All Title Author
Keywords Abstract

PLOS ONE  2013 

A Proteomic Investigation of Soluble Olfactory Proteins in Anopheles gambiae

DOI: 10.1371/journal.pone.0075162

Full-Text   Cite this paper   Add to My Lib

Abstract:

Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) are small soluble polypeptides that bind semiochemicals in the lymph of insect chemosensilla. In the genome of Anopheles gambiae, 66 genes encode OBPs and 8 encode CSPs. Here we monitored their expression through classical proteomics (2D gel-MS analysis) and a shotgun approach. The latter method proved much more sensitive and therefore more suitable for tiny biological samples as mosquitoes antennae and eggs. Females express a larger number and higher quantities of OBPs in their antennae than males (24 vs 19). OBP9 is the most abundant in the antennae of both sexes, as well as in larvae, pupae and eggs. Of the 8 CSPs, 4 were detected in antennae, while SAP3 was the only one expressed in larvae. Our proteomic results are in fairly good agreement with data of RNA expression reported in the literature, except for OBP4 and OBP5, that we could not identify in our analysis, nor could we detect in Western Blot experiments. The relatively limited number of soluble olfactory proteins expressed at relatively high levels in mosquitoes makes further studies on the coding of chemical messages at the OBP level more accessible, providing for few specific targets. Identification of such proteins in Anopheles gambiae might facilitate future studies on host finding behavior in this important disease vector.

