Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Evodiamine Reduces Caffeine-Induced Sleep Disturbances and Excitation in Mice

  • Ko, Yong-Hyun (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Shim, Kyu-Yeon (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Lee, Seok-Yong (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Jang, Choon-Gon (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University)
  • Received : 2017.07.17
  • Accepted : 2017.09.14
  • Published : 2018.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Worldwide, caffeine is among the most commonly used stimulatory substances. Unfortunately, significant caffeine consumption is associated with several adverse effects, ranging from sleep disturbances (including insomnia) to cardiovascular problems. This study investigates whether treatment with the Evodia rutaecarpa aqueous extract (ERAE) from berries and its major molecular component, evodiamine, can reduce the adverse caffeine-induced sleep-related and excitation effects. We combined measurements from the pentobarbital-induced sleep test, the open field test, and the locomotor activity test in mice that had been dosed with caffeine. We found that ERAE and evodiamine administration reduced the degree of caffeine-induced sleep disruption during the sleep test. Additionally, we found that evodiamine significantly inhibits caffeine-induced excitation during the open field test, as well as decreasing hyperlocomotion in the locomotor activity test. Additional in vitro experiments showed that caffeine administration decreased the expression of ${\gamma}$-aminobutyric acid $(GABA)_A$ receptor subunits in the mouse hypothalamus. However, evodiamine treatment significantly reversed this expression reduction. Taken together, our results demonstrate that ERAE and its major compound, evodiamine, provide an excellent candidate for the treatment or prevention of caffeine-induced sleep disturbances and excitatory states, and that the mechanism of these beneficial effects acts, at least in part, through the $GABA_A$-ergic system.

Keywords

References

  1. Cho, S., Yang, H., Yoon, M., Kim, J., Kim, D., Kim, J. and Kim, S. B. (2014) Arousal inhibitory effect of phlorotannins on caffeine in pentobarbital-induced mice. Fish Aquat. Sci. 17, 13-18.
  2. Dunwiddie, T. V. and Masino, S. A. (2001) The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24, 31-55. https://doi.org/10.1146/annurev.neuro.24.1.31
  3. Fredholm, B. B., Battig, K., Holmen, J., Nehlig, A. and Zvartau, E. E. (1999) Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol. Rev. 51, 83-133.
  4. Garrett, B. E. and Holtzman, S. G. (1994) $D_1$ and $D_2$ dopamine receptor antagonists block caffeine-induced stimulation of locomotor activity in rats. Pharmacol. Biochem. Behav. 47, 89-94.
  5. Chagraoui, A., Skiba, M., Thuillez, C. and Thibaut, F. (2016) To what extent is it possible to dissociate the anxiolytic and sedative/hypnotic properties of $GABA_A$ receptors modulators? Prog. Neuropsychopharmacol. Biol. Psychiatry 71, 189-202. https://doi.org/10.1016/j.pnpbp.2016.08.001
  6. Hammer, H., Bader, B. M., Ehnert, C., Bundgaard, C., Bunch, L., Hoestgaard-Jensen, K., Schroeder, O. H., Bastlund, J. F., Gramowski-$Vo{\beta}$, A. and Jensen, A. A. (2015) A multifaceted $GABA_A$ receptor modulator: functional properties and mechanism of action of the sedative-hypnotic and recreational drug methaqualone (quaalude). Mol. Pharmacol. 88, 401-420. https://doi.org/10.1124/mol.115.099291
