Gestational Hypothyroidism Improves the Ability of the Female Offspring to Clear Streptococcus pneumoniae Infection and to Recover From Pneumococcal Pneumonia
Maternal thyroid hormones are essential for proper fetal development. A deficit of these hormones during gestation has enduring consequences in the central nervous system of the offspring, including detrimental learning and impaired memory. Few studies have shown that thyroid hormone deficiency has...
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creator | Nieto, Pamela A Peñaloza, Hernán F Salazar-Echegarai, Francisco J Castellanos, Raquel M Opazo, Maria Cecilia Venegas, Luis Padilla, Oslando Kalergis, Alexis M Riedel, Claudia A Bueno, Susan M |
description | Maternal thyroid hormones are essential for proper fetal development. A deficit of these hormones during gestation has enduring consequences in the central nervous system of the offspring, including detrimental learning and impaired memory. Few studies have shown that thyroid hormone deficiency has a transient effect in the number of T and B cells in the offspring gestated under hypothyroidism; however, there are no studies showing whether maternal hypothyroidism during gestation impacts the response of the offspring to infections. In this study, we have evaluated whether adult mice gestated in hypothyroid mothers have an altered response to pneumococcal pneumonia. We observed that female mice gestated in hypothyroidism have increased survival rate and less bacterial dissemination to blood and brain after an intranasal challenge with Streptococcus pneumoniae. Further, these mice had higher amounts of inflammatory cells in the lungs and reduced production of cytokines characteristic of sepsis in spleen, blood, and brain at 48 hours after infection. Interestingly, mice gestated in hypothyroid mothers had basally increased vascular permeability in the lungs. These observations suggest that gestational hypothyroidism alters the immune response and the physiology of lungs in the offspring, increasing the resistance to respiratory bacterial infections. |
doi_str_mv | 10.1210/en.2015-1957 |
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A deficit of these hormones during gestation has enduring consequences in the central nervous system of the offspring, including detrimental learning and impaired memory. Few studies have shown that thyroid hormone deficiency has a transient effect in the number of T and B cells in the offspring gestated under hypothyroidism; however, there are no studies showing whether maternal hypothyroidism during gestation impacts the response of the offspring to infections. In this study, we have evaluated whether adult mice gestated in hypothyroid mothers have an altered response to pneumococcal pneumonia. We observed that female mice gestated in hypothyroidism have increased survival rate and less bacterial dissemination to blood and brain after an intranasal challenge with Streptococcus pneumoniae. Further, these mice had higher amounts of inflammatory cells in the lungs and reduced production of cytokines characteristic of sepsis in spleen, blood, and brain at 48 hours after infection. Interestingly, mice gestated in hypothyroid mothers had basally increased vascular permeability in the lungs. These observations suggest that gestational hypothyroidism alters the immune response and the physiology of lungs in the offspring, increasing the resistance to respiratory bacterial infections.</description><identifier>ISSN: 0013-7227</identifier><identifier>EISSN: 1945-7170</identifier><identifier>DOI: 10.1210/en.2015-1957</identifier><identifier>PMID: 27035652</identifier><language>eng</language><publisher>United States: Endocrine Society</publisher><subject>Animals ; Bacteria ; Bacterial diseases ; Bacterial infections ; Blood ; Brain ; Brain - immunology ; Brain - microbiology ; Cell survival ; Central nervous system ; Disease Models, Animal ; Disease Resistance - immunology ; Female ; Females ; Fetuses ; Gestation ; Hormones ; Human health and pathology ; Hypothyroidism ; Hypothyroidism - immunology ; Immune response ; Immunological memory ; Life Sciences ; Lung - immunology ; Lung - microbiology ; Lungs ; Lymphocytes B ; Memory cells ; Mice ; Mice, Inbred C57BL ; Neutrophils - physiology ; Offspring ; Pneumococcal Infections - immunology ; Pneumonia ; Pneumonia, Pneumococcal - immunology ; Pregnancy ; Prenatal Exposure Delayed Effects - immunology ; Prenatal Exposure Delayed Effects - microbiology ; Sepsis ; Sepsis - immunology ; Sepsis - microbiology ; Streptococcus infections ; Streptococcus pneumoniae ; Thyroid ; Thyroid gland ; Thyroid hormones</subject><ispartof>Endocrinology (Philadelphia), 2016-06, Vol.157 (6), p.2217-2228</ispartof><rights>Copyright © 2016 by the Endocrine Society</rights><rights>Copyright © 2016 by the Endocrine Society 2016</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-c503t-44ad13b6b22cee80ffd6a1332a077556800af105b620e3631c3cd3cbdb3c771b3</citedby><cites>FETCH-LOGICAL-c503t-44ad13b6b22cee80ffd6a1332a077556800af105b620e3631c3cd3cbdb3c771b3</cites><orcidid>0000-0001-7622-5263</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/27035652$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://inserm.hal.science/inserm-02149148$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Nieto, Pamela A</creatorcontrib><creatorcontrib>Peñaloza, Hernán F</creatorcontrib><creatorcontrib>Salazar-Echegarai, Francisco J</creatorcontrib><creatorcontrib>Castellanos, Raquel M</creatorcontrib><creatorcontrib>Opazo, Maria Cecilia</creatorcontrib><creatorcontrib>Venegas, Luis</creatorcontrib><creatorcontrib>Padilla, Oslando</creatorcontrib><creatorcontrib>Kalergis, Alexis M</creatorcontrib><creatorcontrib>Riedel, Claudia A</creatorcontrib><creatorcontrib>Bueno, Susan M</creatorcontrib><title>Gestational Hypothyroidism Improves the Ability of the Female Offspring to Clear Streptococcus pneumoniae Infection and to Recover From Pneumococcal Pneumonia</title><title>Endocrinology (Philadelphia)</title><addtitle>Endocrinology</addtitle><description>Maternal thyroid hormones are essential for proper fetal development. A deficit of these hormones during gestation has enduring consequences in the central nervous system of the offspring, including detrimental learning and impaired memory. Few studies have shown that thyroid hormone deficiency has a transient effect in the number of T and B cells in the offspring gestated under hypothyroidism; however, there are no studies showing whether maternal hypothyroidism during gestation impacts the response of the offspring to infections. In this study, we have evaluated whether adult mice gestated in hypothyroid mothers have an altered response to pneumococcal pneumonia. We observed that female mice gestated in hypothyroidism have increased survival rate and less bacterial dissemination to blood and brain after an intranasal challenge with Streptococcus pneumoniae. Further, these mice had higher amounts of inflammatory cells in the lungs and reduced production of cytokines characteristic of sepsis in spleen, blood, and brain at 48 hours after infection. Interestingly, mice gestated in hypothyroid mothers had basally increased vascular permeability in the lungs. These observations suggest that gestational hypothyroidism alters the immune response and the physiology of lungs in the offspring, increasing the resistance to respiratory bacterial infections.</description><subject>Animals</subject><subject>Bacteria</subject><subject>Bacterial diseases</subject><subject>Bacterial infections</subject><subject>Blood</subject><subject>Brain</subject><subject>Brain - immunology</subject><subject>Brain - microbiology</subject><subject>Cell survival</subject><subject>Central nervous system</subject><subject>Disease Models, Animal</subject><subject>Disease Resistance - immunology</subject><subject>Female</subject><subject>Females</subject><subject>Fetuses</subject><subject>Gestation</subject><subject>Hormones</subject><subject>Human health and pathology</subject><subject>Hypothyroidism</subject><subject>Hypothyroidism - immunology</subject><subject>Immune response</subject><subject>Immunological memory</subject><subject>Life Sciences</subject><subject>Lung - immunology</subject><subject>Lung - microbiology</subject><subject>Lungs</subject><subject>Lymphocytes