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Original

Trafficking of 5-HT3 and GABAA receptors (Review)

Pages 293-301 | Received 10 Oct 2007, Published online: 09 Jul 2009

References

  • Connolly CN, Wafford KA. The Cys-loop superfamily of ligand-gated ion channels: the impact of receptor structure on function. Biochem Soc Trans 2004; 32: 529–534
  • Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, van Der Oost J, Smit AB, Sixma TK. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 2001; 411: 269–276
  • Thompson AJ, Lummis SC. 5-HT3 receptors. Curr pharm design 2006; 12: 3615–3630
  • Brady CA, Dover TJ, Massoura AN, Princivalle AP, Hope AG, Barnes NM. Identification of 5-HT3A and 5-HT3B receptor subunits in human hippocampus. Neuropharm 2007; 52: 1284–1290
  • Boyd GW, Low P, Dunlop JI, Robertson LA, Vardy A, Lambert JJ, Peters JA, Connolly CN. Assembly and cell surface expression of homomeric and heteromeric 5-HT3 receptors: the role of oligomerization and chaperone proteins. Mol Cell Neuro 2002; 21: 38–50
  • Barrera NP, Herbert P, Henderson RM, Martin IL, Edwardson JM. Atomic force microscopy reveals the stoichiometry and subunit arrangement of 5-HT3 receptors. Proc Natl Acad Sci (USA) 2005; 102: 12595–12600
  • Niesler B, Walstab J, Combrink S, Moller D, Kapeller J, Rietdorf J, Bonisch H, Gothert M, Rappold G, Bruss M. Characterization of the novel human serotonin receptor subunits 5-HT3C,5-HT3D, and 5-HT3E. Mol Pharm 2007; 72: 8–17
  • Quirk PL, Rao S, Roth BL, Siegel RE. Three putative N-glycosylation sites within the murine 5-HT3A receptor sequence affect plasma membrane targeting, ligand binding, and calcium influx in heterologous mammalian cells. J Neuro Res 2004; 77: 498–506
  • Monk SA, Williams JM, Hope AG, Barnes NM. Identification and importance of N-glycosylation of the human 5-hydroxytryptamine3A receptor subunit. Biochem Pharmacol 2004; 68: 1787–1796
  • Boyd GW, Doward AI, Kirkness EF, Millar NS, Connolly CN. Cell surface expression of 5-hydroxytryptamine type 3 receptors is controlled by an endoplasmic reticulum retention signal. J Biol Chem 2003; 278: 27681–27687
  • Connolly CN, Uren JM, Thomas P, Gorrie GH, Gibson A, Smart TG, Moss SJ. Subcellular localization and endocytosis of homomeric gamma2 subunit splice variants of gamma-aminobutyric acid type A receptors. Mol Cell Neuro 1999; 13: 259–271
  • Connolly CN, Krishek BJ, McDonald BJ, Smart TG, Moss SJ. Assembly and cell surface expression of heteromeric and homomeric gamma-aminobutyric acid type A receptors. J Biol Chem 1996; 271: 89–96
  • Cheng A, McDonald NA, Connolly CN. Cell surface expression of 5-hydroxytryptamine type 3 receptors is promoted by RIC-3. J Biol Chem 2005; 280: 22502–22507
  • Millar NS. 2007. RIC-3: A nicotinic acetylcholine receptor chaperone. Brit J Pharmacol Feb 4, [epub ahead of print].