  7. Hong, S. I., Kwon, S. H., Hwang, J. Y., Ma, S. H., Seo, J. Y., Ko, Y. H., Kim, H. C., Lee, S. Y. and Jang, C. G. (2016) Quinpirole increases melatonin-augmented pentobarbital sleep via cortical ERK, p38 MAPK, and PKC in mice. Biomol. Ther. (Seoul) 24, 115-122. https://doi.org/10.4062/biomolther.2015.097
  8. Hughes, R. N. and Hancock, N. J. (2017) Effects of acute caffeine on anxiety-related behavior in rats chronically exposed to the drug, with some evidence of possible withdrawal-reversal. Behav. Brain Res. 321, 87-98. https://doi.org/10.1016/j.bbr.2016.12.019
  9. Jain, N. S., Hirani, K. and Chopde, C. T. (2005) Reversal of caffeine-induced anxiety by neurosteroid 3-alpha-hydroxy-5-alpha-pregnane-20-one in rats. Neuropharmacology 48, 627-638. https://doi.org/10.1016/j.neuropharm.2004.11.016
  10. Jiang, M. L., Zhang, Z. X., Li, Y. Z., Wang, X. H., Yan, W. and Gong, G. Q. (2015) Antidepressant-like effect of evodiamine on chronic unpredictable mild stress rats. Neurosci. Lett. 588, 154-158. https://doi.org/10.1016/j.neulet.2014.12.038
  11. Job, M. O. (2016) Injection of cocaine-amphetamine regulated transcript (CART) peptide into the nucleus accumbens does not inhibit caffeine-induced locomotor activity: implications for CART peptide mechanism. Pharmacol. Biochem. Behav. 148, 8-14. https://doi.org/10.1016/j.pbb.2016.05.001
  12. Kardos, J. and Blandl, T. (1994) Inhibition of a gamma aminobutyric acid A receptor by caffeine. Neuroreport 5, 1249-1252. https://doi.org/10.1097/00001756-199406020-00023
  13. Kayir, H. and Uzbay, I. T. (2004) Evidence for the role of nitric oxide in caffeine-induced locomotor activity in mice. Psychopharmacology (Berl.) 172, 11-15. https://doi.org/10.1007/s00213-003-1625-5
  14. Kwon, Y. O., Hong, J. T. and Oh, K. W. (2017) Rosmarinic acid potentiates pentobarbital-induced sleep behaviors and non-rapid eye movement (NREM) sleep through the activation of $GABA_A$-ergic systems. Biomol. Ther. (Seoul) 25, 105-111. https://doi.org/10.4062/biomolther.2016.035
  15. Lalonde, R. and Strazielle, C. (2010) Relations between open-field, elevated plus-maze, and emergence tests in C57BL/6J and BALB/c mice injected with GABA- and 5HT-anxiolytic agents. Fundam. Clin. Pharmacol. 24, 365-376.
  16. Liao, J. F., Huang, S. Y., Jan, Y. M., Yu, L. L. and Chen, C. F. (1998) Central inhibitory effects of water extract of Acori graminei rhizoma in mice. J. Ethnopharmacol. 61, 185-193. https://doi.org/10.1016/S0378-8741(98)00042-7
  17. Li, S., An, J., Sun, C. K. and Li, Z. W. (2004) Inhibitory effect of caffeine on GABA-activated current in acutely isolated rat dorsal root ganglion neurons. Sheng Li Xue Bao 56, 384-388.
  18. Li, S., Wang, C., Wang, W., Dong, H., Hou, P. and Tang, Y. (2008) Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci. 82, 934-942. https://doi.org/10.1016/j.lfs.2008.02.010
  19. 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
  20. Ma, Y., Ma, H., Jo, Y. J., Kim, D. S., Woo, S. S., Li, R., Hong, J. T., Moon, D. C., Oh, K. W. and Eun, J. S. (2008) Honokiol potentiates pentobarbital-induced sleeping behaviors through $GABA_A$ receptor Cl- channel activation. Biomol. Ther. (Seoul) 16, 328-335. https://doi.org/10.4062/biomolther.2008.16.4.328
  21. Misra, A. L., Vadlamani, N. L. and Pontani, R. B. (1986) Effect of caffeine on cocaine locomotor stimulant activity in rats. Pharmacol. Biochem. Behav. 24, 761-764. https://doi.org/10.1016/0091-3057(86)90587-3
  22. Mohler, H., Benke, D., Benson, J., Luscher, B. and Fritschy, J. M. (1995) $GABA_A$-receptor subtypes in vivo: cellular localization, pharmacology and regulation. Adv. Biochem. Psychopharmacol. 48, 41-56.
