Transient receptor potential vanilloid 1 channels modulate the synaptic effects of TNF-α and of IL-1β in experimental autoimmune encephalomyelitis

Neurobiology of Disease

Volumn 43, Issue 3, 2011, Pages 669-677

  Musumeci, Gabriele ^a,b   Grasselli, Giorgio ^a,b   Rossi, Silvia ^a,b   De Chiara, Valentina ^a,b   Musella, Alessandra ^a,b   Motta, Caterina ^a,b   Studer, Valeria ^a,b   Bernardi, Giorgio ^a,b   Haji, Nabila ^b,d   Sepman, Helena ^a,b   Fresegna, Diego ^b   Maccarrone, Mauro ^b,c   Mandolesi, Georgia ^a,b   Centonze, Diego ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF TERAMO   (Italy)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

EAE; EPSCs; IPSCs; Multiple sclerosis; Neuroprotection; Striatum; TRPV1

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; VANILLOID RECEPTOR 1;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHRONICITY; CONTROLLED STUDY; DISEASE MODEL; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC TRANSMISSION; GLUTAMATE TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; KNOCKOUT MOUSE; MOTOR DYSFUNCTION; MOUSE; MULTIPLE SCLEROSIS; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; SYNAPSE;

ANIMALS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; INFLAMMATION; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERLEUKIN-1BETA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; SYNAPSES; TRPV CATION CHANNELS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 79960207611     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.05.018     Document Type: Article

References (56)

