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PLOS ONE  2013 

The Co-Expression Pattern of Odorant Binding Proteins and Olfactory Receptors Identify Distinct Trichoid Sensilla on the Antenna of the Malaria Mosquito Anopheles gambiae

DOI: 10.1371/journal.pone.0069412

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Abstract:

The initial steps of odorant recognition in the insect olfactory system involve odorant binding proteins (OBPs) and odorant receptors (ORs). While large families of OBPs have been identified in the malaria vector A. gambiae, little is known about their expression pattern in the numerous sensory hairs of the female antenna. We applied whole mount fluorescence in Situ hybridization (WM-FISH) and fluorescence immunohistochemistry (WM-FIHC) to investigate the sensilla co-expression of eight A. gambiae OBPs (AgOBPs), most notably AgOBP1 and AgOBP4, which all have abundant transcripts in female antenna. WM-FISH analysis of female antennae using AgOBP-specific probes revealed marked differences in the number of cells expressing each various AgOBPs. Testing combinations of AgOBP probes in two-color WM-FISH resulted in distinct cellular labeling patterns, indicating a combinatorial expression of AgOBPs and revealing distinct AgOBP requirements for various functional sensilla types. WM-FIHC with antisera to AgOBP1 and AgOBP4 confirmed expression of the respective proteins by support cells and demonstrated a location of OBPs within sensilla trichodea. Based on the finding that AgOBP1 and AgOBP4 as well as the receptor type AgOR2 are involved in the recognition of indole, experiments were performed to explore if the AgOBP-types and AgOR2 are co-expressed in distinct olfactory sensilla. Applying two-color WM-FISH with AgOBP-specific probes and probes specific for AgOR2 revealed a close association of support cells bearing transcripts for AgOBP1 and AgOBP4 and neurons with a transcript for the receptor AgOR2. Moreover, combined WM-FISH/-FIHC approaches using an AgOR2-specific riboprobe and AgOBP-specific antisera revealed the expression of the “ligand-matched” AgOBP1, AgOBP4 and AgOR2 to single trichoid hairs. This result substantiates the notion that a specific response to indole is mediated by an interplay of the proteins.

