Palmitoylethanolamide is a disease-modifying agent in peripheral neuropathy: Pain relief and neuroprotection share a PPAR-alpha-mediated mechanism

Mediators of Inflammation

Volumn 2013, Issue , 2013, Pages

  Di Cesare Mannelli, L ^a   D'Agostino, G ^b   Pacini, A ^a   Russo, R ^b   Zanardelli, M ^a   Ghelardini, C ^a   Calignano, A ^b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD86 ANTIGEN; MYELIN; PALMIDROL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; ENDOCANNABINOID; ETHANOLAMINE DERIVATIVE; PALMITIC ACID DERIVATIVE;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; EDEMA; HISTOPATHOLOGY; MACROPHAGE; MALE; MOUSE; MYELIN SHEATH; NERVE FIBER; NEUROPROTECTION; NONHUMAN; PAIN THRESHOLD; PERIPHERAL NERVE; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; ANIMAL; GENETICS; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE MUTANT; WESTERN BLOTTING;

ANIMALIA; MUS; RODENTIA;

ANIMALS; BLOTTING, WESTERN; ENDOCANNABINOIDS; ETHANOLAMINES; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; PALMITIC ACIDS; PERIPHERAL NERVOUS SYSTEM DISEASES; PPAR ALPHA;

EID: 84875477119     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2013/328797     Document Type: Article

References (48)

