DOI: 10.1038/msb.2010.35. Dynamic CRM occupancy reflects a temporal map of developmental progression

Dynamic CRM occupancy reflects a temporal map of developmental progression

10.1038/msb.2010.35

Crossref journal-article

Springer Science and Business Media LLC

Molecular Systems Biology (297)

Abstract

Development is driven by tightly coordinated spatio‐temporal patterns of gene expression, which are initiated through the action of transcription factors (TFs) binding to cis‐regulatory modules (CRMs). Although many studies have investigated how spatial patterns arise, precise temporal control of gene expression is less well understood. Here, we show that dynamic changes in the timing of CRM occupancy is a prevalent feature common to all TFs examined in a developmental ChIP time course to date. CRMs exhibit complex binding patterns that cannot be explained by the sequence motifs or expression of the TFs themselves. The temporal changes in TF binding are highly correlated with dynamic patterns of target gene expression, which in turn reflect transitions in cellular function during different stages of development. Thus, it is not only the timing of a TF's expression, but also its temporal occupancy in refined time windows, which determines temporal gene expression. Systematic measurement of dynamic CRM occupancy may therefore serve as a powerful method to decode dynamic changes in gene expression driving developmental progression.

Bibliography

WilczyÅski, B., & Furlong, E. E. M. (2010). Dynamic CRM occupancy reflects a temporal map of developmental progression. Molecular Systems Biology, 6(1). Portico.

Authors 2

Bartek Wilczyński (first)
Eileen E M Furlong (additional)

References 55 Referenced 39

Dates

Type	When
Created	15 years, 2 months ago (June 23, 2010, 6:54 a.m.)
Deposited	1 year, 8 months ago (Dec. 18, 2023, 3:52 p.m.)
Indexed	1 month ago (July 30, 2025, 6:36 a.m.)
Issued	15 years, 8 months ago (Jan. 1, 2010)
Published	15 years, 8 months ago (Jan. 1, 2010)
Published Online	15 years, 2 months ago (June 22, 2010)
Published Print	15 years, 8 months ago (Jan. 1, 2010)

