Anxiety-like behavior in female mice changes by feeding, possible effect of guanylate cyclase C.
cGMP
elevated plus maze
home cage escape
uroguanylin
Journal
The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
30
04
2019
revised:
14
10
2019
accepted:
22
10
2019
pubmed:
28
10
2019
medline:
22
6
2021
entrez:
27
10
2019
Statut:
ppublish
Résumé
Anxiety disorders are the most frequent mental disorders and are more prevalent in the female population. Up to date, an involvement of guanylate cyclase A and B in anxiety-like behavior has been suggested. In this study, we showed an expression of guanylate cyclase C (GC-C) in the amygdala which is regulated by feeding. Therefore, we further investigated sex differences of GC-C effects on anxiety levels with special attention to female estrous cycle and feeding. The effects of estrous cycle and feeding were investigated by several behavior tests: elevated plus maze, home cage escape and novelty-induced hypophagy. Possible changes in GC-C expression in amygdala and hypothalamus during estrous cycle were established by qPCR. When GC-C is activated (after a meal), the sex difference in all behavior tests used was abolished. As the expression of mRNA for GC-C in the amygdala increases 2 hr after a meal only in female animals, the anxiety levels change after a meal again only in female animals. When the anxiety levels are investigated, it is very important to pay attention not only to estrous cycle in female animals but also when animals were fed compared to the time point of the experiments. Concluding from our results, the sex differences in the incidence of anxiety disorders in humans could be GC-C dependent.
Substances chimiques
RNA, Messenger
0
Guanylate Cyclase
EC 4.6.1.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2781-2790Subventions
Organisme : Croatian Science Foundation
ID : IP-2018-01-7416
Organisme : European Regional Development Fund, Operational Programme Competitiveness and Cohesion
ID : KK.01.1.1.01.0007, CoRE - Neuro
Informations de copyright
© 2019 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
Références
An, X. L., Zou, J. X., Wu, R. Y., Yang, Y., Tai, F. D., Zeng, S. Y., … Broders, H. (2011). Strain and sex differences in anxiety-like and social behaviors in C57BL / 6J and BALB / cJ mice. Experimental Animals, 60, 111-123.
Barkley, M. S., & Bradford, G. E. (1981). Estrous cycle dynamics in different strains of mice. Proceedings of the Society for Experimental Biology and Medicine, 167, 70-77.
Bíró, E., Tóth, G., & Telegdy, G. (1995). Involvement of neurotransmitters in the “anxiolytic- like” action of atrial natriuretic peptide in rats. Neuropeptides, 29, 215-220. https://doi.org/10.1016/0143-4179(95)90063-2
Bíró, E., Tóth, G., & Telegdy, G. (1996). Effect of receptor blockers on brain natriuretic peptide and C-type natriuretic peptide caused anxiolytic state in rats. Neuropeptides, 30, 59-65. https://doi.org/10.1016/S0143-4179(96)90056-6
Butera, P. C. (2010). Estradiol and the control of food intake. Physiology & Behavior, 99, 175-180.
Bychkov, E., Ahmed, M. R., & Gurevich, E. V. (2011). Sex differences in the activity of signalling pathways and expression of G-protein-coupled receptor kinases in the neonatal ventral hippocampal lesion model of schizophrenia. International Journal of Neuropsychopharmacology, 14, 1-15. https://doi.org/10.1017/S1461145710000118
Byers, S. L., Wiles, M. V., Dunn, S. L., & Taft, R. A. (2012). Mouse estrous cycle identification tool and images. PLoS ONE, 7, e35538. https://doi.org/10.1371/journal.pone.0035538
Chang, Y. Y., Yang, C. H., Liang, Y. C., Yeh, C. M., Huang, C. C., & Hsu, K. S. (2009). Estrogen modulates sexually dimorphic contextual fear extinction in rats through estrogen receptor beta. Hippocampus, 19, 1142-1150.
Craske, M. G., Stein, M. B., Eley, T. C., Milad, M. R., Holmes, A., Rapee, R. M., & Wittchen, H. U. (2017). Anxiety disorders. Nature Reviews Disease Primers, 3, 17024.
Fernandes, C., González, M. I., Wilson, C. A., & File, S. E. (1999). Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacology, Biochemistry and Behavior, 64, 731-738. https://doi.org/10.1016/S0091-3057(99)00139-2
Folgueira, C., Beiroa, D., Callon, A., Al-Massadi, O., Barja-Fernandez, S., Senra, A., … Nogueiras, R. (2016). Uroguanylin action in the brain reduces weight gain in obese mice via different efferent autonomic pathways. Diabetes, 65, 421-432. https://doi.org/10.2337/db15-0889
Folgueira, C., Sanchez-Rebordelo, E., Barja-Fernandez, S., Leis, R., Tovar, S., Casanueva, F. F., … Seoane, L. M. (2016). Uroguanylin levels in intestine and plasma are regulated by nutritional status in a leptin-dependent manner. European Journal of Nutrition, 55, 529-536.
Frye, C. A., Petralia, S. M., & Rhodes, M. E. (2000). Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha,5alpha-THP. Pharmacology, Biochemistry and Behavior, 67, 587-596.
Gillies, G. E., & McArthur, S. (2010). Estrogen actions in the brain and the basis for differential action in men and women: A case for sex-specific medicines. Pharmacological Reviews, 62, 155-198.
Goldstein, J. M., Seidman, L. J., Horton, N. J., Makris, N., Kennedy, D. N., Caviness, V. S. Jr, … Tsuang, M. T. (2001). Normal sexual dimorphism of the adult human brain assessed by In Vivo magnetic resonance imaging. Cerebral Cortex, 11, 490-497.
