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Cited by 102Stress Responses and CortisolBirth, Development, and HealthMaternal Mental Health During Pregnancy and Postpartum

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Programming of stress-related behavior and epigenetic neural gene regulation in mice offspring through maternal exposure to predator odor

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St-Cyr, Sophie, McGowan, Patrick O.·2015·Frontiers in Behavioral Neuroscience
DOI 10.3389/fnbeh.2015.00145PMC PMC4450170
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Abstract

Perinatal stress mediated through the mother can lead to long-term alterations in stress-related phenotypes in offspring. The capacity for adaptation to adversity in early life depends in part on the life history of the animal. This study was designed to examine the behavioral and neural response in adult offspring to prenatal exposure to predator odor: an ethologically-relevant psychological stressor. Pregnant mice were exposed daily to predator odors or distilled water control over the second half of the pregnancy. Predator odor exposure lead to a transient decrease in maternal care in the mothers. As adults, the offspring of predator odor-exposed mothers showed increased anti-predator behavior, a predator-odor induced decrease in activity and, in female offspring, an increased corticosterone (CORT) response to predator odor exposure. We found a highly specific response among stress-related genes within limbic brain regions. Transcript abundance of Corticotropin-releasing hormone receptor 1 (CRHR1) was elevated in the amygdala in adult female offspring of predator odor-exposed mothers. In the hippocampus of adult female offspring, decreased Brain-derived neurotrophic factor (BDNF) transcript abundance was correlated with a site-specific decrease in DNA methylation in Bdnf exon IV, indicating the potential contribution of this epigenetic mechanism to maternal programming by maternal predator odor exposure. These data indicate that maternal predator odor exposure alone is sufficient to induce an altered stress-related phenotype in adulthood, with implications for anti-predator behavior in offspring.

