Expression of Cannabinoid Receptors in the Trigeminal Ganglion of the Horse.
Abstract: Cannabinoid receptors are expressed in human and animal trigeminal sensory neurons; however, the expression in the equine trigeminal ganglion is unknown. Ten trigeminal ganglia from five horses were collected post-mortem from an abattoir. The expression of cannabinoid receptors type 1 (CB1R) and type 2 (CB2R), and the cannabinoid-related receptors like transient receptor potential vanilloid type 1 (TRPV1), peroxisome proliferator-activated receptor gamma (PPARɣ), and G protein-related receptor 55 (GPR55) in the trigeminal ganglia (TG) of the horse were studied, using immunofluorescence on cryosections and formalin-fixed paraffin-embedded (FFPE) sections. Neurons and glial cells were identified using fluorescent Nissl staining NeuroTrace and an antibody directed against the glial marker glial fibrillary acidic protein (GFAP), respectively. Macrophages were identified by means of an antibody directed against the macrophages/microglia marker ionized calcium-binding adapter molecule 1 (IBA1). The protein expression of CB1R, CB2R, TRPV1, and PPARɣ was found in the majority of TG neurons in both cryosections and FFPE sections. The expression of GPR55 immunoreactivity was mainly detectable in FFPE sections, with expression in the majority of sensory neurons. Some receptors were also observed in glial cells (CB2R, TRPV1, PPARγ, and GPR55) and inflammatory cells (PPARγ and GPR55). These results support further investigation of such receptors in disorders of equine trigeminal neuronal excitability.
Publication Date: 2023-11-03 PubMed ID: 37958932PubMed Central: PMC10648827DOI: 10.3390/ijms242115949Google Scholar: Lookup
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Summary
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The research paper explores the presence of cannabinoid receptors in the trigeminal ganglia, a bundle of nerves in the horse’s head. These receptors were confirmed to exist in a majority of the nervous cells examined through various staining and immunofluorescence techniques.
Research Methodology and Techniques
- The study was done on ten trigeminal ganglia collected post-mortem from five horses sourced from an abattoir.
- The researchers were focused on identifying the expression of cannabinoid receptors type 1 (CB1R) and type 2 (CB2R), along with other receptors such as transient receptor potential vanilloid type 1 (TRPV1), peroxisome proliferator-activated receptor gamma (PPARɣ), and G protein-related receptor 55 (GPR55) in the horse’s trigeminal ganglia.
- They used immunofluorescence on cryosections and formalin-fixed paraffin-embedded (FFPE) sections, techniques commonly used in neuropathology to visualize and study cell structures and functions.
- Neurons and glial cells, two types of brain cells, were identified using fluorescent Nissl staining NeuroTrace and an antibody against the glial marker glial fibrillary acidic protein (GFAP), respectively.
- Macrophages, a type of immune cell, were identified using an antibody directed against macrophages/microglia marker ionized calcium-binding adapter molecule 1 (IBA1).
Findings of the Research
- The study revealed that CB1R, CB2R, TRPV1, and PPARɣ proteins were found in the majority of trigeminal ganglia neurons in both cryosections and FFPE sections.
- The researchers also noticed that the expression of GPR55 immunoreactivity was mainly detectable in FFPE sections, with its expression present in the majority of the sensory neurons.
- In addition to neurons, glial cells also showed evidence of some receptors (CB2R, TRPV1, PPARγ, and GPR55), with the presence of these receptors also found in certain inflammatory cells (PPARγ and GPR55).
Implications of the Research
- The recognition of these receptor types in the horse’s trigeminal ganglia is significant as it could highlight the potential therapeutic value of cannabinoids and related substances in the treatment of disorders associated with equine trigeminal neuronal excitability.
- As these cannabinoid receptors are expressed in both human and animal trigeminal sensory neurons, findings from this research could also have extended implications for therapeutic interventions for pain or inflammation in other mammals, including humans.
Cite This Article
APA
Zamith Cunha R, Semprini A, Salamanca G, Gobbo F, Morini M, Pickles KJ, Roberts V, Chiocchetti R.
