Repeated stress exposure in mid-adolescence attenuates behavioral, noradrenergic, and epigenetic effects of trauma-like stress in early adult male rats.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
21 10 2020
Historique:
received: 16 04 2020
accepted: 30 09 2020
entrez: 22 10 2020
pubmed: 23 10 2020
medline: 10 4 2021
Statut: epublish

Résumé

Stress in adolescence can regulate vulnerability to traumatic stress in adulthood through region-specific epigenetic activity and catecholamine levels. We hypothesized that stress in adolescence would increase adult trauma vulnerability by impairing extinction-retention, a deficit in PTSD, by (1) altering class IIa histone deacetylases (HDACs), which integrate effects of stress on gene expression, and (2) enhancing norepinephrine in brain regions regulating cognitive effects of trauma. We investigated the effects of adolescent-stress on adult vulnerability to severe stress using the single-prolonged stress (SPS) model in male rats. Rats were exposed to either (1) adolescent-stress (33-35 postnatal days) then SPS (58-60 postnatal days; n = 14), or (2) no adolescent-stress and SPS (58-60 postnatal days; n = 14), or (3) unstressed conditions (n = 8). We then measured extinction-retention, norepinephrine, HDAC4, and HDAC5. As expected, SPS exposure induced an extinction-retention deficit. Adolescent-stress prior to SPS eliminated this deficit, suggesting adolescent-stress conferred resiliency to adult severe stress. Adolescent-stress also conferred region-specific resilience to norepinephrine changes. HDAC4 and HDAC5 were down-regulated following SPS, and these changes were also modulated by adolescent-stress. Regulation of HDAC levels was consistent with the pattern of cognitive effects of SPS; only animals exposed to SPS without adolescent-stress exhibited reduced HDAC4 and HDAC5 in the prelimbic cortex, hippocampus, and striatum. Thus, HDAC regulation caused by severe stress in adulthood interacts with stress history such that seemingly conflicting reports describing effects of adolescent stress on adult PTSD vulnerability may stem in part from dynamic HDAC changes following trauma that are shaped by adolescent stress history.

Identifiants

pubmed: 33087769
doi: 10.1038/s41598-020-74481-3
pii: 10.1038/s41598-020-74481-3
pmc: PMC7578655
doi:

Substances chimiques

HDAC4 protein, rat EC 3.5.1.98
Hdac5 protein, rat EC 3.5.1.98
Histone Deacetylases EC 3.5.1.98
Norepinephrine X4W3ENH1CV

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

17935

Subventions

Organisme : RRD VA
ID : I01 RX002252
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA042057
Pays : United States
Organisme : NIH HHS
ID : R01-DA042057
Pays : United States

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Auteurs

Lauren E Chaby (LE)

Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA. lauren.chaby@gmail.com.
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA. lauren.chaby@gmail.com.

Nareen Sadik (N)

Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA.

Nicole A Burson (NA)

Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA.

Scott Lloyd (S)

Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA.
Research Service, John D. Dingell VA Medical Center, Detroit, MI, USA.

Kelly O'Donnel (K)

Department of Psychology, University of Colorado, Colorado Springs, CO, USA.

Jesse Winters (J)

Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA.

Alana C Conti (AC)

Research Service, John D. Dingell VA Medical Center, Detroit, MI, USA.
Department of Neurosurgery, Wayne State University School of Medicine, Detroit, MI, USA.

Israel Liberzon (I)

Department of Psychiatry, Texas A&M College of Medicine, Bryan, TX, USA.

Shane A Perrine (SA)

Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA.
Research Service, John D. Dingell VA Medical Center, Detroit, MI, USA.

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Classifications MeSH