Extracellular Adenosine Triphosphate Affects the Response of Human Macrophages Infected With Mycobacterium tuberculosis
Granulomas are the hallmark of Mycobacterium tuberculosis infection. As the host fails to control the bacteria, the center of the granuloma exhibits necrosis resulting from the dying of infected macrophages. The release of the intracellular pool of nucleotides into the surrounding medium may modulat...
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| Veröffentlicht in: | The Journal of infectious diseases 2014-09, Vol.210 (5), p.824-833 |
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| creator | Dubois-Colas, Nicolas Petit-Jentreau, Laetitia Barreiro, Luis B. Durand, Sylvère Soubigou, Guillaume Lecointe, Cécile Klibi, Jihène Rezaï, Keyvan Lokiec, François Coppée, Jean-Yves Gicquel, Brigitte Tailleux, Ludovic |
| description | Granulomas are the hallmark of Mycobacterium tuberculosis infection. As the host fails to control the bacteria, the center of the granuloma exhibits necrosis resulting from the dying of infected macrophages. The release of the intracellular pool of nucleotides into the surrounding medium may modulate the response of newly infected macrophages, although this has never been investigated. Here, we show that extracellular adenosine triphosphate (ATP) indirectly modulates the expression of 272 genes in human macrophages infected with M. tuberculosis and that it induces their alternative activation. ATP is rapidly hydrolyzed by the ecto-ATPase CD39 into adenosine monophosphate (AMP), and it is AMP that regulates the macrophage response through the adenosine A2A receptor. Our findings reveal a previously unrecognized role for the purinergic pathway in the host response to M. tuberculosis. Dampening inflammation through signaling via the adenosine A2A receptor may limit tissue damage but may also favor bacterial immune escape. |
| doi_str_mv | 10.1093/infdis/jiu135 |
| format | Article |
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As the host fails to control the bacteria, the center of the granuloma exhibits necrosis resulting from the dying of infected macrophages. The release of the intracellular pool of nucleotides into the surrounding medium may modulate the response of newly infected macrophages, although this has never been investigated. Here, we show that extracellular adenosine triphosphate (ATP) indirectly modulates the expression of 272 genes in human macrophages infected with M. tuberculosis and that it induces their alternative activation. ATP is rapidly hydrolyzed by the ecto-ATPase CD39 into adenosine monophosphate (AMP), and it is AMP that regulates the macrophage response through the adenosine A2A receptor. Our findings reveal a previously unrecognized role for the purinergic pathway in the host response to M. tuberculosis. Dampening inflammation through signaling via the adenosine A2A receptor may limit tissue damage but may also favor bacterial immune escape.</description><identifier>ISSN: 0022-1899</identifier><identifier>EISSN: 1537-6613</identifier><identifier>DOI: 10.1093/infdis/jiu135</identifier><identifier>PMID: 24604822</identifier><identifier>CODEN: JIDIAQ</identifier><language>eng</language><publisher>Oxford: Oxford University Press</publisher><subject>Adenosine Monophosphate ; Adenosine Monophosphate - metabolism ; Adenosine Triphosphate ; Adenosine Triphosphate - metabolism ; Bacteria ; Bacteriology ; Biological and medical sciences ; Cytokines ; Fundamental and applied biological sciences. Psychology ; Fungal infections ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation ; Gene Expression Regulation - drug effects ; Host-Pathogen Interactions ; Human health and pathology ; Humans ; Immunology ; Infections ; Infectious diseases ; Innate immunity ; Life Sciences ; Macrophages ; Macrophages - drug effects ; Macrophages - immunology ; Macrophages - metabolism ; Macrophages - microbiology ; Medical sciences ; Microbiology ; Microbiology and Parasitology ; Miscellaneous ; Mycobacterium tuberculosis ; Mycobacterium tuberculosis - immunology ; PATHOGENESIS AND HOST RESPONSE ; Receptors ; Receptors, Purinergic P1 ; Receptors, Purinergic P1 - metabolism ; Secretion ; Signal Transduction ; T lymphocytes ; Tuberculosis</subject><ispartof>The Journal of infectious diseases, 2014-09, Vol.210 (5), p.824-833</ispartof><rights>Copyright © 2014 Oxford University Press on behalf of the Infectious Diseases Society of America</rights><rights>2015 INIST-CNRS</rights><rights>The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. 