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Cited by 123Air Quality and Health ImpactsMaternal Mental Health During Pregnancy and PostpartumNeurogenesis and neuroplasticity mechanisms

The DOI matches its Crossref record; 59 of the 59 references it cites were found in a registry or an index.

Prenatal Exposure to Urban Air Nanoparticles in Mice Causes Altered Neuronal Differentiation and Depression-Like Responses

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Davis, David A., Bortolato, Marco, Godar, Sean C., Sander, Thomas K., Iwata, Nahoko, Pakbin, Payam, Shih, Jean C., Berhane, Kiros, McConnell, Rob, Sioutas, Constantinos, Finch, Caleb E., Morgan, Todd E.·2013·PLoS ONE
DOI 10.1371/journal.pone.0064128PMC PMC3667185
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Abstract

Emerging evidence suggests that excessive exposure to traffic-derived air pollution during pregnancy may increase the vulnerability to neurodevelopmental alterations that underlie a broad array of neuropsychiatric disorders. We present a mouse model for prenatal exposure to urban freeway nanoparticulate matter (nPM). In prior studies, we developed a model for adult rodent exposure to re-aerosolized urban nPM which caused inflammatory brain responses with altered neuronal glutamatergic functions. nPMs are collected continuously for one month from a local freeway and stored as an aqueous suspension, prior to re-aerosolization for exposure of mice under controlled dose and duration. This paradigm was used for a pilot study of prenatal nPM impact on neonatal neurons and adult behaviors. Adult C57BL/6J female mice were exposed to re-aerosolized nPM (350 µg/m(3)) or control filtered ambient air for 10 weeks (3×5 hour exposures per week), encompassing gestation and oocyte maturation prior to mating. Prenatal nPM did not alter litter size, pup weight, or postnatal growth. Neonatal cerebral cortex neurons at 24 hours in vitro showed impaired differentiation, with 50% reduction of stage 3 neurons with long neurites and correspondingly more undifferentiated neurons at Stages 0 and 1. Neuron number after 24 hours of culture was not altered by prenatal nPM exposure. Addition of exogenous nPM (2 µg/ml) to the cultures impaired pyramidal neuron Stage 3 differentiation by 60%. Adult males showed increased depression-like responses in the tail-suspension test, but not anxiety-related behaviors. These pilot data suggest that prenatal exposure to nPM can alter neuronal differentiation with gender-specific behavioral sequelae that may be relevant to human prenatal exposure to urban vehicular aerosols.

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Crossref · 10.1371/journal.pone.0064128

