Characterisation of Bombyx mori Odorant-binding Proteins Reveals that a General Odorant-binding Protein Discriminates Between Sex Pheromone Components

Journal of Molecular Biology

Volumn 389, Issue 3, 2009, Pages 529-545

  Zhou, Jing Jiang ^a   Robertson, Giles ^b   He, Xiaoli ^a   Dufour, Samuel ^a   Hooper, Antony M ^a   Pickett, John A ^a   Keep, Nicholas H ^b   Field, Linda M ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

olfaction, odorant binding protein, semiochemicals, crystal structure, silkworm

Indexed keywords

ANTENNAL BINDING PROTEIN; ARGININE; BINDING PROTEIN; BOMBYKAL; BOMBYKOL; GENE PRODUCT; GENERAL ODORANT BINDING PROTEIN; ODORANT BINDING PROTEIN; PHEROMONE BINDING PROTEIN; PROTEIN BMORABPX; PROTEIN BMORGOBP2; PROTEIN BMORPBP1; PROTEIN BMORPBP2; SERINE; SEX PHEROMONE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BMORABPX GENE; BMORGOBP1 GENE; BMORGOBP2 GENE; BMORPBP1 GENE; CRYSTAL STRUCTURE; DROSOPHILA; GENE; GENE EXPRESSION; GENOME; HORMONE PROTEIN COMPLEX; HYDROGEN BOND; MOSQUITO; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; QUANTITATIVE ANALYSIS; SILKWORM; SMELLING;

BOMBYX MORI; HEXAPODA;

EID: 65649125608     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.04.015     Document Type: Article

References (73)

