Evidence for a Bigenic Chromatin Subdomain in Regulation of the Fetal-to-Adult Hemoglobin Switch

REFERENCES

• Anderson, K. P., J. A. Lloyd, E. Ponce, S. C. Crable, J. C. Neumann, and J. B. Lingrel. 1993. Regulated expression of the human β-globin gene in transgenic mice requires an upstream globin or nonglobin promoter. Mol. Biol. Cell 4:1077–1085.
   PubMedGoogle Scholar
• Bauchwitz, R., and F. Costantini. 2000. Developmentally distinct effects on human ε-, γ- and δ-globin levels caused by the absence or altered position of the human β-globin gene in YAC transgenic mice. Hum. Mol. Genet. 9:561–574.
   PubMedGoogle Scholar
• Beauchemin, H., M. J. Blouin, and M. Trudel. 2004. Differential regulatory and compensatory responses in hematopoiesis/erythropoiesis in α- and β-globin hemizygous mice. J. Biol. Chem. 279:19471–19480.
   PubMed Web of Science ®Google Scholar
• Bender, M. A., M. Bulger, J. Close, and M. Groudine. 2000. β-Globin gene switching and DNase I sensitivity of the endogenous β-globin locus in mice do not require the locus control region. Mol. Cell 5:387–393.
   PubMed Web of Science ®Google Scholar
• Blouin, M.-J., H. Beauchemin, A. Wright, M. DePaepe, M. Sorette, A.-M. Bleau, B. Nakamoto, C.-N. Ou, G. Stamatoyannopoulos, and M. Trudel. 2000. Genetic correction of sickle cell disease: insights using transgenic mouse models. Nat. Med. 6:177–182.
   PubMed Web of Science ®Google Scholar
• Blouin, M. J., and M. Trudel. 1997. Characterization of the hematopoietic precursors in sickle cell disease of SAD transgenic mouse model. Blood 90:22–23.
   Google Scholar
• Bottardi, S., A. Aumont, F. Grosveld, and E. Milot. 2003. Developmental stage-specific epigenetic control of human β-globin gene expression is potentiated in hematopoietic progenitor cells prior to their transcriptional activation. Blood 102:3989–3997.
   PubMedGoogle Scholar
• Bresnick, E. H., and G. Felsenfeld. 1994. Dual promoter activation by the human β-globin locus control region. Proc. Natl. Acad. Sci. USA 91:1314–1317.
   PubMedGoogle Scholar
• Bungert, J., U. Davé, K.-C. Lim, K. H. Lieuw, J. A. Shavit, Q. Liu, and J. D. Engel. 1995. Synergistic regulation of human β-globin gene switching by locus control region elements HS3 and HS4. Genes Dev. 9:3083–3096.
   PubMedGoogle Scholar
• Bungert, J., K. Tanimoto, S. Patel, Q. Liu, M. Fear, and J. D. Engel. 1999. Hypersensitive site 2 specifies a unique function within the human β-globin locus control region to stimulate globin gene transcription. Mol. Cell. Biol. 19:3062–3072.
   PubMedGoogle Scholar
• Chakalova, L., C. S. Osborne, Y. F. Dai, B. Goyenechea, A. Metaxotou-Mavromati, A. Kattamis, C. Kattamis, and P. Fraser. 2005. The Corfu δβ thalassemia deletion disrupts γ-globin gene silencing and reveals post-transcriptional regulation of HbF expression. Blood 105:2154–2160.
   PubMed Web of Science ®Google Scholar
• Coleman, M. B., J. G. R. Adams, M. H. Steinberg, and W. P. Winter. 1994. A four base pair deletion 5′ to the AγT gene is associated not only with decreased expression of the AγT-globin gene, but also of the Gγ-globin gene in cis. Am. J. Hematol. 47:307–311.
   PubMedGoogle Scholar
• Dekker, J., K. Rippe, M. Dekker, and N. Kleckner. 2002. Capturing chromosome conformation. Science 295:1306–1311.
