Abstract
The structures and functions of many genes are homologous in Drosophilaand humans. Therefore, studying pathological processes in Drosophila, in particular neurogenerative processes accompanied by progressive memory loss, helps to understand the ethiology of corresponding human disorders and to develop therapeutic strategies. It is believed that the development of neurogenerative diseases might result from alterations in the functioning of the heat shock/chaperone machinery. In view of this, we used Drosophila mutant l(1)ts403 with defective synthesis of heat shock proteins for studying learning and memory in a test of conditioned courtship suppression following a heat shock given at different developmental stages. High learning indices were registered immediately and 30 min after training both in the intact controls and in flies subjected to different developmental heat shocks. This indicated normal learning and memory acquisition in the mutant. At the same time, memory retention (3 h after training) suffered to different extent depending on the developmental stage. The remote effects of heat shock given during the formation of the mushroom bodies indicated the important role of this brain structure in the memory formation. The observed memory defects may result from alterations both in mRNA transport and in the functions of molecular chaperones in the l(1)ts403 mutant.
Similar content being viewed by others
References
Smith, D., Whitesell, L., and Katsanis, E., Molecular Chaperones: Biology and Prospects for Pharmacological Intervention, Pharm. Rev., 1998, vol. 50, pp. 493-514.
Ranson, N.A., White, H.E., and Saibil, H.R., Chaperonins, Biochem. J., 1998, vol. 333, pp. 233-242.
Welch, W.J., The Role of Heat-Shock Proteins as Molecular Chaperones, Curr. Opin. Cell Biol., 1991, vol. 3, pp. 1033-1038.
Arking, R., Temperature-Sensitive Cell-Lethal Mutants of Drosophila: Isolation and Characterization, Genetics, 1975, vol. 80, pp. 519-537.
Zhimulev, I.F., Belayeva, E.S., Pokholkova, G.V., et al., Report of New Mutants, Dros. Inf. Serv., 1981, vol. 56, pp. 192-196.
Evgen'ev, M.B., Levin, A.V., and Losovskaya, E.R., The Analysis of Temperature-Sensitive (ts) Mutation Influencing the Expression of Heat Shock-Inducible Genes in D. melanogaster, Mol. Gen. Genet., 1979, vol. 176, pp. 275-280.
Mamon, L.A., Bondarenko, L.V., Tret'yakova, I.V., et al., Consequences of Cell Stress in Drosophila with Altered Synthesis of Heat-Shock Proteins, Vestn. St. Petersburg. Gos. Univ., 1999, no. 4, pp. 100-114.
Evgen'ev, M.B. and Levin, A.V., The Effect of a ts Mutation on the Expression of Heat Shock-Inducible Genes in Drosophila melanogaster: 1. Analysis of Protein Synthesis, Genetika (Moscow), 1980, vol. 16, no. 6, pp. 1026-1029.
Mamon, L.A. and Kutskova, Yu.A., The Role of Heat-Shock Proteins in Restoration of Cell Proliferation after Exposure of D. melanogaster Larvae to a High Temperature, Genetika (Moscow), 1993, vol. 29, no. 5, pp. 791-798.
Mamon, L.A. and Kutskova, Yu.A., The Role of Heat-Shock Proteins in Repair of Mitotic Chromosome Damage Induced by a High Temperature in D. melanogaster, Genetika (Moscow), 1993, vol. 29, no. 4, pp. 606-612.
Mamon, L.A., Mazur, E.L., Churkina, I.V., and Barabanova, L.V., The Effect of High Temperatures on the Nondisjunction Frequency and Loss of the Sex Chromosomes in Females of Drosophila melanogaster Strain l(1)ts403 Defective in the System of Heat-Shock Proteins, Genetika (Moscow), 1990, vol. 26, no. 3, pp. 554-556.
Mamon, L.A., Komarova, A.V., Bondarenko, L.V., et al., Development of Thermotolerance in Drosophila melanogaster Strain l(1)ts403 with Distorted Synthesis of Heat-Shock Proteins, Genetika (Moscow), 1998, vol. 34, no. 7, pp. 920-928.
Mamon, L.A., Nikitina, E.A., Pugacheva, O.M., and Golubkova, E.V., The Effects of the Maternal and Paternal Organisms on Thermosensitivity Determined by the l(1)ts403 Mutation in Drosophila melanogaster Early Embryos, Genetika (Moscow), 1999, vol. 35, no. 8, pp. 1078-1085.
Mamon, L.A., Nikitina, E.A., Pugatchova, O.M., and Golubkova, E.V., The Influence of the l(1)ts403 Allele on the Heat Induction of the Different Malformations in Drosophila melanogaster, 40th Ann. Drosophila Res. Conf., Washington, 1999, p. 731A.
Heisenberg, M., Borst, A., Wagner, S., and Byers, D., Drosophila mushroom body Mutants Are Deficient in Olfactory Learning, J. Neurogenet., 1985, vol. 2, no. 1, pp. 1-30.
