Cannabinoid receptor signalling in neurodegenerative diseases: A potential role for membrane fluidity disturbance

British Journal of Pharmacology

Volumn 163, Issue 7, 2011, Pages 1379-1390

  MacCarrone, M ^a,b   Bernardi, G ^b,c   Agrò, A Finazzi ^c   Centonze, D ^b,c  

^a UNIVERSITY OF TERAMO   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

cholesterol; CRAC domain; endocannabinoid; membrane lipids; neurodegeneration; neurotransmission; palmitoylation; striatum

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; ADENYLATE CYCLASE; ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; ANANDAMIDE; BETA SECRETASE 1; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR; CHOLESTEROL; ENDOCANNABINOID; GAMMA SECRETASE; LEUCINE RICH REPEAT KINASE 2; METABOTROPIC RECEPTOR 5; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARKIN; PRION PROTEIN; VANILLOID RECEPTOR 1; CANNABINOID 2 RECEPTOR; FRAGILE X MENTAL RETARDATION PROTEIN; METHYL BETA CYCLODEXTRIN;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CHOLESTEROL TRANSPORT; CORPUS STRIATUM; DEGENERATIVE DISEASE; DISEASE COURSE; GABAERGIC TRANSMISSION; HUMAN; HUNTINGTON CHOREA; HYDROPHOBICITY; LIPID PEROXIDATION; LIPID RAFT; MEMBRANE FLUIDITY; MULTIPLE SCLEROSIS; NEUROTRANSMISSION; NONHUMAN; OLIGODENDROGLIA; PARKINSON DISEASE; PHOSPHOLIPID BILAYER; PHYSICAL CHEMISTRY; PRION DISEASE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOSOME; FRAGILE X SYNDROME; GABAERGIC SYSTEM; IN VITRO STUDY; INTRACELLULAR SIGNALING; LIPID MEMBRANE; PATHOPHYSIOLOGY; RECEPTOR BINDING; SEQUENCE ANALYSIS;

ANIMALS; BRAIN; ENDOCANNABINOIDS; HUMANS; MEMBRANE FLUIDITY; NEURODEGENERATIVE DISEASES; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION;

EID: 79960290509     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01277.x     Document Type: Review

References (137)

1. Adibhatla RM, Hatcher JF, (2008). Altered lipid metabolism in brain injury and disorders. Subcell Biochem 49: 241-268.
2. Alexander SPH, Mathie A, Peters JA, (2009). Guide to receptors and channels (GRAC). 4th edn. Br J Pharmacol 158: S1-S254.
3. Anderson RG, Kamen BA, Rothberg KG, Lacey SW, (1992). Potocytosis: sequestration and transport of small molecules by caveolae. Science 255: 410-411.
4. Bari M, Paradisi A, Pasquariello N, Maccarrone M, (2005a). Cholesterol-dependent modulation of type 1 cannabinoid receptors in nerve cells. J Neurosci Res 81: 275-283. (Pubitemid 41153342)
5. Bari M, Battista N, Fezza F, Finazzi-Agrò A, Maccarrone M, (2005b). Lipid rafts control signaling of type-1 cannabinoid receptors in neuronal cells. Implications for anandamide-induced apoptosis. J Biol Chem 280: 12212-12220.
