Characterisation of cannabinoid 1 receptor expression in the perikarya, and peripheral and spinal processes of primary sensory neurons

Brain Structure and Function

Volumn 218, Issue 3, 2013, Pages 733-750

  Veress, Gabor ^a,b   Meszar, Zoltan ^b   Muszil, Dora ^b   Avelino, Antonio ^c,d   Matesz, Klara ^b   Mackie, Ken ^e   Nagy, Istvan ^f  

^a Kaposi Mor Teaching Hospital   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c University of Porto   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

^e INDIANA UNIVERSITY   (United States)

^f CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

Author keywords

Anti nociception; Non peptidergic; Peptidergic; Somatosensory; Viscerosensory

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CANNABINOID 1 RECEPTOR; ISOLECTIN B4;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL POPULATION; CONTROLLED STUDY; DORSAL ROOT GANGLIA; GANGLION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MOLECULAR DYNAMICS; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SPINAL CORD;

ANALYSIS OF VARIANCE; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CHOLERA TOXIN; EPIDERMIS; GANGLIA, SPINAL; HIPPOCAMPUS; HORSERADISH PEROXIDASE; KERATINOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; NERVE FIBERS; RATS; RATS, INBRED WKY; RECEPTOR, CANNABINOID, CB1; RNA, MESSENGER; SENSORY RECEPTOR CELLS; SPINAL CORD;

GRIFFONIA SIMPLICIFOLIA;

EID: 84879551326     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-012-0425-2     Document Type: Article

References (117)

