The multiplicity of spinal AA-5-HT anti-nociceptive action in a rat model of neuropathic pain

Pharmacological Research

Volumn 111, Issue , 2016, Pages 251-263

  Malek, Natalia ^a   Kostrzewa, Magdalena ^a   Makuch, Wioletta ^a   Pajak, Agnieszka ^a   Kucharczyk, Mateusz ^a,c   Piscitelli, Fabiana ^b   Przewlocka, Barbara ^a   Di Marzo, Vincenzo ^b   Starowicz, Katarzyna ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

^b CNR   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cannabinoid receptors; Endocannabinoids; FAAH; N acylethanolamines; Neuropathic pain; TRPV1

Indexed keywords

ANTINOCICEPTIVE AGENT; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; FATTY ACID AMIDASE; MESSENGER RNA; N ARACHIDONOYL SEROTONIN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; ACYLGLYCEROL; AMIDASE; AMIDE; ANALGESIC AGENT; ANANDAMIDE; ARACHIDONIC ACID DERIVATIVE; ARACHIDONOYLSEROTONIN; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CNR1 PROTEIN, RAT; CNR2 PROTEIN, RAT; ENDOCANNABINOID; FATTY-ACID AMIDE HYDROLASE; G PROTEIN COUPLED RECEPTOR; GLYCERYL 2-ARACHIDONATE; GPR18 PROTEIN, RAT; GPR55 PROTEIN, RAT; SEROTONIN; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CB2 GENE; CONTROLLED STUDY; DRUG EFFICACY; FAAH GENE; GENE; GENE EXPRESSION; GPR18 GENE; GPR55 GENE; IC50; LUMBAR SPINAL CORD; MALE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPARATIVE STUDY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GENETICS; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; NEURALGIA; NOCICEPTION; PAIN THRESHOLD; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL GANGLION; TIME FACTOR; WISTAR RAT;

AMIDOHYDROLASES; ANALGESICS; ANIMALS; ARACHIDONIC ACIDS; CANNABINOID RECEPTOR ANTAGONISTS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCANNABINOIDS; GANGLIA, SPINAL; GLYCERIDES; INJECTIONS, SPINAL; MALE; NEURALGIA; NOCICEPTION; PAIN THRESHOLD; POLYUNSATURATED ALKAMIDES; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RECEPTORS, CANNABINOID; RECEPTORS, G-PROTEIN-COUPLED; SEROTONIN; SIGNAL TRANSDUCTION; SPINAL CORD; TIME FACTORS; TRPV CATION CHANNELS;

EID: 84976363275     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2016.06.012     Document Type: Article

References (90)

1. [1] Ahn, K., Smith, S.E., Liimatta, M.B., Beidler, D., Sadagopan, N., Dudley, D.T., Young, T., Wren, P., Zhang, Y., Swaney, S., Van Becelaere, K., Blankman, J.L., Nomura, D.K., Bhattachar, S.N., Stiff, C., Nomanbhoy, T.K., Weerapana, E., Johnson, D.S., Cravatt, B.F., Mechanistic and pharmacological characterization of PF-04457845: a highly potent and selective fatty acid amide hydrolase inhibitor that reduces inflammatory and noninflammatory pain. J. Pharmacol. Exp. Ther. 338 (2011), 114–124.
2. [2] Anand, P., Whiteside, G., Fowler, C.J., Hohmann, A.G., Targeting CB2 receptors and the endocannabinoid system for the treatment of pain. Brain Res. Rev. 60 (2009), 255–266.
3. [3] Baamonde, A., Lastra, A., Juarez, L., Hidalgo, A., Menéndez, L., TRPV1 desensitisation and endogenous vanilloid involvement in the enhanced analgesia induced by capsaicin in inflamed tissues. Brain Res. Bull. 67 (2005), 476–481.
4. [4] Balenga, N.A., Martínez-Pinilla, E., Kargl, J., Schröder, R., Peinhaupt, M., Platzer, W., Bálint, Z., Zamarbide, M., Dopeso-Reyes, I.G., Ricobaraza, A., Pérez-Ortiz, J.M., Kostenis, E., Waldhoer, M., Heinemann, A., Franco, R., Heteromerization of GPR55 and cannabinoid CB2 receptors modulates signalling. Br. J. Pharmacol. 171 (2014), 5387–5406.