6. Bari M, Spagnuolo P, Fezza F, Oddi S, Pasquariello N, Finazzi-Agrò A, et al,. (2006). Effect of lipid rafts on Cb2 receptor signaling and 2-arachidonoyl-glycerol metabolism in human immune cells. J Immunol 177: 4971-4980. (Pubitemid 44527566)
7. Bari M, Oddi S, De Simone C, Spagnuolo P, Gasperi V, Battista N, et al,. (2008). Type-1 cannabinoid receptors colocalize with caveolin-1 in neuronal cells. Neuropharmacology 54: 45-50. (Pubitemid 350299413)
8. Barnett-Norris J, Lynch D, Reggio PH, (2005). Lipids, lipid rafts and caveolae: their importance for GPCR signaling and their centrality to the endocannabinoid system. Life Sci 77: 1625-1639. (Pubitemid 41073657)
9. Baron GS, Wehrly K, Dorward DW, Chesebro B, Caughey B, (2002). Conversion of raft-associated prion protein to the protease-resistant state requires insertion of PrP-res (PrP(Sc)) into contiguous membranes. EMBO J 21: 1031-1040. (Pubitemid 34206176)
10. Bate C, Salmona M, Diomede L, Williams A, (2004). Squalestatin cures prioninfected neurons and protects against prion neurotoxicity. J Biol Chem 279: 14983-14990. (Pubitemid 38618891)
11. Bear MF, Huber KM, Warren ST, (2004). The mGluR theory of fragile X mental retardation. Trends Neurosci 27: 370-377. (Pubitemid 38829251)
12. Becher A, White JH, McIlhinney RA, (2001). The gamma-aminobutyric acid receptor B, but not the metabotropic glutamate receptor type-1, associates with lipid rafts in the rat cerebellum. J Neurochem 79: 787-795. (Pubitemid 33086516)
13. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ, et al,. (2006). Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311: 864-868. (Pubitemid 43228853)
14. Bhaskar K, Yen S-H, Lee G, (2005). Disease-related modifications in tau affect the interaction between Fyn and tau. J Biol Chem 280: 35119-35125. (Pubitemid 41532698)
15. Bisogno T, Di Marzo V, (2010). Cannabinoid receptors and endocannabinoids: role in neuroinflammatory and neurodegenerative disorders. CNS Neurol Disord Drug Targets 9: 564-573.
16. Brown DA, London E, (1998). Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14: 111-136. (Pubitemid 29001451)
17. Burstein S, Hunter SA, Renzulli L, (1984). Stimulation of sphingomyelin hydrolysis by cannabidiol in fibroblasts from a Niemann-Pick patient. Biochem Biophys Res Commun 121: 168-173. (Pubitemid 14115388)
18. Carlson NG, Rose JW, (2006). Antioxidants in multiple sclerosis: do they have a role in therapy? CNS Drugs 20: 433-441. (Pubitemid 43830734)
19. Centonze D, Battista N, Rossi S, Mercuri NB, Finazzi-Agrò A, Bernardi G, et al,. (2004). A critical interaction between dopamine D2 receptors and endocannabinoids mediates the effects of cocaine on striatal GABAergic transmission. Neuropsychopharmacology 29: 1488-1497. (Pubitemid 38982241)
20. Centonze D, Rossi S, Prosperetti C, Tscherter A, Bernardi G, Maccarrone M, et al,. (2005). 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 57: 1583-1589. (Pubitemid 40805389)
21. Centonze D, Rossi S, De Chiara V, Prosperetti C, Battista N, Bernardi G, et al,. (2007a). Chronic cocaine sensitizes striatal GABAergic synapses to the stimulation of cannabinoid CB1 receptors. Eur J Neurosci 25: 1631-1640. (Pubitemid 46550007)
22. Centonze D, Bari M, Rossi S, Prosperetti C, Furlan R, Fezza F, et al,. (2007b). The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis. Brain 130: 2543-2553. (Pubitemid 47511703)
23. Centonze D, Battistini L, Maccarrone M, (2008). The endocannabinoid system in peripheral lymphocytes as a mirror of neuroinflammatory diseases. Curr Pharm Design 14: 2370-2382.
24. Chau PL, (2010). New insights into the molecular mechanisms of general anaesthetics. Br J Pharmacol 161: 288-307.
25. Dainese E, Oddi S, Maccarrone M, (2010). Interaction of endocannabinoid receptors with biological membranes. Curr Med Chem 17: 1487-1499.
26. De Chiara V, Errico F, Musella A, Rossi S, Mataluni G, Sacchetti L, et al,. (2010a). Voluntary exercise and sucrose consumption enhance cannabinoid CB1 receptor sensitivity in the striatum. Neuropsychopharmacology 35: 374-387.