1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics Int 11(7):36-42
2. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, Rubino T, Michalski CW, Marsicano G, Monory K, Mackie K, Marian C, Batkai S, Parolaro D, Fischer MJ, Reeh P, Kunos G, Kress M, Lutz B, Woolf CJ, Kuner R (2007) Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 10(7):870-879. doi: 10.1038/nn1916
3. Ahluwalia J, Urban L, Capogna M, Bevan S, Nagy I (2000) Cannabinoid 1 receptors are expressed in nociceptive primary sensory neurons. Neuroscience 100(4):685-688. pii:S0306452200003894
4. Ahluwalia J, Urban L, Bevan S, Capogna M, Nagy I (2002) Cannabinoid 1 receptors are expressed by nerve growth factor- and glial cell-derived neurotrophic factor-responsive primary sensory neurones. Neuroscience 110(4):747-753. pii:S0306452201006017
5. Ahluwalia J, Urban L, Bevan S, Nagy I (2003a) Anandamide regulates neuropeptide release from capsaicin-sensitive primary sensory neurons by activating both the cannabinoid 1 receptor and the vanilloid receptor 1 in vitro. Eur J Neurosci 17(12):2611-2618. pii: 2703
6. Ahluwalia J, Yaqoob M, Urban L, Bevan S, Nagy I (2003b) Activation of capsaicin-sensitive primary sensory neurones induces anandamide production and release. J Neurochem 84(3):585-591. pii: 1550
7. Amaya F, Shimosato G, Kawasaki Y, Hashimoto S, Tanaka Y, Ji RR, Tanaka M (2006) Induction of CB1 cannabinoid receptor by inflammation in primary afferent neurons facilitates antihyperalgesic effect of peripheral CB1 agonist. Pain 124(1-2):175-183. doi: 10.1016/j.pain.2006.04.001
8. Avelino A, Cruz C, Nagy I, Cruz F (2002) Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 109(4):787-798. pii: S0306452201004961
9. Bennett DL, Dmietrieva N, Priestley JV, Clary D, McMahon SB (1996) trkA, CGRP and IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neurosci Lett 206(1):33-36. pii: 0304394096124186
10. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, Monory K, Marsicano G, Matteoli M, Canty A, Irving AJ, Katona I, Yanagawa Y, Rakic P, Lutz B, Mackie K, Harkany T (2007) Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316(5828):1212-1216. doi: 10.1126/science.1137406
11. Binzen U, Greffrath W, Hennessy S, Bausen M, Saaler-Reinhardt S, Treede RD (2006) Co-expression of the voltage-gated potassium channel Kv1.4 with transient receptor potential channels (TRPV1 and TRPV2) and the cannabinoid receptor CB1 in rat dorsal root ganglion neurons. Neuroscience 142(2):527-539. doi: 10.1016/j.neuroscience.2006.06.020
12. Biro T, Toth BI, Hasko G, Paus R, Pacher P (2009) The endocannabinoid system of the skin in health and disease: novel perspectives and therapeutic opportunities. Trends Pharmacol Sci 30(8):411-420. doi: 10.1016/j.tips.2009.05. 004
13. Breese NM, George AC, Pauers LE, Stucky CL (2005) Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 115(1-2):37-49. doi: 10.1016/j.pain.2005.02.010
14. Bridges D, Rice AS, Egertova M, Elphick MR, Winter J, Michael GJ (2003) Localisation of cannabinoid receptor 1 in rat dorsal root ganglion using in situ hybridisation and immunohistochemistry. Neuroscience 119(3):803-812. pii:S0306452203002008
15. Calignano A, La Rana G, Giuffrida A, Piomelli D (1998) Control of pain initiation by endogenous cannabinoids. Nature 394(6690):277-281. doi: 10.1038/28393
16. Carrier EJ, Kearn CS, Barkmeier AJ, Breese NM, Yang W, Nithipatikom K, Pfister SL, Campbell WB, Hillard CJ (2004) Cultured rat microglial cells synthesize the endocannabinoid 2-arachidonylglycerol, which increases proliferation via a CB2 receptor-dependent mechanism. Mol Pharmacol 65(4):999-1007. doi: 10.1124/mol.65.4.99965/4/999
17. Casanova ML, Blazquez C, Martinez-Palacio J, Villanueva C, Fernandez-Acenero MJ, Huffman JW, Jorcano JL, Guzman M (2003) Inhibition of skin tumor growth and angiogenesis in vivo by activation of cannabinoid receptors. J Clin Invest 111(1):43-50. doi: 10.1172/JCI16116
18. Cavanaugh DJ, Lee H, Lo L, Shields SD, Zylka MJ, Basbaum AI, Anderson DJ (2009) Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci USA 106(22):9075-9080. doi: 10.1073/pnas.0901507106
19. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN (1995) A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377(6548):428-431. doi: 10.1038/377428a0
20. Choi JS, Dib-Hajj SD, Waxman SG (2007) Differential slow inactivation and use-dependent inhibition of Nav1.8 channels contribute to distinct firing properties in IB4 + and IB4- DRG neurons. J Neurophysiol 97(2):1258-1265. doi: 10.1152/jn.01033.2006
21. Clapper JR, Moreno-Sanz G, Russo R, Guijarro A, Vacondio F, Duranti A, Tontini A, Sanchini S, Sciolino NR, Spradley JM, Hohmann AG, Calignano A, Mor M, Tarzia G, Piomelli D (2010) Anandamide suppresses pain initiation through a peripheral endocannabinoid mechanism. Nat Neurosci 13(10):1265-1270. doi: 10.1038/nn.2632
22. Deadwyler SA, Hampson RE, Mu J, Whyte A, Childers S (1995) Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J Pharmacol Exp Ther 273(2):734-743
23. Deutsch DG, Goligorsky MS, Schmid PC, Krebsbach RJ, Schmid HH, Das SK, Dey SK, Arreaza G, Thorup C, Stefano G, Moore LC (1997) Production and physiological actions of anandamide in the vasculature of the rat kidney. J Clin Invest 100(6):1538-1546. doi: 10.1172/JCI119677
24. Di Marzo V (2008) Endocannabinoids: synthesis and degradation. Rev Physiol Biochem Pharmacol 160:1-24. doi: 10.1007/112-0505
25. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, Piomelli D (1994) Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372(6507):686-691. doi: 10.1038/372686a0
26. Di Marzo V, De Petrocellis L, Sepe N, Buono A (1996) Biosynthesis of anandamide and related acylethanolamides in mouse J774 macrophages and N18 neuroblastoma cells. Biochem J 316(Pt 3):977-984
27. Di Marzo V, Melck D, Bisogno T, De Petrocellis L (1998) Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci 21(12):521-528. pii:S0166-2236(98)01283-1
28. Di Marzo V, De Petrocellis L, Bisogno T, Melck D (1999) Metabolism of anandamide and 2-arachidonoylglycerol: an historical overview and some recent developments. Lipids 34(Suppl):S319-S325
29. Dinh TP, Freund TF, Piomelli D (2002) A role for monoglyceride lipase in 2-arachidonoylglycerol inactivation. Chem Phys Lipids 121(1-2):149-158. pii:S0009308402001500
30. Dinis P, Charrua A, Avelino A, Yaqoob M, Bevan S, Nagy I, Cruz F (2004) Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. J Neurosci 24(50):11253-11263
31. Dirajlal S, Pauers LE, Stucky CL (2003) Differential response properties of IB(4)-positive and -negative unmyelinated sensory neurons to protons and capsaicin. J Neurophysiol 89(1):513-524. doi: 10.1152/jn.00371.2002
32. Egertova M, Elphick MR (2000) Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422(2):159-171. doi: 10.1002/(SICI)1096-9861(20000626)422:2<159:: AID-CNE1>3.0.CO;2-1
33. Ellington HC, Cotter MA, Cameron NE, Ross RA (2002) The effect of cannabinoids on capsaicin-evoked calcitonin gene-related peptide (CGRP) release from the isolated paw skin of diabetic and non-diabetic rats. Neuropharmacology 42(7):966-975. pii:S0028390802000400
34. Farquhar-Smith WP, Egertova M, Bradbury EJ, McMahon SB, Rice AS, Elphick MR (2000) Cannabinoid CB(1) receptor expression in rat spinal cord. Mol Cell Neurosci 15(6):510-521. doi: 10.1006/mcne.2000.0844
35. Fischbach T, Greffrath W, Nawrath H, Treede RD (2007) Effects of anandamide and noxious heat on intracellular calcium concentration in nociceptive DRG neurons of rats. J Neurophysiol 98(2):929-938. doi: 10.1152/jn.01096.2006
36. Fuxe K, Marcellino D, Woods AS, Giuseppina L, Antonelli T, Ferraro L, Tanganelli S, Agnati LF (2009) Integrated signaling in heterodimers and receptor mosaics of different types of GPCRs of the forebrain: relevance for schizophrenia. J Neural Transm 116(8):923-939. doi: 10.1007/s00702-008-0174-9
37. Gao Y, Vasilyev DV, Goncalves MB, Howell FV, Hobbs C, Reisenberg M, Shen R, Zhang MY, Strassle BW, Lu P, Mark L, Piesla MJ, Deng K, Kouranova EV, Ring RH, Whiteside GT, Bates B, Walsh FS, Williams G, Pangalos MN, Samad TA, Doherty P (2010) Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J Neurosci 30(6):2017-2024. doi: 10.1523/JNEUROSCI.5693-09.2010
