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Featured ArticleArticles, Behavioral/Cognitive

Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation

Ali B. Rodgers, Christopher P. Morgan, Stefanie L. Bronson, Sonia Revello and Tracy L. Bale
Journal of Neuroscience 22 May 2013, 33 (21) 9003-9012; DOI: https://doi.org/10.1523/JNEUROSCI.0914-13.2013
Ali B. Rodgers
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Christopher P. Morgan
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Stefanie L. Bronson
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Sonia Revello
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Tracy L. Bale
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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  • Figure 1.
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    Figure 1.

    Paternal stress experienced throughout puberty or in adulthood elicited stress dysregulation in offspring. A, B, Both male (A) and female (B) offspring of sires that had been exposed to chronic stress throughout puberty or only in adulthood produced less corticosterone relative to offspring of control sires following a 15 min restraint (shaded column). Total AUC of corticosterone production (shown in the inset) showed a significant decrease in both stress groups relative to controls. An expected sex difference in corticosterone production was observed, with females showing a greater response than males. Data are presented as mean ± SEM. n = 6–9 litters per group. *p < 0.05.

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    Figure 2.

    Paternal stress does not alter offspring performance in behavioral assessments or HPA response to an SSRI. A, B, Neither male (A) nor female (B) offspring of stressed sires showed altered PPI of the acoustic startle response compared to control offspring. C, PPI max startle was also unchanged by paternal stress in both sexes. D, No significant differences in time spent immobile on the tail suspension test were observed between control and paternally stressed male or female offspring. E, F, In the Barnes maze spatial learning and memory task, no differences were detected in the latency to learn the task. G, H, In the light–dark box, no treatment group differences were detected for time spent in the light or transitions between the compartments. There was an overall effect of females spending more time in the light compartment than males. I, J, Following administration of an SSRI, citalopram, at time 0 (black arrow), male and female offspring of stressed or control sires exhibited similar stress reactivity. Total AUC of corticosterone production (shown in the inset) did not vary with sex or paternal stress group. Data are presented as mean ± SEM. n = 5–9 litters per group. *p < 0.05.

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    Figure 3.

    Stress axis-related gene expression in offspring pituitary and adrenal glands was not significantly different between control (C), pubertal stress (P), or adult stress (A) groups. A–D, Real-time PCR analysis revealed no effect of paternal stress on pituitary CRFr1 (A), POMC (B), adrenal Mc2r (C), or 11βHSD-1 (D). Sex differences were observed, with males showing higher expression of CRFr1 and 11βHSD-1 and lower expression of Mc2r and POMC relative to females. Data are presented as mean ± SEM. n = 6–8 litters per group. **p < 0.001; ***p < 0.0001.

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    Figure 4.

    Paternal stress experienced throughout puberty or in adulthood produced robust changes in sperm miR content. A, Hierarchical clustering of sperm miR expression isolated a single clade containing all pubertal and adult stress males, and no controls (bolded red line). n = 4 per group. B, Analyses of significant differences in expression of specific miRs revealed nine that were significantly increased in both paternal stress groups. Data are presented as mean ± SEM. *p < 0.05, different from controls; #p < 0.05, different from pubertal stress.

Tables

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    Table 1.

    Summary of gene sets meeting GSEA enrichment criteria of FDR ≤ 0.25, p ≤ 0.01, and NES ≥ 1.6

    TotalPVN (enriched)BNST (enriched)
    c2 (curated)3050 (0.0%)0 (0.0%)
    c3 (motif)77616 (2.1%)114 (14.7%)
    c5 (gene ontology)9690 (0.0%)6 (<1%)
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    Table 2.

    Gene sets enriched in offspring PVN following paternal stress

    Gene setTypeSizeNESpFDR
    NR3CI (GR)c3107−1.6830.0080.235
    CEBPdeltac3212−1.6820.0010.220
    FOXD3c3178−1.6820.0060.207
    miR-522c3144−1.6780.0080.203
    NKX2–5c3109−1.6650.0080.196
    PAX8c388−1.6610.0040.194
    TITF1c3212−1.6570.0020.194
    PIT1c3195−1.6490.0100.201
    DDIT3c3209−1.6410.0040.200
    NFIc3226−1.6330.0010.193
    FOXI3c3165−1.6250.0100.193
    IPFIc3220−1.6170.0010.190
    ARc3227−1.6060.0020.203
    • Members of c3 gene sets share a binding motif for the designated transcription factor or miR. Gene sets defined by conserved sequence only and those not meeting the criteria NES ≥ 1.6, p ≤ 0.01, and FDR ≤ 0.25 were omitted.

  • Table 3.
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    Table 3.

    Gene sets enriched in offspring BNST following paternal stress

    • Members of c3 gene sets share a binding motif for designated transcription factor or miRNA. c3 gene sets sharing the same name represent distinct binding sites for the transcription factor or miR given. Members of c5 gene sets share common ontolgy and do not necessarily represent coregulated genes. Gene sets defined by conserved sequence only and those not meeting the criteria NES ≥ 1.6, p ≤ 0.01, and FDR ≤ 0.25 were omitted. HAT, Histone acetyltransferase.

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    Table 4.

    Common predicted gene targets of the nine identified sperm miRNAs

    • Gray boxes indicate that the given gene was a predicted miR target in miRanda, miRDB, miRwalk, and TargetScan alorigthms. Asterisks denote a predicted function in chromatin regulation, DNA methylation, or miR processing.

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The Journal of Neuroscience: 33 (21)
Journal of Neuroscience
Vol. 33, Issue 21
22 May 2013
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Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation
Ali B. Rodgers, Christopher P. Morgan, Stefanie L. Bronson, Sonia Revello, Tracy L. Bale
Journal of Neuroscience 22 May 2013, 33 (21) 9003-9012; DOI: 10.1523/JNEUROSCI.0914-13.2013

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Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation
Ali B. Rodgers, Christopher P. Morgan, Stefanie L. Bronson, Sonia Revello, Tracy L. Bale
Journal of Neuroscience 22 May 2013, 33 (21) 9003-9012; DOI: 10.1523/JNEUROSCI.0914-13.2013
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