27. De Chiara V, Angelucci F, Rossi S, Musella A, Cavasinni F, Cantarella C, et al,. (2010b). Brain-derived neurotrophic factor controls cannabinoid CB1 receptor function in the striatum. J Neurosci 30: 8127-8137.
28. De Visser L, Van Den Bos R, Stoker AK, Kas MJ, Spruijt BM, (2007). Effects of genetic background and environmental novelty on wheel running as a rewarding behaviour in mice. Behav Brain Res 177: 290-297. (Pubitemid 46149906)
29. Denovan-Wright EM, Robertson HA, (2000). Cannabinoid receptor messenger RNA levels decrease in a subset of neurons of the lateral striatum, cortex and hippocampus of transgenic Huntington's disease mice. Neuroscience 98: 705-713. (Pubitemid 30417587)
30. Di Marzo V, (2009). The endocannabinoid system: its general strategy of action, tools for its pharmacological manipulation and potential therapeutic exploitation. Pharmacol Res 60: 77-84.
31. Di Marzo V, De Petrocellis L, (2010). Endocannabinoids as regulators of transient receptor potential (TRP) channels: a further opportunity to develop new endocannabinoid-based therapeutic drugs. Curr Med Chem 17: 1430-1449.
32. Dietschy JM, Turley SD, (2004). Thematic review series: brain lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 45: 1375-1397. (Pubitemid 39022664)
33. Dirikoc S, Priola SA, Marella M, Zsürger N, Chabry J, (2007). Nonpsychoactive cannabidiol prevents prion accumulation and protects neurons against prion toxicity. J Neurosci 27: 9537-9544. (Pubitemid 47492190)
34. Eckert GP, Wood WG, Müller WE, (2010). Lipid membranes and beta-amyloid: a harmful connection. Curr Protein Pept Sci 11: 319-325.
35. Eisch AJ, Bolaños CA, de Wit J, Simonak RD, Pudiak CM, Barrot M, et al,. (2003). Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression. Biol Psychiatry 54: 994-1005. (Pubitemid 37415034)
36. Epand RM, (2006). Cholesterol and the interaction of proteins with membrane domains. Prog Lipid Res 45: 279-294. (Pubitemid 43818129)
37. Fallon L, Moreau F, Croft BG, Labib N, Gu WJ, Fon EA, (2002). Parkin and CASK/LIN-2 associate via a PDZ-mediated interaction and are co-localized in lipid rafts and postsynaptic densities in brain. J Biol Chem 277: 486-491. (Pubitemid 34952083)
38. Fantini J, Yahi N, (2010). Molecular insights into amyloid regulation by membrane cholesterol and sphingolipids: common mechanisms in neurodegenerative diseases. Expert Rev Mol Med 12: e27.
39. Ferré S, Lluís C, Justinova Z, Quiroz C, Orru M, Navarro G, et al,. (2010). Adenosine-cannabinoid receptor interactions. Implications for striatal function. Br J Pharmacol 160: 443-453.
