Interaction between the protective effects of cannabidiol and palmitoylethanolamide in experimental model of multiple sclerosis in C57BL/6 mice

Neuroscience

Volumn 290, Issue , 2015, Pages 279-287

  Rahimi, A ^a   Faizi, M ^a   Talebi, F ^b   Noorbakhsh, F ^c   Kahrizi, F ^a   Naderi, N ^a  

^a SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b Khatam Al Anbia Hospital   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Cannabidiol; Cannabinoid; EAE; Multiple sclerosis; Palmitoylethanolamide

Indexed keywords

CANNABIDIOL; GAMMA INTERFERON; INTERLEUKIN 17; PALMIDROL; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT; ETHANOLAMINE DERIVATIVE; PALMITIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CELL INFILTRATION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DRUG ANTAGONISM; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; EXPERIMENTAL MODEL; FEMALE; HISTOCHEMISTRY; IMMUNOCOMPETENT CELL; MONOTHERAPY; MOUSE; MULTIPLE SCLEROSIS; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; C57BL MOUSE; DRUG COMBINATION; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOMODULATION; MACROPHAGE; METABOLISM; MICROGLIA; MYELIN SHEATH; NERVE FIBER; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX; SPINAL CORD; TREATMENT OUTCOME;

ANIMALS; ANTI-INFLAMMATORY AGENTS; AXONS; CANNABIDIOL; DRUG THERAPY, COMBINATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ETHANOLAMINES; FEMALE; INTERFERON-GAMMA; INTERLEUKIN-17; MACROPHAGES; MICE, INBRED C57BL; MICROGLIA; MYELIN SHEATH; NEUROIMMUNOMODULATION; PALMITIC ACIDS; SEVERITY OF ILLNESS INDEX; SPINAL CORD; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84922638941     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.01.030     Document Type: Article

References (70)

