Neurosteroids in the context of stress: implications for depressive disorders - PubMed (original) (raw)
Review
Neurosteroids in the context of stress: implications for depressive disorders
Susan S Girdler et al. Pharmacol Ther. 2007 Oct.
Abstract
Animal models indicate that the neuroactive steroids 3alpha,5alpha-THP (allopregnanolone) and 3alpha,5alpha-THDOC (allotetrahydroDOC) are stress responsive, serving as homeostatic mechanisms in restoring normal GABAergic and hypothalamic-pituitary-adrenal (HPA) function following stress. While neurosteroid increases to stress are adaptive in the short term, animal models of chronic stress and depression find lower brain and plasma neurosteroid concentrations and alterations in neurosteroid responses to acute stressors. It has been suggested that disruption in this homeostatic mechanism may play a pathogenic role in some psychiatric disorders related to stress. In humans, neurosteroid depletion is consistently documented in patients with current depression and may reflect their greater chronic stress. Women with the depressive disorder, premenstrual dysphoric disorder (PMDD), have greater daily stress and a greater rate of traumatic stress. While results on baseline concentrations of neuroactive steroids in PMDD are mixed, PMDD women have diminished functional sensitivity of GABA(A) receptors and our laboratory has found blunted allopregnanolone responses to mental stress relative to non-PMDD controls. Similarly, euthymic women with histories of clinical depression, which may represent a large proportion of PMDD women, show more severe dysphoric mood symptoms and blunted allopregnanolone responses to stress versus never-depressed women. It is suggested that failure to mount an appropriate allopregnanolone response to stress may reflect the price of repeated biological adaptations to the increased life stress that is well documented in depressive disorders and altered allopregnanolone stress responsivity may also contribute to the dysregulation seen in HPA axis function in depression.
Figures
Fig. 1
Allopregnanolone levels in plasma and brain of adult Sprague-Dawley male rats after acute swim stress. Rats were subjected to acute stress by swimming for 10 min in ambient temperature water. Allopregnanolone levels were measured by RIA after purification of the steroid by HPLC. The data represent the mean±SEM for 3 separate experiments (_n_=12 rats per time point) for the cerebral cortex and plasma. Stress-induced increases of allopregnanolone in the cerebral cortex and plasma were statistically significant at 10, 40, and 70 min after the initiation of swim stress compared with nonstressed levels at 0 time [analysis of variance (ANOVA), P<0.05; Tukey's honestly significant difference procedure (HSD), P<0.05]. Adapted from Purdy et al. (1991).
Fig. 2
Mean±SEM allopregnanolone levels in response to the GnRH test (*, P<0.01 vs. 0 min) and in response to the CRF test (*, P<0.01 vs. 0 min). Adapted from Genazzani et al. (1998).
Fig. 3
Mean (± SEM) change in luteal phase plasma allopregnanolone (ALLO) during stress in PMDD women and control subjects (#, P<0.010). From Girdler et al. (2001).
Fig. 4
Allopregnanolone response to the adrenocorticotropic hormone (ACTH) test in patients with premenstrual syndrome (shaded bars) and in the control group (white bars) expressed as area under the curve (*, P<0.05). Adapted from Lombardi et al. (2004).
Fig. 5
Change (stress−baseline) in allopregnanolone (ALLO) concentrations at 30 and 60 min post-stress in women as a function of histories of depression (DEP). From Klatzkin et al. (2006a).
Similar articles
- GABAergic neuroactive steroid response to sertraline in premenstrual dysphoric disorder.
Miller KN, Standeven L, Morrow AL, Payne JL, Epperson CN, Hantsoo L. Miller KN, et al. Psychoneuroendocrinology. 2024 Feb;160:106684. doi: 10.1016/j.psyneuen.2023.106684. Epub 2023 Nov 30. Psychoneuroendocrinology. 2024. PMID: 38091917 - Allopregnanolone levels and reactivity to mental stress in premenstrual dysphoric disorder.
Girdler SS, Straneva PA, Light KC, Pedersen CA, Morrow AL. Girdler SS, et al. Biol Psychiatry. 2001 May 1;49(9):788-97. doi: 10.1016/s0006-3223(00)01044-1. Biol Psychiatry. 2001. PMID: 11331087 - Effects of GABA active steroids in the female brain with a focus on the premenstrual dysphoric disorder.