5. [5] Balenga, N.A.B., Aflaki, E., Kargl, J., Platzer, W., Schröder, R., Blättermann, S., Kostenis, E., Brown, A.J., Heinemann, A., Waldhoer, M., GPR55 regulates cannabinoid 2 receptor-mediated responses in human neutrophils. Cell Res. 21 (2011), 1452–1469.
6. [6] Bennett, G.J., Xie, Y.K., A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988), 87–107.
7. [7] Bisogno, T., Maurelli, S., Melck, D., De Petrocellis, L., Di Marzo, V., Biosynthesis, uptake, and degradation of anandamide and palmitoylethanolamide in leukocytes. J. Biol. Chem. 272 (1997), 3315–3323.
8. [8] Bradshaw, H.B., Lee, S.H., McHugh, D., Orphan endogenous lipids and orphan GPCRs: a good match. Prostaglandins Other Lipid Mediat. 89 (2009), 131–134.
9. [9] Brederson, J.-D., Kym, P.R., Szallasi, A., Targeting TRP channels for pain relief. Eur. J. Pharmacol. 716 (2013), 61–76.
10. [10] Bryce, T.N., Budh, C.N., Cardenas, D.D., Dijkers, M., Felix, E.R., Finnerup, N.B., Kennedy, P., Lundeberg, T., Richards, J.S., Rintala, D.H., Siddall, P., Widerstrom-Noga, E., Pain after spinal cord injury: an evidence-based review for clinical practice and research: report of the National Institute on Disability and Rehabilitation Research Spinal Cord Injury Measures meeting. J. Spinal Cord Med. 30 (2007), 421–440.
11. [11] Calignano, A., La Rana, G., Piomelli, D., Antinociceptive activity of the endogenous fatty acid amide, palmitylethanolamide. Eur. J. Pharmacol. 419 (2001), 191–198.
12. [12] Campbell, J.N., Raja, S.N., Meyer, R.A., Mackinnon, S.E., Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32 (1988), 89–94.
13. [13] Caterina, M.J., Leffler, A., Malmberg, A.B., Martin, W.J., Trafton, J., Petersen-Zeitz, K.R., Koltzenburg, M., Basbaum, A.I., Julius, D., Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000), 306–313.
14. [14] Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D., Julius, D., The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997), 816–824.
15. [15] Chang, L., Luo, L., Palmer, J.A., Sutton, S., Wilson, S.J., Barbier, A.J., Breitenbucher, J.G., Chaplan, S.R., Webb, M., Inhibition of fatty acid amide hydrolase produces analgesia by multiple mechanisms. Br. J. Pharmacol. 148 (2006), 102–113.
16. [16] Christie, M.J., Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction. Br. J. Pharmacol. 154 (2008), 384–396.
17. [17] Concannon, R.M., Okine, B.N., Finn, D.P., Dowd, E., Differential upregulation of the cannabinoid CB₂ receptor in neurotoxic and inflammation-driven rat models of Parkinson's disease. Exp. Neurol. 269 (2015), 133–141.
18. [18] Costa, B., Bettoni, I., Petrosino, S., Comelli, F., Giagnoni, G., Di Marzo, V., The dual fatty acid amide hydrolase/TRPV1 blocker, N-arachidonoyl-serotonin, relieves carrageenan-induced inflammation and hyperalgesia in mice. Pharmacol. Res. 61 (2010), 537–546.
19. [19] Costa, B., Comelli, F., Bettoni, I., Colleoni, M., Giagnoni, G., The endogenous fatty acid amide, palmitoylethanolamide, has anti-allodynic and anti-hyperalgesic effects in a murine model of neuropathic pain: involvement of CB(1), TRPV1 and PPARgamma receptors and neurotrophic factors. Pain 139 (2008), 541–550.
20. [20] D'Argenio, G., Valenti, M., Scaglione, G., Cosenza, V., Sorrentini, I., Di Marzo, V., Up-regulation of anandamide levels as an endogenous mechanism and a pharmacological strategy to limit colon inflammation. FASEB J. 20 (2006), 568–570.
