Looping and Interaction between Hypersensitive Sites in the Active β-globin Locus

Tolhuis, Bas; Palstra, Robert-Jan; Splinter, Erik; Grosveld, Frank; de Laat, Wouter

doi:10.1016/s1097-2765(02)00781-5

Cited by 1,344Genomics and Chromatin DynamicsChromatin Remodeling and CancerHemoglobinopathies and Related Disorders

Looping and Interaction between Hypersensitive Sites in the Active β-globin Locus

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Tolhuis, Bas, Palstra, Robert-Jan, Splinter, Erik, Grosveld, Frank, de Laat, Wouter·2002·Molecular Cell

DOI 10.1016/s1097-2765(02)00781-5

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Abstract

Eukaryotic transcription can be regulated over tens or even hundreds of kilobases. We show that such long-range gene regulation in vivo involves spatial interactions between transcriptional elements, with intervening chromatin looping out. The spatial organization of a 200 kb region spanning the murine beta-globin locus was analyzed in expressing erythroid and nonexpressing brain tissue. In brain, the globin cluster adopts a seemingly linear conformation. In erythroid cells the hypersensitive sites of the locus control region (LCR), located 40-60 kb away from the active genes, come in close spatial proximity with these genes. The intervening chromatin with inactive globin genes loops out. Moreover, two distant hypersensitive regions participate in these interactions. We propose that clustering of regulatory elements is key to creating and maintaining active chromatin domains and regulating transcription.

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3C confirmed that the LCR comes into close contact with active β-globin genes, whilst the intervening inactive genes are looped out.
“3C confirmed that the LCR comes into close contact with active β-globin genes, whilst the intervening inactive genes are looped out [266].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [266]
Two papers published in 2002 used different novel biochemical techniques to demonstrate that the β-globin LCR forms chromosomal loops with the active β-globin genes in vivo.
“Two papers published in 2002 used different novel biochemical techniques to demonstrate that the β-globin LCR forms chromosomal loops with the active β-globin genes in vivo.”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [266]
Enhancer-promoter looping occurred in erythroid cells, in which the β-globin genes are expressed, but not in brain cells, in which they are not.
“Enhancer–promoter looping occurred in erythroid cells, in which the β-globin genes are expressed, but not in brain cells, in which they are not [266].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [266]
Remote enhancers in the mouse β-globin gene domain form a single complex to which the genes that need to be activated are recruited.
“It has been shown that remote enhancers in the mouse β-globin gene domain form a single complex to which the genes that need to be activated are recruited [32].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [32]
Active enhancers are often in physical proximity to the promoters they activate, regardless of the genomic distances between these enhancers and promoters.
“First, it was shown that active enhancers are often in physical proximity to the promoters they activate, regardless of the genomic distances between these enhancers and promoters [32,33,34].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [32]

In erythroid cells expressing globin genes, a large CTCF-CTCF loop encompasses the beta-globin genes and the locus control region (LCR), consistent with the organization of the locus in an insulated neighborhood.
“In erythroid cells expressing globin genes, a large CTCF-CTCF loop encompasses the beta-globin genes and the locus control region (LCR), consistent with the organization of the locus in an insulated neighborhood.”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Tolhuis et al., 2002
Tissue-specific CTCF-CTCF loops participate in developmental gene control.
“In fetal brain cells, CTCF binding to one of the beta-globin loop anchor regions is absent and CTCF-CTCF loop formation is not detected (Splinter et al., 2006; Tolhuis et al., 2002), which suggests that tissue-specific CTCF-CTCF loops participate in developmental gene control.”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Tolhuis et al., 2002
Central to the mechanism of globin gene switching is the exclusive interaction between the LCR and globin gene promoters at distinct developmental stages.
“Central to the mechanism of globin gene switching is the exclusive interaction between the LCR and globin gene promoters at distinct developmental stages (Carter et al., 2002; Palstra et al., 2008; Tolhuis et al., 2002).”
From Reactivation of developmentally silenced globin genes by forced chromatin looping (2014) · cites this paper as Tolhuis et al., 2002
In erythroid cells, the locus control region (LCR) is in physical proximity to the β-globin genes in a developmentally dynamic manner.
“In erythroid cells, a powerful distal enhancer called the locus control region (LCR), composed of multiple DNase I hypersensitive sites (HSs), is in physical proximity to the β-globin genes in a developmentally dynamic manner (Carter et al., 2002; Tolhuis et al., 2002).”
From Reactivation of developmentally silenced globin genes by forced chromatin looping (2014) · cites this paper as Tolhuis et al., 2002

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Authors: Tolhuis, B., Palstra, R.-J., Splinter, E., Grosveld, F., & de Laat, W.
Affiliations: Erasmus University Rotterdam (NL)
ORCID: Palstra, Robert-Jan
Splinter, Erik
Grosveld, Frank
Venue: Molecular Cell
Publisher: Elsevier BV
Published: 2002-12
Volume: 10
Issue: 6
Pages: 1453-1465
ISSN: 1097-2765 (ISSN-L)
DOI: 10.1016/s1097-2765(02)00781-5
OpenAlex: W2089894746
Cited by: 1,344
References: 48
Citations by year: 2026: 19 · 2025: 23 · 2024: 39 · 2023: 26 · 2022: 38 · 2021: 44 · 2020: 46 · 2019: 55 · 2018: 58 · 2017: 58 · 2016: 70 · 2015: 68 · 2014: 76 · 2013: 62 · 2012: 84
FWCI: 15.10
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3881 d)
Locations: Molecular Cell (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
Keywords: chromatin looping, long-range gene regulation, beta-globin locus control region, hypersensitive sites, chromatin domains, erythroid cells, brain tissue, transcriptional regulation
MeSH terms: Animals, Binding Sites, Brain, Chromatin, Chromosome Mapping, DNA, Multigene Family, Globins, Liver, Nucleic Acid Conformation, Locus Control Region, Mice

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Looping and Interaction between Hypersensitive Sites in the Active β-globin Locus

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