38. Gratzke C, Streng T, Park A, Christ G, Stief CG, Hedlund P, Andersson KE (2009) Distribution and function of cannabinoid receptors 1 and 2 in the rat, monkey and human bladder. J Urol 181(4):1939-1948
39. Guasti L, Richardson D, Jhaveri M, Eldeeb K, Barrett D, Elphick MR, Alexander SP, Kendall D, Michael GJ, Chapman V (2009) Minocycline treatment inhibits microglial activation and alters spinal levels of endocannabinoids in a rat model of neuropathic pain. Mol Pain 5:35. doi: 10.1186/1744-8069-5-35
40. Guindon J, Guijarro A, Piomelli D, Hohmann AG (2010) Peripheral antinociceptive effects of inhibitors of monoacylglycerol lipase in a rat model of inflammatory pain. Br J Pharmacol. doi: 10.1111/j.1476-5381.2010.01192.x
41. Hayn MH, Ballesteros I, de Miguel F, Coyle CH, Tyagi S, Yoshimura N, Chancellor MB, Tyagi P (2008a) Functional and immunohistochemical characterization of CB1 and CB2 receptors in rat bladder. Urology 72(5):1174-1178
42. Hayn MH, Ballesteros I, de Miguel F, Coyle CH, Tyagi S, Yoshimura N, Chancellor MB, Tyagi P (2008b) Functional and immunohistochemical characterization of CB1 and CB2 receptors in rat bladder. Urology 72(5):1174-1178. doi: 10.1016/j.urology.2008.03.044
43. Hegyi Z, Kis G, Hollo K, Ledent C, Antal M (2009) Neuronal and glial localization of the cannabinoid-1 receptor in the superficial spinal dorsal horn of the rodent spinal cord. Eur J Neurosci 30(2):251-262. doi: 10.1111/j.1460-9568.2009.06816.x
44. Hoffman AF, Riegel AC, Lupica CR (2003) Functional localization of cannabinoid receptors and endogenous cannabinoid production in distinct neuron populations of the hippocampus. Eur J Neurosci 18(3):524-534. pii: 2773
45. Hohmann AG (2002) Spinal and peripheral mechanisms of cannabinoid antinociception: behavioral, neurophysiological and neuroanatomical perspectives. Chem Phys Lipids 121(1-2):173-190 pii: S0009308402001548
46. Hohmann AG, Herkenham M (1999) Localization of central cannabinoid CB1 receptor messenger RNA in neuronal subpopulations of rat dorsal root ganglia: a double-label in situ hybridization study. Neuroscience 90(3):923-931 pii:S0306-4522(98)00524-7
47. Hohmann AG, Tsou K, Walker JM (1998) Cannabinoid modulation of wide dynamic range neurons in the lumbar dorsal horn of the rat by spinally administered WIN55,212-2. Neurosci Lett 257(3):119-122 pii: S0304394098008027
48. Hohmann AG, Briley EM, Herkenham M (1999) Pre- and postsynaptic distribution of cannabinoid and mu opioid receptors in rat spinal cord. Brain Res 822(1-2):17-25 pii: S0006-8993(98)01321-3
49. Howlett AC (1998) The CB1 cannabinoid receptor in the brain. Neurobiol Dis 5 (6 Pt B):405-416. doi: 10.1006/nbdi.1998.0215
50. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54(2):161-202
51. Jaggar SI, Hasnie FS, Sellaturay S, Rice AS (1998) The anti-hyperalgesic actions of the cannabinoid anandamide and the putative CB2 receptor agonist palmitoylethanolamide in visceral and somatic inflammatory pain. Pain 76(1-2):189-199 pii: S0304-3959(98)00041-4
52. Jennings EA, Vaughan CW, Christie MJ (2001) Cannabinoid actions on rat superficial medullary dorsal horn neurons in vitro. J Physiol 534(Pt 3):805-812
53. Jhaveri MD, Richardson D, Kendall DA, Barrett DA, Chapman V (2006) Analgesic effects of fatty acid amide hydrolase inhibition in a rat model of neuropathic pain. J Neurosci 26(51):13318-13327. doi: 10.1523/JNEUROSCI.3326-06. 2006
54. Katona I, Urban GM, Wallace M, Ledent C, Jung KM, Piomelli D, Mackie K, Freund TF (2006) Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26(21):5628-5637. doi: 10.1523/JNEUROSCI. 0309-06.2006
55. Khasabova IA, Simone DA, Seybold VS (2002) Cannabinoids attenuate depolarization-dependent Ca2+ influx in intermediate-size primary afferent neurons of adult rats. Neuroscience 115(2):613-625. pii:S0306452202004499
56. Khasabova IA, Harding-Rose C, Simone DA, Seybold VS (2004) Differential effects of CB1 and opioid agonists on two populations of adult rat dorsal root ganglion neurons. J Neurosci 24(7):1744-1753. doi: 10.1523/JNEUROSCI.4298-03. 200424/7/1744
