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. 2003 Aug;164(4):1447–1457. doi: 10.1093/genetics/164.4.1447

Scribble is essential for olfactory behavior in Drosophila melanogaster.

Indrani Ganguly 1, Trudy F C Mackay 1, Robert R H Anholt 1
PMCID: PMC1462661  PMID: 12930751

Abstract

The ability to discriminate and respond to chemical signals from the environment is an almost universal prerequisite for survival. Here, we report that the scaffold protein Scribble is essential for odor-guided behavior in Drosophila. Previously, we identified a P-element insert line with generalized sexually dimorphic smell impairment, smi97B. We found that the transposon in this line is located between the predicted promoter region and the transcription initiation site of scrib. A deficiency in this region, Df(3R)Tl-X, and two scrib null alleles fail to complement the smell-impaired phenotype of smi97B. Wild-type behavior is restored by precise excision of the P element, scrib mRNA levels correspond with mutant and wild-type phenotypes, and introduction of a full-length scrib transgene in the smi97B mutant rescues the olfactory deficit. Expression of Scrib is widespread in olfactory organs and the central nervous system. Finally, alternative splicing of scrib generates transcripts that differ in the number of leucine-rich repeats and PDZ domains.

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Selected References

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  1. Anand A., Villella A., Ryner L. C., Carlo T., Goodwin S. F., Song H. J., Gailey D. A., Morales A., Hall J. C., Baker B. S. Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics. 2001 Aug;158(4):1569–1595. doi: 10.1093/genetics/158.4.1569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anholt R. R., Lyman R. F., Mackay T. F. Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics. 1996 May;143(1):293–301. doi: 10.1093/genetics/143.1.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ball R., Braun M. M., Mootrey G. T., Vaccine Adverse Event Reporting System Working Group Safety data on meningococcal polysaccharide vaccine from the Vaccine Adverse Event Reporting System. Clin Infect Dis. 2001 Apr 3;32(9):1273–1280. doi: 10.1086/319982. [DOI] [PubMed] [Google Scholar]
  4. Bellen H. J., Kiger J. A., Jr Sexual hyperactivity and reduced longevity of dunce females of Drosophila melanogaster. Genetics. 1987 Jan;115(1):153–160. doi: 10.1093/genetics/115.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benzer S. Genetic dissection of behavior. Sci Am. 1973 Dec;229(6):24–37. doi: 10.1038/scientificamerican1273-24. [DOI] [PubMed] [Google Scholar]
  6. Bilder D., Li M., Perrimon N. Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science. 2000 Jul 7;289(5476):113–116. doi: 10.1126/science.289.5476.113. [DOI] [PubMed] [Google Scholar]
  7. Bilder D. PDZ proteins and polarity: functions from the fly. Trends Genet. 2001 Sep;17(9):511–519. doi: 10.1016/s0168-9525(01)02407-6. [DOI] [PubMed] [Google Scholar]
  8. Bilder D., Perrimon N. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature. 2000 Feb 10;403(6770):676–680. doi: 10.1038/35001108. [DOI] [PubMed] [Google Scholar]
  9. Bowers B. J., Wehner J. M. Ethanol consumption and behavioral impulsivity are increased in protein kinase Cgamma null mutant mice. J Neurosci. 2001 Nov 1;21(21):RC180–RC180. doi: 10.1523/JNEUROSCI.21-21-j0004.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cline T. W., Meyer B. J. Vive la différence: males vs females in flies vs worms. Annu Rev Genet. 1996;30:637–702. doi: 10.1146/annurev.genet.30.1.637. [DOI] [PubMed] [Google Scholar]
  11. Corry D. B. Sex-related differences in the insulin resistance syndrome. Curr Hypertens Rep. 2001 Apr;3(2):124–128. doi: 10.1007/s11906-001-0024-8. [DOI] [PubMed] [Google Scholar]
  12. Fanara Juan José, Robinson Kellie O., Rollmann Stephanie M., Anholt Robert R. H., Mackay Trudy F. C. Vanaso is a candidate quantitative trait gene for Drosophila olfactory behavior. Genetics. 2002 Nov;162(3):1321–1328. doi: 10.1093/genetics/162.3.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fox A. N., Pitts R. J., Robertson H. M., Carlson J. R., Zwiebel L. J. 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. 2001 Nov 27;98(25):14693–14697. doi: 10.1073/pnas.261432998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fujii Shinsuke, Amrein Hubert. Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. EMBO J. 2002 Oct 15;21(20):5353–5363. doi: 10.1093/emboj/cdf556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Graveley Brenton R. Sex, AGility, and the regulation of alternative splicing. Cell. 2002 May 17;109(4):409–412. doi: 10.1016/s0092-8674(02)00750-x. [DOI] [PubMed] [Google Scholar]
  16. Greenspan R. J. A kinder, gentler genetic analysis of behavior: dissection gives way to modulation. Curr Opin Neurobiol. 1997 Dec;7(6):805–811. doi: 10.1016/s0959-4388(97)80139-0. [DOI] [PubMed] [Google Scholar]
