GABA B receptor cell-surface export is controlled by an endoplasmic reticulum gatekeeper

Molecular Psychiatry

Volumn 21, Issue 4, 2016, Pages 480-490

  Doly, S ^a,b,c   Shirvani, H ^a,b,c   Gta, G ^a,b,c   Meye, F J ^d   Emerit, M B ^c,e   Enslen, H ^a,b,c   Achour, L ^a,b,c   Pardo Lopez, L ^a,b,c,i   Yang, S K ^c,e   Armand, V ^c,e   Gardette, R ^c,e   Giros, B ^f,g   Gassmann, M ^h   Bettler, B ^h   Mameli, M ^d   Darmon, M ^c,e   Marullo, S ^a,b,c  

^a INSTITUT COCHIN   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSTITUT DU FER À MOULIN   (France)

^e CENTRE DE PSYCHIATRIE ET NEUROSCIENCES   (France)

^f INSERM   (France)

^g MCGILL UNIVERSITY   (Canada)

^h UNIVERSITY OF BASEL   (Switzerland)

ⁱ INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; AMPHETAMINE; BACLOFEN; CELL SURFACE RECEPTOR; MEMBRANE PROTEIN; PRAF2 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; CARRIER PROTEIN; PRAF2 PROTEIN, HUMAN; PROTEIN SUBUNIT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LYSATE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; ENDOPLASMIC RETICULUM; HEK293 CELL LINE; HUMAN; HUMAN CELL; HYPERACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; LOCOMOTION; MOTOR ACTIVITY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CELL MEMBRANE; KNOCKOUT MOUSE; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; GAMMA-AMINOBUTYRIC ACID; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RECEPTORS, GABA-B;

EID: 84930341731     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.72     Document Type: Article

References (72)

