A conserved cysteine residue in the third transmembrane domain is essential for homomeric 5-HT3 receptor function

Journal of Physiology

Volumn 588, Issue 4, 2010, Pages 603-616

  Wu, Dai Fei ^a   Othman, Nidaa A ^a   Sharp, Douglas ^a   Mahendra, Arjun ^a   Deeb, Tarek Z ^a   Hales, Tim G ^a,b  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALANINE; CYSTEINE; EPITOPE; GLYCINE RECEPTOR; NICOTINIC RECEPTOR; SEROTONIN 3A RECEPTOR; SEROTONIN 3B RECEPTOR; GLYCINE; LEUCINE; MEMBRANE PROTEIN; SERINE; SEROTONIN 3 RECEPTOR; THREONINE;

AMINO ACID SEQUENCE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNALIZATION; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; WESTERN BLOTTING; CELL SURFACE; EMBRYO; RECEPTOR BINDING; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; WHOLE CELL; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CONSERVED SEQUENCE; CYSTEINE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PATCH-CLAMP TECHNIQUES; RECEPTORS, NICOTINIC; RECEPTORS, SEROTONIN, 5-HT3; SEROTONIN;

EID: 77949522347     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.181719     Document Type: Article

References (44)

1. Barnes NM, Hales TG, Lummis SC, Peters JA. The 5-HT3 receptor - the relationship between structure and function. Neuropharmacology 2009, 56:273-284.
2. Bocquet N, Nury H, Baaden M, Le Poupon C, Changeux JP, Delarue M, Corringer PJ. X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 2009, 457:111-114.
3. Bocquet N, Prado de Carvalho L, Cartaud J, Neyton J, Le Poupon C, Taly A, Grutter T, Changeux JP, Corringer PJ. A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family. Nature 2007, 445:116-119.
4. Bollan K, Robertson LA, Tang H, Connolly CN. Multiple assembly signals in gamma-aminobutyric acid (type A) receptor subunits combine to drive receptor construction and composition. Biochem Soc Trans 2003, 31:875-879.
5. 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.
6. 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 Neurosci 2002, 21:38-50.
7. Cadugan DJ, Auerbach A. Conformational dynamics of the αM3 transmembrane helix during acetylcholine receptor channel gating. Biophys J 2007, 93:859-865.
8. Campos-Caro A, Rovira JC, Vicente-Agullo F, Ballesta JJ, Sala S, Criado M, Sala F. Role of the putative transmembrane segment M3 in gating of neuronal nicotinic receptors. Biochemistry 1997, 36:2709-2715.
9. Cheng Y, Prusoff WH. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50% inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 1973, 22:3099-3108.
10. Cruz-Martin A, Mercado JL, Rojas LV, McNamee MG, Lasalde-Dominicci JA. Tryptophan substitutions at lipid-exposed positions of the gamma M3 transmembrane domain increase the macroscopic ionic current response of the Torpedo californica nicotinic acetylcholine receptor. J Membr Biol 2001, 183:61-70.
11. Davies PA, Kirkness EF, Hales TG. Modulation by general anaesthetics of rat GABAA receptors comprised of α1β3 and β3 subunits expressed in human embryonic kidney 293 cells. Br J Pharmacol 1997, 120:899-909.
12. Davies PA, Kirkness EF, Hales TG. Evidence for the formation of functionally distinct αβγe{open} GABAA receptors. J Physiol 2001, 537:101-113.
13. Davies PA, Pistis M, Hanna MC, Peters JA, Lambert JJ, Hales TG, Kirkness EF. The 5-HT3B subunit is a major determinant of serotonin-receptor function. Nature 1999, 397:359-363.
14. Davies PA, Wang W, Hales TG, Kirkness EF. A novel class of ligand-gated ion channel is activated by Zn2+. J Biol Chem 2003, 278:712-717.
15. De Rosa MJ, Corradi J, Bouzat C. Subunit-selective role of the M3 transmembrane domain of the nicotinic acetylcholine receptor in channel gating. Biochim Biophys Acta 2008, 1778:521-529.
16. De Rosa MJ, Rayes D, Spitzmaul G, Bouzat C. Nicotinic receptor M3 transmembrane domain: Position 8¢ contributes to channel gating. Mol Pharmacol 2002, 62:406-414.
17. Deeb TZ, Carland JE, Cooper MA, Livesey MR, Lambert JJ, Peters JA, Hales TG. Dynamic modification of a mutant cytoplasmic cysteine residue modulates the conductance of the human 5-HT3A receptor. J Biol Chem 2007, 282:6172-6182.
18. Fritschy JM, Harvey RJ, Schwarz G. Gephyrin: Where do we stand, where do we go?. Trends Neurosci 2008, 31:257-264.
19. Gotti C, Moretti M, Gaimarri A, Zanardi A, Clementi F, Zoli M. Heterogeneity and complexity of native brain nicotinic receptors. Biochem Pharmacol 2007, 74:1102-1111.