References

[1]  White GB (1974) Anopheles gambiae complex and disease transmission in Africa. Trans R Soc Trop Med Hyg 68: 278-301. doi:10.1016/0035-9203(74)90035-2. PubMed: 4420769.
[2]  Boakye DA, Wilson MD, Appawu MA, Gyapong J (2004) Vector competence, for Wuchereria bancrofti, of the Anopheles populations in the Bongo district of Ghana. Ann Trop Med Parasitol 98: 501-508. doi:10.1179/000349804225003514. PubMed: 15257800.
[3]  Williams MC, Woodall JP, Corbet PS, Gillett JD (1965) O’nyong-Nyong Fever: An Epidemic Virus Disease in East Africa. 8. Virus Isolations from Anopheles Mosquitoes. Trans R Soc Trop Med Hyg 59: 300-306. doi:10.1016/0035-9203(65)90012-X. PubMed: 14298035.
[4]  Takken W, Knols BG (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131-157. doi:10.1146/annurev.ento.44.1.131. PubMed: 9990718.
[5]  Zwiebel LJ, Takken W (2004) Olfactory regulation of mosquito-host interactions. Insect Biochem Mol Biol 34: 645-652. doi:10.1016/j.ibmb.2004.03.017. PubMed: 15242705.
[6]  Pitts RJ, Zwiebel LJ (2006) Antennal sensilla of two female anopheline sibling species with differing host ranges. Malar J 5: 26. doi:10.1186/1475-2875-5-26. PubMed: 16573828.
[7]  Qiu YT, van Loon JJ, Takken W, Meijerink J, Smid HM (2006) Olfactory Coding in Antennal Neurons of the Malaria Mosquito, Anopheles gambiae. Chem Sens 31: 845-863. doi:10.1093/chemse/bjl027. PubMed: 16963500.
[8]  Lu T, Qiu YT, Wang G, Kwon JY, Rutzler M et al. (2007) Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr Biol 17: 1533-1544. doi:10.1016/j.cub.2007.07.062. PubMed: 17764944.
[9]  Kwon HW, Lu T, Rützler M, Zwiebel LJ (2006) Olfactory responses in a gustatory organ of the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 103: 13526-13531. doi:10.1073/pnas.0601107103. PubMed: 16938890.
[10]  Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51: 113-135. doi:10.1146/annurev.ento.51.051705.113646. PubMed: 16332206.
[11]  Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58: 373-391. doi:10.1146/annurev-ento-120811-153635. PubMed: 23020622.
[12]  Blomquist GJ, Vogt RG (2003). Insect pheromone biochemistry and molecular biology. The biosynthesis and detection of pheromones and plant volatiles. London: Elsevier Academic Press.
[13]  Swarup S, Williams TI, Anholt RR (2011) Functional dissection of Odorant binding protein genes in Drosophila melanogaster. Genes Brain Behav 10: 648-657. doi:10.1111/j.1601-183X.2011.00704.x. PubMed: 21605338.
[14]  Zhou JJ, Huang W, Zhang GA, Pickett JA, Field LM (2004) "Plus-C" odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene 327: 117-129. doi:10.1016/j.gene.2003.11.007. PubMed: 14960367.
[15]  Xu PX, Zwiebel LJ, Smith DP (2003) Identification of a distinct family of genes encoding atypical odorant-binding proteins in the malaria vector mosquito, Anopheles gambiae. Insect Mol Biol 12: 549-560. doi:10.1046/j.1365-2583.2003.00440.x. PubMed: 14986916.
[16]  Vogt RG (2002) Odorant binding protein homologues of the malaria mosquito Anopheles gambiae; possible orthologues of the OS-E and OS-F OBPs of Drosophila melanogaster. J Chem Ecol 28: 2371-2376. doi:10.1023/A:1021009311977. PubMed: 12523574.
[17]  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. BMC Genomics 12: 271. doi:10.1186/1471-2164-12-271. PubMed: 21619637.
[18]  Vieira FG, Rozas J (2011) Comparative Genomics of the Odorant-Binding and Chemosensory Protein Gene Families across the Arthropoda: Origin and evolutionary history of the chemosensory system. Genome Biol Evol 3: 476-490. doi:10.1093/gbe/evr033. PubMed: 21527792.
[19]  Fox AN, Pitts RJ, Zwiebel LJ (2002) A cluster of candidate odorant receptors from the malaria vector mosquito, Anopheles gambiae. Chem Sens 27: 453-459. doi:10.1093/chemse/27.5.453. PubMed: 12052782.