References

[1]  Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434: 214–217.
[2]  Turner SL, Li N, Guda T, Githure J, Cardé RT, et al. (2001) Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474: 87–91.
[3]  Corbel V, Stankiewicz M, Pennetier C, Fournier D, Stojan J, et al. (2009) Evidence for inhibition of cholinesterases in insect and mammalian nervous systems by the insect repellent deet. BMC Biology 7: 47.
[4]  Pelosi P, Zhou J-J, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 631: 658–1676.
[5]  Xu P, Atkinson R, Jones DN, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45: 193–200.
[6]  Grosse-Wilde E, Svatos A, Krieger J (2006) A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Senses 31: 547–55.
[7]  Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007) Odorant-Binding Proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5: e118.
[8]  Laughlin JD, Ha TS, Jones DNM, Smith DP (2008) Activation of pheromone-sensitive neurons is mediate by conformational activation of Pheromone-binding protein. Cell 133: 1255–1265.
[9]  Swarup S, Williams TI, Anholt RR (2011) Functional dissection of Odorant binding protein genes in Drosophila melanogaster. Genes Brain Behav 10: 648–657.
[10]  Sun YF, De Biasio F, Qiao HL, Iovinella I, Yang SX, et al. (2012) Two Odorant-Binding Proteins Mediate the Behavioural Response of Aphids to the Alarm Pheromone (E)-?-Farnesene and Structural Analogues. PLoS ONE 7: e32759.
[11]  Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129–149.
[12]  Fox AN, Pitts RJ, Robertson HM, Carlson JR, Zwiebel LJ (2001) Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc Natl Acad Sci U S A 98: 14693–14697.
[13]  Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, et al. (2002) G protein-coupled receptors in Anopheles gambiae. Science 298: 176–178.
[14]  Biessmann H, Nguyen QK, Le D, Walter MF (2005) Microarray-based survey of a subset of putative olfactory genes in the mosquito Anopheles gambiae. Insect Mol Biol 14: 575–589.
[15]  Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464: 66–72.
[16]  Wang G, Carey AF, Carlson JR, Zwiebel LJ (2010) Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci USA 107: 4418–4423.
[17]  Sun Y-L, Huang L-Q, Pelosi P, Wang C-Z (2012) Expression in Antennae and Reproductive Organs Suggests a Dual Role of an Odorant-Binding Protein in Two Sibling Helicoverpa Species. PLoS ONE 7: e30040.
[18]  Calvo E, Mans BJ, Ribeiro JM, Andersen JF (2009) Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein. Proc Natl Acad Sci U S A 106: 3728–3733.
[19]  Zhou JJ, He XL, Pickett JA, Field LM (2008) Identification of odorant-binding proteins of the yellow fever mosquito Aedes aegypti: genome annotation and comparative analyses. Insect Mol Biol 17: 147–163.
[20]  Scaloni A, Monti M, Angeli S, Pelosi P (1999) Structural analyses and disulfide-bridge pairing of two odorant binding proteins from Bombyx mori. Biochem Biophys Res Commun 266: 386–391.
[21]  Leal WS, Nikonova L, Peng G (1999) Disulfide structure of the pheromone binding protein from the silkworm moth, Bombyx mori. FEBS Lett 464: 85–90.
[22]  Lagarde A, Spinelli S, Qiao H, Tegoni M, Pelosi P, et al. (2011) Crystal structure of a novel type of odorant binding protein from Anopheles gambiae, belonging to the C+ class. Biochem J 437: 423–430.
[23]  Wanner KW, Willis LG, Theilmann DA, Isman MB, Feng Q, et al. (2004) Analysis of the insect OS-D-like gene family. J Chem Ecol 30: 889–911.
[24]  Picimbon JF (2003) Biochemistry and Evolution of OBP and CSP proteins. In: Blomquist GJ, Vogt RG (eds) Insect Pheromone Biochemistry and Molecular Biology, Elsevier Academic Press, London, pp 539–566.
[25]  Jacquin-Joly E, Vogt RG, Francois MC, Nagnan-Le Meillour P (2001) Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chem Senses 26: 833–844.
[26]  Maleszka J, Forêt S, Saint R, Maleszka R (2007) RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Dev Genes Evol 217: 189–196.
[27]  Nomura A, Kawasaki K, Kubo T, Natori S (1992) Purification and localization of p10, a novel protein that increases in nymphal regenerating legs of Periplaneta americana American cockroach. Int J Dev Biol 36: 391–398.
[28]  Kitabayashi AN, Arai T, Kubo T, Natori S (1998) Molecular cloning of cDNA for p10, a novel protein that increases in the regenerating legs of Periplaneta americana (American cockroach). Insect Biochem Mol Biol 28: 785–790.
[29]  Dyanov HM, Dzitoeva SG (1995) Method for attachment of microscopic preparations on glass for in situ hybridization, PRINS and in situ PCR studies. Biotechniques 18: 822–826.
[30]  Dani FR, Michelucci E, Francese S, Mastrobuoni G, Cappellozza S, et al. (2011) Odorant-binding proteins and Chemosensory proteins in pheromone detection and release in the silkmoth Bombyx mori. Chem Senses 36: 335–344.
