Characterization of the anandamide induced depolarization of guinea-pig isolated vagus nerve
Open accessAbstract
1. There is considerable interest in elucidating potential endogenously derived agonists of the vanilloid receptor and the role of anandamide in this regard has received considerable attention. In the present study, we have used an electrophysiological technique to investigate the mechanism of activation of vanilloid receptors in an isolated vagal preparation. 2. Both capsaicin and anandamide depolarized de-sheathed whole vagal nerve preparations that was antagonized by the VR1 antagonist, capsazepine (P<0.05) whilst this response was unaltered by the cannabinoid (CB1) selective antagonist SR141716A or the CB2 selective antagonist, SR144528, thereby ruling out a role for cannabinoid receptors in this response. 3. The PKC activator, phorbol-12-myristate-13-acetate (PMA) augmented depolarization to both anandamide and capsaicin and this response was significantly inhibited with the PKC inhibitor, bisindolylmaleimide (BIM) (P<0.05). 4. The role of lipoxygenase products in the depolarization to anandamide was investigated in the presence of the lipoxygenase inhibitor, 5,8,11-Eicosatriynoic acid (ETI). Depolarization to anandamide and arachidonic acid was significantly inhibited in the presence of ET1 (P<0.05). However, in the absence of calcium depolarization to anandamide was not inhibited by ETI. 5. Using confocal microscopy we have demonstrated the presence of vanilloid receptors on both neuropeptide containing nerves and nerves that did not stain for sensory neuropeptides. 6. These results demonstrate that anandamide evokes depolarization of guinea-pig vagus nerve, following activation of vanilloid receptors, a component of which involves the generation of lipoxygenase products. Furthermore, these receptors are distributed in both neuropeptide and non-neuropeptide containing nerves.
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The current device design is fabricated with 16 channels, but it can easily be scaled up to ~1000 channels with the use of previously established process flows.
“The current device design is fabricated with 16 channels, but it can easily be scaled up to ~1000 channels with the use of previously established process flows [29].”
From A novel flexible cuff-like microelectrode for dual purpose, acute and chronic electrical interfacing with the mouse cervical vagus nerve (2017) · cites this paper as [29]
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Anandamide and vanilloid TRPV1 receptors
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“Metabolic products of anandamide have also been implicated in anandamide-induced depolarisation of the guinea-pig isolated vagus nerve that is TRPV1 receptor mediated (Kagaya et al., 2002).”
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“…irritants such as capsaicin and resiniferatoxin, and some endogenous mediators such as acid (Jordt et al., 2000) and anandamide (an endocannabinoid eicosanoid derivative; Zygmunt et al., 1999; Jia et al., 2002; Kagaya et al., 2002), bind directly and open TRPV1 ion channels (Caterina et al., 1997).”
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“…protein kinase C and other kinases (Figure 1) is of particular importance (Premkumar and Ahern, 2000; Tominaga et al., 2001; Vellani et al., 2001; Kagaya et al., 2002; Olah et al., 2002; Bhave et al., 2003; Varga et al., 2006; Vetter et al., 2006; Zhang and McNaughton, 2006; Nilius et al., 2007).”
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“Endogenous lipoxygenase metabolites of AEA have never been detected, but recent data suggest that they may mediate some of the actions ascribed to AEA (Kagaya et al., 2002).”
TRPV1 and the gut: from a tasty receptor for a painful vanilloid to a key player in hyperalgesia
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“…the probability of channel gating by protons, capsaicin, anandamide and/or heat (Premkumar and Ahern, 2000; Vellani et al., 2001; Crandall et al., 2002; Kagaya et al., 2002; Numazaki et al., 2002; Olah et al., 2002; Ahern, 2003; Bhave et al., 2003; Moriyama et al., 2003; Premkumar et al., 2004).”
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Chapter 15 Anandamide and the Vanilloid Receptor (TRPV1)
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“Indeed, it has been demonstrated that when anandamide (100 nM) is injected into the cell, it is very efficacious at inducing TRPV1-mediated plasma membrane currents in DRG neurons [75]; (xii) the rapid metabolism of anandamide inside cell may also limit its activation of TRPV1 [30,76] or potentiate its effect in case…”
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“…been shown to increase the cough reflex via activation of TRPV1 receptors (Jia et al., 2002), and is consistent with data suggesting that anandamide (at high concentrations) activates rat and guinea-pig pulmonary vagal C fibres via TRPV1 receptor activation (Kagaya et al., 2002; Lin & Lee, 2002).”
