Mycobacterium tuberculosis Infection Induces HDAC1-Mediated Suppression of IL-12B Gene Expression in Macrophages

Downregulation of host gene expression is one of the many strategies employed by intracellular pathogens such as Mycobacterium tuberculosis (MTB) to survive inside the macrophages and cause disease. The underlying molecular mechanism behind the downregulation of host defense gene expression is large...

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Published inFrontiers in cellular and infection microbiology Vol. 5; p. 90
Main Authors Chandran, Aneesh, Antony, Cecil, Jose, Leny, Mundayoor, Sathish, Natarajan, Krishnamurthy, Kumar, R Ajay
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 02.12.2015
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Abstract Downregulation of host gene expression is one of the many strategies employed by intracellular pathogens such as Mycobacterium tuberculosis (MTB) to survive inside the macrophages and cause disease. The underlying molecular mechanism behind the downregulation of host defense gene expression is largely unknown. In this study we explored the role of histone deacetylation in macrophages in response to infection by virulent MTB H37Rv in manipulating host gene expression. We show a significant increase in the levels of HDAC1 with a concomitant and marked reduction in the levels of histone H3-acetylation in macrophages containing live, but not killed, virulent MTB. Additionally, we show that HDAC1 is recruited to the promoter of IL-12B in macrophages infected with live, virulent MTB, and the subsequent hypoacetylation of histone H3 suppresses the expression of this gene which plays a key role in initiating Th1 responses. By inhibiting immunologically relevant kinases, and by knockdown of crucial transcriptional regulators, we demonstrate that protein kinase-A (PKA), CREB, and c-Jun play an important role in regulating HDAC1 level in live MTB-infected macrophages. By chromatin immunoprecipitation (ChIP) analysis, we prove that HDAC1 expression is positively regulated by the recruitment of c-Jun to its promoter. Knockdown of HDAC1 in macrophages significantly reduced the survival of intracellular MTB. These observations indicate a novel HDAC1-mediated epigenetic modification induced by live, virulent MTB to subvert the immune system to survive and replicate in the host.
AbstractList Downregulation of host gene expression is one of the many strategies employed by intracellular pathogens such as Mycobacterium tuberculosis (MTB) to survive inside the macrophages and cause disease. The underlying molecular mechanism behind the downregulation of host defense gene expression is largely unknown. In this study we explored the role of histone deacetylation in macrophages in response to infection by virulent MTB H37Rv in manipulating host gene expression. We show a significant increase in the levels of HDAC1 with a concomitant and marked reduction in the levels of histone H3-acetylation in macrophages containing live, but not killed, virulent MTB. Additionally, we show that HDAC1 is recruited to the promoter of IL-12B in macrophages infected with live, virulent MTB, and the subsequent hypoacetylation of histone H3 suppresses the expression of this gene which plays a key role in initiating Th1 responses. By inhibiting immunologically relevant kinases, and by knockdown of crucial transcriptional regulators, we demonstrate that protein kinase-A (PKA), CREB, and c-Jun play an important role in regulating HDAC1 level in live MTB-infected macrophages. By chromatin immunoprecipitation (ChIP) analysis, we prove that HDAC1 expression is positively regulated by the recruitment of c-Jun to its promoter. Knockdown of HDAC1 in macrophages significantly reduced the survival of intracellular MTB. These observations indicate a novel HDAC1-mediated epigenetic modification induced by live, virulent MTB to subvert the immune system to survive and replicate in the host.
Downregulation of host gene expression is one of the many strategies employed by intracellular pathogens such as Mycobacterium tuberculosis (MTB) to survive inside the macrophages and cause disease. The underlying molecular mechanism behind the downregulation of host defense gene expression is largely unknown. In this study we explored the role of histone deacetylation in macrophages in response to infection by virulent MTB H37Rv in manipulating host gene expression. We show a significant increase in the levels of HDAC1 with a concomitant and marked reduction in the levels of histone H3-acetylation in macrophages containing live, but not killed, virulent MTB. Additionally, we show that HDAC1 is recruited to the promoter of IL-12B in macrophages infected with live, virulent MTB, and the subsequent hypoacetylation of histone H3 suppresses the expression of this gene which plays a key role in initiating Th1 responses. By inhibiting immunologically relevant kinases, and by knockdown of crucial transcriptional regulators, we demonstrate that protein kinase-A, CREB and c-Jun play an important role in regulating HDAC1 level in live MTB-infected macrophages. By chromatin immunoprecipitation analysis, we prove that HDAC1 expression is positively regulated by the recruitment of c-Jun to its promoter. Knockdown of HDAC1 in macrophages significantly reduced the survival of intracellular MTB. These observations indicate a novel HDAC1-mediated epigenetic modification induced by live, virulent MTB to subvert the immune system to survive and replicate in the host.
