Compromised steady‐state germinal center activity with age in nonhuman primates
Age‐related reductions in vaccine‐induced B cells in aging indicate that germinal centers (GCs), the anatomical site where the development of humoral responses takes place, may lose efficacy with age. We have investigated the baseline follicular and GC composition in nonhuman primates (NHPs) with re...
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| creator | Shankwitz, Kimberly Pallikkuth, Suresh Sirupangi, Tirupataiah Kirk Kvistad, Daniel Russel, Kyle Blaine Pahwa, Rajendra Gama, Lucio Koup, Richard A. Pan, Li Villinger, Francois Pahwa, Savita Petrovas, Constantinos |
| description | Age‐related reductions in vaccine‐induced B cells in aging indicate that germinal centers (GCs), the anatomical site where the development of humoral responses takes place, may lose efficacy with age. We have investigated the baseline follicular and GC composition in nonhuman primates (NHPs) with respect to their age. There was a marked reduction in follicular area in old animals. We found significantly lower normalized numbers of follicular PD1hi CD4 T (Tfh) and proliferating (Ki67hi) GC B cells with aging, a profile associated with significantly higher numbers of potential follicular suppressor FoxP3hiLag3hi CD4 T cells. Furthermore, a positive correlation was found between Tfh and follicular CD8 T cells (fCD8) only in young animals. Despite the increased levels of circulating preinflammatory factors in aging, young animals had higher numbers of monocytes and granulocytes in the follicles, a profile negatively associated with numbers of Tfh cells. Multiple regression analysis showed an altered association between GC B cells and other GC immune cell populations in old animals suggesting a differential mechanistic regulation of GC activity in aging. Our data demonstrate defective baseline GC composition in old NHPs and provide an immunological base for further understanding the adaptive humoral responses with respect to aging.
Steady‐state germinal center immune reactivity is compromised in aged NHPs. This loss of reactivity is characterized by changes in many GC associated cell populations including Tfh, B cells, and follicular Tregs. |
| doi_str_mv | 10.1111/acel.13087 |
| format | Article |
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Steady‐state germinal center immune reactivity is compromised in aged NHPs. This loss of reactivity is characterized by changes in many GC associated cell populations including Tfh, B cells, and follicular Tregs.</description><identifier>ISSN: 1474-9718</identifier><identifier>EISSN: 1474-9726</identifier><identifier>DOI: 10.1111/acel.13087</identifier><identifier>PMID: 31840398</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Age ; Aging ; Aging - immunology ; Animals ; Antigens ; Antigens, CD - metabolism ; B cells ; B-Lymphocytes - immunology ; CD4 antigen ; CD4-Positive T-Lymphocytes - immunology ; CD4-Positive T-Lymphocytes - metabolism ; CD8 antigen ; CD8-Positive T-Lymphocytes - immunology ; CD8-Positive T-Lymphocytes - metabolism ; Flow cytometry ; Follicles ; Forkhead Transcription Factors - metabolism ; Germinal Center - cytology ; Germinal Center - immunology ; Germinal Center - pathology ; Germinal centers ; Granulocytes - metabolism ; Immune system ; Immunity, Humoral ; Inflammation - immunology ; Inflammation - metabolism ; Inflammation - physiopathology ; Leukocytes (granulocytic) ; Listeria ; Lymph Nodes - cytology ; Lymph Nodes - immunology ; Lymph Nodes - physiopathology ; Lymphocyte Activation Gene 3 Protein ; Lymphocytes ; Lymphocytes B ; Lymphocytes T ; Macaca mulatta ; Monocytes ; Monocytes - metabolism ; Multiple regression analysis ; Nanoparticles ; Older people ; Original Paper ; Original Papers ; T cells ; Tfh cells ; Vaccines</subject><ispartof>Aging cell, 2020-02, Vol.19 (2), p.e13087-n/a</ispartof><rights>2019 The Authors. published by the Anatomical Society and John Wiley & Sons Ltd.</rights><rights>2019 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.</rights><rights>COPYRIGHT 2019 John Wiley & Sons, Inc.