The adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice
We previously have reported that neonatal Bacillus Calmette-Guerin (BCG) vaccination improves neurogenesis and behavior in early life through affecting the neuroimmune milieu in the brain, but it is uncertain whether activation phenotypes and functional changes in T lymphocytes shape brain developme...
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| creator | Song, Dan Qi, Fangfang Liu, ShuaiShuai Tang, Zhongsheng Duan, Jinhai Yao, Zhibin |
| description | We previously have reported that neonatal Bacillus Calmette-Guerin (BCG) vaccination improves neurogenesis and behavior in early life through affecting the neuroimmune milieu in the brain, but it is uncertain whether activation phenotypes and functional changes in T lymphocytes shape brain development. Here, we studied the effects of BCG vaccination via the adoptive transfer of T lymphocytes from the BALB/c wild-type mice into naive mice. Our results show that mice adoptive BCG-induced lymphocytes (BCG->naive mice) showed anxiolytic and antidepressant-like performance when completing an elevated plus maze (EPM) test. Meanwhile, BCG->naive mice possess more cell proliferation and newborn neurons than PBS->naive and nude mice in the hippocampus. IFN-γ and IL-4 levels in the serum of BCG->naive mice also increased, while TNF-α and IL-1β levels were reduced relative to those of PBS->naive and nude mice. We further found that BCG->naive mice showed different repartition of CD4+ and CD8+ T cell to naive (CD62L+CD44low), effector memory (CD62L-CD44hi), central memory (CD62L+CD44hi) and acute/activated effector (CD62L-CD44low) cells in the spleen. Importantly, the adoptive transfer of BCG-induced T lymphocytes infiltrated into the dura mater and brain parenchyma of the nude mice. Activation phenotypes and functional changes in T lymphocytes are very likely to affect the neuroimmune milieu in the brain, and alterations in ratios of splenic CD4+ and CD8+ memory T cells may affect the expression of correlative cytokines in the serum, accounting for our behavioral results. We conclude thus that the adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice. Our work shows that BCG vaccination improves hippocampal cell proliferation outcomes and behaviors, likely as a result of splenic effector/memory T lymphocytes regulating the neuroimmune niche in the brain. |
| doi_str_mv | 10.1371/journal.pone.0225874 |
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Here, we studied the effects of BCG vaccination via the adoptive transfer of T lymphocytes from the BALB/c wild-type mice into naive mice. Our results show that mice adoptive BCG-induced lymphocytes (BCG->naive mice) showed anxiolytic and antidepressant-like performance when completing an elevated plus maze (EPM) test. Meanwhile, BCG->naive mice possess more cell proliferation and newborn neurons than PBS->naive and nude mice in the hippocampus. IFN-γ and IL-4 levels in the serum of BCG->naive mice also increased, while TNF-α and IL-1β levels were reduced relative to those of PBS->naive and nude mice. We further found that BCG->naive mice showed different repartition of CD4+ and CD8+ T cell to naive (CD62L+CD44low), effector memory (CD62L-CD44hi), central memory (CD62L+CD44hi) and acute/activated effector (CD62L-CD44low) cells in the spleen. Importantly, the adoptive transfer of BCG-induced T lymphocytes infiltrated into the dura mater and brain parenchyma of the nude mice. Activation phenotypes and functional changes in T lymphocytes are very likely to affect the neuroimmune milieu in the brain, and alterations in ratios of splenic CD4+ and CD8+ memory T cells may affect the expression of correlative cytokines in the serum, accounting for our behavioral results. We conclude thus that the adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice. Our work shows that BCG vaccination improves hippocampal cell proliferation outcomes and behaviors, likely as a result of splenic effector/memory T lymphocytes regulating the neuroimmune niche in the brain.