Antennal expression pattern of two olfactory receptors and an odorant binding protein implicated in host odor detection by the malaria vector Anopheles gambiae

International Journal of Biological Sciences

Volumn 6, Issue 7, 2010, Pages 614-626

  Schymura, Danuta ^a   Forstner, Maike ^a,d   Schultze, Anna ^a   Kröber, Thomas ^c   Swevers, Luc ^b   Iatrou, Kostas ^b   Krieger, Jürgen ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^c UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^d BAYER CROPSCIENCE AG   (Germany)

Author keywords

mRNA expression; Odorant binding proteins; Odorant receptor proteins; Olfaction; Sexual dimorphism

Indexed keywords

ANOPHELES GAMBIAE;

EID: 78650588918     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.6.614     Document Type: Article

References (55)

1. Smallegange RC, Qiu YT, van Loon JJ, Takken W. Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). Chem. Senses 2005; 30: 145-52.
2. Takken W, Knols BG. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 1999; 44: 131-57.
3. Foster WA. Mosquito sugar feeding and reproductive energetics. Annu. Rev. Entomol. 1995; 40: 443-74.
4. Pitts RJ, Zwiebel LJ. Antennal sensilla of two female anopheline sibling species with differing host ranges. Malaria J. 2006; 5: 26.
5. McIver SB. Sensilla of mosquitoes (Diptera: Culicidae). J. Med. Entomol. 1982; 19: 489-535.
6. Steinbrecht RA, Gnatzy W. Pheromone receptors in Bombyx mori and Antheraea pernyi. I. Reconstruction of the cellular organization of the sensilla trichodea. Cell Tissue Res. 1984; 235: 25-34.
7. Steinbrecht RA, Ozaki M, Ziegelberger G. Immunocytochemical localization of pheromone-binding protein in moth antennae. Cell Tissue Res. 1992; 270: 287-302.
8. Xu PX, Zwiebel LJ, Smith DP. Identification of a distinct family of genes encoding atypical odorant-binding proteins in the malaria vector mosquito, Anopheles gambiae. Insect Mol. Biol. 2003; 12: 549-60.
9. Vogt RG. 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. 2002; 28: 2371-6.
10. Zhou JJ, Huang W, Zhang GA, Pickett JA, Field LM. Plus-C odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene 2004; 327: 117-29.
11. Biessmann H, Walter MF, Dimitratos S, Woods D. Isolation of cDNA clones encoding putative odourant binding proteins from the antennae of the malaria-transmitting mosquito, Anopheles gambiae. Insect Mol Biol 2002; 11: 123-32.
12. Fox AN, Pitts RJ, Zwiebel LJ. A cluster of candidate odorant receptors from the malaria vector mosquito, Anopheles gambiae. Chem. Senses 2002; 27: 453-9.
13. Fox AN, Pitts RJ, Robertson HM, Carlson JR, Zwiebel LJ. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc. Natl. Acad. Sci. USA 2001; 98: 14693-7.
14. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ. G protein- coupled receptors in Anopheles gambiae. Science 2002; 298: 176-8.
15. Hallem EA, Nicole FA, Zwiebel LJ, Carlson JR. Olfaction: mosquito receptor for human-sweat odorant. Nature 2004; 427: 212-3.
16. Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR. Odorant reception in the malaria mosquito Anopheles gambiae. Nature 2010; 464: 66-71.
17. Wang G, Carey AF, Carlson JR, Zwiebel LJ. Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A 2010; 107: 4418-23.
18. Iatrou K, Biessmann H. Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae. Insect Biochem. Mol. Biol. 2008; 38: 268-74.
19. Meijerink J, Braks MA, Brack AA, Adam W, Dekker T, Posthumus MA, van Beek TA, van Loon JJA. Identification of olfactory stimulants for Anopheles gambiae from human sweat samples. J. Chem. Ecol. 2000; 26: 1367-82.
20. Blackwell A, Johnson SN. Electrophysiological investigation of larval water and potential oviposition chemo-attractants for Anopheles gambiae s.s. Ann. Trop. Med. Parasitol. 2000; 94: 389-98.
21. Knudson JT, Eriksson R, Gershenzon J, Stahl B. Diversity and distribution of floral scent. Botanical Review 2006; 72: 1-20.
22. Biessmann H, Andronopoulou E, Biessmann MR, Douris V, Dimitratos SD, Eliopoulos E, Guerin PM, Iatrou K, Justice RW, Krober T, Marinotti O, Tsitoura P, Woods DF, Walter MF. The Anopheles gambiae Odorant Binding Protein 1 (AgamOBP1) mediates indole recognition in the antennae of female mosquitoes. PLoS ONE 2010; 5: e9471.
23. Krieger J, Grosse-Wilde E, Gohl T, Dewer YME, Raming K, Breer H. Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc. Natl. Acad. Sci. U. S. A 2004; 101: 11845-50.
24. Krieger J, Grosse-Wilde E, Gohl T, Breer H. Candidate pheromone receptors of the silkmoth Bombyx mori. Eur. J. Neurosci. 2005; 21: 2167-76.
25. Nakagawa T, Sakurai T, Nishioka T, Touhara K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 2005; 307: 1638-42.