21. [21] Davis, J.B., Gray, J., Gunthorpe, M.J., Hatcher, J.P., Davey, P.T., Overend, P., Harries, M.H., Latcham, J., Clapham, C., Atkinson, K., Hughes, S.A., Rance, K., Grau, E., Harper, A.J., Pugh, P.L., Rogers, D.C., Bingham, S., Randall, A., Sheardown, S.A., Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (2000), 183–187.
22. [22] De Novellis, V., Palazzo, E., Rossi, F., De Petrocellis, L., Petrosino, S., Guida, F., Luongo, L., Migliozzi, A., Cristino, L., Marabese, I., Starowicz, K., Di Marzo, V., Maione, S., Endocannabinoid Research Group, The analgesic effect of N-arachidonoyl-serotonin, a FAAH inhibitor and TRPV1 receptor antagonist, associated with changes in rostral ventromedial medulla and locus coeruleus cell activity in rats. Neuropharmacology 55 (2008), 1105–1113.
23. [23] Di Marzo, V., Manipulation of the endocannabinoid system by a general anaesthetic. Br. J. Pharmacol. 139 (2003), 885–886.
24. [25] Gavva, N.R., Bannon, A.W., Surapaneni, S., Hovland, D.N., Lehto, S.G., Gore, A., Juan, T., Deng, H., Han, B., Klionsky, L., Kuang, R., Le, A., Tamir, R., Wang, J., Youngblood, B., Zhu, D., Norman, M.H., Magal, E., Treanor, J.J.S., Louis, J.-C., The vanilloid receptor TRPV1 is tonically activated in vivo and involved in body temperature regulation. J. Neurosci. 27 (2007), 3366–3374.
25. [26] Gavva, N.R., Treanor, J.J.S., Garami, A., Fang, L., Surapaneni, S., Akrami, A., Alvarez, F., Bak, A., Darling, M., Gore, A., Jang, G.R., Kesslak, J.P., Ni, L., Norman, M.H., Palluconi, G., Rose, M.J., Salfi, M., Tan, E., Romanovsky, A.A., Banfield, C., Davar, G., Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 136 (2008), 202–210.
26. [27] Giordano, C., Cristino, L., Luongo, L., Siniscalco, D., Petrosino, S., Piscitelli, F., Marabese, I., Gatta, L., Rossi, F., Imperatore, R., Palazzo, E., De Novellis, V., Di Marzo, V., Maione, S., TRPV1-dependent and -independent alterations in the limbic cortex of neuropathic mice: impact on glial caspases and pain perception. Cereb. Cortex 22 (2012), 2495–2518.
27. [28] Godlewski, G., Offertáler, L., Wagner, J.A., Kunos, G., Receptors for acylethanolamides-GPR55 and GPR119. Prostaglandins Other Lipid Mediat. 89 (2009), 105–111.
28. [29] Gustafsson, S.B., Wallenius, A., Zackrisson, H., Popova, D., Plym Forshell, L., Jacobsson, S.O.P., Effects of cannabinoids and related fatty acids upon the viability of P19 embryonal carcinoma cells. Arch. Toxicol. 87 (2013), 1939–1951.
29. [30] [30].Ho, W.-S.V., Barrett, D.A., Randall, M.D., Entourage effects of N-palmitoylethanolamide and N-oleoylethanolamide on vasorelaxation to anandamide occur through TRPV1 receptors. Br. J. Pharmacol. 155 (2008), 837–846.
30. [31] Holzer, P., TRPV1 and the gut: from a tasty receptor for a painful vanilloid to a key player in hyperalgesia. Eur. J. Pharmacol. 500 (2004), 231–241.
31. [32] Horowitz, S.H., The diagnostic workup of patients with neuropathic pain. Anesthesiol. Clin. 25 (2007), 699–708 (v).
32. [33] Horvath, G., Kekesi, G., Nagy, E., Benedek, G., The role of TRPV1 receptors in the antinociceptive effect of anandamide at spinal level. Pain 134 (2008), 277–284.
33. [34] Huang, S.M., Bisogno, T., Petros, T.J., Chang, S.Y., Zavitsanos, P.A., Zipkin, R.E., Sivakumar, R., Coop, A., Maeda, D.Y., De Petrocellis, L., Burstein, S., Di Marzo, V., Walker, J.M., Identification of a new class of molecules, the arachidonyl amino acids, and characterization of one member that inhibits pain. J. Biol. Chem. 276 (2001), 42639–42644.
