DNA double-strand breaks activate a multi-functional genetic program in developing lymphocytes
DNA double-strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiological processes. The cellular response to genotoxic DNA breaks includes the activation of transcriptional programs known primarily to regulate cell-cycle checkpoints...
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| Published in | Nature (London) Vol. 456; no. 7223; pp. 819 - 823 |
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| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
11.12.2008
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | DNA double-strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiological processes. The cellular response to genotoxic DNA breaks includes the activation of transcriptional programs known primarily to regulate cell-cycle checkpoints and cell survival. DNA double-strand breaks are generated in all developing lymphocytes during the assembly of antigen receptor genes, a process that is essential for normal lymphocyte development. Here we show that in murine lymphocytes these physiological DNA breaks activate a broad transcriptional program. This program transcends the canonical DNA double-strand break response and includes many genes that regulate diverse cellular processes important for lymphocyte development. Moreover, the expression of several of these genes is regulated similarly in response to genotoxic DNA damage. Thus, physiological DNA double-strand breaks provide cues that can regulate cell-type-specific processes not directly involved in maintaining the integrity of the genome, and genotoxic DNA breaks could disrupt normal cellular functions by corrupting these processes. |
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| AbstractList | DNA double-strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiological processes. The cellular response to genotoxic DNA breaks includes the activation of transcriptional programs known primarily to regulate cell-cycle checkpoints and cell survival. DNA double-strand breaks are generated in all developing lymphocytes during the assembly of antigen receptor genes, a process that is essential for normal lymphocyte development. Here we show that in murine lymphocytes these physiological DNA breaks activate a broad transcriptional program. This program transcends the canonical DNA double-strand break response and includes many genes that regulate diverse cellular processes important for lymphocyte development. Moreover, the expression of several of these genes is regulated similarly in response to genotoxic DNA damage. Thus, physiological DNA double-strand breaks provide cues that can regulate cell-type-specific processes not directly involved in maintaining the integrity of the genome, and genotoxic DNA breaks could disrupt normal cellular functions by corrupting these processes. DNA double strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiologic processes. The cellular response to genotoxic DNA breaks includes the activation of transcriptional programs known primarily to regulate cell cycle checkpoints and cell survival 1 – 5 . DNA double strand breaks are generated in all developing lymphocytes during the assembly of antigen receptor genes, a process that is essential for normal lymphocyte development. Here we demonstrate that these physiologic DNA breaks activate a broad transcriptional program. This program transcends the canonical DNA double strand break response and includes many genes that regulate diverse cellular processes important for lymphocyte development. Moreover, the expression of several of these genes is regulated similarly in response to genotoxic DNA damage. Thus, physiologic DNA double strand breaks provide cues that can regulate cell-type-specific processes not directly involved in maintaining the integrity of the genome, and genotoxic DNA breaks could disrupt normal cellular functions by corrupting these processes. DNA breaks: there for a purpose As part of the response to exogenous DNA damage, the transcription of certain genes involved in cell cycle checkpoints and survival is affected; these changes help the cell to maintain its genomic integrity. There are also situations in which endogenous, physiological DNA double-strand breaks occur. In this work, Bredemeyer et al . show that the breaks which initiate the rearrangement of antigen receptor genes also activate a transcriptional program — but with a difference. Many of the regulated genes are involved in lymphocyte development. Thus, DNA breaks can regulate cell-type-specific processes and not just functions that will allow the cell to repair and survive a DNA break. As part of the response to exogenous DNA damage, the transcription of certain genes involved in cell cycle checkpoints and survival is affected; these changes help the cell to maintain its genomic integrity. There are also situations in which endogenous, physiological DNA double-strand breaks occur. This paper shows that the breaks which initiate the rearrangement of antigen receptor genes also activate a transcriptional program, but with a difference. Many of the regulated genes are involved in lymphocyte development. DNA double-strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiological processes. The cellular response to genotoxic DNA breaks includes the activation of transcriptional programs known primarily to regulate cell-cycle checkpoints and cell survival 1 , 2 , 3 , 4 , 5 . DNA double-strand breaks are generated in all developing lymphocytes during the assembly of antigen receptor genes, a process that is essential for normal lymphocyte development. Here we show that in murine lymphocytes these physiological DNA breaks activate a broad transcriptional program. This program transcends the canonical DNA double-strand break response and includes many genes that regulate diverse cellular processes important for lymphocyte development. Moreover, the expression of several of these genes is regulated similarly in response to genotoxic DNA damage. Thus, physiological DNA double-strand breaks provide cues that can regulate cell-type-specific processes not directly involved in maintaining the integrity of the genome, and genotoxic DNA breaks could disrupt normal cellular functions by corrupting these processes. DNA double-strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiological processes. The cellular response to genotoxic DNA breaks includes the activation of transcriptional programs known primarily to regulate cell-cycle checkpoints and cell survival. DNA double-strand breaks are generated in all developing lymphocytes during the assembly of antigen receptor genes, a process that is essential for normal lymphocyte development. Here we show that in murine lymphocytes these physiological DNA breaks activate a broad transcriptional program. This program transcends the canonical DNA double-strand break response and includes many genes that regulate diverse cellular processes important for lymphocyte development. Moreover, the expression of several of these genes is regulated similarly in response to genotoxic DNA damage. Thus, physiological DNA double-strand breaks provide cues that can regulate cell-type-specific processes not directly involved in maintaining the integrity of the genome, and genotoxic DNA breaks could disrupt normal cellular functions by corrupting these processes. [PUBLICATION ABSTRACT] |