40. Fielding CJ, Fielding PE, (2001). Cellular cholesterol efflux. Biochim Biophys Acta 1533: 175-189. (Pubitemid 33127270)
41. Fivaz M, Vilbois F, Thurnheer S, Pasquali C, Abrami L, Bickel PE, et al,. (2002). Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J 21: 3989-4000. (Pubitemid 34857432)
42. Forneris F, Mattevi A, (2008). Enzymes without borders: mobilizing substrates, delivering products. Science 321: 213-216. (Pubitemid 351989085)
43. Fortin DL, Troyer MD, Nakamura K, Kubo S, Anthony MD, Edwards RH, (2004). Lipid rafts mediate the synaptic localization of alpha-synuclein. J Neurosci 24: 6715-6723. (Pubitemid 38993891)
44. Fourgeaud L, Bessis AS, Rossignol F, Pin JP, Olivo-Marin JC, Hémar A, (2003). The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J Biol Chem 278: 12222-12230. (Pubitemid 36800203)
45. Galbiati F, Razani B, Lisanti MP, (2001). Emerging themes in lipid rafts and caveolae. Cell 106: 403-411. (Pubitemid 32786984)
46. Ge M, Field KA, Aneja R, Holowka D, Baird B, Freed JH, (1999). Electron spin resonance characterization of liquid ordered phase of detergent-resistant membranes from RBL-2H3 cells. Biophys J 77: 925-933. (Pubitemid 29362463)
47. Gerdeman G, Lovinger DM, (2001). CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85: 468-471. (Pubitemid 32062158)
48. A receptor alterations in the human basal ganglia in Huntington's disease. Neuroscience 97: 505-519. (Pubitemid 30320757)
49. Glass M, van Dellen A, Blakemore C, Hannan AJ, Faull RLM, (2004). Delayed onset of Huntington's disease in mice in an enriched environment correlates with delayed loss of cannabinoid CB1 receptors. Neuroscience 123: 207-212. (Pubitemid 37518488)
50. Grimm MO, Grimm HS, Tomic I, Beyreuther K, Hartmann T, Bergmann C, (2008). Independent inhibition of Alzheimer disease beta- and gammasecretase cleavage by lowered cholesterol levels. J Biol Chem 283: 11302-11311.
51. Hanzal-Bayer MF, Hancock JF, (2007). Lipid rafts and membrane traffic. FEBS Lett 581: 2098-2104. (Pubitemid 46709907)
52. Hatano T, Kubo SI, Imai S, Maeda M, Ishikawa K, Mizuno Y, et al,. (2007). Leucine-rich repeat kinase 2 associates with lipid rafts. Hum Mol Genet 16: 678-690. (Pubitemid 46585667)
53. Hayashi H, Campenot RB, Vance DE, Vance JE, (2004). Glial lipoproteins stimulate axon growth of central nervous system neurons in compartmented cultures. J Biol Chem 279: 14009-14015. (Pubitemid 38468935)
54. Hill MN, Gorzalka BB, (2009). Impairments in endocannabinoid signaling and depressive illness. JAMA 301: 1165-1166.
55. 1 cannabinoid receptors and their associated proteins. Curr Med Chem 17: 1382-1393.
56. Huang CC, Lo SW, Hsu KS, (2001). Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol 532: 731-748.
57. Huber KM, Gallagher SM, Warren ST, Bear MF, (2002). Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci U S A 99: 7746-7750. (Pubitemid 34568762)
58. Iuvone T, Esposito G, De Filippis D, Scuderi C, Steardo L, (2009). Cannabidiol: a promising drug for neurodegenerative disorders? CNS Neurosci Ther 15: 65-75.
59. Jamin N, Neumann JM, Ostuni MA, Vu TK, Yao ZX, Murail S, et al,. (2005). Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor. Mol Endocrinol 19: 588-594. (Pubitemid 40349433)
60. Johnson RT, Gibbs CJ, Jr, (1998). Creutzfeldt-Jakob disease and related transmissible spongiform encephalopathies. N Engl J Med 339: 1994-2004. (Pubitemid 29024133)
61. Jung KM, Mangieri R, Stapleton C, Kim J, Fegley D, Wallace M, et al,. (2005). Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Mol Pharmacol 68: 1196-1202. (Pubitemid 41539977)
62. Jung KM, Astarita G, Zhu C, Wallace M, Mackie K, Piomelli D, (2007). A key role for diacylglycerol lipase-alpha in metabotropic glutamate receptor-dependent endocannabinoid mobilization. Mol Pharmacol 72: 612-621. (Pubitemid 47347296)
63. Kalvodova L, Kahya N, Schwille P, Ehehalt R, Verkade P, Drechsel D, et al,. (2005). Lipids as modulators of proteolytic activity of BACE: involvement of cholesterol, glycosphingolipids, and anionic phospholipids in vitro. J Biol Chem 280: 36815-36823. (Pubitemid 41587762)
64. Karten B, Campenot RB, Vance DE, Vance JE, (2006). Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia. J Biol Chem 281: 4049-4057. (Pubitemid 43847830)
