Inhibition of nitric oxide synthase modulates learned helplessness response in female rats

Autores

  • Jaqueline Rocha Borges dos Santos Universidade Federal Rural do Rio de Janeiro

DOI:

https://doi.org/10.53660/1537.prw3050

Palavras-chave:

Nitric oxide synthase, Depression, Stress, Learned helplessness

Resumo

Learned helplessness is the condition of humans or animals that have learned to behave helplessly, failing to respond even though there are opportunities to help themselves by avoiding unpleasant circumstances. It was investigated the participation of nitric oxide (NO) in female Wistar rats in learned helplessness tests. The animals received acute treatment with N–nitro-l-arginine methyl ester (L-NAME, 10 mg/kg or 100 mg/kg), an inhibitor of NO synthase, 30 minutes before random inescapable shock sessions lasting 25 minutes. On the test day, the animals that received L-NAME of 10 mg/kg or 100 mg/kg 24 hours beforehand, demonstrated reduced difference between stress and non-stress groups compared with control groups. The activity of the neuronal nitric oxide synthase was lower in animals pretreated with L-NAME, especially at a dose of 100 mg/kg. These results indicate that acute inhibition of NO synthase improved learned helplessness response, suggesting that NO is involved with stress and depression.

Downloads

Não há dados estatísticos.

Referências

BANGASSER, D.A.; CUARENTA, A. Sex differences in anxiety and depression: circuits and mechanisms. Nat Rev Neurosci., v. 22, n. 11, p. 674-684, 2021. https://doi.org/10.1038/s41583-021-00513-0

BAO A-M.; SWAAB, D.F. The stress systems in depression: a postmortem study. Eur. J. Psychotraumatol., n. 5, p. 26521, 2014. https://doi.org/10.3402/ejpt.v5.26521

BARATTA, M. V.; LESLIE, N.R.; FALLON, I.P.; DOLZANI, S.D.; CHUN, L.E.; TAMALUNAS, A.M.; WATKINS, L.R.; MAIER, S.F. Behavioural and neural sequelae of stressor exposure are not modulated by controllability in females. Eur. J. Neurosci., v. 47, p. 959–967, 2018. https://doi.org/10.1111/ejn.13833

BREDT, D.S.; SNYDER, S.H. Isolation of nitric oxide synthetase, a calmodulin requiring enzyme. Proc. Natl. Acad. Sci USA, v. 87, p. 682-85, 1990. https://doi.org/10.1073/pnas.87.2.682

BREDT, D.S.; SNYDER, S.H. Nitric oxide, a novel neural messenger. Neuron, v. 8, p. 3-11, 1992. https://doi.org/10.1016/0896-6273(92)90104-l

BROOKS, S.D.; HILEMAN, S.M.; CHANTLER, P.D.; MILDE, S.A.; LEMASTER, K.A.; FRISBEE, S.J.; SHOEMAKER, J.K.; JACKSON, D.N.; FRISBEE, J.C. Protection from vascular dysfunction in female rats with chronic stress and depressive symptoms. Am J Physiol Heart Circ Physiol., v. 314, n. 5, p. H1070-H1084, 2018. https://doi.org/10.1152/ajpheart.00647.2017

CHACHLAKI, K.; PREVOT, V. Nitric oxide signalling in the brain and its control of bodily functions. Braz J Pharmacol., v. 177, n. 24, p. 5437-5458, 2020. https://doi.org/10.1111/bph.14800

CZÉH, B.; FUCHS, E.; WIBORG, O.; SIMON, M. Animal models of major depression and their clinical implications. Prog Neuropsychopharmacol Biol Psychiatry, v. 64, p. 293-310, 2016. https://doi.org/10.1016/j.pnpbp.2015.04.004

DALLA, C.; PTYCHOUTIS, P.M.; KOKRAS, N.; PAPADOPOULOU-DAIFOTI, Z. Sex differences in animal models of depression and antidepressant response. Basic Clin Pharmacol Toxicol., v. 106, n. 3, p. 226-33, 2010. https://doi:10.1111/j.1742-7843.2009.00516.x

