The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry

The molecular control of germinal center selection is still being determined. Dalla-Favera and colleagues show that the cell-cycle regulator c-Myc is essential for B cell selection and reentry into the germinal center. After antigenic challenge, B cells enter the dark zone (DZ) of germinal centers (...

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Published in	Nature immunology Vol. 13; no. 11; pp. 1083 - 1091
Main Authors	Dominguez-Sola, David, Victora, Gabriel D, Ying, Carol Y, Phan, Ryan T, Saito, Masumichi, Nussenzweig, Michel C, Dalla-Favera, Riccardo
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.11.2012 Nature Publishing Group
Subjects	631/250/2152/2153/1982 631/250/580 631/67/395 692/699/67/1990/291 Analysis Animals Antigens, CD - genetics Antigens, CD - immunology B cells B-Lymphocytes - immunology B-Lymphocytes - metabolism B-Lymphocytes - pathology Biomedicine Cell Cycle - genetics Cell Cycle - immunology Cell Movement Cell Proliferation Cell Transformation, Neoplastic - genetics Cell Transformation, Neoplastic - immunology Gene Expression Regulation Genes, myc - immunology Genes, Reporter Germinal Center - immunology Germinal Center - metabolism Germinal Center - pathology Green Fluorescent Proteins Immunology Infectious Diseases Lymphoma - genetics Lymphoma - metabolism Lymphoma - pathology Mice Mice, Transgenic Physiological aspects Proto-Oncogene Proteins c-bcl-6 - genetics Proto-Oncogene Proteins c-bcl-6 - immunology Proto-oncogenes Receptors, Antigen, B-Cell - genetics Receptors, Antigen, B-Cell - immunology Signal Transduction T-Lymphocytes - immunology T-Lymphocytes - metabolism T-Lymphocytes - pathology
Online Access	Get full text
ISSN	1529-2908 1529-2916 1529-2916
DOI	10.1038/ni.2428

