DOI QR코드

DOI QR Code

Two combined amino acids promote sleep activity in caffeine-induced sleepless model systems

  • Hong, Ki-Bae (Department of Biological Sciences and Environmental Sciences Program, Southern Illinois University-Edwardsville) ;
  • Park, Yooheon (Dongguk University Research Institute of Biotechnology and Medical Converged Science, Dongguk University) ;
  • Suh, Hyung Joo (Department of Public Health Sciences, Korea University)
  • Received : 2017.10.25
  • Accepted : 2018.03.13
  • Published : 2018.06.01

Abstract

BACKGROUND/OBJECTIVES: The aim of this study was to evaluate the biological and sleep-promoting effects of combined ${\gamma}$-aminobutyric acid (GABA) and 5-hydroxytryptophan (5-HTP) using caffeine-induced sleepless fruit flies, ICR mice, and Sprague-Dawley rats. MATERIALS/METHODS: Video-tracking analysis was applied to investigate behavioral changes of Drosophila melanogaster. Pentobarbital-induced sleep test and electroencephalogram (EEG) patterns were used for analysis of sleep latency, duration, and quantity and quality of sleep in vertebrate models. RESULTS: Administration of combined GABA/5-HTP could significantly reverse the caffeine induced total distance of flies (P < 0.001). Also, individually administered and combined GABA/5-HTP significantly increased the total sleeping time in the caffeine-induced sleepless ICR mice (P < 0.001). In the caffeine-induced sleepless SD-rats, combined GABA/5-HTP showed significant differences in sleep quality between individual amino acid administrations (P < 0.05). CONCLUSIONS: Taken together, we identified inhibitory effects of combined GABA/5-HTP in locomotor activity, sleep quantity and quality in caffeine-induced sleepless models, indicating that combined GABA/5-HTP may be effective in patients with insomnia by providing sufficient sleep.

Keywords

Sleep;caffeine;GABA;5-HTP;insomnia

Acknowledgement

Supported by : Korea Institute for Advancement of Technology (KIAT)

