Isomerization of the proline in the M2-M3 linker is not required for activation of the human 5-HT3A receptor

Journal of Neurochemistry

Volumn 110, Issue 3, 2009, Pages 870-878

  Paulsen, Isabelle M ^a   Martin, Ian L ^b   Dunn, Susan M J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b ASTON UNIVERSITY   (United Kingdom)

Author keywords

5 hydroxytryptamine; 5 hydroxytryptamine type 3 receptor; 5 hydroxytryptamine type 3A receptor; Oocyte expression; Proline isomerization; Receptor activation

Indexed keywords

HISTIDINE; PROLINE; SEROTONIN 3A RECEPTOR; SEROTONIN TRANSPORTER; TRYPTOPHAN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ISOMERIZATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RECEPTOR DOWN REGULATION; SEQUENCE ANALYSIS; TRANSMEMBRANE HELIX;

AMINO ACID SUBSTITUTION; ANIMALS; FEMALE; HISTIDINE; HUMANS; ISOMERISM; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROLINE; PROTEIN SUBUNITS; RECEPTORS, SEROTONIN, 5-HT3; SEROTONIN; TRYPTOPHAN; XENOPUS LAEVIS;

EID: 67650470848     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06180.x     Document Type: Article

References (50)

1. Akk G. Auerbach A. (1999) Activation of muscle nicotinic acetylcholine receptor channels by nicotinic and muscarinic agonists. Brit. J. Pharmacol. 128, 1467 1476.
2. Brejc K., van Dijk W. J., Klaassen R., Schuurmans M., van der Oost J., Smit A. B. Sixma T. K. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411, 269 276. (Pubitemid 32467026)
3. 3A). J. Physiol. 507, 653 666.
4. A ion channel protein. J. Mol. Graph. Model. 25, 721 730. (Pubitemid 46177685)
5. Celie P. H., van Rossum-Fikkert S. E., van Dijk W. J., Brejc K., Smit A. B. Sixma T. K. (2004) Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41, 907 914. (Pubitemid 38429734)
6. Celie P. H., Klaassen R. V., van Rossum-Fikkert S. E., van Elk R., van Nierop P., Smit A. B. Sixma T. K. (2005a) Crystal structure of acetylcholine-binding protein from Bulinus truncatus reveals the conserved structural scaffold and sites of variation in nicotinic acetylcholine receptors. J. Biol. Chem. 280, 26457 26466. (Pubitemid 41022242)
7. Celie P. H., Kasheverov I. E., Mordvintsev D. Y. et al. (2005b) Crystal structure of nicotinic acetylcholine receptor homolog AChBP in complex with an alpha-conotoxin Pn1A variant. Nat. Struct. Mol. Biol. 12, 582 588. (Pubitemid 40980807)
8. a hydrogen bond in prolyl peptides. J. Am. Chem. Soc. 120, 10660 10668. (Pubitemid 28498811)
9. Czajkowski C. (2005) Neurobiology: triggers for channel opening. Nature 438, 167 168. (Pubitemid 41599857)
10. 3B subunit is a major determinant of serotonin-receptor function. Nature 397, 359 363.
11. Eiselé J.-L., Bertrand S., Galzi J.-L., Devillers-Thiéry A., Changeux J.-P. Bertrand D. (1993) Chimaeric nicotinic-serotonergic receptor combines distinct ligand binding and channel specificities. Nature 366, 479 483.
12. Ernst M., Brauchert D., Boresch S. Sieghart W. (2003) Comparative modelling of GABA(A) receptors: limits, insights, future developments. Neuroscience 119, 933 943. (Pubitemid 36776445)
13. 3 receptor stably expressed in HEK 293 cells. Brit. J. Pharmacol. 114, 1211 1221.
14. Grathwohl C. Wutrich K. (1981) Nmr studies of the rates of proline cis-trans isomerization in oligopeptides. Biopolymers 20, 2623 2633.
15. Hansen S. B. Taylor P. (2007) Galanthamine and non-competitive inhibitor binding to ACh-binding protein: evidence for a binding site on non-alpha-subunit interfaces of heteromeric neuronal nicotinic receptors. J. Mol. Biol. 369, 895 901. (Pubitemid 46754061)
16. Hansen S. B., Sulzenbacher G., Huxford T., Marchot P., Taylor P. Bourne Y. (2005) Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBO J. 24, 3635 3646. (Pubitemid 41509370)
17. 2+. J. Physiol. 568.2, 381 396. (Pubitemid 41555446)
18. Ihara M., Okajima T., Yamashita A. et al. (2008) Crystal structures of Lymnaea stagnalis AChBP in complex with neonicotinoid insecticides imidacloprid and clothianidin. Invert Neurosci., 8, 71 81.
19. Jabs A., Weiss M. S. Hilgenfeld R. (1999) Non-proline cis peptide bonds in proteins. J. Mol. Biol. 286, 291 304. (Pubitemid 29078413)
20. 3 receptor channel. Ann. Rev. Physiol. 57, 447 468.
21. Kash T. L., Jenkins A., Kelley J. C., Trudell J. R. Harrison N. L. (2003) Coupling of agonist binding to channel gating in the GABA(A) receptor. Nature 421, 272 275. (Pubitemid 36139131)