57. Khasabova IA, Khasabov SG, Harding-Rose C, Coicou LG, Seybold BA, Lindberg AE, Steevens CD, Simone DA, Seybold VS (2008) A decrease in anandamide signaling contributes to the maintenance of cutaneous mechanical hyperalgesia in a model of bone cancer pain. J Neurosci 28(44):11141-11152. doi: 10.1523/JNEUROSCI.2847-08.2008
58. Kreitzer AC, Regehr WG (2002) Retrograde signaling by endocannabinoids. Curr Opin Neurobiol 12(3):324-330 (pii:S0959438802003288)
59. Lauckner JE, Jensen JB, Chen HY, Lu HC, Hille B, Mackie K (2008) GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proc Natl Acad Sci USA 105(7):2699-2704. doi: 10.1073/pnas.0711278105
60. Lawson SN, Crepps B, Perl ER (2002) Calcitonin gene-related peptide immunoreactivity and afferent receptive properties of dorsal root ganglion neurones in guinea-pigs. J Physiol 540(Pt 3):989-1002
61. Lever IJ, Robinson M, Cibelli M, Paule C, Santha P, Yee L, Hunt SP, Cravatt BF, Elphick MR, Nagy I, Rice ASC (2009) Localization of the endocannabinoid-degrading enzyme fatty acid amide hydrolase in rat dorsal root ganglion cells and its regulation after peripheral nerve injury. J Neurosci 29(12):3766-3780
62. Ligresti A, Cascio MG, Di Marzo V (2005) Endocannabinoid metabolic pathways and enzymes. Curr Drug Targets CNS Neurol Disord 4(6):615-623
63. Maccarrone M, DiRienzo M, Battista N, Gasperi V, Guerrieri P, Rossi A, Finazzi-Agro A (2003) The endocannabinoid system in human keratinocytes. Evidence that anandamide inhibits epidermal differentiation through CB1 receptor-dependent inhibition of protein kinase C, activation protein-1, and transglutaminase. J Biol Chem 278(36):33896-33903. doi: 10.1074/jbc.M303994200
64. Mackie K (2005) Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb Exp Pharmacol 168:299-325
65. Mackie K, Hille B (1992) Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci USA 89(9):3825-3829
66. Mackie K, Lai Y, Westenbroek R, Mitchell R (1995) Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 15(10):6552-6561
67. Maggi CA, Santicioli P, Geppetti P, Furio M, Frilli S, Conte B, Fanciullacci M, Giuliani S, Meli A (1987) The contribution of capsaicin-sensitive innervation to activation of the spinal vesico-vesical reflex in rats: relationship between substance P levels in the urinary bladder and the sensory-efferent function of capsaicin-sensitive sensory neurons. Brain Res 415(1):1-13 pii:0006-8993(87)90263-0
68. Mahmud A, Santha P, Paule CC, Nagy I (2009) Cannabinoid 1 receptor activation inhibits transient receptor potential vanilloid type 1 receptor-mediated cationic influx into rat cultured primary sensory neurons. Neuroscience 162(4):1202-1211. doi: 10.1016/j.neuroscience.2009.05.024
69. Mailleux P, Vanderhaeghen JJ (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48(3):655-668 (pii:0306-4522(92)90409-U)
70. Martin WJ, Lai NK, Patrick SL, Tsou K, Walker JM (1993) Antinociceptive actions of cannabinoids following intraventricular administration in rats. Brain Res 629(2):300-304 (pii:0006-8993(93)91334-O)
71. Martin WJ, Patrick SL, Coffin PO, Tsou K, Walker JM (1995) An examination of the central sites of action of cannabinoid-induced antinociception in the rat. Life Sci 56(23-24):2103-2109
72. Martini L, Thompson D, Kharazia V, Whistler JL (2010) Differential regulation of behavioral tolerance to WIN55,212-2 by GASP1. Neuropsychopharmacology. Neuropsychopharmacology 35(6):1363-1373. doi: 10.1038/npp2010.6
73. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346(6284):561-564. doi: 10.1038/346561a0
74. Merriam FV, Wang ZY, Guerios SD, Bjorling DE (2008) Cannabinoid receptor 2 is increased in acutely and chronically inflamed bladder of rats. Neurosci Lett 445(1):130-134
75. Mitrirattanakul S, Ramakul N, Guerrero AV, Matsuka Y, Ono T, Iwase H, Mackie K, Faull KF, Spigelman I (2006) Site-specific increases in peripheral cannabinoid receptors and their endogenous ligands in a model of neuropathic pain. Pain 126(1-3):102-114. doi: 10.1016/j.pain.2006.06.016
76. Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wolfel B, Dodt HU, Zieglgansberger W, Wotjak CT, Mackie K, Elphick MR, Marsicano G, Lutz B (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51(4):455-466. doi: 10.1016/j.neuron.2006.07.006
