Synergistic regulation of human beta-globin gene switching by locus control region elements HS3 and HS4.

Bungert, J; Davé, U; Lim, K C; Lieuw, K H; Shavit, J A; Liu, Q; Engel, J D

doi:10.1101/gad.9.24.3083

Cited by 183Hemoglobinopathies and Related DisordersGenomics and Chromatin DynamicsHemoglobin structure and function

Synergistic regulation of human beta-globin gene switching by locus control region elements HS3 and HS4.

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Bungert, J, Davé, U, Lim, K C, Lieuw, K H, Shavit, J A, Liu, Q, Engel, J D·1995·Genes & Development

DOI 10.1101/gad.9.24.3083

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Abstract

Proper tissue- and developmental stage-specific transcriptional control over the five genes of the human beta-globin locus is elicited in part by the locus control region (LCR), but the molecular mechanisms that dictate this determined pattern of gene expression during human development are still controversial. By use of homologous recombination in yeast to generate mutations in the LCR within a yeast artificial chromosome (YAC) bearing the entire human beta-globin gene locus, followed by injection of each of the mutated YACs into murine ova, we addressed the function of LCR hypersensitive site (HS) elements 3 and 4 in human beta-globin gene switching. The experiments revealed a number of unexpected properties that are directly attributable to LCR function. First, deletion of either HS3 or HS4 core elements from an otherwise intact YAC results in catastrophic disruption of globin gene expression at all erythroid developmental stages, despite the presence of all other HS elements in the YAC transgenes. If HS3 is used to replace HS4, gene expression is normal at all developmental stages. Conversely, insertion of the HS4 element in place of HS3 results in significant expression changes at every developmental stage, indicating that individual LCR HS elements play distinct roles in stage-specific beta-type globin gene activation. Although the HS4 duplication leads to alteration in the levels of epsilon- and gamma-globin mRNAs during embryonic erythropoiesis, total beta-type globin mRNA synthesis is balanced, thereby leading to the conclusion that all of the human beta-locus genes are competitively regulated. In summary, the human beta-globin HS elements appear to form a single, synergistic functional entity called the LCR, and HS3 and HS4 appear to be individually indispensable to the integrity of this macromolecular complex.

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The mammalian β-globin locus developmental β-globin genes are regulated by a powerful tissue-specific enhancer known as a locus control region (LCR).
“These models were initially applied to the mammalian β-globin locus, in which the developmental β-globin genes are regulated by a powerful tissue-specific enhancer known as a locus control region (LCR) [254–257].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [257]