65. Katona I, Freund TF, (2008). Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med 14: 923-930.
66. Katona I, Urbán GM, Wallace M, Ledent C, Jung KM, Piomelli D, et al,. (2006). Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26: 5628-5637. (Pubitemid 44315254)
67. Kelley AE, (2004). Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44: 161-179. (Pubitemid 39348838)
68. Köfalvi A, Rodrigues RJ, Ledent C, Mackie K, Vizi ES, Cunha RA, et al,. (2005). Involvement of cannabinoid receptors in the regulation of neurotransmitter release in the rodent striatum: a combined immunochemical and pharmacological analysis. J Neurosci 25: 2874-2884. (Pubitemid 40389245)
69. Kubo S-I, Neman VM, Chalkley RJ, Anthony MD, Hattori N, Mizuno Y, et al,. (2005). A combinatorial code for the interaction of alphasynuclein with membranes. J Biol Chem 280: 31664-31672. (Pubitemid 41291913)
70. Kust BM, Copray JC, Brouwer N, Troost D, Boddeke HW, (2002). Elevated levels of neurotrophins inhumanbiceps brachii tissue of amyotrophic lateral sclerosis. Exp Neurol 177: 419-427. (Pubitemid 35366131)
71. 1 receptors in the basal ganglia of a transgenic model of Huntington's disease. Brain Res 929: 236-242. (Pubitemid 34178339)
72. Lenoir M, Serre F, Cantin L, Ahmed SH, (2007). Intense sweetness surpasses cocaine reward. PloS One 2: e698.
73. Lett BT, Grant VL, Koh MT, (2001). Naloxone attenuates the conditioned place preference induced by wheel running in rats. Physiol Behav 72: 355-358. (Pubitemid 32234420)
74. Levine AS, Kotz CM, Gosnell BA, (2003). Sugars: hedonic aspects, neuroregulation, and energy balance. Am J Clin Nutr 78: 834S-842S.
75. Li H, Papadopoulos V, (1998). Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139: 4991-4997. (Pubitemid 28533447)
76. Lindahl E, Sansom MS, (2008). Membrane proteins: molecular dynamics simulations. Curr Opin Struct Biol 18: 425-431.
77. Liu JP, Tang Y, Zhou S, Toh BH, McLean C, Li H, (2010). Cholesterol involvement in the pathogenesis of neurodegenerative diseases. Mol Cell Neurosci 43: 33-42.
78. Lucero HA, Robbins PW, (2004). Lipid rafts-protein association and the regulation of protein activity. Arch Biochem Biophys 426: 208-224. (Pubitemid 38680618)
79. Maccarrone M, (2008). Good news for CB1 receptors: endogenous agonists are in the right place. Br J Pharmacol 153: 179-181.
80. Maccarrone M, Battista N, Centonze D, (2007). The endocannabinoid pathway in Huntington's disease: a comparison with other neurodegenerative diseases. Prog Neurobiol 81: 349-379. (Pubitemid 46528640)
81. Maccarrone M, Rossi S, Bari M, De Chiara V, Fezza F, Musella A, et al,. (2008). Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum. Nat Neurosci 11: 152-159. (Pubitemid 351170502)
82. Maccarrone M, De Chiara V, Gasperi V, Viscomi MT, Rossi S, Oddi S, et al,. (2009). Lipid rafts regulate 2-arachidonoylglycerol metabolism and physiological activity in the striatum. J Neurochem 109: 371-381.
83. Maccarrone M, Gasperi V, Catani MV, Diep TA, Dainese E, Hansen HS, (2010a). The endocannabinoid system and its relevance for nutrition. Annu Rev Nutr 30: 423-440.
84. Maccarrone M, Rossi S, Bari M, De Chiara V, Rapino C, Musella A, et al,. (2010b). Abnormal mGlu 5 receptor/endocannabinoid coupling in mice lacking FMRP and BC1 RNA. Neuropsychopharmacology 35: 1500-1509.
85. Martin M, Dotti CG, Ledesma MD, (2010). Brain cholesterol in normal and pathological aging. Biochim Biophys Acta 1801: 934-944.
86. Moffett S, Brown DA, Linder ME, (2000). Lipid-dependent targeting of G proteins into rafts. J Biol Chem 275: 2191-2198. (Pubitemid 30060849)
87. Mojsilovic-Petrovic J, Jeong GB, Crocker A, Arneja A, David S, Russell D, et al,. (2006). Protecting motor neurons from toxic insult by antagonism of adenosine A2a and Trk receptors. J Neurosci 26: 9250-9263. (Pubitemid 44359851)
88. Musella A, De Chiara V, Rossi S, Cavasinni F, Castelli M, Cantarella C, et al,. (2010). Transient receptor potential vanilloid 1 channels control acetylcholine/2-arachidonoylglicerol coupling in the striatum. Neuroscience 167: 864-871.
89. Narushima M, Uchigashima M, Hashimoto K, Watanabe M, Kano M, (2006). Depolarization-induced suppression of inhibition mediated by endocannabinoids at synapses from fast-spiking interneurons to medium spiny neurons in the striatum. Eur J Neurosci 24: 2246-2252. (Pubitemid 44622345)
90. Narushima M, Uchigashima M, Fukaya M, Matsui M, Manabe T, Hashimoto K, et al,. (2007). Tonic enhancement of endocannabinoid-mediated retrograde suppression of inhibition by cholinergic interneuron activity in the striatum. J Neurosci 27: 496-506. (Pubitemid 46143754)
91. Oddi S, Dainese E, Fezza F, Lanuti M, Barcaroli D, De Laurenzi V, et al,. (2011). Functional characterization of putative cholesterol binding sequence (CRAC) in human type-1 cannabinoid receptor. J Neurochem 116: 858-865.
92. Oh P, Schnitzer JE, (2001). Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol Biol Cell 12: 685-698. (Pubitemid 33052021)
93. Ostermeyer AG, Beckrich BT, Ivarson KA, Grove KE, Brown DA, (1999). Glycosphingolipids are not essential for formation of detergent-resistant membrane rafts in melanoma cells. methyl-betacyclodextrin does not affect cell surface transport of a GPI anchored protein. J Biol Chem 274: 34459-34466. (Pubitemid 129511793)
94. Ostrom RS, Insel PA, (2004). The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 143: 235-245. (Pubitemid 39315143)
95. Packard MG, (2009). Anxiety, cognition, and habit: a multiple memory systems perspective. Brain Res 1293: 121-128.
96. Paila YD, Ganguly S, Chattopadhyay A, (2010). Metabolic depletion of sphingolipids impairs ligand binding and signaling of human serotonin1A receptors. Biochemistry 49: 2389-2397.
97. Pani A, Mandas A, Dessì S, (2010). Cholesterol, Alzheimer's disease, prion disorders: a ménage à trois? Curr Drug Targets 11: 1018-1031.
98. Patel KD, Davison JS, Quentin J, Pittman OJ, Sharkey KA, (2010). Cannabinoid CB2 receptors in health and disease. Curr Med Chem 17: 1394-1410.
99. Pelkmans L, (2005). Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim Biophys Acta 1746: 295-304. (Pubitemid 41815023)
100. Pertwee RG, (2010). Receptors and channels targeted by synthetic cannabinoid receptor agonists and antagonists. Curr Med Chem 17: 1360-1381.
101. Petrosino S, Di Marzo V, (2010). FAAH and MAGL inhibitors: therapeutic opportunities from regulating endocannabinoid levels. Curr Opin Investig Drugs 11: 51-62.
