The endogenous fatty acid amide, palmitoylethanolamide, has anti-allodynic and anti-hyperalgesic effects in a murine model of neuropathic pain: involvement of CB1, TRPV1 and PPARγ receptors and neurotrophic factors

Pain

Volumn 139, Issue 3, 2008, Pages 541-550

  Costa, Barbara ^a   Comelli, Francesca ^a   Bettoni, Isabella ^a   Colleoni, Mariapia ^b   Giagnoni, Gabriella ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Cannabinoid; Neuropathic pain; Neurotrophic factors; Palmitoylethanolamide; Vanilloid

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ANALGESIC AGENT; ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CAPSAZEPINE; GW 6471; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIC FACTOR; PALMIDROL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RIMONABANT; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; DRUG MECHANISM; DRUG TISSUE LEVEL; ENZYME INHIBITION; HYPERALGESIA; IN VIVO STUDY; LIGATION; MALE; MAST CELL DEGRANULATION; MOUSE; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; SCIATIC NERVE;

ANALGESICS, NON-NARCOTIC; ANIMALS; CYTOPLASMIC GRANULES; DRUG EVALUATION, PRECLINICAL; HOT TEMPERATURE; HYPERALGESIA; LIGATION; MAST CELLS; MICE; NERVE GROWTH FACTORS; NF-KAPPA B; PALMITIC ACIDS; PHYSICAL STIMULATION; PPAR ALPHA; PPAR GAMMA; RECEPTOR, CANNABINOID, CB1; SCIATIC NERVE; SCIATICA; SPINAL CORD; TOUCH; TRPV CATION CHANNELS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 53349089891     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2008.06.003     Document Type: Article

References (68)

