Biomolecules & Therapeutics

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

DOI QR Code

Quinpirole Increases Melatonin-Augmented Pentobarbital Sleep via Cortical ERK, p38 MAPK, and PKC in Mice

  • Hong, Sa-Ik (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Kwon, Seung-Hwan (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Hwang, Ji-Young (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Ma, Shi-Xun (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Seo, Jee-Yeon (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Ko, Yong-Hyun (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Kim, Hyoung-Chun (Neurotoxicology Program, College of Pharmacy, Korea Institute of Drug Abuse, Kangwon National University) ;
  • Lee, Seok-Yong (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Jang, Choon-Gon (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University)
  • Received : 2015.07.08
  • Accepted : 2016.01.04
  • Published : 2016.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Sleep, which is an essential part of human life, is modulated by neurotransmitter systems, including gamma-aminobutyric acid (GABA) and dopamine signaling. However, the mechanisms that initiate and maintain sleep remain obscure. In this study, we investigated the relationship between melatonin (MT) and dopamine D2-like receptor signaling in pentobarbital-induced sleep and the intracellular mechanisms of sleep maintenance in the cerebral cortex. In mice, pentobarbital-induced sleep was augmented by intraperitoneal administration of 30 mg/kg MT. To investigate the relationship between MT and D2-like receptors, we administered quinpirole, a D2-like receptor agonist, to MT- and pentobarbital-treated mice. Quinpirole (1 mg/kg, i.p.) increased the duration of MT-augmented sleep in mice. In addition, locomotor activity analysis showed that neither MT nor quinpirole produced sedative effects when administered alone. In order to understand the mechanisms underlying quinpirole-augmented sleep, we measured protein levels of mitogen-activated protein kinases (MAPKs) and cortical protein kinases related to MT signaling. Treatment with quinpirole or MT activated extracellular-signal-regulated kinase 1 and 2 (ERK1/2), p38 MAPK, and protein kinase C (PKC) in the cerebral cortex, while protein kinase A (PKA) activation was not altered significantly. Taken together, our results show that quinpirole increases the duration of MT-augmented sleep through ERK1/2, p38 MAPK, and PKC signaling. These findings suggest that modulation of D2-like receptors might enhance the effect of MT on sleep.

