Differential expression of odorant-binding proteins in the mandibular glands of the honey bee according to caste and age

Journal of Proteome Research

Volumn 10, Issue 8, 2011, Pages 3439-3449

  Iovinella, Immacolata ^a   Dani, Francesca Romana ^b   Niccolini, Alberto ^a   Sagona, Simona ^a   Michelucci, Elena ^b   Gazzano, Angelo ^a   Turillazzi, Stefano ^b   Felicioli, Antonio ^a   Pelosi, Paolo ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Apis mellifera; chemosensory protein; farnesol; ligand binding; mandibular glands; odorant binding protein; proteomics

Indexed keywords

BINDING PROTEIN; CHEMOSENSORY PROTEIN; CHEMOSENSORY PROTEIN 1; CHEMOSENSORY PROTEIN 3; FARNESOL; INSECT PROTEIN; ODORANT BINDING PROTEIN; ODORANT BINDING PROTEIN 1; ODORANT BINDING PROTEIN 11; ODORANT BINDING PROTEIN 13; ODORANT BINDING PROTEIN 14; ODORANT BINDING PROTEIN 15; ODORANT BINDING PROTEIN 16; ODORANT BINDING PROTEIN 17; ODORANT BINDING PROTEIN 18; ODORANT BINDING PROTEIN 19; ODORANT BINDING PROTEIN 2; ODORANT BINDING PROTEIN 20; ODORANT BINDING PROTEIN 21; ODORANT BINDING PROTEIN 4; ODORANT BINDING PROTEIN 5; OLEIC ACID; UNCLASSIFIED DRUG;

AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; HONEYBEE; LIGAND BINDING; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEOMICS; SUBMANDIBULAR GLAND;

AGE FACTORS; ANIMALS; BASE SEQUENCE; BEES; BLOTTING, WESTERN; CLONING, MOLECULAR; DNA PRIMERS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION REGULATION; IMMUNE SERA; INSECT PROTEINS; MALE; MANDIBLE; POLYMERASE CHAIN REACTION; PROTEOMICS; RECEPTORS, ODORANT; SPECTROMETRY, FLUORESCENCE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

APIS MELLIFERA; APOIDEA; HEXAPODA; HYMENOPTERA;

EID: 79961220478     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2000754     Document Type: Article

References (49)