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Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589 · see citing works
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
Sikorski, R. S., & Hieter, P. (1989) · Genetics · doi:10.1093/genetics/122.1.19 · Cited by 8,685 · see citing works
Guide to Yeast Genetics and Molecular Biology
Kurtzman, C. P., Guthrie, C., & Fink, G. R. (1993) · Mycologia · doi:10.2307/3760517 · Cited by 2,382 · see citing works
Position-independent, high-level expression of the human β-globin gene in transgenic mice
Grosveld, F. G., van Assendelft, G. B., Greaves, D. R., & Kollias, G. A. (1987) · Cell · doi:10.1016/0092-8674(87)90584-8 · Cited by 1,908 · see citing works
The Molecular Basis of Blood Diseases.
(1987) · Annals of Internal Medicine · doi:10.7326/0003-4819-107-6-950_3 · Cited by 640 · see citing works
The "beta-like-globin" gene domain in human erythroid cells.
Tuan, D., Solomon, W., Li, Q., & London, I. M. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.19.6384 · Cited by 601 · see citing works
Epigenetic mechanisms underlying the imprinting of the mouse H19 gene.Preprint
Bartolomei, M. S., Webber, A. L., Brunkow, M. E., & Tilghman, S. M. (1993) · Genes & Development · doi:10.1101/gad.7.9.1663 · Cited by 492 · see citing works
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.Preprint
Forrester, W. C., Epner, E. M., Driscoll, M. C., Enver, T., Brice, M. C., Papayannopoulou, T., & Groudine, M. T. (1990) · Genes & Development · doi:10.1101/gad.4.10.1637 · Cited by 464 · see citing works
Globin gene regulation and switching: Circa 1990
Orkin, S. H. (1990) · Cell · doi:10.1016/0092-8674(90)90133-y · Cited by 462 · see citing works
Molecular cloning and characterization of the human β-like globin gene cluster
Fritsch, E. F., Lawn, R. M., & Maniatis, T. (1980) · Cell · doi:10.1016/0092-8674(80)90087-2 · Cited by 452 · see citing works
Evidence for a locus activation region: the formation of developmentally stable hypersensitive sites in globin-expressing hybrids
Forrester, W. C., Takegawa, S., Papayannopoulou, T., Stamatoyannopoulos, G., & Groudine, M. T. (1987) · Nucleic Acids Research · doi:10.1093/nar/15.24.10159 · Cited by 418 · see citing works
A developmentally stable chromatin structure in the human beta-globin gene cluster.
Forrester, W. C., Thompson, C. B., Elder, J. T., & Groudine, M. T. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.5.1359 · Cited by 376 · see citing works
Developmental regulation of human fetal-to-adult globin gene switching in transgenic mice
Enver, T., Raich, N., Ebens, A. J., Papayannopoulou, T., Costantini, F. D., & Stamatoyannopoulos, G. (1990) · Nature · doi:10.1038/344309a0 · Cited by 345 · see citing works
Targeted deletion of 5'HS2 of the murine beta-globin LCR reveals that it is not essential for proper regulation of the beta-globin locus.Preprint
Fiering, S., Epner, E. M., Robinson, K. M., Zhuang, Y., Telling, A., Hu, M., Martin, D. I. K., Enver, T., Ley, T. J., & Groudine, M. T. (1995) · Genes & Development · doi:10.1101/gad.9.18.2203 · Cited by 334 · see citing works
A dominant control region from the human β-globin locus conferring integration site-independent gene expression
Talbot, D., Collis, P., Antoniou, M. N., Vidal, M., Grosveld, F. G., & Greaves, D. R. (1989) · Nature · doi:10.1038/338352a0 · Cited by 330 · see citing works
Detailed analysis of the site 3 region of the human beta‐globin dominant control region.
Talbot, D., Philipsen, S., Fraser, P., & Grosveld, F. G. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07386.x · Cited by 311 · see citing works
Developmental regulation of β-globin gene switching
Choi, O.-R., & Engel, J. D. (1988) · Cell · doi:10.1016/0092-8674(88)90005-0 · Cited by 308 · see citing works
Self-citation
Tandem AP-1-binding sites within the human beta-globin dominant control region function as an inducible enhancer in erythroid cells.Preprint
Ney, P. A., Sorrentino, B. P., McDonagh, K. T., & Nienhuis, A. W. (1990) · Genes & Development · doi:10.1101/gad.4.6.993 · Cited by 291 · see citing works
[13] Eviction and transplacement of mutant genes in yeast
Winston, F., Chumley, F. G., & Fink, G. R. (1983) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(83)01016-2 · Cited by 290 · see citing works
The beta‐globin dominant control region: hypersensitive site 2.
Philipsen, S., Talbot, D., Fraser, P., & Grosveld, F. G. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07385.x · Cited by 281 · see citing works
Human gamma- to beta-globin gene switching in transgenic mice.Preprint
Behringer, R. R., Ryan, T. M., Palmiter, R. D., Brinster, R. L., & Townes, T. M. (1990) · Genes & Development · doi:10.1101/gad.4.3.380 · Cited by 278 · see citing works
Parental imprinting: potentially active chromatin of the repressed maternal allele of the mouse insulin-like growth factor II (Igf2) gene.Preprint
Sasaki, H., Jones, P. A., Chaillet, J. R., Ferguson‐Smith, A. C., Barton, S. C., Reik, W., & Surani, M. A. (1992) · Genes & Development · doi:10.1101/gad.6.10.1843 · Cited by 274 · see citing works
A yeast artificial chromosome covering the tyrosinase gene confers copy number-dependent expression in transgenic mice
Schedl, A., Montoliu, L., Kelsey, G., & Schütz, G. (1993) · Nature · doi:10.1038/362258a0 · Cited by 269 · see citing works
Regulated expression of human Aγ-, β-, and hybrid γβ-globin genes in transgenic mice: Manipulation of the developmental expression patterns
Kollias, G. A., Wrighton, N., Hurst, J., & Grosveld, F. G. (1986) · Cell · doi:10.1016/0092-8674(86)90862-7 · Cited by 267 · see citing works
A single erythroid-specific DNase I super-hypersensitive site activates high levels of human beta-globin gene expression in transgenic mice.Preprint
Ryan, T. M., Behringer, R. R., Martin, N. C., Townes, T. M., Palmiter, R. D., & Brinster, R. L. (1989) · Genes & Development · doi:10.1101/gad.3.3.314 · Cited by 259 · see citing works
Gamma delta beta-thalassemia due to a de novo mutation deleting the 5' beta-globin gene activation-region hypersensitive sites.
Driscoll, M. C., Dobkin, C. S., & Alter, B. P. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.19.7470 · Cited by 233 · see citing works
Each hypersensitive site of the human beta-globin locus control region confers a different developmental pattern of expression on the globin genes
Fraser, P., Pruzina, S., Antoniou, M., & Grosveld, F. (1993) · Genes & Development · doi:10.1101/gad.7.1.106 · Cited by 231 · see citing works
The 5′HS2 of the globin locus control region enhances transcription through the interaction of a multimeric complex binding at two functionally distinct NF‐E2 binding sites.
Talbot, D., & Grosveld, F. G. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07659.x · Cited by 226 · see citing works
Transgenic mice containing a 248-kb yeast artificial chromosome carrying the human beta-globin locus display proper developmental control of human globin genes.
Peterson, K. R., Clegg, C. H., Huxley, C. M., Josephson, B. M., Haugen, H. S., Furukawa, T., & Stamatoyannopoulos, G. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.16.7593 · Cited by 222 · see citing works
Quantitation of RNA using the polymerase chain reaction
Foley, K. P., Leonard, M. W., & Engel, J. D. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90137-7 · Cited by 217 · see citing works
Self-citation
Developmental regulation of a cloned adult β-globin gene in transgenic mice
Magram, J., Chada, K. K., & Costantini, F. D. (1985) · Nature · doi:10.1038/315338a0 · Cited by 213 · see citing works
Developmental regulation of a complete 70-kb human beta-globin locus in transgenic mice.Preprint
Strouboulis, J., Dillon, N., & Grosveld, F. G. (1992) · Genes & Development · doi:10.1101/gad.6.10.1857 · Cited by 210 · see citing works
