Exercise prevents downregulation of hippocampal presynaptic proteins following olanzapine-elicited metabolic dysregulation in rats: distinct roles of inhibitory and excitatory terminals.
Abstract
Schizophrenia patients treated with olanzapine, or other second-generation antipsychotics, frequently develop metabolic side-effects, such as glucose intolerance and increased adiposity. We previously observed that modeling these adverse effects in rodents also resulted in hippocampal shrinkage. Here, we investigated the impact of olanzapine treatment, and the beneficial influence of routine exercise, on the neurosecretion machinery of the hippocampus. Immunodensities and interactions of three soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins (syntaxin-1, synaptosome-associated protein of 25kDa (SNAP-25) and vesicle-associated membrane protein (VAMP)), synaptotagmin and complexins-1/2 were quantified in the hippocampus of sedentary and exercising rats exposed over 9weeks to vehicle (n=28) or olanzapine (10mg/kg/day, n=28). In addition, brain sections from subgroups of sedentary animals (n=8) were co-immunolabeled with antibodies against vesicular GABA (VGAT) and glutamate (VGLUT1) transporters, along with syntaxin-1, and examined by confocal microscopy to detect selective olanzapine effects within inhibitory or excitatory terminals. Following olanzapine treatment, sedentary, but not exercising rats showed downregulated (33-50%) hippocampal densities of SNARE proteins and synaptotagmin, without altering complexin levels. Strikingly, these effects had no consequences on the amount of SNARE protein-protein interactions. Lower immunodensity of presynaptic proteins was associated with reduced CA1 volume and glucose intolerance. Syntaxin-1 depletion appeared more prominent in VGAT-positive terminals within the dentate gyrus, and in non-VGAT/VGLUT1-overlapping areas of CA3. The present findings suggest that chronic exposure to olanzapine may alter hippocampal connectivity, especially in inhibitory terminals within the dentate gyrus, and along the mossy fibers of CA3. Together with previous studies, we propose that exercise-based therapies might be beneficial for patients being treated with olanzapine.
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Recent animal studies have demonstrated that AE was able to reverse most of the damage caused to hippocampal volume and hippocampal synaptic connectivity caused by antipsychotic medication.
“For example, recent animal studies have demonstrated that AE was able to reverse most of damage caused to hippocampal volume and hippocampal synaptic connectivity caused by antipsychotic medication (Barr et al., 2013; Ramos-Miguel et al., 2015).”
From Aerobic Exercise as a Tool to Improve Hippocampal Plasticity and Function in Humans: Practical Implications for Mental Health Treatment (2016) · cites this paper as Ramos-Miguel et al., 2015
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“…studies indicate that chronic olanzapine exposure predicted abnormal hippocampal connectivity, particularly within inhibitory terminals of the DG (Ramos-Miguel et al. 2015), and was associated with DG volume reductions in sedentary rats with exercise reversing the majority of this loss (Barr et…”
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Sadri, I., Nikookheslat, S. D., Karimi, P., Khani, M., & Nadimi, S. (2023) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-023-01360-9 · Cited by 17 · see citing works
“Before experiments, animals were handled daily to reduce stress and adapt to the animal facilities for one week [12].”
Ramos‐Miguel, A., Gicas, K. M., Alamri, J., Beasley, C. L., Dwork, A. J., Mann, J. J., Rosoklija, G. B., Cai, F., Song, W., Barr, A. M., et al. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.015 · Cited by 16 · see citing works
Ramos‐Miguel, A., Barakauskas, V., Alamri, J., Miyauchi, M., Barr, A. M., Beasley, C. L., Rosoklija, G. B., Mann, J. J., Dwork, A. J., Moradian, A., et al. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.045 · Cited by 12 · see citing works
Exercise Modulates Exocytosis: Chemical Insights from the Intracellular Vesicle Perspective
Liu, R., He, X., Liu, J., Sun, Z., Yu, P., Hou, L., & Mao, L. (2025) · Angewandte Chemie International Edition · doi:10.1002/anie.202511277 · Cited by 6 · see citing works
Exercise Modulates Exocytosis: Chemical Insights from the Intracellular Vesicle Perspective
Liu, R., He, X., Liu, J., Sun, Z., Yu, P., Hou, L., & Mao, L. (2025) · Angewandte Chemie · doi:10.1002/ange.202511277 · Cited by 1 · see citing works
Nikookheslat, S. D., Karimi, P., & Sadri, I. (2020) · Medical Journal of Tabriz University of Medical Sciences and Health Services · doi:10.34172/mj.2020.032
Nikookheslat, S. D., Karimi, P., & Sadri, I. (2021) · Medical Journal of Tabriz University of Medical Sciences and Health Services · doi:10.34172/mj.2021.033
- Authors
- Ramos-Miguel, A., Honer, W. G., Boyda, H. N., Sawada, K., Beasley, C. L., Procyshyn, R. M., & Barr, A. M.
- Affiliations
- University of British Columbia (CA)
- BC Mental Health & Substance Use Services (CA)
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2015-08
- Volume
- 301
- Pages
- 298-311
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W570014140
- Cited by
- 18
- References
- 74
- Citations by year
- 2025: 2 · 2024: 1 · 2023: 1 · 2021: 2 · 2020: 1 · 2019: 1 · 2018: 5 · 2017: 2 · 2016: 2 · 2015: 1
- FWCI
- 1.55
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Michael Smith Foundation for Health Research
- BC Schizophrenia Society Foundation
- Canadian Institutes of Health Research (MT-14037, MOP-81112)
- Natural Sciences and Engineering Research Council of Canada (356069-09)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- olanzapine, physical activity, atypical antipsychotics, metabolic side effects, impaired glucose tolerance, hippocampus, presynaptic proteins, SNARE proteins, syntaxin-1, SNAP-25, VAMP, synaptotagmin, complexin, vesicular GABA transporter, vesicular glutamate transporter, dentate gyrus, CA1, CA3, mossy fibers, synaptic plasticity, schizophrenia
- MeSH terms
- Olanzapine, Animals, Benzodiazepines, Disease Models, Animal, Exercise Therapy, Female, Hippocampus, Metabolic Diseases, Nerve Tissue Proteins, Antipsychotic Agents, Down-Regulation, Rats, Sprague-Dawley, SNARE Proteins, R-SNARE Proteins, Rats
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