References

  1. Leger D, Poursain B, Neubauer D, Uchiyama M. An international survey of sleeping problems in the general population. Curr Med Res Opin 2008;24:307-17. https://doi.org/10.1185/030079907X253771
  2. Chen MY, Wang EK, Jeng YJ. Adequate sleep among adolescents is positively associated with health status and health-related behaviors. BMC Public Health 2006;6:59. https://doi.org/10.1186/1471-2458-6-59
  3. Zhang L, Zhao ZX. Objective and subjective measures for sleep disorders. Neurosci Bull 2007;23:236-40. https://doi.org/10.1007/s12264-007-0035-9
  4. Wafford KA, Ebert B. Emerging anti-insomnia drugs: tackling sleeplessness and the quality of wake time. Nat Rev Drug Discov 2008;7:530-40. https://doi.org/10.1038/nrd2464
  5. Schutte-Rodin S, Broch L, Buysse D, Dorsey C, Sateia M. Clinical guideline for the evaluation and management of chronic insomnia in adults. J Clin Sleep Med 2008;4:487-504.
  6. Longo LP, Johnson B. Addiction: part I. Benzodiazepines--side effects, abuse risk and alternatives. Am Fam Physician 2000;61: 2121-8.
  7. Toth LA, Bhargava P. Animal models of sleep disorders. Comp Med 2013;63:91-104.
  8. Haynes PR, Christmann BL, Griffith LC. A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster. eLife 2015;4:e03868.
  9. Yuan Q, Joiner WJ, Sehgal A. A sleep-promoting role for the Drosophila serotonin receptor 1A. Curr Biol 2006;16:1051-62. https://doi.org/10.1016/j.cub.2006.04.032
  10. Bushey D, Tononi G, Cirelli C. Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging. Proc Natl Acad Sci U S A 2015;112: 4785-90. https://doi.org/10.1073/pnas.1419603112
  11. Li Y, Li L, Stephens MJ, Zenner D, Murray KC, Winship IR, Vavrek R, Baker GB, Fouad K, Bennett DJ. Synthesis, transport, and metabolism of serotonin formed from exogenously applied 5-HTP after spinal cord injury in rats. J Neurophysiol 2014;111:145-63. https://doi.org/10.1152/jn.00508.2013
  12. Kuribara H, Asahi T, Tadokoro S. Ethanol enhances, but diazepam and pentobarbital reduce the ambulation-increasing effect of caffeine in mice. Arukoru Kenkyuto Yakubutsu Ison 1992;27:528-39.
  13. Forrest WH Jr, Bellville JW, Brown BW Jr. The interaction of caffeine with pentobarbital as a nighttime hypnotic. Anesthesiology 1972; 36:37-41. https://doi.org/10.1097/00000542-197201000-00007
  14. Shi D, Nikodijevic O, Jacobson KA, Daly JW. Chronic caffeine alters the density of adenosine, adrenergic, cholinergic, GABA, and serotonin receptors and calcium channels in mouse brain. Cell Mol Neurobiol 1993;13:247-61. https://doi.org/10.1007/BF00733753
  15. Lazarus M, Shen HY, Cherasse Y, Qu WM, Huang ZL, Bass CE, Winsky-Sommerer R, Semba K, Fredholm BB, Boison D, Hayaishi O, Urade Y, Chen JF. Arousal effect of caffeine depends on adenosine A2A receptors in the shell of the nucleus accumbens. J Neurosci 2011;31:10067-75. https://doi.org/10.1523/JNEUROSCI.6730-10.2011
  16. Schwierin B, Borbely AA, Tobler I. Effects of N6-cyclopentyladenosine and caffeine on sleep regulation in the rat. Eur J Pharmacol 1996;300:163-71. https://doi.org/10.1016/0014-2999(96)00021-0
  17. Borbely AA, Achermann P. Sleep homeostasis and models of sleep regulation. J Biol Rhythms 1999;14:557-68.
  18. Vyazovskiy VV, Kopp C, Bosch G, Tobler I. The GABAA receptor agonist THIP alters the EEG in waking and sleep of mice. Neuropharmacology 2005;48:617-26. https://doi.org/10.1016/j.neuropharm.2004.12.015
  19. Lancel M, Faulhaber J, Deisz RA. Effect of the GABA uptake inhibitor tiagabine on sleep and EEG power spectra in the rat. Br J Pharmacol 1998;123:1471-7. https://doi.org/10.1038/sj.bjp.0701769
  20. Jouvet M. Sleep and serotonin: an unfinished story. Neuropsychopharmacology 1999;21:24S-27S.
  21. Fukushima T, Ohtsubo T, Tsuda M, Yanagawa Y, Hori Y. Facilitatory actions of serotonin type 3 receptors on GABAergic inhibitory synaptic transmission in the spinal superficial dorsal horn. J Neurophysiol 2009;102:1459-71. https://doi.org/10.1152/jn.91160.2008
  22. Hong KB, Park Y, Suh HJ. Sleep-promoting effects of the GABA/5- HTP mixture in vertebrate models. Behav Brain Res 2016;310:36-41. https://doi.org/10.1016/j.bbr.2016.04.049
  23. Hosie AM, Sattelle DB. Agonist pharmacology of two Drosophila GABA receptor splice variants. Br J Pharmacol 1996;119:1577-85. https://doi.org/10.1111/j.1476-5381.1996.tb16075.x
  24. Leal SM, Neckameyer WS. Pharmacological evidence for GABAergic regulation of specific behaviors in Drosophila melanogaster. J Neurobiol 2002;50:245-61. https://doi.org/10.1002/neu.10030
  25. Baier A, Wittek B, Brembs B. Drosophila as a new model organism for the neurobiology of aggression? J Exp Biol 2002;205:1233-40.
  26. Zhu H, Zhang L, Wang G, He Z, Zhao Y, Xu Y, Gao Y, Zhang L. Sedative and hypnotic effects of supercritical carbon dioxide fluid extraction from Schisandra chinensis in mice. J Food Drug Anal 2016;24:831-8. https://doi.org/10.1016/j.jfda.2016.05.005
  27. Morrow JD, Vikraman S, Imeri L, Opp MR. Effects of serotonergic activation by 5-hydroxytryptophan on sleep and body temperature of C57BL/6J and interleukin-6-deficient mice are dose and time related. Sleep 2008;31:21-33. https://doi.org/10.1093/sleep/31.1.21