Two 3' sequences direct adult erythroid-specific expression of human beta-globin genes in transgenic mice.
Behringer, R. R., Hammer, R. E., Brinster, R. L., Palmiter, R. D., & Townes, T. M. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.20.7056 · Cited by 194 · see citing works
The primary structure of the human ε-globin gene
Baralle, F. E. (1980) · Cell · doi:10.1016/0092-8674(80)90425-0 · Cited by 192 · see citing works
Human γ-globin genes silenced independently of other genes in the β-globin locus
Dillon, N., & Grosveld, F. G. (1991) · Nature · doi:10.1038/350252a0 · Cited by 187 · see citing works
The human beta‐globin gene contains multiple regulatory regions: identification of one promoter and two downstream enhancers.
Antoniou, M. N., deBoer, E., Habets, G. G. M., & Grosveld, F. G. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb02824.x · Cited by 172 · see citing works
Regulated Expression of Globin Chains and the Erythroid Transcription Factor GATA-1 during Erythropoiesis in the Developing Mouse
Whitelaw, E., Tsai, S., Hogben, P., & Orkin, S. H. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.12.6596-6606.1990 · Cited by 163 · see citing works
Autonomous Developmental Control of Human Embryonic Globin Gene Switching in Transgenic Mice
Raich, N., Enver, T., Nakamoto, B., Josephson, B. M., Papayannopoulou, T., & Stamatoyannopoulos, G. (1990) · Science · doi:10.1126/science.2251502 · Cited by 143 · see citing works
Germ-line transmission and developmental regulation of a 150-kb yeast artificial chromosome containing the human beta-globin locus in transgenic mice.
Gaensler, K. M. L., Kitamura, M., & Kan, Y. W. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.23.11381 · Cited by 134 · see citing works
NF‐E2 and GATA binding motifs are required for the formation of DNase I hypersensitive site 4 of the human beta‐globin locus control region.
Stamatoyannopoulos, J. A., Goodwin, A. J., IV, Joyce, T., & Lowrey, C. H. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb06980.x · Cited by 131 · see citing works
Hypersensitive site 4 of the human β globin locus control region
Pruzina, S., Hanscombe, O., Whyatt, D., Grosveld, F. G., & Philipsen, S. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.7.1413 · Cited by 130 · see citing works
Clusters of Master Control Genes Regulate the Development of Higher Organisms
Lewis, E. B. (1992) · JAMA · doi:10.1001/jama.1992.03480110100042 · Cited by 127 · see citing works
A method for the generation of YAC transgenic mice by pronuclear microinjection
Sched, A., Larin, Z., Montoliu, L., Thies, E., Kelsey, G., Lehrach, H. R., & Schuütz, G. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.20.4783 · Cited by 125 · see citing works
Synthetic human beta‐globin 5′HS2 constructs function as locus control regions only in multicopy transgene concatamers.
Ellis, J., Talbot, D., Dillon, N., & Grosveld, F. G. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05638.x · Cited by 121 · see citing works
Human beta-globin gene expression in transgenic mice is enhanced by a distant DNase I hypersensitive site.
Curtin, P. T., Liu, D.-P., Liu, W., Chang, J., & Kan, Y. W. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.18.7082 · Cited by 120 · see citing works
The beta-globin stage selector element factor is erythroid-specific promoter/enhancer binding protein NF-E4.Preprint
Gallarda, J. L., Foley, K. P., Yang, Z., & Engel, J. D. (1989) · Genes & Development · doi:10.1101/gad.3.12a.1845 · Cited by 119 · see citing works
Self-citation
Mapping of DNase I-hypersensitive sites in the upstream DNA of human embryonic epsilon-globin gene in K562 leukemia cells.
Tuan, D. Y. H., & London, I. M. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.9.2718 · Cited by 116 · see citing works
Germ Line Transmission of a Yeast Artificial Chromosome Spanning the Murine α 1 (I) Collagen Locus
Strauss, W. M., Dausman, J. A., Beard, C., Johnson, C. V., Lawrence, J. B., & Jaenisch, R. (1993) · Science · doi:10.1126/science.8096090 · Cited by 116 · see citing works
Inactivation of the human beta-globin gene by targeted insertion into the beta-globin locus control region.Preprint
Kim, C. G., Epner, E. M., Forrester, W. C., & Groudine, M. T. (1992) · Genes & Development · doi:10.1101/gad.6.6.928 · Cited by 109 · see citing works
Individual stage selector element mutations lead to reciprocal changes in beta- vs. epsilon-globin gene transcription: genetic confirmation of promoter competition during globin gene switching.Preprint
Foley, K. P., & Engel, J. D. (1992) · Genes & Development · doi:10.1101/gad.6.5.730 · Cited by 104 · see citing works
Self-citation
Developmental regulation of human β-globin gene transcription: a switch of loyalties?
Engel, J. D. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90248-g · Cited by 99 · see citing works
Self-citation
An Enhancer/Locus Control Region Is Not Sufficient To Open Chromatin
Reitman, M. L., Lee, E., Westphal, H., & Felsenfeld, G. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.7.3990-3998.1993 · Cited by 95 · see citing works
Microinjection of Intact 200- to 500-kb Fragments of YAC DNA into Mammalian Cells
Gnirke, A., Huxley, C. M., Peterson, K., & Olson, M. V. (1993) · Genomics · doi:10.1006/geno.1993.1121 · Cited by 93 · see citing works
Expression of the chicken GATA factor family during early erythroid development and differentiation
Leonard, M. W., Lim, K.-C., & Engel, J. D. (1993) · Development · doi:10.1242/dev.119.2.519 · Cited by 87 · see citing works
Self-citation
Developmentally regulated and erythroid-specific expression of the human embryonic β-globin gene in transgenic mice
Shih, D. M., Wall, R. J., & Shapiro, S. G. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.18.5465 · Cited by 67 · see citing works
Upstream G gamma-globin and downstream beta-globin sequences required for stage-specific expression in transgenic mice.
Trudel, M., Magram, J., Bruckner, L., & Costantini, F. D. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.11.4024 · Cited by 66 · see citing works
Human γ- to β-Globin Gene Switching Using a Mini Construct in Transgenic Mice
Lloyd, J. A., Krakowsky, J. M., Crable, S. C., & Lingrel, J. B. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.4.1561-1567.1992 · Cited by 62 · see citing works
A single beta-globin locus control region element (5' hypersensitive site 2) is sufficient for developmental regulation of human globin genes in transgenic mice.
Morley, B. J., Abbott, C. A., Sharpe, J. A., Lida, J., Chan‐Thomas, P. S., & Wood, W. G. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.5.2057 · Cited by 55 · see citing works
Physical mapping of yeast artificial chromosomes containing sequences from the human β-globin gene region
Gaensler, K. M. L., Burmeister, M., Brownstein, B. H., Taillon‐Miller, P., & Myers, R. (1991) · Genomics · doi:10.1016/0888-7543(91)90188-k · Cited by 38 · see citing works
Vectors for inserting selectable markers in vector arms and human DNA inserts of yeast artificial chromosomes (YACs)
Srivastava, A. K., & Schlessinger, D. (1991) · Gene · doi:10.1016/0378-1119(91)90390-w · Cited by 37 · see citing works
Detection of proteins like human gamma and beta globins in Escherichia coli carrying recombinant DNA plasmids.
Wilson, L. B., Grenett, H. E., Doran, D. M., Garver, F. A., & Wilson, J. T. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.5631 · Cited by 4 · see citing works
Regulated expression of globin chains and the erythroid transcription factor GATA-1 during erythropoiesis in the developing mouse.
Whitelaw, E., Tsai, S. F., Hogben, P., & Orkin, S. H. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.12.6596