Heisenberg, M., Central Brain Function in Insects: Genetic Studies on the Mushroom Bodies and Central Complex in Drosophila, Fortschritte der Zoologie, Band., vol. 39: Neural Basis of Behavioral Adaptations, Stuttgart: Gustav Fischer Verlag, 1994.
de Bell, J.S. and Heisenberg, M., Associative Odor Learning in Drosophila Abolished by Chemical Ablation of Mushroom Bodies, Science, 1994, vol. 263, no. 5143, pp. 692-695.
Boquet, I., Hitier, R., Dumas, M., et al., Central Brain Postembryonic Development in Drosophila: Implication of Genes Expressed at the Interhemispheric Junction, J. Neurobiol., 2000, vol. 42, no 1, pp. 33-48.
Kamyshev, N.G., Iliadi, K.G., and Bragina, J.V., Drosophila Conditioned Courtship: Two Ways of Testing Memory, Learn. Memory, 1999, vol. 6, no. 1, pp. 1-20.
Kamyshev, N.G., Iliadi, K.G., Bragina, Yu.V., et al., Detection of Drosophila Mutants Displaying Memory Defects after Conditioned Courtship Suppression, Fiziol. Zh. im. I.M. Sechenova, 1999, vol. 85, no. 1, pp. 84-92.
Savvateeva, E.V., Popov, A.V., Kamyshev, N.G., et al., Age-Dependent Memory Loss, Synaptic Pathology and Altered Brain Plasticity in the Drosophila Mutant cardinal Accumulating 3-Hydroxykynurenine, J. Neural Transmission, 2000, vol. 107, pp. 581-601.
Sokal, R.R. and Rohlf, F.J., Biometry, Berlin: Freeman, 1995, 3rd ed.
Zhimulev, I.F., Belyaeva, E.S., Pokholkova, G.V., et al., Report of New Mutants, Dros. Inf. Serv., 1982, vol. 58, pp. 210-212.
Wilkie, G.S., Drosophila melanogaster mRNA for Tip Associating Protein (sbr Gene), GenBank/EMBL/DDBJ, 1999, 12.21: AJ251947 (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Search&db=Nucleotide&doptcmdl=GenBank&tool-FlyBase&term-AJ251947[ACCN]).
Tret'yakova, I.V., Molecular Genetic Analysis of a Drosophila melanogaster DNA Region Containing the Vital l(1)ts403 Gene, Cand. Sci. (Biol.) Dissertation, St. Petersburg: St. Petersburg Univ., 2000.
Segref, A., Sharma, K., Doye, V., et al., Mex67p, a Novel Factor for Nuclear mRNA Export, Binds to Both Poly(A)+ RNA and Nuclear Pores, EMBO J., 1997, vol. 16, no. 11, pp. 3256-3271.
Yoon, D.W., Lee, H., Seol, W., et al., Tap: A Novel Cellular Protein That Interacts with Tip of Herpesvirus Saimiri and Induces Lymphocyte Aggregation, Immunity, 1997, vol. 6, no. 5, pp. 571-582.
Braun, I.C., Rohrbach, E., Schmitt, C., and Izaurralde, E., TAP Binds to the Constitutive Transport Element (CTE) through a Novel RNA-Binding Motif That Is Sufficient to Promote CTE-Dependent RNA Export from the Nucleus, EMBO J., 1999, vol. 18, no. 7, pp. 1953-1965.
Tannoch, V.J., Cormier-Regard, S., and Claycomb, W.C., GenBank/EMBL/DDBJ AF093140, (http://www.ncbi.nlm. nih.gov/entrez/query.fcgi?cmd=Search&db=Nucleotide& doptcmdl=GenBank&tool=FlyBase&term=AF093140 [ACCN]).
The C. elegans Sequencing Consortium, Genome Sequence of the Nematode C. elegans: A Platform for Investigating Biology, Science, 1998, vol. 282, no. 5396, pp. 2012-2018.
Nigg, E.A., Nucleocytoplasmic Transport: Signals, Mechanisms and Regulation, Nature, 1997, vol. 386, no. 6627, pp. 779-787.
Lankat-Buttgereit, V. and Tampe, R., The Transporter Associated with Antigen Processing TAP: Structure and Function FEBS Lett., 1999, vol. 31, no. 464, pp. 108-112.
Parsell, D. and Lindquist, S., The Function of Heat-Shock Proteins in Stress Tolerance: Degradation and Reactivation of Damaged Proteins, Annu. Rev. Genet., 1993, vol. 27, pp. 437-496.
Feder, M., Parsell, D., and Lindquist, S., Stress Response and Stress Proteins, Cell Biology of Trauma, Boca Raton: CRC, 1995, pp. 177-191.
Davis, R.L., Physiology and Biochemistry of Drosophila Learning Mutants, Physiol. Rev., 1996, vol. 72, no. 2, pp. 299-317.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Nikitina, E.A., Tokmatcheva, E.V. & Savateeva-Popova, E.V. Heat Shock during the Development of Central Structures of the Drosophila Brain: Memory Formation in the l(1)ts403 Mutant of Drosophila melanogaster. Russian Journal of Genetics 39, 25–31 (2003). https://doi.org/10.1023/A:1022062609102
Issue Date:
DOI: https://doi.org/10.1023/A:1022062609102