20. Guzmán GR, Santiago J, Ricardo A, Martí-Arbona R, Rojas LV, Lasalde-Dominicci JA. Tryptophan scanning mutagenesis in the αM3 transmembrane domain of the Torpedo californica acetylcholine receptor: functional and structural implications. Biochemistry 2003, 42:12243-12250.
21. Hanna MC, Davies PA, Hales TG, Kirkness EF. Evidence for expression of heteromeric serotonin 5-HT3 receptors in rodents. J Neurochem 2000, 75:240-247.
22. Hilf RJ, Dutzler R. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 2008, 452:375-379.
23. Hilf RJ, Dutzler R. Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 2009, 457:115-118.
24. 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.
25. Kilpatrick GJ, Jones BJ, Tyers MB. Identification and distribution of 5-HT3 receptors in rat brain using radioligand binding. Nature 1987, 330:746-748.
26. Koch T, Wu DF, Yang LQ, Brandenburg LO, Hollt V. Role of phospholipase D2 in the agonist-induced and constitutive endocytosis of G-protein coupled receptors. J Neurochem 2006, 97:365-372.
27. Lester HA, Dibas MI, Dahan DS, Leite JF, Dougherty DA. Cys-loop receptors: New twists and turns. Trends Neurosci 2004, 27:329-336.
28. Liang YJ, Wu DF, Stumm R, Hollt V, Koch T. Membrane glycoprotein M6A promotes mu-opioid receptor endocytosis and facilitates receptor sorting into the recycling pathway. Cell Res 2008, 18:768-779.
29. Liang YJ, Wu DF, Yang LQ, Hollt V, Koch T. Interaction of the μ-opioid receptor with synaptophysin influences receptor trafficking and signalling. Mol Pharmacol 2007, 71:123-131.
30. Lugovskoy AA, Maslennikov IV, Utkin YN, Tsetlin VI, Cohen JB, Arseniev AS. Spatial structure of the M3 transmembrane segment of the nicotinic acetylcholine receptor α subunit. Eur J Biochem 1998, 255:455-461.
31. Maricq AV, Peterson AS, Brake AJ, Myers RM, Julius D. Primary structure and functional expression of the 5HT3 receptor, a serotonin-gated ion channel. Science 1991, 254:432-437.
32. McKernan RM, Whiting PJ. Which GABAA-receptor subtypes really occur in the brain?. Trends Neurosci 1996, 19:139-143.
33. Mitchell EA, Herd MB, Gunn BG, Lambert JJ, Belelli D. Neurosteroid modulation of GABAA receptors: Molecular determinants and significance in health and disease. Neurochem Int 2008, 52:588-595.
34. Morton RA, Luo G, Davis MI, Hales TG, Lovinger DM. Fluorophore-assisted light inactivation of recombinant 5-HT3A receptors. 2008 Abstract Viewer/Itinerary Planner 2008, Programme No. 330.6/D13. Society for Neuroscience, Washington, DC
35. Otero-Cruz JD, Baez-Pagan CA, Caraballo-Gonzalez IM, Lasalde-Dominicci JA. Tryptophan-scanning mutagenesis in the αM3 transmembrane domain of the muscle-type acetylcholine receptor. A spring model revealed. J Biol Chem 2007, 282:9162-9171.
36. Otero-Cruz JD, Torres-Nunez DA, Baez-Pagan CA, Lasalde-Dominicci JA. Fourier transform coupled to tryptophan-scanning mutagenesis: Lessons from its application to the prediction of secondary structure in the acetylcholine receptor lipid-exposed transmembrane domains. Biochim Biophys Acta 2008, 1784:1200-1207.
37. Reeves DC, Lummis SC. The molecular basis of the structure and function of the 5-HT3 receptor: A model ligand-gated ion channel (review). Mol Membr Biol 2002, 19:11-26.
38. Rudolph U, Mohler H. Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anaesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 2004, 44:475-498.
39. Stewart A, Davies PA, Kirkness EF, Safa P, Hales TG. Introduction of the 5-HT3B subunit alters the functional properties of 5-HT3 receptors native to neuroblastoma cells. Neuropharmacology 2003, 44:214-223.
40. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J Mol Biol 2005, 346:967-989.
41. Wang HL, Milone M, Ohno K, Shen XM, Tsujino A, Batocchi AP, Tonali P, Brengman J, Engel AG, Sine SM. Acetylcholine receptor M3 domain: Stereochemical and volume contributions to channel gating. Nat Neurosci 1999, 2:226-233.
42. Wu DF, Koch T, Liang YJ, Stumm R, Schulz S, Schroder H, Hollt V. Membrane glycoprotein M6a interacts with the μ-opioid receptor and facilitates receptor endocytosis and recycling. J Biol Chem 2007, 282:22239-22247.
43. Wu DF, Yang LQ, Goschke A, Stumm R, Brandenburg LO, Liang YJ, Hollt V, Koch T. Role of receptor internalization in the agonist-induced desensitization of cannabinoid type 1 receptors. J Neurochem 2008, 104:1132-1143.
44. Xiong W, Hosoi M, Koo BN, Zhang L. Anandamide inhibition of 5-HT3A receptors varies with receptor density and desensitization. Mol Pharmacol 2008, 73:314-322.