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. 1993 Apr;133(4):955–965. doi: 10.1093/genetics/133.4.955

A Genetic Analysis of the Stoned Locus and Its Interaction with Dunce, Shibire and Suppressor of Stoned Variants of Drosophila Melanogaster

T Z Petrovich 1, J Merakovsky 1, L E Kelly 1
PMCID: PMC1205412  PMID: 8462853

Abstract

The genetic complementation patterns of both behavioral and lethal alleles at the stoned locus have been characterized. Mosaic analysis of a stoned lethal allele suggests that stoned functions either in the nervous system or in both the nervous system and musculature, but is not required for gross neural development. The behavioral alleles stn(ts) and stn(C), appear to be defective in a diametrically opposite sense, show interallelic complementation, and indicate distinct roles for the stoned gene product in the visual system and in motor coordination. A number of other neurological mutations have been investigated for their possible interaction with the viable stoned alleles. Mutations at two loci, dunce and shibire, act synergistically with the stn(ts) mutations to cause lethality, but fail to interact with stn(C). A third variant (Suppressor of stoned) has been identified which can suppress the debilitation associated with the stn(ts) mutations. These data, together with a previously identified interaction between the stn(ts) and tan mutants, indicate a central role for the stoned gene product in neuronal function, and suggests that the stoned gene product interacts, either directly or indirectly, with the neural cAMP second messenger system, with the synaptic membrane recycling pathway via dynamin, and with biogenic amine metabolism.