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As the host fails to control the bacteria, the center of the granuloma exhibits necrosis resulting from the dying of infected macrophages. The release of the intracellular pool of nucleotides into the surrounding medium may modulate the response of newly infected macrophages, although this has never been investigated. Here, we show that extracellular adenosine triphosphate (ATP) indirectly modulates the expression of 272 genes in human macrophages infected with M. tuberculosis and that it induces their alternative activation. ATP is rapidly hydrolyzed by the ecto-ATPase CD39 into adenosine monophosphate (AMP), and it is AMP that regulates the macrophage response through the adenosine A2A receptor. Our findings reveal a previously unrecognized role for the purinergic pathway in the host response to M. tuberculosis. Dampening inflammation through signaling via the adenosine A2A receptor may limit tissue damage but may also favor bacterial immune escape.</description><subject>Adenosine Monophosphate</subject><subject>Adenosine Monophosphate - metabolism</subject><subject>Adenosine Triphosphate</subject><subject>Adenosine Triphosphate - metabolism</subject><subject>Bacteria</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>Cytokines</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Fungal infections</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Host-Pathogen Interactions</subject><subject>Human health and pathology</subject><subject>Humans</subject><subject>Immunology</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Innate immunity</subject><subject>Life Sciences</subject><subject>Macrophages</subject><subject>Macrophages - drug effects</subject><subject>Macrophages - immunology</subject><subject>Macrophages - metabolism</subject><subject>Macrophages - microbiology</subject><subject>Medical sciences</subject><subject>Microbiology</subject><subject>Microbiology and Parasitology</subject><subject>Miscellaneous</subject><subject>Mycobacterium tuberculosis</subject><subject>Mycobacterium tuberculosis - immunology</subject><subject>PATHOGENESIS AND HOST RESPONSE</subject><subject>Receptors</subject><subject>Receptors, Purinergic P1</subject><subject>Receptors, Purinergic P1 - metabolism</subject><subject>Secretion</subject><subject>Signal Transduction</subject><subject>T lymphocytes</subject><subject>Tuberculosis</subject><issn>0022-1899</issn><issn>1537-6613</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpF0c1rFDEYBvAgil2rR49KLkIvY_M9meNSarewRZCKxyEz88bJMl_mo9r_3iyzrqcQ8ssT8j4IvafkMyUVv3aT7Vy4PrhEuXyBNlTyslCK8pdoQwhjBdVVdYHehHAghAiuytfogglFhGZsg37f_onetDAMaTAebzuY5uAmwI_eLf0clt5EwFtroY0Bxx7wNwjLPAXAs8W7NJoJP5jWzxn-hIDvp6OEDv9wsccPz-3cmLz3Lo04pgZ8m4b8QHiLXlkzBHh3Wi_R9y-3jze7Yv_17v5muy9awVgsyqqtSg20A6I7wYnpKIWqEcwSaWVDdNUppaSFhijCDFjNtdCVaksgeTySX6Jize3NUC_ejcY_17Nx9W67rxcTIiRfEy6ZzPN4otlfrX7x868EIdajC8fxmAnmFGoqJedUlaz8H51_H4IHe86npD52U6_d1Gs32X88RadmhO6s_5WRwacTMKE1g_VmavP1s9OlEJTy7D6s7hDi7M_ngpdEU835X_UvpCk</recordid><startdate>20140901</startdate><enddate>20140901</enddate><creator>Dubois-Colas, Nicolas</creator><creator>Petit-Jentreau, Laetitia</creator><creator>Barreiro, Luis B.</creator><creator>Durand, Sylvère</creator><creator>Soubigou, Guillaume</creator><creator>Lecointe, Cécile</creator><creator>Klibi, Jihène</creator><creator>Rezaï, Keyvan</creator><creator>Lokiec, François</creator><creator>Coppée, Jean-Yves</creator><creator>Gicquel, Brigitte</creator><creator>Tailleux, Ludovic</creator><general>Oxford University Press</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-6356-1006</orcidid></search><sort><creationdate>20140901</creationdate><title>Extracellular Adenosine Triphosphate Affects the Response of Human Macrophages Infected With Mycobacterium tuberculosis</title><author>Dubois-Colas, Nicolas ; Petit-Jentreau, Laetitia ; Barreiro, Luis B. ; Durand, Sylvère ; Soubigou, Guillaume ; Lecointe, Cécile ; Klibi, Jihène ; Rezaï, Keyvan ; Lokiec, François ; Coppée, Jean-Yves ; Gicquel, Brigitte ; Tailleux, Ludovic</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c422t-79c978e1de08d430ad11e9b42f05f5b089d6665feb0602aef8384896c7e010953</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Adenosine Monophosphate</topic><topic>Adenosine Monophosphate - metabolism</topic><topic>Adenosine Triphosphate</topic><topic>Adenosine Triphosphate - metabolism</topic><topic>Bacteria</topic><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>Cytokines</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Fungal infections</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation</topic><topic>Gene Expression Regulation - drug effects</topic><topic>Host-Pathogen Interactions</topic><topic>Human health and pathology</topic><topic>Humans</topic><topic>Immunology</topic><topic>Infections</topic><topic>Infectious diseases</topic><topic>Innate immunity</topic><topic>Life Sciences</topic><topic>Macrophages</topic><topic>Macrophages - drug effects</topic><topic>Macrophages - immunology</topic><topic>Macrophages - metabolism</topic><topic>Macrophages - microbiology</topic><topic>Medical sciences</topic><topic>Microbiology</topic><topic>Microbiology and Parasitology</topic><topic>Miscellaneous</topic><topic>Mycobacterium tuberculosis</topic><topic>Mycobacterium tuberculosis - immunology</topic><topic>PATHOGENESIS AND HOST RESPONSE</topic><topic>Receptors</topic><topic>Receptors, Purinergic P1</topic><topic>Receptors, Purinergic P1 - metabolism</topic><topic>Secretion</topic><topic>Signal Transduction</topic><topic>T lymphocytes</topic><topic>Tuberculosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dubois-Colas, Nicolas</creatorcontrib><creatorcontrib>Petit-Jentreau, Laetitia</creatorcontrib><creatorcontrib>Barreiro, Luis B.</creatorcontrib><creatorcontrib>Durand, Sylvère</creatorcontrib><creatorcontrib>Soubigou, Guillaume</creatorcontrib><creatorcontrib>Lecointe, Cécile</creatorcontrib><creatorcontrib>Klibi, Jihène</creatorcontrib><creatorcontrib>Rezaï, Keyvan</creatorcontrib><creatorcontrib>Lokiec, François</creatorcontrib><creatorcontrib>Coppée, Jean-Yves</creatorcontrib><creatorcontrib>Gicquel, Brigitte</creatorcontrib><creatorcontrib>Tailleux, Ludovic</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>The Journal of infectious diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dubois-Colas, Nicolas</au><au>Petit-Jentreau, Laetitia</au><au>Barreiro, Luis B.</au><au>Durand, Sylvère</au><au>Soubigou, Guillaume</au><au>Lecointe, Cécile</au><au>Klibi, Jihène</au><au>Rezaï, Keyvan</au><au>Lokiec, François</au><au>Coppée, Jean-Yves</au><au>Gicquel, Brigitte</au><au>Tailleux, Ludovic</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Extracellular Adenosine Triphosphate Affects the Response of Human Macrophages Infected With Mycobacterium tuberculosis</atitle><jtitle>The Journal of infectious diseases</jtitle><addtitle>J Infect Dis</addtitle><date>2014-09-01</date><risdate>2014</risdate><volume>210</volume><issue>5</issue><spage>824</spage><epage>833</epage><pages>824-833</pages><issn>0022-1899</issn><eissn>1537-6613</eissn><coden>JIDIAQ</coden><abstract>Granulomas are the hallmark of Mycobacterium tuberculosis infection. As the host fails to control the bacteria, the center of the granuloma exhibits necrosis resulting from the dying of infected macrophages. The release of the intracellular pool of nucleotides into the surrounding medium may modulate the response of newly infected macrophages, although this has never been investigated. Here, we show that extracellular adenosine triphosphate (ATP) indirectly modulates the expression of 272 genes in human macrophages infected with M. tuberculosis and that it induces their alternative activation. ATP is rapidly hydrolyzed by the ecto-ATPase CD39 into adenosine monophosphate (AMP), and it is AMP that regulates the macrophage response through the adenosine A2A receptor. Our findings reveal a previously unrecognized role for the purinergic pathway in the host response to M. tuberculosis. Dampening inflammation through signaling via the adenosine A2A receptor may limit tissue damage but may also favor bacterial immune escape.</abstract><cop>Oxford</cop><pub>Oxford University Press</pub><pmid>24604822</pmid><doi>10.1093/infdis/jiu135</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-6356-1006</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The Journal of infectious diseases, 2014-09, Vol.210 (5), p.824-833 |
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| source | MEDLINE; Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); Alma/SFX Local Collection |
| subjects | Adenosine Monophosphate Adenosine Monophosphate - metabolism Adenosine Triphosphate Adenosine Triphosphate - metabolism Bacteria Bacteriology Biological and medical sciences Cytokines Fundamental and applied biological sciences. Psychology Fungal infections Gene expression Gene Expression Profiling Gene Expression Regulation Gene Expression Regulation - drug effects Host-Pathogen Interactions Human health and pathology Humans Immunology Infections Infectious diseases Innate immunity Life Sciences Macrophages Macrophages - drug effects Macrophages - immunology Macrophages - metabolism Macrophages - microbiology Medical sciences Microbiology Microbiology and Parasitology Miscellaneous Mycobacterium tuberculosis Mycobacterium tuberculosis - immunology PATHOGENESIS AND HOST RESPONSE Receptors Receptors, Purinergic P1 Receptors, Purinergic P1 - metabolism Secretion Signal Transduction T lymphocytes Tuberculosis |
| title | Extracellular Adenosine Triphosphate Affects the Response of Human Macrophages Infected With Mycobacterium tuberculosis |
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