[20]  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. doi:10.1073/pnas.261432998. PubMed: 11724964.
[21]  Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL et al. (2002) G protein-coupled receptors in Anopheles gambiae. Science 298: 176-178. doi:10.1126/science.1076196. PubMed: 12364795.
[22]  Iatrou K, Biessmann H (2008) Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae. Insect Biochem Mol Biol 38: 268-274. doi:10.1016/j.ibmb.2007.11.008. PubMed: 18207086.
[23]  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. doi:10.1111/j.1365-2583.2005.00590.x. PubMed: 16313558.
[24]  Justice RW, Dimitratos S, Walter MF, Woods DF, Biessmann H (2003) Sexual dimorphic expression of putative antennal carrier protein genes in the malaria vector Anopheles gambiae. Insect Mol Biol 12: 581-594. doi:10.1046/j.1365-2583.2003.00443.x. PubMed: 14986919.
[25]  Schultze A, Schymura D, Forstner M, Krieger J (2012) Expression pattern of a "Plus-C" class odorant binding protein in the antenna of the malaria vector Anopheles gambiae. Insect Mol Biol 21: 187-195. doi:10.1111/j.1365-2583.2011.01125.x. PubMed: 22211989.
[26]  Schymura D, Forstner M, Schultze A, Kr?ber T, Swevers L et al. (2010) Antennal expression pattern of two olfactory receptors and an odorant binding protein implicated in host odor detection by the malaria vector Anopheles gambiae. Int J Biol Sci 6: 614-626. PubMed: 20975820.
[27]  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 U S A 107: 4418-4423. doi:10.1073/pnas.0913392107. PubMed: 20160092.
[28]  Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464: 66-71. doi:10.1038/nature08834. PubMed: 20130575.
[29]  Hallem EA, Nicole FA, Zwiebel LJ, Carlson JR (2004) Olfaction: mosquito receptor for human-sweat odorant. Nature 427: 212-213. doi:10.1038/427212a. PubMed: 14724626.
[30]  Blackwell A, Johnson SN (2000) Electrophysiological investigation of larval water and potential oviposition chemo-attractants for Anopheles gambiae s.s. Ann Trop Med Parasitol 94: 389-398. PubMed: 10945049.
[31]  Meijerink J, Braks MA, Brack AA, Adam W, Dekker T et al. (2000) Identification of olfactory stimulants for Anopheles gambiae from human sweat samples. J Chem Ecol 26: 1367-1382. doi:10.1023/A:1005475422978.
[32]  Qiao H, He X, Schymura D, ld L, Dani FR, et al (2010) Cooperative interactions between odorant-binding proteins of Anopheles gambiae. Cell Mol Life Sci 68: 1799-1813. PubMed: 20957509.
[33]  Pelletier J, Hughes DT, Luetje CW, Leal WS (2010) An odorant receptor from the southern house mosquito Culex pipiens quinquefasciatus sensitive to oviposition attractants. PLOS ONE 5: e10090. doi:10.1371/journal.pone.0010090. PubMed: 20386699.
[34]  Bohbot JD, Jones PL, Wang G, Pitts RJ, Pask GM et al. (2011) Conservation of indole responsive odorant receptors in mosquitoes reveals an ancient olfactory trait. Chem Sens 36: 149-160. doi:10.1093/chemse/bjq105. PubMed: 20956733.
[35]  Biessmann H, Andronopoulou E, Biessmann MR, Douris V, Dimitratos SD et al. (2010) The Anopheles gambiae Odorant Binding Protein 1 (AgamOBP1) mediates indole recognition in the antennae of female mosquitoes. PLOS ONE 5: e9471. doi:10.1371/journal.pone.0009471. PubMed: 20208991.
[36]  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: 34175-34183. doi:10.1074/jbc.M111.274712. PubMed: 21816826.
[37]  Andronopoulou E, Labropoulou V, Douris V, Woods DF, Biessmann H et al. (2006) Specific interactions among odorant-binding proteins of the African malaria vector Anopheles gambiae. Insect Mol Biol 15: 797-811. doi:10.1111/j.1365-2583.2006.00685.x. PubMed: 17201772.
[38]  Angerer LM, Angerer RC (1992) In situ hybridization to cellular RNA with radiolabelled RNA probes. In: DG Wilkinson. In situ hybridization. Oxford: IRL Press. p. 2.
