Aging of Antiviral CD8 + Memory T Cells Fosters Increased Survival, Metabolic Adaptations, and Lymphoid Tissue Homing
Aging of established antiviral T cell memory can foster a series of progressive adaptations that paradoxically improve rather than compromise protective CD8 T cell immunity. We now provide evidence that this gradual evolution, the pace of which is contingent on the precise context of the primary res...
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Veröffentlicht in: | The Journal of immunology (1950) 2019-01, Vol.202 (2), p.460-475 |
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container_title | The Journal of immunology (1950) |
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creator | Davenport, Bennett Eberlein, Jens van der Heide, Verena Jhun, Kevin Nguyen, Tom T Victorino, Francisco Trotta, Andrew Chipuk, Jerry Yi, Zhengzi Zhang, Weijia Clambey, Eric T Scott, Donald K Homann, Dirk |
description | Aging of established antiviral T cell memory can foster a series of progressive adaptations that paradoxically improve rather than compromise protective CD8
T cell immunity. We now provide evidence that this gradual evolution, the pace of which is contingent on the precise context of the primary response, also impinges on the molecular mechanisms that regulate CD8
memory T cell (T
) homeostasis. Over time, CD8
T
generated in the wake of an acute infection with the natural murine pathogen lymphocytic choriomeningitis virus become more resistant to apoptosis and acquire enhanced cytokine responsiveness without adjusting their homeostatic proliferation rates; concurrent metabolic adaptations promote increased CD8
T
quiescence and fitness but also impart the reacquisition of a partial effector-like metabolic profile; and a gradual redistribution of aging CD8
T
from blood and nonlymphoid tissues to lymphatic organs results in CD8
T
accumulations in bone marrow, splenic white pulp, and, particularly, lymph nodes. Altogether, these data demonstrate how temporal alterations of fundamental homeostatic determinants converge to render aged CD8
T
poised for greater recall responses. |
doi_str_mv | 10.4049/jimmunol.1801277 |
format | Article |
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T cell immunity. We now provide evidence that this gradual evolution, the pace of which is contingent on the precise context of the primary response, also impinges on the molecular mechanisms that regulate CD8
memory T cell (T
) homeostasis. Over time, CD8
T
generated in the wake of an acute infection with the natural murine pathogen lymphocytic choriomeningitis virus become more resistant to apoptosis and acquire enhanced cytokine responsiveness without adjusting their homeostatic proliferation rates; concurrent metabolic adaptations promote increased CD8
T
quiescence and fitness but also impart the reacquisition of a partial effector-like metabolic profile; and a gradual redistribution of aging CD8
T
from blood and nonlymphoid tissues to lymphatic organs results in CD8
T
accumulations in bone marrow, splenic white pulp, and, particularly, lymph nodes. Altogether, these data demonstrate how temporal alterations of fundamental homeostatic determinants converge to render aged CD8
T
poised for greater recall responses.</description><identifier>ISSN: 0022-1767</identifier><identifier>EISSN: 1550-6606</identifier><identifier>DOI: 10.4049/jimmunol.1801277</identifier><identifier>PMID: 30552164</identifier><language>eng</language><publisher>United States</publisher><subject>Aging - immunology ; Animals ; Antigens, Viral - immunology ; CD8-Positive T-Lymphocytes - physiology ; Cell Movement ; Cell Survival ; Cells, Cultured ; Immunologic Memory - immunology ; Lymph Nodes - immunology ; Lymphocytic Choriomeningitis - immunology ; Lymphocytic choriomeningitis virus - physiology ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Receptors, Antigen, T-Cell - genetics</subject><ispartof>The Journal of immunology (1950), 2019-01, Vol.202 (2), p.460-475</ispartof><rights>Copyright © 2019 by The American Association of Immunologists, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c396t-1001a179a316f0d80fac89a20123825aaa02bac98871eb9b9bd0c3facbf59b483</citedby><cites>FETCH-LOGICAL-c396t-1001a179a316f0d80fac89a20123825aaa02bac98871eb9b9bd0c3facbf59b483</cites><orcidid>0000-0002-7622-5754 ; 0000-0002-7972-9544 ; 0000-0002-3602-4405 ; 0000-0002-1677-2297 ; 