  • Cheng A, Bollan KA, Greenwood SM, Irving AJ, Connolly CN. Differential subcellular localization of RIC-3 isoforms and their role in determining 5-HT3 receptor composition. J Biol Chem 2007; 282: 26158–26166
  • Lansdell SJ, Gee VJ, Harkness PC, Doward AI, Baker ER, Gibb AJ, Millar NS. RIC-3 enhances functional expression of multiple nicotinic acetylcholine receptor subtypes in mammalian cells. Mol Pharm 2005; 68: 1431–1438
  • Halevi S, Yassin L, Eshel M, Sala F, Sala S, Criado M, Treinin M. Conservation within the RIC-3 gene family. Effectors of mammalian nicotinic acetylcholine receptor expression. J Biol Chem 2003; 278: 34411–34417
  • Lansdell S, Collins T, Yabe A, Gee VJ, Gibb AJ, Millar NS. 2008. Host-cell specific effects of the nicotinic receptor-associated protein RIC-3 revealed by a comparison of human and drosophila RIC-3 homologues. J Neurochem Jan 18, [epub ahead of print].
  • Helekar SA, Patrick J. Peptidyl prolyl cis-trans isomerase activity of cyclophilin A in functional homo-oligomeric receptor expression. Proc Natl Acad Sci (USA) 1997; 94: 5432–5437
  • Ilegems E, Pick HM, Deluz C, Kellenberger S, Vogel H. Noninvasive imaging of 5-HT3 receptor trafficking in live cells: from biosynthesis to endocytosis. J Biol Chem 2004; 279: 53346–53352
  • Emerit MB, Doucet E, Darmon M, Hamon M. Native and cloned 5-HT(3A)(S) receptors are anchored to F-actin in clonal cells and neurons. Mol Cell Neuro 2002; 20: 110–124
  • Green WN, Millar NS. Ion-channel assembly. Trends Neorosci. 1995; 18: 280–287
  • Grailhe R, de Carvalho LP, Paas Y, Le Poupon C, Soudant M, Bregestovski P, Changeux JP, Corringer PJ. Distinct subcellular targeting of fluorescent nicotinic alpha 3 beta 4 and serotoninergic 5-HT3A receptors in hippocampal neurons. Eur J Neurosci 2004; 19: 855–862
  • Koyama S, Matsumoto N, Kubo C, Akaike N. Presynaptic 5-HT3 receptor-mediated modulation of synaptic GABA release in the mechanically dissociated rat amygdala neurons. J Physiol 2000; 529: 373–383
  • Katsurabayashi S, Kubota H, Tokutomi N, Akaike N. A distinct distribution of functional presynaptic 5-HT receptor subtypes on GABAergic nerve terminals projecting to single hippocampal CA1 pyramidal neurons. Neuropharm 2003; 44: 1022–1030
  • Conte D, Legg ED, McCourt AC, Silajdzic E, Nagy GG, Maxwell DJ. Transmitter content, origins and connections of axons in the spinal cord that possess the serotonin (5-hydroxytryptamine) 3 receptor. Neuroscience 2005; 134: 165–173
  • Huang J, Spier AD, Pickel VM. 5-HT3A receptor subunits in the rat medial nucleus of the solitary tract: subcellular distribution and relation to the serotonin transporter. Brain Res 2004; 1028: 156–169
  • Atlason PT, Garside ML, Meddows E, Whiting P, McIlhinney RA. N-Methyl-D-aspartate (NMDA) receptor subunit NR1 forms the substrate for oligomeric assembly of the NMDA receptor. J Biol Chem 2007; 282: 25299–25307
  • Greger IH, Esteban JA. AMPA receptor biogenesis and trafficking. Curr Opin Neurobiol 2007; 17: 289–297
  • Guignet EG, Segura JM, Hovius R, Vogel H. Repetitive reversible labeling of proteins at polyhistidine sequences for single-molecule imaging in live cells. Chemphyschem 2007; 8: 1221–1227
  • Freeman SL, Glatzle J, Robin CS, Valdellon M, Sternini C, Sharp JW, Raybould HE. Ligand-induced 5-HT3 receptor internalization in enteric neurons in rat ileum. Gastroenterol 2006; 131: 97–107
  • Sun H, Hu XQ, Moradel EM, Weight FF, Zhang L. Modulation of 5-HT3 receptor-mediated response and trafficking by activation of protein kinase C. J Biol Chem 2003; 278: 34150–34157
  • Leidenheimer NJ. Regulation of excitation by GABA(A) receptor internalization. Res Prob Cell Diff 2008; 44: 1–28
  • Bollan KA, Baur R, Hales TG, Sigel E, Connolly CN. 2008. The promiscuous role of the epsilon subunit in GABAA receptor biogenesis. Mol Cell Neuro Dec 15, [epub ahead of print].