(2023).
Expression of Cannabinoid Receptors in the Trigeminal Ganglion of the Horse.
Int J Mol Sci, 24(21), 15949.
https://doi.org/10.3390/ijms242115949 Publication
Researcher Affiliations
- Department of Veterinary Medical Sciences, University of Bologna, 37200 Bologna, Italy.
- Department of Veterinary Medical Sciences, University of Bologna, 37200 Bologna, Italy.
- Department of Veterinary Medical Sciences, University of Bologna, 37200 Bologna, Italy.
- Department of Veterinary Medical Sciences, University of Bologna, 37200 Bologna, Italy.
- Department of Veterinary Medical Sciences, University of Bologna, 37200 Bologna, Italy.
- School of Veterinary Medicine and Science, University of Nottingham, Nottingham LE12 5RD, UK.
- Bristol Vet School, University of Bristol, Bristol BS40 5DU, UK.
- Department of Veterinary Medical Sciences, University of Bologna, 37200 Bologna, Italy.
MeSH Terms
- Humans
- Horses
- Animals
- Receptors, Cannabinoid / metabolism
- Trigeminal Ganglion / metabolism
- PPAR gamma / metabolism
- Neurons / metabolism
- Neuroglia / metabolism
- TRPV Cation Channels / genetics
- TRPV Cation Channels / metabolism
Grant Funding
- 2023 / Formula Swiss AG, Swiss
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 84 references
- Ross S.E., Murray J.K., Roberts V.L.H.. Prevalence of Headshaking within the Equine Population in the UK.. Equine Vet. J. 2018;50:73–78.
- Roberts V.L., Fews D., McNamara J.M., Love S.. Trigeminal Nerve Root Demyelination Not Seen in Six Horses Diagnosed with Trigeminal-Mediated Headshaking.. Front. Vet. Sci. 2017;4:72.
- Aleman M., Rhodes D., Williams D.C., Guedes A., Madigan J.E.. Sensory Evoked Potentials of the Trigeminal Nerve for the Diagnosis of Idiopathic Headshaking in a Horse.. J. Vet. Int. Med. 2014;28:250–253.
- Elliott M.B., Ward S.J., Abood M.E., Tuma R.F., Jallo J.I.. Understanding the Endocannabinoid System as a Modulator of the Trigeminal Pain Response to Concussion.. Concussion 2017;2:CNC49.
- Morales P., Hurst D.P., Reggio P.H.. Molecular Targets of the Phytocannabinoids: A Complex Picture.. In: Kinghorn A.D., Falk H., Gibbons S., Kobayashi J., editors. Phytocannabinoids. Volume 103. Springer International Publishing; Cham, Switzerland: 2017. pp. 103–131. Progress in the Chemistry of Organic Natural Products..
- Ligresti A., De Petrocellis L., Di Marzo V.. From Phytocannabinoids to Cannabinoid Receptors and Endocannabinoids: Pleiotropic Physiological and Pathological Roles Through Complex Pharmacology.. Physiol. Rev. 2016;96:1593–1659.
- Liang Y., Huang C., Hsu K.. Therapeutic Potential of Cannabinoids in Trigeminal Neuralgia.. Curr. Drug Targets CNS Neurol. Disord. 2004;3:507–514.
- Lee G., Grovey B., Furnish T., Wallace M.. Medical Cannabis for Neuropathic Pain.. Curr. Pain. Headache Rep. 2018;22:8.
- Ellis K.L., Contino E.K.. Treatment Using Cannabidiol in a Horse with Mechanical Allodynia.. Equine Vet. Educ. 2021;33:e79–e82.
- Sánchez-Aparicio P., Florán B., Rodríguez Velázquez D., Ibancovichi J.A., Varela Guerrero J.A., Recillas S.. Cannabinoids CB2 Receptors, One New Promising Drug Target for Chronic and Degenerative Pain Conditions in Equine Veterinary Patients.. J. Equine Vet. Sci. 2020;85:102880.