22. Lee W. Y. Sine S. M. (2005) Principal pathway coupling agonist binding to channel gating in nicotinic receptors. Nature 438, 243 247. (Pubitemid 41599878)
23. Lee W. Y., Free C. R. Sine S. M. (2008) Nicotinic receptor interloop proline anchors β1-β2 and Cys loop in coupling agonist binding to channel gating. J. Gen. Physiol. 132, 265 278.
24. Lester H. A., Dibas M. I., Dahan D. S., Leite J. F. Dougherty D. A. (2004) Cys-loop receptors: new twists and turns. Trends Neurosci. 27, 329 336. (Pubitemid 38692414)
25. Lummis S. C., Beene D. L., Lee L. W, Lester H. A., Broadhurst R. W. Dougherty D. A. (2005) Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature 438, 248 252. (Pubitemid 41599879)
26. 3 receptor, a serotonin-gated ion channel. Science 254, 432 437. (Pubitemid 21917361)
27. 3 receptor transiently expressed in HEK 293 cells. Amino Acids 17, 243 255. (Pubitemid 30113757)
28. Mokrab Y., Bavro V. N., Mizuguchi K., Todorov N. P., Martin I. L., Dunn S. M. J., Chan S. L. Chau P.-L. (2007) Exploring ligand recognition and ion flow in comparative models of the human GABA type A receptor. J. Mol. Graph. Model. 26, 760 774. (Pubitemid 47628844)
29. 3E. Mol. Pharmacol. 72, 8 17. (Pubitemid 46998520)
30. A receptor examined using Brownian dynamics. Biophys. J. 88, 3286 3299. (Pubitemid 40586580)
31. Pal D. Chakrabarti P. (1999) Cis peptide bonds in proteins: residues involved, their conformations, interactions and locations. J. Mol. Biol. 294, 271 288.
32. 3 receptor-induced currents in N1E-115 neuroblastoma cells. Eur. J. Pharmacol. 151, 491 495. (Pubitemid 18202068)
33. 3 receptor: a model ligand-gated ion channel (review). Mol. Membr. Biol. 19, 11 26. (Pubitemid 34407954)
34. 3 receptor agonist-binding residues using homology modeling. Biophys. J. 84, 2338 2344. (Pubitemid 36373556)
35. Shi T., Spain S. M. Rabenstein D. L. (2003) Unexpectedly fast cis/trans isomerization of Xaa-Pro peptide bonds in disulfide-constrained cyclic peptides. J. Am. Chem. Soc. 126, 790 796. (Pubitemid 38114362)
36. Sine S. M. Engel A. G. (2006) Recent advances in Cys-loop receptor structure and function. Nature 440, 448 455.
37. +-coupled nucleotide transporter (hCNT1) produced in Xenopus oocytes. J. Physiol. 58, 807 823. (Pubitemid 39199106)
38. 3A receptor kinetics: Interpretation within an allosteric kinetic model. J. Neurosci. 27, 13151 13160. (Pubitemid 350220480)
39. Song J., Burrage K., Yuan Z. Huber T. (2006) Prediction of cis/trans isomerization in proteins using PSI-BLAST profiles and secondary structure information. BMC Bioinformatics 7, 124 133.
40. Stewart D. E., Sarkar A. Wampler J. E. (1990) Occurrence and role of cis peptide bonds in protein structures. J. Mol. Biol. 214, 253 260. (Pubitemid 20231222)
41. Sui Q., Borchardt D. Rabenstein D. L. (2007) Kinetics and equilibria of cis/trans isomerization of backbone amide bonds in peptoids. J. Am. Chem. Soc. 129, 12042 12048. (Pubitemid 47512033)
42. 3 receptor binding and function. Neuropharmacology 56, 285 291.
43. A alpha1 receptor using three crystal structures as templates. J. Mol. Graph. Model. 23, 39 49. (Pubitemid 39141244)
44. Ulens C., Hogg R. C., Celie P. H., Bertrand D., Tsetlin V., Smit A. B. Sixma T. K. (2006) Structural determinants of selective alpha-conotoxin binding to a nicotinic acetylcholine receptor homolog AChBP. Proc. Natl Acad. Sci. USA 103, 3615 3620. (Pubitemid 43376604)
45. Unwin N. (1993) Nicotinic acetylcholine receptor at 9 Å resolution. J. Mol. Biol. 229, 1101 1124.
46. Unwin N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J. Mol. Biol. 346, 967 989. (Pubitemid 40215523)
47. Valenzuela C. F., Weign P., Yguerabide J. Johnson D. A. (1994) Transverse distance between the membrane and the agonist binding sites on the Torpedo acetylcholine receptor: a fluorescence study. Biophys. J. 66, 674 682. (Pubitemid 24082986)
48. Xiu X., Hanek A. P., Wang J., Lester H. A. Dougherty D. A. (2005) A unified view of the role of electrostatic interactions in modulating the gating of Cys loop receptors. J. Biol. Chem. 280, 41655 41666. (Pubitemid 41832228)
49. 3 receptor. Brain Res. 533, 46 52. (Pubitemid 20375796)
50. Yuan X., Werner J. M., Knott V., Handford P. A., Campbell I. D. Downing K. (1998) Effects of proline cis-trans isomerization on TB domain secondary structure. Protein Sci. 7, 2127 2135. (Pubitemid 28495799)