Cannabinoid CB1 receptors regulate neuronal TNF-α effects in experimental autoimmune encephalomyelitis

Brain, Behavior, and Immunity

Volumn 25, Issue 6, 2011, Pages 1242-1248

  Rossi, Silvia ^a,b   Furlan, Roberto ^c   Chiara, Valentina De ^a,b   Muzio, Luca ^c   Musella, Alessandra ^a,b   Motta, Caterina ^a,b   Studer, Valeria ^a,b   Cavasinni, Francesca ^a,b   Bernardi, Giorgio ^a,b   Martino, Gianvito ^c   Cravatt, Benjamin F ^d   Lutz, Beat ^e   Maccarrone, Mauro ^b,f   Centonze, Diego ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

^f UNIVERSITY OF TERAMO   (Italy)

Author keywords

Anandamide; EAE; EPSC; Excitotoxicity; FAAH; Neurodegeneration

Indexed keywords

ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; GLUTAMIC ACID; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEGENERATIVE DISEASE; DISEASE COURSE; DISEASE DURATION; DISEASE EXACERBATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; CORPUS STRIATUM; DIZOCILPINE MALEATE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENDOCANNABINOIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GLUTAMIC ACID; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; NEURONS; POLYUNSATURATED ALKAMIDES; RECEPTOR, CANNABINOID, CB1; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, TUMOR NECROSIS FACTOR; TETRAHYDROCANNABINOL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79960264824     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.03.017     Document Type: Article

References (63)