Flagged first, then by citations

Research works printed but not linked: 3

Driscoll, M.C., C.S. Dobkin, and B.P. Alter. 1989. -/SI3-Thalas- semia due to a de novo mutation deleting the 5' [3-globin gene activating-region hypersensitive sites. Proc. Natl. Acad. Sci. 86: 7470-7474.
G. Stamatoyannopoulos, A.W. Nienhuis, P. Majerus, and H. Varmus), pp. 107-155.
W.B. Saunders, Philadelphia, PA.

Sorted by citations

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Looping versus linking: toward a model for long-distance gene activationPreprint
Bulger, M., & Groudine, M. T. (1999) · Genes & Development · doi:10.1101/gad.13.19.2465 · Cited by 483 · see citing works
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Li, Q., Peterson, K. R., Fang, X., & Stamatoyannopoulos, G. (2002) · Blood · doi:10.1182/blood-2002-04-1104 · Cited by 456 · see citing works
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Hardison, R., Slightom, J. L., Gumucio, D. L., Goodman, M., Stojanovic, N., & Miller, W. (1997) · Gene · doi:10.1016/s0378-1119(97)00474-5 · Cited by 230 · see citing works
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Patrinos, G. P., de Krom, M., de Boer, E., Langeveld, A., Imam, A. M. A., Strouboulis, J., de Laat, W., & Grosveld, F. G. (2004) · Genes & Development · doi:10.1101/gad.289704 · Cited by 170 · see citing works
Analysis of Mice Containing a Targeted Deletion of β-Globin Locus Control Region 5′ Hypersensitive Site 3
Hug, B. A., Wesselschmidt, R. L., Fiering, S., Bender, M. A., Epner, E. M., Groudine, M. T., & Ley, T. J. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.6.2906 · Cited by 168 · see citing works
Histone acetylation beyond promoters: long‐range acetylation patterns in the chromatin world*
Forsberg, E. C., & Bresnick, E. H. (2001) · BioEssays · doi:10.1002/bies.1117 · Cited by 153 · see citing works
The human β‐globin locus control region: A center of attraction
Levings, P. P., & Bungert, J. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2002.02797.x · Cited by 144 · see citing works
Self-citation
Activation by locus control regions?
Grosveld, F. G. (1999) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(99)80023-9 · Cited by 143 · see citing works
Locus control regions, chromatin activation and transcription
Fraser, P., & Grosveld, F. G. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80012-4 · Cited by 141 · see citing works
Regulation of β-globin gene expression: straightening out the locus
Martin, D. I. K., Fiering, S., & Groudine, M. T. (1996) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(96)80072-4 · Cited by 141 · see citing works
Rescue of the embryonic lethal hematopoietic defect reveals a critical role for GATA‐2 in urogenital development
Zhou, Y., Lim, K., Onodera, K., Takahashi, S., Ohta, J., Minegishi, N., Tsai, F., Orkin, S. H., Yamamoto, M., & Engel, J. D. (1998) · The EMBO Journal · doi:10.1093/emboj/17.22.6689 · Cited by 139 · see citing works
Self-citation
Activation of β-major globin gene transcription is associated with recruitment of NF-E2 to the β-globin LCR and gene promoter
Sawado, T., Igarashi, K., & Groudine, M. T. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.181344198 · Cited by 129 · see citing works
Transcriptional Behavior of LCR Enhancer Elements Integrated at the Same Chromosomal Locus by Recombinase-Mediated Cassette Exchange
Bouhassira, E. E., Westerman, K. A., & Leboulch, P. (1997) · Blood · doi:10.1182/blood.v90.9.3332 · Cited by 124 · see citing works
Globin Gene Expression Is Reprogrammed in Chimeras Generated by Injecting Adult Hematopoietic Stem Cells into Mouse Blastocysts
Geiger, H., Sick, S., Bonifer, C., & Müller, A. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81210-6 · Cited by 123 · see citing works
Transcriptional Regulation by (Super)Enhancers: From Discovery to Mechanisms
Grosveld, F., van Staalduinen, J., & Stadhouders, R. (2021) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-122220-093818 · Cited by 115 · see citing works
Cooperative activities of hematopoietic regulators recruit RNA polymerase II to a tissue-specific chromatin domain
Johnson, K. D., Grass, J. A., Boyer, M. E., Kiekhaefer, C. M., Blobel, G. A., Weiss, M. J., & Bresnick, E. H. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192285999 · Cited by 113 · see citing works
Effect of deletion of 5'HS3 or 5'HS2 of the human beta-globin locus control region on the developmental regulation of globin gene expression in beta-globin locus yeast artificial chromosome transgenic mice.
Peterson, K. R., Clegg, C. H., Navas, P. A., Norton, E. J., Kimbrough, T. G., & Stamatoyannopoulos, G. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.13.6605 · Cited by 102 · see citing works
Dividing the empire: boundary chromatin elements delimit the territory of enhancers
Udvardy, A. (1999) · The EMBO Journal · doi:10.1093/emboj/18.1.1 · Cited by 101 · see citing works
Embryonic and fetal β‐globin gene repression by the orphan nuclear receptors, TR2 and TR4
Tanabe, O., McPhee, D., Kobayashi, S., Shen, Y., Brandt, W., Jiang, X., Campbell, A. D., Chen, Y., Chang, C. S., Yamamoto, M., et al. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601676 · Cited by 99 · see citing works
Self-citation
Lactoferrin uptake by the rat liver. Characterization of the recognition site and effect of selective modification of arginine residues.
Ziere, G. J., van Dijk, M. C., Bijsterbosch, M. K., & van Berkel, T. J. C. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)49900-6 · Cited by 99 · see citing works
Lentiviral and genome-editing strategies for the treatment of β-hemoglobinopathies
Magrin, E., Miccio, A., & Cavazzana, M. (2019) · Blood · doi:10.1182/blood.2019000949 · Cited by 97 · see citing works
Do LCRs Open Chromatin Domains?
Higgs, D. R. (1998) · Cell · doi:10.1016/s0092-8674(00)81761-4 · Cited by 98 · see citing works
Long range interaction of cis‐DNA elements mediated by architectural transcription factor Bach1
Yoshida, C., Tokumasu, F., Hohmura, K. I., Bungert, J., Hayashi, N., Nagasawa, T., Engel, J. D., Yamamoto, M. P., Takeyasu, K., & Igarashi, K. (1999) · Genes to Cells · doi:10.1046/j.1365-2443.1999.00291.x · Cited by 96 · see citing works
Self-citation
Targeting a SWI/SNF-related chromatin remodeling complex to the β-globin promoter in erythroid cells
Lee, C. H., Murphy, M. R., Lee, J., & Chung, J. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12311 · Cited by 92 · see citing works
Localization of Distant Urogenital System-, Central Nervous System-, and Endocardium-Specific Transcriptional Regulatory Elements in the GATA-3 Locus
Lakshmanan, G., Lieuw, K. H., Lim, K.-C., Gu, Y., Grosveld, F. G., Engel, J. D., & Karis, A. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.2.1558 · Cited by 92 · see citing works
Self-citation
Hypersensitive Site 2 Specifies a Unique Function within the Human β-Globin Locus Control Region To Stimulate Globin Gene Transcription
Bungert, J., Tanimoto, K., Patel, S. M., Liu, Q., Fear, M. W., & Engel, J. D. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.4.3062 · Cited by 89 · see citing works
Self-citation
Developmental Specificity of the Interaction between the Locus Control Region and Embryonic or Fetal Globin Genes in Transgenic Mice with an HS3 Core Deletion
Navas, P. A., Peterson, K. R., Li, Q., Skarpidi, E., Rohde, A. D., Shaw, S. E., Clegg, C. H., Asano, H., & Stamatoyannopoulos, G. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.7.4188 · Cited by 88 · see citing works
Transcriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81 · see citing works
A locus control region at −12 kb of the tyrosinase gene.
