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Action of Citral on the Substantia Gelatinosa Neurons of the Trigeminal Subnucleus Caudalis in Juvenile Mice

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Action of Citral on the Substantia Gelatinosa Neurons of the Trigeminal Subnucleus Caudalis in Juvenile Mice [Downloaded free from http://www.cjphysiology.org on Friday, December 13, 2019, IP: 10.232.74.23] Original Article Action of Citral on the Substantia Gelatinosa Neurons of the Trigeminal Subnucleus Caudalis in Juvenile Mice Thao Thi Phuong Nguyen1,2, Seon Hui Jang1, Soo Joung Park1, Dong Hyu Cho3*, Seong Kyu Han1* 1Department of Oral Physiology, School of Dentistry and Institute of Oral Bioscience, Jeonbuk National University, Jeonju, Republic of Korea, 2Faculty of Odonto – Stomatology, Hue University of Medicine and Pharmacy, Hue University, Hue, Vietnam, 3Department of Obstetrics and Gynecology, Jeonbuk National University Hospital-Jeonbuk, National University Medical School, Jeonju, Republic of Korea Abstract The substantia gelatinosa (SG) of the trigeminal subnucleus caudalis (Vc) is admitted as a pivotal site of integrating and regulating orofacial nociceptive inputs. Although citral (3,7-dimethyl-2,6-octadienal) is involved in antinociception, the action mechanism of citral on the SG neurons of the Vc has not been fully clarified yet. In this study, we examined the direct membrane effects of citral and how citral mediates responses on the SG neurons of the Vc in juvenile mice using a whole-cell patch-clamp technique. Under high chloride pipette solution, citral showed repeatable inward currents that persisted in the presence of tetrodotoxin, a voltage-gated Na+ channel blocker, and 6-cyano-7-nitro-quinoxaline-2,3-dione, a non-N-methyl-D-aspartate (NMDA) glutamate receptor antagonist, D-2-amino-5-phosphonopentanoic acid, an NMDA receptor antagonist. However, the citral-induced inward currents were partially blocked by picrotoxin, a gamma-aminobutyric acid (GABAA)-receptor antagonist, or by strychnine, a glycine receptor antagonist. Further, the citral-induced responses were almost blocked by picrotoxin with strychnine. We also found that citral exhibited additive effect with GABA-induced inward currents and glycine-induced inward currents were potentiated by citral. In addition, citral suppressed the firing activities by positive current injection on the SG neurons of the Vc. Taken together, these results demonstrate that citral has glycine- and/ or GABA-mimetic actions and suggest that citral might be a potential target for orofacial pain modulation by the activation of inhibitory neurotransmission in the SG area of the Vc. Keywords: Citral, gamma-aminobutyric acidA receptor, glycine receptor, patch clamp, substantia gelatinosa neuron INTRODUCTION tools about nociceptive mechanisms through their neuronal modulation abilities.[6] Citral (3,7-dimethyl-2,6-octadienal), The substantia gelatinosa (SG) or lamina II of the spinal dorsal also known as lemonal, is a monoterpene aldehyde consisting horn has been admitted as a gate control for the transmission of isomers geranial and neral chemically.[7] It occupies [1,2] of peripheral pain signals to the higher nociceptive center, 75%–85% of the components of Cymbopogon citrates,[7] whereas the trigeminal subnucleus caudalis (Vc), which commonly named lemongrass, a popular culinary herb in exhibits a structural homology with the spinal dorsal horn Asian cuisines or folk medicine in India.[8] With a typical and is also termed the medullary dorsal horn, initially lemon-like odor, citral is widely used as a flavoring agent, receives nociceptive inputs from the orofacial region.[3,4] The a scent in perfume, or an insect repellent.[9] During the past SG neurons of the Vc play a critical role in receiving and decades, there has been an increasing interest in elucidating regulating orofacial nociception from the thin myelinated Aδ its mechanism of action as well as its medical implications for and unmyelinated C primary afferent fibers.[5] *Address for correspondence: Prof. Seong Kyu Han, Natural compounds from medicinal plants, such as morphine, 567 Baekje-daero, Deokjin-gu, Jeonju-si, Jeollabuk-do, 54896 Republic of Korea. menthol, salicylate, and capsaicin, have been powerful E-mail: [email protected] Prof. Dong Hyu Cho, Received:11-Apr-2019 Revised: 18-Sep-2019 Accepted: 04-Oct-2019 20 Geonji-ro, Deokjin-gu, Jeonju-si, Jeollabuk-do, 54907 Republic of Korea. E-mail: [email protected] Published: 24-Oct-2019 Access this article online This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution‑NonCommercial‑ShareAlike 4.0 License, which allows others to remix, Quick Response Code: tweak, and build upon the work non‑commercially, as long as appropriate credit is given and Website: the new creations are licensed under the identical terms. www.cjphysiology.org For reprints contact: [email protected] DOI: How to cite this article: Nguyen TT, Jang SH, Park SJ, Cho DH, Han SK. 10.4103/CJP.CJP_32_19 Action of citral on the substantia gelatinosa neurons of the trigeminal subnucleus caudalis in juvenile mice. Chin J Physiol 2019;62:175-81. © 2019 Chinese Journal of Physiology | Published by Wolters Kluwer - Medknow 175 [Downloaded free from http://www.cjphysiology.org on Friday, December 13, 2019, IP: 10.232.74.23] Nguyen, et al.: Action of citral on the SG neurons of the Vc human beings. A combination between citral and naproxen, a (in mM): 130 C6H11KO7, 10 KCl, 1 CaCl2, 1 MgCl2, 10 HEPES, nonsteroidal anti-inflammatory drug may decrease nociception 4 Mg-ATP, and 10 EGTA (pH = 7.3 with KOH) was used. The and administer minor gastric damage.