Frailty in old age is associated with decreased interleukin-12/23 production in response to toll-like receptor ligation
Aging is associated with progressive alterations of immune functions, leading to higher susceptibility to bacterial and viral infections and reduced vaccine responses. Data concerning cytokine production in response to Toll-like receptor (TLR) ligands are highly variable in old people, reflecting th...
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| Veröffentlicht in: | PloS one 2013-06, Vol.8 (6), p.e65325-e65325 |
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| creator | Compté, Nathalie Zouaoui Boudjeltia, Karim Vanhaeverbeek, Michel De Breucker, Sandra Tassignon, Joel Trelcat, Anne Pepersack, Thierry Goriely, Stanislas |
| description | Aging is associated with progressive alterations of immune functions, leading to higher susceptibility to bacterial and viral infections and reduced vaccine responses. Data concerning cytokine production in response to Toll-like receptor (TLR) ligands are highly variable in old people, reflecting the heterogeneity of the geriatric population. The aim of our study was to define the relative contribution of age and clinical status on TLR-induced interleukin (IL)-12p70 and IL-23 production as these cytokines play an important role in the protection against intracellular and extracellular pathogens, respectively. For this purpose, we recruited 100 subjects (aged 23-96 years) in the general population or hospitalized for chronic diseases. We collected information on clinical status (medical history, ongoing comorbidities, treatments and geriatric scales), biological parameters (biochemical and hematological tests, telomere length determination, cytomegalovirus serology). Whole blood samples were stimulated with a combination of TLR4 and TLR7/8 ligands. We performed univariate and stepwise backward multivariate analyses regression to define which set of clinical variables could be predictive for IL-12p70 and IL-23 production in these conditions. Our results indicated that age was not correlated with TLR-mediated IL-12p70 and IL-23 production. In contrast, poor nutritional status and frailty in subjects >75 years were associated with decreased IL-12p70 and IL-23 production. By intracytoplasmic staining, we confirmed that production of IL-12/23p40 by conventional dendritic cells (DCs) upon TLR ligation was decreased in frail patients. However, proportion of DCs and monocytes subsets, phenotypic maturation and proximal signaling events were found to be comparable in frail and healthy old subjects. These results suggest the importance of age-associated clinical parameters and not age by itself in the alteration of innate immune responses in old individuals and emphasis the importance of innate immune responses in the susceptibility of frail geriatric patients to infections. |
| doi_str_mv | 10.1371/journal.pone.0065325 |
| format | Article |
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Data concerning cytokine production in response to Toll-like receptor (TLR) ligands are highly variable in old people, reflecting the heterogeneity of the geriatric population. The aim of our study was to define the relative contribution of age and clinical status on TLR-induced interleukin (IL)-12p70 and IL-23 production as these cytokines play an important role in the protection against intracellular and extracellular pathogens, respectively. For this purpose, we recruited 100 subjects (aged 23-96 years) in the general population or hospitalized for chronic diseases. We collected information on clinical status (medical history, ongoing comorbidities, treatments and geriatric scales), biological parameters (biochemical and hematological tests, telomere length determination, cytomegalovirus serology). Whole blood samples were stimulated with a combination of TLR4 and TLR7/8 ligands. We performed univariate and stepwise backward multivariate analyses regression to define which set of clinical variables could be predictive for IL-12p70 and IL-23 production in these conditions. Our results indicated that age was not correlated with TLR-mediated IL-12p70 and IL-23 production. In contrast, poor nutritional status and frailty in subjects >75 years were associated with decreased IL-12p70 and IL-23 production. By intracytoplasmic staining, we confirmed that production of IL-12/23p40 by conventional dendritic cells (DCs) upon TLR ligation was decreased in frail patients. However, proportion of DCs and monocytes subsets, phenotypic maturation and proximal signaling events were found to be comparable in frail and healthy old subjects. These results suggest the importance of age-associated clinical parameters and not age by itself in the alteration of innate immune responses in old individuals and emphasis the importance of innate immune responses in the susceptibility of frail geriatric patients to infections.