Amino acid coevolution reveals three-dimensional structure and functional domains of insect odorant receptors

Nature Communications

Volumn 6, Issue , 2015, Pages

  Hopf, Thomas A ^a,b   Morinaga, Satoshi ^c,d   Ihara, Sayoko ^c,d   Touhara, Kazushige ^c,d   Marks, Debora S ^a   Benton, Richard ^e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LIGAND GATED ION CHANNEL; RECEPTOR; AMINO ACID; OLFACTORY RECEPTOR;

AMINO ACID; COEVOLUTION; INSECT; NEUROLOGY; PROTEIN; THREE-DIMENSIONAL MODELING;

AMINO ACID ANALYSIS; ARTICLE; COEVOLUTION; INSECT; MOLECULAR MODEL; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; OLFACTORY RECEPTOR; XENOPUS;

HEXAPODA;

AMINO ACIDS; ANIMALS; EVOLUTION, MOLECULAR; INSECTS; RECEPTORS, ODORANT; XENOPUS;

EID: 84923079683     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7077     Document Type: Article

References (55)

1. Su, C. Y., Menuz, K. & Carlson, J. R. Olfactory perception: receptors, cells, and circuits. Cell 139, 45-59 (2009).
2. Degennaro, M. et al. orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature 498, 487-491 (2013).
3. Nakagawa, T., Sakurai, T., Nishioka, T. & Touhara, K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307, 1638-1642 (2005).
4. Stensmyr, M. C. et al. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345-1357 (2012).
5. Benton, R. Chemical sensing in Drosophila. Curr. Opin. Neurobiol. 18, 357-363 (2008).
6. Nakagawa, T. & Vosshall, L. B. Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr. Opin. Neurobiol. 19, 284-292 (2009).
7. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A. & Axel, R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-736 (1999).
8. Clyne, P. J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327-338 (1999).
9. Hill, C. A. et al. G protein-coupled receptors in Anopheles gambiae. Science 298, 176-178 (2002).
10. Sakurai, T. et al. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc. Natl Acad. Sci. USA 101, 16653-16658 (2004).
11. Wicher, D. et al. Drosophila odorant receptors are both ligand-gated and cyclicnucleotide-activated cation channels. Nature 452, 1007-1011 (2008).
12. Stengl, M. & Funk, N. W. The role of the coreceptor Orco in insect olfactory transduction. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 199, 897-909 (2013).
13. Lundin, C. et al. Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett. 581, 5601-5604 (2007).
14. Neuhaus, E. M. et al. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat. Neurosci. 8, 15-17 (2005).
15. Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714 (2004).
16. Benton, R., Sachse, S., Michnick, S. W. & Vosshall, L. B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4, e20 (2006).
17. Smart, R. et al. Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem. Mol. Biol. 38, 770-780 (2008).
18. Sato, K. et al. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002-1006 (2008).
19. Silbering, A. F. & Benton, R. Ionotropic and metabotropic mechanisms in chemoreception: "Chance or design"? EMBO Rep. 11, 173-179 (2010).
20. Nakagawa, T., Pellegrino, M., Sato, K., Vosshall, L. B. & Touhara, K. Amino acid residues contributing to function of the heteromeric insect olfactory receptor complex. PLoS ONE 7, e32372 (2012).
21. Carraher, C., Nazmi, A. R., Newcomb, R. D. & Kralicek, A. V. Recombinant expression, detergent solubilisation and purification of insect odorant receptor subunits. Protein Expr. Purif. 90, 160-169 (2013).
22. Sander, C. & Schneider, R. Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 9, 56-68 (1991).
23. Zhang, Y. Progress and challenges in protein structure prediction. Curr. Opin. Struct. Biol. 18, 342-348 (2008).
24. Marks, D. S. et al. Protein 3D structure computed from evolutionary sequence variation. PLoS ONE 6, e28766 (2011).
25. Marks, D. S., Hopf, T. A. & Sander, C. Protein structure prediction from sequence variation. Nat. Biotechnol. 30, 1072-1080 (2012).
26. Lockless, S. W. & Ranganathan, R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286, 295-299 (1999).
27. Suel, G. M., Lockless, S. W., Wall, M. A. & Ranganathan, R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat. Struct. Biol. 10, 59-69 (2003).
28. Hopf, T. A. et al. Three-dimensional structures of membrane proteins from genomic sequencing. Cell 149, 1607-1621 (2012).