1. Doherty GJ, McMahon HT. Mechanisms of Endocytosis. Annu Rev Biochem 2009; 78: 31.31-31.46.
2. Aridor M, Hannan LA. Traffic Jams II: An Update of Diseases of Intracellular Transport. Traffic 2002; 3: 781-790.
3. Hein L, Ishii K, Coughlin SR, Kobilka BK. Intracellular targeting and trafficking of thrombin receptors. A novel mechanism for resensitization of a G protein-coupled receptor. J Biol Chem 1994; 269: 27719-27726.
4. Brismar H, Asghar M, Carey RM, Greengard P, Aperia A. Dopamine-induced recruitment of dopamine D1 receptors to the plasma membrane. Proc Natl Acad Sci USA 1998; 95: 5573-5578.
5. Saito H, Kubota M, Roberts RW, Chi Q, Matsunami H. RTP family members induce functional expression of mammalian odorant receptors. Cell 2004; 119: 679-691.
6. Achour L, Labbe-Juillie C, Scott MGH, Marullo S. An escort for G Protein Coupled Receptors to find their path: implication for regulation of receptor density at the cell surface. Trends Pharmacol Sci 2008; 29: 528-535.
7. Achour L, Scott MG, Shirvani H, Thuret A, Bismuth G, Labbe-Jullie C, et al. CD4 - CCR5 interaction in intracellular compartments contributes to receptor expression at the cell surface. Blood 2009; 113: 1938-1947.
8. Holtback U, Brismar H, DiBona GF, Fu M, Greengard P, Aperia A. Receptor recruitment: a mechanism for interactions between G protein-coupled receptors. Proc Natl Acad Sci USA 1999; 96: 7271-7275.
9. Shirvani H, Achour L, Scott MGH, Thuret A, Bismuth G, Labbe-Juillie C, et al. Internal stores of CCR5 in blood cells. Blood 2011; 118: 1175-1176.
10. Farhan H, Rabouille C. Signalling to and from the secretory pathway. J Cell Sci 2011; 124: 171-180.
11. Kusek J, Yang Q, Witek M, Gruber CW, Nanoff C, Freissmuth M. Chaperoning of the A1-Adenosine receptor by endogenous adenosine - an extension of the retaliatory metabolite concept. Mol Pharmacol 2015; 87: 39-51.
12. McLatchie LM, Fraser NJ, Main MJ, Wise A, Brown J, Thompson N, et al. RAMPs regulate the transport and ligand specificity of the calcitonin- receptor-like receptor. Nature 1998; 393: 333-339.
13. Bermak JC, Li M, Bullock C, Zhou QY. Regulation of transport of the dopamine D1 receptor by a new membrane- associated ER protein. Nat Cell Biol 2001; 3: 492-498.
14. Svenningsson P, Chergui K, Rachleff I, Flajolet M, Zhang X, El Yacoubi M, et al. Alterations in 5-HT1B receptor function by p11 in depression-like states. Science 2006; 311: 77-80.
15. Bergmayr C, Thurner P, Keuerleber S, Kudlacek O, Nanoff C, Freissmuth M, et al. Recruitment of a cytoplasmic chaperone relay by the A2A adenosine receptor. J Biol Chem 2013; 288: 28831-28844.
16. Brock C, Boudier L, Maurel D, Blahos J, Pin JP. Assembly-dependent surface targeting of the heterodimeric GABAB Receptor is controlled by COPI but not 14-3-3. Mol Biol Cell 2005; 16: 5572-5578.
17. Cunningham M, McIntosh K, Pediani JD, Robben J, Cooke AE, Nilsson M, et al. Novel role for proteinase-Activated receptor 2. (PAR2). in membrane trafficking of proteinase-Activated receptor 4. (PAR4). J Biol Chem 2012; 287: 16656-16669.
18. Yamamoto A, Nagano T, Takehara S, Hibi M, Aizawa S. Shisa promotes head formation through the inhibition of receptor protein maturation for the caudalizing factors, Wnt and FGF. Cell 2005; 120: 223-235.
19. Benke D. Mechanisms of GABAB receptor exocytosis, endocytosis, and degradation. Adv Pharmacol 2010; 58: 93-111.
20. Jones KA, Borowsky B, Tamm JA, Craig DA, Durkin MM, Dai M, et al. GABA(B). receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature 1998; 396: 674-679.
21. Kaupmann K, Malitschek B, Schuler V, Heid J, Froestl W, Beck P, et al. GABA(B)- receptor subtypes assemble into functional heteromeric complexes. Nature 1998; 396: 683-687.
22. White JH, Wise A, Main MJ, Green A, Fraser NJ, Disney GH, et al. Heterodimerization is required for the formation of a functional GABA(B). receptor. Nature 1998; 396: 679-682.
23. Vigot R, Barbieri S, Bräuner-Osborne H, Turecek R, Shigemoto R, Zhang YP, et al. Differential compartmentalization and distinct functions of GABAB receptor variants. Neuron 2006; 50: 589-601.
24. Couve A, Filippov AK, Connolly CN, Bettler B, Brown DA, Moss SJ. Intracellular retention of recombinant GABAB receptors. J Biol Chem 1998; 273: 26361-26367.
25. Margeta-Mitrovic M, Jan YN, Jan LY. A trafficking checkpoint controls GABA(B). receptor heterodimerization. Neuron 2000; 27: 97-106.