Montoliu, L., Umland, T., & Schütz, G. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00991.x · Cited by 80 · see citing works
Dynamic GATA Factor Interplay at a Multicomponent Regulatory Region of the GATA-2 Locus
Martowicz, M. L., Grass, J. A., Boyer, M. E., Guend, H., & Bresnick, E. H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406038200 · Cited by 79 · see citing works
The Human β Globin Locus Introduced by YAC Transfer Exhibits a Specific and Reproducible Pattern of Developmental Regulation in Transgenic Mice
Porcu, S., Kitamura, M., Witkowska, E., Zhang, Z., Mutero, A., Lin, C. J., Chang, J., & Gaensler, K. M. L. (1997) · Blood · doi:10.1182/blood.v90.11.4602 · Cited by 79 · see citing works
Context-dependent EKLF responsiveness defines the developmental specificity of the human ɛ-globin gene in erythroid cells of YAC transgenic micePreprint
Tanimoto, K., Liu, Q., Grosveld, F. G., Bungert, J., & Engel, J. D. (2000) · Genes & Development · doi:10.1101/gad.822500 · Cited by 76 · see citing works
Self-citation
Production of transgenic mice with yeast artificial chromosomes
Peterson, K. R., Clegg, C. H., & Li, Q. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01003-2 · Cited by 74 · see citing works
A statistical model for locating regulatory regions in genomic DNA
Crowley, E. M., Roeder, K., & Bina, M. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.0965 · Cited by 70 · see citing works
Molecular aspects of embryonic hemoglobin function
Brittain, T. (2002) · Molecular Aspects of Medicine · doi:10.1016/s0098-2997(02)00004-3 · Cited by 66 · see citing works
Recruitment of Transcription Complexes to the β-Globin Gene Locus in Vivo and in Vitro
Vieira, K. F., Levings, P. P., Hill, M. A., Crusselle‐Davis, V. J., Kang, S.-H. L., Engel, J. D., & Bungert, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408883200 · Cited by 68 · see citing works
Self-citation
Erythroid Krüppel‐like factor (EKLF) contains a multifunctional transcriptional activation domain important for inter‐ and intramolecular interactions.
Chen, X., & Bieker, J. J. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00975.x · Cited by 67 · see citing works
Targeted deletion of 5′HS1 and 5′HS4 of the β-globin locus control region reveals additive activity of the DNaseI hypersensitive sites
Bender, M. A., Roach, J. N., Halow, J. M., Close, J., Alami, R., Bouhassira, E. E., Groudine, M. T., & Fiering, S. (2001) · Blood · doi:10.1182/blood.v98.7.2022 · Cited by 66 · see citing works
Experimental validation of predicted mammalian erythroid cis-regulatory modulesPreprint
Wang, H., Zhang, Y., Cheng, Y., Zhou, Y., King, D. C., Taylor, J., Chiaromonte, F., Kasturi, J., Petrykowska, H. M., Gibb, B., et al. (2006) · Genome Research · doi:10.1101/gr.5353806 · Cited by 60 · see citing works
Chromatin Structure and Control of β-Like Globin Gene Switching
Harju-Baker, S., McQueen, K. J., & Peterson, K. R. (2002) · Experimental Biology and Medicine · doi:10.1177/153537020222700902 · Cited by 58 · see citing works
Definition of Transcriptional Promoters in the Human β Globin Locus Control Region
Routledge, S. J. E., & Proudfoot, N. J. (2002) · Journal of Molecular Biology · doi:10.1016/s0022-2836(02)01011-2 · Cited by 57 · see citing works
Human β-Globin Locus Control Region HS5Contains CTCF- and Developmental Stage-Dependent Enhancer-BlockingActivity in ErythroidCells
Tanimoto, K., Sugiura, A., Omori, A., Felsenfeld, G., Engel, J. D., & Fukamizu, A. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.24.8946-8952.2003 · Cited by 55 · see citing works
Self-citation
Role of DNA Sequences Outside the Cores of DNase Hypersensitive Sites (HSs) in Functions of the β-Globin Locus Control Region
Jackson, J. D., Petrykowska, H. M., Philipsen, S., Miller, W., & Hardison, R. C. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.20.11871 · Cited by 55 · see citing works
The hypersensitive sites of the murine β-globin locus control region act independently to affect nuclear localization and transcriptional elongation
Bender, M. A., Ragoczy, T., Lee, J., Byron, R., Telling, A., Dean, A., & Groudine, M. (2012) · Blood · doi:10.1182/blood-2011-09-380485 · Cited by 53 · see citing works
Developmental regulation of eukaryotic gene loci
Bonifer, C. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02029-1 · Cited by 52 · see citing works
Reconstitution of Human β-Globin Locus Control Region Hypersensitive Sites in the Absence of Chromatin Assembly
Leach, K. M., Nightingale, K. P., Igarashi, K., Levings, P. P., Engel, J. D., Becker, P. B., & Bungert, J. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.8.2629-2640.2001 · Cited by 52 · see citing works
Self-citation
Fine Tuning of Globin Gene Expression by DNA Methylation
Goren, A., Simchen, G., Fibach, E., Szabó, P. E., Tanimoto, K., Chakalova, L., Pfeifer, G. P., Fraser, P., Engel, J. D., & Cedar, H. (2006) · PLoS ONE · doi:10.1371/journal.pone.0000046 · Cited by 50 · see citing works
Self-citation
Distinct Domains of Erythroid Kruüppel-Like Factor Modulate Chromatin Remodeling and Transactivation at the Endogenous β-Globin Gene Promoter
Brown, R. C., Pattison, S. T., van Ree, J. H., Coghill, E., Perkins, A. C., Jane, S. M., & Cunningham, J. M. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.1.161-170.2002 · Cited by 50 · see citing works
Mutation of gene-proximal regulatory elements disrupts human ɛ-, γ-, and β-globin expression in yeast artificial chromosome transgenic mice
Liu, Q., Bungert, J., & Engel, J. D. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.1.169 · Cited by 50 · see citing works
Self-citation
Genomic Domains and Regulatory Elements Operating at the Domain Level
Razin, S. V., Farrell, C. M., & Targa, F. R. (2003) · International review of cytology · doi:10.1016/s0074-7696(03)01002-7 · Cited by 49 · see citing works
Developmental elimination of ectopic projection sites for the transgenic OR gene that has lost zone specificity in the olfactory epithelium
Nakatani, H., Serizawa, S., Nakajima, M., Imai, T., & Sakano, H. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02998.x · Cited by 49 · see citing works
Sequences Flanking Hypersensitive Sites of the β-Globin Locus Control Region Are Required for Synergistic Enhancement
Molete, J. M., Petrykowska, H. M., Bouhassira, E. E., Feng, Y., Miller, W., & Hardison, R. C. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.9.2969-2980.2001 · Cited by 49 · see citing works
Role of NF-Y in In Vivo Regulation of the γ-Globin Gene
Duan, Z., Stamatoyannopoulos, G., & Li, Q. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.9.3083-3095.2001 · Cited by 49 · see citing works
Transcriptional control of globin gene switching during vertebrate development
Baron, M. H. (1997) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(96)00195-9 · Cited by 46 · see citing works
Transcriptional Mechanisms Underlying Hemoglobin SynthesisPreprint
Katsumura, K. R., DeVilbiss, A., Pope, N. J., Johnson, K. D., & Bresnick, E. H. (2013) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a015412 · Cited by 43 · see citing works
Phase Separation and Transcription Regulation: Are Super-Enhancers and Locus Control Regions Primary Sites of Transcription Complex Assembly?
Gurumurthy, A., Shen, Y., Gunn, E. M., & Bungert, J. (2019) · BioEssays · doi:10.1002/bies.201800164 · Cited by 41 · see citing works
Self-citation
Synergism between hypersensitive sites confers long-range gene activation by the β-globin locus control region
Bresnick, E. H., & Tze, L. E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.9.4566 · Cited by 41 · see citing works
The 5′HS4 core element of the human β-globin locus control region is required for high-level globin gene expression in definitive but not in primitive erythropoiesis 1 1Edited by M. Yaniv