1. Aloe L., Leon A., and Levi-Montalcini R. A proposed autacoid mechanism controllino mastocyte behaviour. Agents Actions 39 (1993) C145-C147
2. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
3. Ben Shabat S., Fride E., Sheskin T., Tamiri T., Rhee M.H., Vogel Z., et al. An entourage effect: inactive endogenous fatty acid glycerol esters enhance 2-arachidonoylglicerol cannabinoid activity. Eur J Pharmacol 353 (1998) 23-31
4. Bouaboula M., Hilairet S., Marchand J., Fajas L., Le Fur G., and Casellas P. Anandamide induced PPARγ transcriptional activation and 3T3-L1 preadipocyte differentiation. Eur J Pharmacol 517 (2005) 174-181
5. Boucher T.J., Okuse K., Bennett D.L., Munson J.B., Wood J.N., and McMahon S.B. Potent analgesic effects of GDNF in neuropathic pain states. Science 290 (2000) 124-127
6. Calignano A., La Rana G., Giuffrida A., and Piomelli D. Control of pain initiation by endogenous cannabinoids. Nature 394 (1998) 277-281
7. Capasso R., Izzo A.A., Fezza F., Pinto A., Papasso F., Mascolo N., et al. Inhibitory effect of palmitoylethanolamide on gastrointestinal motility in mice. Br J Pharmacol 134 (2001) 945-950
8. Conti S., Costa B., Colleoni M., Parolaro D., and Giagnoni G. Antinflammatory action of endocannabinoid palmitoylethanolamide and the synthetic cannabinoid nabilone in a model of acute inflammation in the rat. Br J Pharmacol 135 (2002) 181-187
9. Costa B., Conti S., Giagnoni G., and Colleoni M. Therapeutic effect of the endogenous fatty acid amide, palmitoylethanolamide, in rat acute inflammation: inhibition of nitric oxide and cyclo-oxygenase systems. Br J Pharmacol 137 (2002) 413-420
10. De Petrocellis L., Bisogno T., Ligresti A., Bifulco M., Melck D., and Di Marzo V. Effect on cancer cell proliferation of palmitoylethanolamide, a fatty acid amide interacting with both the cannabinoid and vanilloid signalling systems. Fundam Clin Pharmacol 16 (2002) 297-302
11. Dong Z.Q., Wang Y.Q., Ma F., Xie H., and Wu G.C. Down-regulation of GFRalpha-1 expression by antisense oligodeoxynucleotide aggravates thermal hyperalgesia in a rat model of neuropathic pain. Neuropharmacology 50 (2006) 393-403
12. Farquhar-Smith W.P., Jaggar S.I., and Rice A.S. Attenuation of nerve growth factor-induced visceral hyperalgesia via cannabinoid CB(1) and CB(2)-like receptors. Pain 97 (2002) 11-21
13. Farquhar-Smith W.P., and Rice A.S. A novel neuroimmune mechanism in cannabinoid-mediated attenuation of nerve growth factor-induced hyperalgesia. Anesthesiology 99 (2003) 1391-1401
14. Feinstein D. Therapeutic potential of peroxisome proliferators-activated receptor agonists for neurological disease. Diab Tech Ther 5 (2003) 67-73
15. Franklin A., Parmentier-Batteur S., Walter L., Greenberg D.A., and Stella N. Palmitoylethanolamide increases after focal cerebral ischemia and potentiates microglial cell motility. J Neurosci 23 (2003) 7767-7775
16. Garcia-Bueno B., Madrigal J.L., Lizasoain I., Moro M.A., Lorenzo P., and Leza J.C. Peroxisome proliferator-activated receptor gamma activation decreases neuroinflammation in brain after stress in rats. Biol Psychiatry 57 (2005) 885-894
17. Hargreaves K.M., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
18. Helyes Z., Nemeth J., Than M., Bolcskei K., Pinter E., and Szolcsanyi J. Inhibitory effect of anandamide on resiniferatoxin-induced sensory neuropeptide release in vivo and neuropathic hyperalgesia in the rat. Life Sci 73 (2003) 2345-2353
19. Herzberg U., Eliav E., Dorsey J.M., Gracely R.H., and Kopin I.J. NGF involvement in pain induced by chronic constriction injury of the rat sciatic nerve. Neuroreport 8 (1997) 1613-1618
20. Horigome K., Pryor J.C., Bullock E.D., and Johnson Jr. E.M. Mediator release from mast cells by nerve growth factor, neurotrophin specificity and receptor mediation. J Biol Chem 268 (1993) 14881-14887
21. Jack D.B. Aliamides: a new approach to the treatment of inflammation. Drug News Perspectives 9 (1996) 93-98
22. Jaggar S.I., Hasnie F.S., Sellaturay S., and Rice A.C. The anti-hyperalgesic actions of the cannabinoid anandamide and the putative CB2 receptor agonist palmitoylethanolamide in visceral and somatic inflammatory pain. Pain 76 (1998) 189-199
23. Jonsson K.O., Vandervoorde S., Lambert D.M., Tiger G., and Fowler C.J. Effects of homologues and analogues of palmitoylethanolamide upon the inactivation of the endocannabinoid anandamide. Br J Pharmacol 133 (2001) 1263-1275