1. Steinbrecht R.A. Experimental morphology of insect olfaction: tracer studies, X-ray microanalysis, autoradiography, and immunocytochemistry with silkmoth antennae. Microsc. Res. Tech. 22 (1992) 336-350
2. Steinbrecht R.A. Odorant-binding proteins: expression and function. Ann. N. Y. Acad. Sci. 30 (1998) 323-332
3. Laue M., Steinbrecht R.A., and Ziegelberger G. Immunocytochemical localization of general odourant-binding protein in olfactory sensilla of the silkmoth Antheraea polyphemus. Naturwissenschaften 81 (1994) 178-180
4. Pikielny C.W., Hasan G., Rouyer F., and Rosbash M. Members of a family of Drosophila putative odourant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12 (1994) 35-49
5. Shanbhag S.R., Hekmat-Scafe D., Kim M.S., Park S.K., Carlson J.R., Pikielny C., et al. Expression mosaic of odourant-binding proteins in Drosophila olfactory organs. Microsc. Res. Tech. 55 (2001) 297-306
6. Ishida Y., Chiang V., and Leal W.S. Protein that makes sense in the Argentine ant. Naturwissenschaften 89 (2002) 505-507
7. Leal W.S. Proteins that make sense. In: Blomquist G.J., and Vogt R.G. (Eds). Insect Pheromone Biochemistry and Molecular Biology, the Biosynthesis and Detection of Pheromones and Plant Volatiles (2003), Elsevier Academic Press, London 447-476
8. Krieger J., Grosse-Wilde E., Gohl T., and Breer H. Candidate pheromone receptors of the silkmoth Bombyx mori. Eur. J. Neurosci. 21 (2005) 2167-2176
9. Breer H., Krieger J., and Raming K. A novel class of binding proteins in the antennae of the silkmoth Antheraea pernyi. Insect Biochem. 20 (1990) 735-740
10. Krieger J., Gänssle H., Raming K., and Breer H. Odorant binding proteins of Heliothis virescens. Insect Biochem. Mol. Biol. 23 (1993) 449-456
11. Scaloni A., Monti M., Angeli S., and Pelosi P. Structural analysis and disulfide-bridge pairing of two odorant-binding proteins from Bombyx mori. Biochem. Biophys. Res. Commun. 266 (1999) 386-391
12. Leal W.S., Nikonova L., and Peng G. Disulfide structure of the pheromone binding protein from the silkworm moth, Bombyx mori. FEBS Lett. 24 (1999) 85-90
13. Sandler B.H., Nikonova L., Leal W.S., and Clardy J. Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem. Biol. 7 (2000) 143-151
14. Zhou J.-J., Huang W.-S., Zhang G.A., Pickett J.A., and Field L.M. ''Plus-C'' odourant-binding protein genes in two Drosophila species and the malaria mosquito An. gambiae. Gene 327 (2004) 117-129
15. Li Z.X., Pickett J.A., Field L.M., and Zhou J.-J. Identification and expression of odorant-binding proteins of the malaria-carrying mosquitoes Anopheles gambiae and Anopheles arabiensis. Arch. Insect Biochem. Physiol. 58 (2004) 175-189
16. Zhou J.-J., Kan Y., Antoniw J., Pickett J.A., and Field L.M. Genome and EST analyses and expression of a gene family with putative functions in insect chemoreception. Chem. Senses 31 (2006) 453-465
17. Zhou J.-J., He X.L., Pickett J.A., and Field L.M. Identification of odorant-binding proteins of the yellow fever mosquito Aedes aegypti: genome annotation and comparative analyses. Insect Mol. Biol. 17 (2008) 147-163
18. Vogt R.G., and Riddiford L.M. Pheromone binding and inactivation by moth antennae. Nature 293 (1981) 161-163
19. Robertson H.M., Martos R., Sears C.R., Todres E.Z., Walden K.K., and Nardi J.B. Diversity of odourant binding proteins revealed by an expressed sequence tag project on male Manduca sexta moth antennae. Insect Mol. Biol. 8 (1999) 501-518
20. Krieger J., von Nickisch-Rosenegk E., Mameli M., Pelosi P., and Breer H. Binding proteins from the antennae of Bombyx mori. Insect Biochem. Mol. Biol. 26 (1996) 297-307
21. Maida R., Mameli M., Müller B., Krieger J., and Steinbrecht R.A. The expression pattern of four odorant-binding proteins in male and female silk moths, Bombyx mori. J. Neurocytol. 34 (2005) 149-163
22. Pelosi P., Zhou J.-J., Ban L.P., and Calvello M. Soluble proteins in insect chemical communication. Cell Mol. Life Sci. 63 (2006) 1658-1676
23. Györgyi T.K., Roby-Shemkovitz A.J., and Lerner M.R. Characterization and cDNA cloning of the pheromone-binding protein from the tobacco hornworm, Manduca sexta: a tissue-specific developmentally regulated protein. Proc. Natl Acad. Sci. USA 85 (1988) 9851-9855
24. Callahan F.E., Vogt R.G., Tucker M.L., Dickens J.C., and Mattoo A.K. High level expression of "male specific" pheromone binding proteins (PBPs) in the antennae of female noctuiid moths. Insect Biochem. Mol. Biol. 30 (2000) 507-514
25. Vogt R.G., Rogers M.E., Franco M.D., and Sun M. A comparative study of odorant binding protein genes: differential expression of the PBP1-GOBP2 gene cluster in Manduca sexta (Lepidoptera) and the organization of OBP genes in Drosophila melanogaster (Diptera). J. Exp. Biol. 205 (2002) 719-744
26. Picimbon J.F., and Gadenne C. Evolution of noctuid pheromone binding proteins: identification of PBP in the black cutworm moth, Agrotis ipsilon. Insect Biochem. Mol. Biol. 32 (2002) 839-846
27. Vogt R.G., Rybczynski R., and Lerner M.R. Molecular cloning and sequencing of general odorant-binding proteins GOBP1 and GOBP2 from the tobacco hawk moth Manduca sexta: comparisons with other insect OBPs and their signal peptides. J. Neurosci. 11 (1991) 2972-2984
28. Krieger J., Raming K., and Breer H. Cloning of genomic and complementary DNA encoding insect pheromone binding proteins: evidence for microdiversity. Biochim. Biophys. Acta 1088 (1991) 277-284
29. Krieger J., Mameli M., and Breer H. Elements of the olfactory signaling pathways in insect antennae. Invert. Neurosci. 3 (1997) 137-144
30. Vogt R.G., Callahan F.E., Rogers M.E., and Dickens J.C. Odorant binding protein diversity and distribution among the insect orders, as indicated by LAP, an OBP-related protein of the true bug Lygus lineolaris (Hemiptera, Heteroptera). Chem. Senses 24 (1999) 481-495
31. Pophof B. Pheromone-binding proteins contribute to the activation of olfactory receptor neurons in the silkmoths Antheraea polyphemus and Bombyx mori. Chem. Senses 29 (2004) 117-125
32. Xu P., Atkinson R., Jones D.N., and Smith D.P. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45 (2005) 193-200