Navas, P. A., Peterson, K. R., Li, Q., McArthur, M., & Stamatoyannopoulos, G. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4939 · Cited by 41 · see citing works
Sickle Cell Disease: From Genetics to Curative Approaches
Hardouin, G., Magrin, E., Corsia, A., Cavazzana, M., Miccio, A., & Semeraro, M. (2023) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-120122-081037 · Cited by 40 · see citing works
Antagonistic Regulation of β-Globin Gene Expression by Helix-Loop-Helix Proteins USF and TFII-I
Crusselle‐Davis, V. J., Vieira, K. F., Zhou, Z., Anantharaman, A., & Bungert, J. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01770-05 · Cited by 38 · see citing works
Self-citation
Hypersensitive site 6 of the Th2 locus control region is essential for Th2 cytokine expression
Williams, A., Lee, G. R., Spilianakis, C. G., Hwang, S. S., Eisenbarth, S. C., & Flavell, R. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304720110 · Cited by 37 · see citing works
Evaluation of beta-globin gene therapy constructs in single copy transgenic mice
Ellis, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.6.1296 · Cited by 37 · see citing works
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
Sabatino, D. E., Cline, A. P., Gallagher, P. G., Garrett, L. J., Stamatoyannopoulos, G., Forget, B. G., & Bodine, D. M. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.11.6634 · Cited by 37 · see citing works
In Vivo Formation of a Human β-Globin Locus Control Region Core Element Requires Binding Sites for Multiple Factors Including GATA-1, NF-E2, Erythroid Kruppel-like Factor, and Sp1
Goodwin, A. J., IV, McInerney, J. M., Glander, M. A., Pomerantz, O., & Lowrey, C. H. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008410200 · Cited by 36 · see citing works
LCR-dependent gene expression in beta-globin YAC transgenics: detailed structural studies validate functional analysis even in the presence of fragmented YACs
Peterson, K. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.13.2079 · Cited by 36 · see citing works
Silencers and locus control regions: opposite sides of the same coin
Kamakaka, R. T. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(96)10074-8 · Cited by 36 · see citing works
Current status of globin gene therapy for the treatment of β‐thalassaemia
Lisowski, L., & Sadelain, M. (2008) · British Journal of Haematology · doi:10.1111/j.1365-2141.2008.07098.x · Cited by 41 · see citing works
Independent formation of DnaseI hypersensitive sites in the murine β-globin locus control region
Bender, M. A., Mehaffey, M. G., Telling, A., Hug, B. A., Ley, T. J., Groudine, M. T., & Fiering, S. (2000) · Blood · doi:10.1182/blood.v95.11.3600 · Cited by 35 · see citing works
Recombinogenic targeting: a new approach to genomic analysis—a review
Shashikant, C. S., Carr, J. L., Bhargava, J., Bentley, K. L., & Ruddle, F. H. (1998) · Gene · doi:10.1016/s0378-1119(98)00369-2 · Cited by 35 · see citing works
Locus control region mediated regulation of adult β‐globin gene expression
Liang, S. Y., Moghimi, B., Yang, T. P., Strouboulis, J., & Bungert, J. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21820 · Cited by 34 · see citing works
Self-citation
Adult Stage γ-Globin Silencing Is Mediated by a Promoter Direct Repeat Element
Omori, A., Tanabe, O., Engel, J. D., Fukamizu, A., & Tanimoto, K. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.9.3443-3451.2005 · Cited by 33 · see citing works
Self-citation
Phylogenetic Footprinting of Hypersensitive Site 3 of the β-Globin Locus Control Region
Shelton, D. A., Stegman, L. D., Hardison, R. C., Miller, W., Bock, J. H., Slightom, J. L., Goodman, M., & Gumucio, D. L. (1997) · Blood · doi:10.1182/blood.v89.9.3457 · Cited by 32 · see citing works
Genome Editing for β-Hemoglobinopathies: Advances and Challenges
Frati, G., & Miccio, A. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10030482 · Cited by 31 · see citing works
Transgenic mice expressing small interfering RNA against Gata4 point to a crucial role of Gata4 in the heart and gonads
Thurisch, B., Liang, S. Y., Sarioglu, N. M. E., Schomburg, L., Bungert, J., & Dame, C. (2009) · Journal of Molecular Endocrinology · doi:10.1677/jme-09-0030 · Cited by 30 · see citing works
Self-citation
The beta‐globin locus control region versus gene therapy vectors: a struggle for expression
Ellis, J., & Pannell, D. (2001) · Clinical Genetics · doi:10.1034/j.1399-0004.2001.590103.x · Cited by 30 · see citing works
Human hematopoiesis in murine embryos after injecting human cord blood–derived hematopoietic stem cells into murine blastocysts
Harder, F., Henschler, R., Junghahn, I., Lamers, M. C., & Müller, A. M. (2002) · Blood · doi:10.1182/blood.v99.2.719 · Cited by 30 · see citing works
Recruitment of transcription complexes to the β‐globin locus control region and transcription of hypersensitive site 3 prior to erythroid differentiation of murine embryonic stem cells
Levings, P. P., Zhou, Z., Vieira, K. F., Crusselle‐Davis, V. J., & Bungert, J. (2006) · FEBS Journal · doi:10.1111/j.1742-4658.2005.05107.x · Cited by 29 · see citing works
Self-citation
Proper Developmental Control of Human Globin Genes Reproduced by Transgenic Mice Containing a 160-kb BAC Carrying the Human β-Globin Locus
Huang, Y., Liu, D., Wu, L., Li, T.-C., Wu, M., Feng, D.-X., & Liang, C. (2000) · Blood Cells Molecules and Diseases · doi:10.1006/bcmd.2000.0339 · Cited by 29 · see citing works
Structural Analysis and Mapping of DNase I Hypersensitivity of HS5 of the β-Globin Locus Control Region
Li, Q., Zhang, M., Duan, Z., & Stamatoyannopoulos, G. (1999) · Genomics · doi:10.1006/geno.1999.5954 · Cited by 29 · see citing works
Chimaerism and erythroid marker expression after microinjection of human acute myeloid leukaemia cells into murine blastocysts
Dürr, M., Harder, F., Merkel, A., Bug, G., Henschler, R., & Müller, A. M. (2003) · Oncogene · doi:10.1038/sj.onc.1207134 · Cited by 28 · see citing works
Individual LCR hypersensitive sites cooperate to generate an open chromatin domain spanning the human β‐globin locus
Li, G., Lim, K.-C., Engel, J. D., & Bungert, J. (1998) · Genes to Cells · doi:10.1046/j.1365-2443.1998.00200.x · Cited by 28 · see citing works
Self-citation
Enhancer switching in cell lineage priming is linked to eRNA, Brg1’s AT-hook, and SWI/SNF recruitment
Saha, D., Animireddy, S., Lee, J., Thommen, A., Murvin, M. M., Lu, Y., Calabrese, J. M., & Bartholomew, B. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.03.013 · Cited by 28 · see citing works
Cooperativeness of the Higher Chromatin Structure of the β-Globin Locus Revealed by the Deletion Mutations of DNase I Hypersensitive site 3 of the LCR
Fang, X., Xiang, P., Yin, W., Stamatoyannopoulos, G., & Li, Q. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.09.072 · Cited by 27 · see citing works
Artificial chromosome-based transgenes in the study of genome function
Heaney, J. D., & Bronson, S. K. (2006) · Mammalian Genome · doi:10.1007/s00335-006-0023-9 · Cited by 27 · see citing works
Synergistic and Additive Properties of the Beta-Globin Locus Control Region (LCR) Revealed by 5′HS3 Deletion Mutations: Implication for LCR Chromatin Architecture
Fang, X., Sun, J., Xiang, P., Yu, M., Navas, P. A., Peterson, K. R., Stamatoyannopoulos, G., & Li, Q. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.16.7033-7041.2005 · Cited by 27 · see citing works
Developmental Regulation of the β-Globin Gene Locus
Chakalova, L., Carter, D., Debrand, E., Goyenechea, B., Horton, A., Miles, J., Osborne, C. S., & Fraser, P. (2005) · Springer eBooks · doi:10.1007/3-540-27310-7_8 · Cited by 25 · see citing works