B</subject><subject>Memory cells</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neutrophils - physiology</subject><subject>Offspring</subject><subject>Pneumococcal Infections - immunology</subject><subject>Pneumonia</subject><subject>Pneumonia, Pneumococcal - immunology</subject><subject>Pregnancy</subject><subject>Prenatal Exposure Delayed Effects - immunology</subject><subject>Prenatal Exposure Delayed Effects - microbiology</subject><subject>Sepsis</subject><subject>Sepsis - immunology</subject><subject>Sepsis - microbiology</subject><subject>Streptococcus infections</subject><subject>Streptococcus pneumoniae</subject><subject>Thyroid</subject><subject>Thyroid gland</subject><subject>Thyroid hormones</subject><issn>0013-7227</issn><issn>1945-7170</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk9r3DAQxU1pabZpbz0XQQ_poU41kmXZx2XpZhcWEvrnLGR53HWwJVeyA_tl-lkrZzcJlJaexMBvnt7MvCR5C_QSGNBPaC8ZBZFCKeSzZAFlJlIJkj5PFpQCTyVj8ix5FcJtLLMs4y-TMyYpF7lgi-TXFYZRj62zuiObw-DG_cG7tm5DT7b94N0dBjLukSyrtmvHA3HNfbnGXndIrpsmDL61P8joyKpD7cnX0eMwOuOMmQIZLE69s61GsrUNmvknom0981_QRHlP1t715OYenLuikZuHrtfJi0Z3Ad-c3vPk-_rzt9Um3V1fbVfLXWoE5WOaZboGXuUVYwaxoE1T5xo4Z5pKKUReUKoboKLKGUWeczDc1NxUdcWNlFDx8-TjUXevOxUH6rU_KKdbtVnuVGsD-l5RBlkJWXEHEf9wxOOCfk5xg6pvg8Gu0xbdFBQUJRQFk6X8PypLXlIqgEX0_R_orZt8PExQHDiVVLBMPlk13oXgsXn0C1TNiVBo1ZwINSci4u9OolPVY_0IP0QgAhdHwE3Dv6TSkxQ_kmhrZ-LVcfAYwpPLvxr4DQ3bz2I</recordid><startdate>201606</startdate><enddate>201606</enddate><creator>Nieto, Pamela A</creator><creator>Peñaloza, Hernán F</creator><creator>Salazar-Echegarai, Francisco J</creator><creator>Castellanos, Raquel M</creator><creator>Opazo, Maria Cecilia</creator><creator>Venegas, Luis</creator><creator>Padilla, Oslando</creator><creator>Kalergis, Alexis M</creator><creator>Riedel, Claudia A</creator><creator>Bueno, Susan M</creator><general>Endocrine Society</general><general>Oxford University Press</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>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TM</scope><scope>7TO</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>7QL</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0001-7622-5263</orcidid></search><sort><creationdate>201606</creationdate><title>Gestational Hypothyroidism Improves the Ability of the Female Offspring to Clear Streptococcus pneumoniae Infection and to Recover From Pneumococcal Pneumonia</title><author>Nieto, Pamela A ; Peñaloza, Hernán F ; Salazar-Echegarai, Francisco J ; Castellanos, Raquel M ; Opazo, Maria Cecilia ; Venegas, Luis ; Padilla, Oslando ; Kalergis, Alexis M ; Riedel, Claudia A ; Bueno, Susan M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c503t-44ad13b6b22cee80ffd6a1332a077556800af105b620e3631c3cd3cbdb3c771b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Bacteria</topic><topic>Bacterial diseases</topic><topic>Bacterial infections</topic><topic>Blood</topic><topic>Brain</topic><topic>Brain - immunology</topic><topic>Brain - microbiology</topic><topic>Cell survival</topic><topic>Central nervous system</topic><topic>Disease Models, Animal</topic><topic>Disease Resistance - immunology</topic><topic>Female</topic><topic>Females</topic><topic>Fetuses</topic><topic>Gestation</topic><topic>Hormones</topic><topic>Human health and pathology</topic><topic>Hypothyroidism</topic><topic>Hypothyroidism - immunology</topic><topic>Immune response</topic><topic>Immunological memory</topic><topic>Life Sciences</topic><topic>Lung - immunology</topic><topic>Lung - microbiology</topic><topic>Lungs</topic><topic>Lymphocytes B</topic><topic>Memory cells</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Neutrophils - physiology</topic><topic>Offspring</topic><topic>Pneumococcal Infections - immunology</topic><topic>Pneumonia</topic><topic>Pneumonia, Pneumococcal - immunology</topic><topic>Pregnancy</topic><topic>Prenatal Exposure Delayed Effects - immunology</topic><topic>Prenatal Exposure Delayed Effects - microbiology</topic><topic>Sepsis</topic><topic>Sepsis - immunology</topic><topic>Sepsis - microbiology</topic><topic>Streptococcus infections</topic><topic>Streptococcus pneumoniae</topic><topic>Thyroid</topic><topic>Thyroid gland</topic><topic>Thyroid