  28. Zhao X, Cui XY, Wang LE, Zhang YH. Potentiating effect of diltiazem on pentobarbital-induced hypnosis is augmented by serotonergic system: the TMN and VLPO as key elements in the pathway. Neuropharmacology 2009;56:937-43. https://doi.org/10.1016/j.neuropharm.2009.01.017
  29. Mabunga DF, Gpmzales EL, Kim HJ, Choung SY. Treatment of GABA from fermented rice germ ameliorates caffeine-induced sleep disturbance in mice. Biomol Ther 2015;23:268-74. https://doi.org/10.4062/biomolther.2015.022
  30. Vanover KE, Davis RE. Role of 5-HT2A receptor antagonists in the treatment of insomnia. Nat Sci Sleep 2010;2:139-50.
  31. Hong KB, Park Y, Suh HJ. Sleep-promoting effects of a GABA/5-HTP mixture: Behavioral changes and neuromodulation in an invertebrate model. Life Sci 2016;150:42-9. https://doi.org/10.1016/j.lfs.2016.02.086
  32. Al-Shamma HA, Anderson C, Chuang E, Luthringer R, Grottick AJ, Hauser E, Morgan M, Shanahan W, Teegarden BR, Thomsen WJ, Behan D. Nelotanserin, a novel selective human 5-hydroxytryptamine2A inverse agonist for the treatment of insomnia. J Pharmacol Exp Ther 2010;332:281-90. https://doi.org/10.1124/jpet.109.160994
  33. Gmeiner F, Kolodziejczyk A, Yoshii T, Rieger D, Nassel DR, Helfrich- Forster C. GABA(B) receptors play an essential role in maintaining sleep during the second half of the night in Drosophila melanogaster. J Exp Biol 2013;216:3837-43. https://doi.org/10.1242/jeb.085563
  34. Kantrowitz J, Citrome L, Javitt D. GABA(B) receptors, schizophrenia and sleep dysfunction: a review of the relationship and its potential clinical and therapeutic implications. CNS Drugs 2009;23:681-91. https://doi.org/10.2165/00023210-200923080-00005
  35. Javitt DC, Hashim A, Sershen H. Modulation of striatal dopamine release by glycine transport inhibitors. Neuropsychopharmacology 2005;30:649-56. https://doi.org/10.1038/sj.npp.1300589
  36. Vacher CM, Gassmann M, Desrayaud S, Challet E, Bradaia A, Hoyer D, Waldmeier P, Kaupmann K, Pevet P, Bettler B. Hyperdopaminergia and altered locomotor activity in GABAB1-deficient mice. J Neurochem 2006;97:979-91. https://doi.org/10.1111/j.1471-4159.2006.03806.x
  37. Arnaud C, Gauthier P, Gottesmann C. Study of a GABAC receptor antagonist on sleep-waking behavior in rats. Psychopharmacology (Berl) 2001;154:415-9. https://doi.org/10.1007/s002130000653
  38. Ciranna L. Serotonin as a modulator of glutamate- and GABAmediated neurotransmission: implications in physiological functions and in pathology. Curr Neuropharmacol 2006;4:101-14. https://doi.org/10.2174/157015906776359540
  39. Chung BY, Kilman VL, Keath JR, Pitman JL, Allada R. The GABA(A) receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr Biol 2009;19:386-90.
  40. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E, Hodge JJ, Kang K, Liu X, Garrity PA, Rosbash M, Griffith LC. PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 2008;60:672-82. https://doi.org/10.1016/j.neuron.2008.10.042
  41. Wright KP Jr, Bogan RK, Wyatt JK. Shift work and the assessment and management of shift work disorder (SWD). Sleep Med Rev 2013;17:41-54. https://doi.org/10.1016/j.smrv.2012.02.002
  42. Ko CH, Koon CM, Yu SL, Lee KY, Lau CB, Chan EH, Wing YK, Fung KP, Leung PC. Hypnotic effects of a novel anti-insomnia formula on Drosophila insomnia model. Chin J Integr Med 2016;22:335-43. https://doi.org/10.1007/s11655-014-1625-1
  43. Palkovits M. The rat brain in stereotaxic coordinates. Neuropeptides 1983;3:319. https://doi.org/10.1016/0143-4179(83)90049-5
  44. Paterson LM, Wilson SJ, Nutt DJ, Hutson PH, Ivarsson M. Characterisation of the effects of caffeine on sleep in the rat: a potential model of sleep disruption. J Psychopharmacol 2009;23: 475-86. https://doi.org/10.1177/0269881109104846
  45. Revel FG, Gottowik J, Gatti S, Wettstein JG, Moreau JL. Rodent models of insomnia: a review of experimental procedures that induce sleep disturbances. Neurosci Biobehav Rev 2009;33:874-99. https://doi.org/10.1016/j.neubiorev.2009.03.002
  46. Gilestro GF. Video tracking and analysis of sleep in Drosophila melanogaster. Nat Protoc 2012;7:995-1007. https://doi.org/10.1038/nprot.2012.041
  47. Deboer T. Technologies of sleep research. Cell Mol Life Sci 2007;64: 1227-35. https://doi.org/10.1007/s00018-007-6533-0
  48. Wang ZJ, Yu B, Zhang XQ, Sheng ZF, Li SJ, Huang YL, Cao Q, Cui XY, Cui SY, Zhang YH. Correlations between depression behaviors and sleep parameters after repeated corticosterone injections in rats. Acta Pharmacol Sin 2014;35:879-88. https://doi.org/10.1038/aps.2014.44
  49. Ribeiro JA, Sebastiao AM. Caffeine and adenosine. J Alzheimers Dis 2010;20 Suppl 1:S3-15. https://doi.org/10.3233/JAD-2010-1379
  50. Jabbar SB, Hanly MG. Fatal caffeine overdose: a case report and review of literature. Am J Forensic Med Pathol 2013;34:321-4. https://doi.org/10.1097/PAF.0000000000000058
  51. Snel J, Lorist MM. Effects of caffeine on sleep and cognition. Prog Brain Res 2011;190:105-17.
  52. Paterson LM, Wilson SJ, Nutt DJ, Hutson PH, Ivarsson M. A translational, caffeine-induced model of onset insomnia in rats and healthy volunteers. Psychopharmacology (Berl) 2007;191:943-50. https://doi.org/10.1007/s00213-006-0672-0