- Luedke C., Wilhelm T.. Cannabinoids in Equine Medicine.. In: Cital S., Kramer K., Hughston L., Gaynor J.S., editors. Cannabis Therapy in Veterinary Medicine: A Complete Guide. Springer International Publishing; Cham, Switzerland: 2021. pp. 295–305..
- Zamith Cunha R., Zannoni A., Salamanca G., De Silva M., Rinnovati R., Gramenzi A., Forni M., Chiocchetti R.. Expression of Cannabinoid (CB1 and CB2) and Cannabinoid-Related Receptors (TRPV1, GPR55, and PPARα) in the Synovial Membrane of the Horse Metacarpophalangeal Joint.. Front. Vet. Sci. 2023;10:1045030.
- Chiocchetti R., Rinnovati R., Tagliavia C., Stanzani A., Galiazzo G., Giancola F., Silva M.D., Capodanno Y., Spadari A.. Localisation of Cannabinoid and Cannabinoid-Related Receptors in the Equine Dorsal Root Ganglia.. Equine Vet. J. 2021;53:549–557.
- Galiazzo G., Tagliavia C., Giancola F., Rinnovati R., Sadeghinezhad J., Bombardi C., Grandis A., Pietra M., Chiocchetti R.. Localisation of Cannabinoid and Cannabinoid-Related Receptors in the Horse Ileum.. J. Equine Vet. Sci. 2021;104:103688.
- Tajti J., Szok D., Csáti A., Szabó Á., Tanaka M., Vécsei L.. Exploring Novel Therapeutic Targets in the Common Pathogenic Factors in Migraine and Neuropathic Pain.. Int. J. Mol. Sci. 2023;24:4114.
- Greco R., Demartini C., Zanaboni A.M., Francavilla M., De Icco R., Ahmad L., Tassorelli C.. The Endocannabinoid System and Related Lipids as Potential Targets for the Treatment of Migraine-related Pain.. Headache 2022;62:227–240.
- Richardson D., Pearson R.G., Kurian N., Latif M.L., Garle M.J., Barrett D.A., Kendall D.A., Scammell B.E., Reeve A.J., Chapman V.. Characterisation of the Cannabinoid Receptor System in Synovial Tissue and Fluid in Patients with Osteoarthritis and Rheumatoid Arthritis.. Arthritis Res. Ther. 2008;10:R43.
- O’Brien M., McDougall J.J.. Cannabis and Joints: Scientific Evidence for the Alleviation of Osteoarthritis Pain by Cannabinoids.. Curr. Opin. Pharmacol. 2018;40:104–109.
- Lowe H., Toyang N., Steele B., Bryant J., Ngwa W.. The Endocannabinoid System: A Potential Target for the Treatment of Various Diseases.. Int. J. Mol. Sci. 2021;22:9472.
- Fiani B., Sarhadi K.J., Soula M., Zafar A., Quadri S.A.. Current Application of Cannabidiol (CBD) in the Management and Treatment of Neurological Disorders.. Neurol. Sci. 2020;41:3085–3098.
- Longworth J., Szafron M., Gruza A., Da Silva K.. Cannabis and Cannabinoid Medications for the Treatment of Chronic Orofacial Pain: A Scoping Review.. Dent. Rev. 2023;3:100063.
- Price T.J., Helesic G., Parghi D., Hargreaves K.M., Flores C.M.. The Neuronal Distribution of Cannabinoid Receptor Type 1 in the Trigeminal Ganglion of the Rat.. Neuroscience 2003;120:155–162.
- Christiansen I.M., Edvinsson J.C.A., Reducha P.V., Edvinsson L., Haanes K.A.. Dual Action of the Cannabinoid Receptor 1 Ligand Arachidonyl-2′-Chloroethylamide on Calcitonin Gene-Related Peptide Release.. J. Headache Pain. 2022;23:30.
- Aleman M., Williams D.C., Brosnan R.J., Nieto J.E., Pickles K.J., Berger J., Lecouteur R.A., Holliday T.A., Madigan J.E.. Sensory Nerve Conduction and Somatosensory Evoked Potentials of the Trigeminal Nerve in Horses with Idiopathic Headshaking.. J. Vet. Intern. Med. 2013;27:1571–1580.