[31]  Zhou XH, Ban LP, Iovinella I, Zhao LJ, Gao Q, et al. (2012) Diversity, abundance and sex-specific expression of chemosensory proteins in the reproductive organs of the locust Locusta migratoria manilensis. Biol Chem 394: 43–54.
[32]  Angeli S, Ceron F, Scaloni A, Monti M, Monteforti G, et al. (1999) Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. Eur J Biochem 262: 745–754.
[33]  Biessmann H, Walter MF, Dimitratos S, Woods DF (2002) Isolation of cDNA clones encoding putative odorant binding proteins from the antennae of the malaria-transmitting mosquito, Anopheles gambiae. Insect Mol Biol 11: 123–132.
[34]  Iovinella I, Bozza F, Caputo B, Della Torre A, Pelosi P (2013) Ligand-binding study of Anopheles gambiae chemosensory proteins. Chem Senses 38: 409–19.
[35]  Pitts RJ, Rinker DC, Jones PL, Rokas A, Zwiebel LJ (2011) Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. Genomics 12: 271–288.
[36]  Amenya DA, Chou W, Li J, Yan GY, Gershon PD, et al. (2010) Proteomics reveals novel components of the Anopheles gambiae eggshell. J Ins Physol 56: 1414–1419.
[37]  Wogulis M, Morgan T, Ishida Y, Leal WS, Wilson DK (2006) The crystal structure of an odorant binding protein from Anopheles gambiae: evidence for a common ligand release mechanism. Biochem Biophys Res Commun 339: 157–164.
[38]  Ren H, Yang G, Winberg G, Turin L, Mershin A, et al. (2009) The crystal structure of an Anopheles gambiae odorant-binding protein agamobp22a and complexes with bound odorants. direct submission PDB ID 3QME.
[39]  Lagarde A, Spinelli S, Tegoni M, He X, Field L, et al. (2011) The crystal structure of odorant binding protein 7 from Anopheles gambiae exhibits an outstanding adaptability of its binding site. J Mol Biol 414 (3) 401–12 doi: 10.1016/j.jmb.2011.10.005.
[40]  Tsitsanou KE, Thireou T, Drakou CE, Koussis K, Keramioti MV, et al. (2012) Anopheles gambiae odorant binding protein crystal complex with the synthetic repellent DEET: implications for structure-based design of novel mosquito repellents. Cell Mol Life Sci 69: 283–297.
[41]  Ziemba BP, Murphy EJ, Edlin HT, Jones DN (2013) A novel mechanism of ligand binding and release in the odorant binding protein 20 from the malaria mosquito Anopheles gambiae. Protein Sci 22: 11–21.
[42]  Davrazou F, Dong E, Murphy EJ, Johnson HT, Jones DN (2011) New insights into the mechanism of odorant detection by the malaria-transmitting mosquito Anopheles gambiae. J Biol Chem 286: 34175–83.
[43]  Qiao H, He XL, Schymura D, Ban L, Field L, et al. (2011) Cooperative interactions between Odorant-Binding Proteins of Anopheles gambiae. Cell Mol Life Sci 68: 1799–813.
[44]  Della Torre A, Fanello C, Akogbeto M, Dossou-yovo J, Favia G, et al. (2001) Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol Biol 10: 9–18.
[45]  Iovinella I, Felicioli A, Niccolini A, Dani FR, Michelucci E, et al. (2011) Odorant-Binding Proteins in the mandibular glands of the honeybee as putative carriers of semiochemicals. J Proteome Res 10: 3439–3449.
[46]  Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896–906.
[47]  Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, et al. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794–805.
[48]  Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Research 40: D290–D301.
[49]  Ban LP, Scaloni A, Brandazza A, Angeli S, Zhang L, et al. (2003) Chemosensory proteins of Locusta migratoria. Insect Mol Biol 12: 125–134.
[50]  Calvello M, Guerra N, Brandazza A, D'Ambrosio C, Scaloni A, et al. (2003) Soluble proteins of chemical communication in the social wasp Polistes dominulus. Cell Mol Life Sci 60: 1933–1943.
[51]  Kyhse-Andersen J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10: 203–209.
[52]  Anholt RR, Williams TI (2010) The soluble proteome of the Drosophila antenna. Chem Senses 35: 21–30.
[53]  Justice R, Dimitratos S, Walter MF, Woods DF, Biessmann H (2003) Sexual dimorphism of antennal gene expression in the malaria vector Anopheles gambiae. Insect Mol Biol 12: 581–594.
[54]  Kalume DE, Okulate M, Zhong J, Reddy R, Suresh S, et al. (2005) A proteomic analysis of salivary glands of female Anopheles gambiae mosquito. Proteomics 5: 3765–3777.
[55]  Zhu W, Smith JW, Huang CM (2010) Mass Spectrometry-based Label-Free Quantitative Proteomics. J Biomed Biotechnol 840518. doi:10.1155/2010/840518.
[56]  Dani FR, Francese S, Mastrobuoni G, Felicioli A, Caputo B, et al. (2008) Exploring Proteins in Anopheles gambiae Male and Female Antennae through MALDI Mass Spectrometry Profiling. PLOSone 3: e2822 doi: 10.1371/journal.pone.0002822.
[57]  Paskewitz SM, Shi L (2005) The hemolymph proteome of Anopheles gambiae. Insect Biochem Mol Biol 35: 815–824.
[58]  Zhou S, Stone EA, Mackay TF, Anholt RR (2009) Plasticity of the chemoreceptor repertoire in Drosophila melanogaster. PLoS Genet 5 (10) e1000681.

Full-Text

comments powered by Disqus