Downregulation of host gene expression is one of the many strategies employed by intracellular pathogens such as Mycobacterium tuberculosis (MTB) to survive inside the macrophages and cause disease. The underlying molecular mechanism behind the downregulation of host defense gene expression is largely unknown. In this study we explored the role of histone deacetylation in macrophages in response to infection by virulent MTB H37Rv in manipulating host gene expression. We show a significant increase in the levels of HDAC1 with a concomitant and marked reduction in the levels of histone H3-acetylation in macrophages containing live, but not killed, virulent MTB. Additionally, we show that HDAC1 is recruited to the promoter of IL-12B in macrophages infected with live, virulent MTB, and the subsequent hypoacetylation of histone H3 suppresses the expression of this gene which plays a key role in initiating Th1 responses. By inhibiting immunologically relevant kinases, and by knockdown of crucial transcriptional regulators, we demonstrate that protein kinase-A (PKA), CREB, and c-Jun play an important role in regulating HDAC1 level in live MTB-infected macrophages. By chromatin immunoprecipitation (ChIP) analysis, we prove that HDAC1 expression is positively regulated by the recruitment of c-Jun to its promoter. Knockdown of HDAC1 in macrophages significantly reduced the survival of intracellular MTB. These observations indicate a novel HDAC1-mediated epigenetic modification induced by live, virulent MTB to subvert the immune system to survive and replicate in the host.
Author Jose, Leny
Antony, Cecil
Chandran, Aneesh
Kumar, R Ajay
Mundayoor, Sathish
Natarajan, Krishnamurthy
AuthorAffiliation 2 Infectious Diseases Laboratory, Dr. B. R. Ambedkar Centre for Biomedical Research, University of Delhi Delhi, India
1 Mycobacterium Research Group, Tropical Disease Biology, Rajiv Gandhi Centre for Biotechnology Thiruvananthapuram, India
AuthorAffiliation_xml – name: 1 Mycobacterium Research Group, Tropical Disease Biology, Rajiv Gandhi Centre for Biotechnology Thiruvananthapuram, India
– name: 2 Infectious Diseases Laboratory, Dr. B. R. Ambedkar Centre for Biomedical Research, University of Delhi Delhi, India
Author_xml – sequence: 1
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  surname: Chandran
  fullname: Chandran, Aneesh
  organization: Mycobacterium Research Group, Tropical Disease Biology, Rajiv Gandhi Centre for Biotechnology Thiruvananthapuram, India
– sequence: 2
  givenname: Cecil
  surname: Antony
  fullname: Antony, Cecil
  organization: Infectious Diseases Laboratory, Dr. B. R. Ambedkar Centre for Biomedical Research, University of Delhi Delhi, India
– sequence: 3
  givenname: Leny
  surname: Jose
  fullname: Jose, Leny
  organization: Mycobacterium Research Group, Tropical Disease Biology, Rajiv Gandhi Centre for Biotechnology Thiruvananthapuram, India
– sequence: 4
  givenname: Sathish
  surname: Mundayoor
  fullname: Mundayoor, Sathish
  organization: Mycobacterium Research Group, Tropical Disease Biology, Rajiv Gandhi Centre for Biotechnology Thiruvananthapuram, India
– sequence: 5
  givenname: Krishnamurthy
  surname: Natarajan
  fullname: Natarajan, Krishnamurthy
  organization: Infectious Diseases Laboratory, Dr. B. R. Ambedkar Centre for Biomedical Research, University of Delhi Delhi, India
– sequence: 6
  givenname: R Ajay
  surname: Kumar
  fullname: Kumar, R Ajay
  organization: Mycobacterium Research Group, Tropical Disease Biology, Rajiv Gandhi Centre for Biotechnology Thiruvananthapuram, India
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Keywords c-jun
epigenetic modifications
CREB
THP-1 macrophages
host-pathogen
interleukin-12
Language English
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Reviewed by: Jyothi Rengarajan, Emory University School of Medicine, USA; Janice Endsley, University of Texas Medical Branch, USA; Buka Samten, University of Texas Health Science Center at Tyler, USA
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SSID ssj0000702893
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Snippet Downregulation of host gene expression is one of the many strategies employed by intracellular pathogens such as Mycobacterium tuberculosis (MTB) to survive...
Downregulation of host gene expression is one of the many strategies employed by intracellular pathogens such as Mycobacterium tuberculosis (MTB) to survive...
SourceID doaj
pubmedcentral
proquest
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage 90
SubjectTerms c-jun
CREB
Down-Regulation
Epigenesis, Genetic
epigenetic modifications
Histone Deacetylase 1 - metabolism
host-pathogen
Host-Pathogen Interactions
Interleukin-12
Interleukin-12 - biosynthesis
Macrophages - immunology
Macrophages - microbiology
Microbial Viability
Microbiology
Mycobacterium tuberculosis - immunology
THP-1 macrophages
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Title Mycobacterium tuberculosis Infection Induces HDAC1-Mediated Suppression of IL-12B Gene Expression in Macrophages
URI https://www.ncbi.nlm.nih.gov/pubmed/26697414
https://search.proquest.com/docview/1751673524
https://pubmed.ncbi.nlm.nih.gov/PMC4667035
https://doaj.org/article/44068d09779a44d9886b7e648d762f23
Volume 5
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