Browse > Article
http://dx.doi.org/10.4196/kjpp.2020.24.5.433

Inhibitory actions of borneol on the substantia gelatinosa neurons of the trigeminal subnucleus caudalis in mice  

Nguyen, Phuong Thao Thi (Department of Oral Physiology, School of Dentistry & Institute of Oral Bioscience, Jeonbuk National University)
Jang, Seon Hui (Department of Oral Physiology, School of Dentistry & Institute of Oral Bioscience, Jeonbuk National University)
Rijal, Santosh (Department of Oral Physiology, School of Dentistry & Institute of Oral Bioscience, Jeonbuk National University)
Park, Soo Joung (Department of Oral Physiology, School of Dentistry & Institute of Oral Bioscience, Jeonbuk National University)
Han, Seong Kyu (Department of Oral Physiology, School of Dentistry & Institute of Oral Bioscience, Jeonbuk National University)
Publication Information
The Korean Journal of Physiology and Pharmacology / v.24, no.5, 2020 , pp. 433-440 More about this Journal
Abstract
The substantia gelatinosa (SG) of the trigeminal subnucleus caudalis (Vc) is the first relay site for the orofacial nociceptive inputs via the thin myelinated Aδ and unmyelinated C primary afferent fibers. Borneol, one of the valuable time-honored herbal ingredients in traditional Chinese medicine, is a popular treatment for anxiety, anesthesia, and antinociception. However, to date, little is known as to how borneol acts on the SG neurons of the Vc. To close this gap, the whole-cell patch-clamp technique was applied to elucidate the antinociceptive mechanism responding for the actions of borneol on the SG neurons of the Vc in mice. In the voltage-clamp mode, holding at -60 mV, the borneol-induced non-desensitizing inward currents were not affected by tetrodotoxin, a voltage-gated Na+ channel blocker, 6-cyano-7-nitro-quinoxaline-2,3-dione, a non-N-methyl-ᴅ-aspartate (NMDA) glutamate receptor antagonist and DL-2-amino-5-phosphonopentanoic acid, an NMDA receptor antagonist. However, borneol-induced inward currents were partially decreased in the presence of picrotoxin, a γ-aminobutyric acid (GABA)A receptor antagonist, or strychnine, a glycine receptor antagonist, and was almost suppressed in the presence of picrotoxin and strychnine. Though borneol did not show any effect on the glycine-induced inward currents, borneol enhanced GABA-mediated responses. Beside, borneol enhanced the GABA-induced hyperpolarization under the current-clamp mode. Altogether, we suggest that borneol contributes in part toward mediating the inhibitory GABA and glycine transmission on the SG neurons of the Vc and may serve as an herbal therapeutic for orofacial pain ailments.
Keywords
Borneol; GABA receptors; Glycine receptors; Patch-clamp techniques; Substantia gelatinosa;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Romero-Reyes M, Uyanik JM. Orofacial pain management: current perspectives. J Pain Res. 2014;7:99-115.   DOI
2 Melzack R, Wall PD. Pain mechanisms: a new theory. Science. 1965;150(3699):971-979.   DOI
3 Tsai CM, Chiang CY, Yu XM, Sessle BJ. Involvement of trigeminal subnucleus caudalis (medullary dorsal horn) in craniofacial nociceptive reflex activity. Pain. 1999;81:115-128.   DOI
4 Ren K, Dubner R. The role of trigeminal interpolaris-caudalis transition zone in persistent orofacial pain. Int Rev Neurobiol. 2011;97:207-225.   DOI
5 Sessle BJ. Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med. 2000;11:57-91.   DOI
6 Hattori A. [Camphor in the Edo era - camphor and borneol for medicines]. Yakushigaku Zasshi. 2000;35:49-54. Japanese.
7 Almeida JR, Souza GR, Silva JC, Saraiva SR, Junior RG, Quintans Jde S, Barreto Rde S, Bonjardim LR, Cavalcanti SC, Quintans LJ Jr. Borneol, a bicyclic monoterpene alcohol, reduces nociceptive behavior and inflammatory response in mice. ScientificWorldJournal. 2013;2013:808460.
