Altered Basal Lipid Metabolism Underlies the Functional Impairment of Naive CD8 + T Cells in Elderly Humans
Aging is associated with functional deficits in the naive T cell compartment, which compromise the generation of de novo immune responses against previously unencountered Ags. The mechanisms that underlie this phenomenon have nonetheless remained unclear. We found that naive CD8 T cells in elderly h...
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| Veröffentlicht in: | The Journal of immunology (1950) 2022-02, Vol.208 (3), p.562-570 |
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| creator | Nicoli, Francesco Cabral-Piccin, Mariela P Papagno, Laura Gallerani, Eleonora Fusaro, Mathieu Folcher, Victor Dubois, Marion Clave, Emmanuel Vallet, Hélène Frere, Justin J Gostick, Emma Llewellyn-Lacey, Sian Price, David A Toubert, Antoine Dupré, Loïc Boddaert, Jacques Caputo, Antonella Gavioli, Riccardo Appay, Victor |
| description | Aging is associated with functional deficits in the naive T cell compartment, which compromise the generation of de novo immune responses against previously unencountered Ags. The mechanisms that underlie this phenomenon have nonetheless remained unclear. We found that naive CD8
T cells in elderly humans were prone to apoptosis and proliferated suboptimally in response to stimulation via the TCR. These abnormalities were associated with dysregulated lipid metabolism under homeostatic conditions and enhanced levels of basal activation. Importantly, reversal of the bioenergetic anomalies with lipid-altering drugs, such as rosiglitazone, almost completely restored the Ag responsiveness of naive CD8
T cells. Interventions that favor lipid catabolism may therefore find utility as adjunctive therapies in the elderly to promote vaccine-induced immunity against targetable cancers and emerging pathogens, such as seasonal influenza viruses and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). |
| doi_str_mv | 10.4049/jimmunol.2100194 |
| format | Article |
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T cells in elderly humans were prone to apoptosis and proliferated suboptimally in response to stimulation via the TCR. These abnormalities were associated with dysregulated lipid metabolism under homeostatic conditions and enhanced levels of basal activation. Importantly, reversal of the bioenergetic anomalies with lipid-altering drugs, such as rosiglitazone, almost completely restored the Ag responsiveness of naive CD8
T cells. Interventions that favor lipid catabolism may therefore find utility as adjunctive therapies in the elderly to promote vaccine-induced immunity against targetable cancers and emerging pathogens, such as seasonal influenza viruses and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2).</description><identifier>ISSN: 0022-1767</identifier><identifier>EISSN: 1550-6606</identifier><identifier>DOI: 10.4049/jimmunol.2100194</identifier><identifier>PMID: 35031578</identifier><language>eng</language><publisher>United States: Publisher : Baltimore : Williams & Wilkins, c1950-. Latest Publisher : Bethesda, MD : American Association of Immunologists</publisher><subject>Adult ; Aged ; Aged, 80 and over ; Aging - immunology ; Apoptosis ; Cancer Vaccines - immunology ; CD8-Positive T-Lymphocytes - immunology ; CD8-Positive T-Lymphocytes - metabolism ; Cell Division ; COVID-19 - immunology ; Female ; Fenofibrate - pharmacology ; Glucose - metabolism ; HLA-A2 Antigen - immunology ; Human health and pathology ; Humans ; Hypolipidemic Agents - pharmacology ; Hypolipidemic Agents - therapeutic use ; Immunocompetence - drug effects ; Infectious diseases ; Influenza, Human - immunology ; Life Sciences ; Lipid Metabolism - drug effects ; Lymphocyte Activation ; Male ; MART-1 Antigen - chemistry ; MART-1 Antigen - immunology ; Middle Aged ; Neoplasms - immunology ; Peptide Fragments - immunology ; Rosiglitazone - pharmacology ; Single-Blind Method ; Vaccination ; Viral Vaccines - immunology ; Young Adult</subject><ispartof>The Journal of immunology (1950), 2022-02, Vol.208 (3), p.562-570</ispartof><rights>Copyright © 2022 by The American Association of Immunologists, Inc.