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Selected References

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  1. 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]
  2. Booker R., Quinn W. G. Conditioning of leg position in normal and mutant Drosophila. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3940–3944. doi: 10.1073/pnas.78.6.3940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buxbaum J. D., Dudai Y. In vivo protein phosphorylation in Drosophila mutants defective in learning and memory. Neurosci Lett. 1989 Oct 9;104(3):351–355. doi: 10.1016/0304-3940(89)90602-2. [DOI] [PubMed] [Google Scholar]
  4. Byers D., Davis R. L., Kiger J. A., Jr Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature. 1981 Jan 1;289(5793):79–81. doi: 10.1038/289079a0. [DOI] [PubMed] [Google Scholar]
  5. Campos A. R., Grossman D., White K. Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J Neurogenet. 1985 Jun;2(3):197–218. doi: 10.3109/01677068509100150. [DOI] [PubMed] [Google Scholar]
  6. Chen M. S., Obar R. A., Schroeder C. C., Austin T. W., Poodry C. A., Wadsworth S. C., Vallee R. B. Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature. 1991 Jun 13;351(6327):583–586. doi: 10.1038/351583a0. [DOI] [PubMed] [Google Scholar]
  7. Cherry J. R., Johnson T. R., Dollard C., Shuster J. R., Denis C. L. Cyclic AMP-dependent protein kinase phosphorylates and inactivates the yeast transcriptional activator ADR1. Cell. 1989 Feb 10;56(3):409–419. doi: 10.1016/0092-8674(89)90244-4. [DOI] [PubMed] [Google Scholar]
  8. Corfas G., Dudai Y. Morphology of a sensory neuron in Drosophila is abnormal in memory mutants and changes during aging. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7252–7256. doi: 10.1073/pnas.88.16.7252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davis R. L., Kiger J. A., Jr Dunce mutants of Drosophila melanogaster: mutants defective in the cyclic AMP phosphodiesterase enzyme system. J Cell Biol. 1981 Jul;90(1):101–107. doi: 10.1083/jcb.90.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dévay P., Friedrich P. Cyclic AMP-induced phosphorylation of 27.5-kDa protein(s) in larval brains of normal and memory-mutant Drosophila melanogaster. J Neurogenet. 1987 Dec;4(6):275–284. [PubMed] [Google Scholar]
  11. Dévay P., Pintér M., Yalcin A. S., Friedrich P. Altered autophosphorylation of adenosine 3',5'-phosphate-dependent protein kinase in the dunce memory mutant of Drosophila melanogaster. Neuroscience. 1986 May;18(1):193–203. doi: 10.1016/0306-4522(86)90188-0. [DOI] [PubMed] [Google Scholar]
  12. Dévay P., Solti M., Kiss I., Dombrádi, Friedrich P. Differences in protein phosphorylation in vivo and in vitro between wild type and dunce mutant strains of Drosophila melanogaster. Int J Biochem. 1984;16(12):1401–1408. doi: 10.1016/0020-711x(84)90248-9. [DOI] [PubMed] [Google Scholar]
  13. Ganetzky B. Genetic studies of membrane excitability in Drosophila: lethal interaction between two temperature-sensitive paralytic mutations. Genetics. 1984 Dec;108(4):897–911. doi: 10.1093/genetics/108.4.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grigliatti T. A., Hall L., Rosenbluth R., Suzuki D. T. Temperature-sensitive mutations in Drosophila melanogaster. XIV. A selection of immobile adults. Mol Gen Genet. 1973 Jan 24;120(2):107–114. doi: 10.1007/BF00267238. [DOI] [PubMed] [Google Scholar]
  15. Hinton C W. The Behavior of an Unstable Ring Chromosome of Drosophila Melanogaster. Genetics. 1955 Nov;40(6):951–961. doi: 10.1093/genetics/40.6.951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Homyk T., Jr, Pye Q. Some mutations affecting neural or muscular tissues alter the physiological components of the electroretinogram in Drosophila. J Neurogenet. 1989 Jan;5(1):37–48. doi: 10.3109/01677068909167263. [DOI] [PubMed] [Google Scholar]
  17. Homyk T., Sheppard D. E. Behavioral Mutants of DROSOPHILA MELANOGASTER. I. Isolation and Mapping of Mutations Which Decrease Flight Ability. Genetics. 1977 Sep;87(1):95–104. doi: 10.1093/genetics/87.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hotta Y., Benzer S. Mapping of behaviour in Drosophila mosaics. Nature. 1972 Dec 29;240(5383):527–535. doi: 10.1038/240527a0. [DOI] [PubMed] [Google Scholar]
  19. Jan Y. N., Jan L. Y., Dennis M. J. Two mutations of synaptic transmission in Drosophila. Proc R Soc Lond B Biol Sci. 1977 Jul 28;198(1130):87–108. doi: 10.1098/rspb.1977.0087. [DOI] [PubMed] [Google Scholar]
  20. Kelly L. E. An altered electroretinogram transient associated with an unusual jump response in a mutant of Drosophila. Cell Mol Neurobiol. 1983 Jun;3(2):143–149. doi: 10.1007/BF00735278. [DOI] [PubMed] [Google Scholar]