   PubMed Web of Science ®Google Scholar
• Dillon, N., and F. Grosveld. 1991. Human γ-globin genes silenced independently of other genes in the β-globin locus. Nature 350:252–254.
   PubMedGoogle Scholar
• Dostie, J., T. A. Richmond, R. A. Arnaout, R. R. Selzer, W. L. Lee, T. A. Honan, E. D. Rubio, A. Krumm, J. Lamb, C. Nusbaum, R. D. Green, and J. Dekker. 2006. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 16:1299–1309.
   PubMed Web of Science ®Google Scholar
• Eleouet, J. F., and P. H. Romeo. 1993. CCACC-binding or simian-virus-40-protein-1-binding proteins cooperate with human GATA-1 to direct erythroid-specific transcription and to mediate 5′ hypersensitive site 2 sensitivity of a TATA-less promoter. Eur. J. Biochem. 212:763–770.
   PubMedGoogle Scholar
• Fang, X., P. Xiang, W. Yin, G. Stamatoyannopoulos, and Q. Li. 2007. Cooperativeness of the higher chromatin structure of the β-globin locus revealed by the deletion mutations of the DNase I hypersensitive site 3 of the LCR. J. Mol. Biol. 365:31–37.
   PubMedGoogle Scholar
• Feng, Y. Q., R. Desprat, H. Fu, E. Olivier, C. M. Lin, A. Lobell, S. N. Gowda, M. I. Aladjem, and E. E. Bouhassira. 2006. DNA methylation supports intrinsic epigenetic memory in mammalian cells. PLoS Genet. 2:e65.
   PubMedGoogle Scholar
• Forget, B. G. 1998. Molecular basis of hereditary persistence of fetal hemoglobin. Ann. N. Y. Acad. Sci. 850:38–44.
   PubMed Web of Science ®Google Scholar
• Fraser, S. T., J. Isern, and M. H. Baron. 2007. Maturation and enucleation of primitive erythroblasts during mouse embryogenesis is accompanied by changes in cell-surface antigen expression. Blood 109:343–352.
   PubMedGoogle Scholar
• Gaensler, K. M., Z. Zhang, C. Lin, S. Yang, K. Hardt, and L. Flebbe-Rehwaldt. 2003. Sequences in the Aγ-delta intergenic region are not required for stage-specific regulation of the human β-globin gene locus. Proc. Natl. Acad. Sci. USA 100:3374–3379.
   PubMedGoogle Scholar
• Gilman, J. G., N. Mishima, X. J. Wen, T. A. Stoming, J. Lobel, and T. H. Huisman. 1988. Distal CCAAT box deletion in the Aγ globin gene of two black adolescents with elevated fetal Aγ globin. Nucleic Acids Res. 16:10635–10642.
   PubMed Web of Science ®Google Scholar
• Goren, A., G. Simchen, E. Fibach, P. E. Szabo, K. Tanimoto, L. Chakalova, G. P. Pfeifer, P. J. Fraser, J. D. Engel, and H. Cedar. 2006. Fine tuning of globin gene expression by DNA methylation. PLoS ONE 1:e46.
   PubMedGoogle Scholar
• Gribnau, J., K. Diderich, S. Priuzina, R. Calzolari, and P. Fraser. 2000. Intergenic transcription and developmental remodelling of chromatin subdomains in the human β-globin locus. Mol. Cell 5:377–386.
   PubMedGoogle Scholar
• Hanscombe, O., D. Whyatt, P. Fraser, N. Yannoutsos, D. Greaves, N. Dillon, and F. Grosveld. 1991. Importance of globin gene order for correct developmental expression. Genes Dev. 5:1387–1394.
   PubMedGoogle Scholar
• Harju, S., P. A. Navas, G. Stamatoyannopoulos, and K. R. Peterson. 2005. Genome architecture of the human β-globin locus affects developmental regulation of gene expression. Mol. Cell. Biol. 25:8765–8778.