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0225874</identifier><identifier>PMID: 32240169</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Activation ; Adoptive transfer ; Antianxiety agents ; Antidepressants ; Anxiety ; Bacillus Calmette-Guerin vaccine ; BCG ; Behavior ; Bias ; Biology and Life Sciences ; Brain ; CD4 antigen ; CD8 antigen ; Cell growth ; Cell proliferation ; Chinese medicine ; Cytokines ; Dura mater ; Effector cells ; Hippocampus ; House mouse ; IL-1β ; Immunological memory ; Interleukin 4 ; L-selectin ; Laboratory animals ; Lymphocytes ; Lymphocytes T ; Medical research ; Medicine and Health Sciences ; Memory cells ; Neonates ; Neurobiology ; Neurogenesis ; Neurons ; Neurosciences ; Newborn infants ; Parenchyma ; Phenotypes ; Research and Analysis Methods ; Rodents ; Social Sciences ; Spleen ; T cells ; Tranquilizing agents ; Tumor necrosis factor-α ; Vaccination ; γ-Interferon</subject><ispartof>PloS one, 2020-04, Vol.15 (4), p.e0225874-e0225874</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Song et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2020 Song et al 2020 Song et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-bfa688c28429f3f8d75c8fc2fc5c44aaadb2e3d7bdbe7a383d6df758507ac6753</citedby><cites>FETCH-LOGICAL-c692t-bfa688c28429f3f8d75c8fc2fc5c44aaadb2e3d7bdbe7a383d6df758507ac6753</cites><orcidid>0000-0003-1613-9157</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/PMC7117742/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7117742/$$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/32240169$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Li, Xiao-Jiang</contributor><creatorcontrib>Song, Dan</creatorcontrib><creatorcontrib>Qi, Fangfang</creatorcontrib><creatorcontrib>Liu, ShuaiShuai</creatorcontrib><creatorcontrib>Tang, Zhongsheng</creatorcontrib><creatorcontrib>Duan, Jinhai</creatorcontrib><creatorcontrib>Yao, Zhibin</creatorcontrib><title>The adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>We previously have reported that neonatal Bacillus Calmette-Guerin (BCG) vaccination improves neurogenesis and behavior in early life through affecting the neuroimmune milieu in the brain, but it is uncertain whether activation phenotypes and functional changes in T lymphocytes shape brain development. Here, we studied the effects of BCG vaccination via the adoptive transfer of T lymphocytes from the BALB/c wild-type mice into naive mice. Our results show that mice adoptive BCG-induced lymphocytes (BCG->naive mice) showed anxiolytic and antidepressant-like performance when completing an elevated plus maze (EPM) test. Meanwhile, BCG->naive mice possess more cell proliferation and newborn neurons than PBS->naive and nude mice in the hippocampus. IFN-γ and IL-4 levels in the serum of BCG->naive mice also increased, while TNF-α and IL-1β levels were reduced relative to those of PBS->naive and nude mice. We further found that BCG->naive mice showed different repartition of CD4+ and CD8+ T cell to naive (CD62L+CD44low), effector memory (CD62L-CD44hi), central memory (CD62L+CD44hi) and acute/activated effector (CD62L-CD44low) cells in the spleen. Importantly, the adoptive transfer of BCG-induced T lymphocytes infiltrated into the dura mater and brain parenchyma of the nude mice. Activation phenotypes and functional changes in T lymphocytes are very likely to affect the neuroimmune milieu in the brain, and alterations in ratios of splenic CD4+ and CD8+ memory T cells may affect the expression of correlative cytokines in the serum, accounting for our behavioral results. We conclude thus that the adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice. Our work shows that BCG vaccination improves hippocampal cell proliferation outcomes and behaviors, likely as a result of splenic effector/memory T lymphocytes regulating the neuroimmune niche in the brain.