102. Pike LJ, (2005). Growth factor receptors, lipid rafts and caveolae: an evolving story. Biochim Biophys Acta 1746: 260-273. (Pubitemid 41818991)
103. Pontier SM, Percherancier Y, Galandrin S, Breit A, Gales C, Bouvier M, (2008). Cholesterol-dependent separation of the beta2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J Biol Chem 283: 24659-24672.
104. Prinetti A, Loberto N, Chigorno V, Sonnino S, (2009). Glycosphingolipid behaviour in complex membranes. Biochim Biophys Acta 1788: 184-193.
105. Richfield EK, Herkenham M, (1994). Selective vulnerability in Huntington's disease: preferential loss of cannabinoid receptors in lateral globus pallidus. Ann Neurol 36: 577-584. (Pubitemid 24309369)
106. Rimmerman N, Hughes HV, Bradshaw HB, Pazos MX, Mackie K, Prieto AL, et al,. (2008). Compartmentalization of endocannabinoids into lipid rafts in a dorsal root ganglion cell line. Br J Pharmacol 153: 380-389.
107. Rodriguez-Oroz MC, Jahanshahi M, Krack P, Litvan I, Macias R, Bezard E, et al,. (2009). Initial clinical manifestations of Parkinson's disease: features and pathophysiological mechanisms. Lancet Neurol 8: 1128-1139.
108. Rossi S, De Chiara V, Musella A, Kusayanagi H, Mataluni G, Bernardi G, et al,. (2008). Chronic psychoemotional stress impairs cannabinoid-receptor- mediated control of GABA transmission in the striatum. J Neurosci 28: 7284-7292.
109. Rossi S, De Chiara V, Musella A, Mataluni G, Sacchetti L, Siracusano A, et al,. (2009). Caffeine drinking potentiates cannabinoid transmission in the striatum: interaction with stress effects. Neuropharmacology 56: 590-597.
110. Rossi S, Bernardi G, Centonze D, (2010a). The endocannabinoid system in the inflammatory and neurodegenerative processes of multiple sclerosis and of amyotrophic lateral sclerosis. Exp Neurol 224: 92-102.
111. Rossi S, De Chiara V, Musella A, Sacchetti L, Cantarella C, Castelli M, et al,. (2010b). Preservation of striatal cannabinoid CB1 receptor function correlates with the antianxiety effects of fatty acid amide hydrolase inhibition. Mol Pharmacol 78: 260-268.
112. Rossi S, De Chiara V, Musella A, Cozzolino M, Bernardi G, Maccarrone M, et al,. (2010c). Abnormal sensitivity of cannabinoid CB1 receptors in the striatum of mice with experimental amyotrophic lateral sclerosis. Amyotroph Lateral Scler 11: 83-90.
113. Schengrund CL, (2010). Lipid rafts: keys to neurodegeneration. Brain Res Bull 82: 7-17.
114. Schrattenholz A, Soskic V, (2006). NMDA receptors are not alone: dynamic regulation of NMDA receptor structure and function by neuregulins and transient cholesterol-rich membrane domains leads to disease-specific nuances of glutamate-signalling. Curr Top Med Chem 6: 663-686.
115. Schweitzer JK, Krivda JP, D'Souza-Schorey C, (2009). Neurodegeneration in Niemann-Pick Type C disease and Huntington's disease: impact of defects in membrane trafficking. Curr Drug Targets 10: 653-665.
116. 1A receptors. Biochemistry 49: 5426-5435.
117. Silvestri L, Caputo V, Bellacchio E, Atorino L, Dallapiccola B, Valente EM, et al,. (2005). Mitochondral import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum Mol Genet 14: 3477-3492. (Pubitemid 41672130)
118. Simons M, Keller P, De Strooper B, Beyreuther K, Dotti CG, Simons K, (1998). Cholesterol depletion inhibits the generation of β-amyloid in hippocampal neurons. Proc Natl Acad Sci U S A 95: 6460-6464. (Pubitemid 28249035)
119. Simpson EH, Kellendonk C, Kandel E, (2010). A possible role for the striatum in the pathogenesis of the cognitive symptoms of schizophrenia. Neuron 65: 585-596.
