Cited by 396Developmental Biology and Gene RegulationGenomics and Chromatin DynamicsGene Regulatory Network Analysis

Shadow Enhancers Foster Robustness of Drosophila Gastrulation

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Perry, Michael W., Boettiger, Alistair N., Bothma, Jacques P., Levine, Michael·2010·Current Biology

Abstract

Critical developmental control genes sometimes contain "shadow" enhancers that can be located in remote positions, including the introns of neighboring genes [1]. They nonetheless produce patterns of gene expression that are the same as or similar to those produced by more proximal primary enhancers. It was suggested that shadow enhancers help foster robustness in gene expression in response to environmental or genetic perturbations [2, 3]. We critically tested this hypothesis by employing a combination of bacterial artificial chromosome (BAC) recombineering and quantitative confocal imaging methods [2, 4]. Evidence is presented that the snail gene is regulated by a distal shadow enhancer located within a neighboring locus. Removal of the proximal primary enhancer does not significantly perturb snail function, including the repression of neurogenic genes and formation of the ventral furrow during gastrulation at normal temperatures. However, at elevated temperatures, there is sporadic loss of snail expression and coincident disruptions in gastrulation. Similar defects are observed at normal temperatures upon reductions in the levels of Dorsal, a key activator of snail expression (reviewed in [5]). These results suggest that shadow enhancers represent a novel mechanism of canalization whereby complex developmental processes "bring about one definite end-result regardless of minor variations in conditions" [6].

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Crossref · 10.1016/j.cub.2010.07.043

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  • Multiple enhancers may provide robustness in gene expression.

    “From the data presented here and from others29, 30, it seems likely that multiple enhancers may provide robustness in gene expression.”

    From Genetic dissection of the α-globin super-enhancer in vivo (2016) · cites this paper as [30]

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Research works printed but not linked: 28

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Cited by

Sorted by citations

Authors
Perry, M. W., Boettiger, A. N., Bothma, J. P., & Levine, M.
Affiliations
University of California, Berkeley (US)
Corresponding author
Levine, Michael
Venue
Current Biology
Publisher
Elsevier BV
Published
2010-09
Volume
20
Issue
17
Pages
1562-1567
ISSN
0960-9822 (ISSN-L)
OpenAlex
W2021373833
Cited by
396
References
4
Citations by year
2026: 19 · 2025: 22 · 2024: 25 · 2023: 21 · 2022: 17 · 2021: 25 · 2020: 32 · 2019: 25 · 2018: 24 · 2017: 23 · 2016: 23 · 2015: 26 · 2014: 30 · 2013: 31 · 2012: 24
FWCI
10.82
Type
journal article
Language
en
Open access
Locations
  • Current Biology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (GM46638)
  • National Science Foundation
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords
Drosophila gastrulation, ventral furrow formation, developmental robustness, canalization, Dorsal, temperature sensitivity, gene expression regulation, intronic enhancer
MeSH terms
Animals, Drosophila, Chromosomes, Artificial, Bacterial, Gastrulation

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