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0065325</identifier><identifier>PMID: 23755218</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Activities of daily living ; Adult ; Age ; Aged ; Aged, 80 and over ; Aging ; Analysis ; Bacteria ; Blood & organ donations ; Cells, Cultured ; Chronic diseases ; Chronic illnesses ; Comorbidity ; Cytokines ; Cytomegalovirus ; Dendritic cells ; Dendritic Cells - immunology ; Dendritic Cells - metabolism ; Disease susceptibility ; Family medical history ; Female ; Frail Elderly ; Frailty ; Geriatrics ; Health aspects ; Health care ; Hematology ; Heterogeneity ; Hospitals ; Humans ; Imidazoles - pharmacology ; Immune response ; Immune system ; Immunity, Innate ; Immunology ; Infections ; Influenza ; Innate immunity ; Intercellular Adhesion Molecule-1 - metabolism ; Interleukin 12 ; Interleukin 23 ; Interleukin-12 - biosynthesis ; Interleukin-23 - biosynthesis ; Interleukins ; Laboratories ; Ligands ; Lipopolysaccharides - pharmacology ; Male ; Medicine ; Middle Aged ; Monocytes ; Nosocomial infections ; Nutritional status ; Nutritional Status - immunology ; Older people ; Patients ; Production management ; Proteins ; Recruitment ; Regression analysis ; Rodents ; Serology ; Signal Transduction ; Signaling ; Telomeres ; TLR4 protein ; TLR7 protein ; Toll-like receptors ; Toll-Like Receptors - agonists ; Toll-Like Receptors - metabolism ; Type 2 diabetes ; Vaccines ; Viral infections ; Womens health ; Young Adult</subject><ispartof>PloS one, 2013-06, Vol.8 (6), p.e65325-e65325</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Compté et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Compté et al 2013 Compté et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-5682d1e5d20e3e1e335abb8e6b3677a8ea89a7deb0167852b063e3e51448bd053</citedby><cites>FETCH-LOGICAL-c692t-5682d1e5d20e3e1e335abb8e6b3677a8ea89a7deb0167852b063e3e51448bd053</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3673922/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3673922/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23755218$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Fitzgerald-Bocarsly, Patricia</contributor><creatorcontrib>Compté, Nathalie</creatorcontrib><creatorcontrib>Zouaoui Boudjeltia, Karim</creatorcontrib><creatorcontrib>Vanhaeverbeek, Michel</creatorcontrib><creatorcontrib>De Breucker, Sandra</creatorcontrib><creatorcontrib>Tassignon, Joel</creatorcontrib><creatorcontrib>Trelcat, Anne</creatorcontrib><creatorcontrib>Pepersack, Thierry</creatorcontrib><creatorcontrib>Goriely, Stanislas</creatorcontrib><title>Frailty in old age is associated with decreased interleukin-12/23 production in response to toll-like receptor ligation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Aging is associated with progressive alterations of immune functions, leading to higher susceptibility to bacterial and viral infections and reduced vaccine responses. Data concerning cytokine production in response to Toll-like receptor (TLR) ligands are highly variable in old people, reflecting the heterogeneity of the geriatric population. The aim of our study was to define the relative contribution of age and clinical status on TLR-induced interleukin (IL)-12p70 and IL-23 production as these cytokines play an important role in the protection against intracellular and extracellular pathogens, respectively. For this purpose, we recruited 100 subjects (aged 23-96 years) in the general population or hospitalized for chronic diseases. We collected information on clinical status (medical history, ongoing comorbidities, treatments and geriatric scales), biological parameters (biochemical and hematological tests, telomere length determination, cytomegalovirus serology). Whole blood samples were stimulated with a combination of TLR4 and TLR7/8 ligands. We performed univariate and stepwise backward