1. Dyck P. J., The causes, classification and treatment of peripheral neuropathy. The New England Journal of Medicine 1982 307 283 286 10.1056/NEJM198207293070504 (Pubitemid 12081699)
2. Baron R., Mechanisms of disease: neuropathic pain-a clinical perspective. Nature Clinical Practice Neurology 2006 2 95 106 10.1038/ncpneuro0113 (Pubitemid 43210250)
3. Tal M., A role for inflammation in chronic pain. Current Review of Pain 1999 3 440 446 10.1007/s11916-999-0071-4
4. Vivoli E., Di Cesare Mannelli L., Salvicchi A., Bartolini A., Koverech A., Nicolai R., Benatti P., Ghelardini C., Acetyl-l-carnitine increases artemin level and prevents neurotrophic factor alterations during neuropathy. Neuroscience 2010 167 4 1168 1174 2-s2.0-77952553820 10.1016/j.neuroscience. 2010.03.017
5. Üçeyler N., Göbel K., Meuth S. G., Ortler S., Stoll G., Sommer C., Wiendl H., Kleinschnitz C., Deficiency of the negative immune regulator B7-H1 enhances inflammation and neuropathic pain after chronic constriction injury of mouse sciatic nerve. Experimental Neurology 2010 222 1 153 160 2-s2.0-77649342966 10.1016/j.expneurol.2009.12.026
6. Gomez-Nicola D., Valle-Argos B., Suardiaz M., Taylor J. S., Nieto-Sampedro M., Role of IL-15 in spinal cord and sciatic nerve after chronic constriction injuty: regulation of macrophage and T-cell infilatration. Journal of Neurochemistry 2008 107 1741 1752 10.1111/j.1471-4159.2008.05746.x
7. Pacini A., Di Cesare Mannelli L., Bonaccini L., Ronzoni S., Bartolini A., Ghelardini C., Protective effect of alpha7 nAChR: behavioural and morphological features on neuropathy. Pain 2010 150 3 542 549 2-s2.0-77955588896 10.1016/j.pain.2010.06.014
8. Hu P., McLachlan E. M., Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat. Neuroscience 2002 112 1 23 38 2-s2.0-0037067053 10.1016/S0306-4522(02)00065-9 (Pubitemid 34603495)
9. Morin N., Owolabi S. A., Harty M. W., Papa E. F., Tracy T. F., Shaw S. K., Kim M., Saab C. Y., Neutrophils invade lumbar dorsal root ganglia after chronic constriction injury of the sciatic nerve. Journal of Neuroimmunology 2007 184 1-2 164 171 2-s2.0-33847685669 10.1016/j.jneuroim.2006.12.009 (Pubitemid 46365998)
10. Di Cesare Mannelli L., Ghelardini C., Calvani M., Nicolai R., Mosconi L., Vivoli E., Pacini A., Bartolini A., Protective effect of acetyl-L-carnitine on the apoptotic pathway of peripheral neuropathy. European Journal of Neuroscience 2007 26 4 820 827 2-s2.0-34547994382 10.1111/j.1460-9568.2007.05722.x (Pubitemid 47274617)
11. Calignano A., La Rana G., Giuffrida A., Piomelli D., Control of pain initiation by endogenous cannabinoids. Nature 1998 394 6690 277 281 2-s2.0-0032537734 10.1038/28393 (Pubitemid 28335039)
12. LoVerme J., Russo R., La Rana G., Fu J., Farthing J., Mattace-Raso G., Meli R., Hohmann A., Calignano A., Piomelli D., Rapid broad-spectrum analgesia through activation of peroxisome proliferator-activated receptor- α Journal of Pharmacology and Experimental Therapeutics 2006 319 3 1051 1061 2-s2.0-33751166817 10.1124/jpet.106.111385
13. Lambert D. M., Vandevoorde S., Diependaele G., Govaerts S. J., Robert A. R., Anticonvulsant activity of N-palmitoylethanolamide, a putative endocannabinoid, in mice. Epilepsia 2001 42 3 321 327 2-s2.0-0035060264 10.1046/j.1528-1157.2001.41499.x (Pubitemid 32275910)
14. D'Agostino G., Russo R., Avagliano C., Cristiano C., Meli R., Calignano A., Palmitoylethanolamide protects against the amyloid- β 25-35-induced learning and memory impairment in mice, an experimental model of Alzheimer disease. Neuropsychopharmacology 2012 37 1784 1792 10.1038/npp.2012.25
15. Mazzari S., Canella R., Petrelli L., Marcolongo G., Leon A., N-(2-Hydroxyethyl) hexadecanamide is orally active in reducing edema formation and inflammatory hyperalgesia by down-modulating mast cell activation. European Journal of Pharmacology 1996 300 3 227 236 2-s2.0-0029865544 10.1016/0014-2999(96)00015-5
16. Ross R. A., Brockie H. C., Pertwee R. G., Inhibition of nitric oxide production in RAW264.7 macrophages by cannabinoids and palmitoylethanolamide. European Journal of Pharmacology 2000 401 2 121 130 2-s2.0-0034604755 10.1016/S0014-2999(00)00437-4 (Pubitemid 30488186)