8 Bhatia SP, Letizia CS, Api AM. Fragrance material review on borneol. Food Chem Toxicol. 2008;46 Suppl 11:S77-S80.   DOI
9 Zhou HH, Zhang L, Zhou QG, Fang Y, Ge WH. (+)-Borneol attenuates oxaliplatin-induced neuropathic hyperalgesia in mice. Neuroreport. 2016;27:160-165.   DOI
10 Jiang J, Shen YY, Li J, Lin YH, Luo CX, Zhu DY. (+)-Borneol alleviates mechanical hyperalgesia in models of chronic inflammatory and neuropathic pain in mice. Eur J Pharmacol. 2015;757:53-58.   DOI
11 Nesterkina M, Kravchenko I. Synthesis and pharmacological properties of novel esters based on monoterpenoids and glycine. Pharmaceuticals (Basel). 2017;10:47.   DOI
12 Takaishi M, Uchida K, Fujita F, Tominaga M. Inhibitory effects of monoterpenes on human TRPA1 and the structural basis of their activity. J Physiol Sci. 2014;64:47-57.   DOI
13 Nguyen TTP, Jang SH, Park SJ, Cho DH, Han SK. Action of citral on the substantia gelatinosa neurons of the trigeminal subnucleus caudalis in juvenile mice. Chin J Physiol. 2019;62:175-181.   DOI
14 Katz B, Miledi R. Tetrodotoxin-resistant electric activity in presynaptic terminals. J Physiol. 1969;203:459-487.   DOI
15 Todd AJ, Watt C, Spike RC, Sieghart W. Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci. 1996;16:974-982.   DOI
16 Narahashi T. Chemicals as tools in the study of excitable membranes. Physiol Rev. 1974;54:813-889.   DOI
17 Carpenter TS, Lau EY, Lightstone FC. Identification of a possible secondary picrotoxin-binding site on the GABAA receptor. Chem Res Toxicol. 2013;26:1444-1454.   DOI
18 Dutertre S, Becker CM, Betz H. Inhibitory glycine receptors: an update. J Biol Chem. 2012;287:40216-40223.   DOI
19 Sherkheli MA, Schreiner B, Haq R, Werner M, Hatt H. Borneol inhibits TRPA1, a proinflammatory and noxious pain-sensing cation channel. Pak J Pharm Sci. 2015;28:1357-1363.
20 Granger RE, Campbell EL, Johnston GA. (+)- and (-)-borneol: efficacious positive modulators of GABA action at human recombinant alpha1beta2gamma2L GABAA receptors. Biochem Pharmacol. 2005;69:1101-1111.   DOI
21 Chen GL, Lei M, Zhou LP, Zeng B, Zou F. Borneol is a TRPM8 agonist that increases ocular surface wetness. PLoS One. 2016;11:e0158868.   DOI
22 Chinese Pharmacopoeia Commission. Pharmacopoeia of the People's Republic of China. Beijing: China Medical Science Press; 2010. p.161-162.
23 Ji J, Zhang R, Li H, Zhu J, Pan Y, Guo Q. Analgesic and anti-inflammatory effects and mechanism of action of borneol on photodynamic therapy of acne. Environ Toxicol Pharmacol. 2020;75:103329.   DOI
24 Hall AC, Turcotte CM, Betts BA, Yeung WY, Agyeman AS, Burk LA. Modulation of human GABAA and glycine receptor currents by menthol and related monoterpenoids. Eur J Pharmacol. 2004;506:9-16.   DOI
25 Bowery NG, Smart TG. GABA and glycine as neurotransmitters: a brief history. Br J Pharmacol. 2006;147(Suppl 1):S109-S119.   DOI
26 Cao B, Ni HY, Li J, Zhou Y, Bian XL, Tao Y, Cai CY, Qin C, Wu HY, Chang L, Luo CX, Zhu DY. (+)-Borneol suppresses conditioned fear recall and anxiety-like behaviors in mice. Biochem Biophys Res Commun. 2018;495:1588-1593.   DOI
27 Zhang N, Liu P, He X. [Effect of single-used borneol and combining it with diazepam on content of neurotransmitter in corpus striatum of rats]. Zhongguo Zhong Yao Za Zhi. 2011;36:3180-3183. Chinese.
28 Todd AJ, Sullivan AC. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol. 1990;296:496-505.   DOI