multivariate analyses regression to define which set of clinical variables could be predictive for IL-12p70 and IL-23 production in these conditions. Our results indicated that age was not correlated with TLR-mediated IL-12p70 and IL-23 production. In contrast, poor nutritional status and frailty in subjects >75 years were associated with decreased IL-12p70 and IL-23 production. By intracytoplasmic staining, we confirmed that production of IL-12/23p40 by conventional dendritic cells (DCs) upon TLR ligation was decreased in frail patients. However, proportion of DCs and monocytes subsets, phenotypic maturation and proximal signaling events were found to be comparable in frail and healthy old subjects. 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pharmacology</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity, Innate</subject><subject>Immunology</subject><subject>Infections</subject><subject>Influenza</subject><subject>Innate immunity</subject><subject>Intercellular Adhesion Molecule-1 - metabolism</subject><subject>Interleukin 12</subject><subject>Interleukin 23</subject><subject>Interleukin-12 - biosynthesis</subject><subject>Interleukin-23 - biosynthesis</subject><subject>Interleukins</subject><subject>Laboratories</subject><subject>Ligands</subject><subject>Lipopolysaccharides - pharmacology</subject><subject>Male</subject><subject>Medicine</subject><subject>Middle Aged</subject><subject>Monocytes</subject><subject>Nosocomial infections</subject><subject>Nutritional status</subject><subject>Nutritional Status - immunology</subject><subject>Older people</subject><subject>Patients</subject><subject>Production management</subject><subject>Proteins</subject><subject>Recruitment</subject><subject>Regression analysis</subject><subject>Rodents</subject><subject>Serology</subject><subject>Signal Transduction</subject><subject>Signaling</subject><subject>Telomeres</subject><subject>TLR4 protein</subject><subject>TLR7 protein</subject><subject>Toll-like receptors</subject><subject>Toll-Like Receptors - agonists</subject><subject>Toll-Like Receptors - metabolism</subject><subject>Type 2 diabetes</subject><subject>Vaccines</subject><subject>Viral infections</subject><subject>Womens health</subject><subject>Young Adult</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11r2zAUhs3YWLtu_2BshsHYLpzqw5KVm0Ep6xYoFPZ1K2TpxFGrWKkkr-u_n9ykJR69GDZYPnrOK51XOkXxGqMZpg0-vvRD6JWbbXwPM4Q4o4Q9KQ7xnJKKE0Sf7o0PihcxXiLEqOD8eXFAaMMYweKwuDkLyrp0W9q-9M6UqoPSxlLF6LVVCUx5Y9OqNKADqJh_bZ8gOBiubF9hckxouQneDDpZ348iAWLeUYQy-fw6Vzl7BTmqYZN8KJ3t1Ii-LJ4tlYvwavc9Kn6eff5x-rU6v_iyOD05rzSfk1QxLojBwAxBQAEDpUy1rQDeUt40SoASc9UYaBHmjWCkRZxmkOG6Fq3J9R4Vb7e6G-ej3HkWJaacYSEQ5ZlYbAnj1aXcBLtW4VZ6ZeVdwIdOqpCsdiBbqnF2eklVTesWs1Y3oBvNNDZGaFBZ69NutaFdg9HQp6DcRHQ609uV7Pxvmauhc0KywIedQPDXA8Qk1zZqcE714Ie7fWdHKOI4o-_-QR-vbkd1Khdg-6XP6-pRVJ7UjahxQ-omU7NHqPwYWFudL9jS5vgk4eMkITMJ_qRODTHKxfdv_89e_Jqy7_fYFSiXVtG7YbwycQrWW1AHH2OA5YPJGMmxP-7dkGN_yF1_5LQ3-wf0kHTfEPQvgTALgg</recordid><startdate>20130605</startdate><enddate>20130605</enddate><creator>Compté, Nathalie</creator><creator>Zouaoui Boudjeltia, Karim</creator><creator>Vanhaeverbeek, Michel</creator><creator>De Breucker, Sandra</creator><creator>Tassignon, Joel</creator><creator>Trelcat, Anne</creator><creator>Pepersack, Thierry</creator><creator>Goriely, Stanislas</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130605</creationdate><title>Frailty in old age is associated with decreased interleukin-12/23 production in response to toll-like receptor ligation</title><author>Compté, Nathalie ; Zouaoui Boudjeltia, Karim ; Vanhaeverbeek, Michel ; De Breucker, Sandra ; Tassignon, Joel ; Trelcat, Anne ; Pepersack, Thierry ; Goriely, Stanislas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-5682d1e5d20e3e1e335abb8e6b3677a8ea89a7deb0167852b063e3e51448bd053</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Activities of daily living</topic><topic>Adult</topic><topic>Age</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Aging</topic><topic>Analysis</topic><topic>Bacteria</topic><topic>Blood & organ donations</topic><topic>Cells, Cultured</topic><topic>Chronic diseases</topic><topic>Chronic illnesses</topic><topic>Comorbidity</topic><topic>Cytokines</topic><topic>Cytomegalovirus</topic><topic>Dendritic cells</topic><topic>Dendritic Cells - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Compté, Nathalie</au><au>Zouaoui