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Cited by 31Neurotransmitter Receptor Influence on BehaviorNeuropeptides and Animal PhysiologyNeuroscience and Neuropharmacology Research

Sex differences in neuroplasticity- and stress-related gene expression and protein levels in the rat hippocampus following oxycodone conditioned place preference

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Randesi, Matthew, Contoreggi, Natalina H., Zhou, Yan, Rubin, Batsheva R., Bellamy, Julia R., Yu, Fangmin, Gray, Jason D., McEwen, Bruce S. +2 more·2019·Neuroscience
DOI 10.1016/j.neuroscience.2019.04.047PMC PMC7746310
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Abstract

Prescription opioid abuse is a serious public health issue. Recently, we showed that female and male Sprague-Dawley rats acquire conditioned place preference (CPP) to the mu opioid receptor agonist oxycodone. Anatomical analysis of the hippocampus from these rats unveiled sex differences in the opioid system in a way that would support excitation and opiate associative learning processes especially in females. In this study, we examined the expression and protein densities of opioid, plasticity, stress and related kinase and signaling molecules in the hippocampus of female and male rats following oxycodone CPP. Oxycodone CPP females have: a) increases in ARC (activity regulated cytoskeletal-associated protein)-immunoreactivity (ir) in CA3 pyramidal cells; b) decreases in Npy (neuropeptide Y) gene expression in the medial hippocampus but higher numbers of NPY-containing hilar interneurons compared to males; c) increases in Crhr2 (corticotropin releasing factor receptor 2) expression in CA2/3; d) increases in Akt1 (AKT serine/threonine kinase 1) expression in medial hippocampus; and e) decreases in phosphorylated MAPK (mitogen activated protein kinase)-ir in CA1 and dentate gyrus. Oxycodone CPP males have: a) increases in Bdnf (brain derived-neurotrophic factor) expression, which is known to be produced in granule cells, relative to females; b) elevated Mapk1 expression and pMAPK-ir in the dentate hilus which harbors newly generated granule cells; and c) increases in CRHR1-ir in CA3 pyramidal cell soma. These sex-specific changes in plasticity, stress and kinase markers in hippocampal circuitry parallel previously observed sex differences in the opioid system after oxycodone CPP.

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  • The ARC protein is an inducible transcription factor associated with increased synaptic plasticity and is expressed at higher levels in females compared to males.

    “The ARC protein is an inducible transcription factor associated with increased synaptic plasticity and has been reported to be expressed at higher levels in females compared to males (15).”

    From Puberty Blocker, Leuprolide, Reduces Sex Differences in Rough-and-Tumble Play and Anxiety-like Behavior in Juvenile Rats (2024) · cites this paper as [15]

    The Discussion describes Arc as an immediate early gene involved in synaptic plasticity, not as a transcription factor. The Results report higher ARC protein immunoreactivity in females than males in specific rat hippocampal regions and experimental conditions, but do not establish that females generally have higher ARC levels. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Female rats had significantly higher ARC mRNA levels than male rats.

    “Our findings are consistent with previous studies indicating that female rats had significantly higher ARC mRNA levels than male rats (15).”

    From Puberty Blocker, Leuprolide, Reduces Sex Differences in Rough-and-Tumble Play and Anxiety-like Behavior in Juvenile Rats (2024) · cites this paper as [15]

    The Results (Plasticity genes and related proteins) report significantly higher Arc mRNA in saline-treated females than saline-treated males in the lateral hippocampus (p = 0.048). The claim omits those condition and region qualifiers; the Discussion notes that after oxycodone CPP, males’ Arc mRNA rose to levels equivalent to females’. (LLM, conf=0.88)

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Randesi, M., Contoreggi, N. H., Zhou, Y., Rubin, B. R., Bellamy, J. R., Yu, F., Gray, J. D., McEwen, B. S., Milner, T. A., & Kreek, M. J.
Affiliations
  • Rockefeller University (US)
  • Weill Cornell Medicine (US)
Corresponding author
Milner, Teresa A.
ORCID
Venue
Neuroscience
Publisher
Elsevier BV
Published
2019-07
Volume
410
Pages
274-292
ISSN
0306-4522 (ISSN-L)
DOI
10.1016/j.neuroscience.2019.04.047
PMC
PMC7746310
OpenAlex
W2944004946
Cited by
31
References
4
Citations by year
2026: 6 · 2025: 2 · 2024: 4 · 2023: 5 · 2022: 2 · 2021: 7 · 2020: 3 · 2019: 1
FWCI
1.55
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (MH041256, MH102065, HL098351, HL 136520)
  • National Institute on Drug Abuse (DA08259)
  • Hope for Depression Research Foundation
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
sex differences, oxycodone, conditioned place preference, opioid use disorder, hippocampus, neuroplasticity, stress response, mu-opioid receptor, brain-derived neurotrophic factor, neuropeptide Y, corticotropin-releasing factor receptor, AKT1, MAPK signaling, Arc, CA3 pyramidal cells, dentate gyrus, prescription opioid abuse
MeSH terms
Analgesics, Opioid, Animals, Conditioning, Psychological, Female, Hippocampus, Male, Neuronal Plasticity, Oxycodone, Sex Characteristics, Stress, Psychological, Gene Expression, Rats, Sprague-Dawley, Brain-Derived Neurotrophic Factor, Mitogen-Activated Protein Kinase Kinases, Rats

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