0000-0002-6268-1767</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30552164$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Davenport, Bennett</creatorcontrib><creatorcontrib>Eberlein, Jens</creatorcontrib><creatorcontrib>van der Heide, Verena</creatorcontrib><creatorcontrib>Jhun, Kevin</creatorcontrib><creatorcontrib>Nguyen, Tom T</creatorcontrib><creatorcontrib>Victorino, Francisco</creatorcontrib><creatorcontrib>Trotta, Andrew</creatorcontrib><creatorcontrib>Chipuk, Jerry</creatorcontrib><creatorcontrib>Yi, Zhengzi</creatorcontrib><creatorcontrib>Zhang, Weijia</creatorcontrib><creatorcontrib>Clambey, Eric T</creatorcontrib><creatorcontrib>Scott, Donald K</creatorcontrib><creatorcontrib>Homann, Dirk</creatorcontrib><title>Aging of Antiviral CD8 + Memory T Cells Fosters Increased Survival, Metabolic Adaptations, and Lymphoid Tissue Homing</title><title>The Journal of immunology (1950)</title><addtitle>J Immunol</addtitle><description>Aging of established antiviral T cell memory can foster a series of progressive adaptations that paradoxically improve rather than compromise protective CD8
T cell immunity. We now provide evidence that this gradual evolution, the pace of which is contingent on the precise context of the primary response, also impinges on the molecular mechanisms that regulate CD8
memory T cell (T
) homeostasis. Over time, CD8
T
generated in the wake of an acute infection with the natural murine pathogen lymphocytic choriomeningitis virus become more resistant to apoptosis and acquire enhanced cytokine responsiveness without adjusting their homeostatic proliferation rates; concurrent metabolic adaptations promote increased CD8
T
quiescence and fitness but also impart the reacquisition of a partial effector-like metabolic profile; and a gradual redistribution of aging CD8
T
from blood and nonlymphoid tissues to lymphatic organs results in CD8
T
accumulations in bone marrow, splenic white pulp, and, particularly, lymph nodes. Altogether, these data demonstrate how temporal alterations of fundamental homeostatic determinants converge to render aged CD8
T
poised for greater recall responses.</description><subject>Aging - immunology</subject><subject>Animals</subject><subject>Antigens, Viral - immunology</subject><subject>CD8-Positive T-Lymphocytes - physiology</subject><subject>Cell Movement</subject><subject>Cell Survival</subject><subject>Cells, Cultured</subject><subject>Immunologic Memory - immunology</subject><subject>Lymph Nodes - immunology</subject><subject>Lymphocytic Choriomeningitis - immunology</subject><subject>Lymphocytic choriomeningitis virus - physiology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Receptors, Antigen, T-Cell - genetics</subject><issn>0022-1767</issn><issn>1550-6606</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUcFO3DAQtapWZQvce6p8rAShYyd2nEul1bYUpK16YDlbE8dZjBJ7aycr7d_jigUVzWEO896befMI-czgqoKq-fboxnH2YbhiChiv63dkwYSAQkqQ78kCgPOC1bI-IZ9SegQACbz6SE5KEIIzWS3IvNw6v6Whp0s_ub2LONDVD0Uv6G87hnigG7qyw5DodUiTjYneehMtJtvRuznu3R6HywydsA2DM3TZ4W7CyQWfLin6jq4P4-4huI5uXEqzpTdhzPvOyIceh2TPj_2U3F__3KxuivWfX7er5bowZSOnggEwZHWDJZM9dAp6NKpBnr2WigtEBN6iaZSqmW2bXB2YMoPaXjRtpcpT8v1Zdze3o-2M9VM2qHfRjRgPOqDTbyfePeht2GtZCgVcZIGvR4EY_s42TXp0yeSHoLdhTpozUUupFDQZCs9QE0NK0favaxjof2npl7T0Ma1M-fL_ea-El3jKJ6czk_c</recordid><startdate>20190115</startdate><enddate>20190115</enddate><creator>Davenport, Bennett</creator><creator>Eberlein, Jens</creator><creator>van der Heide, Verena</creator><creator>Jhun, Kevin</creator><creator>Nguyen, Tom T</creator><creator>Victorino, Francisco</creator><creator>Trotta, Andrew</creator><creator>Chipuk, Jerry</creator><creator>Yi, Zhengzi</creator><creator>Zhang, Weijia</creator><creator>Clambey, Eric T</creator><creator>Scott, Donald K</creator><creator>Homann, Dirk</creator><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>5PM</scope><orcidid>https://orcid.org/0000-0002-7622-5754</orcidid><orcidid>https://orcid.org/0000-0002-7972-9544</orcidid><orcidid>https://orcid.org/0000-0002-3602-4405</orcidid><orcidid>https://orcid.org/0000-0002-1677-2297</orcidid><orcidid>https://orcid.org/0000-0002-6268-1767</orcidid></search><sort><creationdate>20190115</creationdate><title>Aging of Antiviral CD8 + Memory T Cells Fosters Increased Survival, Metabolic Adaptations, and Lymphoid Tissue Homing</title><author>Davenport, Bennett ; Eberlein, Jens ; van der Heide, Verena ; Jhun, Kevin ; Nguyen, Tom T ; Victorino, Francisco ; Trotta, Andrew ; Chipuk, Jerry ; Yi, Zhengzi ; Zhang, Weijia ; Clambey, Eric T ; Scott, Donald K ; Homann, Dirk</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c396t-1001a179a316f0d80fac89a20123825aaa02bac98871eb9b9bd0c3facbf59b483</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Aging - immunology</topic><topic>Animals</topic><topic>Antigens, Viral - immunology</topic><topic>CD8-Positive T-Lymphocytes - physiology</topic><topic>Cell Movement</topic><topic>Cell Survival</topic><topic>Cells, Cultured</topic><topic>Immunologic Memory - immunology</topic><topic>Lymph Nodes - immunology</topic><topic>Lymphocytic Choriomeningitis - immunology</topic><topic>Lymphocytic choriomeningitis virus - physiology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Transgenic</topic><topic>Receptors, Antigen, T-Cell - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Davenport, Bennett</creatorcontrib><creatorcontrib>Eberlein, Jens</creatorcontrib><creatorcontrib>van der Heide, Verena</creatorcontrib><creatorcontrib>Jhun, Kevin</creatorcontrib><creatorcontrib>Nguyen, Tom T</creatorcontrib><creatorcontrib>Victorino, Francisco</creatorcontrib><creatorcontrib>Trotta, Andrew</creatorcontrib><creatorcontrib>Chipuk, Jerry</creatorcontrib><creatorcontrib>Yi, Zhengzi</creatorcontrib><creatorcontrib>Zhang, Weijia</creatorcontrib><creatorcontrib>Clambey, Eric T</creatorcontrib><creatorcontrib>Scott, Donald K</creatorcontrib><creatorcontrib>Homann, Dirk</creatorcontrib><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>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of immunology (1950)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Davenport, Bennett</au><au>Eberlein, Jens</au><au>van der Heide, Verena</au><au>Jhun, Kevin</au><au>Nguyen, Tom T</au><au>Victorino, Francisco</au><au>Trotta, Andrew</au><au>Chipuk, Jerry</au><au>Yi, Zhengzi</au><au>Zhang, Weijia</au><au>Clambey, Eric T</au><au>Scott, Donald K</au><au>Homann, Dirk</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Aging of Antiviral CD8 + Memory T Cells Fosters Increased Survival, Metabolic Adaptations, and Lymphoid Tissue Homing</atitle><jtitle>The Journal of immunology (1950)</jtitle><addtitle>J Immunol</addtitle><date>2019-01-15</date><risdate>2019</risdate><volume>202</volume><issue>2</issue><spage>460</spage><epage>475</epage><pages>460-475</pages><issn>0022-1767</issn><eissn>1550-6606</eissn><abstract>Aging of established antiviral T cell memory can foster a series of progressive adaptations that paradoxically improve rather than compromise protective CD8
T cell immunity. We now provide evidence that this gradual evolution, the pace of which is contingent on the precise context of the primary response, also impinges on the molecular mechanisms that regulate CD8
memory T cell (T
) homeostasis. Over time, CD8
T
generated in the wake of an acute infection with the natural murine pathogen lymphocytic choriomeningitis virus become more resistant to apoptosis and acquire enhanced cytokine responsiveness without adjusting their homeostatic proliferation rates; concurrent metabolic adaptations promote increased CD8
T
quiescence and fitness but also impart the reacquisition of a partial effector-like metabolic profile; and a gradual redistribution of aging CD8
T
from blood and nonlymphoid tissues to lymphatic organs results in CD8
T
accumulations in bone marrow, splenic white pulp, and, particularly, lymph nodes. Altogether, these data demonstrate how temporal alterations of fundamental homeostatic determinants converge to render aged CD8
T
poised for greater recall responses.</abstract><cop>United States</cop><pmid>30552164</pmid><doi>10.4049/jimmunol.1801277</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-7622-5754</orcidid><orcidid>https://orcid.org/0000-0002-7972-9544</orcidid><orcidid>https://orcid.org/0000-0002-3602-4405</orcidid><orcidid>https://orcid.org/0000-0002-1677-2297</orcidid><orcidid>https://orcid.org/0000-0002-6268-1767</orcidid><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
subjects | Aging - immunology Animals Antigens, Viral - immunology CD8-Positive T-Lymphocytes - physiology Cell Movement Cell Survival Cells, Cultured Immunologic Memory - immunology Lymph Nodes - immunology Lymphocytic Choriomeningitis - immunology Lymphocytic choriomeningitis virus - physiology Mice Mice, Inbred C57BL Mice, Transgenic Receptors, Antigen, T-Cell - genetics |
title | Aging of Antiviral CD8 + Memory T Cells Fosters Increased Survival, Metabolic Adaptations, and Lymphoid Tissue Homing |
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