Keywords

References

  1. Abrial, E., Betourne, A., Etievant, A., Lucas, G., Scarna, H., Lambas- Senas, L. and Haddjeri, N. (2015) Protein kinase C inhibition rescues manic-like behaviors and hippocampal cell proliferation deficits in the sleep deprivation model of mania. Int. J. Neuropsychopharmacol. 18, pyu031.
  2. Binfare, R. W., Mantovani, M., Budni, J., Santos, A. R. and Rodrigues, A. L. (2010) Involvement of dopamine receptors in the antidepressant- like effect of melatonin in the tail suspension test. Eur. J. Pharmacol. 638, 78-83. https://doi.org/10.1016/j.ejphar.2010.04.011
  3. Bondi, C. D., McKeon, R. M., Bennett, J. M., Ignatius, P. F., Brydon, L., Jockers, R., Melan, M. A. and Witt-Enderby, P. A. (2008) MT1 melatonin receptor internalization underlies melatonin-induced morphologic changes in Chinese hamster ovary cells and these processes are dependent on $G_i$ proteins, MEK 1/2 and microtubule modulation. J. Pineal Res. 44, 288-298. https://doi.org/10.1111/j.1600-079X.2007.00525.x
  4. Brandon, N. J., Delmas, P., Kittler, J. T., McDonald, B. J., Sieghart, W., Brown, D. A., Smart, T. G. and Moss, S. J. (2000) $GABA_A$ receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J. Biol. Chem. 275, 38856-38862. https://doi.org/10.1074/jbc.M004910200
  5. Brandon, N. J., Jovanovic, J. N., Smart, T. G. and Moss, S. J. (2002) Receptor for activated C kinase-1 facilitates protein kinase Cdependent phosphorylation and functional modulation of $GABA_A$ receptors with the activation of G-protein-coupled receptors. J. Neurosci. 22, 6353-6361. https://doi.org/10.1523/JNEUROSCI.22-15-06353.2002
  6. Canales, J. J. and Iversen, S. D. (2000) Dynamic dopamine receptor interactions in the core and shell of nucleus accumbens differentially coordinate the expression of unconditioned motor behaviors. Synapse 36, 297-306. https://doi.org/10.1002/(SICI)1098-2396(20000615)36:4<297::AID-SYN6>3.0.CO;2-M
  7. Costandi, M. (2013) Neurodegeneration: amyloid awakenings. Nature 497, S19-S20. https://doi.org/10.1038/497S19a
  8. Cui, Y., Costa, R. M., Murphy, G. G., Elgersma, Y., Zhu, Y., Gutmann, D. H., Parada, L. F., Mody, I. and Silva, A. J. (2008) Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 135, 549-560. https://doi.org/10.1016/j.cell.2008.09.060
  9. Datta, S. (2007) Activation of pedunculopontine tegmental PKA prevents $GABA_B$ receptor activation-mediated rapid eye movement sleep suppression in the freely moving rat. J. Neurophysiol. 97, 3841-3850. https://doi.org/10.1152/jn.00263.2007
  10. Di Marzo, V., Vial, D., Sokoloff, P., Schwartz, J. C. and Piomelli, D. (1993) Selection of alternative G-mediated signaling pathways at the dopamine $D_2$ receptor by protein kinase C. J. Neurosci. 13, 4846-4853. https://doi.org/10.1523/JNEUROSCI.13-11-04846.1993
  11. Dimpfel, W. (2008) Pharmacological modulation of dopaminergic brain activity and its reflection in spectral frequencies of the rat electropharmacogram. Neuropsychobiology 58, 178-186. https://doi.org/10.1159/000191124
  12. Dumoulin, M. C., Aton, S. J., Watson, A. J., Renouard, L., Coleman, T. and Frank, M. G. (2015) Extracellular signal-regulated kinase (ERK) activity during sleep consolidates cortical plasticity in vivo. Cereb. Cortex 25, 507-515. https://doi.org/10.1093/cercor/bht250
  13. Dyugovskaya, L., Polyakov, A., Cohen-Kaplan, V., Lavie, P. and Lavie, L. (2012) Bax/Mcl-1 balance affects neutrophil survival in intermittent hypoxia and obstructive sleep apnea: effects of p38MAPK and ERK1/2 signaling. J. Transl. Med. 10, 211. https://doi.org/10.1186/1479-5876-10-211
  14. El Helou, J., Belanger-Nelson, E., Freyburger, M., Dorsaz, S., Curie, T., La Spada, F., Gaudreault, P. O., Beaumont, E., Pouliot, P., Lesage, F., Frank, M. G., Franken, P. and Mongrain, V. (2013) Neuroligin-1 links neuronal activity to sleep-wake regulation. Proc. Natl. Acad. Sci. U.S.A. 110, 9974-9979. https://doi.org/10.1073/pnas.1221381110
  15. Foltenyi, K., Greenspan, R. J. and Newport, J. W. (2007) Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat. Neurosci. 10, 1160-1167. https://doi.org/10.1038/nn1957
  16. Hellman, K., Hernandez, P., Park, A. and Abel, T. (2010) Genetic evidence for a role for protein kinase A in the maintenance of sleep and thalamocortical oscillations. Sleep 33, 19-28. https://doi.org/10.1093/sleep/33.1.19
  17. Holmes, S. W. and Sugden, D. (1982) Effects of melatonin on sleep and neurochemistry in the rat. Br. J. Pharmacol. 76, 95-101. https://doi.org/10.1111/j.1476-5381.1982.tb09194.x
  18. Ikeda, M., Hojo, Y., Komatsuzaki, Y., Okamoto, M., Kato, A., Takeda, T. and Kawato, S. (2015) Hippocampal spine changes across the sleep-wake cycle: corticosterone and kinases. J. Endocrinol. 226, M13-M27. https://doi.org/10.1530/JOE-15-0078
  19. Jia, J., Zhu, F., Ma, X., Cao, Z., Li, Y. and Chen, Y. Z. (2009) Mechanisms of drug combinations: interaction and network perspectives. Nat. Rev. Drug Discov. 8, 111-128. https://doi.org/10.1038/nrd2683
  20. Joung, H. Y., Kang, Y. M., Lee, B. J., Chung, S. Y., Kim, K. S. and Shim, I. (2015) Sedative-Hypnotic and Receptor Binding Studies of Fermented Marine Organisms. Biomol. Ther. (Seoul) 23, 479-485. https://doi.org/10.4062/biomolther.2014.122
  21. Jung, E. Y. and Shim, I. (2011) Differential DAergic Control of D1 and D2 Receptor Agonist Over Locomotor Activity and GABA Level in the Striatum. Exp. Neurobiol. 20, 153-157. https://doi.org/10.5607/en.2011.20.3.153
  22. Kim, J. W., Kim, C. S., Hu, Z., Han, J. Y., Kim, S. K., Yoo, S. K., Yeo, Y. M., Chong, M. S., Lee, K., Hong, J. T. and Oh, K. W. (2012) Enhancement of pentobarbital-induced sleep by apigenin through chloride ion channel activation. Arch. Pharm. Res. 35, 367-373. https://doi.org/10.1007/s12272-012-0218-4