   PubMedGoogle Scholar
• Hodge, D., E. Coghill, J. Keys, T. Maguire, B. Hartmann, A. McDowall, M. J. Weiss, S. Grimmond, and A. Perkins. 2006. A global role for EKLF in definitive and primitive erythropoiesis. Blood 107:3359–3370.
   PubMed Web of Science ®Google Scholar
• Hu, X., M. Bulger, J. N. Roach, S. K. Eszterhas, E. Olivier, E. E. Bouhassira, M. Groudine, and S. Fiering. 2004. Promoters of the murine embryonic β-like globin genes Ey and βh1 do not compete for interaction with the β-globin locus control region. Proc. Natl. Acad. Sci. USA 100:1111–1115.
   Google Scholar
• Jane, S. M., D. L. Gumucio, P. A. Ney, J. M. Cunningham, and A. W. Nienhuis. 1993. Methylation-enhanced binding of Sp1 to the stage selector element of the human γ-globin gene promoter may regulate developmental specificity of expression. Mol. Cell. Biol. 13:3272–3281.
   PubMed Web of Science ®Google Scholar
• Johnson, K. D., J. A. Grass, C. Park, H. Im, K. Choi, and E. H. Bresnick. 2003. Highly restricted localization of RNA polymerase II within a locus control region of a tissue-specific chromatin domain. Mol. Cell. Biol. 23:6484–6493.
   PubMedGoogle Scholar
• Katsube, T., and Y. Fukumaki. 1995. A role for the distal CCAAT box of the γ-globin gene in Hb switching. J. Biochem. 117:68–76.
   PubMed Web of Science ®Google Scholar
• Keys, J. R., M. R. Tallack, Y. Zhan, P. Papathanasiou, C. C. Goodnow, K. M. Gaensler, M. Crossley, J. Dekker, and A. C. Perkins. 2008. A mechanism for Ikaros regulation of human globin gene switching. Br. J. Haematol. 141:398–406.
   PubMed Web of Science ®Google Scholar
• Kulozik, A. E., N. Yarwood, and R. W. Jones. 1988. The Corfu δβ0 thalassemia: a small deletion acts at a distance to selectively abolish β-globin gene expression. Blood 71:1509.
   Google Scholar
• Liu, L. R., Z. W. Du, H. L. Zhao, X. L. Liu, X. D. Huang, J. Shen, L. M. Ju, F. D. Fang, and J. W. Zhang. 2005. T to C substitution at −175 or −173 of the γ-globin promoter affects GATA-1 and Oct-1 binding in vitro differently but can independently reproduce the hereditary persistence of fetal hemoglobin phenotype in transgenic mice. J. Biol. Chem. 280:7452–7459.
   PubMed Web of Science ®Google Scholar
• Lloyd, J. A., S. S. Case, E. Ponce, and J. B. Lingrel. 1994. Positive transcriptional regulation of the human γ-globin gene. γPE is a novel nuclear factor with multiple binding sites near the gene. J. Biol. Chem. 269:19385–19393.
   PubMedGoogle Scholar
• Lloyd, J. A., J. M. Krakowsky, S. C. Crable, and J. B. Lingrel. 1992. Human γ- to β-globin gene switching using a mini construct in transgenic mice. Mol. Cell. Biol. 12:1561–1567.
   PubMed Web of Science ®Google Scholar
• Matsuo, K., J. Silke, O. Georgiev, P. Marti, N. Giovannini, and D. Rungger. 1998. An embryonic demethylation mechanism involving binding of transcription factors to replicating DNA. EMBO J. 17:1446–1453.
   PubMedGoogle Scholar
• Mignotte, V., J. F. Eleouet, N. Raich, and P.-H. Romeo. 1989. Cis- and trans-acting elements involved in the regulation of the erythroid promoter of the human porphobilinogen deaminase gene. Proc. Natl. Acad. Sci. USA 86:6548–6552.