29. Hallem, E. A., Ho, M. G. & Carlson, J. R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965-979 (2004).
30. Nichols, A. S. & Luetje, C. W. Transmembrane segment 3 of Drosophila melanogaster odorant receptor subunit 85B contributes to ligand-receptor interactions. J. Biol. Chem. 285, 11854-11862 (2010).
31. Tsitoura, P. et al. Expression and membrane topology of Anopheles gambiae odorant receptors in lepidopteran insect cells. PLoS ONE 5, e15428 (2010).
32. Yamauchi, T. et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423, 762-769 (2003).
33. Jin, X., Ha, T. S. & Smith, D. P. SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc. Natl Acad. Sci. USA 105, 10996-11001 (2008).
34. Xu, P. & Leal, W. S. Probing insect odorant receptors with their cognate ligands: insights into structural features. Biochem. Biophys. Res. Commun. 435, 477-482 (2013).
35. Turner, R. M. et al. Mutational analysis of cysteine residues of the insect odorant co-receptor (Orco) from Drosophila melanogaster reveals differential effects on agonist-and odorant/tuning receptor-dependent activation. J. Biol. Chem. 289, 31837-31845 (2014).
36. Dobritsa, A. A., van der Goes van Naters, W., Warr, C. G., Steinbrecht, R. A. & Carlson, J. R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827-841 (2003).
37. Jones, P. L., Pask, G. M., Rinker, D. C. & Zwiebel, L. J. Functional agonism of insect odorant receptor ion channels. Proc. Natl Acad. Sci. USA 108, 8821-8825 (2011).
38. Pellegrino, M., Steinbach, N., Stensmyr, M. C., Hansson, B. S. & Vosshall, L. B. A natural polymorphism alters odour and DEET sensitivity in an insect odorant receptor. Nature 478, 511-514 (2011).
39. Leary, G. P. et al. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc. Natl Acad. Sci. USA 109, 14081-14086 (2012).
40. Hughes, D. T., Wang, G., Zwiebel, L. J. & Luetje, C. W. A determinant of odorant specificity is located at the extracellular loop 2-transmembrane domain 4 interface of an Anopheles gambiae odorant receptor subunit. Chem. Senses 39, 761-769 (2014).
41. Pask, G. M., Jones, P. L., Rutzler, M., Rinker, D. C. & Zwiebel, L. J. Heteromeric Anopheline odorant receptors exhibit distinct channel properties. PLoS ONE 6, e28774 (2011).
42. Nichols, A. S., Chen, S. & Luetje, C. W. Subunit Contributions to Insect Olfactory Receptor Function: Channel Block and Odorant Recognition. Chem. Senses. 36, 781-790 (2011).
43. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010).
44. Gertz, E. M., Yu, Y. K., Agarwala, R., Schaffer, A. A. & Altschul, S. F. Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol. 4, 41 (2006).
45. Eddy, S. R. Accelerated Profile HMM Searches. PLoS Comput. Biol. 7, e1002195 (2011).
46. Ekeberg, M., Lovkvist, C., Lan, Y., Weigt, M. & Aurell, E. Improved contact prediction in proteins: using pseudolikelihoods to infer Potts models. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 87, 012707 (2013).
47. Balakrishnan, S., Kamisetty, H., Carbonell, J. G., Lee, S. I. & Langmead, C. J. Learning generative models for protein fold families. Proteins 79, 1061-1078 (2011).
48. Kamisetty, H., Ovchinnikov, S. & Baker, D. Assessing the utility of coevolutionbased residue-residue contact predictions in a sequence-and structure-rich era. Proc. Natl Acad. Sci. USA 110, 15674-15679 (2013).
49. Kall, L., Krogh, A. & Sonnhammer, E. L. An HMM posterior decoder for sequence feature prediction that includes homology information. Bioinformatics 21(Suppl 1): i251-i257 (2005).
50. Bernsel, A., Viklund, H., Hennerdal, A. & Elofsson, A. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 37, W465-W468 (2009).
51. Nugent, T. & Jones, D. T. Transmembrane protein topology prediction using support vector machines. BMC Bioinform 10, 159 (2009).
52. Jones, D. T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292, 195-202 (1999).
53. Brunger, A. T. Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733 (2007).
54. Katada, S., Nakagawa, T., Kataoka, H. & Touhara, K. Odorant response assays for a heterologously expressed olfactory receptor. Biochem. Biophys. Res. Commun. 305, 964-969 (2003).
55. Cherezov, V. et al. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318, 1258-1265 (2007).