Histone demethylase LSD1 is required for germinal center formation and BCL6-driven lymphomagenesis

Germinal center (GC) B cells feature repression of many gene enhancers to establish their characteristic transcriptome. Here we show that conditional deletion of Lsd1 in GCs significantly impaired GC formation, associated with failure to repress immune synapse genes linked to GC exit, which are also...

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Published inNature immunology Vol. 20; no. 1; pp. 86 - 96
Main Authors Hatzi, Katerina, Geng, Huimin, Doane, Ashley S., Meydan, Cem, LaRiviere, Reed, Cardenas, Mariano, Duy, Cihangir, Shen, Hao, Vidal, Maria Nieves Calvo, Baslan, Timour, Mohammad, Helai P., Kruger, Ryan G., Shaknovich, Rita, Haberman, Ann M., Inghirami, Giorgio, Lowe, Scott W., Melnick, Ari M.
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.01.2019
Nature Publishing Group
Subjects
631/250/1619/40
631/250/2152/2153/1982
631/250/2502/2170
631/67/1990/291
Animals
B cells
B-Lymphocytes - physiology
Bcl-6 protein
Biomedical and Life Sciences
Biomedicine
Carcinogenesis
Clonal deletion
CRISPR
CRISPR-Cas Systems
Dependence
Development and progression
DNA, Intergenic - genetics
Enhancers
Gene expression
Genes
Genetic aspects
Germinal Center - immunology
Germinal Center - pathology
Germinal centers
Histone Demethylases - genetics
Histone Demethylases - metabolism
Hyperplasia
Immune response
Immune response (humoral)
Immunological Synapses - genetics
Immunology
Infectious Diseases
Introns - genetics
Lymphocytes B
Lymphoma
Lymphoma - genetics
Lymphoma - metabolism
Lymphomas
Mice
Mice, Inbred C57BL
Mice, Knockout
Proto-Oncogene Proteins c-bcl-6 - genetics
Proto-Oncogene Proteins c-bcl-6 - metabolism
Transcription
Transcription (Genetics)
Transcription factors
Tumors
Online AccessGet full text

