Intrauterine inflammation induces sex-specific effects on neuroinflammation, white matter, and behavior

Makinson, Ryan; Lloyd, Kelsey; Rayasam, Aditya; McKee, Sarah; Brown, Amy; Barila, Guillermo; Grissom, Nicola; George, Robert; Marini, Matt; Fabry, Zsuzsanna; Elovitz, Michal; Reyes, Teresa M.

doi:10.1016/j.bbi.2017.07.016

Cited by 67Neuroinflammation and Neurodegeneration MechanismsTryptophan and brain disordersNeonatal and fetal brain pathology

Intrauterine inflammation induces sex-specific effects on neuroinflammation, white matter, and behavior

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Makinson, Ryan, Lloyd, Kelsey, Rayasam, Aditya, McKee, Sarah, Brown, Amy, Barila, Guillermo, Grissom, Nicola, George, Robert +4 more·2017·Brain Behavior and Immunity

DOI 10.1016/j.bbi.2017.07.016PMC PMC6916731

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Abstract

Exposure to inflammation during pregnancy has been linked to adverse neurodevelopmental consequences for the offspring. One common route through which a developing fetus is exposed to inflammation is with intrauterine inflammation. To that end, we utilized an animal model of intrauterine inflammation (IUI; intrauterine lipopolysaccharide (LPS) administration, 50µg, E15) to assess placental and fetal brain inflammatory responses, white matter integrity, anxiety-related behaviors (elevated zero maze, light dark box, open field), microglial counts, and the CNS cytokine response to an acute injection of LPS in both males and females. These studies revealed that for multiple endpoints (fetal brain cytokine levels, cytokine response to adult LPS challenge) male IUI offspring were uniquely affected by intrauterine inflammation, while for other endpoints (behavior, microglial number) both sexes were similarly affected. These data advance our understanding of sex-specific effects of early life exposure to inflammation in a translationally- relevant model.

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Animal models of systemic prenatal infection induce anxiety-like behavior alterations in offspring.
“These animal models of systemic prenatal infection induce changes in neurobehavioral development consistent with human psychopathology including alterations in offspring anxiety-like behavior (Arsenault et al., 2014; Makinson et al., 2017; Penteado et al., 2014; Schaafsma, W. et al., 2017)”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Makinson et al., 2017

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Neuroinflammation as a risk factor for attention deficit hyperactivity disorder
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Authors: Makinson, R., Lloyd, K., Rayasam, A., McKee, S., Brown, A., Barila, G., Grissom, N., George, R., Marini, M., Fabry, Z., Elovitz, M., & Reyes, T. M.
Affiliations: University of Cincinnati (US)
University of Wisconsin–Madison (US)
University of Pennsylvania (US)
Corresponding author: Reyes, Teresa M.
ORCID: Makinson, Ryan
Lloyd, Kelsey
Rayasam, Aditya
Brown, Amy
Grissom, Nicola
Elovitz, Michal
Reyes, Teresa M.
Venue: Brain Behavior and Immunity
Publisher: Elsevier BV
Published: 2017-11
Volume: 66
Pages: 277-288
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2017.07.016
PMC: PMC6916731
OpenAlex: W2738244128
Cited by: 67
References: 83
Citations by year: 2026: 4 · 2025: 3 · 2024: 5 · 2023: 5 · 2022: 10 · 2021: 9 · 2020: 8 · 2019: 13 · 2018: 9 · 2017: 1
FWCI: 4.23
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH087978, R21MH100828)
National Institute of General Medical Sciences (T32GM007507)
National Institute of Neurological Disorders and Stroke (R01NS037570, R56NS037570)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD076032)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
Keywords: intrauterine inflammation, lipopolysaccharide, sex differences, neuroinflammation, white matter integrity, anxiety-like behavior, microglia, placental inflammation, brain development
MeSH terms: Animals, Behavior, Animal, Brain, Disease Models, Animal, Encephalitis, Female, Inflammation, Lipopolysaccharides, Placenta, Pregnancy, Pregnancy Complications, Sex Characteristics, Uterine Diseases, Mice, White Matter

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Intrauterine inflammation induces sex-specific effects on neuroinflammation, white matter, and behavior

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