120. Singer SJ, Nicolson GL, (1972). The fluid mosaic model of the structure of cell membranes. Science 175: 720-731.
121. Sipione S, Rigamonti D, Valenza M, Zuccato C, Conti L, Pritchard J, et al,. (2002). Early transcriptional profiles in huntingtin-inducible striatal cells by microarray analyses. Hum Mol Genet 11: 1953-1965. (Pubitemid 34919271)
122. Smart EJ, De Rose RA, Farber SA, (2004). Annexin 2-caveolin 1 complex is a target of ezetimibe and regulates intestinal cholesterol transport. Proc Natl Acad Sci U S A 101: 3450-3455. (Pubitemid 38338215)
123. Szabo B, Dörner L, Pfreundtner C, Nörenberg W, Starke K, (1998). Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience 85: 395-403. (Pubitemid 28218661)
124. Uchigashima M, Narushima M, Fukaya M, Katona I, Kano M, Watanabe M, (2007). Subcellular arrangement of molecules for 2-arachidonoyl-glycerol- mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27: 3663-3676. (Pubitemid 46557660)
125. Uittenbogaard A, Everson WV, Matveev SV, Smart EJ, (2002). Cholesteryl ester is transported from caveolae to internal membranes as part of a caveolin-annexin II lipid-protein complex. J Biol Chem 277: 4925-4931. (Pubitemid 34968530)
126. Valencia A, Reeves PB, Sapp E, Li S, Alexander J, Kegel KB, et al,. (2009). Mutant huntingtin and glycogen synthase kinase 3-β accumulate in neuronal lipid rafts of a presymptomatic knock-in mouse model of Huntington's disease. J Neurosci Res 29: 6106-6116.
127. Valenza M, Cattaneo E, (2006). Cholesterol dysfunction in neurodegenerative diseases: is Huntington's disease in the list? Prog Neurobiol 80: 165-176. (Pubitemid 44821504)
128. Vance JE, Karten B, Hayashi H, (2006). Lipid dynamics in neurons. Biochem Soc Trans 34: 399-403. (Pubitemid 43953997)
129. Vaya J, Schipper HM, (2007). Oxysterols, cholesterol homeostasis, and Alzheimer disease. J Neurochem 102: 1727-1737. (Pubitemid 47329280)
130. Volkow ND, Wise RA, (2005). How can drug addiction help us understand obesity? Nat Neurosci 8: 555-560. (Pubitemid 40594193)
131. Werme M, Thoren P, Olson L, Brene S, (2000). Running and cocaine both upregulate dynorphin mRNA in medial caudate putamen. Eur J Neurosci 12: 2967-2974.
132. Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ, et al,. (2002). Delta FosB regulates wheel running. J Neurosci 22: 8133-8138. (Pubitemid 35379119)
133. Xie HQ, Liang D, Leung KW, Chen VP, Zhu KY, Chan WK, et al,. (2010). Targeting acetylcholinesterase to membrane rafts: a function mediated by the proline-rich membrane anchor (PRiMA) in neurons. J Biol Chem 285: 11537-11546.
134. Xu X, London E, (2000). The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 39: 843-849. (Pubitemid 30075310)
135. Yin HH, Lovinger DM, (2006). Frequency-specific and D2 receptor-mediated inhibition of glutamate release by retrograde endocannabinoid signaling. Proc Natl Acad Sci U S A 103: 8251-8256. (Pubitemid 43801084)
136. Yin HH, Adermark L, Lovinger DM, (2008). Neurotensin reduces glutamatergic transmission in the dorsolateral striatum via retrograde endocannabinoid signaling. Neuropharmacology 54: 79-86. (Pubitemid 350299398)
137. Zuccato C, Valenza M, Cattaneo E, (2010). Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol Rev 90: 905-981.