1. Arevalo-Martin A., 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., Di Marzo V. Endocannabinoids control spasticity in a multiple sclerosis model. FASEB J. 2001, 15:300-302.
3. Baraczka K., Pozsonyi T., Szüts I., Ormos G., Nékám K. Increased levels of tumor necrosis alpha and soluble vascular endothelial adhesion molecule-1 in the cerebrospinal fluid of patients with connective tissue diseases and multiple sclerosis. Acta Microbiol. Immunol. Hung. 2003, 50:339-348.
4. Bakshi R., Benedict R.H., Bermel R.A., Caruthers S.D., Puli S.R., Tjoa C.W., Fabiano A.J., Jacobs L. T2 hypointensity in the deep gray matter of patients with multiple sclerosis: a quantitative magnetic resonance imaging study. Arch. Neurol. 2002, 59:62-68.
5. Bermel R.A., Innus M.D., Tjoa C.W., Bakshi R. Selective caudate atrophy in multiple sclerosis: a 3D MRI parcellation study. Neuroreport 2003, 14:335-339.
6. Block M.L., Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76:77-98.
7. Bolton C., Paul C. MK-801 limits neurovascular dysfunction during experimental allergic encephalomyelitis. J. Pharmacol. Exp. Ther. 1997, 282:397-402.
8. Centonze D., Rossi S., Prosperetti C., Tscherter A., Bernardi G., Maccarrone M., Calabresi P. Abnormal sensitivity to cannabinoid receptor stimulation might contribute to altered gamma-aminobutyric acid transmission in the striatum of R6/2 Huntington's disease mice. Biol. Psychiatry 2005, 57:1583-1589.
9. Centonze D., Bari M., Rossi S., Prosperetti C., Furlan R., Fezza F., De Chiara V., Battistini L., Bernardi G., Bernardini S., Martino G., Maccarrone M. The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis. Brain 2007, 130:2543-2553.
10. Centonze D., Muzio L., Rossi S., Cavasinni F., De Chiara V., Bergami A., Musella A., D'Amelio M., Cavallucci V., Martorana A., Bergamaschi A., Cencioni M.T., Diamantini A., Butti E., Comi G., Bernardi G., Cecconi F., Battistini L., Furlan R., Martino G. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J. Neurosci. 2009, 29:3442-3452.
11. Chevaleyre V., Takahashi K.A., Castello P.E. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 2006, 29:37-76.
12. Cravatt B.F., Demarest K., Patricelli M.P., Bracey M.H., Giang D.K., Martin B.R., Lichtman A.H. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. USA 2001, 98:9371-9376.
13. 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.
14. Croxford J.L., Pryce G., Jackson S.J., Ledent C., Giovannoni G., Pertwee R.G., Yamamura T., Baker D. Cannabinoid-mediated neuroprotection, not immunosuppression, may be more relevant to multiple sclerosis. J. Neuroimmunol. 2008, 193:120-129.
15. Cumiskey D., Curran B.P., Herron C.E., O'Connor J.J. A role for inflammatory mediators in the IL-18 mediated attenuation of LTP in the rat dentate gyrus. Neuropharmacology 2007, 52:1616-1623.
16. Devane W.A., Dysarz F.A., Johnson M., Melvin L.S., Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 1988, 34:605-613.
17. Eljaschewitsch E., Witting A., Mawrin C., Lee T., Schmidt P.M., Wolf S., Hoertnagl H., Raine C.S., Schneider-Stock R., Nitsch R., Ullrich O. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 2006, 49:67-79.
18. Fernandez-Ruiz J., Pazos M.R., Garci{dotless}a-Arencibia M., Sagredo O., Ramos J.A. Role of CB2 receptors in neuroprotective effects of cannabinoids. Mol. Cell. Endocrinol. 2008, 286:91-96.
19. Gerdeman G., Lovinger D.M. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 2001, 85:468-471.
20. Grundy R.I., Rabuffetti M., Beltramo M. Cannabinoids and neuroprotection. Mol. Neurobiol. 2001, 24:29-51.
21. Harkany T., Mackie K., Doherty P. Wiring and firing neuronal networks: endocannabinoids take center stage. Curr. Opin. Neurobiol. 2008, 18:338-345.
22. Howlett A.C., Bidaut-Russell M., Devane W.A., Melvin L.S., Johnson M.R., Herkenham M. The cannabinoid receptor: biochemical, anatomical and behavioral characterization. Trends Neurosci. 1990, 13:420-423.
23. Huang C.C., Lo S.W., Hsu K.S. Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J. Physiol. 2001, 532:731-748.