26. Pagano A, Rovelli G, Mosbacher J, Lohmann T, Duthey B, Stauffer D, et al. C-terminal interaction is essential for surface trafficking but not for heteromeric assembly of GABA(b). receptors. J Neurosci 2001; 21: 1189-1202.
27. Restituito S, Couve A, Bawagan H, Jourdain S, Pangalos MN, Calver AR, et al. Multiple motifs regulate the trafficking of GABA(B). receptors at distinct checkpoints within the secretory pathway. Mol Cell Neurosci 2005; 28: 747-756.
28. Kniazeff J, Galvez T, Labesse G, Pin JP. No ligand binding in the GB2 subunit of the GABA(B). receptor is required for activation and allosteric interaction between the subunits. J Neurosci 2002; 22: 7352-7361.
29. Margeta-Mitrovic M, Jan YN, Jan LY. Function of GB1and GB2 subunits in G protein coupling of GABA(B). receptors. Proc Natl Acad Sci USA 2001; 98: 14649-14654.
30. Robbins MJ, Calver AR, Filippov AK, Hirst WD, Russell RB, Wood MD, et al. GABA(B2). is essential for G-protein coupling of the GABA(B). receptor heterodimer. J Neurosci 2001; 21: 8043-8052.
31. Villemure JF, Adam L, Bevan NJ, Gearing K, Chenier S, Bouvier M. Subcellular distribution of GABA(B). receptor homo- and hetero-dimers. Biochem J 2005; 388: 47-55.
32. Laffray S, Bouali-Benazzouz R, Papon MA, Favereaux A, Jiang Y, Holm T, et al. Impairment of GABAB receptor dimer by endogenous 14-3-3zeta in chronic pain conditions. EMBO J 2012; 31: 3239-3251.
33. Maier PJ, Zemoura K, Acuna MA, Yevenes GE, Zeilhofer HU, Benke D. Ischemia-like oxygen and glucose deprivation mediates down-regulation of cell surface γ- aminobutyric acidB receptors via the endoplasmic reticulum. (ER). stress-Induced transcription factor CCAAT/enhancer-binding protein. (C/EBP)-homologous protein. (CHOP). J Biol Chem 2014; 289: 12896-12907.
34. Kantamneni S, Holman D, Wilkinson KA, Nishimune A, Henley JM. GISP increases neurotransmitter receptor stability by down-regulating ESCRT-mediated lysosomal degradation. Neurosci Lett 2009; 452: 106-110.
35. Abdul-Ghani M, Gougeon PY, Prosser DC, Da-Silva LF, Ngsee JK. PRA isoforms are targeted to distinct membrane compartments. J Biol Chem 2001; 276: 6225-6233.
36. Fo CS, Coleman CS, Wallick CJ, Vine AL, Bachmann AS. Genomic organization, expression profile, and characterization of the new protein PRA1 domain family, member 2. (PRAF2). Gene 2006; 371: 154-165.
37. Sivars U, Aivazian D, Pfeffer SR. Yip3 catalyses the dissociation of endosomal Rab- GDI complexes. Nature 2003; 425: 856-859.
38. Lin CI, Orlov I, Ruggiero AM, Dykes-Hoberg M, Lee A, Jackson M, et al. Modulation of the neuronal glutamate transporter EAAC1 by the interacting protein GTRAP3-18. Nature 2001; 410: 84-88.
39. Ruggiero AM, Liu Y, Vidensky S, Maier S, Jung E, Farhan H, et al. The endoplasmic reticulum exit of glutamate transporter is regulated by the inducible mammalian Yip6b/GTRAP3-18 protein. J Biol Chem 2008; 283: 6175-6183.
40. Schweneker M, Bachmann AS, Moelling K. JM4 is a four-transmembrane protein binding to the CCR5 receptor. FEBS Lett 2005; 579: 1751-1758.
41. Koomoa DL, Go RC, Wester K, Bachmann AS. Expression profile of PRAF2 in the human brain and enrichment in synaptic vesicles. Neurosci Lett 2008; 436: 171-176.
42. Borsics T, Lundberg E, Geerts D, Koomoa DL, Koster J, Wester K, et al. Subcellular distribution and expression of prenylated Rab acceptor 1 domain family, member 2. (PRAF2). in malignant glioma: influence on cell survival and migration. Cancer Sci 2010; 101: 1624-1631.
43. Petaja-Repo UE, Hogue M, Laperriere A, Walker P, Bouvier M. Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human delta opioid receptor. J Biol Chem 2000; 275: 13727-13736.
44. Galvez T, Duthey B, Kniazeff J, Blahos J, Rovelli G, Bettler B, et al. Allosteric interactions between GB1 and GB2 subunits are required for optimal GABA(B). receptor function. EMBO J 2001; 20: 2152-2159.
45. Marullo S, Bouvier M. Resonance energy transfer approaches in molecular pharmacology and beyond. Trends Pharmacol Sci 2007; 28: 362-365.
46. Achour L, Kamal M, Jockers R, Marullo S. Using quantitative BRET to assess G protein-coupled receptor homo- and heterodimerization. Methods Mol Biol 2011; 756: 183-200.
47. Pinard A, Seddik R, Bettler B. GABAB receptors: physiological functions and mechanisms of diversity. Adv Pharmacol 2010; 58: 231-255.
48. Cruz HG, Ivanova T, Lunn ML, Stoffel M, Slesinger PA, Luscher C. Bi-directional effects of GABA(B). receptor agonists on the mesolimbic dopamine system. Nat Neurosci 2004; 7: 153-159.
49. Koob GF, Swerdlow NR. The functional output of the mesolimbic dopamine system. Ann NY Acad Sci 1988; 537: 216-227.