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“…(vanilloid 1) receptors, either by direct mechanisms (Zygmunt et al., 1999; see also Pacher et al., 2004, for a recent study investigating the haemodynamic effects of AEA in TRPV1 / mice) or as a result of lipoxygenase- derived metabolites (Kagaya et al., 2002) (review, see Ross, 2003).”
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“This receptor is predominantly found on afferent axons implicated in pain transduction [17,18] but it is clear that it is also found in afferents innervating the viscera [17] and in jugular ganglion neurones with projections to the lung [19–21].”
BackgroundModulation of sensory nerve function and the cough reflex: Understanding disease pathogenesis
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Direct Anandamide Activation of TRPV1 Produces Divergent Calcium and Current Responses
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“Peripherally, AEA is reported to sensitize and activate vagal afferents via a TRPV1 dependent mechanism (Kagaya et al., 2002; Lee et al., 2003; Lin et al., 2009).”
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TRPV1 Antagonists as Potential Antitussive Agents
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“Anandamide evokes vagal nerve depolarization [ 46 ] and induces contractile responses in guinea pig isolated bronchus [39] , effects that are mediated by stimulation of TRPV1.”
BackgroundFowler, C. J., Jonsson, K., Andersson, A., Juntunen, J., Järvinen, T., Vandevoorde, S., Lambert, D. M., Jerman, J. C., & Smart, D. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00392-7 · Cited by 46 · see citing works
“Indeed, in the guinea-pig bronchus and vagus nerve, pharmacological evidence was reported to suggest that lipoxygenase-derived metabolites of anandamide contribute to the Caps-sensitive actions of this compound [52,53].”
Elias, A. N., & Hofflich, H. (2008) · The American Journal of Medicine · doi:10.1016/j.amjmed.2007.08.036 · Cited by 40 · see citing works
Saitoh, C., Kitada, C., Uchida, W., Chancellor, M. B., de Groat, W. C., & Yoshimura, N. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.05.016 · Cited by 39 · see citing works
“On the other hand, in previous reports using bronchial rings or vagus nerves isolated from guinea-pigs, the contraction or depolarization responses induced by anandamide completely disappeared after capsaicin pre-treatment (Tucker et al., 2001,Kagaya et al., 2002).”
ResultWatanabe, N., Horie, S., Spina, D., Michael, G. J., Page, C. P., & Priestley, J. V. (2008) · International Archives of Allergy and Immunology · doi:10.1159/000126057 · Cited by 38 · see citing works
“as well as in jugular and nodose ganglia that project into the lung [”
BackgroundEffects of functionalized silver nanoparticles on aggregation of human blood platelets
Hajtuch, J., Hante, N. K., Tomczyk, E., Wójcik, M., Radomski, M. W., Santos-Martínez, M. J., & Inkielewicz‐Stępniak, I. (2019) · International Journal of Nanomedicine · doi:10.2147/ijn.s213499 · Cited by 37 · see citing works
Turning up the Heat on Pain: TRPV1 Receptors in Pain and Inflammation
Malmberg, A. B., & Bley, K. R. (2005) · Birkhäuser Basel eBooks · doi:10.1007/3-7643-7379-2 · Cited by 37 · see citing works
Németh, J., Helyes, Z., Thán, M., Jakab, B., Pintér, E., & Szolcsányi, J. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01221-1 · Cited by 37 · see citing works
TRPV1 Antagonists as Analgesic Agents
Trevisani, M., & Gatti, R. (2013) · The Open Pain Journal · doi:10.2174/1876386301306010108 · Cited by 34 · see citing works
“(1) is of pivotal importance [51, 58-65].”
