Maternal viral infection causes global alterations in porcine fetal microglia

Maternal infections during pregnancy are associated with increased risk of neurodevelopmental disorders, although the precise mechanisms remain to be elucidated. Previously, we established a maternal immune activation (MIA) model using swine, which results in altered social behaviors of piglet offsp...

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Published in	Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 40; pp. 20190 - 20200
Main Authors	Antonson, Adrienne M., Lawson, Marcus A., Caputo, Megan P., Matt, Stephanie M., Leyshon, Brian J., Johnson, Rodney W.
Format	Journal Article
Language	English
Published	United States National Academy of Sciences 01.10.2019
Series	PNAS Plus
Subjects	Abnormalities Amygdala Animals Behavior, Animal Biological Sciences Brain Chemotactic response Disease Models, Animal Female Fetal Diseases - etiology Fetal Diseases - metabolism Fetuses Gene expression Immune response Infections Livestock Major histocompatibility complex Microglia Neurodevelopmental disorders Neurons - metabolism Neurotransmitter Agents - metabolism Offspring Phagocytes PNAS Plus Pregnancy Pregnancy Complications, Infectious - veterinary Priming Swine Swine Diseases - virology Viral infections Virus Diseases - veterinary Viruses maternal immune activation neurodevelopment microglia pig prenatal inflammation
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Abstract	Maternal infections during pregnancy are associated with increased risk of neurodevelopmental disorders, although the precise mechanisms remain to be elucidated. Previously, we established a maternal immune activation (MIA) model using swine, which results in altered social behaviors of piglet offspring. These behavioral abnormalities occurred in the absence of microglia priming. Thus, we examined fetal microglial activity during prenatal development in response to maternal infection with live porcine reproductive and respiratory syndrome virus. Fetuses were obtained by cesarean sections performed 7 and 21 d postinoculation (dpi). MIA fetuses had reduced brain weights at 21 dpi compared to controls. Furthermore, MIA microglia increased expression of major histocompatibility complex class II that was coupled with reduced phagocytic and chemotactic activity compared to controls. High-throughput gene-expression analysis of microglial-enriched genes involved in neurodevelopment, the microglia sensome, and inflammation revealed differential regulation in primary microglia and in whole amygdala tissue. Microglia density was increased in the fetal amygdala at 7 dpi. Our data also reveal widespread sexual dimorphisms in microglial gene expression and demonstrate that the consequences of MIA are sex dependent. Overall, these results indicate that fetal microglia are significantly altered by maternal viral infection, presenting a potential mechanism through which MIA impacts prenatal brain development and function.
AbstractList	Maternal infections during pregnancy are associated with increased risk of neurodevelopmental disorders, although the precise mechanisms remain to be elucidated. Previously, we established a maternal immune activation (MIA) model using swine, which results in altered social behaviors of piglet offspring. These behavioral abnormalities occurred in the absence of microglia priming. Thus, we examined fetal microglial activity during prenatal development in response to maternal infection with live porcine reproductive and respiratory syndrome virus. Fetuses were obtained by cesarean sections performed 7 and 21 d postinoculation (dpi). MIA fetuses had reduced brain weights at 21 dpi compared to controls. Furthermore, MIA microglia increased expression of major histocompatibility complex class II that was coupled with reduced phagocytic and chemotactic activity compared to controls. High-throughput gene-expression analysis of microglial-enriched genes involved in neurodevelopment, the microglia sensome, and inflammation revealed differential regulation in primary microglia and in whole amygdala tissue. Microglia density was increased in the fetal amygdala at 7 dpi. Our data also reveal widespread sexual dimorphisms in microglial gene expression and demonstrate that the consequences of MIA are sex dependent. Overall, these results indicate that fetal microglia are significantly altered by maternal viral infection, presenting a potential mechanism through which MIA impacts prenatal brain development and function. Mental