[39]  Ott SR (2008) Confocal microscopy in large insect brains: zinc-formaldehyde fixation improves synapsin immunostaining and preservation of morphology in whole-mounts. J Neurosci Methods 172: 220-230. doi:10.1016/j.jneumeth.2008.04.031. PubMed: 18585788.
[40]  Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63: 1658-1676. doi:10.1007/s00018-005-5607-0. PubMed: 16786224.
[41]  Forstner M, Breer H, Krieger J (2009) A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int J Biol Sci 5: 745-757. PubMed: 20011135.
[42]  Grosse-Wilde E, Gohl T, Bouché E, Breer H, Krieger J (2007) Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci 25: 2364-2373. doi:10.1111/j.1460-9568.2007.05512.x. PubMed: 17445234.
[43]  Nardi JB, Miller LA, Walden KK, Rovelstad S, Wang L et al. (2003) Expression patterns of odorant-binding proteins in antennae of the moth Manduca sexta. Cell Tissue Res 313: 321-333. doi:10.1007/s00441-003-0766-5. PubMed: 12905063.
[44]  Maida R, Mameli M, Müller B, Krieger J, Steinbrecht RA (2005) The expression pattern of four odorant-binding proteins in male and female silk moths, Bombyx mori. J Neurocytol 34: 149-163. doi:10.1007/s11068-005-5054-8. PubMed: 16374716.
[45]  Shanbhag SR, Hekmat-Scafe D, Kim MS, Park SK, Carlson JR et al. (2001) Expression mosaic of odorant-binding proteins in Drosophila olfactory organs. Microsc Res Tech 55: 297-306. doi:10.1002/jemt.1179. PubMed: 11754509.
[46]  Hekmat-Scafe DS, Steinbrecht RA, Carlson JR (1997) Coexpression of two odorant-binding protein homologs in Drosophila: implications for olfactory coding. J Neurosci 17: 1616-1624. PubMed: 9030621.
[47]  Xu YL, He P, Zhang L, Fang SQ, Dong SL et al. (2009) Large-scale identification of odorant-binding proteins and chemosensory proteins from expressed sequence tags in insects. BMC Genomics 10: 632. doi:10.1186/1471-2164-10-632. PubMed: 20034407.
[48]  Manoharan M, Fuk Ng, Va?tinadapoulé A, Frumence E, Sowdhamini R et al. (2013) Comparative genomics of odorant binding proteins in Anopheles gambiae, Aedes aegypti, and Culex quinquefasciatus. Genome Biol Evol 5: 163-180. doi:10.1093/gbe/evs131. PubMed: 23292137.
[49]  Shanbhag SR, Smith DP, Steinbrecht RA (2005) Three odorant-binding proteins are co-expressed in sensilla trichodea of Drosophila melanogaster. Arthropod Struct Dev 34: 153-165. doi:10.1016/j.asd.2005.01.003.
[50]  Laughlin JD, Ha TS, Jones DN, Smith DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133: 1255-1265. doi:10.1016/j.cell.2008.04.046. PubMed: 18585358.
[51]  Xu PX, Atkinson R, Jones DNM, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45: 193-200. doi:10.1016/j.neuron.2004.12.031. PubMed: 15664171.
[52]  Grosse-Wilde E, Svatos A, Krieger J (2006) A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Sens 31: 547-555. doi:10.1093/chemse/bjj059.
[53]  Syed Z, Ishida Y, Taylor K, Kimbrell DA, Leal WS (2006) Pheromone reception in fruit flies expressing a moth’s odorant receptor. Proc Natl Acad Sci U S A 103: 16538-16543. doi:10.1073/pnas.0607874103. PubMed: 17060610.
[54]  Steinbrecht RA (1970) Zur Morphometrie der Antenne des Seidenspinners, Bombyx mori L.: Zahl und Verteilung der Riechsensillen (Insecta, Lepidoptera). Z Morph Tiere 68: 93-126.
[55]  Meng LZ, Wu CH, Wicklein M, Kaissling K-E, Bestmann H-J (1989) Number and sensitivity of three types of pheromone receptor cells in Antheraea pernyi and A. polyphemus. J Comp Physiol A 165: 139-146. doi:10.1007/BF00619188.
[56]  Takken W, Knols BG (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131-157. doi:10.1146/annurev.ento.44.1.131. PubMed: 9990718.
[57]  Zwiebel LJ, Takken W (2004) Olfactory regulation of mosquito-host interactions. Insect Biochem Mol Biol 34: 645-652. doi:10.1016/j.ibmb.2004.03.017. PubMed: 15242705.

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