24. Jean-Gilles L., Feng S., Tench C.R., Chapman V., Kendall D.A., Barrett D.A., Constantinescu C.S. Plasma endocannabinoid levels in multiple sclerosis. J. Neurol. Sci. 2009, 287:212-215.
25. Kawanokuchi J., Mizuno T., Takeuchi H., Kato H., Wang J., Mitsuma N., Suzumura A. Production of interferon-gamma by microglia. Mult. Scler. 2006, 12:558-564.
26. Khademi M., Wallström E., Andersson M., Piehl F., Di Marco R., Olsson T. Reduction of both pro- and anti-inflammatory cytokines after 6 months of interferon beta-1a treatment of multiple sclerosis. J. Neuroimmunol. 2000, 103:202-210.
27. Lai A.Y., Swayze R.D., El-Husseini A., Song C. Interleukin-1 beta modulates AMPA receptor expression and phosphorylation in hippocampal neurons. J. Neuroimmunol. 2006, 175:97-106.
28. Lovinger D.M. Presynaptic modulation by endocannabinoids. Handb. Exp. Pharmacol. 2008, 184:435-477.
29. Lyman W.D., Sonett J.R., Brosnan C.F., Elkin R., Bornstein M.B. Delta 9-tetrahydrocannabinol: a novel treatment for experimental autoimmune encephalomyelitis. J. Neuroimmunol. 1989, 23:73-81.
30. Maccarrone M., Rossi S., Bari M., De Chiara V., Fezza F., Musella A., Gasperi V., Prosperetti C., Bernardi G., Finazzi-Agrò A., Cravatt B.F., Centonze D. Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum. Nat. Neurosci. 2008, 11:152-1529.
31. Maresz K., Pryce G., Ponomarev E.D., Marsicano G., Croxford J.L., Shriver L.P., et al. 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.
32. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., Hermann H., Tang J., Hofmann C., Zieglgänsberger W., Di Marzo V., Lutz B. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002, 418:530-534.
33. Marsicano G., Goodenough S., Monory K., Hermann H., Eder M., Cannich A., Azad S.C., Cascio M.G., Gutiérrez S.O., van der Stelt M., López-Rodriguez M.L., Casanova E., Schütz G., Zieglgänsberger W., Di Marzo V., Behl C., Lutz B. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 2003, 302:84-88.
34. Matute C., Alberdi E., Domercq M., Pérez-Cerdá F., Pérez-Samartín A., Sánchez-Gómez M.V. The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci. 2001, 24:224-230.
35. Mestre L., Correa F., Arevalo-Martin 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.
36. Mestre L., Docagne F., Correa F., Loría F., Hernangómez 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.
37. Mizuno T., Zhang G., Takeuchi H., Kawanokuchi J., Wang J., Sonobe Y., Jin S., Takada N., Komatsu Y., Suzumura A. Interferon-gamma directly induces neurotoxicity through a neuron specific, calcium-permeable complex of IFN-gamma receptor and AMPA GluR1 receptor. FASEB J. 2008, 22:1797-1806.
38. Monory K., Massa F., Egertová M., Eder M., Blaudzun H., Westenbroek R., Kelsch W., Jacob W., Marsch R., Ekker M., Long J., Rubenstein J.L., Goebbels S., Nave K.A., During M., Klugmann M., Wölfel B., Dodt H.U., Zieglgänsberger W., Wotjak C.T., Mackie K., Elphick M.R., Marsicano G., Lutz B. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 2006, 51:455-466.
39. Murphy A.C., Lalor S.J., Lynch M.A., Mills K.H. Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis. Brain Behav. Immun. 2010, 24:641-651.
40. Muzio L., Martino G., Furlan R. Multifaceted aspects of inflammation in multiple sclerosis: The role of microglia. J. Neuroimmunol. 2007, 191:39-44.
41. Ortega-Gutierrez S., Molina-Holgado E., Arevalo-Martin A., Correa F., Viso A., Lopez-Rodriguez M.L., Di Marzo V., Guaza C. Activation of the endocannabinoid system as a therapeutic approach in a murine model of multiple sclerosis. FASEB J. 2005, 19:1338-1343.
42. Palazuelos J., Davoust N., Julien B., Hatterer E., Aguado T., Mechoulam R., Benito C., Romero J., Silva A., Guzman M., Nataf S., Glave-Roperh I. The CB2 cannabinoid receptor controls myeloid progenitor trafficking. Involvement in the pathogenesis of an animal model of multiple sclerosis. J. Biol. Chem. 2008, 283:13320-13329.
43. Piomelli D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 2003, 4:873-884.
44. Pitt D., Werner P., Raine C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 2000, 6:67-70.