1. Arévalo-Martín Á., Vela J.M., Molina-Holgado E., Borrell J., Guaza C. Therapeutic action of cannabinoids in a murine model of multiple sclerosis. J Neurosci 2003, 23:2511-2516.
2. Baker D., Pryce G., Croxford J.L., Brown P., Pertwee R.G., Makriyannis A., Khanolkar A., Layward L., Fezza F., Bisogno T. Endocannabinoids control spasticity in a multiple sclerosis model. FASEB J 2001, 15:300-302.
3. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238.
4. Bisogno T., Hanuš L., De Petrocellis L., Tchilibon S., Ponde D.E., Brandi I., Moriello A.S., Davis J.B., Mechoulam R., Di Marzo V. Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br J Pharmacol 2001, 134:845-852.
5. Bonica J. The need of a taxonomy. Pain 1979, 6:247-248.
6. Buccellato E., Carretta D., Utan A., Cavina C., Speroni E., Grassi G., Candeletti S., Romualdi P. Acute and chronic cannabinoid extracts administration affects motor function in a CREAE model of multiple sclerosis. J Ethnopharmacol 2011, 133:1033-1038.
7. 2 and TNFα release from canine skin mast cells. Vet Immunol Immunopathol 2010, 133:9-15.
8. Collin C., Davies P., Mutiboko I., Ratcliffe S. Randomized controlled trial of cannabis-based medicine in spasticity caused by multiple sclerosis. Eur J Neurol 2007, 14:290-296.
9. 1, TRPV1 and PPARγ receptors and neurotrophic factors. Pain 2008, 139:541-550.
10. Croxford J.L., Miller S.D. Immunoregulation of a viral model of multiple sclerosis using the synthetic cannabinoid R (+) WIN55, 212. J Clin Invest 2003, 111:1231-1240.
11. D'Agostino G., La Rana G., Russo R., Sasso O., Iacono A., Esposito E., Mattace Raso G., Cuzzocrea S., LoVerme J., Piomelli D. Central administration of palmitoylethanolamide reduces hyperalgesia in mice via inhibition of NF-κB nuclear signalling in dorsal root ganglia. Eur J Pharmacol 2009, 613:54-59.
12. De Petrocellis L., Davis J.B., Di Marzo V. Palmitoylethanolamide enhances anandamide stimulation of human vanilloid VR1 receptors. FEBS Lett 2001, 506:253-256.
13. Di Cesare Mannelli L., D'Agostino G., Pacini A., Russo R., Zanardelli M., Ghelardini C., Calignano A. Palmitoylethanolamide is a disease-modifying agent in peripheral neuropathy: pain relief and neuroprotection share a PPAR-alpha-mediated mechanism. Mediators Inflamm 2013, 2013:1-12. Article ID: 328797. 10.1155/2013/328797.
14. Docagne F., Muñetón V., Clemente D., Ali C., Loría F., Correa F., Hernangómez M., Mestre L., Vivien D., Guaza C. Excitotoxicity in a chronic model of multiple sclerosis: neuroprotective effects of cannabinoids through CB1 and CB2 receptor activation. Mol Cell Neurosci 2007, 34:551-561.
15. El-behi M., Rostami A., Ciric B. Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol 2010, 5:189-197.
16. Esposito G., Capoccia E., Turco F., Palumbo I., Lu J., Steardo A., Cuomo R., Sarnelli G., Steardo L. Palmitoylethanolamide improves colon inflammation through an enteric glia/toll like receptor 4-dependent PPAR-α activation. Gut 2013, 10.1136/gutjnl-2013-305005.
17. Franklin A., Parmentier-Batteur S., Walter L., Greenberg D.A., Stella N. Palmitoylethanolamide increases after focal cerebral ischemia and potentiates microglial cell motility. J Neurosci 2003, 23:7767-7775.
18. Guan L.-P., Sui X., Deng X.-Q., Zhao D.-H., Qu Y.-L., Quan Z.-S. N-palmitoylethanolamide derivatives: synthesis and studies on anticonvulsant and antidepressant activities. Med Chem Res 2011, 20:601-606.
19. Hammarberg H., Lidman O., Lundberg C., Eltayeb S., Gielen A., Muhallab S., Svenningsson A., Lindå H., van Der Meide P., Cullheim S. Neuroprotection by encephalomyelitis: rescue of mechanically injured neurons and neurotrophin production by CNS-infiltrating T and natural killer cells. J Neurosci 2000, 20:5283-5291.
20. Hampson A., Grimaldi M., Axelrod J., Wink D. Cannabidiol and (-) δ9-tetrahydrocannabinol are neuroprotective antioxidants. Proc Natl Acad Sci 1998, 95:8268-8273.
21. Harvey B.S., Ohlsson K.S., Mååg J.L., Musgrave I.F., Smid S.D. Contrasting protective effects of cannabinoids against oxidative stress and amyloid-β evoked neurotoxicity in vitro. NeuroToxicology 2012, 33:138-146.
22. Hesselink J.M.K. New targets in pain, non-neuronal cells, and the role of palmitoylethanolamide. Open Pain J 2012, 5.
23. Izzo A.A., Borrelli F., Capasso R., Di Marzo V., Mechoulam R. Non-psychotropic plant cannabinoids: new therapeutic opportunities from an ancient herb. Trends Pharmacol Sci 2009, 30:515-527.
24. Jin W., Dong C. IL-17 cytokines in immunity and inflammation. Emerg Microbes Infect 2013, 2:e60.
25. Kafami L., Etesami I., Felfeli M., Enayati N., Ghiaghi R., Aminian A., Dehpour A. Methadone diminishes neuroinflammation and disease severity in EAE through modulating T cell function. J Neuroimmunol 2013, 255:39-44.