DI, S.; MAXSON, M.M.; FRANCO, A.; TASKER, J.G. Glucocorticoids regulate glutamate and GABA synapse-specific retrograde transmission via divergent nongenomic signaling pathways. J Neurosci., v. 29, n. 2, p. 393-401, 2009. https://doi.org/10.1523/JNEUROSCI.4546-08.2009

FARIA, M.S.; MUSCARÁ, M.N.; MORENO JUNIOR, H.; TEIXEIRA, S.A.; DIAS, H.B.; DE OLIVEIRA, B.; GRAEFF, F.G.; DE NUCCI, G. Acute inhibition of nitric oxide synthesis induces anxiolysis in the plus maze test. Eur J Pharmacol., v. 323, n. 1, p. 37-43, 1997. https://doi.org/10.1016/S0014-2999(97)00027-7

GAO, S-F.; LU, Y-R.; SHI, L-G.; WU, X-Y.; SUN, B.; FU, X-Y.; LUO, J-H.; BAO, A-M. Nitric oxide synthase and nitric oxide alterations in chronically stressed rats: a model for nitric oxide in major depressive disorder. Psychoneuroendocrinology, v. 47, p. 136-40, 2014. https://doi.org/10.1016/j.psyneuen.2014.05.009

GARTHWAITE, J. Concepts of neural nitric oxide‐mediated transmission. Euro J Neurosci., v. 27, p. 2783-802, 2008. https://doi.org/10.1111/j.1460-9568.2008.06285.x

GHASEMI, M. Nitric oxide: Antidepressant mechanisms and inflammation. Adv Pharmacol., v. 86, p. 121-152, 2019. https://doi.org/10.1016/bs.apha.2019.04.004

GROSSMAN, A. B.; ROSSANSMITH, W. G.; KABIGTING, E. B.; CADD, G.; CLIFTON, D.; STEINER, R. A. The distribution of hypothalamic nitric oxide synthase mRNA in relation to gonadotropin-releasing hormone neurons. J Endocrinol., v. 140, p. R5-R8, 1994. https://doi.org/10.1677/joe.0.140r005

HARVEY, B. H. Adaptive plasticity during stress and depression and the role of glutamate-nitric oxide pathways. S Afr Psychiatry Rev., v. 9, p. 132-9, 2006. https://doi.org/10.4314/ajpsy.v9i3.30214

HERMINI, A. H.; TEIXEIRA, N. A.; MENDES, V. E.; PEREIRA, D. G. Development of a software to control depression experiments through the "learned helplessness" model. Phys Med Biol., v. 39 (Part 1), p. 430, 1994.

JOCA, S. R. L.; SARTIM, A. G.; RONCALHO, A. L.; DINIZ, C. F. A.; WEGENER, G. Nitric oxide signalling and antidepressant action revisited. Cell Tissue Res., v. 377, n 1, p. 45-58, 2019. https://doi.org/10.1007/s00441-018-02987-4

JOCA, S. R. L.; GUIMARÃES, F. S. Inhibition of neuronal nitric oxide synthase in the rat hippocampus induces antidepressant-like effects. Psychopharmacology (Berl), v. 185, n. 3, p. 298-305, 2006. https://doi.org/10.1007/s00213-006-0326-2

KAEHLER, S. T.; SINGEWALD, N.; SINNER, C.; PHILIPPU, A. Nitric oxide modulates the release of serotonin in the rat hypothalamus. Brain Res., v. 835, p. 346-9, 1999. https://doi.org/10.1016/S0006-8993(99)01599-1

KOUROSH-ARAMI, M.; HOSSEINI, N.; MOHSENZADEGAN, M.; KOMAKI A.; JOGHATAEI, M. T. Neurophysiologic implications of neuronal nitric oxide synthase. Rev Neurosci., v. 31, n. 6, p. 617-636, 2020. https://doi.org/10.1515/revneuro-2019-0111

LU, Y-R.; ZHANG, Y.; RAO, Y-B.; CHEN, X.; LOU, H-F.; ZHANG, Y.; XIE, H-Y.; FANG, P.; HU, L-W. The changes in, and relationship between, plasma nitric oxide and corticotropin-releasing hormone in patients with major depressive disorder. Clin Exp Pharmacol Physiol., v. 45, n. 1, p. 10-15, 2018. https://doi.org/10.1111/1440-1681.12826

MAIER, S. F.; SELIGMAN, M. E. P. Learned helplessness: theory and evidence. J Exp Psychol Gen., v. 105, n. 3-46, 1976. https://doi.org/10.1037/0096-3445.105.1.3

McLEOD, T. M.; LÓPEZ-FIGUEROA, A. L.; LÓPEZ-FIGUEROA, M. O. Nitric oxide, stress, and depression. Psychopharmacol Bull., v. 35, n. 1, p. 24-41, 2001.