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Abstract	The molecular control of germinal center selection is still being determined. Dalla-Favera and colleagues show that the cell-cycle regulator c-Myc is essential for B cell selection and reentry into the germinal center. After antigenic challenge, B cells enter the dark zone (DZ) of germinal centers (GCs) to proliferate and hypermutate their immunoglobulin genes. Mutants with greater affinity for the antigen are positively selected in the light zone (LZ) to either differentiate into plasma and memory cells or reenter the DZ. The molecular circuits that govern positive selection in the GC are not known. We show here that the GC reaction required biphasic regulation of expression of the cell-cycle regulator c-Myc that involved its transient induction during early GC commitment, its repression by Bcl-6 in DZ B cells and its reinduction in B cells selected for reentry into the DZ. Inhibition of c-Myc in vivo led to GC collapse, which indicated an essential role for c-Myc in GCs. Our results have implications for the mechanism of GC selection and the role of c-Myc in lymphomagenesis.
AbstractList	After antigenic challenge, B cells enter the dark zone (DZ) of germinal centers (GCs) to proliferate and hypermutate their immunoglobulin genes. Mutants with greater affinity for the antigen are positively selected in the light zone (LZ) to either differentiate into plasma and memory cells or reenter the DZ. The molecular circuits that govern positive selection in the GC are not known. We show here that the GC reaction required biphasic regulation of expression of the cell-cycle regulator c-Myc that involved its transient induction during early GC commitment, its repression by Bcl-6 in DZ B cells and its reinduction in B cells selected for reentry into the DZ. Inhibition of c-Myc in vivo led to GC collapse, which indicated an essential role for c-Myc in GCs. Our results have implications for the mechanism of GC selection and the role of c-Myc in lymphomagenesis. After antigenic challenge, B cells enter the dark zone (DZ) of germinal centers (GCs) to proliferate and hypermutate their immunoglobulin genes. Mutants with greater affinity for the antigen are positively selected in the light zone (LZ) to either differentiate into plasma and memory cells or reenter the DZ. The molecular circuits that govern positive selection in the GC are not known. We show here that the GC reaction required biphasic regulation of expression of the cell-cycle regulator c-Myc that involved its transient induction during early GC commitment, its repression by Bcl-6 in DZ B cells and its reinduction in B cells selected for reentry into the DZ. Inhibition of c-Myc in vivo led to GC collapse, which indicated an essential role for c-Myc in GCs. Our results have implications for the mechanism of GC selection and the role of c-Myc in lymphomagenesis.After antigenic challenge, B cells enter the dark zone (DZ) of germinal centers (GCs) to proliferate and hypermutate their immunoglobulin genes. Mutants with greater affinity for the antigen are positively selected in the light zone (LZ) to either differentiate into plasma and memory cells or reenter the DZ. The molecular circuits that govern positive selection in the GC are not known. We show here that the GC reaction required biphasic regulation of expression of the cell-cycle regulator c-Myc that involved its transient induction during early GC commitment, its repression by Bcl-6 in DZ B cells and its reinduction in B cells selected for reentry into the DZ. Inhibition of c-Myc in vivo led to GC collapse, which indicated an essential role for c-Myc in GCs. Our results have implications for the mechanism of GC selection and the role of c-Myc in lymphomagenesis. The molecular control of germinal center selection is still being determined. Dalla-Favera and colleagues show that the cell-cycle regulator c-Myc is essential for B cell selection and reentry into the germinal center. After antigenic challenge, B cells enter the dark zone (DZ) of germinal centers (GCs) to proliferate and hypermutate their immunoglobulin genes. Mutants with greater affinity for the antigen are positively selected in the light zone (LZ) to either differentiate into plasma and memory cells or reenter the DZ. The molecular circuits that govern positive selection in the GC are not known. We show here that the GC reaction required biphasic regulation of expression of the cell-cycle regulator c-Myc that involved its transient induction during early GC commitment, its repression by Bcl-6 in DZ B cells and its reinduction in B cells selected for reentry into the DZ. Inhibition of c-Myc in vivo led to GC collapse, which indicated an essential role for c-Myc in GCs. Our results have implications for the mechanism of GC selection and the role of c-Myc in lymphomagenesis.
Audience	Academic
Author	Nussenzweig, Michel C Phan, Ryan T Dominguez-Sola, David Ying, Carol Y Saito, Masumichi Victora, Gabriel D Dalla-Favera, Riccardo
Author_xml	– sequence: 1 givenname: David surname: Dominguez-Sola fullname: Dominguez-Sola, David organization: Institute for Cancer Genetics, Columbia University – sequence: 2 givenname: Gabriel D surname: Victora fullname: Victora, Gabriel D organization: Laboratory of Molecular Immunology, The Rockefeller University, Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts, USA (G.D.V.), Department of Medicine, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, California, USA (R.T.P.), and Department of Safety Research on Blood and Biological Products, National Institute of Infectious Diseases, Tokyo, Japan (M.S.) – sequence: 3 givenname: Carol Y surname: Ying fullname: Ying, Carol Y organization: Institute for Cancer Genetics, Columbia University – sequence: 4 givenname: Ryan T surname: Phan fullname: Phan, Ryan T organization: Institute for Cancer Genetics, Columbia University, Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts, USA (G.D.V.), Department of Medicine, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, California, USA (R.T.P.), and Department of Safety Research on Blood and Biological Products, National Institute of Infectious Diseases, Tokyo, Japan (M.S.) – sequence: 5 givenname: Masumichi surname: Saito fullname: Saito, Masumichi organization: Institute for Cancer Genetics, Columbia University, Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts, USA (G.D.V.), Department of Medicine, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, California, USA (R.T.P.), and Department of Safety Research on Blood and Biological Products, National Institute of Infectious Diseases, Tokyo, Japan (M.S.) – sequence: 6 givenname: Michel C surname: Nussenzweig fullname: Nussenzweig, Michel C email: nussen@mail.rockefeller.edu organization: Laboratory of Molecular Immunology, The Rockefeller University, Howard Hughes Medical Institute – sequence: 7 givenname: Riccardo surname: Dalla-Favera fullname: Dalla-Favera, Riccardo email: rd10@columbia.edu organization: Institute for Cancer Genetics, Columbia University, Herbert Irving Comprehensive Cancer Center, Columbia University, Department of Pathology and Cell Biology, Columbia University, Department of Genetics and Development, Columbia University, Department of Microbiology and Immunology, Columbia University
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/23001145$$D View this record in MEDLINE/PubMed
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Snippet	The molecular control of germinal center selection is still being determined. Dalla-Favera and colleagues show that the cell-cycle regulator c-Myc is essential... After antigenic challenge, B cells enter the dark zone (DZ) of germinal centers (GCs) to proliferate and hypermutate their immunoglobulin genes. Mutants with...
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SubjectTerms	631/250/2152/2153/1982 631/250/580 631/67/395 692/699/67/1990/291 Analysis Animals Antigens, CD - genetics Antigens, CD - immunology B cells B-Lymphocytes - immunology B-Lymphocytes - metabolism B-Lymphocytes - pathology Biomedicine Cell Cycle - genetics Cell Cycle - immunology Cell Movement Cell Proliferation Cell Transformation, Neoplastic - genetics Cell Transformation, Neoplastic - immunology Gene Expression Regulation Genes, myc - immunology Genes, Reporter Germinal Center - immunology Germinal Center - metabolism Germinal Center - pathology Green Fluorescent Proteins Immunology Infectious Diseases Lymphoma - genetics Lymphoma - metabolism Lymphoma - pathology Mice Mice, Transgenic Physiological aspects Proto-Oncogene Proteins c-bcl-6 - genetics Proto-Oncogene Proteins c-bcl-6 - immunology Proto-oncogenes Receptors, Antigen, B-Cell - genetics Receptors, Antigen, B-Cell - immunology Signal Transduction T-Lymphocytes - immunology T-Lymphocytes - metabolism T-Lymphocytes - pathology
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Title	The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry
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