  • Jones BL, Henderson LP. Trafficking and potential assembly patterns of epsilon-containing GABAA receptors. J Neurochem 2007; 103: 1258–1271
  • Bonnert TP, McKernan RM, Farrar S, le Bourdelles B, Heavens RP, Smith DW, Hewson L, Rigby MR, Sirinathsinghji DJ, Brown N, Wafford KA, Whiting PJ. theta, a novel gamma-aminobutyric acid type A receptor subunit. Proc Natl Acad Sci (USA) 1999; 96: 9891–9896
  • Chen ZW, Olsen RW. GABAA receptor associated proteins: a key factor regulating GABAA receptor function. J Neurochem 2007; 100: 279–294
  • Kittler JT, Rostaing P, Schiavo G, Fritschy JM, Olsen R, Triller A, Moss SJ. The subcellular distribution of GABARAP and its ability to interact with NSF suggest a role for this protein in the intracellular transport of GABA(A) receptors. Mol Cell Neuro 2001; 18: 13–25
  • Boileau AJ, Pearce RA, Czajkowski C. Tandem subunits effectively constrain GABAA receptor stoichiometry and recapitulate receptor kinetics but are insensitive to GABAA receptor-associated protein. J Neurosci 2005; 25: 11219–11230
  • Kanematsu T, Jang IS, Yamaguchi T, Nagahama H, Yoshimura K, Hidaka K, Matsuda M, Takeuchi H, Misumi Y, Nakayama K, Yamamoto T, Akaike N, Hirata M, Nakayama K. Role of the PLC-related, catalytically inactive protein p130 in GABA(A) receptor function. EMBO J 2002; 21: 1004–1011
  • Li RW, Serwanski DR, Miralles CP, Li X, Charych E, Riquelme R, Huganir RL., de Blas AL. GRIP1 in GABAergic synapses. J Comp Neurol 2005; 488: 11–27
  • Bedford FK, Kittler JT, Muller E, Thomas P, Uren JM, Merlo D, Wisden W, Triller A, Smart TG, Moss SJ. GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat Neuro 2001; 4: 908–916
  • Keller CA, Yuan X, Panzanelli P, Martin ML, Alldred M, Sassoe-Pognetto M, Luscher B. The gamma2 subunit of GABA(A) receptors is a substrate for palmitoylation by GODZ. J Neurosci 2004; 24: 5881–5891
  • Fang C, Deng L, Keller CA, Fukata M, Fukata Y, Chen G, Luscher B. GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J Neurosci 2006; 26: 12758–12768
  • Rathenberg J, Kittler JT, Moss SJ. Palmitoylation regulates the clustering and cell surface stability of GABAA receptors. Mol Cell Neuro 2004; 26: 251–257
  • Drisdel RC, Manzana E, Green WN. The role of palmitoylation in functional expression of nicotinic alpha7 receptors. J Neurosci 2004; 24: 10502–10510
  • Charych EI, Yu W, Miralles CP, Serwanski DR, Li X, Rubio M, De Blas AL. The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the beta subunits of the GABA receptors. J Neurochem 2004; 90: 173–189
  • Brickley K, Smith MJ, Beck M, Stephenson FA. GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J Biol Chem 2005; 280: 14723–14732
  • Beck M, Brickley K, Wilkinson HL, Sharma S, Smith M, Chazot PL, Pollard S, Stephenson FA. Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J Biol Chem 2002; 277: 30079–30090
  • Baer K, Essrich C, Benson JA, Benke D, Bluethmann H, Fritschy JM, Luscher B. Postsynaptic clustering of gamma-aminobutyric acid type A receptors by the gamma3 subunit in vivo. Proc Natl Acad Sci (USA) 1999; 96: 12860–12865
  • Nusser Z, Sieghart W, Somogyi P. Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 1998; 18: 1693–1703