50. Labouebe G, Lomazzi M, Cruz HG, Creton C, Lujan R, Li M, et al. RGS2 modulates coupling between GABAB receptors and GIRK channels in dopamine neurons of the ventral tegmental area. Nat Neurosci 2007; 10: 1559-1568.
51. Erhardt S, Mathe JM, Chergui K, Engberg G, Svensson TH. GABA(B). receptormediated modulation of the firing pattern of ventral tegmental area dopamine neurons in vivo. Naunyn Schmiedebergs Arch Pharmacol 2002; 365: 173-180.
52. SmoldersDe Klippel I, Sarre N, Ebinger S, Michotte G, Tonic Y. GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely moving rat. Eur J Physiol 1995; 284: 83-91.
53. Bartoletti M, Gubellini C, Ricci F, Gaiardi M. The GABAB agonist baclofen blocks the expression of sensitisation to the locomotor stimulant effect of amphetamine. Behav Pharmacol 2004; 15: 397-401.
54. Bartoletti M, Gubellini C, Ricci F, Gaiardi M. Baclofen blocks the development of sensitization to the locomotor stimulant effect of amphetamine. Behav Pharmacol 2005; 16: 553-558.
55. Zhou W, Mailloux AW, McGinty JF. Intracerebral baclofen administration decreases amphetamine-induced behavior and neuropeptide gene expression in the striatum. Neuropsychopharmacology 2005; 30: 880-890.
56. Schuler V, Luscher C, Blanchet C, Klix N, Sansig G, Klebs K, et al. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B). responses in mice lacking GABA(B(1)). Neuron 2001; 31: 47-58.
57. Pycock CJ. Turning behaviour in animals. Neuroscience 1980; 5: 461-514.
58. Koshikawa N. Role of the nucleus accumbens and the striatum in the production of turning behaviour in intact rats. Rev Neurosci 1994; 5: 331-346.
59. Kitamura M, Koshikawa N, Yoneshige N, Cools AR. Behavioural and neurochemical effects of cholinergic and dopaminergic agonists administered into the accumbal core and shell in rats. Neuropharmacology 1999; 38: 1397-1407.
60. Schwarting RK, Huston JP. Unilateral 6-hydroxydopamine lesions of meso-striatal dopamine neurons and their physiological sequelae. Prog Neurobiol 1996; 49: 215-266.
61. Gassmann M, Shaban H, Vigot R, Sansig G, Haller C, Barbieri S, et al. Redistribution of GABAB(1). protein and atypical GABAB responses in GABAB(2)-deficient mice. J Neurosci 2004; 24: 6086-6097.
62. Vacher CM, Gassmann M, Desrayaud S, Challet E, Bradaia A, Hoyer D, et al. Hyperdopaminergia and altered locomotor activity in GABAB1-deficient mice. J Neurochem 2006; 97: 979-991.
63. Mombereau C, Kaupmann K, Gassmann M, Bettler B, Van Der Putten H, Cryan JF. Altered anxiety and depression-related behavior in mice lacking GABAB(2). receptor subunits. Neuroreport 2005; 16: 307-310.
64. Colombo G, Melis S, Brunetti G, Serra S, Vacca G, Carai MA, et al. GABA(B). receptor inhibition causes locomotor stimulation in mice. Eur J Physiol 2001; 433: 101-104.
65. Moore EM, Boehm SL 2nd. Site-specific microinjection of baclofen into the anterior ventral tegmental area reduces binge-like ethanol intake in male C57BL/ 6J mice. Behav Neurosci 2009; 123: 555-563.
66. Spasic D, Raemaekers T, Dillen K, Declerck I, Baert V, Serneels L, et al. Rer1p competes with APH-1 for binding to nicastrin and regulates gammasecretase complex assembly in the early secretory pathway. J Cell Biol 2007; 176: 629-640.
67. Dwyer ND, Troemel ER, Sengupta P, Bargmann CI. Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-Associated protein. Cell 1998; 93: 455-466.
68. Metherell LA, Chapple JP, Cooray S, David A, Becker C, Ruschendorf F, et al. Mutations in MRAP, encoding a new interacting partner of the ACTH receptor, cause familial glucocorticoid deficiency type 2. Nat Genet 2005; 37: 166-170.
69. Donato R. Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1999; 1450: 191-231.
70. Alexander B, Warner-Schmidt J, Eriksson T, Tamminga C, Arango-Llievano M, Ghose S, et al. Reversal of depressed behaviors in mice by p11 gene therapy in the nucleus accumbens. Sci Transl Med 2010; 2: 54ra76.
71. Conn PM, Ulloa-Aguirre A, Ito J, Janovick JA. G protein-coupled receptor trafficking in health and disease: lessons learned to prepare for therapeutic mutant rescue in vivo. Pharmacol Rev 2007; 59: 225-250.
72. Valenzano KJ, Benjamin ER, René P, Bouvier MPharmacological chaperons: potential for the treatment of hereditary diseases caused by mutations in G protein-coupled receptors. In: Gilchrist A. (ed). GPCR Molecular Pharmacology and Drug targeting: Shifting Paradigms and New Directions. Wiley: Hoboken, NJ, USA, 2010, pp 460-491.