Effects of human locus control region elements HS2 and HS3 on human β-globin gene expression in transgenic mouse
Jia, C., Huang, S., Yan, J., Xiao, Y., Ren, Z., & Zeng, Y. (2003) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2003.07.001 · Cited by 12 · see citing works
Developmental Specificity of the Interaction between the Locus Control Region and Embryonic or Fetal Globin Genes in Transgenic Mice with an HS3 Core Deletion
Navas, P. A., Peterson, K. R., Li, Q., Skarpidi, E., Rohde, A. D., Shaw, S. E., Clegg, C. H., Asano, H., & Stamatoyannopoulos, G. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.7.4188 · Cited by 88 · see citing works
Effect of deletion of 5'HS3 or 5'HS2 of the human beta-globin locus control region on the developmental regulation of globin gene expression in beta-globin locus yeast artificial chromosome transgenic mice.
Peterson, K. R., Clegg, C. H., Navas, P. A., Norton, E. J., Kimbrough, T. G., & Stamatoyannopoulos, G. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.13.6605 · Cited by 102 · see citing works
A Single β-Globin Locus Control Region Element (5' Hypersensitive Site 2) Is Sufficient for Developmental Regulation of Human Globin Genes in Transgenic Mice
Morley, B. J., Abbott, C. A., Sharpe, J. A., Lida, J., Chan‐Thomas, P. S., & Wood, W. G. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.5.2057-2066.1992 · Cited by 4 · see citing works
A single beta-globin locus control region element (5' hypersensitive site 2) is sufficient for developmental regulation of human globin genes in transgenic mice.
Morley, B. J., Abbott, C. A., Sharpe, J. A., Lida, J., Chan‐Thomas, P. S., & Wood, W. G. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.5.2057 · Cited by 55 · see citing works