Funders 0

None

BibTeX

@article{Wilczy_ski_2010, title={Dynamic CRM occupancy reflects a temporal map of developmental progression}, volume={6}, ISSN={1744-4292}, url={http://dx.doi.org/10.1038/msb.2010.35}, DOI={10.1038/msb.2010.35}, number={1}, journal={Molecular Systems Biology}, publisher={Springer Science and Business Media LLC}, author={Wilczyński, Bartek and Furlong, Eileen E M}, year={2010}, month=jan }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        30
      ]
    ],
    "date-time": "2025-07-30T10:36:34Z",
    "timestamp": 1753871794534,
    "version": "3.41.2"
  },
  "reference-count": 55,
  "publisher": "Springer Science and Business Media LLC",
  "issue": "1",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2010,
            6,
            22
          ]
        ],
        "date-time": "2010-06-22T00:00:00Z",
        "timestamp": 1277164800000
      },
      "content-version": "vor",
      "delay-in-days": 172,
      "URL": "http://creativecommons.org/licenses/by-nc-sa/3.0/"
    }
  ],
  "content-domain": {
    "domain": [
      "www.embopress.org"
    ],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2010,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Development is driven by tightly coordinated spatio\u2010temporal patterns of gene expression, which are initiated through the action of transcription factors (TFs) binding to <jats:italic>cis</jats:italic>\u2010regulatory modules (CRMs). Although many studies have investigated how spatial patterns arise, precise temporal control of gene expression is less well understood. Here, we show that dynamic changes in the timing of CRM occupancy is a prevalent feature common to all TFs examined in a developmental ChIP time course to date. CRMs exhibit complex binding patterns that cannot be explained by the sequence motifs or expression of the TFs themselves. The temporal changes in TF binding are highly correlated with dynamic patterns of target gene expression, which in turn reflect transitions in cellular function during different stages of development. Thus, it is not only the timing of a TF's expression, but also its temporal occupancy in refined time windows, which determines temporal gene expression. Systematic measurement of dynamic CRM occupancy may therefore serve as a powerful method to decode dynamic changes in gene expression driving developmental progression.</jats:p>",
  "DOI": "10.1038/msb.2010.35",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2010,
        6,
        23
      ]
    ],
    "date-time": "2010-06-23T10:54:12Z",
    "timestamp": 1277290452000
  },
  "update-policy": "https://doi.org/10.1002/crossmark_policy",
  "source": "Crossref",
  "is-referenced-by-count": 39,
  "title": "Dynamic CRM occupancy reflects a temporal map of developmental progression",
  "prefix": "10.1038",
  "volume": "6",
  "author": [
    {
      "given": "Bartek",
      "family": "Wilczy\u0144ski",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Genome Biology, European Molecular Biology Laboratory (EMBL)  Heidelberg Germany"
        }
      ]
    },
    {
      "given": "Eileen E M",
      "family": "Furlong",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Genome Biology, European Molecular Biology Laboratory (EMBL)  Heidelberg Germany"
        }
      ]
    }
  ],
  "member": "297",
  "published-online": {
    "date-parts": [
      [
        2010,
        6,
        22
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_6_2_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/75556"
    },
    {
      "key": "e_1_2_6_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.7.7b.1325"
    },
    {
      "key": "e_1_2_6_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/19.2.185"
    },
    {
      "key": "e_1_2_6_5_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.9.6.730"
    },
    {
      "key": "e_1_2_6_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1097-2765(00)80305-6"
    },
    {
      "key": "e_1_2_6_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1999.9298"
    },
    {
      "key": "e_1_2_6_8_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng1917"
    },
    {
      "key": "e_1_2_6_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.cell.2008.04.043"
    },
    {
      "key": "e_1_2_6_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/btp163"
    },
    {
      "key": "e_1_2_6_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/msb4100067"
    },
    {
      "key": "e_1_2_6_12_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/bth078"
    },
    {
      "key": "e_1_2_6_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.pcbi.0030007"
    },
    {
      "key": "e_1_2_6_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1242/dev.128.22.4489"
    },
    {
      "key": "e_1_2_6_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2105-5-31"
    },
    {
      "key": "e_1_2_6_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1065175"
    },
    {
      "key": "e_1_2_6_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.pbio.0020352"
    },
    {
      "key": "e_1_2_6_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.pgen.0030216"
    },
    {
      "key": "e_1_2_6_19_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/btm440"
    },
    {
      "key": "e_1_2_6_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)00105-7"
    },
    {
      "key": "e_1_2_6_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature02800"
    },
    {
      "key": "e_1_2_6_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/15.7.563"
    },
    {
      "key": "e_1_2_6_23_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.6.8.1518"
    },
    {
      "key": "e_1_2_6_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.437607"
    },
    {
      "key": "e_1_2_6_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/msb.2009.52"
    },
    {
      "key": "e_1_2_6_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/scisignal.2000140"
    },
    {
      "key": "e_1_2_6_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.477908"
    },
    {
      "key": "e_1_2_6_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1242/dev.01687"
    },
    {
      "key": "e_1_2_6_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1075090"
    },
    {
      "key": "e_1_2_6_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.9.1568"
    },
    {
      "key": "e_1_2_6_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.2000.9792"
    },
    {
      "key": "e_1_2_6_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/gb-2007-8-6-r101"
    },
    {
      "key": "e_1_2_6_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.pbio.0060027"
    },
    {
      "key": "e_1_2_6_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.91.12.5662"
    },
    {
      "key": "e_1_2_6_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.276.5317.1404"
    },
    {
      "key": "e_1_2_6_36_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.devcel.2009.01.006"
    },
    {
      "key": "e_1_2_6_37_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature02782"
    },
    {
      "key": "e_1_2_6_38_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/gb-2009-10-7-r80"
    },
    {
      "key": "e_1_2_6_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0808382106"
    },
    {
      "key": "e_1_2_6_40_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.91.16.7520"
    },
    {
      "key": "e_1_2_6_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1781909"
    },
    {
      "key": "e_1_2_6_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/btl565"
    },
    {
      "key": "e_1_2_6_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/gkh012"
    },
    {
      "key": "e_1_2_6_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1509007"
    },
    {
      "key": "e_1_2_6_45_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.devcel.2006.04.009"
    },
    {
      "key": "e_1_2_6_46_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gr.3715005"
    },
    {
      "key": "e_1_2_6_47_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng.375"
    },
    {
      "key": "e_1_2_6_48_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/15.8.3439"
    },
    {
      "key": "e_1_2_6_49_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/gb-2002-3-12-research0088"
    },
    {
      "key": "e_1_2_6_50_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/btp213"
    },
    {
      "key": "e_1_2_6_51_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1693008"
    },
    {
      "key": "e_1_2_6_52_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2105-7-505"
    },
    {
      "key": "e_1_2_6_53_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(94)90546-0"
    },
    {
      "key": "e_1_2_6_54_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.917101"
    },
    {
      "key": "e_1_2_6_55_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1509607"
    },
    {
      "key": "e_1_2_6_56_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature08531"
    }
  ],
  "container-title": "Molecular Systems Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1038%2Fmsb.2010.35",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1038/msb.2010.35",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/full-xml/10.1038/msb.2010.35",
      "content-type": "application/xml",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://www.embopress.org/doi/pdf/10.1038/msb.2010.35",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        12,
        18
      ]
    ],
    "date-time": "2023-12-18T20:52:26Z",
    "timestamp": 1702932746000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.embopress.org/doi/10.1038/msb.2010.35"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2010,
        1
      ]
    ]
  },
  "references-count": 55,
  "journal-issue": {
    "issue": "1",
    "published-print": {
      "date-parts": [
        [
          2010,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1038/msb.2010.35"
  ],
  "URL": "http://dx.doi.org/10.1038/msb.2010.35",
  "relation": {},
  "ISSN": [
    "1744-4292",
    "1744-4292"
  ],
  "subject": [],
  "container-title-short": "Molecular Systems Biology",
  "published": {
    "date-parts": [
      [
        2010,
        1
      ]
    ]
  },
  "assertion": [
    {
      "value": "2009-12-18",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2010-04-30",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2010-06-22",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ],
  "article-number": "383"
}