26. Kim B.S., Jin Y.-H., Meng L., Hou W., Kang H.S., Park H.S., Koh C.-S. IL-1 signal affects both protection and pathogenesis of virus-induced chronic CNS demyelinating disease. J Neuroinflamm 2012, 9:1-13.
27. Komiyama Y., Nakae S., Matsuki T., Nambu A., Ishigame H., Kakuta S., Sudo K., Iwakura Y. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol 2006, 177:566-573.
28. Kozela E., Lev N., Kaushansky N., Eilam R., Rimmerman N., Levy R., Ben-Nun A., Juknat A., Vogel Z. Cannabidiol inhibits pathogenic T cells, decreases spinal microglial activation and ameliorates multiple sclerosis-like disease in C57BL/6 mice. Br J Pharmacol 2011, 163:1507-1519.
29. Lambert D.M., Di Marzo V. The palmitoylethanolamide and oleamide enigmas two fatty acid amides cannabimimetic?. Curr Med Chem 1999, 6:757-773.
30. Lambert D.M., DiPaolo F.G., Sonveaux P., Kanyonyo M., Govaerts S.J., Hermans E., Bueb J.-L., Delzenne N.M., Tschirhart E.J. Analogues and homologues of N-palmitoylethanolamide, a putative endogenous CB2 cannabinoid, as potential ligands for the cannabinoid receptors. Biochim Biophys Acta (BBA) Mol Cell Biol Lipids 1999, 1440:266-274.
31. 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, 42:321-327.
32. Lastres-Becker I., Molina-Holgado F., Ramos J.A., Mechoulam R., Fernández-Ruiz J. Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson's disease. Neurobiol Dis 2005, 19:96-107.
33. Lauckner J.E., Jensen J.B., Chen H.-Y., Lu H.-C., Hille B., Mackie K. GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proc Natl Acad Sci 2008, 105:2699-2704.
34. Lee C.-Y., Wey S.-P., Liao M.-H., Hsu W.-L., Wu H.-Y., Jan T.-R. A comparative study on cannabidiol-induced apoptosis in murine thymocytes and EL-4 thymoma cells. Int Immunopharmacol 2008, 8:732-740.
35. Liou G.I., Auchampach J.A., Hillard C.J., Zhu G., Yousufzai B., Mian S., Khan S., Khalifa Y. Mediation of cannabidiol anti-inflammation in the retina by equilibrative nucleoside transporter and A2A adenosine receptor. Invest Ophthalmol Vis Sci 2008, 49:5526-5531.
36. Loría F., Petrosino S., Mestre L., Spagnolo A., Correa F., Hernangómez M., Guaza C., Di Marzo V., Docagne F. Study of the regulation of the endocannabinoid system in a virus model of multiple sclerosis reveals a therapeutic effect of palmitoylethanolamide. Eur J Neurosci 2008, 28:633-641.
37. Malfait A., Gallily R., Sumariwalla P., Malik A., Andreakos E., Mechoulam R., Feldmann M. The nonpsychoactive cannabis constituent cannabidiol is an oral anti-arthritic therapeutic in murine collagen-induced arthritis. Proc Natl Acad Sci 2000, 97:9561-9566.
38. Maresz K., Pryce G., Ponomarev E.D., Marsicano G., Croxford J.L., Shriver L.P., Ledent C., Cheng X., Carrier E.J., Mann M.K. Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells. Nat Med 2007, 13:492-497.
39. Mestre L., Correa F., Arévalo-Martín A., Molina-Holgado E., Valenti M., Ortar G., Di Marzo V., Guaza C. Pharmacological modulation of the endocannabinoid system in a viral model of multiple sclerosis. J Neurochem 2005, 92:1327-1339.
40. Mestre L., Docagne F., Correa F., Loría F., Hernangomez M., Borrell J., Guaza C. A cannabinoid agonist interferes with the progression of a chronic model of multiple sclerosis by downregulating adhesion molecules. Mol Cell Neurosci 2009, 40:258-266.
41. Miller D., Weinshenker B., Filippi M., Banwell B., Cohen J., Freedman M., Galetta S., Hutchinson M., Johnson R., Kappos L. Differential diagnosis of suspected multiple sclerosis: a consensus approach. Mult Scler 2008, 14:1157-1174.
42. Mozafari S., Javan M., Sherafat M.A., Mirnajafi-Zadeh J., Heibatollahi M., Pour-Beiranvand S., Tiraihi T., Ahmadiani A. Analysis of structural and molecular events associated with adult rat optic chiasm and nerves demyelination and remyelination; possible role for 3rd ventricle proliferating cells. NeuroMol Med 2011, 13:138-150.
43. Naderi N., Majidi M., Mousavi Z., Tusi S.K., Mansouri Z., Khodagholi F. The interaction between intrathecal administration of low doses of palmitoylethanolamide and AM251 in formalin-induced pain related behavior and spinal cord IL1-β expression in rats. Neurochem Res 2012, 37:778-785.
44. Ni X., Geller E.B., Eppihimer M.J., Eisenstein T.K., Adler M.W., Tuma R.F. Win 55212-2, a cannabinoid receptor agonist, attenuates leukocyte/endothelial interactions in an experimental autoimmune encephalomyelitis model. Mult Scler 2004, 10:158-164.
45. Oh S.-s., Kim D., Kim D.-H., Chang H.H., Sohn K.-C., Kim K.H., Jung S.H., Lee B.K., Kim J.H., Kim K.D. NDRG2 correlated with favorable recurrence-free survival inhibits metastasis of mouse breast cancer cells via attenuation of active TGF-β production. Carcinogenesis 2012, 33:1882-1888.