34. [35] Huggins, J.P., Smart, T.S., Langman, S., Taylor, L., Young, T., An efficient randomised, placebo-controlled clinical trial with the irreversible fatty acid amide hydrolase-1 inhibitor PF-04457845, which modulates endocannabinoids but fails to induce effective analgesia in patients with pain due to osteoarthritis of the knee. Pain 153 (2012), 1837–1846.
35. [36] Ibrahim, M.M., Rude, M.L., Stagg, N.J., Mata, H.P., Lai, J., Vanderah, T.W., Porreca, F., Buckley, N.E., Makriyannis, A., Malan, T.P., CB2 cannabinoid receptor mediation of antinociception. Pain 122 (2006), 36–42.
36. [37] Jayamanne, A., Greenwood, R., Mitchell, V.A., Aslan, S., Piomelli, D., Vaughan, C.W., Actions of the FAAH inhibitor URB597 in neuropathic and inflammatory chronic pain models. Br. J. Pharmacol. 147 (2006), 281–288.
37. [38] Jeong, H.-J., Vandenberg, R.J., Vaughan, C.W., N-arachidonyl-glycine modulates synaptic transmission in superficial dorsal horn. Br. J. Pharmacol. 161 (2010), 925–935.
38. [39] Jonsson, K.O., Vandevoorde, S., Lambert, D.M., Tiger, G., Fowler, C.J., Effects of homologues and analogues of palmitoylethanolamide upon the inactivation of the endocannabinoid anandamide. Br. J. Pharmacol. 133 (2001), 1263–1275.
39. [40] Kallendrusch, S., Kremzow, S., Nowicki, M., Grabiec, U., Winkelmann, R., Benz, A., Kraft, R., Bechmann, I., Dehghani, F., Koch, M., The G protein-coupled receptor 55 ligand l-α-lysophosphatidylinositol exerts microglia-dependent neuroprotection after excitotoxic lesion. Glia 61 (2013), 1822–1831.
40. [41] Kamei, J., Zushida, K., Morita, K., Sasaki, M., Tanaka, S., Role of vanilloid VR1 receptor in thermal allodynia and hyperalgesia in diabetic mice. Eur. J. Pharmacol. 422 (2001), 83–86.
41. [42] Kim, Y.S., Chu, Y., Han, L., Li, M., Li, Z., Lavinka, P.C., Sun, S., Tang, Z., Park, K., Caterina, M.J., Ren, K., Dubner, R., Wei, F., Dong, X., Central terminal sensitization of TRPV1 by descending serotonergic facilitation modulates chronic pain. Neuron 81 (2014), 873–887.
42. [43] Kinsey, S.G., Long, J.Z., O'Neal, S.T., Abdullah, R.A., Poklis, J.L., Boger, D.L., Cravatt, B.F., Lichtman, A.H., Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain. J. Pharmacol. Exp. Ther. 330 (2009), 902–910.
43. [44] Kohno, M., Hasegawa, H., Inoue, A., Muraoka, M., Miyazaki, T., Oka, K., Yasukawa, M., Identification of N-arachidonylglycine as the endogenous ligand for orphan G-protein-coupled receptor GPR18. Biochem. Biophys. Res. Commun. 347 (2006), 827–832.
44. [45] Krum, H., Liew, D., Aw, J., Haas, S., Cardiovascular effects of selective cyclooxygenase-2 inhibitors. Exp. Rev. Cardiovasc. Ther. 2 (2004), 265–270.
45. [46] Labuz, D., Spahn, V., Celik, M.Ö., Machelska, H., Opioids and TRPV1 in the peripheral control of neuropathic pain—defining a target site in the injured nerve. Neuropharmacology 101 (2015), 330–340.
46. [47] Lo Verme, J., Fu, J., Astarita, G., La Rana, G., Russo, R., Calignano, A., Piomelli, D., The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide. Mol. Pharmacol. 67 (2005), 15–19.
47. [48] Luongo, L., Palazzo, E., Tambaro, S., Giordano, C., Gatta, L., Scafuro, M.A., Rossi, F.S., Lazzari, P., Pani, L., De Novellis, V., Malcangio, M., Maione, S., 1-(2′,4′-dichlorophenyl)-6-methyl-N-cyclohexylamine-1,4-dihydroindeno[1,2-c]pyrazole-3-carboxamide, a novel CB2 agonist, alleviates neuropathic pain through functional microglial changes in mice. Neurobiol. Dis. 37 (2010), 177–185.