17. Solorzano C., Zhu C., Battista N., Astarita G., Lodola A., Rivara S., Mor M., Russo R., Maccarrone M., Antonietti F., Duranti A., Tontini A., Cuzzocrea S., Tarzia G., Piomelli D., Selective N-acylethanolamine-hydrolyzing acid amidase inhibition reveals a key role for endogenous palmitoylethanolamide in inflammation. Proceedings of the National Academy of Sciences of the United States of America 2009 106 49 20966 20971 2-s2.0-73949084238 10.1073/pnas.0907417106
18. Lo Verme J., Fu J., Astarita G., La Rana G., Russo R., Calignano A., Piomelli D., The nuclear receptor peroxisome proliferator-activated receptor- α mediates the anti-inflammatory actions of palmitoylethanolamide. Molecular Pharmacology 2005 67 1 15 19 2-s2.0-11244328917 10.1124/mol.104.006353 (Pubitemid 40069962)
19. Daynes R. A., Jones D. C., Emerging roles of PPARs in inflammation and immunity. Nature Reviews Immunology 2002 2 10 748 759 2-s2.0-0036779687 10.1038/nri912 (Pubitemid 37328715)
20. LoVerme J., La Rana G., Russo R., Calignano A., Piomelli D., The search for the palmitoylethanolamide receptor. Life Sciences 2005 77 14 1685 1698 2-s2.0-23044438547 10.1016/j.lfs.2005.05.012 (Pubitemid 41073662)
21. Russo R., LoVerme J., La Rana G., Compton T. R., Parrott J., Duranti A., Tontini A., Mor M., Tarzia G., Calignano A., Piomelli D., The fatty acid amide hydrolase inhibitor URB597 (cyclohexylcarbamic acid 3′-carbamoylbiphenyl- 3-yl ester) reduces neuropathic pain after oral administration in mice. Journal of Pharmacology and Experimental Therapeutics 2007 322 1 236 242 2-s2.0-34250750792 10.1124/jpet.107.119941 (Pubitemid 46956375)
22. Kihara M., Zollman P. J., Schmelzer J. D., Low P. A., The influence of dose of microspheres on nerve blood flow, electrophysiology, and fiber degeneration of rat peripheral nerve. Muscle and Nerve 1993 16 12 1383 1389 2-s2.0-0027452053 10.1002/mus.880161218 (Pubitemid 23351092)
23. Attal N., Cruccu G., Baron R., Haanpää M., Hansson P., Jensen T. S., Nurmikko T., EFNS guidelines on the pharmacological treatment of neuropathic pain: 2010 revision. European Journal of Neurology 2010 17, article 1113-e88
24. Cui J. G., Holmin S., Mathiesen T., Meyerson B. A., Linderoth B., Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain 2000 88 3 239 248 2-s2.0-0034578946 10.1016/S0304-3959(00)00331-6
25. Kleinschnitz C., Brinkhoff J., Sommer C., Stoll G., Contralateral cytokine gene induction after peripheral nerve lesions: dependence on the mode of injury and NMDA receptor signaling. Molecular Brain Research 2005 136 1-2 23 28 2-s2.0-18944371012 10.1016/j.molbrainres.2004.12.015 (Pubitemid 40704605)
26. Kigerl K. A., Gensel J. C., Ankeny D. P., Alexander J. K., Donnelly D. J., Popovich P. G., Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. Journal of Neuroscience 2009 29 43 13435 13444 2-s2.0-70350558453 10.1523/JNEUROSCI.3257-09.2009
27. Ding A. H., Nathan C. F., Stuehr D. J., Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production. Journal of Immunology 1988 141 7 2407 2412 2-s2.0-0023706894
28. Willingale H. L., Gardiner N. J., McLymont N., Giblett S., Grubb B. D., Prostanoids synthesized by cyclo-oxygenase isoforms in rat spinal cord and their contribution to the development of neuronal hyperexcitability. British Journal of Pharmacology 1997 122 8 1593 1604 2-s2.0-0031463351 10.1038/sj.bjp.0701548 (Pubitemid 28000185)
29. Zhu X. Y., Huang C. S., Li Q., Chang R. M., Song Z. B., Zou W. Y., Guo Q. L., p300 exerts an epigenetic role in chronic neuropathic pain through its acetyltransferase activity in rats following chronic constriction injury (CCI). Molecular Pain 2012 8 84 10.1186/1744-8069-8-84
30. Lindenlaub T., Teuteberg P., Hartung T., Sommer C., Effects of neutralizing antibodies to TNF-alpha on pain-related behavior and nerve regeneration in mice with chronic constriction injury. Brain Research 2000 866 1-2 15 22 2-s2.0-0034595723 10.1016/S0006-8993(00)02190-9 (Pubitemid 30313003)
31. Mackie K., Stella N., Cannabinoid receptors and endocannabinoids: evidence for new players. The AAPS Journal 2006 8 E298 E306
32. Berdyshev E. V., Cannabinoid receptors and the regulation of immune response. Chem. Phys. Lipids 2000 108 169 190 10.1016/S0009-3084(00)00195-X