Lees, G., & Dougalis, A. (2003) · Brain Research · doi:10.1016/j.brainres.2003.10.019 · Cited by 32 · see citing works
Hadley, S. H., Bahia, P. K., & Taylor‐Clark, T. E. (2014) · Molecular Pharmacology · doi:10.1124/mol.113.091272 · Cited by 27 · see citing works
“In particular, PKC has been shown to induce hyperexcitability via tetrodotoxin-resistant voltage-gated Na1 channels in both vagal (Kagaya et al., 2002; Ikeda et al., 2005; Matsumoto et al., 2007) and DRG neurons (Baker, 2005; Hayase et al., 2007; Wu et al., 2012), indicating possible candidates for…”
BackgroundPeripheral Mechanisms II: The Pharmacology of Peripherally Active Antitussive Drugs
Spina, D., McFadzean, I., Bertram, F., & Page, C. P. (2009) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-79842-2_8 · Cited by 25 · see citing works
“…those of guinea pigs (Spina et al. 1998), although TRPV1-positive nerves have been described in the lung which do not contain sensory neuropeptides (Kagaya et al. 2002; Watanabe et al. 2005, 2006), suggesting that capsaicin-mediated effects may be able to occur independently of the release of…”
BackgroundFernández-Carvajal, A. M., Fernandez-Ballester, G. J., Devesa, I., González-Ros, J. M., & Ferrer-Montiel, A. V. (2011) · Pharmaceuticals · doi:10.3390/ph5010016 · Cited by 25 · see citing works
“Sensitization of the ion channel depends on several mechanisms among which phosphorylation by protein kinase A (PKA), protein kinase C (PKC) and other kinases is of particular importance [27-33].”
BackgroundDudášová, A., Keir, S. D., Parsons, M. E., Molleman, A., & Page, C. P. (2013) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2013.02.002 · Cited by 24 · see citing works
Cannabinoid Receptor Agonists Inhibit Sensory Nerve Activation in Guinea Pig Airways
Yoshihara, S., Morimoto, H., Yamada, Y., Abe, T., & Arisaka, O. (2004) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200306-775oc · Cited by 22 · see citing works
Effect of Anandamide on Cytosolic Ca2+ Levels and Proliferation in Canine Renal Tubular Cells
Yeh, J., Cheng, H., Huang, C., Chung, H., Chiu, H., Yang, Y., Yeh, M., Chen, W., Kao, C., Chou, C., et al. (2006) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2006.pto_350.x · Cited by 21 · see citing works
Anandamide in primary sensory neurons: too much of a good thing?
Valente, J. D. S., Varga, A., Ananthan, K., Khajuria, A., & Nagy, I. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12467 · Cited by 20 · see citing works
“…FAAH inhibition, some anandamide degradation may go through alternative pathways (i.e. through cyclooxygenase 2 and lipoxygenase), and some products of those pathways are algogens (Craib et al., 2001; Kagaya et al., 2002; Matias et al., 2004; Gatta et al., 2012; Piscitelli & Di Marzo, 2012).”
BackgroundCui, Y., D’Agostino, B., Risse, P., Marrocco, G., Naline, E., Zhang, Y., Chen, H., Finance, O., Rinaldi, M. L., Rossi, F., et al. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.06.040 · Cited by 19 · see citing works
Malcher‐Lopes, R., & Buzzi, M. (2009) · Vitamins and hormones · doi:10.1016/s0083-6729(09)81011-x · Cited by 18 · see citing works
The use of the rat isolated vagus nerve for functional measurements of the effect of drugs in vitro
Docherty, R. J., Charlesworth, G., Farrag, K., Bhattacharjee, A., & Costa, S. K. P. (2005) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2004.08.011 · Cited by 16 · see citing works
Oxidative stress as activators of sensory nerves for cough
Taylor‐Clark, T. E. (2015) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2015.06.003 · Cited by 16 · see citing works
Sabetian, P., & Yoo, P. B. (2019) · Journal of Neural Engineering · doi:10.1088/1741-2552/ab5551 · Cited by 11 · see citing works
Non-CB1, Non-CB2 Receptors for Endocannabinoids
PETROCELLIS, L. D., & Marzo, V. D. (2005) · CRC Press eBooks · doi:10.1201/9781420023640.ch6 · Cited by 9 · see citing works
Fırat, P. G., Demirel, E. E., Demirel, S., Dikçi, S., Türköz, Y., & Özyalın, F. (2019) · Current Eye Research · doi:10.1080/02713683.2019.1578378 · Cited by 7 · see citing works
Targeting TRPV1: Challenges and Issues in Pain Management
Trevisani, M., & SZALLASI, A. (2010) · The Open Drug Discovery Journal · doi:10.2174/1877381801002010037 · Cited by 4 · see citing works
“Indeed, several inflammatory mediators (e.g. prostaglandins) enhance activation of TRPV1 by capsaicin and/or heat via a PKA-dependent pathway.”