NELSON, R. J.; KRIEGSFELD, L. J.; DAWSON, V. L.; DAWSON, T. M. Effects of nitric oxide on neuroendocrine function and behavior. Front Neuroendocrinology, v. 18, p. 463-491, 1997. https://doi.org/10.1006/frne.1997.0156

OVERMIER, J. B. On learned helplessness. Integr Physiol Behav Sci., v. 37, n. 1, p. 4-8, 2002. https://doi.org/10.1007/BF02688801

PAUL, E. J.; KALK, E.; TOSSELL, K.; IRVINE, E. E.; FRANKS, N. P.; WISDEN, W.; WITHERS, D. J.; LEIPER, J.; UNGLESS, M. A. nNOS-expressing neurons in the ventral tegmental area and substantia nigra pars compacta. eNeuro., v. 5, n. 5, p. ENEURO.0381-18.2018, 2018. https://doi.org/10.1523/ENEURO.0381-18.2018

PHILIPPU, A. Nitric oxide: a universal modulator of brain function. Curr Med Chem., v. 23, n. 24, p. 2643-2652, 2016. https://doi.org/10.2174/0929867323666160627120408

PRAST, H.; PHILIPPU, A. Nitric oxide as modulator of neuronal function. Prog Neurobiol., v. 64, p. 51-68, 2001. https://doi.org/10.1016/S0301-0082(00)00044-7

RIEDEL, W. Role of nitric oxide in the control of the hypothalamic pituitary adrenocortical axis. Z Rheumatol., v. 59, p. 36-42, 2000. https://doi.org/10.1007/s003930070016

RIVIER, C.; SHEN, G. H. In the rat, endogenous nitric oxide modulates the response of the hypothalamic-pituitary-adrenal axis to interleukin-1, vasopressin, and oxytocin. J Neurosci., v. 14, p. 1985-1993, 1994. https://doi.org/10.1523/JNEUROSCI.14-04-01985.1994

RIVIER, C. Role of nitric oxide and carbon monoxide in modulating the ACTH response to immune and nonimmune signals. Neuroimmunomodulation, v. 5, p. 203-13, 1998. https://doi.org/10.1159/000026338

SAMHSA. National Survey on Drug Use and Health (NSDUH), 2018. US Department of Health & Human Services https://www.samhsa.gov/data/data-we-collect/nsduh-national-survey-drug-use-and-health

SELIGMAN, M. E.; MAIER, S. F. Failure to escape traumatic shock. J Exp Psychol., v. 74, p. 1-9, 1967. https://doi.org/10.1037/h0024514

SEVGI, S.; OZEK, M.; EROGLU, L. L-NAME prevents anxiety-like and depression-like behavior in rats exposed to restraint stress. Methods Find Exp Clin Pharmacol., v. 28, n. 2, p. 95-9, 2006. https://doi.org/10.1358/mf.2006.28.2.977840

SHAHIN, S.; BANERJEE, S.; SWARUP, V.; SINGH, S. P.; CHATURVEDI, C. M. From the cover: 2.45-GHz microwave radiation impairs hippocampal learning and spatial memory: involvement of local stress mechanism-induced suppression of iGluR/ERK/CREB signaling. Toxicol Sci., v. 161, n. 2, p. 349-374, 2018. https://doi.org/10.1093/toxsci/kfx221

SHERWIN, E.; GIGLIUCCI, V.; HARKIN, A. Regional specific modulation of neuronal activation associated with nitric oxide synthase inhibitors in an animal model of antidepressant activity. Behav Brain Res., v. 316, p. 18-28, 2017. https://doi.org/10.1016/j.bbr.2016.08.049

SILVA, M.; AGUIAR, D. C.; DINIZ, C. R.; GUIMARÃES, F. S.; JOCA, S. R. Neuronal NOS inhibitor and conventional antidepressant drugs attenuate stress-induced fos expression in overlapping brain regions. Cell Mol Neurobiol., v. 32, n. 3, p. 443-53, 2012. https://doi.org/10.1007/s10571-011-9775-1

SIPEK, A. Lithium and Ebstein’s anomaly. Cor Vasa, v. 31, p. 149-156, 1989.