Boudjeltia, Karim</au><au>Vanhaeverbeek, Michel</au><au>De Breucker, Sandra</au><au>Tassignon, Joel</au><au>Trelcat, Anne</au><au>Pepersack, Thierry</au><au>Goriely, Stanislas</au><au>Fitzgerald-Bocarsly, Patricia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Frailty in old age is associated with decreased interleukin-12/23 production in response to toll-like receptor ligation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-06-05</date><risdate>2013</risdate><volume>8</volume><issue>6</issue><spage>e65325</spage><epage>e65325</epage><pages>e65325-e65325</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Aging is associated with progressive alterations of immune functions, leading to higher susceptibility to bacterial and viral infections and reduced vaccine responses. Data concerning cytokine production in response to Toll-like receptor (TLR) ligands are highly variable in old people, reflecting the heterogeneity of the geriatric population. The aim of our study was to define the relative contribution of age and clinical status on TLR-induced interleukin (IL)-12p70 and IL-23 production as these cytokines play an important role in the protection against intracellular and extracellular pathogens, respectively. For this purpose, we recruited 100 subjects (aged 23-96 years) in the general population or hospitalized for chronic diseases. We collected information on clinical status (medical history, ongoing comorbidities, treatments and geriatric scales), biological parameters (biochemical and hematological tests, telomere length determination, cytomegalovirus serology). Whole blood samples were stimulated with a combination of TLR4 and TLR7/8 ligands. We performed univariate and stepwise backward multivariate analyses regression to define which set of clinical variables could be predictive for IL-12p70 and IL-23 production in these conditions. Our results indicated that age was not correlated with TLR-mediated IL-12p70 and IL-23 production. In contrast, poor nutritional status and frailty in subjects >75 years were associated with decreased IL-12p70 and IL-23 production. By intracytoplasmic staining, we confirmed that production of IL-12/23p40 by conventional dendritic cells (DCs) upon TLR ligation was decreased in frail patients. However, proportion of DCs and monocytes subsets, phenotypic maturation and proximal signaling events were found to be comparable in frail and healthy old subjects. These results suggest the importance of age-associated clinical parameters and not age by itself in the alteration of innate immune responses in old individuals and emphasis the importance of innate immune responses in the susceptibility of frail geriatric patients to infections.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23755218</pmid><doi>10.1371/journal.pone.0065325</doi><tpages>e65325</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-06, Vol.8 (6), p.e65325-e65325 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1365188036 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Activities of daily living Adult Age Aged Aged, 80 and over Aging Analysis Bacteria Blood & organ donations Cells, Cultured Chronic diseases Chronic illnesses Comorbidity Cytokines Cytomegalovirus Dendritic cells Dendritic Cells - immunology Dendritic Cells - metabolism Disease susceptibility Family medical history Female Frail Elderly Frailty Geriatrics Health aspects Health care Hematology Heterogeneity Hospitals Humans Imidazoles - pharmacology Immune response Immune system Immunity, Innate Immunology Infections Influenza Innate immunity Intercellular Adhesion Molecule-1 - metabolism Interleukin 12 Interleukin 23 Interleukin-12 - biosynthesis Interleukin-23 - biosynthesis Interleukins Laboratories Ligands Lipopolysaccharides - pharmacology Male Medicine Middle Aged Monocytes Nosocomial infections Nutritional status Nutritional Status - immunology Older people Patients Production management Proteins Recruitment Regression analysis Rodents Serology Signal Transduction Signaling Telomeres TLR4 protein TLR7 protein Toll-like receptors Toll-Like Receptors - agonists Toll-Like Receptors - metabolism Type 2 diabetes Vaccines Viral infections Womens health Young Adult |
| title | Frailty in old age is associated with decreased interleukin-12/23 production in response to toll-like receptor ligation |
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