  23. Lee, M. Y., Heo, J. S. and Han, H. J. (2006) Dopamine regulates cell cycle regulatory proteins via cAMP, $Ca^{2+}$/PKC, MAPKs, and NF-${\kappa}B$ in mouse embryonic stem cells. J. Cell. Physiol. 208, 399-406. https://doi.org/10.1002/jcp.20674
  24. Lees, G., Edwards, M. D., Hassoni, A. A., Ganellin, C. R. and Galanakis, D. (1998) Modulation of GABA(A) receptors and inhibitory synaptic currents by the endogenous CNS sleep regulator cis-9,10-octadecenoamide (cOA). Br. J. Pharmacol. 124, 873-882. https://doi.org/10.1038/sj.bjp.0701918
  25. Li, G. L., Li, P. and Yang, X. L. (2001) Melatonin modulates ${\gamma}$-aminobutyric $acid_A$ receptor-mediated currents on isolated carp retinal neurons. Neurosci. Lett. 301, 49-53. https://doi.org/10.1016/S0304-3940(01)01558-0
  26. Lim, H., Jang, S., Lee, Y., Moon, S., Kim, J. and Oh, S. (2012) Enhancement of Anxiety and Modulation of TH and pERK Expressions in Amygdala by Repeated Injections of Corticosterone. Biomol. Ther. (Seoul) 20, 418-424. https://doi.org/10.4062/biomolther.2012.20.4.418
  27. Ma, H., Kim, C. S., Ma, Y., Nam, S. Y., Kim, D. S., Woo, S. S., Hong, J. T. and Oh, K. W. (2009) Magnolol enhances pentobarbital-induced sleeping behaviors: possible involvement of GABAergic systems. Phytother. Res. 23, 1340-1344. https://doi.org/10.1002/ptr.2773
  28. Ma, Y., Han, H., Nam, S. Y., Kim, Y. B., Hong, J. T., Yun, Y. P. and Oh, K. W. (2008) Cyclopeptide alkaloid fraction from Zizyphi Spinosi Semen enhances pentobarbital-induced sleeping behaviors. J. Ethnopharmacol. 117, 318-324. https://doi.org/10.1016/j.jep.2008.02.006
  29. Miyamoto, M. (2009) Pharmacology of ramelteon, a selective $MT_1/MT_2$ receptor agonist: a novel therapeutic drug for sleep disorders. CNS Neurosci. Ther. 15, 32-51. https://doi.org/10.1111/j.1755-5949.2008.00066.x
  30. Pandi-Perumal, S. R., Trakht, I., Srinivasan, V., Spence, D. W., Maestroni, G. J., Zisapel, N. and Cardinali, D. P. (2008) Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Prog. Neurobiol. 85, 335-353. https://doi.org/10.1016/j.pneurobio.2008.04.001
  31. Parry, B. L., Fernando Martinez, L., Maurer, E. L., Lopez, A. M., Sorenson, D. and Meliska, C. J. (2006) Sleep, rhythms and women's mood. Part II. Menopause. Sleep Med. Rev. 10, 197-208. https://doi.org/10.1016/j.smrv.2005.09.004
  32. Proença, M. B., Dombrowski, P. A., Da Cunha, C., Fischer, L., Ferraz, A. C. and Lima, M. M. (2014) Dopaminergic D2 receptor is a key player in the substantia nigra pars compacta neuronal activation mediated by REM sleep deprivation. Neuropharmacology 76 Pt A, 118-126. https://doi.org/10.1016/j.neuropharm.2013.08.024
  33. Schindler, C. W. and Carmona, G. N. (2002) Effects of dopamine agonists and antagonists on locomotor activity in male and female rats. Pharmacol. Biochem. Behav. 72, 857-863. https://doi.org/10.1016/S0091-3057(02)00770-0
  34. 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
  35. Sugden, D. (1983) Psychopharmacological effects of melatonin in mouse and rat. J. Pharmacol. Exp. Ther. 227, 587-591.
  36. Takahashi, A., Mikami, M. and Yang, J. (2007) p38 mitogen-activated protein kinase independent SB203580 block of $H_2O_2$-induced increase in GABAergic mIPSC amplitude. Neuroreport 18, 963-967. https://doi.org/10.1097/WNR.0b013e3281a032a3
  37. Vilar, A., de Lemos, L., Patraca, I., Martinez, N., Folch, J., Junyent, F., Verdaguer, E., Pallas, M., Auladell, C. and Camins, A. (2014) Melatonin suppresses nitric oxide production in glial cultures by proinflammatory cytokines through p38 MAPK inhibition. Free Radic. Res. 48, 119-128. https://doi.org/10.3109/10715762.2013.845295
  38. Volkow, N. D., Tomasi, D., Wang, G. J., Telang, F., Fowler, J. S., Logan, J., Benveniste, H., Kim, R., Thanos, P. K. and Ferre, S. (2012) Evidence that sleep deprivation downregulates dopamine D2R in ventral striatum in the human brain. J. Neurosci. 32, 6711-6717. https://doi.org/10.1523/JNEUROSCI.0045-12.2012
  39. Wan, X., Mathers, D. A. and Puil, E. (2003) Pentobarbital modulates intrinsic and GABA-receptor conductances in thalamocortical inhibition. Neuroscience 121, 947-958. https://doi.org/10.1016/j.neuroscience.2003.07.002
  40. Wang, F., Li, J. C., Wu, C. F., Yang, J. Y., Xu, F. and Peng, F. (2002) Hypnotic activity of melatonin: involvement of semicarbazide hydrochloride, blocker of synthetic enzyme for GABA. Acta Pharmacol. Sin. 23, 860-864.
  41. Wilhelmsen-Langeland, A., Saxvig, I. W., Pallesen, S., Nordhus, I. H., Vedaa, O., Lundervold, A. J. and Bjorvatn, B. (2013) A randomized controlled trial with bright light and melatonin for the treatment of delayed sleep phase disorder: effects on subjective and objective sleepiness and cognitive function. J. Biol. Rhythms 28, 306-321. https://doi.org/10.1177/0748730413500126
  42. Wood, L. J., Nail, L. M., Perrin, N. A., Elsea, C. R., Fischer, A. and Druker, B. J. (2006) The cancer chemotherapy drug etoposide (VP- 16) induces proinflammatory cytokine production and sickness behavior- like symptoms in a mouse model of cancer chemotherapyrelated symptoms. Biol. Res. Nurs. 8, 157-169. https://doi.org/10.1177/1099800406290932
  43. Yan, Z., Feng, J., Fienberg, A. A. and Greengard, P. (1999) $D_2$ dopamine receptors induce mitogen-activated protein kinase and cAMP response element-binding protein phosphorylation in neurons. Proc. Natl. Acad. Sci. U.S.A. 96, 11607-11612. https://doi.org/10.1073/pnas.96.20.11607
  44. Zawilska, J. and Iuvone, P. M. (1990) Alpha-2 adrenergic activity of bromocriptine and quinpirole in chicken pineal gland. Effects on melatonin synthesis and [$^3H$]rauwolscine binding. J. Pharmacol. Exp. Ther. 255, 1047-1052.