1. Pelosi, P. Odorant-binding proteins Crit. Rev. Biochem Mol. Biol. 1994, 29, 199-228 (Pubitemid 24175936)
2. Tegoni, M.; Pelosi, P.; Vincent, F.; Spinelli, S.; Campanacci, V.; Grolli, S.; Ramoni, R.; Cambillau, C. Mammalian odorant binding proteins Biochim. Biophys. Acta 2000, 1482, 229-240
3. Vogt, R. G.; Riddiford, L. M. Pheromone binding and inactivation by moth antennae Nature 1981, 293, 161-163 (Pubitemid 11009908)
4. Angeli, S.; Ceron, F.; Scaloni, A.; Monti, M.; Monteforti, G.; Minnocci, A.; Petacchi, R.; Pelosi, P. Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria Eur. J. Biochem. 1999, 262, 745-754 (Pubitemid 29291032)
5. Vogt, R. G. Molecular basis of pheromone detection in insects. In Comprehensive Insect Physiology, Biochemistry, Pharmacology and Molecular Biology. Vol. 3. Endocrinology; Gilbert, L. I.; Iatrou, K.; Gill, S., Eds. Elsevier: London, 2005; pp 753-804.
6. Pelosi, P.; Zhou, J.-J.; Ban, L. P.; Calvello, M. Soluble proteins in insect chemical communication Cell. Mol. Life Sci. 2006, 63, 1658-1676 (Pubitemid 44252179)
7. Finlayson, J. S.; Asofsky, R.; Potter, M.; Runner, C. C. Major urinary protein complex of normal mice: origin Science 1965, 149, 981-982
8. Shaw, P. H.; Held, W. A.; Hastie, N. D. The gene family for major urinary proteins: expression in several secretory tissues of the mouse Cell 1983, 32, 755-761 (Pubitemid 13087931)
9. Cavaggioni, A.; Sorbi, R. T.; Keen, J. N.; Pappin, D. J. C.; Findlay, J. B. C. Homology between the pyrazine-binding protein from nasal mucosa and major urinary proteins FEBS Lett. 1987, 212, 225-228 (Pubitemid 17034755)
10. Cavaggioni, A.; Mucignat-Caretta, C. Major urinary proteins, alpha(2U)-globulins and aphrodisin Biochim. Biophys. Acta 2000, 1482, 218-228
11. Marchese, S.; Pes, D.; Scaloni, A.; Carbone, V.; Pelosi, P. Lipocalins of boar salivary glands binding odours and pheromones Eur. J. Biochem. 1998, 252, 563-568 (Pubitemid 28156882)
12. Spinelli, S.; Vincent, F.; Pelosi, P.; Tegoni, M.; Cambillau, C. Boar salivary lipocalin. Three-dimensional X-ray structure and androsterol/ androstenone docking simulations Eur. J. Biochem. 2002, 269, 2449-2456 (Pubitemid 34539272)
13. Shahan, K. M.; Denaro, M.; Gilmartin, M.; Shi, Y.; Derman, E. Expression of six mouse major urinary protein genes in the mammary, parotid, sublingual, submaxillary and lachrymal glands and in the liver Mol. Cell. Biol. 1987, 7, 1947-1954 (Pubitemid 17059184)
14. Singer, A. G.; Macrides, F. Composition of an aphrodisiac pheromone Chem. Senses 1993, 18, 630
15. Briand, L.; Huet, J.; Perez, V.; Lenoir, G.; Nespoulous, C.; Boucher, Y.; Trotier, D.; Pernollet, J. C. Odorant and pheromone binding by aphrodisin, a hamster aphrodisiac protein FEBS Lett. 2000, 476, 179-185 (Pubitemid 30410813)
16. D'Innocenzo, B.; Salzano, A. M.; D'Ambrosio, C.; Gazzano, A.; Niccolini, A.; Sorce, C.; Dani, F. R.; Scaloni, A.; Pelosi, P. Secretory proteins as potential semiochemical carriers in the horse Biochemistry 2006, 45, 13418-13428 (Pubitemid 44748488)
17. Zeng, C.; Spielman, A.; Vowels, B. R.; Leyden, J.; Biemann, K.; Preti, G. A human axillary odorant is carried by apolipoprotein D Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 6626-6630 (Pubitemid 26230359)
18. Bacchini, A.; Gaetani, E.; Cavaggioni, A. Pheromone-binding proteins in the mouse mus musculus Experientia 1992, 48, 419-421
19. Jacquin-Joly, E.; Vogt, R. G.; Francois, M. C.; Nagnan-Le Meillour, P. Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae Chem. Senses 2001, 26, 833-844 (Pubitemid 32899103)
20. Dyanov, H. M.; Dzitoeva, S. G. Method for attachment of microscopic preparations on glass for in situ hybridization, PRINS and in situ PCR studies Biotechniques 1995, 18, 822-826
21. Li, S.; Picimbon, J.-F.; Ji, S. D.; Kan, Y. C.; Qiao, C. L.; Zhou, J.-J.; Pelosi, P. Multiple functions of an odorant-binding protein in the mosquito Aedes aegypti Biochem. Biophys. Res. Commun. 2008, 372, 464-468
22. Vogel, H.; Heidel, A. J.; Heckel, D. G.; Groot, A. T. Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens BMC Genomics 2010, 11, 29
23. Dani, F. R.; Michelucci, E.; Francese, S.; Mastrobuoni, G.; Cappellozza, S.; La Marca, G.; Niccolini, A.; Felicioli, A.; Moneti, G.; Pelosi, P. Odorant-binding proteins and Chemosensory proteins in pheromone detection and release in the silkmoth Bombyx mori. Chem. Senses 2011, DOI: 10.1093/chemse/bjq137.
24. Slessor, K. N.; Winston, M. L.; Le Conte, Y. Pheromone communication in the honeybee (Apis mellifera L.) J. Chem. Ecol. 2005, 31, 2731-2745 (Pubitemid 41597345)
25. Slessor, K. N.; Kaminski, L.-A.; King, G. G. S.; Borden, J. H.; Winston, M. L. Semiochemical basis of the retinue response to queen honey bees Nature 1988, 332, 354-356