24. Knotkova H., Pappagallo M., and Szallasi A. Capsaicin (TRPV1 agonist) therapy for pain relief: farewell or revival?. Clin J Pain 24 (2008) 142-154
25. Lambert D.M., and Di Marzo V. The palmitoylethanolamide and oleamide enigmas: are these two fatty acid amides cannabimimetic?. Curr Med Chem 6 (1999) 757-773
26. Lambert D.M., Vandervoorde S., Diependaele G., Govaerts S.J., and Robert A.R. Anticonvulsant activity of N-palmitoylethanolamide, a putative endocannabinoid, in mice. Epilepsia 42 (2001) 321-327
27. Lambert D.M., Vandervoorde S., Jonsson K., and Fowler C.J. The palmitoylethanolamide family: a new class of anti-inflammatory agents?. Curr Med Chem 9 (2002) 663-674
28. Leon A., Buriani A., Dal Toso R., Fabris M., Romanello S., Aloe L., et al. Mast cells synthesize, store and release nerve growth factor. Proc Natl Acad Sci USA 91 (1994) 3739-3743
29. Levi-Montalcini R., Skaper S.D., Dal Toso R., Petrelli L., and Leon A. Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci 19 (1996) 514-520
30. Li L., Xian C.J., Zhong J.H., and Zhou X.F. Lumbar 5 ventral root transection-induced upregulation of nerve growth factor in sensory neurons and their target tissues: a mechanism in neuropathic pain. Mol Cell Neurosci 23 (2003) 232-250
31. Lim G., Sung B., Ji R.R., and Mao J. Upregulation of spinal cannabinoid-1-receptors following nerve injury enhances the effects of WIN-55,212-2 on neuropathic pain behaviours in rats. Pain 105 (2003) 275-283
32. Lo Verme J., La Rana G., Russo R., Calignano A., and Piomelli D. The search for the palmitoylethanolamide receptor. Life Sci 77 (2005) 1685-1698
33. Luna-Medina R., Cortes-Canteli M., Alonso M., Santos A., Martinez A., and Perez-Castillo A. Regulation of inflammatory response in neural cells in vitro by thiadiazolidinones derivatives through peroxisome proliferator-activated receptors gamma activation. J Biol Chem 280 (2005) 21453-21462
34. Mackie K., and Stella N. Cannabinoid receptors and endocannabinoids: evidence for new players. AAPS J 8 (2006) E298-E306
35. Malin S.A., Molliver D.C., Koerber H.R., Cornuet P., Frye R., Albers K.M., et al. Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J Neurosci 26 (2006) 8588-8599
36. Marcinkiewicz M., Marcinkiewicz J., Chen A., Leclaire F., Chretien M., and Richardson P. Nerve growth factor and proprotein convertases furin and PC7 in transacted sciatic nerves segments cultured in conditioned media: their presence in Schwann cells, macrophages, and smooth muscle cells. J Comp Neurol 403 (1999) 471-485
37. Mazzari S., Canella R., Petrelli L., Marcolongo G., and Leon A. N-(2-hydroxyethyl)hexadecanamide is orally active in reducing edema formation and inflammatory hyperalgesia by down-modulating mast cell activation. Eur J Pharmacol 300 (1996) 227-236
38. Mechoulam R., Fride E., and Di Marzo V. Endocannabinoids. Eur J Pharmacol 359 (1998) 1-18
39. Moalem G., and Tracey D.J. Immune and inflammatory mechanisms in neuropathic pain. Brain Res Rev 51 (2006) 240-264
40. Obata K., Tsujino H., Yamanaka H., Yi D., Fukuoka T., Hashimoto N., et al. Expression of neurotrophic factors in the dorsal root ganglion in a rat model of lumbar disc herniation. Pain 99 (2002) 121-132
41. Okamoto Y., Morishita J., Tsuboi K., Tonai T., and Ueda N. Molecular characterization of a phospholipase D generating anandamide and its congeners. J Biol Chem 279 (2004) 5298-5305
42. Olsson Y. Mast cells in the nervous system. Int Rev Cytol 24 (1968) 27-30
43. Park S.W., Yi J.H., Miranpuri G., Satriotomo I., Bowen K., Resnick D.K., et al. Thiazolidinedione class of peroxisome proliferators-activated receptor γ agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J Pharmacol Exp Ther 320 (2007) 1002-1012
44. Petrosino S., Palazzo E., de Novellis V., Bisogno T., Rossi F., Maione S., et al. Changes in spinal and supraspinal endocannabinoid levels in neuropathic rats. Neuropharmacology 52 (2007) 415-422
45. Pezet S., and McMahon S.B. Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29 (2006) 507-538
46. Ramer M.S., and Bisby M.A. Adrenergic innervation of rat sensory ganglia following proximal or distal painful sciatic neuropathy: distinct mechanisms revealed by anti-NGF treatment. Eur J Neurosci 11 (1999) 837-846