46. Oka S., Kimura S., Toshida T., Ota R., Yamashita A., Sugiura T. Lysophosphatidylinositol induces rapid phosphorylation of p38 mitogen-activated protein kinase and activating transcription factor 2 in HEK293 cells expressing GPR55 and IM-9 lymphoblastoid cells. J Biochem 2010, 147:671-678.
47. Paterniti I., Impellizzeri D., Di Paola R., Navarra M., Cuzzocrea S., Esposito E. A new co-ultramicronized composite including palmitoylethanolamide and luteolin to prevent neuroinflammation in spinal cord injury. J Neuroinflamm 2013, 10:91.
48. Pertwee R. The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: δ9-tetrahydrocannabinol, cannabidiol and δ9-tetrahydrocannabivarin. Br J Pharmacol 2008, 153:199-215.
49. Pertwee R.G. The pharmacology and therapeutic potential of cannabidiol. Cannabinoids 2004, 32-83. Kluwer Academic/Plenum Publishers.
50. Pomeroy I.M., Matthews P.M., Frank J.A., Jordan E.K., Esiri M.M. Demyelinated neocortical lesions in marmoset autoimmune encephalomyelitis mimic those in multiple sclerosis. Brain 2005, 128:2713-2721.
51. Power C., Henry S., Del Bigio M.R., Larsen P.H., Corbett D., Imai Y., Yong V.W., Peeling J. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol 2003, 53:731-742.
52. Prat A., Antel J. Pathogenesis of multiple sclerosis. Curr Opin Neurol 2005, 18:225-230.
53. Renno T., Krakowski M., Piccirillo C., Lin J., Owens T. TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines. J Immunol 1995, 154:944-953.
54. Rieder S.A., Chauhan A., Singh U., Nagarkatti M., Nagarkatti P. Cannabinoid-induced apoptosis in immune cells as a pathway to immunosuppression. Immunobiology 2010, 215:598-605.
55. Rog D.J., Nurmikko T.J., Friede T., Young C.A. Randomized, controlled trial of cannabis-based medicine in central pain in multiple sclerosis. Neurology 2005, 65:812-819.
56. 9-tetrahydrocannabinol/cannabidiol for neuropathic pain associated with multiple sclerosis: An uncontrolled, open-label, 2-year extension trial. Clin Ther 2007, 29:2068-2079.
57. Ryberg E., Larsson N., Sjögren S., Hjorth S., Hermansson N.O., Leonova J., Elebring T., Nilsson K., Drmota T., Greasley P. The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 2007, 152:1092-1101.
58. 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-α. J Neuroinflamm 2012, 9:131.
59. Seehusen F., Baumgärtner W. Axonal pathology and loss precede demyelination and accompany chronic lesions in a spontaneously occurring animal model of multiple sclerosis. Brain Pathol 2010, 20:551-559.
60. Sherafat M.A., Javan M., Mozafari S., Mirnajafi-Zadeh J., Motamedi F. Castration attenuates myelin repair following lysolecithin induced demyelination in rat optic chiasm: an evaluation using visual evoked potential, marker genes expression and myelin staining. Neurochem Res 2011, 36:1887-1895.
61. Smart D., Jonsson K.O., Vandevoorde S., Lambert D.M., Fowler C.J. 'Entourage' effects of N-acyl ethanolamines at human vanilloid receptors. Comparison of effects upon anandamide-induced vanilloid receptor activation and upon anandamide metabolism. Br J Pharmacol 2002, 136:452-458.
62. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005, 23:683-747.
63. 9 tetrahydrocannabinol and cannabidiol alter cytokine production by human immune cells. Immunopharmacology 1998, 40:179-185.
64. 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. The putative cannabinoid receptor GPR55 plays a role in mechanical hyperalgesia associated with inflammatory and neuropathic pain. Pain 2008, 139:225-236.
65. Steinman L., Martin R., Bernard C., Conlon P., Oksenberg J.R. Multiple sclerosis: deeper understanding of its pathogenesis reveals new targets for therapy. Annu Rev Neurosci 2002, 25:491-505.
66. Tsutsui S., Noorbakhsh F., Sullivan A., Henderson A.J., Warren K., Toney-Earley K., Waltz S.E., Power C. RON-regulated innate immunity is protective in an animal model of multiple sclerosis. Ann Neurol 2005, 57:883-895.
67. Tsutsui S., Schnermann J., Noorbakhsh F., Henry S., Yong V.W., Winston B.W., Warren K., Power C. A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J Neurosci 2004, 24:1521-1529.
68. Verme J.L., 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. Mol Pharmacol 2005, 67:15-19.
69. Watanabe K., Kayano Y., Matsunaga T., Yamamoto I., Yoshimura H. Inhibition of anandamide amidase activity in mouse brain microsomes by cannabinoids. Biol Pharmaceut Bull 1996, 19:1109-1111.
70. Zajicek J., Fox P., Sanders H., Wright D., Vickery J., Nunn A., Thompson A. Cannabinoids for treatment of spasticity and other symptoms related to multiple sclerosis (CAMS study): multicentre randomised placebo-controlled trial. Lancet 2003, 362:1517-1526.