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Figure 1 Preliminary testing in adult females showing (A) bobcat (3 mL) and coyote (5 mL) urine elicited avoidance of the predator odor source relative to distilled water control and (B) elevated basal CORT levels after a week of unpredictable 1 h daily predator odor exposure. Data are average ± SEM. Predator Odor (PO); Control (C). *P ≤ 0.05, effect of predator odor exposure.
Figure 1 Preliminary testing in adult females showing (A) bobcat (3 mL) and coyote (5 mL) urine elicited avoidance of the predator odor source relative to distilled water control and (B) elevated basal CORT levels after a week of unpredictable 1 h daily predator odor exposure. Data are average ± SEM. Predator Odor (PO); Control (C). *P ≤ 0.05, effect of predator odor exposure.CC BY · PubMed Central
Figure 2 Maternal behavior in predator odor exposed (PO) and control (C) dams, showing the proportion of time spent licking the pups. Data are average ± SEM. *P ≤ 0.05, effect of predator odor exposure.
Figure 2 Maternal behavior in predator odor exposed (PO) and control (C) dams, showing the proportion of time spent licking the pups. Data are average ± SEM. *P ≤ 0.05, effect of predator odor exposure.CC BY · PubMed Central
Figure 3 Adult offspring from dams exposed to predator odor during pregnancy (PO) show increased avoidance and decreased predator-odor associated activity compared to control (C) adult offspring. M, male; F, female. (A) Predator odor exposure setup. Representative 30-min. tracing of locomotor activity from (B) control and (C) maternal predator odor-exposed adult offspring. (D) Average distance to the predator odor and (E) overall distance travelled. Data are average ± SEM. Bars, *P ≤ 0.05, ***P ≤ 0.001, main effect of maternal predator odor exposure; #P ≤ 0.10, *P ≤ 0.05, **P ≤ 0.01 post hoc comparison within sex.
Figure 3 Adult offspring from dams exposed to predator odor during pregnancy (PO) show increased avoidance and decreased predator-odor associated activity compared to control (C) adult offspring. M, male; F, female. (A) Predator odor exposure setup. Representative 30-min. tracing of locomotor activity from (B) control and (C) maternal predator odor-exposed adult offspring. (D) Average distance to the predator odor and (E) overall distance travelled. Data are average ± SEM. Bars, *P ≤ 0.05, ***P ≤ 0.001, main effect of maternal predator odor exposure; #P ≤ 0.10, *P ≤ 0.05, **P ≤ 0.01 post hoc comparison within sex.CC BY · PubMed Central
Figure 4 Adult offspring from dams exposed to predator odor during pregnancy (PO) show an altered predator odor-challenged levels of CORT to a predator odor compared to control (C) adult offspring. M, male; F, female. The black line shows the duration of the predator odor exposure. Data are average ± SEM. *P ≤ 0.05, post hoc comparison within female offspring.
Figure 4 Adult offspring from dams exposed to predator odor during pregnancy (PO) show an altered predator odor-challenged levels of CORT to a predator odor compared to control (C) adult offspring. M, male; F, female. The black line shows the duration of the predator odor exposure. Data are average ± SEM. *P ≤ 0.05, post hoc comparison within female offspring.CC BY · PubMed Central
Figure 5 Prenatal exposure to predator odor leads to differences in transcript abundance in the hippocampus and amygdala of the adult offspring. C, control; PO, offspring of predator odor exposed dams. Respectively, hippocampal and amygdala BDNF (A) and CRHR1 (B) transcript relative abundance corrected using YWHAZ transcript level. Data are average ± SEM. Bars, *P ≤ 0.05, main effect of maternal predator odor exposure; *P ≤ 0.05, post hoc comparison within sex.
Figure 5 Prenatal exposure to predator odor leads to differences in transcript abundance in the hippocampus and amygdala of the adult offspring. C, control; PO, offspring of predator odor exposed dams. Respectively, hippocampal and amygdala BDNF (A) and CRHR1 (B) transcript relative abundance corrected using YWHAZ transcript level. Data are average ± SEM. Bars, *P ≤ 0.05, main effect of maternal predator odor exposure; *P ≤ 0.05, post hoc comparison within sex.CC BY · PubMed Central
Figure 6 DNA methyation level of the Bdnf exon IV in the hippocampus of female offspring of predator odor exposed (PO) and control (C) dams. (A) Region sequenced with transcription initiation site (bent arrow) and CpG sites. (B) DNA methylation level (%) of the 4 sequenced CpG sites. (C) Correlation between the hippocampal BDNF expression and the hippocampal Bdnf exon IV CpG3 methylation level (%) (P = 0.03). Data are average ± SEM. *P ≤ 0.05, effect of maternal predator odor.
Figure 6 DNA methyation level of the Bdnf exon IV in the hippocampus of female offspring of predator odor exposed (PO) and control (C) dams. (A) Region sequenced with transcription initiation site (bent arrow) and CpG sites. (B) DNA methylation level (%) of the 4 sequenced CpG sites. (C) Correlation between the hippocampal BDNF expression and the hippocampal Bdnf exon IV CpG3 methylation level (%) (P = 0.03). Data are average ± SEM. *P ≤ 0.05, effect of maternal predator odor.CC BY · PubMed Central

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Metadata

Authors
St-Cyr, S., & McGowan, P. O.
Affiliations
University of Toronto (CA)
Corresponding author
McGowan, Patrick O.
ORCID
Venue
Frontiers in Behavioral Neuroscience
Publisher
Frontiers Media SA
Published
2015-06-01
Volume
9
Pages
145-145
ISSN
1662-5153 (ISSN-L)
DOI
10.3389/fnbeh.2015.00145
PMC
PMC4450170
OpenAlex
W1494806802
Cited by
102
References
51
Citations by year
2026: 3 · 2025: 7 · 2024: 8 · 2023: 9 · 2022: 6 · 2021: 11 · 2020: 13 · 2019: 16 · 2018: 5 · 2017: 12 · 2016: 11 · 2015: 1
FWCI
5.03
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (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)
Funders
Natural Sciences and Engineering Research Council of Canada
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Keywords
prenatal stress, maternal programming, predator odor, antipredator behavior, maternal care, CRHR1, brain-derived neurotrophic factor, DNA methylation, epigenetic regulation, amygdala, hippocampus, limbic system, life history

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