   PubMed Web of Science ®Google Scholar
• Mignotte, V., L. Wall, E. deBoer, F. Grosveld, and P. H. Romeo. 1989. Two tissue-specific factors bind the erythroid promoter of the human porphobilinogen deaminase gene. Nucleic Acids Res. 17:37–54.
   PubMed Web of Science ®Google Scholar
• Miles, J., J. A. Mitchell, L. Chakalova, B. Goyenechea, C. S. Osborne, L. O'Neill, K. Tanimoto, J. D. Engel, and P. Fraser. 2007. Intergenic transcription, cell-cycle and the developmentally regulated epigenetic profile of the human β-globin locus. PLoS ONE 2:e630.
   PubMedGoogle Scholar
• Omori, A., O. Tanabe, J. D. Engel, Y. Fukamizu, and K. Tanimoto. 2005. Adult-stage γ-globin silencing is mediated by a promoter direct repeat element. Mol. Cell. Biol. 25:3443–3451.
   PubMed Web of Science ®Google Scholar
• O'Neill, D., K. Bornschlegel, M. Flamm, M. Castle, and A. Bank. 1991. A DNA-binding factor in adult hematopoietic cells interacts with a pyrimidine-rich domain upstream from the human δ-globin gene. Proc. Natl. Acad. Sci. USA 88:8953–8957.
   PubMedGoogle Scholar
• Patrinos, G. P., M. de Krom, E. de Boer, A. Langeveld, A. M. A. Imam, J. Strouboulis, W. de Laat, and F. G. Grosveld. 2004. Multiple interactions between regulatory regions are required to stabilize an active chromatin hub. Genes Dev. 18:1495–1509.
   PubMed Web of Science ®Google Scholar
• Peterson, K. R., C. H. Clegg, Q. Li, and G. Stamatoyannopoulos. 1997. Production of transgenic mice with yeast artificial chromosomes. Trends Genet. 13:61–66.
   PubMedGoogle Scholar
• Pistidda, P., L. Frogheri, L. Oggiano, L. Guiso, L. Manca, F. Dore, B. Masala, J. G. Gilman, and M. Longinotti. 1995. Fetal hemoglobin expression in compound heterozygotes for −117(G→A) Aγ HPFH and β0 39 nonsense thalassemia. Am. J. Hematol. 49:264–270.
   Google Scholar
• Plant, K. E., S. J. Routledge, and N. J. Proudfoot. 2001. Intergenic transcription in the human β-globin gene cluster. Mol. Cell. Biol. 21:6507–6514.
   PubMedGoogle Scholar
• Raich, N., T. Enver, B. Nakamoto, B. Josephson, T. Papayannopoulou, and G. Stamatoyannopoulos. 1990. Autonomous development control of human embryonic globin gene switching in transgenic mice. Science 250:1147–1149.
   PubMedGoogle Scholar
• Reik, A., A. Telling, G. Zitnik, D. Cimbora, E. Epner, and M. Groudine. 1998. The locus control region is necessary for gene expression in the human β-globin locus but not the maintenance of an open chromatin structure in erythroid cells. Mol. Cell. Biol. 18:5992–6000.
   PubMed Web of Science ®Google Scholar
• Russell, J. E., and S. A. Liebhaber. 1998. Reversal of lethal α- and β-thalassemias in mice by expression of human embryonic globins. Blood 92:3057–3063.
   PubMedGoogle Scholar
• Ryan, T. M., C.-W. Sun, J. Ren, and T. M. Townes. 2000. Human γ-globin gene promoter element regulates human β-globin gene development specificity. Nucleic Acids Res. 28:2736–2740.
   PubMedGoogle Scholar
• Sabatino, D. E., A. P. Cline, P. G. Gallagher, L. J. Garrett, G. Stamatoyannopoulos, B. G. Forget, and D. M. Bodine. 1998. Substitution of the human β-spectrin promoter for the human Aγ-globin promoter prevents silencing of a linked human β-globin gene in transgenic mice. Mol. Cell. Biol. 18:6634–6640.