</description><subject>Activation</subject><subject>Adoptive transfer</subject><subject>Antianxiety agents</subject><subject>Antidepressants</subject><subject>Anxiety</subject><subject>Bacillus Calmette-Guerin vaccine</subject><subject>BCG</subject><subject>Behavior</subject><subject>Bias</subject><subject>Biology and Life Sciences</subject><subject>Brain</subject><subject>CD4 antigen</subject><subject>CD8 antigen</subject><subject>Cell growth</subject><subject>Cell proliferation</subject><subject>Chinese medicine</subject><subject>Cytokines</subject><subject>Dura mater</subject><subject>Effector cells</subject><subject>Hippocampus</subject><subject>House mouse</subject><subject>IL-1β</subject><subject>Immunological memory</subject><subject>Interleukin 4</subject><subject>L-selectin</subject><subject>Laboratory animals</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>Memory cells</subject><subject>Neonates</subject><subject>Neurobiology</subject><subject>Neurogenesis</subject><subject>Neurons</subject><subject>Neurosciences</subject><subject>Newborn infants</subject><subject>Parenchyma</subject><subject>Phenotypes</subject><subject>Research and Analysis Methods</subject><subject>Rodents</subject><subject>Social Sciences</subject><subject>Spleen</subject><subject>T cells</subject><subject>Tranquilizing agents</subject><subject>Tumor necrosis factor-α</subject><subject>Vaccination</subject><subject>γ-Interferon</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><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>eNqNk8Fu1DAQhiMEoqXwBggsISE47JLYSZxckMoKSqVKlWDhajn2eOPi2MF2qu6z8LI47bbqoh6QDx7Z3_zjGc9k2csiXxaEFh8u3OQtN8vRWVjmGFcNLR9lh0VL8KLGOXl8zz7InoVwkecVaer6aXZAMC7zom4Psz_rHhCXboz6ElD03AYFHjmFPq1OFtrKSYBEa2S2w9g7sY0QkHA2et1Nsx0d6vU4OsGHkRskwBg0emd0UuFRO4u4lSjCMIIPyb7SELcLo38B6qDnl9p5pC3SwzBZQBKUFhpsRIMW8Dx7orgJ8GK3H2U_vnxer74uzs5PTlfHZwtRtzguOsXrphG4KXGriGokrUSjBFaiEmXJOZcdBiJpJzugnDRE1lLRqqlyykVNK3KUvb7RHY0LbFfXwDBpKloURV4m4vSGkI5fsNHrgfstc1yz6wPnN4z7qIUBJpWSOe6EqGteJrvjsi3KtsuxqkpakqT1cRdt6gaQImXrudkT3b-xumcbd8nSWygtcRJ4txPw7vcEIbJBh7nw3IKbrt9d4wS2M_rmH_Th7HbUhqcEtFUuxRWzKDuuixZTSvMmUcsHqLQkpM9KTah0Ot9zeL_nMLcNXMUNn0Jgp9-__T97_nOffXuP7YGb2Adnprnbwj5Y3oDCuxA8qLsiFzmbZ-i2GmyeIbaboeT26v4H3TndDg35C6K4G48</recordid><startdate>20200402</startdate><enddate>20200402</enddate><creator>Song, 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adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice</title><author>Song, Dan ; Qi, Fangfang ; Liu, ShuaiShuai ; Tang, Zhongsheng ; Duan, Jinhai ; Yao, Zhibin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-bfa688c28429f3f8d75c8fc2fc5c44aaadb2e3d7bdbe7a383d6df758507ac6753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Activation</topic><topic>Adoptive transfer</topic><topic>Antianxiety agents</topic><topic>Antidepressants</topic><topic>Anxiety</topic><topic>Bacillus Calmette-Guerin vaccine</topic><topic>BCG</topic><topic>Behavior</topic><topic>Bias</topic><topic>Biology and Life Sciences</topic><topic>Brain</topic><topic>CD4 antigen</topic><topic>CD8 antigen</topic><topic>Cell growth</topic><topic>Cell proliferation</topic><topic>Chinese medicine</topic><topic>Cytokines</topic><topic>Dura mater</topic><topic>Effector cells</topic><topic>Hippocampus</topic><topic>House mouse</topic><topic>IL-1β</topic><topic>Immunological memory</topic><topic>Interleukin 4</topic><topic>L-selectin</topic><topic>Laboratory animals</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Medical research</topic><topic>Medicine and Health Sciences</topic><topic>Memory cells</topic><topic>Neonates</topic><topic>Neurobiology</topic><topic>Neurogenesis</topic><topic>Neurons</topic><topic>Neurosciences</topic><topic>Newborn infants</topic><topic>Parenchyma</topic><topic>Phenotypes</topic><topic>Research and Analysis Methods</topic><topic>Rodents</topic><topic>Social Sciences</topic><topic>Spleen</topic><topic>T cells</topic><topic>Tranquilizing agents</topic><topic>Tumor necrosis 