45. Pryce G., Ahmed Z., Hankey D.J., Jackson S.J., Croxford J.L., Pocock J.M., Ledent C., Petzold A., Thompson A.J., Giovannoni G., Cuzner M.L., Baker D. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 2003, 126:2191-2202.
46. Rossi S., Furlan R., De Chiara V., Musella A., Lo Giudice T., Mataluni G., Cavasinni F., Cantarella C., Bernardi G., Muzio L., Martorana A., Martino G., Centonze D. Exercise attenuates the clinical, synaptic and dendritic abnormalities of experimental autoimmune encephalomyelitis. Neurobiol. Dis. 2009, 36:51-59.
47. Rossi S., Bernardi G., Centonze D. The endocannabinoid system in the inflammatory and neurodegenerative processes of multiple sclerosis and of amyotrophic lateral sclerosis. Exp. Neurol. 2010, 224:92-102.
48. Rossi S., De Chiara V., Furlan R., Musella A., Cavasinni F., Muzio L., Bernardi G., Martino G., Centonze D. Abnormal activity of the Na/Ca exchanger enhances glutamate transmission in experimental autoimmune encephalomyelitis. Brain Behav. Immun. 2010, 24:1379-1385.
49. Rossi S., Buttari F., Studer V., Motta C., Gravina P., Castelli M., Mantovani V., De Chiara V., Musella A., Fiore S., Masini S., Bernardi G., Maccarrone M., Bernardini S., Centonze D. The (AAT)n repeat of the cannabinoid CB1 receptor gene influences disease progression in relapsing multiple sclerosis. Mult. Scler. 2011, 17:281-288.
50. Rovaris M., Barnes D., Woodrofe N., du Boulay G.H., Thorpe J.W., Thompson A.J., McDonald W.I., Miller D.H. Patterns of disease activity in multiple sclerosis patients: a study with quantitative gadoliniumenhanced brain MRI and cytokine measurement in different clinical subgroups. J. Neurol. 1996, 243:536-542.
51. Schwartz M., Butovsky O., Brück W., Hanisch U.K. Microglial phenotype: is the commitment reversible?. Trends Neurosci. 2006, 29:68-74.
52. Smith T., Groom A., Zhu B., Turski L. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat. Med. 2000, 6:62-66.
53. Srinivasan R., Sailasuta N., Hurd R., Nelson S., Pelletier D. Evidence of elevated glutamate in multiple sclerosis using magnetic resonance spectroscopy at 3 T. Brain 2005, 128:1016-1025.
54. Stellwagen D., Beattie E.C., Seo J.Y., Malenka R.C. Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J. Neurosci. 2005, 25:3219-3228.
55. Stellwagen D., Malenka R.C. Synaptic scaling mediated by glial TNF-alpha. Nature 2006, 440:1054-1059.
56. Tao G., Datta S., He R., Nelson F., Wolinsky J.S., Narayana P.A. Deep gray matter atrophy in multiple sclerosis: a tensor based morphometry. J. Neurol. Sci. 2009, 282:39-46.
57. Vercellino M., Merola A., Piacentino C., Votta B., Capello E., Mancardi G.L., Mutani R., Giordana M.T., Cavalla P. Altered glutamate reuptake in relapsing-remitting and secondary progressive multiple sclerosis cortex: correlation with microglia infiltration, demyelination, and neuronal and synaptic damage. J. Neuropathol. Exp. Neurol. 2007, 66:732-739.
58. Wallström E., Diener P., Ljungdahl A., Khademi M., Nilsson C.G., Olsson T. Memantine abrogates neurological deficits, but not CNS inflammation, in Lewis rat experimental autoimmune encephalomyelitis. J. Neurol. Sci. 1996, 137:89-96.
59. Walter L., Stella N. Cannabinoids and neuroinflammation. Br. J. Pharmacol. 2004, 141:775-785.
60. Webb M., Luo L., Ma J.Y., Tham C.S. Genetic deletion of fatty acid amide hydrolase results in improved long-term outcome in chronic autoimmune encephalitis. Neurosci. Lett. 2008, 439:106-110.
61. Wirguin I., Mechoulam R., Breuer A., Schezen E., Weidenfeld J., Brenner T. Suppression of experimental autoimmune encephalomyelitis by cannabinoids. Immunopharmacology 1994, 28:209-214.
62. Zhang M., Martin B.R., Adler M.W., Razdan R.J., Kong W., Ganea D., Tuma R.F. Modulation of cannabinoid receptor activation as a neuroprotective strategy for EAE and stroke. J. Neuroimmune Pharmacol. 2009, 4:249-259.
63. Zhao P., Leonoudakis D., Abood M.E., Beattie E.C. Cannabinoid receptor activation reduces TNFalpha-Induced surface localization of AMPAR-type glutamate receptors and excitotoxicity. Neuropharmacology 2010, 58:551-558.