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Figure 1 Prenatal exposure to maternally inhaled nPM impairs postnatal differentiation and neurite initiation in cultured neurons. Cerebral cortex neurons from day 1 pups were grown 24 hours in primary culture. a) Neuronal numbers (median±IQR) did not differ by prenatal nPM inhalation exposure (nPM) vs. filtered room air (CTL). b) Stages of neuron differentiation, green: βIII-tubulin and red: F-actin; scale bar, 10 µm. Prenatal exposure to nPM reduced the proportion of Stage 3 neurons with definitive neurite extension (Stage 3 non-pyramidal & pyramidal, with elongated neurites ≥15 µm)(median±IQR). c) Summary of prenatal nPM effects on neurite elongation: CTL Air, 30% of neurons had neurites ≥15 µm; nPM, 12% of neurons in nPM Air cultures (P<0.0001). N = 5 neuronal cultures/group.
Figure 1 Prenatal exposure to maternally inhaled nPM impairs postnatal differentiation and neurite initiation in cultured neurons. Cerebral cortex neurons from day 1 pups were grown 24 hours in primary culture. a) Neuronal numbers (median±IQR) did not differ by prenatal nPM inhalation exposure (nPM) vs. filtered room air (CTL). b) Stages of neuron differentiation, green: βIII-tubulin and red: F-actin; scale bar, 10 µm. Prenatal exposure to nPM reduced the proportion of Stage 3 neurons with definitive neurite extension (Stage 3 non-pyramidal & pyramidal, with elongated neurites ≥15 µm)(median±IQR). c) Summary of prenatal nPM effects on neurite elongation: CTL Air, 30% of neurons had neurites ≥15 µm; nPM, 12% of neurons in nPM Air cultures (P<0.0001). N = 5 neuronal cultures/group.CC BY · PubMed Central
Figure 2 Postnatal effects of exogenous nPM on Stage 3 neurons in vitro. Data show the median proportions (± IQR) of pyramidal neurons (P) and non-pyramidal neurons (NP) from each postnatal cultures of nPM challenged cells (combining prenatal nPM and control air combined; N = 10 cultures/group). The proportion of Stage 3 pyramidal neurons to all Stage 3 types was reduced from 30% in replicate postnatal control cultures to 12% in cultures exposed to exogenous nPM (P<0.001).
Figure 2 Postnatal effects of exogenous nPM on Stage 3 neurons in vitro. Data show the median proportions (± IQR) of pyramidal neurons (P) and non-pyramidal neurons (NP) from each postnatal cultures of nPM challenged cells (combining prenatal nPM and control air combined; N = 10 cultures/group). The proportion of Stage 3 pyramidal neurons to all Stage 3 types was reduced from 30% in replicate postnatal control cultures to 12% in cultures exposed to exogenous nPM (P<0.001).CC BY · PubMed Central
Figure 3 Prenatal nPM exposure and gender-specific adult behavior. Tail-suspension test. Males, but not females after prenatal nPM exposure exhibited depression-like responses in the lower latency prior to immobility and a longer immobility during suspension. However, nPM females were not affected. Data is expressed as median+IQR, P<0.05, N = 5–10 mice/group.
Figure 3 Prenatal nPM exposure and gender-specific adult behavior. Tail-suspension test. Males, but not females after prenatal nPM exposure exhibited depression-like responses in the lower latency prior to immobility and a longer immobility during suspension. However, nPM females were not affected. Data is expressed as median+IQR, P<0.05, N = 5–10 mice/group.CC BY · PubMed Central

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  1. Crawley JN (2000) What’s wrong with my mouse? New York Wiley-Liss.

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Metadata

Authors
Davis, D. A., Bortolato, M., Godar, S. C., Sander, T. K., Iwata, N., Pakbin, P., Shih, J. C., Berhane, K., McConnell, R., Sioutas, C., Finch, C. E., & Morgan, T. E.
Affiliations
  • University of Southern California (US)
  • University of Kansas (US)
Corresponding author
Finch, Caleb E.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-05-29
Volume
8
Issue
5
Pages
e64128
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0064128
PMC
PMC3667185
OpenAlex
W2102920891
Cited by
123
References
59
Citations by year
2026: 2 · 2025: 3 · 2024: 11 · 2023: 8 · 2022: 14 · 2021: 6 · 2020: 16 · 2019: 9 · 2018: 11 · 2017: 12 · 2016: 11 · 2015: 9 · 2014: 10 · 2013: 1
FWCI
7.58
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • KU ScholarWorks (The University of Kansas) (submittedVersion, cc-by)
Funders
  • National Institutes of Health
  • National Institute on Aging (R21AG040683, R21AG040753, T32AG000037)
  • National Institute of Environmental Health Sciences (P30ES007048)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD070611)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
prenatal air pollution exposure, traffic-related air pollution, neuronal differentiation, cortical neurons, depression-like behavior, anxiety-like behavior, brain development, sex differences, mouse model
MeSH terms
Air Pollutants, Animals, Animals, Newborn, Cell Differentiation, Cells, Cultured, Cities, Depressive Disorder, Female, Hippocampus, Humans, Male, Mice, Inbred C57BL, Neurons, Pilot Projects, Pregnancy, Prenatal Exposure Delayed Effects, Blotting, Western, Neurites, Maze Learning, JNK Mitogen-Activated Protein Kinases, Mice, Particulate Matter, Nanoparticles

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