1. Alawi K., Keeble J. The paradoxical role of the transient receptor potential vanilloid 1 receptor in inflammation. Pharmacol. Ther. 2010, 125:181-195.
2. 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.
3. Bánvölgyi A., Pálinkás L., Berki R., Clark N., Grant A.D., Helyes Z., Pozsgai G., Szolcsányi J., Brain S.D., Pintér E. Evidence for a novel protective role of the vanilloid TRPV1 receptor in a cutaneous contact allergic dermatitis model. J. Neuroimmunol. 2005, 169:86-96.
4. Bánvölgyi A., Pozsgai G., Brain S.D., Helyes Z.S., Szolcsányi J., Ghosh M., Melegh B., Pintér E. Mustard oil induces a transient receptor potential vanilloid 1 receptor-independent neurogenic inflammation and a non-neurogenic cellular inflammatory component in mice. Neuroscience 2004, 125:449-459.
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. Bhat R., Axtell R., Mitra A., Miranda M., Lock C., Tsien R.W., Steinman L. Inhibitory role for GABA in autoimmune inflammation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2580-2585.
7. Bhave G., Zhu W., Wang H., Brasier D.J., Oxford G.S., Gereau R.W. cAMPdependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 2002, 35:721-731.
8. Bolton C., Paul C. MK-801 limits neurovascular dysfunction during experimental allergic encephalomyelitis. J. Pharmacol. Exp. Ther. 1997, 282:397-402.
9. Brain S.D., Williams T.J., Tippins J.R., Morris H.R., MacIntyre I. Calcitonin gene-related peptide is a potent vasodilator. Nature 1985, 313:54-56.
10. Cao T., Pintér E., Al-Rashed S., Gerard N., Hoult J.R., Brain S.D. Neurokinin-1 receptor agonists are involved in mediating neutrophil accumulation in the inflamed, but not normal, cutaneous microvasculature: an in vivo study using neurokinin-1 receptor knockout mice. J. Immunol. 2000, 164:5424-5429.
11. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288:306-313.
12. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
13. 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.
14. Centonze D., Muzio L., Rossi S., Furlan R., Bernardi G., Martino G. The link between inflammation, synaptic transmission and neurodegeneration in multiple sclerosis. Cell Death Differ. 2010, 17:1083-1091.
15. Clark N., Keeble J., Fernandes E.S., Starr A., Liang L., Sudgen D., de Winter P., Brain S.D. The transient receptor potential vanilloid 1 (TRPV1) receptor protects against the onset of sepsis after endotoxin. FASEB J. 2007, 21:3747-3755.
16. Costa S.K., Starr A., Hyslop S., Gilmore D., Brain S.D. How important are NK1 receptors for influencing microvascular inflammation and itch in the skin? Studies using Phoneutria nigriventer venom. Vascul. Pharmacol. 2006, 45:209-214.
17. Engler A., Aeschlimann A., Simmen B.R., Michel B.A., Gay R.E., Gay S., Sprott H. Expression of transient receptor potential vanilloid 1 (TRPV1) in synovial fibroblasts from patients with osteoarthritis and rheumatoid arthritis. Biochem. Biophys. Res. Commun. 2007, 359:884-888.
18. Ghilardi J.R., Rohrich H., Lindsay T.H., Sevick M.A., Schwei M.J., Kubota K., Halvorson K.G., Poblete J., Chaplan S.R., Dubin A.E., Carruthers N.I., Swanson D., Kuskowski M., Flores C.M., Julius D., Mantyh P.W. Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain. J. Neurosci. 2005, 25:3126-3131.
19. Gibson H.E., Edwards J.G., Page R.S., Van Hook M.J., Kauer J.A. TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 2008, 57:746-759.
20. Goswami C., Rademacher N., Smalla K.H., Kalscheuer V., Ropers H.H., Gundelfinger E.D., Hucho T. TRPV1 acts as a synaptic protein and regulates vesicle recycling. J. Cell Sci. 2010, 123:2045-2057.
21. Helyes Z., Pintér E., Nemeth J., Szolcsányi J. Pharmacological targets for the inhibition of neurogenic inflammation. Curr. Med. Chem. 2003, 2:191-218.
22. Hudson L.J., Bevan S., Wotherspoon G., Gentry C., Fox A., Winter J. VR1 protein expression increases in undamaged DRG neurons after partial nerve injury. Eur. J. Neurosci. 2001, 13:2105-2114.
23. Kauer J.A., Gibson H.E. Hot flash: TRPV channels in the brain. Trends Neurosci. 2009, 32:215-224.
24. Keeble J., Russell F., Curtis B., Starr A., Pintér E., Brain S.D. Involvement of transient receptor potential vanilloid 1 in the vascular and hyperalgesic components of joint inflammation. Arthritis Rheum. 2005, 52:3248-3256.
25. Kawaguchi Y., Wilson C.J., Augood S.J., Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 1995, 18:527-535.
26. Lembeck F., Holzer P. Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn Schmiedebergs Arch. Pharmacol. 1979, 310:175-183.
27. Liu B., Zhang C., Qin F. Functional recovery from desensitization of vanilloid receptor TRPV1 requires resynthesis of phosphatidylinositol 4,5-biphosphate. J. Neurosci. 2005, 25:4835-4843.
28. 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, 11:152-159.
29. Massa F., Sibaev A., Mariscano G., Blaudzun H., Storr M., Lutz B. Vanilloid receptor (TRPV1)-deficient mice show increased susceptibility to dinitrobenzene sulphonic acid induced colitis. J. Mol. Med. 2006, 84:142-146.
30. 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.
31. Mohapatra D.P., Nau C. Desensitization of capsaicin-activated currents in the vanilloid receptor TRPV1 is decreased by the cyclic AMP-dependent protein kinase pathway. J. Biol. Chem. 2003, 278:50080-50090.
32. Musella A., De Chiara V., Rossi S., Cavasinni F., Castelli M., Cantarella C., Mataluni G., Bernardi G., Centonze D. Transient receptor potential vanilloid 1 channels control acetylcholine/2-arachidonoylglicerol coupling in the striatum. Neuroscience 2010, 167:864-871.
33. Musella A., De Chiara V., Rossi S., Prosperetti C., Bernardi G., Maccarrone M., Centonze D. TRPV1 channels facilitate glutamate transmission in the striatum. Mol. Cell. Neurosci. 2009, 40:89-97.
34. Numazaki M., Tominaga T., Takeuchi K., Murayama N., Toyooka H., Tominaga M. Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:8002-8006.
35. Pintér E., Helyes Z., Szolcsányi J. Inhibitory effect of somatostatin on inflammation and nociception. Pharmacol. Ther. 2006, 112:440-456.
36. Pitt D., Werner P., Raine C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 2000, 6:67-70.
37. Prescott E.D., Julius D. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 2003, 300:1284-1288.
38. Rashid M.H., Inoue M., Bakoshi S., Ueda H. Switching of bradykinin-mediated nociception following partial sciatic nerve injury in mice. J. Pharmacol. Exp. Ther. 2003, 308:1158-1164.
39. Rosenbaum T., Gordon-Shaag A., Munari M., Gordon S.E. Ca2+/calmodulin modulates TRPV1 activation by capsaicin. J. Gen. Physiol. 2004, 123:53-62.
40. 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.
41. Rossi S., Muzio L., De Chiara V., Grasselli G., Musella A., Musumeci G., Mandolesi G., De Ceglia R., Maida S., Biffi E., Pedrocchi A., Menegon A., Bernardi G., Furlan R., Martino G., Centonze D. Impaired striatal GABA transmission in experimental autoimmune encephalomyelitis. Brain Behav. Immun. 2010, Oct 20 [Epub ahead of print].
42. Smith T., Groom A., Zhu B., Turski L. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat. Med. 2000, 6:62-66.
43. Starowicz K., Maione S., Cristino L., Palazzo E., Marabese I., Rossi F., de Novellis V., Di Marzo V. Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. J. Neurosci. 2007, 27:13739-13749.
44. Stein A.T., Ufret-Vincenty C.A., Hua L., Santana L.F., Gordon S.E. Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J. Gen. Physiol. 2006, 128:509-522.
45. Steinman L. Multiple sclerosis: a two-stage disease. Nat. Immunol. 2001, 2:762-764.
46. 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.
47. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D. The capsaicin receptor integrates multiple pain producing stimuli. Neuron 1998, 21:531-543.
48. Tominaga M., Tominaga T. Structure and function of TRPV1. Pflugers Arch. 2005, 451:143-150.
49. Toth A., Boczan J., Kedei N., Lizanecz E., Bagi Z., Papp Z., Edes I., Csiba L., Blumberg P.M. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res. Mol. Brain Res. 2005, 135:162-168.
50. Tóth D.M., Szoke E., Bölcskei K., Kvell K., Bender B., Bosze Z., Szolcsányi J., Sándor Z. Nociception, neurogenic inflammation and thermoregulation in TRPV1 knockdown transgenic mice. Cell. Mol. Life Sci. 2010, Nov 11 [Epub ahead of print].
51. Vaishnava P., Wang D.H. Capsaicin sensitive-sensory nerves and blood pressure regulation. Curr. Med. Chem. Cardiovasc. Hematol. Agents 2003, 1:177-188.
52. Vignes J.R., Deloire M.S., Petry K.G., Nagy F. Characterization and restoration of altered inhibitory and excitatory control of micturition reflex in experimental autoimmune encephalomyelitis in rats. J. Physiol. 2007, 578:439-450.
53. 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.
54. Wang L., Wang D.H. TRPV1 gene knockout impairs postischemic recovery in isolated perfused heart in mice. Circulation 2005, 112:3617-3623.
55. Wilson C.J., Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 1996, 16:2397-2410.
56. Zhao B., Schwartz J.P. Involvement of cytokines in normal CNS development and neurological diseases: recent progress and perspectives. J. Neurosci. Res. 1998, 52:7-16.