33. Syed Z., Ishida Y., Taylor K., Kimbrell D.A., and Leal W.S. Pheromone reception in fruit flies expressing a moth's odorant receptor. Proc. Natl Acad. Sci. USA 103 (2006) 16538-16543
34. Grosse-Wilde E., Svatos A., and Krieger J. A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses 31 (2006) 547-555
35. Ha T.S., and Smith D.P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J. Neurosci. 26 (2006) 8727-8733
36. Benton R., Vannice K.S., and Vosshall L.B. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450 (2007) 289-293
37. Laughlin J.D., Ha T.S., Jones D.N.M., and Smith D.P. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133 (2008) 1255-1265
38. Maida R., Proebstl T., and Laue M. Heterogeneity of odorant-binding proteins in the antennae of Bombyx mori. Chem. Senses 22 (1997) 503-515
39. Maida R., Steinbrecht A., Ziegelberger G., and Pelosi P. The pheromone binding protein of Bombyx mori: Purification, characterization and immunochemical localization. Insect Biochem. Mol. Biol. 23 (1993) 243-253
40. Leal W.S., Chen A.M., Ishida Y., Chiang V.P., Erickson M.L., Morgan T.I., and Tsuruda J.M. Kinetics and molecular properties of pheromone binding and release. Proc. Natl Acad. Sci. USA 102 (2005) 5386-5391
41. Leal W.S., Chen A.M., and Erickson M.L. Selective and pH-dependent binding of a moth pheromone to a pheromone-binding protein. J. Chem. Ecol. 31 (2005) 2493-2499
42. Wojtasek H., and Leal W.S. Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J. Biol. Chem. 274 (1999) 30950-30956
43. Lautenschlager C., Leal W.S., and Clardy J. Coil-to-helix transition and ligand release of Bombyx mori pheromone-binding protein. Biochem. Biophys. Res. Commun. 335 (2005) 1044-1050
44. Horst R., Damberger F., Luginbühl P., Güntert P., Peng G., Nikonova L., et al. NMR structure reveals intramolecular regulation mechanism for pheromone binding and release. Proc. Natl Acad. Sci. USA 98 (2001) 14374-14379
45. Lee D., Damberger F.F., Peng G., Horst R., Güntert P., Nikonova L., et al. NMR structure of the unliganded Bombyx mori pheromone-binding protein at physiological pH. FEBS Lett. 531 (2002) 314-318
46. Damberger F., Nikonova L., Horst R., Peng G., Leal W.S., and Wüthrich K. NMR characterization of a pH-dependent equilibrium between two folded solution conformations of the pheromone-binding protein from Bombyx mori. Protein Sci. 9 (2000) 1038-1041
47. Nakagawa T., Sakurai T., Nishioka T., and Touhara K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307 (2005) 1638-1642
48. Dobritsa A.A., van der Goes van Naters W., Warr C.G., Steinbrecht R.A., and Carlson J.R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37 (2003) 827-841
49. Forstner M., Gohl T., Breer H., and Krieger J. Candidate pheromone binding proteins of the silkmoth Bombyx mori. Invert. Neurosci. 6 (2006) 177-187
50. Kaissling K.E., Kasang G., Bestmann H.J., Stransky W., and Vostrowsky O. A new pheromone of the silkworm moth Bombyx mori. Naturwissenschaften 65 (1978) 382-384
51. Butenandt A., Beckmann R., and Stamm D. Über den Sexuallockstoff des Seidenspinners. II. Konstitution und Konfiguration des Bombykols. Z. Physiol. Chem. 324 (1961) 84-87
52. Oldham N.J., Krieger J., Breer H., Fischedick A., Hoskovec M., and Svato A. Analysis of the silkworm moth pheromone binding protein-pheromone complex by electrospray ionization-mass spectrometry. Angew. Chem. Int. Ed. Engl. 39 (2000) 4341-4343
53. Oldham N.J., Krieger J., Breer H., and Svatos A. Detection and removal of an artefact fatty acid from the binding site of recombinant Bombyx mori pheromone-binding protein. Chem. Senses 26 (2001) 529-531
54. Zubkov S., Gronenborn A.M., Byeon I.J., and Mohanty S. Structural consequences of the pH-induced conformational switch in A. polyphemus pheromone-binding protein: mechanisms of ligand release. J. Mol. Biol. 354 (2005) 1081-1090
55. Gräter F., de Groot B.L., Jiang H., and Grubmüller H. Ligand-release pathways in the pheromone-binding protein of Bombyx mori. Structure 14 (2006) 1567-1576
56. Gräter F., Xu W., Leal W., and Grubmüller H. Pheromone discrimination by the pheromone-binding protein of Bombyx mori. Structure 14 (2006) 1577-1586
57. Forêt S., and Maleszka R. Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res. 16 (2006) 1404-1413
58. Zhou J.J., Zhang G.A., Huang W., Birkett M.A., Field L.M., Pickett J.A., and Pelosi P. Revisiting the odorant-binding protein LUSH of Drosophila melanogaster: evidence for odour recognition and discrimination. FEBS Lett. 558 (2004) 23-26
59. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software. J. Appl. Crystallogr. 40 (2007) 658-674
60. Malnic B., Hirono J., Sato T., and Buck L.B. Combinatorial receptor codes for odors. Cell 96 (1999) 713-723
61. Kajiya K., Inaki K., Tanaka M., Haga T., Kataoka H., and Touhara K. Molecular bases of odor discrimination: Reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 21 (2001) 6018-6025
62. Lautenschlager C., Leal W.S., and Clardy J. Bombyx mori pheromone-binding protein binding nonpheromone ligands: implications for pheromone recognition. Structure 15 (2007) 1148-1154
63. Pesenti M.E., Spinelli S., Bezirard V., Briand L., Pernollet J.C., Tegoni M., and Cambillau C. Structural basis of the honey bee PBP pheromone and pH-induced conformational change. J. Mol. Biol. 380 (2008) 158-169
64. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
65. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
66. Saitou N., and Nei M. The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
67. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) 2002-2007
68. Ramakers C., Ruijter J.M., Deprez R.H., and Moorman A.F. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339 (2003) 62-66
69. Leslie, A. G. W. (1992). Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography, no. 26.
70. Keegan R.M., and Winn M.D. Automated search-model discovery and preparation for structure solution by molecular replacement. Acta Crystallogr. D 63 (2007) 447-457
71. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53 (1997) 240-255
72. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W., et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58 (2002) 1948-1954
73. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60 (2004) 2126-2132