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-7751b319ebbd04744cc68110ca5c0eb04388db7775824a5197e9138b453303573</citedby><cites>FETCH-LOGICAL-c375t-7751b319ebbd04744cc68110ca5c0eb04388db7775824a5197e9138b453303573</cites><orcidid>0000-0001-9416-2737 ; 0000-0002-7805-4290 ; 0000-0001-8217-5039 ; 0000-0002-7308-7317 ; 0000-0002-7514-8873 ; 0000-0003-2914-9610 ; 0000-0002-7278-6503 ; 0000-0002-1241-0299 ; 0000-0001-7599-3658 ; 0000-0002-3593-5055</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35031578$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://ut3-toulouseinp.hal.science/hal-03777022$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Nicoli, Francesco</creatorcontrib><creatorcontrib>Cabral-Piccin, Mariela P</creatorcontrib><creatorcontrib>Papagno, Laura</creatorcontrib><creatorcontrib>Gallerani, Eleonora</creatorcontrib><creatorcontrib>Fusaro, Mathieu</creatorcontrib><creatorcontrib>Folcher, Victor</creatorcontrib><creatorcontrib>Dubois, Marion</creatorcontrib><creatorcontrib>Clave, Emmanuel</creatorcontrib><creatorcontrib>Vallet, Hélène</creatorcontrib><creatorcontrib>Frere, Justin J</creatorcontrib><creatorcontrib>Gostick, Emma</creatorcontrib><creatorcontrib>Llewellyn-Lacey, Sian</creatorcontrib><creatorcontrib>Price, David A</creatorcontrib><creatorcontrib>Toubert, Antoine</creatorcontrib><creatorcontrib>Dupré, Loïc</creatorcontrib><creatorcontrib>Boddaert, Jacques</creatorcontrib><creatorcontrib>Caputo, Antonella</creatorcontrib><creatorcontrib>Gavioli, Riccardo</creatorcontrib><creatorcontrib>Appay, Victor</creatorcontrib><title>Altered Basal Lipid Metabolism Underlies the Functional Impairment of Naive CD8 + T Cells in Elderly Humans</title><title>The Journal of immunology (1950)</title><addtitle>J Immunol</addtitle><description>Aging is associated with functional deficits in the naive T cell compartment, which compromise the generation of de novo immune responses against previously unencountered Ags. The mechanisms that underlie this phenomenon have nonetheless remained unclear. We found that naive CD8
T cells in elderly humans were prone to apoptosis and proliferated suboptimally in response to stimulation via the TCR. These abnormalities were associated with dysregulated lipid metabolism under homeostatic conditions and enhanced levels of basal activation. Importantly, reversal of the bioenergetic anomalies with lipid-altering drugs, such as rosiglitazone, almost completely restored the Ag responsiveness of naive CD8
T cells. Interventions that favor lipid catabolism may therefore find utility as adjunctive therapies in the elderly to promote vaccine-induced immunity against targetable cancers and emerging pathogens, such as seasonal influenza viruses and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2).</description><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Aging - immunology</subject><subject>Apoptosis</subject><subject>Cancer Vaccines - immunology</subject><subject>CD8-Positive T-Lymphocytes - immunology</subject><subject>CD8-Positive T-Lymphocytes - metabolism</subject><subject>Cell Division</subject><subject>COVID-19 - immunology</subject><subject>Female</subject><subject>Fenofibrate - pharmacology</subject><subject>Glucose - metabolism</subject><subject>HLA-A2 Antigen - immunology</subject><subject>Human health and pathology</subject><subject>Humans</subject><subject>Hypolipidemic Agents - pharmacology</subject><subject>Hypolipidemic Agents - therapeutic use</subject><subject>Immunocompetence - drug effects</subject><subject>Infectious diseases</subject><subject>Influenza, Human - immunology</subject><subject>Life Sciences</subject><subject>Lipid Metabolism - drug effects</subject><subject>Lymphocyte Activation</subject><subject>Male</subject><subject>MART-1 Antigen - chemistry</subject><subject>MART-1 Antigen - immunology</subject><subject>Middle Aged</subject><subject>Neoplasms - immunology</subject><subject>Peptide Fragments - immunology</subject><subject>Rosiglitazone - pharmacology</subject><subject>Single-Blind Method</subject><subject>Vaccination</subject><subject>Viral Vaccines - immunology</subject><subject>Young Adult</subject><issn>0022-1767</issn><issn>1550-6606</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kM1PwjAYhxujEUTvnkyvxgzfru26HXGCkEy9wHlptxKK7UbWjYT_3hE-Tm_y5nl-hwehZwJjBix53xrnuqq245AAkITdoCHhHIIogugWDQHCMCAiEgP04P0WACII2T0aUA6UcBEP0d_EtrrRJf6QXlqcmZ0p8bdupaqt8Q6vqlI31miP243Gs64qWlNXPblwO2kap6sW12v8I81e4_Qzxm94iVNtrcemwlN7tA943jlZ-Ud0t5bW66fzHaHVbLpM50H2-7VIJ1lQUMHbQAhOFCWJVqoEJhgriigmBArJC9AKGI3jUokei0MmOUmETgiNFeOUAuWCjtDraXcjbb5rjJPNIa-lyeeTLD_-gPZ232ZPehZObNHU3jd6fRUI5MfG-aVxfm7cKy8nZdcpp8urcIlK_wGejncD</recordid><startdate>20220201</startdate><enddate>20220201</enddate><creator>Nicoli, Francesco</creator><creator>Cabral-Piccin, Mariela P</creator><creator>Papagno, Laura</creator><creator>Gallerani, Eleonora</creator><creator>Fusaro, Mathieu</creator><creator>Folcher, Victor</creator><creator>Dubois, Marion</creator><creator>Clave, Emmanuel</creator><creator>Vallet, Hélène</creator><creator>Frere, Justin J</creator><creator>Gostick, Emma</creator><creator>Llewellyn-Lacey, Sian</creator><creator>Price, David A</creator><creator>Toubert, Antoine</creator><creator>Dupré, Loïc</creator><creator>Boddaert, Jacques</creator><creator>Caputo, Antonella</creator><creator>Gavioli, Riccardo</creator><creator>Appay, Victor</creator><general>Publisher : Baltimore : Williams & Wilkins, c1950-. Latest Publisher : Bethesda, MD : American Association of Immunologists</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>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0001-9416-2737</orcidid><orcidid>https://orcid.org/0000-0002-7805-4290</orcidid><orcidid>https://orcid.org/0000-0001-8217-5039</orcidid><orcidid>https://orcid.org/0000-0002-7308-7317</orcidid><orcidid>https://orcid.org/0000-0002-7514-8873</orcidid><orcidid>https://orcid.org/0000-0003-2914-9610</orcidid><orcidid>https://orcid.org/0000-0002-7278-6503</orcidid><orcidid>https://orcid.org/0000-0002-1241-0299</orcidid><orcidid>https://orcid.org/0000-0001-7599-3658</orcidid><orcidid>https://orcid.org/0000-0002-3593-5055</orcidid></search><sort><creationdate>20220201</creationdate><title>Altered Basal Lipid Metabolism Underlies the Functional Impairment of Naive CD8 + T Cells in Elderly Humans</title><author>Nicoli, Francesco ; Cabral-Piccin, Mariela P ; Papagno, Laura ; Gallerani, Eleonora ; Fusaro, Mathieu ; Folcher, Victor ; Dubois, Marion ; Clave, Emmanuel ; Vallet, Hélène ; Frere, Justin J ; Gostick, Emma ; Llewellyn-Lacey, Sian ; Price, David A ; Toubert, Antoine ; Dupré, Loïc ; Boddaert, Jacques ; Caputo, Antonella ; Gavioli, Riccardo ; Appay, Victor</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-7751b319ebbd04744cc68110ca5c0eb04388db7775824a5197e9138b453303573</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Aging - immunology</topic><topic>Apoptosis</topic><topic>Cancer Vaccines - immunology</topic><topic>CD8-Positive T-Lymphocytes - immunology</topic><topic>CD8-Positive T-Lymphocytes - metabolism</topic><topic>Cell Division</topic><topic>COVID-19 - immunology</topic><topic>Female</topic><topic>Fenofibrate - pharmacology</topic><topic>Glucose - metabolism</topic><topic>HLA-A2 Antigen - immunology</topic><topic>Human health and pathology</topic><topic>Humans</topic><topic>Hypolipidemic Agents - pharmacology</topic><topic>Hypolipidemic Agents - therapeutic use</topic><topic>Immunocompetence - drug effects</topic><topic>Infectious diseases</topic><topic>Influenza, Human - immunology</topic><topic>Life Sciences</topic><topic>Lipid Metabolism - drug effects</topic><topic>Lymphocyte Activation</topic><topic>Male</topic><topic>MART-1 Antigen - chemistry</topic><topic>MART-1 Antigen - immunology</topic><topic>Middle Aged</topic><topic>Neoplasms - immunology</topic><topic>Peptide Fragments - immunology</topic><topic>Rosiglitazone - pharmacology</topic><topic>Single-Blind Method</topic><topic>Vaccination</topic><topic>Viral Vaccines - immunology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nicoli, Francesco</creatorcontrib><creatorcontrib>Cabral-Piccin, Mariela P</creatorcontrib><creatorcontrib>Papagno, Laura</creatorcontrib><creatorcontrib>Gallerani, Eleonora</creatorcontrib><creatorcontrib>Fusaro, Mathieu</creatorcontrib><creatorcontrib>Folcher, Victor</creatorcontrib><creatorcontrib>Dubois, Marion</creatorcontrib><creatorcontrib>Clave, Emmanuel</creatorcontrib><creatorcontrib>Vallet, Hélène</creatorcontrib><creatorcontrib>Frere, Justin J</creatorcontrib><creatorcontrib>Gostick, Emma</creatorcontrib><creatorcontrib>Llewellyn-Lacey, Sian</creatorcontrib><creatorcontrib>Price, David A</creatorcontrib><creatorcontrib>Toubert, Antoine</creatorcontrib><creatorcontrib>Dupré, Loïc</creatorcontrib><creatorcontrib>Boddaert, Jacques</creatorcontrib><creatorcontrib>Caputo, Antonella</creatorcontrib><creatorcontrib>Gavioli, Riccardo</creatorcontrib><creatorcontrib>Appay, Victor</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>The Journal of immunology (1950)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nicoli, Francesco</au><au>Cabral-Piccin, Mariela P</au><au>Papagno, Laura</au><au>Gallerani, Eleonora</au><au>Fusaro, Mathieu</au><au>Folcher, Victor</au><au>Dubois, Marion</au><au>Clave, Emmanuel</au><au>Vallet, Hélène</au><au>Frere, Justin J</au><au>Gostick, Emma</au><au>Llewellyn-Lacey, Sian</au><au>Price, David A</au><au>Toubert, Antoine</au><au>Dupré, Loïc</au><au>Boddaert, Jacques</au><au>Caputo, Antonella</au><au>Gavioli, Riccardo</au><au>Appay, Victor</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Altered Basal Lipid Metabolism Underlies the Functional Impairment of Naive CD8 + T Cells in Elderly Humans</atitle><jtitle>The Journal of immunology (1950)</jtitle><addtitle>J Immunol</addtitle><date>2022-02-01</date><risdate>2022</risdate><volume>208</volume><issue>3</issue><spage>562</spage><epage>570</epage><pages>562-570</pages><issn>0022-1767</issn><eissn>1550-6606</eissn><abstract>Aging is associated with functional deficits in the naive T cell compartment, which compromise the generation of de novo immune responses against previously unencountered Ags. The mechanisms that underlie this phenomenon have nonetheless remained unclear. We found that naive CD8
T cells in elderly humans were prone to apoptosis and proliferated suboptimally in response to stimulation via the TCR. These abnormalities were associated with dysregulated lipid metabolism under homeostatic conditions and enhanced levels of basal activation. Importantly, reversal of the bioenergetic anomalies with lipid-altering drugs, such as rosiglitazone, almost completely restored the Ag responsiveness of naive CD8
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| ispartof | The Journal of immunology (1950), 2022-02, Vol.208 (3), p.562-570 |
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| subjects | Adult Aged Aged, 80 and over Aging - immunology Apoptosis Cancer Vaccines - immunology CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism Cell Division COVID-19 - immunology Female Fenofibrate - pharmacology Glucose - metabolism HLA-A2 Antigen - immunology Human health and pathology Humans Hypolipidemic Agents - pharmacology Hypolipidemic Agents - therapeutic use Immunocompetence - drug effects Infectious diseases Influenza, Human - immunology Life Sciences Lipid Metabolism - drug effects Lymphocyte Activation Male MART-1 Antigen - chemistry MART-1 Antigen - immunology Middle Aged Neoplasms - immunology Peptide Fragments - immunology Rosiglitazone - pharmacology Single-Blind Method Vaccination Viral Vaccines - immunology Young Adult |
| title | Altered Basal Lipid Metabolism Underlies the Functional Impairment of Naive CD8 + T Cells in Elderly Humans |
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