health disorders account for approximately 14% of the worldwide burden of disease and affect people of all age groups and socioeconomic statuses. Prenatal exposure to maternal infection increases the risk of developing certain mental health disorders, most notably schizophrenia and autism. Maternally derived cytokines, up-regulated during infection, may lead to an aberrant proinflammatory and phagocytic shift in fetal microglia, the resident immune cells of the brain. As these cells perform essential processes that aid in the highly orchestrated progression of brain development, modifications in their prenatal phenotype could be detrimental. Using swine, a highly translatable animal model, we show that fetal microglia activity is globally altered by maternal infection, a finding that could have far-reaching implications for neuropsychiatric disorders. Maternal infections during pregnancy are associated with increased risk of neurodevelopmental disorders, although the precise mechanisms remain to be elucidated. Previously, we established a maternal immune activation (MIA) model using swine, which results in altered social behaviors of piglet offspring. These behavioral abnormalities occurred in the absence of microglia priming. Thus, we examined fetal microglial activity during prenatal development in response to maternal infection with live porcine reproductive and respiratory syndrome virus. Fetuses were obtained by cesarean sections performed 7 and 21 d postinoculation (dpi). MIA fetuses had reduced brain weights at 21 dpi compared to controls. Furthermore, MIA microglia increased expression of major histocompatibility complex class II that was coupled with reduced phagocytic and chemotactic activity compared to controls. High-throughput gene-expression analysis of microglial-enriched genes involved in neurodevelopment, the microglia sensome, and inflammation revealed differential regulation in primary microglia and in whole amygdala tissue. Microglia density was increased in the fetal amygdala at 7 dpi. Our data also reveal widespread sexual dimorphisms in microglial gene expression and demonstrate that the consequences of MIA are sex dependent. Overall, these results indicate that fetal microglia are significantly altered by maternal viral infection, presenting a potential mechanism through which MIA impacts prenatal brain development and function.
Author	Caputo, Megan P. Leyshon, Brian J. Lawson, Marcus A. Johnson, Rodney W. Matt, Stephanie M. Antonson, Adrienne M.
Author_xml	– sequence: 1 givenname: Adrienne M. surname: Antonson fullname: Antonson, Adrienne M. – sequence: 2 givenname: Marcus A. surname: Lawson fullname: Lawson, Marcus A. – sequence: 3 givenname: Megan P. surname: Caputo fullname: Caputo, Megan P. – sequence: 4 givenname: Stephanie M. surname: Matt fullname: Matt, Stephanie M. – sequence: 5 givenname: Brian J. surname: Leyshon fullname: Leyshon, Brian J. – sequence: 6 givenname: Rodney W. surname: Johnson fullname: Johnson, Rodney W.
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by Christopher A. Walsh, Children’s Hospital Boston, Boston, MA, and approved August 27, 2019 (received for review October 9, 2018) Author contributions: A.M.A., M.A.L., and R.W.J. designed research; A.M.A., M.A.L., M.P.C., S.M.M., and B.J.L. performed research; A.M.A., M.P.C., and S.M.M. analyzed data; A.M.A., M.A.L., and R.W.J. interpreted data; and A.M.A. wrote the paper.
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Snippet	Maternal infections during pregnancy are associated with increased risk of neurodevelopmental disorders, although the precise mechanisms remain to be... Mental health disorders account for approximately 14% of the worldwide burden of disease and affect people of all age groups and socioeconomic statuses....
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SubjectTerms	Abnormalities Amygdala Animals Behavior, Animal Biological Sciences Brain Chemotactic response Disease Models, Animal Female Fetal Diseases - etiology Fetal Diseases - metabolism Fetuses Gene expression Immune response Infections Livestock Major histocompatibility complex Microglia Neurodevelopmental disorders Neurons - metabolism Neurotransmitter Agents - metabolism Offspring Phagocytes PNAS Plus Pregnancy Pregnancy Complications, Infectious - veterinary Priming Swine Swine Diseases - virology Viral infections Virus Diseases - veterinary Viruses
Title	Maternal viral infection causes global alterations in porcine fetal microglia
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