Update on fetal hemoglobin gene regulation in hemoglobinopathies. Curr Opin Pediatr. 2011;23(1):1-8.