48. [49] Maione, S., Bisogno, T., De Novellis, V., Palazzo, E., Cristino, L., Valenti, M., Petrosino, S., Guglielmotti, V., Rossi, F., Di Marzo, V., Elevation of endocannabinoid levels in the ventrolateral periaqueductal grey through inhibition of fatty acid amide hydrolase affects descending nociceptive pathways via both cannabinoid receptor type 1 and transient receptor potential vanilloid type-1 receptors. J. Pharmacol. Exp. Ther. 316 (2006), 969–982.
49. [50] Maione, S., De Petrocellis, L., De Novellis, V., Moriello, A.S., Petrosino, S., Palazzo, E., Rossi, F.S., Woodward, D.F., Di Marzo, V., Analgesic actions of N-arachidonoyl-serotonin, a fatty acid amide hydrolase inhibitor with antagonistic activity at vanilloid TRPV1 receptors. Br. J. Pharmacol. 150 (2007), 766–781.
50. [51] Malek, N., Kucharczyk, M., Starowicz, K., Alterations in the anandamide metabolism in the development of neuropathic pain. Biomed. Res. Int., 2014, 2014, 686908.
51. [52] Malek, N., Mrugala, M., Makuch, W., Kolosowska, N., Przewlocka, B., Binkowski, M., Czaja, M., Morera, E., Di Marzo, V., Starowicz, K., A multi-target approach for pain treatment: dual inhibition of fatty acid amide hydrolase and TRPV1 in a rat model of osteoarthritis. Pain 156 (2015), 890–903.
52. [53] Malek, N., Popiolek-Barczyk, K., Mika, J., Przewlocka, B., Starowicz, K., Anandamide, Acting via CB2 Receptors, Alleviates LPS-Induced Neuroinflammation in Rat Primary Microglial Cultures. Neural Plast., 2015, 2015, 130639.
53. [54] McHugh, D., Hu, S.S.J., Rimmerman, N., Juknat, A., Vogel, Z., Walker, J.M., Bradshaw, H.B., N-arachidonoyl glycine, an abundant endogenous lipid, potently drives directed cellular migration through GPR18, the putative abnormal cannabidiol receptor. BMC Neurosci., 11, 2010, 44.
54. [55] Micale, V., Cristino, L., Tamburella, A., Petrosino, S., Leggio, G.M., Drago, F., Di Marzo, V., Anxiolytic effects in mice of a dual blocker of fatty acid amide hydrolase and transient receptor potential vanilloid type-1 channels. Neuropsychopharmacology 34 (2009), 593–606.
55. [56] Morera, E., De Petrocellis, L., Morera, L., Moriello, A.S., Ligresti, A., Nalli, M., Woodward, D.F., Di Marzo, V., Ortar, G., Synthesis and biological evaluation of piperazinyl carbamates and ureas as fatty acid amide hydrolase (FAAH) and transient receptor potential (TRP) channel dual ligands. Bioorg. Med. Chem. Lett. 19 (2009), 6806–6809.
56. [57] Nuytten, D., Kupers, R., Lammens, M., Dom, R., Van Hees, J., Gybels, J., Further evidence for myelinated as well as unmyelinated fibre damage in a rat model of neuropathic pain. Exp. Brain Res. 91 (1992), 73–78.
57. [58] Ortar, G., Cascio, M.G., De Petrocellis, L., Morera, E., Rossi, F., Schiano-Moriello, A., Nalli, M., De Novellis, V., Woodward, D.F., Maione, S., Di Marzo, V., New N-arachidonoylserotonin analogues with potential dual mechanism of action against pain. J. Med. Chem. 50 (2007), 6554–6569.
58. [59] Osikowicz, M., Mika, J., Makuch, W., Przewlocka, B., Glutamate receptor ligands attenuate allodynia and hyperalgesia and potentiate morphine effects in a mouse model of neuropathic pain. Pain 139 (2008), 117–126.
59. [60] Pacher, P., Mechoulam, R., Is lipid signaling through cannabinoid 2 receptors part of a protective system? Prog. Lipid Res. 50 (2011), 193–211.
