International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Melatonin inhibits nicotinic acetylcholine receptor functions in bovine chromaffin cells

  • Jo, Su-Hyun (Department of Physiology, Institute of Bioscience and Biotechnology, BK21 Plus Graduate Program, Kangwon National University School of Medicine) ;
  • Lee, Seung-Hyun (Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry) ;
  • Kim, Kyong-Tai (Department of Life Sciences, Division of Integrative Bioscience and Biotechnology, Pohang University of Science and Technology) ;
  • Choi, Se-Young (Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry)
  • Received : 2019.05.31
  • Accepted : 2019.06.11
  • Published : 2019.06.30
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Abstract

Melatonin is a neurotransmitter that modulates various physiological phenomena including regulation and maintenance of the circadian rhythm. Nicotinic acetylcholine receptors (nAChRs) play an important role in oral functions including orofacial muscle contraction, salivary secretion, and tooth development. However, knowledge regarding physiological crosstalk between melatonin and nAChRs is limited. In the present study, the melatonin-mediated modulation of nAChR functions using bovine adrenal chromaffin cells, a representative model for the study of nAChRs, was investigated. Melatonin inhibited the nicotinic agonist dimethylphenylpiperazinium (DMPP) iodide-induced cytosolic free $Ca^{2+}$ concentration ($[Ca^{2+}]_i$) increase and norepinephrine secretion in a concentration-dependent manner. The inhibitory effect of melatonin on the DMPP-induced $[Ca^{2+}]_i$ increase was observed when the melatonin treatment was performed simultaneously with DMPP. The results indicate that melatonin inhibits nAChR functions in both peripheral and central nervous systems.