  23. Mukhopadhyay, S. and Poddar, M. K. (1995) Caffeine-induced locomotor activity: possible involvement of GABAergic-dopaminergicadenosinergic interaction. Neurochem. Res. 20, 39-44.
  24. Mukhopadhyay, S. and Poddar, M. K. (2000) Long-term caffeine inhibits Ehrlich ascites carcinoma cell-induced induction of central GABAergic activity. Neurochem. Res. 25, 1457-1463. https://doi.org/10.1023/A:1007681124227
  25. Nitz, D. and Siegel, J. M. (1996) GABA release in posterior hypothalamus across sleep-wake cycle. Am. J. Physiol. 271, R1707-R1712.
  26. Powell, K. R. and Holtzman S. G. (1998) Lack of NMDA receptor involvement in caffeine-induced locomotor stimulation and tolerance in rats. Pharmacol. Biochem. Behav. 59, 433-438. https://doi.org/10.1016/S0091-3057(97)00447-4
  27. Prediger, R. D., Da Cunha, C. and Takahashi, R. N. (2005) Antagonistic interaction between adenosine A2A and dopamine D2 receptors modulates the social recognition memory in reserpine-treated rats. Behav. Pharmacol. 16, 209-218. https://doi.org/10.1097/01.fbp.0000166825.62130.9a
  28. Prut, L. and Belzung, C. (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review. Eur. J. Pharmacol. 463, 3-33. https://doi.org/10.1016/S0014-2999(03)01272-X
  29. Roca, D. J., Schiller, G. D. and Farb, D. H. (1988) Chronic caffeine or theophylline exposure reduces ${\gamma}$-aminobutyric acid/benzodiazepine receptor site interactions. Mol. Pharmacol. 33, 481-485.
  30. Sakata, K., Jin, L. and Jha, S. (2010) Lack of promoter IV-driven BDNF transcription results in depression-like behavior. Genes Brain Behav. 9, 712-721. https://doi.org/10.1111/j.1601-183X.2010.00605.x
  31. Seifi, M., Brown, J. F., Mills, J., Bhandari, P., Belelli, D., Lambert, J. J., Rudolph, U. and Swinny, J. D. (2014) Molecular and functional diversity of GABA-A receptors in the enteric nervous system of the mouse colon. J. Neurosci. 34, 10361-10378. https://doi.org/10.1523/JNEUROSCI.0441-14.2014
  32. Shah, V. K., Choi, J. J., Han, J. Y., Lee, M. K., Hong, J. T. and Oh, K. W. (2014) Pachymic acid enhances pentobarbital-induced sleeping behaviors via $GABA_A$-ergic systems in mice. Biomol. Ther. (Seoul) 22, 314-320. https://doi.org/10.4062/biomolther.2014.045
  33. Shin, Y. W., Bae, E. A., Cai, X. F., Lee, J. J. and Kim, D. H. (2007) In vitro and in vivo antiallergic effect of the fructus of Evodia rutaecarpa and its constituents. Biol. Pharm. Bull. 30, 197-199. https://doi.org/10.1248/bpb.30.197
  34. Solinas, M., Ferre, S., You, Z. B., Karcz-Kubicha, M., Popoli, P. and Goldberg, S. R. (2002) Caffeine induces dopamine and glutamate release in the shell of the nucleus accumbens. J. Neurosci. 22, 6321-6324. https://doi.org/10.1523/JNEUROSCI.22-15-06321.2002
  35. Sudakov, S. K., Nazarova, G. A., Alekseeva, E. V. and Kolpakov, A. A. (2015) Peripheral administration of a ${\mu}$-opioid receptor agonist DAMGO suppresses the anxiolytic and stimulatory effects of caffeine. Bull. Exp. Biol. Med. 158, 295-297. https://doi.org/10.1007/s10517-015-2744-9