Bixo M, Johansson M, Timby E, Michalski L, Bäckström T. Bixo M, et al. J Neuroendocrinol. 2018 Feb;30(2). doi: 10.1111/jne.12553. J Neuroendocrinol. 2018. PMID: 29072794 Review. - The Role of HPA Axis and Allopregnanolone on the Neurobiology of Major Depressive Disorders and PTSD.
Almeida FB, Pinna G, Barros HMT. Almeida FB, et al. Int J Mol Sci. 2021 May 23;22(11):5495. doi: 10.3390/ijms22115495. Int J Mol Sci. 2021. PMID: 34071053 Free PMC article. Review. - Histories of depression, allopregnanolone responses to stress, and premenstrual symptoms in women.
Klatzkin RR, Morrow AL, Light KC, Pedersen CA, Girdler SS. Klatzkin RR, et al. Biol Psychol. 2006 Jan;71(1):2-11. doi: 10.1016/j.biopsycho.2005.02.007. Epub 2005 Jun 13. Biol Psychol. 2006. PMID: 15951099
Cited by
- Postpartum depression: psychoneuroimmunological underpinnings and treatment.
Anderson G, Maes M. Anderson G, et al. Neuropsychiatr Dis Treat. 2013;9:277-87. doi: 10.2147/NDT.S25320. Epub 2013 Feb 21. Neuropsychiatr Dis Treat. 2013. PMID: 23459664 Free PMC article. - Neuroactive Steroids and GABAergic Involvement in the Neuroendocrine Dysfunction Associated With Major Depressive Disorder and Postpartum Depression.
Maguire J. Maguire J. Front Cell Neurosci. 2019 Mar 8;13:83. doi: 10.3389/fncel.2019.00083. eCollection 2019. Front Cell Neurosci. 2019. PMID: 30906252 Free PMC article. Review. - Neurosteroid biosynthesis regulates sexually dimorphic fear and aggressive behavior in mice.
Pinna G, Agis-Balboa RC, Pibiri F, Nelson M, Guidotti A, Costa E. Pinna G, et al. Neurochem Res. 2008 Oct;33(10):1990-2007. doi: 10.1007/s11064-008-9718-5. Epub 2008 May 13. Neurochem Res. 2008. PMID: 18473173 Review. - Neuropathic pain promotes adaptive changes in gene expression in brain networks involved in stress and depression.
Descalzi G, Mitsi V, Purushothaman I, Gaspari S, Avrampou K, Loh YE, Shen L, Zachariou V. Descalzi G, et al. Sci Signal. 2017 Mar 21;10(471):eaaj1549. doi: 10.1126/scisignal.aaj1549. Sci Signal. 2017. PMID: 28325815 Free PMC article. - Prefrontal allopregnanolone mediates the adverse effects of acute stress in a mouse model of tic pathophysiology.
Cadeddu R, Van Zandt M, Santovito LS, Odeh K, Anderson CJ, Flanagan D, Nordkild P, Pinna G, Pittenger C, Bortolato M. Cadeddu R, et al. Neuropsychopharmacology. 2023 Aug;48(9):1288-1299. doi: 10.1038/s41386-023-01603-6. Epub 2023 May 17. Neuropsychopharmacology. 2023. PMID: 37198434 Free PMC article.
References
- Akwa Y, Purdy RH, Koob GF, Britton KT. The amygdale mediates the anxiolytic-like effect of the neurosteroid allopregnanolone in rat. Behav Brain Res. 1999;106:119–125. - PubMed
- Andreen L, Sundstrom-Poromaa I, Bixo M, Nyberg S, Backstrom T. Allopregnanolone concentration and mood-a bimodal association in postmenopausal women treated with oral progesterone. Psychopharmacology. 2006;187:209–221. - PubMed
- Bancroft J, Cook A, Davidson D, Bennie J, Goodwin G. Blunting of neuroendocrine responses to infusion of L-tryptophan in women with perimenstrual mood change. Psychol Med. 1991;21:305–312. - PubMed
- Barbaccia ML, Roscetti G, Trabucchi M, Mostallino MC, Concas A, Purdy RH, et al. Time-dependent changes in rat brain neuroactive steroid concentrations and GABA A receptor function after acute stress. Neuroendocrinology. 1996;63:166–172. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
- M01 RR000046/RR/NCRR NIH HHS/United States
- R01 MH051246-04/MH/NIMH NIH HHS/United States
- R01 MH051246/MH/NIMH NIH HHS/United States
- MH051246/MH/NIMH NIH HHS/United States
- RR00046/RR/NCRR NIH HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical