Cannabinoid receptor-interacting protein 1a modulates CB1 receptor signaling and regulation

Molecular Pharmacology

Volumn 87, Issue 4, 2015, Pages 747-765

  Smith, Tricia H ^a   Blume, Lawrence C ^c   Straiker, Alex ^d   Cox, Jordan O ^a   David, Bethany G ^a   Secor McVoy, Julie R ^a   Sayers, Katherine W ^b   Poklis, Justin L ^a   Abdullah, Rehab A ^a   Egertová, Michaela ^e   Chen, Ching Kang ^b   Mackie, Ken ^d   Elphick, Maurice R ^e   Howlett, Allyn C ^c   Selley, Dana E ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^d INDIANA UNIVERSITY   (United States)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR INTERACTING PROTEIN 1A; GUANINE NUCLEOTIDE BINDING PROTEIN; RIMONABANT; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CARRIER PROTEIN; CNRIP1 PROTEIN, RAT; ENDOCANNABINOID;

ANIMAL TISSUE; ARTICLE; DOWN REGULATION; EMBRYO; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEK293 CELL LINE; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INVERSE AGONISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; STABLE TRANSFECTION; STOICHIOMETRY; TISSUE PREPARATION; AGONISTS; ANIMAL; CELL LINE; CEREBELLUM; CYTOLOGY; GENETICS; HIPPOCAMPUS; MALE; METABOLISM; MOUSE; NERVE CELL; RADIOASSAY; SPRAGUE DAWLEY RAT;

ANIMALS; CARRIER PROTEINS; CELL LINE; CEREBELLUM; ENDOCANNABINOIDS; GTP-BINDING PROTEINS; HIPPOCAMPUS; HUMANS; MALE; MICE; NEURONS; RADIOLIGAND ASSAY; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION;

EID: 84982179168     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.096495     Document Type: Article

References (64)

1. Abood ME, Ditto KE, Noel MA, Showalter VM, and Tao Q (1997) Isolation and expression of a mouse CB1 cannabinoid receptor gene. Comparison of binding properties with those of native CB1 receptors in mouse brain and N18TG2 neuroblastoma cells. Biochem Pharmacol 53:207-214.
2. Anavi-Goffer S, Fleischer D, Hurst DP, Lynch DL, Barnett-Norris J, Shi S, Lewis DL, Mukhopadhyay S, Howlett AC, and Reggio PH et al. (2007) Helix 8 Leu in the CB1 cannabinoid receptor contributes to selective signal transduction mechanisms. J Biol Chem 282:25100-25113.
3. Atwood BK, Lopez J, Wager-Miller J, Mackie K, and Straiker A (2011) Expression of G protein-coupled receptors and related proteins in HEK293, AtT20, BV2, and N18 cell lines as revealed by microarray analysis. BMC Genomics 12:14.
4. Bakshi K, Mercier RW, and Pavlopoulos S (2007) Interaction of a fragment of the cannabinoid CB1 receptor C-terminus with arrestin-2. FEBS Lett 581:5009-5016.
5. Bekkers JM and Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 88:7834-7838.
6. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urbán GM, Monory K, Marsicano G, Matteoli M, and Canty A et al. (2007) Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316:1212-1216.
7. Blume LC, Bass CE, Childers SR, Dalton GD, Roberts DC, Richardson JM, Xiao R, Selley DE, and Howlett AC (2013) Striatal CB1 and D2 receptors regulate expression of each other, CRIP1A and d opioid systems. J Neurochem 124:808-820.
8. Blume L, Eldeeb K, Bass CE, Selley DE, and Howlett AC (2015) Cannabinoid receptor interacting protein (CRIP1a) attenuates CB1R signaling in neuronal cells. Cell Signal 27:716-726.
9. Bojnik E, Turunç E, Armaǧan G, Kanit L, Benyhe S, Yalçin A, and Borsodi A (2012) Changes in the cannabinoid (CB1) receptor expression level and G-protein activation in kainic acid induced seizures. Epilepsy Res 99:64-68.
10. Breivogel CS, Griffin G, DiMarzo V, andMartin BR (2001) Evidence for a new G proteincoupled cannabinoid receptor in mouse brain. Mol Pharmacol 60:155-163.
11. Daigle TL, Kwok ML, and Mackie K (2008) Regulation of CB1 cannabinoid receptor internalization by a promiscuous phosphorylation-dependent mechanism. J Neurochem 106:70-82.
12. Di Marzo V, Breivogel CS, Tao Q, Bridgen DT, Razdan RK, Zimmer AM, Zimmer A, and Martin BR (2000) Levels, metabolism, and pharmacological activity of anandamide in CB(1) cannabinoid receptor knockoutmice: evidence for non-CB(1), non-CB(2) receptor-mediated actions of anandamide in mouse brain. J Neurochem 75:2434-2444.
13. Falenski KW, Blair RE, Sim-Selley LJ, Martin BR, and DeLorenzo RJ (2007) Status epilepticus causes a long-lasting redistribution of hippocampal cannabinoid type 1 receptor expression and function in the rat pilocarpine model of acquired epilepsy. Neuroscience 146:1232-1244.
14. Furshpan EJ, MacLeish PR, O'Lague PH, and Potter DD (1976) Chemical transmission between rat sympathetic neurons and cardiac myocytes developing in microcultures: evidence for cholinergic, adrenergic, and dual-function neurons. Proc Natl Acad Sci USA 73:4225-4229.
15. Glass M and Northup JK (1999) Agonist selective regulation of G proteins by cannabinoid CB(1) and CB(2) receptors. Mol Pharmacol 56:1362-1369.
16. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, and Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583.
17. Hirvonen J, Goodwin RS, Li CT, Terry GE, Zoghbi SS, Morse C, Pike VW, Volkow ND, Huestis MA, and Innis RB (2012) Reversible and regionally selective downregulation of brain cannabinoid CB1 receptors in chronic daily cannabis smokers. Mol Psychiatry 17:642-649.
18. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, and Martin BR et al. (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54: 161-202.
19. Howlett AC, Blume LC, and Dalton GD (2010) CB(1) cannabinoid receptors and their associated proteins. Curr Med Chem 17:1382-1393.
20. Hsieh C, Brown S, Derleth C, and Mackie K (1999) Internalization and recycling of the CB1 cannabinoid receptor. J Neurochem 73:493-501.
21. Hu SS, Arnold A, Hutchens JM, Radicke J, Cravatt BF, Wager-Miller J, Mackie K, and Straiker A (2010) Architecture of cannabinoid signaling in mouse retina. J Comp Neurol 518:3848-3866.
22. Jain T, Wager-Miller J, Mackie K, and Straiker A (2013) Diacylglycerol lipasea (DAGLa) and DAGLb cooperatively regulate the production of 2-arachidonoyl glycerol in autaptic hippocampal neurons. Mol Pharmacol 84:296-302.
23. Jiang M, Deng L, and Chen G (2004) High Ca(21)-phosphate transfection efficiency enables single neuron gene analysis. Gene Ther 11:1303-1311.
24. Jin W, Brown S, Roche JP, Hsieh C, Celver JP, Kovoor A, Chavkin C, and Mackie K (1999) Distinct domains of the CB1 cannabinoid receptor mediate desensitization and internalization. J Neurosci 19:3773-3780.
25. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, and Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309-380.
26. Lazenka MF, Selley DE, and Sim-Selley LJ (2013) Brain regional differences in CB1 receptor adaptation and regulation of transcription. Life Sci 92:446-452.
27. Leterrier C, Bonnard D, Carrel D, Rossier J, and Lenkei Z (2004) Constitutive endocytic cycle of the CB1 cannabinoid receptor. J Biol Chem. 279:36013-36021.
28. Leterrier C, Lainé J, Darmon M, Boudin H, Rossier J, and Lenkei Z (2006) Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci. 26:3141-3153.
29. Levison SW and McCarthy KD (1991) Characterization and partial purification of AIM: a plasma protein that induces rat cerebral type 2 astroglia from bipotential glial progenitors. J Neurochem 57:782-794.
30. Lind GE, Danielsen SA, Ahlquist T, Merok MA, Andresen K, Skotheim RI, Hektoen M, Rognum TO, Meling GI, and Hoff G et al. (2011) Identification of an epigenetic biomarker panel with high sensitivity and specificity for colorectal cancer and adenomas. Mol Cancer 10:85.
31. Ludányi A, Eross L, Czirják S, Vajda J, Halász P, Watanabe M, Palkovits M, Maglóczky Z, Freund TF, and Katona I (2008) Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J Neurosci 28:2976-2990.
32. Martini L, Waldhoer M, Pusch M, Kharazia V, Fong J, Lee JH, Freissmuth C, and Whistler JL (2007) Ligand-induced down-regulation of the cannabinoid 1 receptor is mediated by the G-protein-coupled receptor-associated sorting protein GASP1. FASEB J 21:802-811.
33. Martini L, Thompson D, Kharazia V, and Whistler JL (2010) Differential regulation of behavioral tolerance to WIN55, 212-2 by GASP1. Neuropsychopharmacology 35: 1363-1373.
34. McDonald NA, Henstridge CM, Connolly CN, and Irving AJ (2007) An essential role for constitutive endocytosis, but not activity, in the axonal targeting of the CB1 cannabinoid receptor. Mol Pharmacol 71:976-984.
35. McIntosh HH, Song C, and Howlett AC (1998) CB1 cannabinoid receptor: cellular regulation and distribution in N18TG2 neuroblastoma cells. Brain Res Mol Brain Res 53:163-173.
36. Meschler JP, Kraichely DM, Wilken GH, and Howlett AC (2000) Inverse agonist properties of N-(piperidin-1-yl)-5-(4-chlorophenyl)-1-(2, 4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide HCl (SR141716A) and 1-(2-chlorophenyl)-4-cyano-5-(4-methoxyphenyl)-1H-pyrazole-3-carboxyl ic acid phenylamide (CP-272871) for the CB (1) cannabinoid receptor. In Process Citation Biochem Pharmacol 60:1315-1323.
37. Meyer AH, Katona I, Blatow M, Rozov A, and Monyer H (2002) In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22:7055-7064.
38. Morgan DJ, Davis BJ, Kearn CS, Marcus D, Cook AJ, Wager-Miller J, Straiker A, Myoga MH, Karduck J, and Leishman E et al. (2014) Mutation of putative GRK phosphorylation sites in the cannabinoid receptor 1 (CB1R) confers resistance to cannabinoid tolerance and hypersensitivity to cannabinoids in mice. J Neurosci 34: 5152-5163.
39. Mukhopadhyay S and Howlett AC (2001) CB1 receptor-G protein association. Subtype selectivity is determined by distinct intracellular domains. Eur J Biochem 268:499-505.
40. Mukhopadhyay S and Howlett AC (2005) Chemically distinct ligands promote differential CB1 cannabinoid receptor-Gi protein interactions. Mol Pharmacol. 67: 2016-2024.
41. Nguyen PT, Schmid CL, Raehal KM, Selley DE, Bohn LM, and Sim-Selley LJ (2012) β-arrestin2 regulates cannabinoid CB1 receptor signaling and adaptation in a central nervous system region-dependent manner. Biol Psychiatry 71:714-724.
42. Nie J and Lewis DL (2001a) The proximal and distal C-terminal tail domains of the CB1 cannabinoid receptor mediate G protein coupling. Neuroscience 107:161-167.
43. Nie J and Lewis DL (2001b) Structural domains of the CB1 cannabinoid receptor that contribute to constitutive activity and G-protein sequestration. J Neurosci 21: 8758-8764.
44. Niehaus JL, Liu Y, Wallis KT, EgertováM, Bhartur SG, Mukhopadhyay S, Shi S, He H, Selley DE, and Howlett AC et al. (2007) CB1 cannabinoid receptor activity is modulated by the cannabinoid receptor interacting protein CRIP 1a. Mol Pharmacol 72: 1557-1566.
45. Oster B, Thorsen K, Lamy P, Wojdacz TK, Hansen LL, Birkenkamp-Demtröder K, Sørensen KD, Laurberg S, Orntoft TF,, and Andersen CL (2011) Identification and validation of highly frequent CpG island hypermethylation in colorectal adenomas and carcinomas. Int J Cancer 129:2855-2866.
46. Pacher P, Bátkai S, and Kunos G (2006) The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58:389-462
47. Rozenfeld R and Devi LA (2008) Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J 22:2311-2322.
48. Seifert R and Wenzel-Seifert K (2002) Constitutive activity of G-protein-coupled receptors: cause of disease and common property of wild-type receptors. Naunyn Schmiedebergs Arch Pharmacol 366:381-416.
49. Shapira M, Gafni M, and Sarne Y (2003) Long-term interactions between opioid and cannabinoid agonists at the cellular level: cross-desensitization and downregulation. Brain Res 960:190-200.
50. Sim-Selley LJ (2003) Regulation of cannabinoid CB1 receptors in the central nervous system by chronic cannabinoids. Crit Rev Neurobiol 15:91-119.
51. Sim-Selley LJ, Brunk LK, and Selley DE (2001) Inhibitory effects of SR141716A on G-protein activation in rat brain. Eur J Pharmacol 414:135-143.
52. Sim-Selley LJ, Schechter NS, Rorrer WK, Dalton GD, Hernandez J, Martin BR, and Selley DE (2006) Prolonged recovery rate of CB1 receptor adaptation after cessation of long-term cannabinoid administration. Mol Pharmacol 70: 986-996.
53. Singh SN, Bakshi K, Mercier RW, Makriyannis A, and Pavlopoulos S (2011) Binding between a distal C-terminus fragment of cannabinoid receptor 1 and arrestin-2. Biochemistry 50:2223-2234.
54. Smith TH, Sim-Selley LJ, and Selley DE (2010) Cannabinoid CB1 receptor-interacting proteins: novel targets for central nervous system drug discovery? Br J Pharmacol 160:454-466.
55. Stauffer B, Wallis KT, Wilson SP, Egertová M, Elphick MR, Lewis DL, and Hardy LR (2011) CRIP1a switches cannabinoid receptor agonist/antagonist-mediated protection from glutamate excitotoxicity. Neurosci Lett 503:224-228.
56. Straiker A and Mackie K (2005) Depolarization-induced suppression of excitation in murine autaptic hippocampal neurones. J Physiol 569:501-517.
57. Straiker A and Mackie K (2009) Cannabinoid signaling in inhibitory autaptic hippocampal neurons. Neuroscience 163:190-201.
58. Straiker A, Hu SS, Long JZ, Arnold A, Wager-Miller J, Cravatt BF, and Mackie K (2009) Monoacylglycerol lipase limits the duration of endocannabinoid-mediated depolarization-induced suppression of excitation in autaptic hippocampal neurons. Mol Pharmacol 76:1220-1227.
59. Straiker A, Wager-Miller J, Hutchens J, and Mackie K (2012) Differential signalling in human cannabinoid CB1 receptors and their splice variants in autaptic hippocampal neurones. Br J Pharmacol 165:2660-2671.
60. Straiker AJ, Borden CR, and Sullivan JM (2002) G-protein alpha subunit isoforms couple differentially to receptors that mediate presynaptic inhibition at rat hippocampal synapses. J Neurosci 22:2460-2468.
61. Sunyer T, Monastirsky B, Codina J, and Birnbaumer L (1989) Studies on nucleotide and receptor regulation of Gi proteins: effects of pertussis toxin. Mol Endocrinol 3: 1115-1124.
62. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, and Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467: 60-79.
63. Tzavara ET, Valjent E, Firmo C, Mas M, Beslot F, Defer N, Roques BP, Hanoune J, and Maldonado R (2000) Cannabinoid withdrawal is dependent upon PKA activation in the cerebellum. Eur J Neurosci 12:1038-1046.
64. Villares J (2007) Chronic use of marijuana decreases cannabinoid receptor binding and mRNA expression in the human brain. Neuroscience 145:323-334.