</rights><rights>2019. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5437-3226e3ea94344dfdd52a6e5b65a64e919658bdd2204eac371d7c27378ddbbe753</citedby><cites>FETCH-LOGICAL-c5437-3226e3ea94344dfdd52a6e5b65a64e919658bdd2204eac371d7c27378ddbbe753</cites><orcidid>0000-0002-5067-5810</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6996951/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6996951/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1417,11562,27924,27925,45574,45575,46052,46476,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31840398$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shankwitz, Kimberly</creatorcontrib><creatorcontrib>Pallikkuth, Suresh</creatorcontrib><creatorcontrib>Sirupangi, Tirupataiah</creatorcontrib><creatorcontrib>Kirk Kvistad, Daniel</creatorcontrib><creatorcontrib>Russel, Kyle Blaine</creatorcontrib><creatorcontrib>Pahwa, Rajendra</creatorcontrib><creatorcontrib>Gama, Lucio</creatorcontrib><creatorcontrib>Koup, Richard A.</creatorcontrib><creatorcontrib>Pan, Li</creatorcontrib><creatorcontrib>Villinger, Francois</creatorcontrib><creatorcontrib>Pahwa, Savita</creatorcontrib><creatorcontrib>Petrovas, Constantinos</creatorcontrib><title>Compromised steady‐state germinal center activity with age in nonhuman primates</title><title>Aging cell</title><addtitle>Aging Cell</addtitle><description>Age‐related reductions in vaccine‐induced B cells in aging indicate that germinal centers (GCs), the anatomical site where the development of humoral responses takes place, may lose efficacy with age. We have investigated the baseline follicular and GC composition in nonhuman primates (NHPs) with respect to their age. There was a marked reduction in follicular area in old animals. We found significantly lower normalized numbers of follicular PD1hi CD4 T (Tfh) and proliferating (Ki67hi) GC B cells with aging, a profile associated with significantly higher numbers of potential follicular suppressor FoxP3hiLag3hi CD4 T cells. Furthermore, a positive correlation was found between Tfh and follicular CD8 T cells (fCD8) only in young animals. Despite the increased levels of circulating preinflammatory factors in aging, young animals had higher numbers of monocytes and granulocytes in the follicles, a profile negatively associated with numbers of Tfh cells. Multiple regression analysis showed an altered association between GC B cells and other GC immune cell populations in old animals suggesting a differential mechanistic regulation of GC activity in aging. Our data demonstrate defective baseline GC composition in old NHPs and provide an immunological base for further understanding the adaptive humoral responses with respect to aging.
Steady‐state germinal center immune reactivity is compromised in aged NHPs. This loss of reactivity is characterized by changes in many GC associated cell populations including Tfh, B cells, and follicular Tregs.</description><subject>Age</subject><subject>Aging</subject><subject>Aging - immunology</subject><subject>Animals</subject><subject>Antigens</subject><subject>Antigens, CD - metabolism</subject><subject>B cells</subject><subject>B-Lymphocytes - immunology</subject><subject>CD4 antigen</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>CD4-Positive T-Lymphocytes - metabolism</subject><subject>CD8 antigen</subject><subject>CD8-Positive T-Lymphocytes - immunology</subject><subject>CD8-Positive T-Lymphocytes - metabolism</subject><subject>Flow cytometry</subject><subject>Follicles</subject><subject>Forkhead Transcription Factors - metabolism</subject><subject>Germinal Center - cytology</subject><subject>Germinal Center - immunology</subject><subject>Germinal Center - pathology</subject><subject>Germinal centers</subject><subject>Granulocytes - metabolism</subject><subject>Immune system</subject><subject>Immunity, Humoral</subject><subject>Inflammation - immunology</subject><subject>Inflammation - metabolism</subject><subject>Inflammation - physiopathology</subject><subject>Leukocytes (granulocytic)</subject><subject>Listeria</subject><subject>Lymph Nodes - cytology</subject><subject>Lymph Nodes - immunology</subject><subject>Lymph Nodes - physiopathology</subject><subject>Lymphocyte Activation Gene 3 Protein</subject><subject>Lymphocytes</subject><subject>Lymphocytes B</subject><subject>Lymphocytes T</subject><subject>Macaca mulatta</subject><subject>Monocytes</subject><subject>Monocytes - metabolism</subject><subject>Multiple regression analysis</subject><subject>Nanoparticles</subject><subject>Older people</subject><subject>Original Paper</subject><subject>Original Papers</subject><subject>T cells</subject><subject>Tfh cells</subject><subject>Vaccines</subject><issn>1474-9718</issn><issn>1474-9726</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kt9qFDEUxgex2Fq98QEk4I0IuyaTf5MbYVlaFRZE0OuQmZzZTZlJ1mSmZe98hD5jn6SZbt1akSYXCcnvfOfw8RXFG4LnJK-PpoFuTiiu5LPihDDJZkqW4vnhTqrj4mVKFxgTqTB9URxTUjFMVXVSfF-GfhtD7xJYlAYwdnfz-zoNZgC0htg7bzrUgB8gItMM7tINO3Tlhg0ya0DOIx_8ZuyNR9vo-lyVXhVHrekSvL4_T4uf52c_ll9mq2-fvy4Xq1nDGZUzWpYCKBjFKGO2tZaXRgCvBTeCgSJK8Kq2tiwxA9NQSaxsSkllZW1dg-T0tPi0192OdQ92mjGaTt-NEXc6GKcf_3i30etwqYVSQnGSBd7fC8Twa4Q06OxCtrIzHsKYdEmnfoxxldF3_6AXYYzZmkwxwSkmXIgnKcoxyXKMP1Br04F2vg15umZqrRcSy0pUFJeZmv-HyttC75rgoXX5_VHBh31BE0NKEdqDEwTrKSZ6iom-i0mG3_7t3QH9k4sMkD1wldvsnpDSi-XZai96C0-Tx2s</recordid><startdate>202002</startdate><enddate>202002</enddate><creator>Shankwitz, Kimberly</creator><creator>Pallikkuth, Suresh</creator><creator>Sirupangi, Tirupataiah</creator><creator>Kirk Kvistad, Daniel</creator><creator>Russel, Kyle Blaine</creator><creator>Pahwa, Rajendra</creator><creator>Gama, Lucio</creator><creator>Koup, Richard A.</creator><creator>Pan, Li</creator><creator>Villinger, Francois</creator><creator>Pahwa, Savita</creator><creator>Petrovas, Constantinos</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>7QP</scope><scope>7TK</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5067-5810</orcidid></search><sort><creationdate>202002</creationdate><title>Compromised steady‐state germinal center activity with age in nonhuman primates</title><author>Shankwitz, Kimberly ; Pallikkuth, Suresh ; Sirupangi, Tirupataiah ; Kirk Kvistad, Daniel ; Russel, Kyle Blaine ; Pahwa, Rajendra ; Gama, Lucio ; Koup, Richard A. ; Pan, Li ; Villinger, Francois ; Pahwa, Savita ; Petrovas, Constantinos</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5437-3226e3ea94344dfdd52a6e5b65a64e919658bdd2204eac371d7c27378ddbbe753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Age</topic><topic>Aging</topic><topic>Aging - immunology</topic><topic>Animals</topic><topic>Antigens</topic><topic>Antigens, CD - metabolism</topic><topic>B cells</topic><topic>B-Lymphocytes - immunology</topic><topic>CD4 antigen</topic><topic>CD4-Positive T-Lymphocytes - immunology</topic><topic>CD4-Positive T-Lymphocytes - metabolism</topic><topic>CD8 antigen</topic><topic>CD8-Positive T-Lymphocytes - immunology</topic><topic>CD8-Positive T-Lymphocytes - metabolism</topic><topic>Flow cytometry</topic><topic>Follicles</topic><topic>Forkhead Transcription Factors - metabolism</topic><topic>Germinal Center - cytology</topic><topic>Germinal Center - immunology</topic><topic>Germinal Center - pathology</topic><topic>Germinal centers</topic><topic>Granulocytes - metabolism</topic><topic>Immune system</topic><topic>Immunity, Humoral</topic><topic>Inflammation - immunology</topic><topic>Inflammation - metabolism</topic><topic>Inflammation - physiopathology</topic><topic>Leukocytes (granulocytic)</topic><topic>Listeria</topic><topic>Lymph Nodes - cytology</topic><topic>Lymph Nodes - immunology</topic><topic>Lymph Nodes - physiopathology</topic><topic>Lymphocyte Activation Gene 3 Protein</topic><topic>Lymphocytes</topic><topic>Lymphocytes B</topic><topic>Lymphocytes T</topic><topic>Macaca mulatta</topic><topic>Monocytes</topic><topic>Monocytes - metabolism</topic><topic>Multiple regression analysis</topic><topic>Nanoparticles</topic><topic>Older people</topic><topic>Original Paper</topic><topic>Original Papers</topic><topic>T cells</topic><topic>Tfh cells</topic><topic>Vaccines</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shankwitz, Kimberly</creatorcontrib><creatorcontrib>Pallikkuth, Suresh</creatorcontrib><creatorcontrib>Sirupangi, Tirupataiah</creatorcontrib><creatorcontrib>Kirk Kvistad, Daniel</creatorcontrib><creatorcontrib>Russel, Kyle Blaine</creatorcontrib><creatorcontrib>Pahwa, Rajendra</creatorcontrib><creatorcontrib>Gama, Lucio</creatorcontrib><creatorcontrib>Koup, Richard A.