47. Rodriguez de Fonseca F., Navarro M., Gomez R., Escuredo L., Nava F., Fu J., et al. An anorexic lipid mediator regulated by feeding. Nature 414 (2001) 209-212
48. Ruiz G., and Banos J.E. The effect of endoneurial nerve growth factor on calcitonin gene-related peptide expression in primary sensory neurons. Brain Res 1042 (2005) 44-52
49. Ruiz G., Ceballos D., and Baños J.E. Behavioral and histological effects of endoneurial administration of nerve growth factor: possible implications in neuropathic pain. Brain Res 1011 (2004) 1-6
50. Sakai A., Asada M., Seno N., and Suzuki H. Involvement of neural cell adhesion molecule signaling in glial cell line-derived neurotrophic factor-induced analgesia in a rat model of neuropathic pain. Pain 137 (2008) 378-388
51. Schmid H.H., and Berdyshev E.V. Cannabinoid receptor-inactive N-acylethanolamines and other fatty acid amides: metabolism and function. Prostaglandins Leukot Essent Fatty Acids 66 (2002) 363-376
52. Sheerin A.H., Zhang X., Saucier D.M., and Corcoran M.E. Selective antiepileptic effects of N-palmitoylethanolamide, a putative endocannabinoid. Epilepsia 45 (2004) 1184-1188
53. Showalter V.M., Compton D.R., Martin B.R., and Abood M.E. Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): identification of cannabinoid receptor subtype selective ligands. J Pharmacol Exp Ther 278 (1996) 989-999
54. Skaper S.D., Pollock M., and Facci L. Mast cells differentially express and release active high molecular weight neurotrophins. Brain Res Mol Brain Res 97 (2001) 177-185
55. Smart D., Jonsson K.O., Vandevoorde S., Lambert D.M., and Fowler C.J. 'Entourage' effect of N-acyl ethanolamines at human vanilloid receptors. Comparison of effects upon anandamide-induced vanilloid receptor activation and upon anandamide metabolism. Br J Pharmacol 136 (2002) 452-458
56. Sommer C., and Schafers M. Painful mononeuropathy in C57BL/Wld mice with delayed wallerian degeneration: differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity. Brain Res 784 (1998) 154-162
57. Sommer C., Schmidt C., and George A. Hyperalgesia in experimental neuropathy is dependent on the TNF receptor 1. Exp Neurol 151 (1998) 138-142
58. Storer P.D., Xu J., Chavis J., and Drew P.D. Peroxisome proliferator-activated receptor gamma agonists inhibit the activation of microglia and astrocytes: implications for multiple sclerosis. J Neuroimmunol 161 (2005) 113-122
59. Sugiura T., Kondo S., Kishimoto S., Miyashita T., Nakane S., Kodaka T., et al. Evidence that 2-arachidonoylglycerol but not N-palmitoylethanolamine or anandamide is the physiological ligand for the cannabinoid CB2 receptor. Comparison of the agonistic activities of various cannabinoid receptor ligands in HL-60 cells. J Biol Chem 275 (2000) 605-612
60. Thacker M.A., Clark A.K., Marchand F., and McMahon S.B. Pathophysiology of peripheral neuropathic pain: immune cells and molecules. Anesth Analog 105 (2007) 838-847
61. Ueda N., Yamanaka K., and Yamamoto S. Purification and characterization of an acid amidase selective for N-palmitoylethanolamine, a putative endogenous anti-inflammatory substance. J Biol Chem 276 (2001) 35552-35557
62. Wallace V.C.J., Segerdahl A.R., Lambert D.M., Vandevoorde S., Blackbeard J., Pheby T., et al. The effect of the palmitoylethanolamide analogue, palmitoylallylamide (L-29) on pain behaviour in rodent models of neuropathy. Br J Pharmacol 151 (2007) 1117-1128
63. Wilson-Gerwing T.D., Dmyterko M.V., Zochodne D.W., Johnston J.M., and Verge V.M. Neurotrophin-3 suppresses thermal hyperalgesia associated with neuropathic pain and attenuates transient receptor potential vanilloid receptor-1 expression in adult sensory neurons. J Neurosci 25 (2005) 758-767
64. Zhou X.F., Deng Y.S., Xian C.J., and Zhong J.H. Neurotrophins from dorsal root ganglia trigger allodynia after spinal nerve injury in rats. Eur J Neurosci 12 (2000) 100-105
65. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110
66. Zochodne D.W., and Cheng C. Neurotrophins and other growth factors in the regenerative milieu of proximal nerve stump tips. J Anat 196 (2000) 279-283
67. Zuo Y., Perkins N.M., Tracey D.J., and Geczy C.L. Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells. Pain 105 (2003) 467-479
68. Zygmunt P.M., Petersson J., Andersson D.A., Chuang H., Sorgard M., Di Marzo V., et al. Vanilloid receptors on sensory nerves mediate the vasodilatator action of anandamide. Nature 400 (1999) 452-457