60. [61] Paszcuk, A.F., Dutra, R.C., Da Silva, K.A.B.S., Quintão, N.L.M., Campos, M.M., Calixto, J.B., Cannabinoid agonists inhibit neuropathic pain induced by brachial plexus avulsion in mice by affecting glial cells and MAP kinases. PLoS One, 6, 2011, e24034.
61. [62] Pertwee, R.G., Pharmacology of cannabinoid receptor ligands. Curr. Med. Chem. 6 (1999), 635–664.
62. [63] Piper, A.S., Yeats, J.C., Bevan, S., Docherty, R.J., A study of the voltage dependence of capsaicin-activated membrane currents in rat sensory neurones before and after acute desensitization. J. Physiol. (Lond.) 518:Pt 3 (1999), 721–733.
63. [64] Piscitelli, F., Di Marzo, V., Redundancy of endocannabinoid inactivation: new challenges and opportunities for pain control. ACS Chem. Neurosci. 3 (2012), 356–363.
64. [65] Racz, I., Nadal, X., Alferink, J., Baños, J.E., Rehnelt, J., Martín, M., Pintado, B., Gutierrez-Adan, A., Sanguino, E., Manzanares, J., Zimmer, A., Maldonado, R., Crucial role of CB(2) cannabinoid receptor in the regulation of central immune responses during neuropathic pain. J. Neurosci. 28 (2008), 12125–12135.
65. [66] Re, G., Barbero, R., Miolo, A., Di Marzo, V., Palmitoylethanolamide, endocannabinoids and related cannabimimetic compounds in protection against tissue inflammation and pain: potential use in companion animals. Vet. J. 173 (2007), 21–30.
66. [67] Romero-Sandoval, A., Nutile-McMenemy, N., DeLeo, J.A., Spinal microglial and perivascular cell cannabinoid receptor type 2 activation reduces behavioral hypersensitivity without tolerance after peripheral nerve injury. Anesthesiology 108 (2008), 722–734.
67. [68] Sapunar, D., Kostic, S., Banozic, A., Puljak, L., Dorsal root ganglion— a potential new therapeutic target for neuropathic pain. J. Pain Res. 5 (2012), 31–38.
68. [69] Schmöle, A.-C., Lundt, R., Ternes, S., Albayram, Ö., Ulas, T., Schultze, J.L., Bano, D., Nicotera, P., Alferink, J., Zimmer, A., Cannabinoid receptor 2 deficiency results in reduced neuroinflammation in an Alzheimer's disease mouse model. Neurobiol. Aging 36 (2015), 710–719.
69. [70] Seabrook, G.R., Sutton, K.G., Jarolimek, W., Hollingworth, G.J., Teague, S., Webb, J., Clark, N., Boyce, S., Kerby, J., Ali, Z., Chou, M., Middleton, R., Kaczorowski, G., Jones, A.B., Functional properties of the high-affinity TRPV1 (VR1) vanilloid receptor antagonist (4-hydroxy-5-iodo-3-methoxyphenylacetate ester) iodo-resiniferatoxin. J. Pharmacol. Exp. Ther. 303 (2002), 1052–1060.
70. [71] Shaqura, M., Khalefa, B.I., Shakibaei, M., Zöllner, C., Al-Khrasani, M., Fürst, S., Schäfer, M., Mousa, S.A., New insights into mechanisms of opioid inhibitory effects on capsaicin-induced TRPV1 activity during painful diabetic neuropathy. Neuropharmacology 85 (2014), 142–150.
71. [72] Siemens, J., Zhou, S., Piskorowski, R., Nikai, T., Lumpkin, E.A., Basbaum, A.I., King, D., Julius, D., Spider toxins activate the capsaicin receptor to produce inflammatory pain. Nature 444 (2006), 208–212.
72. [73] Skaper, S.D., Facci, L., Giusti, P., Glia and mast cells as targets for palmitoylethanolamide: an anti-inflammatory and neuroprotective lipid mediator. Mol. Neurobiol. 48 (2013), 340–352.
73. [74] Starowicz, K., Maione, S., Cristino, L., Palazzo, E., Marabese, I., Rossi, F., De Novellis, V., Di Marzo, V., Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. J. Neurosci. 27 (2007), 13739–13749.
