Genome-wide chromatin state transitions associated with developmental and environmental cues

Jiang Zhu; Mazhar Adli; James Y. Zou; Griet Verstappen; Michael Coyne; Xiaolan Zhang; Timothy Durham; Mohammad Miri; Vikram Deshpande; Philip L. De Jager; David A. Bennett; Joseph A. Houmard; Deborah M. Muoio; Tamer T. Onder; Ray Camahort; Chad A. Cowan; Alexander Meissner; Charles B. Epstein; Noam Shoresh; Bradley E. Bernstein

doi:10.1016/j.cell.2012.12.033

Genome-wide chromatin state transitions associated with developmental and environmental cues

Jiang Zhu, Mazhar Adli^*, James Y. Zou, Griet Verstappen, Michael Coyne, Xiaolan Zhang, Timothy Durham, Mohammad Miri, Vikram Deshpande, Philip L. De Jager, David A. Bennett, Joseph A. Houmard, Deborah M. Muoio, Tamer T. Onder, Ray Camahort, Chad A. Cowan, Alexander Meissner, Charles B. Epstein, Noam Shoresh, Bradley E. Bernstein

^*Corresponding author for this work

Obstetrics and Gynecology

Research output: Contribution to journal › Article › peer-review

429 Scopus citations

Abstract

Differences in chromatin organization are key to the multiplicity of cell states that arise from a single genetic background, yet the landscapes of in vivo tissues remain largely uncharted. Here, we mapped chromatin genome-wide in a large and diverse collection of human tissues and stem cells. The maps yield unprecedented annotations of functional genomic elements and their regulation across developmental stages, lineages, and cellular environments. They also reveal global features of the epigenome, related to nuclear architecture, that also vary across cellular phenotypes. Specifically, developmental specification is accompanied by progressive chromatin restriction as the default state transitions from dynamic remodeling to generalized compaction. Exposure to serum in vitro triggers a distinct transition that involves de novo establishment of domains with features of constitutive heterochromatin. We describe how these global chromatin state transitions relate to chromosome and nuclear architecture, and discuss their implications for lineage fidelity, cellular senescence, and reprogramming.

Original language	English (US)
Pages (from-to)	642-654
Number of pages	13
Journal	Cell
Volume	152
Issue number	3
DOIs	https://doi.org/10.1016/j.cell.2012.12.033
State	Published - Jan 31 2013

Funding

We acknowledge members of the Broad Institute’s Epigenomics Program and Genome Sequencing and Analysis Program, and the NIH Epigenomics Mapping Consortium for constructive comments. We thank Kevin Eggan for ES and iPS lines; Allen Powe and Steve Stice for neural cells; Greg Lauwers and the MGH Tissue Repository for tissue procurement; and David Flowers, Irwin Bernstein, John Stamatoyannopoulos and Shelly Heimfeld for blood samples. We also thank Leslie Gaffney and Lauren Solomon for assistance with figures. This research was supported by the NIH Common Fund (U01 ES017155); the National Human Genome Research Institute (U54 HG004570); the National Heart, Lung and Blood Institute (U01 HL100395); the National Institute on Aging (P30 AG10161); the Howard Hughes Medical Institute; the Starr Cancer Consortium; and the Burroughs Wellcome Fund.

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2012.12.033

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Zhu, J., Adli, M., Zou, J. Y., Verstappen, G., Coyne, M., Zhang, X., Durham, T., Miri, M., Deshpande, V., De Jager, P. L., Bennett, D. A., Houmard, J. A., Muoio, D. M., Onder, T. T., Camahort, R., Cowan, C. A., Meissner, A., Epstein, C. B., Shoresh, N., & Bernstein, B. E. (2013). Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell, 152(3), 642-654. https://doi.org/10.1016/j.cell.2012.12.033

@article{b80f33abdb384e2cac85fda0405b7f9a,

title = "Genome-wide chromatin state transitions associated with developmental and environmental cues",

abstract = "Differences in chromatin organization are key to the multiplicity of cell states that arise from a single genetic background, yet the landscapes of in vivo tissues remain largely uncharted. Here, we mapped chromatin genome-wide in a large and diverse collection of human tissues and stem cells. The maps yield unprecedented annotations of functional genomic elements and their regulation across developmental stages, lineages, and cellular environments. They also reveal global features of the epigenome, related to nuclear architecture, that also vary across cellular phenotypes. Specifically, developmental specification is accompanied by progressive chromatin restriction as the default state transitions from dynamic remodeling to generalized compaction. Exposure to serum in vitro triggers a distinct transition that involves de novo establishment of domains with features of constitutive heterochromatin. We describe how these global chromatin state transitions relate to chromosome and nuclear architecture, and discuss their implications for lineage fidelity, cellular senescence, and reprogramming.",

author = "Jiang Zhu and Mazhar Adli and Zou, {James Y.} and Griet Verstappen and Michael Coyne and Xiaolan Zhang and Timothy Durham and Mohammad Miri and Vikram Deshpande and {De Jager}, {Philip L.} and Bennett, {David A.} and Houmard, {Joseph A.} and Muoio, {Deborah M.} and Onder, {Tamer T.} and Ray Camahort and Cowan, {Chad A.} and Alexander Meissner and Epstein, {Charles B.} and Noam Shoresh and Bernstein, {Bradley E.}",