  17. Griffith L. C., Verselis L. M., Aitken K. M., Kyriacou C. P., Danho W., Greenspan R. J. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron. 1993 Mar;10(3):501–509. doi: 10.1016/0896-6273(93)90337-q. [DOI] [PubMed] [Google Scholar]
  18. Heimbeck G., Bugnon V., Gendre N., Häberlin C., Stocker R. F. Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J Neurosci. 1999 Aug 1;19(15):6599–6609. doi: 10.1523/JNEUROSCI.19-15-06599.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jin W., Riley R. M., Wolfinger R. D., White K. P., Passador-Gurgel G., Gibson G. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat Genet. 2001 Dec;29(4):389–395. doi: 10.1038/ng766. [DOI] [PubMed] [Google Scholar]
  20. Kulkarni Nalini H., Yamamoto Akihiko H., Robinson Kellie O., Mackay Trudy F. C., Anholt Robert R. H. The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. Genetics. 2002 Aug;161(4):1507–1516. doi: 10.1093/genetics/161.4.1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Li M., Marhold J., Gatos A., Török I., Mechler B. M. Differential expression of two scribble isoforms during Drosophila embryogenesis. Mech Dev. 2001 Oct;108(1-2):185–190. doi: 10.1016/s0925-4773(01)00482-8. [DOI] [PubMed] [Google Scholar]
  22. Mackay T. F., Hackett J. B., Lyman R. F., Wayne M. L., Anholt R. R. Quantitative genetic variation of odor-guided behavior in a natural population of Drosophila melanogaster. Genetics. 1996 Oct;144(2):727–735. doi: 10.1093/genetics/144.2.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mackay T. F., Hackett J. B., Lyman R. F., Wayne M. L., Anholt R. R. Quantitative genetic variation of odor-guided behavior in a natural population of Drosophila melanogaster. Genetics. 1996 Oct;144(2):727–735. doi: 10.1093/genetics/144.2.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mathew Dennis, Gramates L. Sian, Packard Mary, Thomas Ulrich, Bilder David, Perrimon Norbert, Gorczyca Michael, Budnik Vivian. Recruitment of scribble to the synaptic scaffolding complex requires GUK-holder, a novel DLG binding protein. Curr Biol. 2002 Apr 2;12(7):531–539. doi: 10.1016/s0960-9822(02)00758-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nadeau J. H., Frankel W. N. The roads from phenotypic variation to gene discovery: mutagenesis versus QTLs. Nat Genet. 2000 Aug;25(4):381–384. doi: 10.1038/78051. [DOI] [PubMed] [Google Scholar]
  26. Price J. L., Blau J., Rothenfluh A., Abodeely M., Kloss B., Young M. W. double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell. 1998 Jul 10;94(1):83–95. doi: 10.1016/s0092-8674(00)81224-6. [DOI] [PubMed] [Google Scholar]
  27. Roche John P., Packard Mary C., Moeckel-Cole Stephanie, Budnik Vivian. Regulation of synaptic plasticity and synaptic vesicle dynamics by the PDZ protein Scribble. J Neurosci. 2002 Aug 1;22(15):6471–6479. doi: 10.1523/JNEUROSCI.22-15-06471.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shaver S. A., Varnam C. J., Hilliker A. J., Sokolowski M. B. The foraging gene affects adult but not larval olfactory-related behavior in Drosophila melanogaster. Behav Brain Res. 1998 Sep;95(1):23–29. doi: 10.1016/s0166-4328(97)00206-4. [DOI] [PubMed] [Google Scholar]
  29. Sheng M., Sala C. PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci. 2001;24:1–29. doi: 10.1146/annurev.neuro.24.1.1. [DOI] [PubMed] [Google Scholar]
  30. Sokolowski M. B. Genes for normal behavioral variation: recent clues from flies and worms. Neuron. 1998 Sep;21(3):463–466. doi: 10.1016/s0896-6273(00)80556-5. [DOI] [PubMed] [Google Scholar]
  31. Towne B., Almasy L., Siervogel R. M., Blangero J. Effects of genotype x sex interaction on linkage analysis of visual event-related evoked potentials. Genet Epidemiol. 1999;17 (Suppl 1):S355–S360. doi: 10.1002/gepi.1370170760. [DOI] [PubMed] [Google Scholar]
  32. Tully T. Discovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13460–13467. doi: 10.1073/pnas.93.24.13460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vosshall L. B. The molecular logic of olfaction in Drosophila. Chem Senses. 2001 Feb;26(2):207–213. doi: 10.1093/chemse/26.2.207. [DOI] [PubMed] [Google Scholar]
  34. Warr C., Clyne P., de Bruyne M., Kim J., Carlson J. R. Olfaction in Drosophila: coding, genetics and e-genetics. Chem Senses. 2001 Feb;26(2):201–206. doi: 10.1093/chemse/26.2.201. [DOI] [PubMed] [Google Scholar]
  35. Wu L. P., Choe K. M., Lu Y., Anderson K. V. Drosophila immunity: genes on the third chromosome required for the response to bacterial infection. Genetics. 2001 Sep;159(1):189–199. doi: 10.1093/genetics/159.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yang P., Shaver S. A., Hilliker A. J., Sokolowski M. B. Abnormal turning behavior in Drosophila larvae. Identification and molecular analysis of scribbler (sbb). Genetics. 2000 Jul;155(3):1161–1174. doi: 10.1093/genetics/155.3.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]

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