- Greco R., Gasperi V., Maccarrone M., Tassorelli C.. The Endocannabinoid System and Migraine.. Exp. Neurol. 2010;224:85–91.
- Russo D., Bombardi C., Castellani G., Chiocchetti R.. Characterization of Spinal Ganglion Neurons in Horse (Equus caballus). A Morphometric, Neurochemical and Tracing Study.. Neuroscience 2011;176:53–71.
- Ahluwalia J., Urban L., Capogna M., Bevan S., Nagy I.. Cannabinoid 1 Receptors Are Expressed in Nociceptive Primary Sensory Neurons.. Neuroscience 2000;100:685–688.
- Bridges D., Rice A.S.C., Egertová M., Elphick M.R., Winter J., Michael G.J.. Localisation of Cannabinoid Receptor 1 in Rat Dorsal Root Ganglion Using in Situ Hybridisation and Immunohistochemistry.. Neuroscience 2003;119:803–812.
- Agarwal N., Pacher P., Tegeder I., Amaya F., Constantin C.E., Brenner G.J., Rubino T., Michalski C.W., Marsicano G., Monory K.. Cannabinoids Mediate Analgesia Largely via Peripheral Type 1 Cannabinoid Receptors in Nociceptors.. Nat. Neuro Sci. 2007;10:870–879.
- Chiocchetti R., Galiazzo G., Tagliavia C., Stanzani A., Giancola F., Menchetti M., Militerno G., Bernardini C., Forni M., Mandrioli L.. Cellular Distribution of Canonical and Putative Cannabinoid Receptors in Canine Cervical Dorsal Root Ganglia.. Front. Vet. Sci. 2019;6:313.
- Khasabova I.A., Simone D.A., Seybold V.S.. Cannabinoids Attenuate Depolarization-Dependent Ca2+ Influx in Intermediate-Size Primary Afferent Neurons of Adult Rats.. Neuroscience 2002;115:613–625.
- Lalonde M.R., Jollimore C.A.B., Stevens K., Barnes S., Kelly M.E.M.. Cannabinoid Receptor-Mediated Inhibition of Calcium Signaling in Rat Retinal Ganglion Cells.. Mol. Vis. 2006;12:1160–1166.
- Zhang Y., Xie H., Lei G., Li F., Pan J., Liu C., Liu Z., Liu L., Cao X.. Regulatory Effects of Anandamide on Intracellular Ca2+ Concentration Increase in Trigeminal Ganglion Neurons.. Neural Regen. Res. 2014;9:878.
- Price T.J., Patwardhan A., Akopian A.N., Hargreaves K.M., Flores C.M.. Modulation of Trigeminal Sensory Neuron Activity by the Dual Cannabinoid-Vanilloid Agonists Anandamide, N -Arachidonoyl-Dopamine and Arachidonyl-2-Chloroethylamide: Cannabinoid-Vanilloid Modulation of Trigeminal Neuron Activity.. Br. J. Pharmacol. 2004;141:1118–1130.
- Akerman S., Holland P.R., Goadsby P.J.. Cannabinoid (CB1) Receptor Activation Inhibits Trigeminovascular Neurons.. J. Pharmacol. Exp. Ther. 2007;320:64–71.
- Atwood B.K., Mackie K.. CB2: A Cannabinoid Receptor with an Identity Crisis.. Br. J. Pharmacol. 2010;160:467–479.
- Anand U., Otto W.R., Sanchez-Herrera D., Facer P., Yiangou Y., Korchev Y., Birch R., Benham C., Bountra C., Chessell I.P.. Cannabinoid Receptor CB2 Localisation and Agonist-Mediated Inhibition of Capsaicin Responses in Human Sensory Neurons.. Pain 2008;138:667–680.