77. Morisset V, Urban L (2001) Cannabinoid-induced presynaptic inhibition of glutamatergic EPSCs in substantia gelatinosa neurons of the rat spinal cord. J Neurophysiol 86(1):40-48
78. Morisset V, Ahluwalia J, Nagy I, Urban L (2001) Possible mechanisms of cannabinoid-induced antinociception in the spinal cord. Eur J Pharmacol 429(1-3):93-100. pii: S0014299901013097
79. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365(6441):61-65. doi: 10.1038/365061a0
80. Nyilas R, Gregg LC, Mackie K, Watanabe M, Zimmer A, Hohmann AG, Katona I (2009) Molecular architecture of endocannabinoid signaling at nociceptive synapses mediating analgesia. Eur J Neurosci 29(10):1964-1978. doi: 10.1111/j.1460-9568.2009.06751.x
81. Ong WY, Mackie K (1999) A light and electron microscopic study of the CB1 cannabinoid receptor in the primate spinal cord. J Neurocytol 28(1):39-45
82. Pernia-Andrade AJ, Kato A, Witschi R, Nyilas R, Katona I, Freund TF, Watanabe M, Filitz J, Koppert W, Schuttler J, Ji G, Neugebauer V, Marsicano G, Lutz B, Vanegas H, Zeilhofer HU (2009) Spinal endocannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain sensitization. Science 325(5941):760-764. doi: 10.1126/science.1171870
83. Perry MJ, Lawson SN (1993) Neurofilaments in rat and cat spinal cord: a comparative immunocytochemical study of phosphorylated and non-phosphorylated subunits. Cell Tissue Res 272(2):249-256
84. Pertwee RG (2001) Cannabinoid receptors and pain. Prog Neurobiol 63(5):569-611. pii: S0301-0082(00)00031-9
85. Pertwee RG (2005) Pharmacological actions of cannabinoids. Handb Exp Pharmacol 168:1-51
86. Petrosino S, Palazzo E, de Novellis V, Bisogno T, Rossi F, Maione S, Di Marzo V (2007) Changes in spinal and supraspinal endocannabinoid levels in neuropathic rats. Neuropharmacology 52(2):415-422. doi: 10.1016/j.neuropharm. 2006.08.011
87. Plenderleith MB, Snow PJ (1993) The plant lectin Bandeiraea simplicifolia I-B4 identifies a subpopulation of small diameter primary sensory neurones which innervate the skin in the rat. Neurosci Lett 159(1-2):17-20
88. Potenzieri C, Brink TS, Pacharinsak C, Simone DA (2008) Cannabinoid modulation of cutaneous Adelta nociceptors during inflammation. J Neurophysiol 100(5):2794-2806. doi: 10.1152/jn.90809.2008
89. Price J (1985) An immunohistochemical and quantitative examination of dorsal root ganglion neuronal subpopulations. J Neurosci 5(8):2051-2059
90. Price TJ, Helesic G, Parghi D, Hargreaves KM, Flores CM (2003) The neuronal distribution of cannabinoid receptor type 1 in the trigeminal ganglion of the rat. Neuroscience 120(1):155-162. pii: S0306452203003336
91. Puighermanal E, Marsicano G, Busquets-Garcia A, Lutz B, Maldonado R, Ozaita A (2009) Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat Neurosci 12(9):1152-1158. doi: 10.1038/nn.2369
92. Richardson JD, Aanonsen L, Hargreaves KM (1998a) Antihyperalgesic effects of spinal cannabinoids. Eur J Pharmacol 345(2):145-153. pii: S0014-2999(97)01621-X
93. Richardson JD, Kilo S, Hargreaves KM (1998b) Cannabinoids reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain 75(1):111-119. pii:S0304395997002133
94. Rozenfeld R, Devi LA (2008) Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J 22(7):2311-2322. doi: 10.1096/fj.07-102731
95. Sagar DR, Kelly S, Millns PJ, O'Shaughnessey CT, Kendall DA, Chapman V (2005) Inhibitory effects of CB1 and CB2 receptor agonists on responses of DRG neurons and dorsal horn neurons in neuropathic rats. Eur J Neurosci 22(2):371-379. doi: 10.1111/j.1460-9568.2005.04206.x
96. Salio C, Fischer J, Franzoni MF, Mackie K, Kaneko T, Conrath M (2001) CB1-cannabinoid and mu-opioid receptor co-localization on postsynaptic target in the rat dorsal horn. NeuroReport 12(17):3689-3692
97. Salio C, Fischer J, Franzoni MF, Conrath M (2002) Pre- and postsynaptic localizations of the CB1 cannabinoid receptor in the dorsal horn of the rat spinal cord. Neuroscience 110(4):755-764. pii:S030645220100584X
98. Santha P, Jenes A, Somogyi C, Nagy I (2010a) The endogenous cannabinoid anandamide inhibits transient receptor potential vanilloid type 1 receptor-mediated currents in rat cultured primary sensory neurons. Acta Physiol Hung 97(2):149-158. doi: 10.1556/APhysiol.97.2010.2.1
