Systematic integration of GATA transcription factors and epigenomes via IDEAS paints the regulatory landscape of hematopoietic cells

Ross C. Hardison, Yu Zhang, Cheryl A. Keller, Guanjue Xiang, Elisabeth F. Heuston, Lin An, Jens Lichtenberg, Belinda M. Giardine, David Bodine, Shaun Mahony, Qunhua Li, Feng Yue, Mitchell J. Weiss, Gerd A. Blobel, James Taylor, Jim Hughes, Douglas R. Higgs, Berthold Göttgens

Research output: Contribution to journalReview article

Abstract

Members of the GATA family of transcription factors play key roles in the differentiation of specific cell lineages by regulating the expression of target genes. Three GATA factors play distinct roles in hematopoietic differentiation. In order to better understand how these GATA factors function to regulate genes throughout the genome, we are studying the epigenomic and transcriptional landscapes of hematopoietic cells in a model-driven, integrative fashion. We have formed the collaborative multi-lab VISION project to conduct ValIdated Systematic IntegratiON of epigenomic data in mouse and human hematopoiesis. The epigenomic data included nuclease accessibility in chromatin, CTCF occupancy, and histone H3 modifications for 20 cell types covering hematopoietic stem cells, multilineage progenitor cells, and mature cells across the blood cell lineages of mouse. The analysis used the Integrative and Discriminative Epigenome Annotation System (IDEAS), which learns all common combinations of features (epigenetic states) simultaneously in two dimensions—along chromosomes and across cell types. The result is a segmentation that effectively paints the regulatory landscape in readily interpretable views, revealing constitutively active or silent loci as well as the loci specifically induced or repressed in each stage and lineage. Nuclease accessible DNA segments in active chromatin states were designated candidate cis-regulatory elements in each cell type, providing one of the most comprehensive registries of candidate hematopoietic regulatory elements to date. Applications of VISION resources are illustrated for the regulation of genes encoding GATA1, GATA2, GATA3, and Ikaros. VISION resources are freely available from our website http://usevision.org.

Original languageEnglish (US)
Pages (from-to)27-38
Number of pages12
JournalIUBMB Life
Volume72
Issue number1
DOIs
StatePublished - Jan 1 2020

Fingerprint

GATA Transcription Factors
Paint
Epigenomics
Genes
Chromatin
Cells
Cell Lineage
Gene encoding
Deoxyribonucleases
Chromosomes
Stem cells
Histone Code
Histones
Websites
Blood
Transcription Factors
Hematopoiesis
Hematopoietic Stem Cells
Registries
Blood Cells

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Genetics
  • Clinical Biochemistry
  • Cell Biology

Cite this

Hardison, Ross C. ; Zhang, Yu ; Keller, Cheryl A. ; Xiang, Guanjue ; Heuston, Elisabeth F. ; An, Lin ; Lichtenberg, Jens ; Giardine, Belinda M. ; Bodine, David ; Mahony, Shaun ; Li, Qunhua ; Yue, Feng ; Weiss, Mitchell J. ; Blobel, Gerd A. ; Taylor, James ; Hughes, Jim ; Higgs, Douglas R. ; Göttgens, Berthold. / Systematic integration of GATA transcription factors and epigenomes via IDEAS paints the regulatory landscape of hematopoietic cells. In: IUBMB Life. 2020 ; Vol. 72, No. 1. pp. 27-38.
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abstract = "Members of the GATA family of transcription factors play key roles in the differentiation of specific cell lineages by regulating the expression of target genes. Three GATA factors play distinct roles in hematopoietic differentiation. In order to better understand how these GATA factors function to regulate genes throughout the genome, we are studying the epigenomic and transcriptional landscapes of hematopoietic cells in a model-driven, integrative fashion. We have formed the collaborative multi-lab VISION project to conduct ValIdated Systematic IntegratiON of epigenomic data in mouse and human hematopoiesis. The epigenomic data included nuclease accessibility in chromatin, CTCF occupancy, and histone H3 modifications for 20 cell types covering hematopoietic stem cells, multilineage progenitor cells, and mature cells across the blood cell lineages of mouse. The analysis used the Integrative and Discriminative Epigenome Annotation System (IDEAS), which learns all common combinations of features (epigenetic states) simultaneously in two dimensions—along chromosomes and across cell types. The result is a segmentation that effectively paints the regulatory landscape in readily interpretable views, revealing constitutively active or silent loci as well as the loci specifically induced or repressed in each stage and lineage. Nuclease accessible DNA segments in active chromatin states were designated candidate cis-regulatory elements in each cell type, providing one of the most comprehensive registries of candidate hematopoietic regulatory elements to date. Applications of VISION resources are illustrated for the regulation of genes encoding GATA1, GATA2, GATA3, and Ikaros. VISION resources are freely available from our website http://usevision.org.",
author = "Hardison, {Ross C.} and Yu Zhang and Keller, {Cheryl A.} and Guanjue Xiang and Heuston, {Elisabeth F.} and Lin An and Jens Lichtenberg and Giardine, {Belinda M.} and David Bodine and Shaun Mahony and Qunhua Li and Feng Yue and Weiss, {Mitchell J.} and Blobel, {Gerd A.} and James Taylor and Jim Hughes and Higgs, {Douglas R.} and Berthold G{\"o}ttgens",
year = "2020",
month = "1",
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Hardison, RC, Zhang, Y, Keller, CA, Xiang, G, Heuston, EF, An, L, Lichtenberg, J, Giardine, BM, Bodine, D, Mahony, S, Li, Q, Yue, F, Weiss, MJ, Blobel, GA, Taylor, J, Hughes, J, Higgs, DR & Göttgens, B 2020, 'Systematic integration of GATA transcription factors and epigenomes via IDEAS paints the regulatory landscape of hematopoietic cells', IUBMB Life, vol. 72, no. 1, pp. 27-38. https://doi.org/10.1002/iub.2195