- Gutierrez T., Crystal J.D., Zvonok A.M., Makriyannis A., Hohmann A.G.. Self-Medication of a Cannabinoid CB2 Agonist in an Animal Model of Neuropathic Pain.. Pain 2011;152:1976–1987.
- Rogers N.. Cannabinoid Receptor with an “identity Crisis” Gets a Second Look.. Nat. Med. 2015;21:966–967.
- Svízenská I.H., Brázda V., Klusáková I., Dubový P.. Bilateral Changes of Cannabinoid Receptor Type 2 Protein and mRNA in the Dorsal Root Ganglia of a Rat Neuropathic Pain Model.. J. Histochem. Cytochem. 2013;61:529–547.
- Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D.. The Cloned Capsaicin Receptor Integrates Multiple Pain-Producing Stimuli.. Neuron 1998;21:531–543.
- Russo D., Clavenzani P., Sorteni C., Bo Minelli L., Botti M., Gazza F., Panu R., Ragionieri L., Chiocchetti R.. Neurochemical Features of Boar Lumbosacral Dorsal Root Ganglion Neurons and Characterization of Sensory Neurons Innervating the Urinary Bladder Trigone.. J. Comp. Neurol. 2013;521:342–366.
- Tanimoto T., Takeda M., Nasu M., Kadoi J., Matsumoto S.. Immunohistochemical Co-Expression of Carbonic Anhydrase II with Kv1.4 and TRPV1 in Rat Small-Diameter Trigeminal Ganglion Neurons.. Brain Res. 2005;1044:262–265.
- Ichikawa H., Sugimoto T.. VR1-Immunoreactive Primary Sensory Neurons in the Rat Trigeminal Ganglion.. Brain Res. 2001;890:184–188.
- Patapoutian A., Peier A.M., Story G.M., Viswanath V.. ThermoTRP Channels and beyond: Mechanisms of Temperature Sensation.. Nat. Rev. Neurosci. 2003;4:529–539.
- Culshaw A.J., Bevan S., Christiansen M., Copp P., Davis A., Davis C., Dyson A., Dziadulewicz E.K., Edwards L., Eggelte H.. Identification and Biological Characterization of 6-Aryl-7-Isopropylquinazolinones as Novel TRPV1 Antagonists That Are Effective in Models of Chronic Pain.. J. Med. Chem. 2006;49:471–474.
- Krause J.E., Chenard B.L., Cortright D.N.. Transient Receptor Potential Ion Channels as Targets for the Discovery of Pain Therapeutics.. Curr. Opin. Investig. Drugs. 2005;6:48–57.
- Marwaha L., Bansal Y., Singh R., Saroj P., Sodhi R.K., Kuhad A.. Niflumic Acid, a TRPV1 Channel Modulator, Ameliorates Stavudine-Induced Neuropathic Pain.. Inflammopharmacol. 2016;24:319–334.
- Sagar D.R., Gaw A.G., Okine B.N., Woodhams S.G., Wong A., Kendall D.A., Chapman V.. Dynamic Regulation of the Endocannabinoid System: Implications for Analgesia.. Mol. Pain. 2009;5:59.
- Di Marzo V., Piscitelli F.. The Endocannabinoid System and Its Modulation by Phytocannabinoids.. Neurotherapeutics 2015;12:692–698.
- Mlost J., Bryk M., Starowicz K.. Cannabidiol for Pain Treatment: Focus on Pharmacology and Mechanism of Action.. Int. J. Mol. Sci. 2020;21:8870.
- Barak Y., Nelson M.C., Ong E.S., Jones Y.Z., Ruiz-Lozano P., Chien K.R., Koder A., Evans R.M.. PPARγ Is Required for Placental, Cardiac, and Adipose Tissue Development.. Mol. Cell. 1999;4:585–595.
- Tontonoz P., Spiegelman B.M.. Fat and Beyond: The Diverse Biology of PPARγ.. Annu. Rev. Biochem. 2008;77:289–312.
- Zhao X., Ou Z., Grotta J.C., Waxham N., Aronowski J.. Peroxisome-Proliferator-Activated Receptor-Gamma (PPARγ) Activation Protects Neurons from NMDA Excitotoxicity.. Brain Res. 2006;1073–1074:460–469.
