Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Linalool Ameliorates Memory Loss and Behavioral Impairment Induced by REM-Sleep Deprivation through the Serotonergic Pathway

  • Received : 2018.05.02
  • Accepted : 2018.05.30
  • Published : 2018.07.01
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Abstract

Rapid eye movement (REM) sleep has an essential role in the process of learning and memory in the hippocampus. It has been reported that linalool, a major component of Lavandula angustifolia, has antioxidant, anti-inflammatory, and neuroprotective effects, along with other effects. However, the effect of linalool on the cognitive impairment and behavioral alterations that are induced by REM-sleep deprivation has not yet been elucidated. Several studies have reported that REM-sleep deprivation-induced memory deficits provide a well-known model of behavioral alterations. In the present study, we examined whether linalool elicited an anti-stress effect, reversing the behavioral alterations observed following REM-sleep deprivation in mice. Furthermore, we investigated the underlying mechanism of the effect of linalool. Spatial memory and learning memory were assessed through Y maze and passive avoidance tests, respectively, and the forced swimming test was used to evaluate anti-stress activity. The mechanisms through which linalool improves memory loss and behavioral alterations in sleep-deprived mice appeared to be through an increase in the serotonin levels. Linalool significantly ameliorated the spatial and learning memory deficits, and stress activity observed in sleep-deprived animals. Moreover, linalool led to serotonin release, and cortisol level reduction. Our findings suggest that linalool has beneficial effects on the memory loss and behavioral alterations induced by REM-sleep deprivation through the regulation of serotonin levels.