SONG, X.; VILARES, I. Assessing the relationship between the human learned helplessness depression model and anhedonia. PLoS One, v. 16, n. 3, p. e0249056, 2021. https://doi.org/10.1371/journal.pone.0249056

STANQUINI, L. A.; BIOJONE, C.; GUIMARÃES, F. S.; JOCA, S. R. Repeated treatment with nitric oxide synthase inhibitor attenuates learned helplessness development in rats and increases hippocampal BDNF expression. Acta Neuropsychiatr., v. 30, n. 3, p. 127-136, 2018. https://doi.org/10.1017/neu.2017.28

VOLKE, V.; WEGENER, G.; BOURIN, M.; VASAR, E. Antidepressant- and anxiolytic-like effects of selective neuronal NOS inhibitor 1-(2-trifluoromethylphenyl)-imidazole in mice. Behav Brain Res., v. 140, n. 1-2, p. 141-7, 2003. https://doi.org/10.1016/S0166-4328(02)00312-1

WANG, J.; LI, J.; YU, M.; WANG, Y.; MA Y. An enhanced expression of hypothalamic neuronal nitric oxide synthase in a rat model of simulated transport stress. BMC Vet Res., v. 15, n. 1, p. 323, 2019. https://doi.org/10.1186/s12917-019-2071-x

WEGENER, G.; VOLKE, V. Nitric oxide synthase inhibitors as antidepressants. Pharmaceuticals (Basel), v. 3, n. 1, p. 273-299, 2010. https://doi.org/10.3390/ph3010273

WEGENER, A. J.; NEIGH G. N. Animal models of anxiety and depression: incorporating the underlying mechanisms of sex differences in macroglia biology. Front Behav Neurosci., v0 15, 780190, 2021. https://doi:10.3389/fnbeh.2021.780190

WILLNER, P. The validity of animal models of depression. Psychopharmacology, v. 83, p. 1-16, 1984. https://doi.org/10.1007/BF00427414

WILLNER, P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl), v. 134, p. 319 –329, 1997. https://doi.org/10.1007/s002130050456

YAMADA, K.; NODA, Y.; NAKAYAMA, S.; KOMORI, Y.; SUGIHARA, H.; HASEGAWA, T.; NABESHIMA, T. Role of nitric oxide in learning and memory and in monoamine metabolism in the rat brain. Br J Pharmacol., v. 115, p. 852-8, 1995. https://doi.org/10.1111/j.1476-5381.1995.tb15011.x

ZHOU, Q-G.; ZHU, X-H.; NEMES, A.D.; ZHU, D-Y. Neuronal nitric oxide synthase and affective disorders. IBRO Rep., v. 5, p. 116-132, 2018. https://doi.org/10.1016/j.ibror.2018.11.004

ZHU, L-J.; LIU, M-Y.; LI, H.; LIU, X.; CHEN, C.; HAN, Z.; WU, H-Y.; XING JING, X.; ZHOU, H-H.; SUH, H.; ZHU, D-Y.; ZHOU, Q-G. The different roles of glucocorticoids in the hippocampus and hypothalamus in chronic stress-induced HPA axis hyperactivity. PLoS One, v. 9, n. 5, p. e97689, 2014. https://doi.org/10.1371/journal.pone.0097689

Downloads

Publicado

2023-12-11

Como Citar

Santos, J. R. B. dos. (2023). Inhibition of nitric oxide synthase modulates learned helplessness response in female rats. Peer Review, 5(25), 504–518. https://doi.org/10.53660/1537.prw3050

Edição

Seção

Articles