74. [75] Starowicz, K., Makuch, W., Korostynski, M., Malek, N., Slezak, M., Zychowska, M., Petrosino, S., De Petrocellis, L., Cristino, L., Przewlocka, B., Di Marzo, V., Full inhibition of spinal FAAH leads to TRPV1-mediated analgesic effects in neuropathic rats and possible lipoxygenase-mediated remodeling of anandamide metabolism. PLoS One, 8, 2013, e60040.
75. [76] Starowicz, K., Przewlocka, B., Modulation of neuropathic-pain-related behaviour by the spinal endocannabinoid/endovanilloid system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 (2012), 3286–3299.
76. [77] Staton, P.C., Hatcher, J.P., Walker, D.J., Morrison, A.D., Shapland, E.M., Hughes, J.P., Chong, E., Mander, P.K., Green, P.J., Billinton, A., Fulleylove, M., Lancaster, H.C., Smith, J.C., Bailey, L.T., Wise, A., Brown, A.J., Richardson, J.C., Chessell, I.P., The putative cannabinoid receptor GPR55 plays a role in mechanical hyperalgesia associated with inflammatory and neuropathic pain. Pain 139 (2008), 225–236.
77. [78] Stella, N., Endocannabinoid signaling in microglial cells. Neuropharmacology 56:Suppl. 1 (2009), 244–253.
78. [79] 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 21 (1998), 531–543.
79. [80] Ueda, M., Iwasaki, H., Wang, S., Murata, E., Poon, K.Y.T., Mao, J., Martyn, J.A.J., Cannabinoid receptor type 1 antagonist, AM251, attenuates mechanical allodynia and thermal hyperalgesia after burn injury. Anesthesiology 121 (2014), 1311–1319.
80. [81] Vincenzi, F., Targa, M., Corciulo, C., Tabrizi, M.A., Merighi, S., Gessi, S., Saponaro, G., Baraldi, P.G., Borea, P.A., Varani, K., Antinociceptive effects of the selective CB2 agonist MT178 in inflammatory and chronic rodent pain models. Pain 154 (2013), 864–873.
81. [82] Walker, K.M., Urban, L., Medhurst, S.J., Patel, S., Panesar, M., Fox, A.J., McIntyre, P., The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain. J. Pharmacol. Exp. Ther. 304 (2003), 56–62.
82. [83] Wang, D., Couture, R., Hong, Y., Activated microglia in the spinal cord underlies diabetic neuropathic pain. Eur. J. Pharmacol. 728 (2014), 59–66.
83. [84] Wolkers, C.P.B., Barbosa Junior, A., Menescal-de-Oliveira, L., Hoffmann, A., Acute administration of a cannabinoid CB1 receptor antagonist impairs stress-induced antinociception in fish. Physiol. Behav. 142 (2015), 37–41.
84. [85] Yaksh, T.L., Rudy, T.A., Chronic catheterization of the spinal subarachnoid space. Physiol. Behav. 17 (1976), 1031–1036.
85. [86] Yang, H., Zhou, J., Lehmann, C., GPR55—a putative type 3 cannabinoid receptor in inflammation. J. Basic Clin. Physiol. Pharmacol., 2015.
86. [87] Zhang, G., Chen, W., Lao, L., Marvizón, J.C.G., Cannabinoid CB1 receptor facilitation of substance P release in the rat spinal cord, measured as neurokinin 1 receptor internalization. Eur. J. Neurosci. 31 (2010), 225–237.
87. [88] Zhang, J., Hoffert, C., Vu, H.K., Groblewski, T., Ahmad, S., O'Donnell, D., Induction of CB2 receptor expression in the rat spinal cord of neuropathic but not inflammatory chronic pain models. Eur. J. Neurosci. 17 (2003), 2750–2754.
88. [89] Zhuo, M., Wu, G., Wu, L.-J., Neuronal and microglial mechanisms of neuropathic pain. Mol. Brain, 4, 2011, 31.
89. [90] Zimmermann, M., Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983), 109–110.
90. [91] Zygmunt, P.M., Petersson, J., Andersson, D.A., Chuang, H., Sørgård, M., Di Marzo, V., Julius, D., Högestätt, E.D., Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400 (1999), 452–457.