| Audience | Academic |
| Author | Mandik-Nayak, Laura Paules, Richard S Helmink, Beth A Bassing, Craig H Sleckman, Barry P Weaver, Brian K Collins, Jennifer B Innes, Cynthia L Mahowald, Grace K Walker, Laura M Allen, Paul M McGinnis, Lisa M Schreiber, Robert D Bredemeyer, Andrea L Calderon, Boris Gapud, Eric J May, Michael J |
| AuthorAffiliation | 2 Environmental Stress and Cancer Group, and NIEHS Microarray Group, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 1 Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110 5 Abramson Family Cancer Research Institute, Philadelphia, PA 19104 4 Department of Pathology and Laboratory Medicine, Center for Childhood Cancer Research, Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine 3 School of Veterinary Medicine, Center for Childhood Cancer Research, Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine |
| AuthorAffiliation_xml | – name: 1 Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110 – name: 2 Environmental Stress and Cancer Group, and NIEHS Microarray Group, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina – name: 3 School of Veterinary Medicine, Center for Childhood Cancer Research, Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine – name: 4 Department of Pathology and Laboratory Medicine, Center for Childhood Cancer Research, Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine – name: 5 Abramson Family Cancer Research Institute, Philadelphia, PA 19104 |
| Author_xml | – sequence: 1 givenname: Barry P surname: Sleckman fullname: Sleckman, Barry P organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 2 givenname: Andrea L surname: Bredemeyer fullname: Bredemeyer, Andrea L organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 3 givenname: Beth A surname: Helmink fullname: Helmink, Beth A organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 4 givenname: Cynthia L surname: Innes fullname: Innes, Cynthia L organization: Environmental Stress and Cancer Group, and NIEHS Microarray Group, National Institute of Environmental Health Sciences – sequence: 5 givenname: Boris surname: Calderon fullname: Calderon, Boris organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 6 givenname: Lisa M surname: McGinnis fullname: McGinnis, Lisa M organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 7 givenname: Grace K surname: Mahowald fullname: Mahowald, Grace K organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 8 givenname: Eric J surname: Gapud fullname: Gapud, Eric J organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 9 givenname: Laura M surname: Walker fullname: Walker, Laura M organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 10 givenname: Jennifer B surname: Collins fullname: Collins, Jennifer B organization: Environmental Stress and Cancer Group, and NIEHS Microarray Group, National Institute of Environmental Health Sciences – sequence: 11 givenname: Brian K surname: Weaver fullname: Weaver, Brian K organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 12 givenname: Laura surname: Mandik-Nayak fullname: Mandik-Nayak, Laura organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 13 givenname: Robert D surname: Schreiber fullname: Schreiber, Robert D organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 14 givenname: Paul M surname: Allen fullname: Allen, Paul M organization: Department of Pathology and Immunology, Washington University School of Medicine – sequence: 15 givenname: Michael J surname: May fullname: May, Michael J – sequence: 16 givenname: Richard S surname: Paules fullname: Paules, Richard S organization: Environmental Stress and Cancer Group, and NIEHS Microarray Group, National Institute of Environmental Health Sciences – sequence: 17 givenname: Craig H surname: Bassing fullname: Bassing, Craig H organization: Abramson Family Cancer Research Institute |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=20896627$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/18849970$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Macmillan Publishers Limited. All rights reserved 2008 2009 INIST-CNRS COPYRIGHT 2008 Nature Publishing Group Copyright Nature Publishing Group Dec 11, 2008 |
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| Keywords | Double strand break Regulation(control) Cell differentiation Lymphocyte DNA |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The microarray gene expression data has been deposited in NCBI's Gene Expression Omnibus accessible through GEO Series accession number GSE9024 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE9024). These authors contributed equally Author Information |
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| Snippet | DNA double-strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiological processes. The... DNA breaks: there for a purpose As part of the response to exogenous DNA damage, the transcription of certain genes involved in cell cycle checkpoints and... DNA double strand breaks are generated by genotoxic agents and by cellular endonucleases as intermediates of several important physiologic processes. The... |
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| SubjectTerms | Animals Apoptosis Ataxia Telangiectasia Mutated Proteins B-Lymphocytes - drug effects B-Lymphocytes - metabolism Biological and medical sciences Bone marrow Cell cycle Cell Cycle Proteins - drug effects Cell Line Deoxyribonucleic acid DNA DNA Breaks, Double-Stranded DNA damage DNA-Binding Proteins - drug effects Enzyme Inhibitors - pharmacology Fundamental and applied biological sciences. Psychology Fundamental immunology Gene expression Gene Expression Profiling Gene Expression Regulation, Developmental - drug effects Gene Expression Regulation, Developmental - genetics Genetic aspects Genetics Homeodomain Proteins - metabolism Humanities and Social Sciences Immunobiology Kinases letter Lymphocytes Lymphoid cells: ontogeny, maturation, markers, receptors, circulation and recirculation Mice Mice, Knockout Mice, SCID multidisciplinary NF-kappa B - metabolism Physiological aspects Physiology Protein-Serine-Threonine Kinases - drug effects Proteins Science Science (multidisciplinary) Tumor Suppressor Proteins - drug effects |
| Title | DNA double-strand breaks activate a multi-functional genetic program in developing lymphocytes |
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