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References

  1. Andersen, M. L., Martins, P. J., D'Almeida, V., Bignotto, M. and Tufik, S. (2005) Endocrinological and catecholaminergic alterations during sleep deprivation and recovery in male rats. J. Sleep Res. 14, 83-90. https://doi.org/10.1111/j.1365-2869.2004.00428.x
  2. Anjos, P. J., Lima, A. O., Cunha, P. S., De Sousa, D. P., Onofre, A. S., Ribeiro, T. P., Medeiros, I. A., Antoniolli, A. R., Quintans-Junior, L. J. and Santosa, M. R. (2013) Cardiovascular effects induced by linalool in normotensive and hypertensive rats. Z. Naturforsch., C, J. Biosci. 68, 181-190. https://doi.org/10.5560/ZNC.2013.68c0181
  3. de la Pena, J. B., Kim, C. A., Lee, H. L., Yoon, S. Y., Kim, H. J., Hong, E. Y., Kim, G. H., Ryu, J. H., Lee, Y. S., Kim, K. M. and Cheong, J. H. (2014) Luteolin mediates the antidepressant-like effects of Cirsium japonicum in mice, possibly through modulation of the GABAA receptor. Arch. Pharm. Res. 37, 263-269. https://doi.org/10.1007/s12272-013-0229-9
  4. de Lima, M. N., Laranja, D. C., Bromberg, E., Roesler, R. and Schroder, N. (2005) Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behav. Brain Res. 156, 139-143. https://doi.org/10.1016/j.bbr.2004.05.016
  5. Dimitrov, S., Lange, T., Tieken, S., Fehm, H. L. and Born, J. (2004) Sleep associated regulation of T helper 1/T helper 2 cytokine balance in humans. Brain Behav. Immun. 18, 341-348. https://doi.org/10.1016/j.bbi.2003.08.004
  6. Dunn, A. J. and Welch, J. (1991) Stress- and endotoxin-induced increases in brain tryptophan and serotonin metabolism depend on sympathetic nervous system activity. J. Neurochem. 57, 1615-1622. https://doi.org/10.1111/j.1471-4159.1991.tb06359.x
  7. Fadda, P. and Fratta, W. (1997) Stress-induced sleep deprivation modifies corticotropin releasing factor (CRF) levels and CRF binding in rat brain and pituitary. Pharmacol. Res. 35, 443-446. https://doi.org/10.1006/phrs.1997.0155
  8. Giedke, H. and Schwarzler, F. (2002) Therapeutic use of sleep deprivation in depression. Sleep Med. Rev. 6, 361-377. https://doi.org/10.1053/smrv.2002.0235
  9. Guzman-Gutierrez, S. L., Gomez-Cansino, R., Garcia-Zebadua, J. C., Jimenez-Perez, N. C. and Reyes-Chilpa, R. (2012) Antidepressant activity of Litsea glaucescens essential oil: identification of beta-pinene and linalool as active principles. J. Ethnopharmacol. 143, 673-679. https://doi.org/10.1016/j.jep.2012.07.026
  10. Higuchi, M., Suzuki, Y., Yatani, Y., Kitagawa, Y., Nagayasu, K., Shirakawa, H., Nakagawa, T. and Kaneko, S. (2008) Augmentation of serotonin release by sustained exposure to MDMA and methamphetamine in rat organotypic mesencephalic slice cultures containing raphe serotonergic neurons. J. Neurochem. 106, 2410-2420. https://doi.org/10.1111/j.1471-4159.2008.05583.x
  11. Hu, Y., Liu, M., Liu, P., Yan, J. J., Liu, M. Y., Zhang, G. Q., Zhou, X. J. and Yu, B. Y. (2013) Effect of kai xin san on learning and memory in a rat model of paradoxical sleep deprivation. J. Med. Food 16, 280-287. https://doi.org/10.1089/jmf.2012.2486
  12. Huang, L. Z., Wei, L., Zhao, H. F., Huang, B. K., Rahman, K. and Qin, L. P. (2011) The effect of Eleutheroside E on behavioral alterations in murine sleep deprivation stress model. Eur. J. Pharmacol. 658, 150-155. https://doi.org/10.1016/j.ejphar.2011.02.036
  13. Huo, M., Cui, X., Xue, J., Chi, G., Gao, R., Deng, X., Guan, S., Wei, J., Soromou, L. W., Feng, H. and Wang, D. (2013) Anti-inflammatory effects of linalool in RAW 264.7 macrophages and lipopolysaccharide-induced lung injury model. J. Surg. Res. 180, e47-e54. https://doi.org/10.1016/j.jss.2012.10.050
  14. Kwon, S. H., Ma, S. X., Joo, H. J., Lee, S. Y. and Jang, C. G. (2013) Inhibitory effects of eucommia ulmoides Oliv. Bark on scopolamine-induced learning and memory deficits in mice. Biomol. Ther. (Seoul) 21, 462-469. https://doi.org/10.4062/biomolther.2013.074
  15. Linck, V. M., da Silva, A. L., Figueiro, M., Piato, A. L., Herrmann, A. P., Dupont Birck, F., Caramao, E. B., Nunes, D. S., Moreno, P. R. and Elisabetsky, E. (2009) Inhaled linalool-induced sedation in mice. Phytomedicine 16, 303-307. https://doi.org/10.1016/j.phymed.2008.08.001
  16. Ma, Q. P. (2001) Co-localization of 5-HT(1B/1D/1F) receptors and glutamate in trigeminal ganglia in rats. Neuroreport 12, 1589-1591. https://doi.org/10.1097/00001756-200106130-00015
  17. Mabunga, D. F., Gonzales, E. L., Kim, H. J. and Choung, S. Y. (2015) Treatment of GABA from fermented rice germ ameliorates caffeine-induced sleep disturbance in mice. Biomol. Ther. (Seoul) 23, 268-274. https://doi.org/10.4062/biomolther.2015.022
  18. Mathangi, D. C., Shyamala, R. and Subhashini, A. S. (2012) Effect of REM sleep deprivation on the antioxidant status in the brain of Wistar rats. Ann. Neurosci. 19, 161-164.
  19. Mirescu, C., Peters, J. D., Noiman, L. and Gould, E. (2006) Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proc. Natl. Acad. Sci. U.S.A. 103, 19170-19175. https://doi.org/10.1073/pnas.0608644103
  20. Park, H., Seol, G. H., Ryu, S. and Choi, I. Y. (2016) Neuroprotective effects of (-)-linalool against oxygen-glucose deprivation-induced neuronal injury. Arch. Pharm. Res. 39, 555-564. https://doi.org/10.1007/s12272-016-0714-z
  21. Roberts, R. E. and Duong, H. T. (2014) The prospective association between sleep deprivation and depression among adolescents. Sleep 37, 239-244.
  22. Sabogal-Guaqueta, A. M., Osorio, E. and Cardona-Gomez, G. P. (2016) Linalool reverses neuropathological and behavioral impairments in old triple transgenic Alzheimer's mice. Neuropharmacology 102, 111-120. https://doi.org/10.1016/j.neuropharm.2015.11.002
  23. Scheer, F. A., Hilton, M. F., Mantzoros, C. S. and Shea, S. A. (2009) Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. U.S.A. 106, 4453-4458. https://doi.org/10.1073/pnas.0808180106
  24. Silva Brum, L. F., Emanuelli, T., Souza, D. O. and Elisabetsky, E. (2001) Effects of linalool on glutamate release and uptake in mouse cortical synaptosomes. Neurochem. Res. 26, 191-194. https://doi.org/10.1023/A:1010904214482
  25. Silva, R. H., Abilio, V. C., Takatsu, A. L., Kameda, S. R., Grassl, C., Chehin, A. B., Medrano, W. A., Calzavara, M. B., Registro, S., Andersen, M. L., Machado, R. B., Carvalho, R. C., Ribeiro Rde, A., Tufik, S. and Frussa-Filho, R. (2004) Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology 46, 895-903. https://doi.org/10.1016/j.neuropharm.2003.11.032
  26. Silvestri, A. J. (2005) REM sleep deprivation affects extinction of cued but not contextual fear conditioning. Physiol. Behav. 84, 343-349. https://doi.org/10.1016/j.physbeh.2004.11.011
  27. Suchecki, D., Duarte Palma, B. and Tufik, S. (2000) Sleep rebound in animals deprived of paradoxical sleep by the modified multiple platform method. Brain Res. 875, 14-22. https://doi.org/10.1016/S0006-8993(00)02531-2
  28. Tadavarty, R., Kaan, T. K. and Sastry, B. R. (2009) Long-term depression of excitatory synaptic transmission in rat hippocampal CA1 neurons following sleep-deprivation. Exp. Neurol. 216, 239-242. https://doi.org/10.1016/j.expneurol.2008.11.012
  29. van Hulzen, Z. J. and Coenen, A. M. (1981) Paradoxical sleep deprivation and locomotor activity in rats. Physiol. Behav. 27, 741-744. https://doi.org/10.1016/0031-9384(81)90250-X
  30. Williams, E., Stewart-Knox, B., Helander, A., McConville, C., Bradbury, I. and Rowland, I. (2006) Associations between whole-blood serotonin and subjective mood in healthy male volunteers. Biol. Psychol. 71, 171-174. https://doi.org/10.1016/j.biopsycho.2005.03.002
  31. Zhang, C., Zhao, X., Mao, X., Liu, A., Liu, Z., Li, X., Bi, K. and Jia, Y. (2014) Pharmacological evaluation of sedative and hypnotic effects of schizandrin through the modification of pentobarbital-induced sleep behaviors in mice. Eur. J. Pharmacol. 744, 157-163. https://doi.org/10.1016/j.ejphar.2014.09.012

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