  36. Sweeney, P., Levack, R., Watters, J., Xu, Z. and Yang, Y. (2016) Caffeine increases food intake while reducing anxiety-related behaviors. Appetite 101, 171-177. https://doi.org/10.1016/j.appet.2016.03.013
  37. Ticku, M. K. and Maksay, G. (1983) Convulsant/depressant site of action at the allosteric benzodiazepine-GABA receptor-ionophore complex. Life Sci. 33, 2363-2375. https://doi.org/10.1016/0024-3205(83)90630-6
  38. Turek, F. W. and Losse-Olson, S. (1986) A benzodiazepine used in the treatment of insomnia phase-shifts the mammalian circadian clock. Nature 321, 167-168. https://doi.org/10.1038/321167a0
  39. Wafford, K. A. and Ebert, B. (2006) Gaboxadol--a new awakening in sleep. Curr. Opin. Pharmacol. 6, 30-36. https://doi.org/10.1016/j.coph.2005.10.004
  40. Yanovsky, Y., Schubring, S., Fleischer, W., Gisselmann, G., Zhu, X. R., Lubbert, H., Hatt, H., Rudolph, U., Haas, H. L. and Sergeeva, O. A. (2012) $GABA_A$ receptors involved in sleep and anaesthesia: ${\beta}1$- versus ${\beta}3$-containing assemblies. Pflugers Arch. 463, 187-199. https://doi.org/10.1007/s00424-011-0988-4
  41. Yuan, S. M., Gao, K., Wang, D. M., Quan, X. Z., Liu, J. N., Ma, C. M., Qin, C. and Zhang, L. F. (2011) Evodiamine improves congnitive abilities in SAMP8 and APP(swe)/PS1(${\Delta}E9$) transgenic mouse models of Alzheimer's disease. Acta Pharmacol. Sin. 32, 295-302. https://doi.org/10.1038/aps.2010.230
  42. Zecharia, A. Y., Nelson, L. E., Gent, T. C., Schumacher, M., Jurd, R., Rudolph, U., Brickley, S. G., Maze, M. and Franks, N. P. (2009) The involvement of hypothalamic sleep pathways in general anesthesia: testing the hypothesis using the $GABA_A$ receptor ${\beta}_3N265M$ knock-in mouse. J. Neurosci. 29, 2177-2187. https://doi.org/10.1523/JNEUROSCI.4997-08.2009
  43. Zhang, Q., Yu, Y. P., Ye, Y. L., Zhang, J. T., Zhang, W. P. and Wei, E. Q. (2011) Spatiotemporal properties of locomotor activity after administration of central nervous stimulants and sedatives in mice. Pharmacol. Biochem. Behav. 97, 577-585. https://doi.org/10.1016/j.pbb.2010.09.011
  44. Zhao, T., Zhang, X., Zhao, Y., Zhang, L., Bai, X., Zhang, J., Zhao, X., Chen, L., Wang, L. and Cui, L. (2014) Pretreatment by evodiamine is neuroprotective in cerebral ischemia: up-regulated pAkt, $pGSK3{\beta}$, down-regulated NF-${\kappa}B$ expression, and ameliorated BBB permeability. Neurochem. Res. 39, 1612-1620. https://doi.org/10.1007/s11064-014-1356-5

Cited by

  1. Evodiamine alleviates kidney ischemia reperfusion injury in rats: A biochemical and histopathological study vol.120, pp.10, 2018, https://doi.org/10.1002/jcb.28976
  2. Hypnotic Effects of Lactobacillus fermentum PS150TM on Pentobarbital-Induced Sleep in Mice vol.11, pp.10, 2018, https://doi.org/10.3390/nu11102409
  3. Caffeine versus antioxidant combination (Antox) and their role in modifying cadmium‐induced testicular injury in adult male albino rats vol.53, pp.2, 2018, https://doi.org/10.1111/and.13948