- Quintanilla R.A., Utreras E., Cabezas-Opazo F.A.. Role of PPARγ in the Differentiation and Function of Neurons.. PPAR Res. 2014;2014:e768594.
- Maeda T., Kishioka S.. International Review of Neurobiology.. Volume 85. Academic Press; Cambridge, MA, USA: 2009. Chapter 13 PPAR and Pain; pp. 165–177..
- Lyons D.N., Zhang L., Danaher R.J., Miller C.S., Westlund K.N.. PPARγ agonists attenuate trigeminal neuropathic pain.. Clin. J. Pain. 2017;33:1071–1080.
- Churi S.B., Abdel-Aleem O.S., Tumber K.K., Scuderi-Porter H., Taylor B.K.. Intrathecal Rosiglitazone Acts at Peroxisome Proliferator-Activated Receptor-Gamma to Rapidly Inhibit Neuropathic Pain in Rats.. J. Pain. 2008;9:639–649.
- Vučković S., Srebro D., Vujović K.S., Vučetić Č., Prostran M.. Cannabinoids and Pain: New Insights From Old Molecules.. Front. Pharmacol. 2018;9:1259.
- Aviram J., Samuelly-Leichtag G.. Efficacy of Cannabis-Based Medicines for Pain Management: A Systematic Review and Meta-Analysis of Randomized Controlled Trials.. Pain Physician. 2017;20:E755–E796.
- Hill K.P.. Medical Marijuana for Treatment of Chronic Pain and Other Medical and Psychiatric Problems: A Clinical Review.. JAMA 2015;313:2474.
- Chu Y., Jia S., Xu K., Liu Q., Mai L., Liu J., Fan W., Huang F.. Single-Cell Transcriptomic Profile of Satellite Glial Cells in Trigeminal Ganglion.. Front. Mol. Neurosci. 2023;16:1117065.
- Takahashi Y., Hasegawa-Moriyama M., Sakurai T., Inada E.. The Macrophage-Mediated Effects of the Peroxisome Proliferator-Activated Receptor-Gamma Agonist Rosiglitazone Attenuate Tactile Allodynia in the Early Phase of Neuropathic Pain Development.. Anesth. Analg. 2011;113:398–404.
- Hasegawa-Moriyama M., Kurimoto T., Nakama M., Godai K., Kojima M., Kuwaki T., Kanmura Y.. Peroxisome Proliferator-Activated Receptor-Gamma Agonist Rosiglitazone Attenuates Inflammatory Pain through the Induction of Heme Oxygenase-1 in Macrophages.. Pain 2013;154:1402–1412.
- Ryberg E., Larsson N., Sjögren S., Hjorth S., Hermansson N.-O., Leonova J., Elebring T., Nilsson K., Drmota T., Greasley P.J.. The Orphan Receptor GPR55 Is a Novel Cannabinoid Receptor.. Br. J. Pharmacol. 2007;152:1092–1101.
- Console-Bram L., Marcu J., Abood M.E.. Cannabinoid Receptors: Nomenclature and Pharmacological Principles.. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2012;38:4–15.
- Chiocchetti R., De Silva M., Aspidi F., Cunha R.Z., Gobbo F., Tagliavia C., Sarli G., Morini M.. Distribution of Cannabinoid Receptors in Keratinocytes of Healthy Dogs and Dogs with Atopic Dermatitis.. Front. Vet. Sci. 2022;9:915896.
- Ono T., Yamashita T., Kano R., Inoue M., Okada S., Kano K., Koizumi S., Iwabuchi K., Hirabayashi Y., Matsuo I.. GPR55 Contributes to Neutrophil Recruitment and Mechanical Pain Induction after Spinal Cord Compression in Mice.. Brain Behav. Immun. 2023;110:276–287.
- Carey L.M., Gutierrez T., Deng L., Lee W.-H., Mackie K., Hohmann A.G.. Inflammatory and Neuropathic Nociception Is Preserved in GPR55 Knockout Mice.. Sci. Rep. 2017;7:944.