26. Mitsuno H, Sakurai T, Murai M, Yasuda T, Kugimiya S, Ozawa R, Toyohara H, Takabayashi J, Miyoshi H, Nishioka T. Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur. J. Neurosci. 2008; 28: 893-902.
27. Krieger J, Gondesen I, Forstner M, Gohl T, Dewer Y, Breer H. HR11 and HR13 receptor-expressing neurons are housed together in pheromone-responsive sensilla trichodea of male Heliothis virescens. Chem. Senses 2009; 34: 469-77.
28. Pitts RJ, Fox AN, Zwiebel LJ. A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A 2004; 101: 5058-63.
29. Tsitoura P, Andronopoulou E, Tsikou D, Agalou A, Papakonstantinou MP, Kotzia GA, Labropoulou V, Swevers L, Georgoussi Z, Iatrou K. Expression and membrane topology of Anopheles gambiae odorant receptors in lepidopteran insect cells. PLoS ONE 2010; in press.
30. Timmermann SE, Briegel H. Water depth and larval density affect development and accumulation of reserves in laboratory populations of mosquitoes. Bull. Soc. Vector Ecol. 1993; 18: 174-87.
31. Angerer LM, Angerer RC. In situ hybridization to cellular RNA with radiolabelled RNA probes. In: Wilkinson DG, ed. In situ hybridization. Oxford: IRL Press, 1992.
32. Belton P. Attraction of male mosquitoes to sound. J. Am. Mosq. Control Assoc. 1994; 10: 297-301.
33. Forstner M, Gohl T, Breer H, Krieger J. Candidate pheromone binding proteins of the silkmoth Bombyx mori. Invert. Neurosci. 2006; 6: 177-87.
34. Qiu YT, van Loon JJ, Takken W, Meijerink J, Smid HM. Olfactory Coding in Antennal Neurons of the Malaria Mosquito, Anopheles gambiae. Chem. Senses 2006; 31: 845-63.
35. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 1999; 96: 725-36.
36. Vosshall LB, Wong AM, Axel R. An olfactory sensory map in the fly brain. Cell 2000; 102: 147-59.
37. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 1999; 22: 327-38.
38. Howell PI, Knols BG. Male mating biology. Malar J. 2009; 8 (Suppl 2): S8.
39. Ray A, van Naters WG, Shiraiwa T, Carlson JR. Mechanisms of odor receptor gene choice in Drosophila. Neuron 2007; 53: 353-69.
40. Clyne PJ, Certel SJ, de Bruyne M, Zaslavsky L, Johnson WA, Carlson JR. The odor specificities of a subset of olfactory receptor neurons are governed by Acj6, a POU-domain transcription factor. Neuron 1999; 22: 339-47.
41. Miller CJ, Carlson JR. Regulation of Odor Receptor Genes in Trichoid Sensilla of the Drosophila Antenna. Genetics 2010; 186:79-95.
42. Miyamichi K, Serizawa S, Kimura HM, Sakano H. Continuous and Overlapping Expression Domains of Odorant Receptor Genes in the Olfactory Epithelium Determine the Dorsal/Ventral Positioning of Glomeruli in the Olfactory Bulb. J. Neurosci. 2005; 25: 3586-92.
43. Iwema CL, Fang H, Kurtz DB, Youngentob SL, Schwob JE. Odorant receptor expression patterns are restored in lesion- recovered rat olfactory epithelium. J. Neurosci. 2004; 24: 356-69.
44. Ressler KJ, Sullivan SL, Buck LB. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 1993; 73: 597-609.
45. Vassar R, Ngai J, Axel R. Spati al segregati on of odor ant recept or expression in the mamalian olfactory epithelium. Cell 1993; 74: 309-18.
46. Forstner M, Breer H, Krieger J. A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int. J. Biol. Sci. 2009; 5: 745-57.
47. Grosse-Wilde E, Gohl T, Bouche E, Breer H, Krieger J. Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur. J. Neurosci. 2007; 25: 2364-73.
48. Grosse-Wilde E, Svatos A, Krieger J. A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses 2006; 31: 547-55.
49. Laughlin JD, Ha TS, Jones DN, Smith DP. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 2008; 133: 1255-65.
50. Xu PX, Atkinson R, Jones DNM, Smith DP. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 2005; 45: 193-200.
51. Shanbhag SR, Smith DP, Steinbrecht RA. Three odorant- binding proteins are co-expressed in sensilla trichodea of Drosophila melanogaster. Arthropod Structure & Development 2005; 34: 153-65.
52. Qiao H, Xiaoli H, Schymura D, Ban L, Field L, Dani FR, Michelucci E, Caputo B, della Torre A, Iatrou K, Krieger J, Zhou JJ, Pelosi P. Coomparative interactions between odorant- binding proteins of Anophels gambiae. Cell. Mol. Life Sci. 2010; in press.
53. Andronopoulou E, Labropoulou V, Douris V, Woods DF, Biessmann H, Iatrou K. Specific interactions among odorant- binding proteins of the African malaria vector Anopheles gambiae. Insect Mol. Biol. 2006; 15: 797-811.
54. Tegoni M, Ramoni R, Bignetti E, Spinelli S, Cambillau C. Domain swapping creates a third putative combining site in bovi ne odorant bi ndi ng protei n di mer. Nature Struct. Biol. 1996; 3: 863-7.
55. Bianchet MA, Bains G, Pelosi P, Pevsner J, Snyder SH, Monaco HL, Amzel LM. The three-dimensional structure of bovine odorant binding protein and its mechanism of odor recognition. Nature Struct. Biol. 1996; 3: 934-9.