33. Glass C. K., Ogawa S., Combinatorial roles of nuclear receptors in inflammation and immunity. Nature Reviews Immunology 2006 6 44 55 10.1038/nri1748 (Pubitemid 43279752)
34. Straus D. S., Glass C. K., Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms. Trends in Immunology 2007 28 551 558 10.1016/j.it.2007.09.003 (Pubitemid 350101420)
35. Inoue H., Jiang X. F., Katayama T., Osada S., Umesono K., Namura S., Brain protection by resveratrol and fenofibrate against stroke requires peroxisome proliferator-activated receptor α in mice. Neuroscience Letters 2003 352 3 203 206 2-s2.0-1642268085 10.1016/j.neulet.2003.09.001 (Pubitemid 38367603)
36. Deplanque D., Gelé P., Pétrault O., Six I., Furman C., Bouly M., Nion S., Dupuis B., Leys D., Fruchart J. C., Cecchelli R., Staels B., Duriez P., Bordet R., Peroxisome proliferator-activated receptor- α activation as a mechanism of preventive neuroprotection induced by chronic fenofibrate treatment. Journal of Neuroscience 2003 23 15 6264 6271 2-s2.0-0038720453 (Pubitemid 36875628)
37. Genovese T., Esposito E., Mazzon E., Crisafulli C., Paterniti I., Di Paola R., Galuppo M., Bramanti P., Cuzzocrea S., PPAR- α modulate the anti-inflammatory effect of glucocorticoids in the secondary damage in experimental spinal cord trauma. Pharmacological Research 2009 59 5 338 350 2-s2.0-63549121184 10.1016/j.phrs.2009.01.018
38. Almad A., Lash A. T., Wei P., Lovett-Racke A. E., The PPAR alpha agonist gemfibrozil is an ineffective treatment for spinal cord injured mice. Experimental Neurology 2011 232 309 317
39. Skaper S. D., Buriani A., Dal Toso R., Petrelii L., Romanello S., Facci L., Leon A., The ALIAmide palmitoylethanolamide and cannabinoids, but not anandamide, are protective in a delayed postglutamate paradigm of excitotoxic death in cerebellar granule neurons. Proceedings of the National Academy of Sciences of the United States of America 1996 93 9 3984 3989 2-s2.0-0029870716 10.1073/pnas.93.9.3984 (Pubitemid 26146721)
40. Koch M., Kreutz S., Böttger C., Benz A., Maronde E., Ghadban C., Korf H. W., Dehghani F., Palmitoylethanolamide protects dentate gyrus granule cells via peroxisome proliferator-activated receptor-alpha. Neurotoxicity Research 2011 19 2 330 340 2-s2.0-79751535002 10.1007/s12640-010-9166-2
41. Esposito E., Impellizzeri D., Mazzon E., Paterniti I., Cuzzocrea S., Neuroprotective activities of Palmitoylethanolamide in an animal model of parkinson's disease. PLoS ONE 2012 7, article e41880 10.1371/journal.pone. 0041880
42. Scuderi C., Valenza M., Stecca C., Esposito G., Carratù M. R., Steardo L., Palmitoylethanolamide exerts neuroprotective effects in mixed neuroglial cultures and organotypic hippocampal slices via peroxisome proliferator-activated receptor-alpha. Journal of Neuroinflammation 2012 9m article 49
43. Woodhams P. L., MacDonald R. E., Collins S. D., Chessell I. P., Day N. C., Localisation and modulation of prostanoid receptors EP1 and EP4 in the rat chronic constriction injury model of neuropathic pain. European Journal of Pain 2007 11 6 605 613 2-s2.0-34249284127 10.1016/j.ejpain.2006.09.005 (Pubitemid 46818055)
44. Mannaerts G. P., Van Veldhoven P. P., Gibson G., Lake B., Metabolic role of mammalian peroxisomes. Proceedings of the Peroxisomes: Biology and Importance in Toxicology and Medicine 1993 London, UK Taylor & Francis 19 62
45. Wanders R. J., Waterham H. R., Peroxisomal disorders: the single peroxisomal enzyme deficiencies. 1763 Biochimica et Biophysica Acta 2006 1707 1720
46. Steinberg S., Dodt G., Raymond G. V., Braverman N. E., Moser A. B., Moser H. W., Peroxisome biogenesis disorders. Biochimica et Biophysica Acta 2006 1763 1733 1748 (Pubitemid 44880484)
47. Baes M., Aubourg P., Peroxisomes, myelination, and axonal integrity in the CNS. Neuroscientist 2009 15 367 379 10.1177/1073858409336297
48. Genovese T., Esposito E., Mazzon E., Di Paola R., Meli R., Bramanti P., Piomelli D., Calignano A., Cuzzocrea S., Effects of palmitoylethanolamide on signaling pathways implicated in the development of spinal cord injury. Journal of Pharmacology and Experimental Therapeutics 2008 326 1 12 23 2-s2.0-45749149121 10.1124/jpet.108.136903 (Pubitemid 351872139)