99. Santha P, Oszlacs O, Dux M, Dobos I, Jancso G (2010b) Inhibition of glucosylceramide synthase reversibly decreases the capsaicin-induced activation and TRPV1 expression of cultured dorsal root ganglion neurons. Pain. doi: 10.1016/j.pain.2010.04.006
100. Sanudo-Pena MC, Strangman NM, Mackie K, Walker JM, Tsou K (1999) CB1 receptor localization in rat spinal cord and roots, dorsal root ganglion, and peripheral nerve. Zhongguo Yao Li Xue Bao 20(12):1115-1120
101. Silverman JD, Kruger L (1988) Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. Somatosens Res 5(3):259-267
102. Soneji ND, Paule CC, Mlynarczyk M, Nagy I (2010) Effects of cannabinoids on capsaicin receptor activity following exposure of primary sensory neurons to inflammatory mediators. Life Sci 87 (5-6):162-168. doi: 10.1016/j.lfs.2010.06. 003
103. Song C, Howlett AC (1995) Rat brain cannabinoid receptors are N-linked glycosylated proteins. Life Sci 56(23-24):1983-1989
104. Spradley JM, Guindon J, Hohmann AG (2010) Inhibitors of monoacylglycerol lipase, fatty-acid amide hydrolase and endocannabinoid transport differentially suppress capsaicin-induced behavioral sensitization through peripheral endocannabinoid mechanisms. Pharmacol Res 62(3):249-258. doi: 10.1016/j.phrs.2010.03.007
105. Stander S, Schmelz M, Metze D, Luger T, Rukwied R (2005) Distribution of cannabinoid receptor 1 (CB1) and 2 (CB2) on sensory nerve fibers and adnexal structures in human skin. J Dermatol Sci 38(3):177-188. doi: 10.1016/j.jdermsci.2005.01.007
106. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388(6644):773-778. doi: 10.1038/42015
107. Sugiura T, Kishimoto S, Oka S, Gokoh M (2006) Biochemistry, pharmacology and physiology of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Prog Lipid Res 45(5):405-446. doi: 10.1016/j.plipres.2006.03.003
108. Suplita RL 2nd, Gutierrez T, Fegley D, Piomelli D, Hohmann AG (2006) Endocannabinoids at the spinal level regulate, but do not mediate, nonopioid stress-induced analgesia. Neuropharmacology 50(3):372-379. doi: 10.1016/j.neuropharm.2005.10.007
109. Szabo B, Urbanski MJ, Bisogno T, Di Marzo V, Mendiguren A, Baer WU, Freiman I (2006) Depolarization-induced retrograde synaptic inhibition in the mouse cerebellar cortex is mediated by 2-arachidonoylglycerol. J Physiol 577(Pt 1):263-280. doi: 10.1113/jphysiol.2006.119362
110. Tanimura A, Yamazaki M, Hashimotodani Y, Uchigashima M, Kawata S, Abe M, Kita Y, Hashimoto K, Shimizu T, Watanabe M, Sakimura K, Kano M (2010) The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron 65 (3):320-327. doi: 10.1016/j.neuron.2010.01.021
111. Twitchell W, Brown S, Mackie K (1997) Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 78(1):43-50
112. Tyagi V, Philips BJ, Su R, Smaldone MC, Erickson VL, Chancellor MB, Yoshimura N, Tyagi P (2009) Differential expression of functional cannabinoid receptors in human bladder detrusor and urothelium. J Urol 181(4):1932-1938
113. Vellani V, Zachrisson O, McNaughton PA (2004) Functional bradykinin B1 receptors are expressed in nociceptive neurones and are upregulated by the neurotrophin GDNF. J Physiol 560(Pt 2):391-401. doi: 10.1113/jphysiol.2004. 067462jphysiol.2004.067462
114. Walczak JS, Price TJ, Cervero F (2009) Cannabinoid CB1 receptors are expressed in the mouse urinary bladder and their activation modulates afferent bladder activity. Neuroscience 159(3):1154-1163
115. Westlake TM, Howlett AC, Bonner TI, Matsuda LA, Herkenham M (1994) Cannabinoid receptor binding and messenger RNA expression in human brain: an in vitro receptor autoradiography and in situ hybridization histochemistry study of normal aged and Alzheimer's brains. Neuroscience 63(3):637-652. pii:0306-4522(94)90511-8
116. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410(6828):588-592. doi: 10.1038/3506907635069076
117. Zhang F, Hong S, Stone V, Smith PJ (2007) Expression of cannabinoid CB1 receptors in models of diabetic neuropathy. J Pharmacol Exp Ther 323(2):508-515. doi: 10.1124/jpet.107.128272