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Abstract Germinal center (GC) B cells feature repression of many gene enhancers to establish their characteristic transcriptome. Here we show that conditional deletion of Lsd1 in GCs significantly impaired GC formation, associated with failure to repress immune synapse genes linked to GC exit, which are also direct targets of the transcriptional repressor BCL6. We found that BCL6 directly binds LSD1 and recruits it primarily to intergenic and intronic enhancers. Conditional deletion of Lsd1 suppressed GC hyperplasia caused by constitutive expression of BCL6 and significantly delayed BCL6-driven lymphomagenesis. Administration of catalytic inhibitors of LSD1 had little effect on GC formation or GC-derived lymphoma cells. Using a CRISPR-Cas9 domain screen, we found instead that the LSD1 Tower domain was critical for dependence on LSD1 in GC-derived B cells. These results indicate an essential role for LSD1 in the humoral immune response, where it modulates enhancer function by forming repression complexes with BCL6. Germinal center B cells undergo reiterative rounds of proliferation and selection. Melnick and colleagues show that the histone demethylase LSD1 is necessary for this reiterative process via its interactions with the transcription factor BCL6.
AbstractList Germinal center (GC) B cells feature repression of many gene enhancers to establish their characteristic transcriptome. Here we show that conditional deletion of Lsd1 in GCs significantly impaired GC formation, associated with failure to repress immune synapse genes linked to GC exit, which are also direct targets of the transcriptional repressor BCL6. We found that BCL6 directly binds LSD1 and recruits it primarily to intergenic and intronic enhancers. Conditional deletion of Lsd1 suppressed GC hyperplasia caused by constitutive expression of BCL6 and significantly delayed BCL6-driven lymphomagenesis. Administration of catalytic inhibitors of LSD1 had little effect on GC formation or GC-derived lymphoma cells. Using a CRISPR-Cas9 domain screen, we found instead that the LSD1 Tower domain was critical for dependence on LSD1 in GC-derived B cells. These results indicate an essential role for LSD1 in the humoral immune response, where it modulates enhancer function by forming repression complexes with BCL6.
Germinal center (GC) B cells feature repression of many gene enhancers to establish their characteristic transcriptome. Here we show that conditional deletion of Lsd1 in GCs significantly impaired GC formation, associated with failure to repress immune synapse genes linked to GC exit, which are also direct targets of the transcriptional repressor BCL6. We found that BCL6 directly binds LSD1 and recruits it primarily to intergenic and intronic enhancers. Conditional deletion of Lsd1 suppressed GC hyperplasia caused by constitutive expression of BCL6 and significantly delayed BCL6-driven lymphomagenesis. Administration of catalytic inhibitors of LSD1 had little effect on GC formation or GC-derived lymphoma cells. Using a CRISPR-Cas9 domain screen, we found instead that the LSD1 Tower domain was critical for dependence on LSD1 in GC-derived B cells. These results indicate an essential role for LSD1 in the humoral immune response, where it modulates enhancer function by forming repression complexes with BCL6. Germinal center B cells undergo reiterative rounds of proliferation and selection. Melnick and colleagues show that the histone demethylase LSD1 is necessary for this reiterative process via its interactions with the transcription factor BCL6.
Germinal center (GC) B cells feature repression of many gene enhancers to establish their characteristic transcriptome. Here we show that conditional deletion of Lsd1 in GCs significantly impaired GC formation, associated with to failure to repress immune synapse genes linked to GC exit, which are also direct targets of the BCL6 transcriptional repressor. We found that BCL6 directly binds and recruits LSD1, primarily to intergenic and intronic enhancers. Conditional deletion of Lsd1 suppressed GC hyperplasia caused by constitutive expression of Bcl6, and significantly delayed Bcl6-driven lymphomagenesis. Administration of LSD1 catalytic inhibitors had little effect on GC formation or GC derived lymphoma cells. Using a CRISPR/Cas9 domain screen we found instead that the LSD1 Tower domain was critical for LSD1 dependency in GC derived B cells. These results indicate an essential role of LSD1 in the humoral immune response, where it modulates enhancer function by forming repression complexes with BCL6.
Germinal center (GC) B cells feature repression of many gene enhancers to establish their characteristic transcriptome. Here we show that conditional deletion of Lsd1 in GCs significantly impaired GC formation, associated with failure to repress immune synapse genes linked to GC exit, which are also direct targets of the transcriptional repressor BCL6. We found that BCL6 directly binds LSD1 and recruits it primarily to intergenic and intronic enhancers. Conditional deletion of Lsd1 suppressed GC hyperplasia caused by constitutive expression of BCL6 and significantly delayed BCL6-driven lymphomagenesis. Administration of catalytic inhibitors of LSD1 had little effect on GC formation or GC-derived lymphoma cells. Using a CRISPR-Cas9 domain screen, we found instead that the LSD1 Tower domain was critical for dependence on LSD1 in GC-derived B cells. These results indicate an essential role for LSD1 in the humoral immune response, where it modulates enhancer function by forming repression complexes with BCL6. Germinal center B cells undergo reiterative rounds of proliferation and selection. Melnick and colleagues show that the histone demethylase LSD1 is necessary for this reiterative process via its interactions with the transcription factor BCL6.
Audience Academic
Author Hatzi, Katerina
Vidal, Maria Nieves Calvo
Baslan, Timour
Mohammad, Helai P.
Inghirami, Giorgio
Shaknovich, Rita
Geng, Huimin
Lowe, Scott W.
Melnick, Ari M.
Shen, Hao
Kruger, Ryan G.
Haberman, Ann M.
Meydan, Cem
LaRiviere, Reed
Doane, Ashley S.
Cardenas, Mariano
Duy, Cihangir
AuthorAffiliation 2 Cancer Biology and Genetics Program, Sloan-Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York, USA
8 Howard Hughes Medical Institute, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
7 Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York, USA
9 Present address: High Throughput and Spectroscopy Resource Center, Rockefeller University, New York, New York, USA
1 Department of Medicine, Division of Hematology & Medical Oncology, Weill Cornell Medicine, New York, New York, USA
3 Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California, USA
4 Institute for Computational Biomedicine, Dept. of Physiology and Biophysics, Weill Cornell Medicine, New York, New York, USA
6 Department of Laboratory Medicine, Department of Immunobiology Yale University School of Medicine, New Haven, USA
5 Cancer Epigenetics Department, GlaxoSmithKline, Collegeville, PA 19426, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30538335$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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ISSN 1529-2908
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Issue 1
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Notes K.H. conceptualized the study, designed and performed the experiments, analyzed the data and wrote the manuscript. H.G, A.S.D and C.M performed bioinfomatic analyses. R.L., M.C, C.D, H.S., M.N.C.V, T.B and R.S. assisted in experiments. H.P.M. and R.G.K provided GSK-LSD1 inhibitor and technical advice regarding drug treatments. A.M.H edited the manuscript and provided technical advice with flow cytometry and IHC. G.I performed pathological evaluation of transplanted mice. S.W.L. cosupervised the study. A.M.M. conceptualized and supervised the study and wrote the manuscript.
Present address: Cancer Genetics Incorporated, Rutherford, New Jersey, USA
Author contributions
ORCID 0000-0002-8074-2287
OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC6294324
PMID 30538335
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  year: 2019
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  day: 01
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PublicationTitle Nature immunology
PublicationTitleAbbrev Nat Immunol
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PublicationYear 2019
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Snippet Germinal center (GC) B cells feature repression of many gene enhancers to establish their characteristic transcriptome. Here we show that conditional deletion...
SourceID pubmedcentral
proquest
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pubmed
springer
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StartPage 86
SubjectTerms 631/250/1619/40
631/250/2152/2153/1982
631/250/2502/2170
631/67/1990/291
Animals
B cells
B-Lymphocytes - physiology
Bcl-6 protein
Biomedical and Life Sciences
Biomedicine
Carcinogenesis
Clonal deletion
CRISPR
CRISPR-Cas Systems
Dependence
Development and progression
DNA, Intergenic - genetics
Enhancers
Gene expression
Genes
Genetic aspects
Germinal Center - immunology
Germinal Center - pathology
Germinal centers
Histone Demethylases - genetics
Histone Demethylases - metabolism
Hyperplasia
Immune response
Immune response (humoral)
Immunological Synapses - genetics
Immunology
Infectious Diseases
Introns - genetics
Lymphocytes B
Lymphoma
Lymphoma - genetics
Lymphoma - metabolism
Lymphomas
Mice
Mice, Inbred C57BL
Mice, Knockout
Proto-Oncogene Proteins c-bcl-6 - genetics
Proto-Oncogene Proteins c-bcl-6 - metabolism
Transcription
Transcription (Genetics)
Transcription factors
Tumors
Title Histone demethylase LSD1 is required for germinal center formation and BCL6-driven lymphomagenesis
URI https://link.springer.com/article/10.1038/s41590-018-0273-1
https://www.ncbi.nlm.nih.gov/pubmed/30538335
https://www.proquest.com/docview/2154627894
https://pubmed.ncbi.nlm.nih.gov/PMC6294324
Volume 20
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