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Dan</au><au>Qi, Fangfang</au><au>Liu, ShuaiShuai</au><au>Tang, Zhongsheng</au><au>Duan, Jinhai</au><au>Yao, Zhibin</au><au>Li, Xiao-Jiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-04-02</date><risdate>2020</risdate><volume>15</volume><issue>4</issue><spage>e0225874</spage><epage>e0225874</epage><pages>e0225874-e0225874</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>We previously have reported that neonatal Bacillus Calmette-Guerin (BCG) vaccination improves neurogenesis and behavior in early life through affecting the neuroimmune milieu in the brain, but it is uncertain whether activation phenotypes and functional changes in T lymphocytes shape brain development. Here, we studied the effects of BCG vaccination via the adoptive transfer of T lymphocytes from the BALB/c wild-type mice into naive mice. Our results show that mice adoptive BCG-induced lymphocytes (BCG->naive mice) showed anxiolytic and antidepressant-like performance when completing an elevated plus maze (EPM) test. Meanwhile, BCG->naive mice possess more cell proliferation and newborn neurons than PBS->naive and nude mice in the hippocampus. IFN-γ and IL-4 levels in the serum of BCG->naive mice also increased, while TNF-α and IL-1β levels were reduced relative to those of PBS->naive and nude mice. We further found that BCG->naive mice showed different repartition of CD4+ and CD8+ T cell to naive (CD62L+CD44low), effector memory (CD62L-CD44hi), central memory (CD62L+CD44hi) and acute/activated effector (CD62L-CD44low) cells in the spleen. Importantly, the adoptive transfer of BCG-induced T lymphocytes infiltrated into the dura mater and brain parenchyma of the nude mice. Activation phenotypes and functional changes in T lymphocytes are very likely to affect the neuroimmune milieu in the brain, and alterations in ratios of splenic CD4+ and CD8+ memory T cells may affect the expression of correlative cytokines in the serum, accounting for our behavioral results. We conclude thus that the adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice. Our work shows that BCG vaccination improves hippocampal cell proliferation outcomes and behaviors, likely as a result of splenic effector/memory T lymphocytes regulating the neuroimmune niche in the brain.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32240169</pmid><doi>10.1371/journal.pone.0225874</doi><tpages>e0225874</tpages><orcidid>https://orcid.org/0000-0003-1613-9157</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Activation Adoptive transfer Antianxiety agents Antidepressants Anxiety Bacillus Calmette-Guerin vaccine BCG Behavior Bias Biology and Life Sciences Brain CD4 antigen CD8 antigen Cell growth Cell proliferation Chinese medicine Cytokines Dura mater Effector cells Hippocampus House mouse IL-1β Immunological memory Interleukin 4 L-selectin Laboratory animals Lymphocytes Lymphocytes T Medical research Medicine and Health Sciences Memory cells Neonates Neurobiology Neurogenesis Neurons Neurosciences Newborn infants Parenchyma Phenotypes Research and Analysis Methods Rodents Social Sciences Spleen T cells Tranquilizing agents Tumor necrosis factor-α Vaccination γ-Interferon |
| title | The adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-20T22%3A49%3A56IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20adoptive%20transfer%20of%20BCG-induced%20T%20lymphocytes%20contributes%20to%20hippocampal%20cell%20proliferation%20and%20tempers%20anxiety-like%20behavior%20in%20immune%20deficient%20mice&rft.jtitle=PloS%20one&rft.au=Song,%20Dan&rft.date=2020-04-02&rft.volume=15&rft.issue=4&rft.spage=e0225874&rft.epage=e0225874&rft.pages=e0225874-e0225874&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0225874&rft_dat=%3Cgale_plos_%3EA619277708%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2385711104&rft_id=info:pmid/32240169&rft_galeid=A619277708&rft_doaj_id=oai_doaj_org_article_dffd02bcc66a4ffdbad9149b02f54743&rfr_iscdi=true |