[10] In addition, with an action potentials induced by current injection of +70 pA were aldehyde function, citral can bind to proteins and induce a counted to compare the number of firings. conformational change, and thus actively manifest antiseptic The tip resistances of the recording electrodes reached from properties that fight both fungal and bacterial infection.[11] 4 to 6 MΩ when filled with KCl-based internal solution. Citral and the leaf extract of lemongrass also act as a calcium Once a gigaohm seal was formed with SG neurons, a slight antagonist and affect spasmolysis through visceral smooth negative pressure was applied to get the whole-cell mode. muscle activity.[8] Although citral has been proved to have Signals were consecutively transferred to an Axopatch antinociceptive effects,[10,12,13] up to date, there have been 200B (Molecular Devices, CA, USA) for amplifying and an little reports about an orofacial pain function of citral. To Axon Digidata 1550B (Molecular Devices, CA, USA) for examine the action of citral on an orofacial nociception site digitizing. Collected data were analyzed with the Axon pClamp in the central nervous system (CNS), we used a whole-cell patch-clamp recording to investigate the direct membrane 10.6 software (Molecular Devices, CA, USA) and Origin 8 currents induced by citral and involved receptors on the SG software (OriginLab Corp., Northampton, MA, USA). neurons of the Vc. Chemicals and statistics All drugs, including citral, picrotoxin, strychnine, glycine, MATERIALS AND METHODS gamma-aminobutyric acid (GABA), and chemicals for Experimental procedure ACSF, were purchased from Sigma-Aldrich (USA), except for 6-cyano-7-nitro-quinoxaline-2,3-dione (CNQX), Animals and brain slice preparation D-2-amino-5-phosphonopentanoic acid (AP5), and Experiments were performed with the permission of the tetrodotoxin (TTX), which were produced by Tocris Experimental Animal Care and Ethics Committee of Jeonbuk Bioscience (Ellisville, MO, USA). Tested drugs were dissolved National University (CBNU 2017–0082). Male and female in ACSF and superfused at known concentrations. ICR mice (postnatal 8–20 days) were housed under a 12 h light/dark cycle (light on at 06:00) and were supplied with All data were shown as the mean ± standard error of the mean. food and water ad libitum. All mice were capitated between A paired t-test was used to compare the difference between 10:00 and 12:00, and the brains were rapidly dissected and the two groups. Level of statistical significance was defined immersed in ice-cold artificial cerebrospinal fluid (ACSF) as P < 0.05. with the following chemical compounds (in mM): 126 NaCl, 2.5 KCl, 2.4 CaCl , 1.2 MgCl , 11 D-glucose, 1.4 NaH PO , 2 2 2 4 RESULTS and 25 NaHCO (pH 7.3–7.4, bubbled with 95% O and 5% 3 2 In this study, 57 neurons of the Vc from 35 juvenile CO2). The brainstem containing the Vc was fixed to 4% agar by cyanoacrylate and then, excised in ice-cold ACSF using a mice aged 8–20 postnatal days were used for whole-cell vibratome (VT1200S, Leica, Nussluch, Eisfeld, Germany). patch-clamp recordings, in which 52 neurons were tested The coronal slices (200 μm in thickness) with the rostral part under voltage-clamp mode and 5 neurons for current pulse of Vc were kept in oxygenated ACSF for at least an hour at experiments. Mean amplitude of citral (2 mM)-induced inward room temperature before electrophysiological recording. current was at 62.4 ± 5.43 pA (n = 52). Whole-cell patch-clamp recording Nondesensitizing and repeatable responses by citral The coronal slices were relocated to the recording chamber, In voltage-clamp mode, citral was consecutively applied submerged, and constantly superfused with ACSF at to examine whether SG neurons were desensitized by the 4–5 ml/min. Slices were observed under an upright repeatable application. The citral-induced inward currents microscope (BX51W1, Olympus, Tokyo, Japan) with by the second application were similar in amplitude to those differential interference contrast optics. The SG neurons of of the first application in 12 neurons tested [Figure 1a]. the Vc were identified as a translucent band, just medial to There was no significant difference in the mean amplitude the spinal trigeminal tract traveling along the lateral edge of of citral-induced inward currents between the first the brain slices. (67.3 ± 7.03 pA) and the second (67.9 ± 8.14 pA) applications [n = 12, P > 0.05; Figure 1b]. Therefore, SG neurons of the Borosilicate glass capillary tubes (PG52151-4, WPI, Vc are not desensitized by the successively administered Sarasota, USA) were pulled on a Flaming Brown puller (P-97, citral-induced inward currents.
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