</creatorcontrib><creatorcontrib>Pan, Li</creatorcontrib><creatorcontrib>Villinger, Francois</creatorcontrib><creatorcontrib>Pahwa, Savita</creatorcontrib><creatorcontrib>Petrovas, Constantinos</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Aging cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shankwitz, Kimberly</au><au>Pallikkuth, Suresh</au><au>Sirupangi, Tirupataiah</au><au>Kirk Kvistad, Daniel</au><au>Russel, Kyle Blaine</au><au>Pahwa, Rajendra</au><au>Gama, Lucio</au><au>Koup, Richard A.</au><au>Pan, Li</au><au>Villinger, Francois</au><au>Pahwa, Savita</au><au>Petrovas, Constantinos</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Compromised steady‐state germinal center activity with age in nonhuman primates</atitle><jtitle>Aging cell</jtitle><addtitle>Aging Cell</addtitle><date>2020-02</date><risdate>2020</risdate><volume>19</volume><issue>2</issue><spage>e13087</spage><epage>n/a</epage><pages>e13087-n/a</pages><issn>1474-9718</issn><eissn>1474-9726</eissn><abstract>Age‐related reductions in vaccine‐induced B cells in aging indicate that germinal centers (GCs), the anatomical site where the development of humoral responses takes place, may lose efficacy with age. We have investigated the baseline follicular and GC composition in nonhuman primates (NHPs) with respect to their age. There was a marked reduction in follicular area in old animals. We found significantly lower normalized numbers of follicular PD1hi CD4 T (Tfh) and proliferating (Ki67hi) GC B cells with aging, a profile associated with significantly higher numbers of potential follicular suppressor FoxP3hiLag3hi CD4 T cells. Furthermore, a positive correlation was found between Tfh and follicular CD8 T cells (fCD8) only in young animals. Despite the increased levels of circulating preinflammatory factors in aging, young animals had higher numbers of monocytes and granulocytes in the follicles, a profile negatively associated with numbers of Tfh cells. Multiple regression analysis showed an altered association between GC B cells and other GC immune cell populations in old animals suggesting a differential mechanistic regulation of GC activity in aging. Our data demonstrate defective baseline GC composition in old NHPs and provide an immunological base for further understanding the adaptive humoral responses with respect to aging.
Steady‐state germinal center immune reactivity is compromised in aged NHPs. This loss of reactivity is characterized by changes in many GC associated cell populations including Tfh, B cells, and follicular Tregs.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>31840398</pmid><doi>10.1111/acel.13087</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-5067-5810</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Age Aging Aging - immunology Animals Antigens Antigens, CD - metabolism B cells B-Lymphocytes - immunology CD4 antigen CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism CD8 antigen CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism Flow cytometry Follicles Forkhead Transcription Factors - metabolism Germinal Center - cytology Germinal Center - immunology Germinal Center - pathology Germinal centers Granulocytes - metabolism Immune system Immunity, Humoral Inflammation - immunology Inflammation - metabolism Inflammation - physiopathology Leukocytes (granulocytic) Listeria Lymph Nodes - cytology Lymph Nodes - immunology Lymph Nodes - physiopathology Lymphocyte Activation Gene 3 Protein Lymphocytes Lymphocytes B Lymphocytes T Macaca mulatta Monocytes Monocytes - metabolism Multiple regression analysis Nanoparticles Older people Original Paper Original Papers T cells Tfh cells Vaccines |
| title | Compromised steady‐state germinal center activity with age in nonhuman primates |
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