  • Anagnostaras SG, Craske MG, Fanselow MS. Anxiety: at the intersection of genes and experience. Nat Neuro 1999; 2: 780–782
  • Michels G, Moss SJ. GABAA receptors: properties and trafficking. Crit Rev Biochem Mol Biol 2007; 42: 3–14
  • Kneussel M, Loebrich S. Trafficking and synaptic anchoring of ionotropic inhibitory neurotransmitter receptors. Biology of the cell/under the auspices of the E Cell Biol Org 2007; 99: 297–309
  • Thomas P, Mortensen M, Hosie AM, Smart TG. Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat Neuro 2005; 8: 889–897
  • Jacob TC, Bogdanov YD, Magnus C, Saliba RS, Kittler JT, Haydon PG, Moss SJ. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci 2005; 25: 10469–10478
  • Bogdanov Y, Michels G, Armstrong-Gold C, Haydon PG, Lindstrom J, Pangalos M, Moss SJ. Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J 2006; 25: 4381–4389
  • Connolly C N, Kittler JT, Thomas P, Uren JM, Brandon NJ, Smart TG, Moss SJ. Cell surface stability of gamma-aminobutyric acid type A receptors. Dependence on protein kinase C activity and subunit composition. J Biol Chem 1999; 274: 36565–36572
  • Kanematsu T, Fujii M, Mizokami A, Kittler JT, Nabekura J, Moss SJ, Hirata M. Phospholipase C-related inactive protein is implicated in the constitutive internalization of GABAA receptors mediated by clathrin and AP2 adaptor complex. J Neurochem 2007; 101: 898–905
  • Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia-Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z, Moss SJ. Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci (USA) 2005; 102: 14871–14876
  • Herring D, Huang R, Singh M, Dillon GH, Leidenheimer NJ. PKC modulation of GABAA receptor endocytosis and function is inhibited by mutation of a dileucine motif within the receptor beta 2 subunit. Neuropharm 2005; 48: 181–194
  • Kittler JT, Thomas P, Tretter V, Bogdanov YD, Haucke V, Smart TG, Moss SJ. Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc Natl Acad Sci (USA) 2004; 101: 12736–12741
  • Goto H, Terunuma M, Kanematsu T, Misumi Y, Moss SJ, Hirata M. Direct interaction of N-ethylmaleimide-sensitive factor with GABA(A) receptor beta subunits. Mol Cell Neuro 2005; 30: 197–206
  • Blair RE, Sombati S, Lawrence DC, McCay BD, DeLorenzo RJ. Epileptogenesis causes acute and chronic increases in GABAA receptor endocytosis that contributes to the induction and maintenance of seizures in the hippocampal culture model of acquired epilepsy. J Pharm Exp Ther 2004; 310: 871–880
  • Goodkin HP, Sun C, Yeh JL, Mangan PS, Kapur J. GABA(A) receptor internalization during seizures. Epilepsia (Suppl.) 5 2007; 48: 109–113
  • Kang JQ, Shen W, Macdonald RL. Why does fever trigger febrile seizures? GABAA receptor gamma2 subunit mutations associated with idiopathic generalized epilepsies have temperature-dependent trafficking deficiencies. J Neurosci 2006; 26: 2590–2597
  • Naylor DE, Liu H, Wasterlain CG. Trafficking of GABA(A) receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J Neurosci 2005; 25: 7724–7733
  • Mielke JG, Wang YT. Insulin exerts neuroprotection by counteracting the decrease in cell-surface GABA receptors following oxygen-glucose deprivation in cultured cortical neurons. J Neurochem 2005; 92: 103–113

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