Authors: Bungert, J., Davé, U., Lim, K. C., Lieuw, K. H., Shavit, J. A., Liu, Q., & Engel, J. D.
Affiliations: Northwestern University (US)
ORCID: Bungert, J
Davé, U
Shavit, J A
Engel, J D
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 1995-12-15
Volume: 9
Issue: 24
Pages: 3083-3096
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.9.24.3083
OpenAlex: W2050579225
Cited by: 183
References: 63
Citations by year: 2025: 1 · 2024: 1 · 2023: 1 · 2021: 5 · 2019: 2 · 2018: 4 · 2017: 1 · 2015: 1 · 2013: 2 · 2012: 4
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Genes & Development (publishedVersion)
PubMed (publishedVersion)
Funders: Northwestern University
Harvard University
University of Minnesota
Deutsches Krebsforschungszentrum
Deutsche Forschungsgemeinschaft
National Institutes of Health
National Heart, Lung, and Blood Institute (HL 24415, R01HL024415)
Topics: Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
Keywords: locus control region, HS3, hypersensitive sites, erythroid development, stage-specific gene expression, embryonic erythropoiesis, epsilon-globin, gamma-globin, competitive regulation, globin gene expression, yeast artificial chromosomes
MeSH terms: Animals, Base Sequence, Globins, Humans, Mice, Transgenic, Molecular Sequence Data, Mutation, Oligodeoxyribonucleotides, RNA, Messenger, Transcriptional Activation, Polymerase Chain Reaction, Chromosomes, Artificial, Yeast, Gene Expression Regulation, Developmental, Mice

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Synergistic regulation of human beta-globin gene switching by locus control region elements HS3 and HS4.

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