Influence of Mild Chronic Stress and Social Isolation on Acute Ozone-Induced Alterations in Stress Biomarkers and Brain-Region-Specific Gene Expression in Male Wistar–Kyoto Rats

Valdez, Matthew C.; Freeborn, Danielle L.; Valdez, Joseph M.; Henriquez, Andres R.; Snow, Samantha J.; Jackson, Thomas W.; Kodavanti, Prasada Rao S.; Kodavanti, Urmila P.

doi:10.3390/antiox12111964

Influence of Mild Chronic Stress and Social Isolation on Acute Ozone-Induced Alterations in Stress Biomarkers and Brain-Region-Specific Gene Expression in Male Wistar–Kyoto Rats

Journal Article · Wed Nov 01 00:00:00 EDT 2023 · Antioxidants

DOI:https://doi.org/10.3390/antiox12111964· OSTI ID:2471300

^[1]; Freeborn, Danielle L. ^[2]; Valdez, Joseph M. ^[1]; Henriquez, Andres R. ^[3]; Snow, Samantha J. ^[2]; ^[4]; ^[1]; Kodavanti, Urmila P. ^[2]

US Environmental Protection Agency (EPA), Research Triangle Park, NC (United States); Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
US Environmental Protection Agency (EPA), Research Triangle Park, NC (United States)
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States); US Environmental Protection Agency (EPA), Research Triangle Park, NC (United States)

Individuals with psychosocial stress often experience an exaggerated response to air pollutants. Ozone (O₃) exposure has been associated with the activation of the neuroendocrine stress-response system. We hypothesized that preexistent mild chronic stress plus social isolation (CS), or social isolation (SI) alone, would exacerbate the acute effects of O₃ exposure on the circulating adrenal-derived stress hormones, and the expression of the genes regulating glucocorticoid stress signaling via an altered stress adaptation in a brain-region-specific manner. Male Wistar–Kyoto rats (5 weeks old) were socially isolated, plus were subjected to either CS (noise, confinement, fear, uncomfortable living, hectic activity, and single housing), SI (single housing only, restricted handling and no enrichment) or no stress (NS; double housing, frequent handling and enrichment provided) for 8 weeks. The rats were then exposed to either air or O₃ (0.8 ppm for 4 h), and the samples were collected immediately after. The indicators of sympathetic and hypothalamic–pituitary axis (HPA) activation (i.e., epinephrine, corticosterone, and lymphopenia) increased with O₃ exposure, but there were no effects from CS or SI, except for the depletion of serum BDNF. CS and SI revealed small changes in brain-region-specific glucocorticoid-signaling-associated markers of gene expression in the air-exposed rats (hypothalamic Nr3c1, Nr3c2 Hsp90aa1, Hspa4 and Cnr1 inhibition in SI; hippocampal HSP90aa1 increase in SI; and inhibition of the bed nucleus of the stria terminalis (BNST) Cnr1 in CS). Gene expression across all brain regions was altered by O₃, reflective of glucocorticoid signaling effects, such as Fkbp5 in NS, CS and SI. The SI effects on Fkbp5 were greatest for SI in BNST. O₃ increased Cnr2 expression in the hypothalamus and olfactory bulbs of the NS and SI groups. O₃, in all stress conditions, generally inhibited the expression of Nr3c1 in all brain regions, Nr3c2 in the hippocampus and hypothalamus and Bdnf in the hippocampus. SI, in general, showed slightly greater O₃-induced changes when compared to NS and CS. Serum metabolomics revealed increased sphingomyelins in the air-exposed SI and O₃-exposed NS, with underlying SI dampening some of the O₃-induced changes. These results suggest a potential link between preexistent SI and acute O₃-induced increases in the circulating adrenal-derived stress hormones and brain-region-specific gene expression changes in glucocorticoid signaling, which may partly underlie the stress dynamic in those with long-term SI.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: US Environmental Protection Agency (EPA); USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 2471300

Journal Information:: Antioxidants, Journal Name: Antioxidants Journal Issue: 11 Vol. 12; ISSN 2076-3921; ISSN ANTIGE

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

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Influence of Mild Chronic Stress and Social Isolation on Acute Ozone-Induced Alterations in Stress Biomarkers and Brain-Region-Specific Gene Expression in Male Wistar–Kyoto Rats

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