Enhanced cerebellar myelination with concomitant iron elevation and ultrastructural irregularities following prenatal exposure to ambient particulate matter in the mouse

Klocke, Carolyn; Sherina, Valeriia; Graham, Uschi M.; Gunderson, Jakob; Allen, Joshua L.; Sobolewski, Marissa; Blum, Jason L.; Zelikoff, Judith T.; Cory-Slechta, Deborah A.

doi:10.1080/08958378.2018.1533053

Cited by 41Air Quality and Health ImpactsAutism Spectrum Disorder ResearchHeavy Metal Exposure and Toxicity

Enhanced cerebellar myelination with concomitant iron elevation and ultrastructural irregularities following prenatal exposure to ambient particulate matter in the mouse

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Klocke, Carolyn, Sherina, Valeriia, Graham, Uschi M., Gunderson, Jakob, Allen, Joshua L., Sobolewski, Marissa, Blum, Jason L., Zelikoff, Judith T. +1 more·2018·Inhalation Toxicology

DOI 10.1080/08958378.2018.1533053PMC PMC6400059

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Abstract

Accumulating evidence indicates the developing central nervous system (CNS) is a target of air pollution toxicity. Epidemiological reports increasingly demonstrate that exposure to the particulate matter (PM) fraction of air pollution during neurodevelopment is associated with an increased risk of neurodevelopmental disorders (NDDs) such as autism spectrum disorder (ASD). These observations are supported by animal studies demonstrating prenatal exposure to concentrated ambient PM induces neuropathologies characteristic of ASD, including ventriculomegaly and aberrant corpus callosum (CC) myelination. Given the role of the CC and cerebellum in ASD etiology, this study tested whether prenatal exposure to concentrated ambient particles (CAPs) produced pathological features in offspring CC and cerebella consistent with ASD. Analysis of cerebellar myelin density revealed male-specific hypermyelination in CAPs-exposed offspring at postnatal days (PNDs) 11-15 without alteration of cerebellar area. Atomic absorption spectroscopy (AAS) revealed elevated iron (Fe) in the cerebellum of CAPs-exposed female offspring at PNDs 11-15, which connects with previously observed elevated Fe in the female CC. The presence of Fe inclusions, along with aluminum (Al) and silicon (Si) inclusions, were confirmed at nanoscale resolution in the CC along with ultrastructural myelin sheath damage. Furthermore, RNAseq and gene ontology (GO) enrichment analyses revealed cerebellar gene expression was significantly affected by sex and prenatal CAPs exposure with significant enrichment in inflammation and transmembrane transport processes that could underlie observed myelin and metal pathologies. Overall, this study highlights the ability of PM exposure to disrupt myelinogenesis and elucidates novel molecular targets of PM-induced developmental neurotoxicity.

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Prenatal exposure to ultrafine PM increased cerebellum iron concentrations in female offspring.
“Subsequently, Klocke et al. [62] observed a similar increase in cerebellum Fe concentrations in female offspring exposed prenatally.”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [62]
The Results (Cerebellar Fe content; page unavailable) report significantly elevated cerebellar Fe concentration in female offspring after prenatal CAPs exposure. The Materials and methods (Animals and exposures; page unavailable) say CAPs included both PM2.5 and ultrafine particles, so the study does not establish that ultrafine PM specifically caused the increase. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Iron, aluminum, and silicon inclusions presented in the corpus callosum with ultrastructural myelin sheath damage after prenatal ultrafine PM exposure.
“Iron, as well as aluminum and silicon inclusions, also presented in the CC with ultrastructural myelin sheath damage.”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [62]

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Authors: Klocke, C., Sherina, V., Graham, U. M., Gunderson, J., Allen, J. L., Sobolewski, M., Blum, J. L., Zelikoff, J. T., & Cory-Slechta, D. A.
Affiliations: University of Rochester Medicine (US)
University of Kentucky (US)
New York University (US)
Department of Environmental Medicine, University of Rochester School of Medicine, Rochester, NY, USA;
Corresponding author: Klocke, Carolyn
ORCID: Klocke, Carolyn
Graham, Uschi M.
Gunderson, Jakob
Sobolewski, Marissa
Blum, Jason L.
Zelikoff, Judith T.
Venue: Inhalation Toxicology
Publisher: Informa UK Limited
Published: 2018-08-24
Volume: 30
Issue: 9-10
Pages: 381-396
ISSN: 0895-8378 (ISSN-L)
1091-7691
DOI: 10.1080/08958378.2018.1533053
PMC: PMC6400059
OpenAlex: W2906560729
Cited by: 41
References: 104
Citations by year: 2026: 2 · 2025: 1 · 2024: 3 · 2023: 5 · 2022: 9 · 2021: 10 · 2020: 9 · 2019: 2
FWCI: 2.59
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Inhalation Toxicology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Figshare (submittedVersion, cc-by)
Figshare (cc-by)
Funders: National Institutes of Environmental Health Sciences (P30 ES001247, R01 ES025541, T32 ES07026, P30 ES000260, 21-F12-13)
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
Keywords: ambient particulate matter, prenatal air pollution exposure, autism spectrum disorder, developmental neurotoxicity, iron accumulation, metallic inclusions, sex differences, neurodevelopmental disorders
MeSH terms: Air Pollution, Animals, Cerebellum, Corpus Callosum, Female, Iron, Male, Myelin Sheath, Pregnancy, Prenatal Exposure Delayed Effects, Mice, Particulate Matter

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Enhanced cerebellar myelination with concomitant iron elevation and ultrastructural irregularities following prenatal exposure to ambient particulate matter in the mouse

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