26. Le Conte, Y.; Arnold, G.; Trouiller, J.; Masson, C. Identification of a brood pheromone in honeybees Naturwissenschaften 1990, 77, 334-336 (Pubitemid 20272121)
27. Moritz, R. F. A.; Burgin, H. Group response to alarm pheromones in socialwasps and the honeybees Ethology 1987, 76, 15-26
28. Dani, F. R.; Jones, G. R.; Corsi, S.; Beard, R.; Pradella, D.; Turillazzi, S. Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes Chem. Senses 2005, 30, 477-489 (Pubitemid 41158333)
29. Swanson, J. A.; Torto, B.; Kells, S. A.; Mesce, K. A.; Tumlinson, J. H.; Spivak, M. Odorants that Induce Hygienic Behavior in Honeybees: Identification of Volatile Compounds in Chalkbrood-Infected Honeybee Larvae J. Chem. Ecol. 2009, 35, 1108-1116
30. Le Conte, Y.; Hefetz, A. Primer Pheromones in Social Hymenoptera Annu. Rev. Entomol. 2008, 53, 523-542 (Pubitemid 351341953)
31. Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera Nature 2006, 443, 931-949
32. Forêt, S.; 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. 2006, 16, 1404-1413 (Pubitemid 44664683)
33. Forêt, S.; Wanner, K. W.; Maleszka, R. Chemosensory proteins in the honey bee: Insights from the annotated genome, comparative analyses and expressional profiling Insect Biochem. Mol. Biol. 2006, 37, 19-28 (Pubitemid 44908971)
34. Dani, F. R.; Iovinella, I.; Felicioli, A.; Niccolini, A.; Calvello, M. A.; Carucci, M. G.; Qiao, H.; Pieraccini, G.; Turillazzi, S.; Moneti, G.; Pelosi, P. Mapping the Expression of Soluble Olfactory Proteins in the Honeybee J. Proteome Res. 2010, 9, 1822-1833
35. Ban, L. P.; Scaloni, A.; Brandazza, A.; Angeli, S.; Zhang, L.; Yan, Y. H.; Pelosi, P. Chemosensory proteins of Locusta migratoria Insect Mol. Biol. 2003, 12, 125-134 (Pubitemid 36400263)
36. Calvello, M.; Guerra, N.; Brandazza, A.; D'Ambrosio, C.; Scaloni, A.; Dani, F. R.; Turillazzi, S.; Pelosi, P. Soluble proteins of chemical communication in the social wasp Polistes dominulus Cell. Mol. Life Sci. 2003, 60, 1933-1943 (Pubitemid 37222588)
37. Kyhse-Andersen, J. Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose J. Biochem. Biophys. Methods 1984, 10, 203-209 (Pubitemid 15171298)
38. Dani, F. R.; Francese, S.; Mastrobuoni, G.; Felicioli, A.; Caputo, B.; Simard, F.; Pieraccini, G.; Moneti, G.; Coluzzi, M.; Della Torre, A.; Turillazzi, S. Exploring proteins in Anopheles gambiae male and female antennae through MALDI mass spectrometry profiling PLoS One 2008, 3, e2822
39. Guex, N.; Peitsch, M. C. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modelling Electrophoresis 1997, 18, 2714-2723 (Pubitemid 28059943)
40. Schwede, T.; Kopp, J.; Guex, N.; Peitsch, M. C. SWISS-MODEL: an automated protein homology-modeling server Nucleic Acids Res. 2003, 31, 3381-3385 (Pubitemid 37442164)
41. Arnold, K.; Bordoli, L.; Kopp, J.; Schwede, T. The SWISS-MODEL Workspace: A web-based environment for protein structure homology modelling Bioinformatics 2006, 22, 195-201 (Pubitemid 43205406)
42. Pesenti, M. E.; Spinelli, S.; Bezirard, V.; Briand, L.; Pernollet, J. C.; Campanacci, V.; Tegoni, M.; Cambillau, C. Structural Basis of the Honey Bee PBP Pheromone and pH-induced Conformational Change J. Mol. Biol. 2008, 380, 158-169
43. Pesenti, M. E.; Spinelli, S.; Bezirard, V.; Briand, L.; Pernollet, J. C.; Campanacci, V.; Tegoni, M.; Cambillau, C. Queen bee pheromone binding protein pH-induced domain swapping favors pheromone release J. Mol. Biol. 2009, 390, 981-990
44. Zhou, J-J; Robertson, G.; He, X.; Dufour, S.; Hooper, A. M.; Pickett, J. A.; Keep, N. H.; Field, L. M. Characterisation of Bombyx mori Odorant-binding proteins reveals that a general odorant-binding protein discriminates between sex pheromone components J. Mol. Biol. 2009, 389, 529-545
45. Demeure, K.; Quinton, L.; Gabelica, V.; De Pauw, E. Rational Selection of the Optimum MALDI Matrix for Top-Down Proteomics by In-Source Decay Anal. Chem. 2007, 79, 8678-8685 (Pubitemid 350171379)
46. Lartigue, A.; Gruez, A.; Spinelli, S.; Riviere, S.; Brossut, R.; Tegoni, M.; Cambillau, C. The crystal structure of a cockroach pheromone-binding protein suggests a new ligand332. binding and release mechanism J. Biol. Chem. 2003, 278, 30213-30218 (Pubitemid 36962415)
47. Engels, W.; Rosenkranz, P.; Adler, A.; Tghizadeh, T.; Lubke, G.; Francke, W. Mandibular gland volatiles and their ontogenetic patterns in queen honey bee Apis mellifera carnica J. Insect Physiol. 1997, 43, 307-313 (Pubitemid 27324686)
48. Pickett, J. A.; Williams, I. H.; Martin, A. P.; Smith, M. C. Nasonov pheromone of the honey bee, Apis mellifera l. (Hymenoptera: Apidae). Part I. Chemical characterization J. Chem. Ecol. 1980, 6, 425-434
49. Maisonnasse, A.; Alaux, C.; Beslay, D.; Crauser, D.; Christian Gines, C.; Plettner, E.; Le Conte, Y. New insights into honey bee (Apis mellifera) pheromone communication. Is the queen mandibular pheromone alone in colony regulation? Front. Zool. 2010, 7, 18