hormones</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nieto, Pamela A</creatorcontrib><creatorcontrib>Peñaloza, Hernán F</creatorcontrib><creatorcontrib>Salazar-Echegarai, Francisco J</creatorcontrib><creatorcontrib>Castellanos, Raquel M</creatorcontrib><creatorcontrib>Opazo, Maria Cecilia</creatorcontrib><creatorcontrib>Venegas, Luis</creatorcontrib><creatorcontrib>Padilla, Oslando</creatorcontrib><creatorcontrib>Kalergis, Alexis M</creatorcontrib><creatorcontrib>Riedel, Claudia A</creatorcontrib><creatorcontrib>Bueno, Susan M</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Endocrinology (Philadelphia)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nieto, Pamela A</au><au>Peñaloza, Hernán F</au><au>Salazar-Echegarai, Francisco J</au><au>Castellanos, Raquel M</au><au>Opazo, Maria Cecilia</au><au>Venegas, Luis</au><au>Padilla, Oslando</au><au>Kalergis, Alexis M</au><au>Riedel, Claudia A</au><au>Bueno, Susan M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gestational Hypothyroidism Improves the Ability of the Female Offspring to Clear Streptococcus pneumoniae Infection and to Recover From Pneumococcal Pneumonia</atitle><jtitle>Endocrinology (Philadelphia)</jtitle><addtitle>Endocrinology</addtitle><date>2016-06</date><risdate>2016</risdate><volume>157</volume><issue>6</issue><spage>2217</spage><epage>2228</epage><pages>2217-2228</pages><issn>0013-7227</issn><eissn>1945-7170</eissn><abstract>Maternal thyroid hormones are essential for proper fetal development. A deficit of these hormones during gestation has enduring consequences in the central nervous system of the offspring, including detrimental learning and impaired memory. Few studies have shown that thyroid hormone deficiency has a transient effect in the number of T and B cells in the offspring gestated under hypothyroidism; however, there are no studies showing whether maternal hypothyroidism during gestation impacts the response of the offspring to infections. In this study, we have evaluated whether adult mice gestated in hypothyroid mothers have an altered response to pneumococcal pneumonia. We observed that female mice gestated in hypothyroidism have increased survival rate and less bacterial dissemination to blood and brain after an intranasal challenge with Streptococcus pneumoniae. Further, these mice had higher amounts of inflammatory cells in the lungs and reduced production of cytokines characteristic of sepsis in spleen, blood, and brain at 48 hours after infection. Interestingly, mice gestated in hypothyroid mothers had basally increased vascular permeability in the lungs. These observations suggest that gestational hypothyroidism alters the immune response and the physiology of lungs in the offspring, increasing the resistance to respiratory bacterial infections.</abstract><cop>United States</cop><pub>Endocrine Society</pub><pmid>27035652</pmid><doi>10.1210/en.2015-1957</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-7622-5263</orcidid><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Journals@Ovid Complete; Oxford University Press Journals All Titles (1996-Current); Alma/SFX Local Collection |
subjects | Animals Bacteria Bacterial diseases Bacterial infections Blood Brain Brain - immunology Brain - microbiology Cell survival Central nervous system Disease Models, Animal Disease Resistance - immunology Female Females Fetuses Gestation Hormones Human health and pathology Hypothyroidism Hypothyroidism - immunology Immune response Immunological memory Life Sciences Lung - immunology Lung - microbiology Lungs Lymphocytes B Memory cells Mice Mice, Inbred C57BL Neutrophils - physiology Offspring Pneumococcal Infections - immunology Pneumonia Pneumonia, Pneumococcal - immunology Pregnancy Prenatal Exposure Delayed Effects - immunology Prenatal Exposure Delayed Effects - microbiology Sepsis Sepsis - immunology Sepsis - microbiology Streptococcus infections Streptococcus pneumoniae Thyroid Thyroid gland Thyroid hormones |
title | Gestational Hypothyroidism Improves the Ability of the Female Offspring to Clear Streptococcus pneumoniae Infection and to Recover From Pneumococcal Pneumonia |
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