BackgroundPharmacology of Peripherally Acting Antitussives
Reynolds, S. M., Spina, D., & Page, C. P. (2003) · doi:10.1002/9780470755846.ch23 · Cited by 4 · see citing works
Transient receptor potential (TRP) channel and cough
塩谷隆信, 一洋, 佐., 正明, 佐., & 博之, 渡. (2008) · Folia Pharmacologica Japonica · doi:10.1254/fpj.131.417 · Cited by 2 · see citing works
Vanilloid (TRPV1) and Other Transient Receptor Potential Channels
Trevisani, M., & SZALLASI, A. (2009) · doi:10.1002/9780470522226.ch8 · Cited by 2 · see citing works
A comparison of the pharmacological modulation of hyperalgesia and bronchial hyperresponsiveness
Spina, D. (2003) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/s1094-5539(02)00173-6 · Cited by 2 · see citing works
Endocannabinoids and vanilloid TRPV1 receptors
Ross, R. A. (2005) · Birkhäuser Basel eBooks · doi:10.1007/3-7643-7379-2_5 · Cited by 1 · see citing works
Belvisi, M. G., & Barnes, P. J. (2005) · Birkhäuser Basel eBooks · doi:10.1007/3-7643-7379-2_9 · Cited by 1 · see citing works
“These data together with the finding that anandamide activates rat pulmonary vagal C-fibres through the activation of TRPV1 [42] and depolarizes the guinea pig vagus nerve axon [ 74 ] provides a mechanistic explanation for the tussive effect observed with anandamide.”
ResultModulation of Sensory Nerve Function and the Cough Reflex
Nasra, J. (2008) · Spiral (Imperial College London) · doi:10.25560/4252 · Cited by 1 · see citing works
Molecular Biology of TRPV1 and Related Receptors
Hwang, S. W. (2005) · CRC Press eBooks · doi:10.1201/b14188-5
Pharmacology of the Oxidative Metabolites of Endocannabinoids
Ross, R. A. (2005) · CRC Press eBooks · doi:10.1201/9781420023640.ch12
Directionally Sensitive Low-noise Neural Recording Using Tetrapolar Nerve Cuff Electrode
Sabetian, P. (2020) · TSpace (University of Toronto)
Molecular Biology of TRPV1 and Related Receptors
Hwang, S. W. (2005) · Lung biology in health and disease · doi:10.1201/b14188-2
Stadler, A. (2010) · mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich)
- Authors
- Kagaya, M., Lamb, J., Robbins, J., Page, C. P., & Spina, D.
- Affiliations
- King's College London (GB)
- The University of Western Australia (AU)
- Corresponding author
- Spina, Domenico
- Venue
- British Journal of Pharmacology
- Publisher
- Wiley
- Published
- 2002-09
- Volume
- 137
- Issue
- 1
- Pages
- 39-48
- ISSN
- 0007-1188 (ISSN-L)
- 1476-5381
- PMC
- PMC1573467
- OpenAlex
- W2075825616
- Cited by
- 61
- References
- 60
- Citations by year
- 2022: 1 · 2020: 1 · 2019: 4 · 2017: 2 · 2015: 4 · 2014: 2 · 2013: 4
- FWCI
- 3.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- British Journal of Pharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Keywords
- anandamide, vanilloid receptor, TRPV1, vagus nerve, capsaicin, capsazepine, protein kinase C, lipoxygenase products, eicosatrienoic acid, arachidonic acid, neuropeptides, endocannabinoids, endovanilloids
- MeSH terms
- Action Potentials, Animals, Arachidonic Acids, Calcium, Capsaicin, Electrophysiology, Guinea Pigs, Protein Kinase C, Receptors, Drug, Vagus Nerve, Lipoxygenase Inhibitors, Microscopy, Confocal, Enzyme Activators, Receptors, Cannabinoid, Polyunsaturated Alkamides, Endocannabinoids, In Vitro Techniques
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