Gong, R., Ding, C., Hu, J., Lu, Y., Liu, F., Mann, E., … Luo, M. (2011). Role for the membrane receptor guanylyl cyclase-C in attention deficiency and hyperactive behavior. Science, 333, 1642-1646. https://doi.org/10.1126/science.1207675
Hodes, A., & Lichtstein, D. (2014). Natriuretic hormones in brain function. Frontiers in Endocrinology, 5, 201. https://doi.org/10.3389/fendo.2014.00201
Kellner, M., Knaudt, K., Jahn, H., Holsboer, F., & Wiedemann, K. (1998). Atrial natriuretic hormone in lactate-induced panic attacks: Mode of release and endocrine and pathophysiological consequences. Journal of Psychiatric Research, 32, 37-48. https://doi.org/10.1016/S0022-3956(97)00034-4
Lebron-milad, K., Abbs, B., Milad, M. R., Linnman, C., Rougemount-Bücking, A., Zeidan, M. A., … Goldstein, J. M. (2012). Sex differences in the neurobiology of fear conditioning and extinction : A preliminary fMRI study of shared sex differences with stress-arousal circuitry. Biology of Mood & Anxiety Disorders, 2, 7.
Lorenz, J. N., Nieman, M., Sabo, J., Sanford, L. P., Hawkins, J. A., Elitsur, N., … Cohen, M. B. (2003). Uroguanylin knockout mice have increased blood pressure and impaired natriuretic response to enteral NaCl load. The Journal of Clinical Investigation, 112, 1244-1254.
Maguire, J. L., Stell, B. M., Rafizadeh, M., & Mody, I. (2005). Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nature Neuroscience, 8, 797-804.
Mann, E. A., Jump, M. L., Wu, J., Yee, E., & Giannella, R. A. (1997). Mice lacking the guanylyl cyclase C receptor are resistant to STa-induced intestinal secretion. Biochemical and Biophysical Research Communications, 239, 463-466. https://doi.org/10.1006/bbrc.1997.7487
Martin, E. I., Ressler, K. J., Binder, E., & Nemeroff, C. B. (2009). The neurobiology of anxiety disorders: Brain imaging, genetics, and psychoneuroendocrinology. Psychiatric Clinics of North America, 32, 549-575.
McLean, C. P., Asnaani, A., Litz, B. T., & Hofmann, S. G. (2011). Gender differences in anxiety disorders: Prevalence, course of illness, comorbidity and burden of illness. Journal of Psychiatric Research, 45, 1027-1035. https://doi.org/10.1016/j.jpsychires.2011.03.006
Meyer, T., & Herrmann-Lingen, C. (2017). Natriuretic peptides in anxiety and panic disorder. Vitamins and Hormones, 103, 131-145.
Montkowski, A., Jahn, H., Ströhle, A., Poettig, M., Holsboer, F., & Wiedemann, K. (1998). C-type natriuretic peptide exerts effects opposing those of atrial natriuretic peptide on anxiety-related behaviour in rats. Brain Research, 792, 358-360.
Murphy, M., & Mercer, J. G. (2013). Diet-regulated anxiety. International Journal of Endocrinology, 2013, 701967.
Paré, W. P., Tejani-butt, S., & Kluczynski, J. (2001). The emergence test: Effects of psychotropic drugs on neophobic disposition in Wistar Kyoto (WKY) and Sprague Dawley rats. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 25, 1615-1628.
Potter, L. R. (2011). Guanylyl cyclase structure, function and regulation. Cellular Signalling, 23, 1921-1926.
Rugarn, O., Hammar, M., Theodorsson, A., Theodorsson, E., & Stenfors, C. (1999). Sex differences in neuropeptide distribution in the rat brain. Peptides, 20, 81-86. https://doi.org/10.1016/S0196-9781(98)00139-9
Salehi, M. M., Namavar, M. R., Jafarzadeh Shirazi, M. R., Rahmanifar, F., & Tamadon, A. (2012). A simple method for isolation of the anteroventral periventricular and arcuate. Anatomy, 6-7, 48-51.
Ströhle, A., Jahn, H., Montkowski, A., Liebsch, G., Boll, E., Landgraf, R., … Wiedemann, K. (1997). Central and peripheral administration of atriopeptin is anxiolytic in rats. Neuroendocrinology, 65, 210-215. https://doi.org/10.1159/000127274
Ströhle, A., Kellner, M., Holsboer, F., & Wiedemann, K. (2001). Anxiolytic activity of atrial natriuretic peptide in patients with panic disorder. American Journal of Psychiatry, 158, 1514-1516.
Tabatadze, N., Huang, G., May, R. M., Jain, A., & Woolley, C. S. (2015). Sex differences in molecular signaling at inhibitory synapses in the hippocampus. Journal of Neuroscience, 35, 11252-11265.
Valentino, M. A., Lin, J. E., Snook, A. E., Li, P., Kim, G. W., Marszalowicz, G., … Waldman, S. A. (2011). A uroguanylin-GUCY2C endocrine axis regulates feeding in mice. The Journal of Clinical Investigation, 121, 3578-3588.
Wittchen, H. U., Jacobi, F., Rehm, J., Gustavsson, A., Svensson, M., Jönsson, B., … Steinhausen, H. C. (2011). The size and burden of mental disorders and other disorders of the brain in Europe 2010. European Neuropsychopharmacology, 21, 655-679.
Zapala, M. A., Hovatta, I., Ellison, J. A., Wodicka, L., Del Rio, J. A., Tennant, R., … Barlow, C. (2005). Adult mouse brain gene expression patterns bear an embryologic imprint. Proceedings of the National Academy of Sciences of the United States of America, 102, 10357-10362.