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References

  1. Cipolla-Neto J, Amaral FGD. Melatonin as a hormone: new physiological and clinical insights. Endocr Rev 2018;39:990-1028. doi: 10.1210/er.2018-00084.
  2. Shafabakhsh R, Reiter RJ, Mirzaei H, Teymoordash SN, Asemi Z. Melatonin: a new inhibitor agent for cervical cancer treatment. J Cell Physiol 2019. doi: 10.1002/jcp.28865. [Epub ahead of print]
  3. Kim TD, Woo KC, Cho S, Ha DC, Jang SK, Kim KT. Rhythmic control of AANAT translation by hnRNP Q in circadian melatonin production. Genes Dev 2007;21:797-810. doi: 10.1101/gad.1519507.
  4. Hardeland R. Aging, melatonin, and the pro- and anti-inflammatory networks. Int J Mol Sci 2019;20:E1223. doi: 10.3390/ijms20051223.
  5. Tarocco A, Caroccia N, Morciano G, Wieckowski MR, Ancora G, Garani G, Pinton P. Melatonin as a master regulator of cell death and inflammation: molecular mechanisms and clinical implications for newborn care. Cell Death Dis 2019;10:317. doi: 10.1038/s41419-019-1556-7.
  6. Bloem B, Poorthuis RB, Mansvelder HD. Cholinergic modulation of the medial prefrontal cortex: the role of nicotinic receptors in attention and regulation of neuronal activity. Front Neural Circuits 2014;8:17. doi: 10.3389/fncir.2014.00017.
  7. Yoon JY, Jung SR, Hille B, Koh DS. Modulation of nicotinic receptor channels by adrenergic stimulation in rat pinealocytes. Am J Physiol Cell Physiol 2014;306:C726-35. doi: 10.1152/ajpcell.00354.2013.
  8. Yawo H. Rectification of synaptic and acetylcholine currents in the mouse submandibular ganglion cells. J Physiol 1989;417:307-22. doi: 10.1113/jphysiol.1989.sp017803.
  9. Kashiwagi Y, Yanagita M, Kojima Y, Shimabukuro Y, Murakami S. Nicotine up-regulates IL-8 expression in human gingival epithelial cells following stimulation with IL-1${\beta}$ or P. gingivalis lipopolysaccharide via nicotinic acetylcholine receptor signalling. Arch Oral Biol 2012;57:483-90. doi: 10.1016/j.archoralbio.2011.10.007.
  10. Johnson GK, Guthmiller JM, Joly S, Organ CC, Dawson DV. Interleukin-1 and interleukin-8 in nicotine- and lipopolysaccharide-exposed gingival keratinocyte cultures. J Periodontal Res 2010;45:583-8. doi: 10.1111/j.1600-0765.2009.01262.x.
  11. Almasri A, Wisithphrom K, Windsor LJ, Olson B. Nicotine and lipopolysaccharide affect cytokine expression from gingival fibroblasts. J Periodontol 2007;78:533-41. doi: 10.1902/jop.2007.060296.
  12. Wu X, Gao H, Xiao D, Luo S, Zhao Z. Effects of tensile stress on the alpha1 nicotinic acetylcholine receptor expression in maxillofacial skeletal myocytes. Mol Cell Biochem 2008;311:51-6. doi: 10.1007/s11010-007-9693-1.
  13. Rogers SW, Gahring LC. Nicotinic receptor Alpha7 expression during tooth morphogenesis reveals functional pleiotropy. PLoS One 2012;7:e36467. doi: 10.1371/journal.pone.0036467.
  14. Fenwick EM, Marty A, Neher E. A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J Physiol 1982;331:577-97. doi: 10.1113/jphysiol.1982.sp014393.
  15. Higgins LS, Berg DK. A desensitized form of neuronal acetylcholine receptor detected by 3H-nicotine binding on bovine adrenal chromaffin cells. J Neurosci 1988;8:1436-46. https://doi.org/10.1523/JNEUROSCI.08-04-01436.1988
  16. Artalejo CR, Adams ME, Fox AP. Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells. Nature 1994;367:72-6. doi: 10.1038/367072a0.
  17. Kilpatrick DL, Ledbetter FH, Carson KA, Kirshner AG, Slepetis R, Kirshner N. Stability of bovine adrenal medulla cells in culture. J Neurochem 1980;35:679-92. doi: 10.1111/j.1471-4159.1980.tb03707.x
  18. Kim KT, Choi SY, Park TJ. Neomycin inhibits catecholamine secretion by blocking nicotinic acetylcholine receptors in bovine adrenal chromaffin cells. J Pharmacol Exp Ther 1999;288:73-80.
  19. Lee K, Kim YJ, Choi LM, Choi S, Nam H, Ko HY, Chung G, Lee JH, Jo SH, Lee G, Choi SY, Park K. Human salivary gland cells express bradykinin receptors that modulate the expression of proinflammatory cytokines. Eur J Oral Sci 2017;125:18-27. doi: 10.1111/eos.12324.
  20. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985;260:3440-50. https://doi.org/10.1016/S0021-9258(19)83641-4
  21. Markus RP, Zago WM, Carneiro RC. Melatonin modulation of presynaptic nicotinic acetylcholine receptors in the rat vas deferens. J Pharmacol Exp Ther 1996;279:18-22. doi:10.1590/S0100-879X1999000800010.
  22. Barajas-Lopez C, Peres AL, Espinosa-Luna R, Reyes-Vazquez C, Prieto-Gomez B. Melatonin modulates cholinergic transmission by blocking nicotinic channels in the guinea-pig submucous plexus. Eur J Pharmacol 1996;312:319-25. doi:10.1016/0014-2999(96)00481-5.
  23. Parada E, Egea J, Buendia I, Negredo P, Cunha AC, Cardoso S, Soares MP, Lopez MG. The microglial ${\alpha}$7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid Redox Signal 2013;19:1135-48. doi: 10.1089/ars.2012.4671.
  24. Oishi A, Cecon E, Jockers R. Melatonin receptor signaling:impact of receptor oligomerization on receptor function. Int Rev Cell Mol Biol 2018;338:59-77. doi: 10.1016/bs.ircmb.2018.02.002.
  25. Lax P. Melatonin inhibits nicotinic currents in cultured rat cerebellar granule neurons. J Pineal Res 2008;44:70-7. doi:10.1111/j.1600-079X.2007.00481.x.
  26. Choi TY, Kwon JE, Durrance ES, Jo SH, Choi SY, Kim KT. Melatonin inhibits voltage-sensitive Ca(2+) channel-mediated neurotransmitter release. Brain Res 2014;1557:34-42. doi:10.1016/j.brainres.2014.02.023.
  27. Markus RP, Silva CL, Franco DG, Barbosa EM Jr, Ferreira ZS. Is modulation of nicotinic acetylcholine receptors by melatonin relevant for therapy with cholinergic drugs? Pharmacol Ther 2010;126:251-62. doi: 10.1016/j.pharmthera.2010.02.009.