note = "Funding Information: We acknowledge members of the Broad Institute{\textquoteright}s Epigenomics Program and Genome Sequencing and Analysis Program, and the NIH Epigenomics Mapping Consortium for constructive comments. We thank Kevin Eggan for ES and iPS lines; Allen Powe and Steve Stice for neural cells; Greg Lauwers and the MGH Tissue Repository for tissue procurement; and David Flowers, Irwin Bernstein, John Stamatoyannopoulos and Shelly Heimfeld for blood samples. We also thank Leslie Gaffney and Lauren Solomon for assistance with figures. This research was supported by the NIH Common Fund (U01 ES017155); the National Human Genome Research Institute (U54 HG004570); the National Heart, Lung and Blood Institute (U01 HL100395); the National Institute on Aging (P30 AG10161); the Howard Hughes Medical Institute; the Starr Cancer Consortium; and the Burroughs Wellcome Fund. ",

year = "2013",

month = jan,

day = "31",

doi = "10.1016/j.cell.2012.12.033",

language = "English (US)",

volume = "152",

pages = "642--654",

journal = "Cell",

issn = "0092-8674",

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Zhu, J, Adli, M, Zou, JY, Verstappen, G, Coyne, M, Zhang, X, Durham, T, Miri, M, Deshpande, V, De Jager, PL, Bennett, DA, Houmard, JA, Muoio, DM, Onder, TT, Camahort, R, Cowan, CA, Meissner, A, Epstein, CB, Shoresh, N & Bernstein, BE 2013, 'Genome-wide chromatin state transitions associated with developmental and environmental cues', Cell, vol. 152, no. 3, pp. 642-654. https://doi.org/10.1016/j.cell.2012.12.033

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T1 - Genome-wide chromatin state transitions associated with developmental and environmental cues

AU - Zhu, Jiang

AU - Adli, Mazhar

AU - Zou, James Y.

AU - Verstappen, Griet

AU - Coyne, Michael

AU - Zhang, Xiaolan

AU - Durham, Timothy

AU - Miri, Mohammad

AU - Deshpande, Vikram

AU - De Jager, Philip L.

AU - Bennett, David A.

AU - Houmard, Joseph A.

AU - Muoio, Deborah M.

AU - Onder, Tamer T.

AU - Camahort, Ray

AU - Cowan, Chad A.

AU - Meissner, Alexander

AU - Epstein, Charles B.

AU - Shoresh, Noam

AU - Bernstein, Bradley E.

N1 - Funding Information: We acknowledge members of the Broad Institute’s Epigenomics Program and Genome Sequencing and Analysis Program, and the NIH Epigenomics Mapping Consortium for constructive comments. We thank Kevin Eggan for ES and iPS lines; Allen Powe and Steve Stice for neural cells; Greg Lauwers and the MGH Tissue Repository for tissue procurement; and David Flowers, Irwin Bernstein, John Stamatoyannopoulos and Shelly Heimfeld for blood samples. We also thank Leslie Gaffney and Lauren Solomon for assistance with figures. This research was supported by the NIH Common Fund (U01 ES017155); the National Human Genome Research Institute (U54 HG004570); the National Heart, Lung and Blood Institute (U01 HL100395); the National Institute on Aging (P30 AG10161); the Howard Hughes Medical Institute; the Starr Cancer Consortium; and the Burroughs Wellcome Fund.

PY - 2013/1/31

Y1 - 2013/1/31

N2 - Differences in chromatin organization are key to the multiplicity of cell states that arise from a single genetic background, yet the landscapes of in vivo tissues remain largely uncharted. Here, we mapped chromatin genome-wide in a large and diverse collection of human tissues and stem cells. The maps yield unprecedented annotations of functional genomic elements and their regulation across developmental stages, lineages, and cellular environments. They also reveal global features of the epigenome, related to nuclear architecture, that also vary across cellular phenotypes. Specifically, developmental specification is accompanied by progressive chromatin restriction as the default state transitions from dynamic remodeling to generalized compaction. Exposure to serum in vitro triggers a distinct transition that involves de novo establishment of domains with features of constitutive heterochromatin. We describe how these global chromatin state transitions relate to chromosome and nuclear architecture, and discuss their implications for lineage fidelity, cellular senescence, and reprogramming.

AB - Differences in chromatin organization are key to the multiplicity of cell states that arise from a single genetic background, yet the landscapes of in vivo tissues remain largely uncharted. Here, we mapped chromatin genome-wide in a large and diverse collection of human tissues and stem cells. The maps yield unprecedented annotations of functional genomic elements and their regulation across developmental stages, lineages, and cellular environments. They also reveal global features of the epigenome, related to nuclear architecture, that also vary across cellular phenotypes. Specifically, developmental specification is accompanied by progressive chromatin restriction as the default state transitions from dynamic remodeling to generalized compaction. Exposure to serum in vitro triggers a distinct transition that involves de novo establishment of domains with features of constitutive heterochromatin. We describe how these global chromatin state transitions relate to chromosome and nuclear architecture, and discuss their implications for lineage fidelity, cellular senescence, and reprogramming.

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Genome-wide chromatin state transitions associated with developmental and environmental cues

Abstract

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ASJC Scopus subject areas

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