Cited by

  1. MPTP-Induced Dopamine Depletion in Basolateral Amygdala via Decrease of D2R Activation Suppresses GABAA Receptors Expression and LTD Induction Leading to Anxiety-Like Behaviors vol.10, 2017, https://doi.org/10.3389/fnmol.2017.00247
  2. PAL-12, a new anti-aging hexa-peptoid, inhibits UVB-induced photoaging in human dermal fibroblasts and 3D reconstructed human full skin model, Keraskin-FT™ 2017, https://doi.org/10.1007/s00403-017-1768-6
  3. Liquiritigenin ameliorates memory and cognitive impairment through cholinergic and BDNF pathways in the mouse hippocampus 2017, https://doi.org/10.1007/s12272-017-0954-6
  4. Fast and slow Ca 2+ -dependent hyperpolarization mechanisms connect membrane potential and sleep homeostasis vol.44, 2017, https://doi.org/10.1016/j.conb.2017.05.007
  5. Evodiamine Reduces Caffeine-Induced Sleep Disturbances and Excitation in Mice vol.26, pp.5, 2018, https://doi.org/10.4062/biomolther.2017.146
  6. Dorsal hypothalamic dopaminergic neurons play an inhibitory role in the hypothalamic-pituitary-adrenal axis via activation of D2R in mice pp.17481708, 2018, https://doi.org/10.1111/apha.13187
  7. 6,7,4′-Trihydroxyisoflavone, a major metabolite of daidzein, improves learning and memory via the cholinergic system and the p-CREB/BDNF signaling pathway in mice vol.826, pp.None, 2018, https://doi.org/10.1016/j.ejphar.2018.02.048
  8. Melatonin MT 1 and MT 2 receptor ERK signaling is differentially dependent on G i/o and G q/11 proteins vol.68, pp.4, 2016, https://doi.org/10.1111/jpi.12641