• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Oct 1998; 150(2): 711–721.
PMCID: PMC1460366

LUSH odorant-binding protein mediates chemosensory responses to alcohols in Drosophila melanogaster.

Abstract

The molecular mechanisms mediating chemosensory discrimination in insects are unknown. Using the enhancer trapping approach, we identified a new Drosophila mutant, lush, with odorant-specific defects in olfactory behavior. lush mutant flies are abnormally attracted to high concentrations of ethanol, propanol, and butanol but have normal chemosensory responses to other odorants. We show that wild-type flies have an active olfactory avoidance mechanism to prevent attraction to concentrated alcohol, and this response is defective in lush mutants. This suggests that the defective olfactory behavior associated with the lush mutation may result from a specific defect in chemoavoidance. lush mutants have a 3-kb deletion that produces a null allele of a new member of the invertebrate odorant-binding protein family, LUSH. LUSH is normally expressed exclusively in a subset of trichoid chemosensory sensilla located on the ventral-lateral surface of the third antennal segment. LUSH is secreted from nonneuronal support cells into the sensillum lymph that bathes the olfactory neurons within these sensilla. Reintroduction of a cloned wild-type copy of lush into the mutant background completely restores wild-type olfactory behavior, demonstrating that this odorant-binding protein is required in a subset of sensilla for normal chemosensory behavior to a subset of odorants. These findings provide direct evidence that odorant-binding proteins are required for normal chemosensory behavior in Drosophila and may partially determine the chemical specificity of olfactory neurons in vivo.