   PubMed Web of Science ®Google Scholar
• Sengupta, P. K., D. Lavelle, and J. DeSimone. 1994. Increased binding of Sp1 to the γ-globin gene promoter upon site-specific cytosine methylation. Am. J. Hematol. 46:169–172.
   PubMedGoogle Scholar
• Shih, D. M., R. J. Wall, and S. G. Shapiro. 1993. A 5′ control region of the human ε-globin gene is sufficient for embryonic specificity in transgenic mice. J. Biol. Chem. 268:30066–30071.
   Google Scholar
• Stamatoyannopoulos, G., B. Josephson, J.-W. Zhang, and Q. Li. 1993. Developmental regulation of human γ-globin genes in transgenic mice. Mol. Cell. Biol. 13:7636–7644.
   PubMed Web of Science ®Google Scholar
• Tanimoto, K., Q. Liu, J. Bungert, and J. D. Engel. 1999. Effects of altered gene order or orientation of the locus control region on human β-globin gene expression in mice. Nature 398:344–348.
   PubMedGoogle Scholar
• Thivierge, C., A. Kurbegovic, M. Couillard, R. Guillaume, O. Cote, and M. Trudel. 2006. Overexpression of PKD1 causes polycystic kidney disease. Mol. Cell. Biol. 26:1538–1548.
   PubMed Web of Science ®Google Scholar
• Tolhuis, B., R. J. Palstra, E. Splinter, F. Grosveld, and W. de Latt. 2002. Looping and interaction between hypersensitive sites in the active β-globin locus. Mol. Cell 10:1453–1465.
   PubMed Web of Science ®Google Scholar
• Trudel, M., J. Magram, L. Bruckner, and F. Costantini. 1987. Upstream Gγ-globin and downstream β-globin gene domain in human erythroid cells. Mol. Cell. Biol. 7:4024–4029.
   PubMedGoogle Scholar
• Trudel, M., J. Magram, K. Chada, R. Wilson, and F. Costantini. 1987. Expression of normal, mutant and hybrid human globin genes in transgenic mice, p. 305-321. In G. Stamatoyannopoulos and A. Nienhuis (ed.), The regulation of hemoglobin switch. Alan R. Liss, Inc., Baltimore, MD.
   Google Scholar
• Trudel, M., N. Saadane, M.-C. Garel, J. Bardakdjian-Michau, Y. Blouquit, J.-L. Guerquin-Kern, P. Rouyer-Fessard, D. Vidaud, A. Pachnis, P.-H. Romeo, Y. Beuzard, and F. Costantini. 1991. Towards a transgenic mouse model of sickle cell disease: hemoglobin SAD. EMBO J. 10:3157–3165.
   PubMed Web of Science ®Google Scholar
• Turek-Plewa, J., and P. P. Jagodzinski. 2005. The role of mammalian DNA methyltransferases in the regulation of gene expression. Cell. Mol. Biol. Lett. 10:631–647.
   PubMed Web of Science ®Google Scholar
• Weatherhall, D. J., and J. B. Clegg (ed.). 2001. The thalassaemia syndromes. Blackwell Science, Oxford, United Kingdom.
   Google Scholar
• Wijgerde, M., F. Grosveld, and P. Fraser. 1995. Transcription complex stability and chromatin dynamics in vivo. Nature 377:209–213.
   PubMed Web of Science ®Google Scholar
• Yin, W., G. Barkess, X. Fang, P. Xiang, H. Cao, and G. Stamatoyannopoulos. 2007. Histone acetylation at the human β-globin locus changes with developmental age. Blood 110:4101–4107.
   PubMedGoogle Scholar
• Yu, M., H. Han, P. Xiang, Q. Li, and G. Stamatoyannopoulos. 2006. Autonomous silencing as well as competition controls γ-globin gene expression during development. Mol. Cell. Biol. 26:4775–4781.
   PubMedGoogle Scholar