Systematic integration of GATA transcription factors and epigenomes via IDEAS paints the regulatory landscape of hematopoietic cells. / Hardison, Ross C.; Zhang, Yu; Keller, Cheryl A.; Xiang, Guanjue; Heuston, Elisabeth F.; An, Lin; Lichtenberg, Jens; Giardine, Belinda M.; Bodine, David; Mahony, Shaun; Li, Qunhua; Yue, Feng; Weiss, Mitchell J.; Blobel, Gerd A.; Taylor, James; Hughes, Jim; Higgs, Douglas R.; Göttgens, Berthold.

In: IUBMB Life, Vol. 72, No. 1, 01.01.2020, p. 27-38.

Research output: Contribution to journalReview article

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T1 - Systematic integration of GATA transcription factors and epigenomes via IDEAS paints the regulatory landscape of hematopoietic cells

AU - Hardison, Ross C.

AU - Zhang, Yu

AU - Keller, Cheryl A.

AU - Xiang, Guanjue

AU - Heuston, Elisabeth F.

AU - An, Lin

AU - Lichtenberg, Jens

AU - Giardine, Belinda M.

AU - Bodine, David

AU - Mahony, Shaun

AU - Li, Qunhua

AU - Yue, Feng

AU - Weiss, Mitchell J.

AU - Blobel, Gerd A.

AU - Taylor, James

AU - Hughes, Jim

AU - Higgs, Douglas R.

AU - Göttgens, Berthold

PY - 2020/1/1

Y1 - 2020/1/1

N2 - Members of the GATA family of transcription factors play key roles in the differentiation of specific cell lineages by regulating the expression of target genes. Three GATA factors play distinct roles in hematopoietic differentiation. In order to better understand how these GATA factors function to regulate genes throughout the genome, we are studying the epigenomic and transcriptional landscapes of hematopoietic cells in a model-driven, integrative fashion. We have formed the collaborative multi-lab VISION project to conduct ValIdated Systematic IntegratiON of epigenomic data in mouse and human hematopoiesis. The epigenomic data included nuclease accessibility in chromatin, CTCF occupancy, and histone H3 modifications for 20 cell types covering hematopoietic stem cells, multilineage progenitor cells, and mature cells across the blood cell lineages of mouse. The analysis used the Integrative and Discriminative Epigenome Annotation System (IDEAS), which learns all common combinations of features (epigenetic states) simultaneously in two dimensions—along chromosomes and across cell types. The result is a segmentation that effectively paints the regulatory landscape in readily interpretable views, revealing constitutively active or silent loci as well as the loci specifically induced or repressed in each stage and lineage. Nuclease accessible DNA segments in active chromatin states were designated candidate cis-regulatory elements in each cell type, providing one of the most comprehensive registries of candidate hematopoietic regulatory elements to date. Applications of VISION resources are illustrated for the regulation of genes encoding GATA1, GATA2, GATA3, and Ikaros. VISION resources are freely available from our website http://usevision.org.

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