Full Text

The Full Text of this article is available as a PDF (506K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991 Apr 5;65(1):175–187. [PubMed]
  • Callahan CA, Thomas JB. Tau-beta-galactosidase, an axon-targeted fusion protein. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5972–5976. [PMC free article] [PubMed]
  • Chakir M, Peridy O, Capy P, Pla E, David JR. Adaptation to alcoholic fermentation in Drosophila: a parallel selection imposed by environmental ethanol and acetic acid. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3621–3625. [PMC free article] [PubMed]
  • Cinelli AR, Hamilton KA, Kauer JS. Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. J Neurophysiol. 1995 May;73(5):2053–2071. [PubMed]
  • Davis RL, Cherry J, Dauwalder B, Han PL, Skoulakis E. The cyclic AMP system and Drosophila learning. Mol Cell Biochem. 1995 Aug-Sep;149-150:271–278. [PubMed]
  • Du G, Prestwich GD. Protein structure encodes the ligand binding specificity in pheromone binding proteins. Biochemistry. 1995 Jul 11;34(27):8726–8732. [PubMed]
  • Dubin AE, Heald NL, Cleveland B, Carlson JR, Harris GL. Scutoid mutation of Drosophila melanogaster specifically decreases olfactory responses to short-chain acetate esters and ketones. J Neurobiol. 1995 Oct;28(2):214–233. [PubMed]
  • Flower DR. The lipocalin protein family: structure and function. Biochem J. 1996 Aug 15;318(Pt 1):1–14. [PMC free article] [PubMed]
  • Györgyi TK, Roby-Shemkovitz AJ, Lerner MR. 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 U S A. 1988 Dec;85(24):9851–9855. [PMC free article] [PubMed]
  • Hall JC. The mating of a fly. Science. 1994 Jun 17;264(5166):1702–1714. [PubMed]
  • Hartenstein V, Posakony JW. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development. 1989 Oct;107(2):389–405. [PubMed]
  • Hekmat-Scafe DS, Steinbrecht RA, Carlson JR. Coexpression of two odorant-binding protein homologs in Drosophila: implications for olfactory coding. J Neurosci. 1997 Mar 1;17(5):1616–1624. [PubMed]
  • Alcorta E. Characterization of the electroantennogram in Drosophila melanogaster and its use for identifying olfactory capture and transduction mutants. J Neurophysiol. 1991 Mar;65(3):702–714. [PubMed]
  • Karess RE, Rubin GM. Analysis of P transposable element functions in Drosophila. Cell. 1984 Aug;38(1):135–146. [PubMed]
  • Alcorta E, Rubio J. Genetical analysis of intrapopulational variation in olfactory response in Drosophila melanogaster. Heredity (Edinb) 1988 Feb;60(Pt 1):7–14. [PubMed]
  • Alcorta E, Rubio J. Intrapopulational variation of olfactory responses in Drosophila melanogaster. Behav Genet. 1989 Mar;19(2):285–299. [PubMed]
  • Langer-Safer PR, Levine M, Ward DC. Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4381–4385. [PMC free article] [PubMed]
  • Ayer RK, Jr, Carlson J. Olfactory physiology in the Drosophila antenna and maxillary palp: acj6 distinguishes two classes of odorant pathways. J Neurobiol. 1992 Oct;23(8):965–982. [PubMed]
  • Bargmann CI, Horvitz HR. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron. 1991 Nov;7(5):729–742. [PubMed]
  • Bargmann CI, Thomas JH, Horvitz HR. Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol. 1990;55:529–538. [PubMed]
  • Bargmann CI, Hartwieg E, Horvitz HR. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell. 1993 Aug 13;74(3):515–527. [PubMed]
  • Bellen HJ, O'Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring WJ. P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 1989 Sep;3(9):1288–1300. [PubMed]
  • Monte P, Woodard C, Ayer R, Lilly M, Sun H, Carlson J. Characterization of the larval olfactory response in Drosophila and its genetic basis. Behav Genet. 1989 Mar;19(2):267–283. [PubMed]
  • Pelosi P. Odorant-binding proteins. Crit Rev Biochem Mol Biol. 1994;29(3):199–228. [PubMed]
  • Pelosi P, Baldaccini NE, Pisanelli AM. Identification of a specific olfactory receptor for 2-isobutyl-3-methoxypyrazine. Biochem J. 1982 Jan 1;201(1):245–248. [PMC free article] [PubMed]
  • Smith DP. Olfactory mechanisms in Drosophila melanogaster. Curr Opin Neurobiol. 1996 Aug;6(4):500–505. [PubMed]
  • Smith DP, Ranganathan R, Hardy RW, Marx J, Tsuchida T, Zuker CS. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science. 1991 Dec 6;254(5037):1478–1484. [PubMed]
  • Pevsner J, Hou V, Snowman AM, Snyder SH. Odorant-binding protein. Characterization of ligand binding. J Biol Chem. 1990 Apr 15;265(11):6118–6125. [PubMed]
  • Stamnes MA, Shieh BH, Chuman L, Harris GL, Zuker CS. The cyclophilin homolog ninaA is a tissue-specific integral membrane protein required for the proper synthesis of a subset of Drosophila rhodopsins. Cell. 1991 Apr 19;65(2):219–227. [PubMed]
  • Pfeiffer CA, Johnston RE. Hormonal and behavioral responses of male hamsters to females and female odors: roles of olfaction, the vomeronasal system, and sexual experience. Physiol Behav. 1994 Jan;55(1):129–138. [PubMed]
  • Pikielny CW, Hasan G, Rouyer F, Rosbash M. Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron. 1994 Jan;12(1):35–49. [PubMed]
  • Steinbrecht RA. Are odorant-binding proteins involved in odorant discrimination? Chem Senses. 1996 Dec;21(6):719–727. [PubMed]
  • Stocker RF. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 1994 Jan;275(1):3–26. [PubMed]
  • Stocker RF, Singh RN, Schorderet M, Siddiqi O. Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res. 1983;232(2):237–248. [PubMed]
  • Raming K, Krieger J, Breer H. Molecular cloning of an insect pheromone-binding protein. FEBS Lett. 1989 Oct 9;256(1-2):215–218. [PubMed]
  • Raming K, Krieger J, Breer H. Primary structure of a pheromone-binding protein from Antheraea pernyi: homologies with other ligand-carrying proteins. J Comp Physiol B. 1990;160(5):503–509. [PubMed]
  • Tripoulas NA, Hersperger E, La Jeunesse D, Shearn A. Molecular genetic analysis of the Drosophila melanogaster gene absent, small or homeotic discs1 (ash1). Genetics. 1994 Aug;137(4):1027–1038. [PMC free article] [PubMed]
  • Riesgo-Escovar J, Woodard C, Gaines P, Carlson J. Development and organization of the Drosophila olfactory system: an analysis using enhancer traps. J Neurobiol. 1992 Oct;23(8):947–964. [PubMed]
  • Troemel ER, Kimmel BE, Bargmann CI. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell. 1997 Oct 17;91(2):161–169. [PubMed]
  • Riesgo-Escovar JR, Piekos WB, Carlson JR. The Drosophila antenna: ultrastructural and physiological studies in wild-type and lozenge mutants. J Comp Physiol A. 1997 Feb;180(2):151–160. [PubMed]
  • Vogt RG, Riddiford LM. Pheromone binding and inactivation by moth antennae. Nature. 1981 Sep 10;293(5828):161–163. [PubMed]
  • Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. [PMC free article] [PubMed]
  • Vogt RG, Riddiford LM, Prestwich GD. Kinetic properties of a sex pheromone-degrading enzyme: the sensillar esterase of Antheraea polyphemus. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8827–8831. [PMC free article] [PubMed]
  • Rodrigues V. Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res. 1988 Jun 21;453(1-2):299–307. [PubMed]
  • Rodrigues V, Buchner E. [3H]2-deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster. Brain Res. 1984 Dec 24;324(2):374–378. [PubMed]
  • Vogt RG, Rybczynski R, Lerner MR. 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. 1991 Oct;11(10):2972–2984. [PubMed]
  • Roelofs WL. Chemistry of sex attraction. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):44–49. [PMC free article] [PubMed]
  • Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA, Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. [PubMed]
  • von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. [PMC free article] [PubMed]
  • Woodard C, Huang T, Sun H, Helfand SL, Carlson J. Genetic analysis of olfactory behavior in Drosophila: a new screen yields the ota mutants. Genetics. 1989 Oct;123(2):315–326. [PMC free article] [PubMed]
  • Sass GL, Mohler JD, Walsh RC, Kalfayan LJ, Searles LL. Structure and expression of hybrid dysgenesis-induced alleles of the ovarian tumor (otu) gene in Drosophila melanogaster. Genetics. 1993 Feb;133(2):253–263. [PMC free article] [PubMed]
  • Zhao H, Ivic L, Otaki JM, Hashimoto M, Mikoshiba K, Firestein S. Functional expression of a mammalian odorant receptor. Science. 1998 Jan 9;279(5348):237–242. [PubMed]
  • Sengupta P, Chou JH, Bargmann CI. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell. 1996 Mar 22;84(6):899–909. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Cited in Books
    Cited in Books
    PubMed Central articles cited in books
  • Gene
    Gene
    Gene links
  • GEO Profiles
    GEO Profiles
    Related GEO records
  • HomoloGene
    HomoloGene
    HomoloGene links
  • MedGen
    MedGen
    Related information in MedGen
  • Pathways + GO
    Pathways + GO
    Pathways, annotations and biological systems (BioSystems) that cite the current article.
  • Protein
    Protein
    Published protein sequences
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links
  • Taxonomy
    Taxonomy
    Related taxonomy entry
  • Taxonomy Tree
    Taxonomy Tree

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...