  21. Kelly L. E., Suzuki D. T. The effects of increased temperature on electroretinograms of temperature-sensitive paralysis mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1974 Dec;71(12):4906–4909. doi: 10.1073/pnas.71.12.4906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kelly L. E. The regulation of phosphorylation of a specific protein in synaptosomal fractions from Drosophila heads: the effects of light and two visual mutants. Cell Mol Neurobiol. 1983 Jun;3(2):127–141. doi: 10.1007/BF00735277. [DOI] [PubMed] [Google Scholar]
  23. Kessell I., Holst B. D., Roth T. F. Membranous intermediates in endocytosis are labile, as shown in a temperature-sensitive mutant. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4968–4972. doi: 10.1073/pnas.86.13.4968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Koenig J. H., Ikeda K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci. 1989 Nov;9(11):3844–3860. doi: 10.1523/JNEUROSCI.09-11-03844.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kosaka T., Ikeda K. Reversible blockage of membrane retrieval and endocytosis in the garland cell of the temperature-sensitive mutant of Drosophila melanogaster, shibirets1. J Cell Biol. 1983 Aug;97(2):499–507. doi: 10.1083/jcb.97.2.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lifschytz E., Falk R. Fine structure analysis of a chromosome segment in Drosophila melanogaster: analysis of ethyl methanesulphonate-induced lethals. Mutat Res. 1969 Jul-Aug;8(1):147–155. doi: 10.1016/0027-5107(69)90149-3. [DOI] [PubMed] [Google Scholar]
  27. Livingstone M. S. Genetic dissection of Drosophila adenylate cyclase. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5992–5996. doi: 10.1073/pnas.82.17.5992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Livingstone M. S., Sziber P. P., Quinn W. G. Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell. 1984 May;37(1):205–215. doi: 10.1016/0092-8674(84)90316-7. [DOI] [PubMed] [Google Scholar]
  29. Loughney K., Kreber R., Ganetzky B. Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell. 1989 Sep 22;58(6):1143–1154. doi: 10.1016/0092-8674(89)90512-6. [DOI] [PubMed] [Google Scholar]
  30. Masur S. K., Kim Y. T., Wu C. F. Reversible inhibition of endocytosis in cultured neurons from the Drosophila temperature-sensitive mutant shibirets1. J Neurogenet. 1990 Apr;6(3):191–206. doi: 10.3109/01677069009107110. [DOI] [PubMed] [Google Scholar]
  31. Miklos G. L., Kelly L. E., Coombe P. E., Leeds C., Lefevre G. Localization of the genes shaking-B, small optic lobes, sluggish-A, stoned and stress-sensitive-C to a well-defined region on the X-chromosome of Drosophila melanogaster. J Neurogenet. 1987 Jan;4(1):1–19. doi: 10.3109/01677068709102329. [DOI] [PubMed] [Google Scholar]
  32. Modolell J., Bender W., Meselson M. Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7.3-kilobase mobile element. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1678–1682. doi: 10.1073/pnas.80.6.1678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Papazian D. M., Schwarz T. L., Tempel B. L., Jan Y. N., Jan L. Y. Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science. 1987 Aug 14;237(4816):749–753. doi: 10.1126/science.2441470. [DOI] [PubMed] [Google Scholar]
  34. Poodry C. A., Edgar L. Reversible alteration in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire. J Cell Biol. 1979 Jun;81(3):520–527. doi: 10.1083/jcb.81.3.520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rabinow L., Birchler J. A. Interactions of vestigial and scabrous with the Notch locus of Drosophila melanogaster. Genetics. 1990 May;125(1):41–50. doi: 10.1093/genetics/125.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ripoll P., Garcia-Bellido A. Cell autonomous lethals in Drosophila melanogaster. Nat New Biol. 1973 Jan 3;241(105):15–16. doi: 10.1038/newbio241015a0. [DOI] [PubMed] [Google Scholar]
  37. Salkoff L. Genetic and voltage-clamp analysis of a Drosophila potassium channel. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 1):221–231. doi: 10.1101/sqb.1983.048.01.025. [DOI] [PubMed] [Google Scholar]
  38. Salz H. K., Davis R. L., Kiger J. A. Genetic Analysis of Chromomere 3d4 in DROSOPHILA MELANOGASTER: The DUNCE and SPERM-AMOTILE Genes. Genetics. 1982 Apr;100(4):587–596. doi: 10.1093/genetics/100.4.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tsuruhara T., Koenig J. H., Ikeda K. Synchronized endocytosis studied in the oocyte of a temperature-sensitive mutant of Drosophila melanogaster. Cell Tissue Res. 1990 Feb;259(2):199–207. doi: 10.1007/BF00318441. [DOI] [PubMed] [Google Scholar]
  40. White K., DeCelles N. L., Enlow T. C. Genetic and developmental analysis of the locus vnd in Drosophila melanogaster. Genetics. 1983 Jul;104(3):433–448. doi: 10.1093/genetics/104.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wright T. R. The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv Genet. 1987;24:127–222. [PubMed] [Google Scholar]
  42. van der Bliek A. M., Meyerowitz E. M. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature. 1991 May 30;351(6325):411–414. doi: 10.1038/351411a0. [DOI] [PubMed] [Google Scholar]

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