Increased enhancer–promoter interactions during developmental enhancer activation in mammals

Chen, Zhuoxin; Snetkova, Valentina; Bower, Grace; Jacinto, Sandra; Clock, Benjamin; Dizehchi, Atrin; Barozzi, Iros; Mannion, Brandon J.; Alcaina-Caro, Ana; Lopez-Rios, Javier; Dickel, Diane E.; Visel, Axel; Pennacchio, Len A.; Kvon, Evgeny Z.

doi:10.1038/s41588-024-01681-2

Title: Increased enhancer–promoter interactions during developmental enhancer activation in mammals

Journal Article · 20 March 2024 · Nature Genetics

DOI: https://doi.org/10.1038/s41588-024-01681-2 · OSTI ID:2472917

^[1];

^[2]; Bower, Grace ^[1]; Jacinto, Sandra ^[1];

^[1]; Dizehchi, Atrin ^[1];

^[3];

^[4];

^[5];

^[6]; Dickel, Diane E. ^[7];

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Univ. of California, Irvine, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Medical University of Vienna (Austria)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
Universidad Pablo de Olavide, Seville (Spain)
Universidad Pablo de Olavide, Seville (Spain); Universidad Loyola Andalucía, Seville (Spain)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Octant, Inc, Emeryville, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Merced, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Remote enhancers are thought to interact with their target promoters via physical proximity, yet the importance of this proximity for enhancer function remains unclear. Here, in this study, we investigate the three-dimensional (3D) conformation of enhancers during mammalian development by generating high-resolution tissue-resolved contact maps for nearly a thousand enhancers with characterized in vivo activities in ten murine embryonic tissues. Sixty-one percent of developmental enhancers bypass their neighboring genes, which are often marked by promoter CpG methylation. The majority of enhancers display tissue-specific 3D conformations, and both enhancer-promoter and enhancer-enhancer interactions are moderately but consistently increased upon enhancer activation in vivo. Less than 14% of enhancer-promoter interactions form stably across tissues; however, these invariant interactions form in the absence of the enhancer and are likely mediated by adjacent CTCF binding. Our results highlight the general importance of enhancer-promoter physical proximity for developmental gene activation in mammals.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: María de Maeztu; Ministry of Science, Innovation and Universities (MICIU); National Institutes of Health (NIH); National Science Foundation (NSF); Simons Foundation; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2472917

Journal Information:: Nature Genetics, Journal Name: Nature Genetics Journal Issue: 4 Vol. 56; ISSN 1061-4036

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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