- Yang R., Du J., Li L., Xu X., Liang S.. Central Role of Purinergic Receptors with Inflammation in Neuropathic Pain-Related Macrophage-SGC-Neuron Triad.. Neuropharmacology 2023;228:109445.
- Lu X., Richardson P.M.. Inflammation near the Nerve Cell Body Enhances Axonal Regeneration.. J. Neurosci. 1991;11:972–978.
- Liu F.-Y., Sun Y.-N., Wang F.-T., Li Q., Su L., Zhao Z.-F., Meng X.-L., Zhao H., Wu X., Sun Q.. Activation of Satellite Glial Cells in Lumbar Dorsal Root Ganglia Contributes to Neuropathic Pain after Spinal Nerve Ligation.. Brain Res. 2012;1427:65–77.
- Dubový P., Jančálek R., Klusáková I., Svíženská I., Pejchalová K.. Intra- and Extraneuronal Changes of Immunofluorescence Staining for TNF- and TNFR1 in the Dorsal Root Ganglia of Rat Peripheral Neuropathic Pain Models.. Cell Mol. Neurobiol. 2006;26:1203–1215.
- Takeda M., Tanimoto T., Kadoi J., Nasu M., Takahashi M., Kitagawa J., Matsumoto S.. Enhanced Excitability of Nociceptive Trigeminal Ganglion Neurons by Satellite Glial Cytokine Following Peripheral Inflammation.. Pain 2007;129:155–166.
- Dubový P., Klusáková I., Svíženská I., Brázda V.. Satellite Glial Cells Express IL-6 and Corresponding Signal-Transducing Receptors in the Dorsal Root Ganglia of Rat Neuropathic Pain Model.. Neuron Glia Biol. 2010;6:73–83.
- Hanani M.. Satellite Glial Cells in Sensory Ganglia: From Form to Function.. Brain Res. Rev. 2005;48:457–476.
- Ohara P.T., Vit J.-P., Bhargava A., Romero M., Sundberg C., Charles A.C., Jasmin L.. Gliopathic Pain: When Satellite Glial Cells Go Bad.. Neuroscientist 2009;15:450–463.
- Takeda K., Muramatsu M., Chikuma T., Kato T.. Effect of Memantine on the Levels of Neuropeptides and Microglial Cells in the Brain Regions of Rats with Neuropathic Pain.. J. Mol. Neurosci. 2009;39:380–390.
- Huang T.-Y., Belzer V., Hanani M.. Gap Junctions in Dorsal Root Ganglia: Possible Contribution to Visceral Pain.. Eur. J. Pain. 2010;14:49.e1–49.e11.
- Jasmin L., Vit J.-P., Bhargava A., Ohara P.T.. Can Satellite Glial Cells Be Therapeutic Targets for Pain Control?. Neuron Glia Biol. 2010;6:63–71.
- Costa F.A.L., Neto F.L.M.. Satellite Glial Cells in Sensory Ganglia: Its Role in Pain.. BJAN 2015;65:73–81.
- Ye Y., Salvo E., Romero-Reyes M., Akerman S., Shimizu E., Kobayashi Y., Michot B., Gibbs J.. Glia and Orofacial Pain: Progress and Future Directions.. Int. J. Mol. Sci. 2021;22:5345.
- Kupczyk P., Rykala M., Serek P., Pawlak A., Slowikowski B., Holysz M., Chodaczek G., Madej J.P., Ziolkowski P., Niedzwiedz A.. The Cannabinoid Receptors System in Horses: Tissue Distribution and Cellular Identification in Skin.. J. Vet. Intern. Med. 2022;36:1508–1524.
- Galiazzo G., Giancola F., Stanzani A., Fracassi F., Bernardini C., Forni M., Pietra M., Chiocchetti R.. Localization of Cannabinoid Receptors CB1, CB2, GPR55, and PPARα in the Canine Gastrointestinal Tract.. Histochem. Cell Biol. 2018;150:187–205.
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