The effect of the white mutation on learning and memory in Drosophila under heat shock
DOI:
https://doi.org/10.33910/2687-1270-2024-5-1-72-82Keywords:
Drosophila, white mutation, learning, memory, heat shock, conditioned courtship suppression, mushroom bodies, central complexAbstract
Since 1910, genetic research involving the mutant white Drosophila melanogaster has played a fundamental role in modern biology. Such experiments rapidly followed the emergence of germline transformation methods, which made it possible to create transgenic Drosophila strains, which significantly expanded the possibilities for studying many biological processes, including behavior. The white gene is characterized by pleiotropic action affecting not only vision, but also other important aspects of life, among them various forms of behavior, learning and memory. By comparing the results of our previous work, aimed at studying the learning ability and memory formation in mutant w1118 in the intact control and under heat shock in adults, with the findings of the present work, aimed at analyzing the influence of stage-specific temperature effects on these processes, we can state the retention of learning and memory processes in the mutant w1118 both in the intact control and under heat shock at various stages of ontogenesis in the conditioned courtship suppression paradigm. This should be factored into the choice of methodological approaches when planning behavioral experiments involving transgenic strains against a white genetic background.
References
Anaka, M., MacDonald, C. D., Barkova, E. et al. (2008) The white gene of Drosophila melanogaster encodes a protein with a role in courtship behavior. Journal of Neurogenetics, vol. 22, no. 4, pp. 243–276. https://doi.org/10.1080/01677060802309629 (In English)
Bang, S., Hyun, S., Hong, S. T. et al. (2011) Dopamine signalling in mushroom bodies regulates temperature-preference behaviour in Drosophila. PLoS Genetics, vol. 7, no. 3, article e1001346. https://doi.org/10.1371/journal.pgen.1001346 (In English)
Borycz, J., Borycz, J. A., Kubow, A. et al. (2008) Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain. Journal of Experimental Biology, vol. 211, no. 21, pp. 3454–3466. https://doi.org/10.1242/jeb.021162 (In English)
Buhl, E., Kottler, B., Hodge, J. J. L., Hirth, F. (2021) Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila. Scientific Reports, vol. 11, no. 1, article 155. https://doi.org/10.1038/s41598-020-80103-9 (In English)
Campbell, J. L., Nash, H. A. (2001) Volatile general anesthetics reveal a neurobiological role for the white and brown genes of Drosophila melanogaster. Journal of Neurobiology, vol. 49, no. 4, pp. 339–349. https://doi.org/10.1002/neu.10009 (In English)
Chan, R. F., Lewellyn, L., DeLoyth, J. M. et al. (2014) Contrasting influences of Drosophila white/mini-white on ethanol sensitivity in two different behaviouralbehavioral assays. Alcoholism: Clinical and Experimental Research, vol. 38, no. 6, pp. 1582–1593. https://doi.org/10.1111/acer.12421 (In English)
Diegelmann, S., Zars, M., Zars, T. (2006) Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila. Learning & Memory, vol. 13, no. 1, pp. 72–83. https://doi.org/10.1101/lm.45506 (In English)
Evans, J. M., Day, J. P., Cabrero, P. et al. (2008) A new role for a classical gene: White transports cyclic GMP. Journal of Experimental Biology, vol. 211, no. 6, pp. 890–899. https://doi.org/10.1242/jeb.014837 (In English)
Ferreiro, M. J., Pérez, C., Marchesano, M. (2018) Drosophila melanogaster white mutant w1118 undergo retinal degeneration. Frontiers in Neuroscience, vol. 11, article 732. https://doi.org/10.3389/fnins.2017.00732 (In English)
Johnston, D. St. (2013) Using mutants, knockdowns, and transgenesis to investigate gene function in Drosophila. Wiley Interdisciplinary Reviews: Developmental Biology, vol. 2, no. 5, pp. 587–613. https://doi.org/10.1002/wdev.101 (In English)
Haddadi, M., Nongthomba, U., Jahromi, S. R., Ramesh, S. R. (2016) Transgenic Drosophila model to study apolipoprotein E4-induced neurodegeneration. Behavioural Brain Research, vol. 301, pp. 10–18. https://doi.org/10.1016/j.bbr.2015.12.022 (In English)
Hanesch, U., Fischbach, K.-F., Heisenberg, M. (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell and Tissue Research, vol. 257, no. 2, pp. 343–366. https://doi.org/10.1007/BF00261838 (In English)
Heisenberg, M., Borst, A., Wagner, S., Byers, D. (1985) Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics, vol. 2, no. 1, pp. 1–30. https://doi.org/10.3109/01677068509100140 (In English)
Hersh, B. M. (2016) More than meets the eye: A primer for “Timing of locomotor recovery from anoxia modulated by the white gene in Drosophila melanogaster”. Genetics, vol. 204, no. 4, pp. 1369–1375. https://doi.org/10.1534/genetics.116.196519 (In English)
Hoyer, S. C., Eckart, A., Herrel, A. et al. (2008) Octopamine in male aggression of Drosophila. Current Biology, vol. 18, no. 3, pp. 159–167. https://doi.org/10.1016/j.cub.2007.12.052 (In English)
Kamyshev, N. G., Iliadi, K. G., Bragina, J. V. (1999) Drosophila conditioned courtship: Two ways of testing memory. Learning & Memory, vol. 6, no. 1, pp. 1–20. https://pubmed.ncbi.nlm.nih.gov/10355520 (In English)
Kostenko, V. V. (2017) Sravnitel’niyj analiz priznakov polovogo povedeniya u mutantov lokusa white imago Drosophila melanogaster [Comparative analysis of mating behavior characteristics of mutants at the white locus of Drosophila melanogaster]. Uchenye zapiski Kazanskogo universiteta. Seriya Estestvennye nauki, vol. 159, no. 2. pp. 293–305. (In Russian)
Kostenko, V. V., Vorob’eva, L. I. (2012) Vliyanie allelej lokusa white i geneticheskogo fona na lokomotornuyu aktivnost’ imago Drosophila melanogaster [The influence of white alleles and genetic background on locomotor activity of adult Drosophila melanogaster]. Vestnik Khar’kovskogo Natsional’nogo Universiteta imeni. V. N. Karazina, Seriya: Biologiya, vol. 16, no. 1035. pp. 90–96. (In Russian)
Krstic, D., Boll, W., Noll, M. (2013) Influence of the white locus on the courtship behavior of Drosophila males. PLoS One, vol. 8, no. 10, article e77904. https://doi.org/10.1371/journal.pone.0077904 (In English)
Lee, T., Lee, A., Luo, L. (1999) Development of the Drosophila mushroom bodies: Sequential generation of three distinct types of neurons from a neuroblast. Development, vol. 126, no. 18, pp. 4065–4076. https://doi.org/10.1242/dev.126.18.4065 (In English)
Masek, P., Keene, A. C. (2016) Gustatory processing and taste memory in Drosophila. Journal of Neurogenetics, vol. 30, no. 2, pp. 112–121. https://doi.org/10.1080/01677063.2016.1185104 (In English)
Morgan, T. H. (1910) Sex-limited inheritance in Drosophila. Science, vol. 32, no. 812, pp. 120–122. https://doi.org/10.1126/science.32.812.120 (In English)
Myers, J. L., Porter, M., Narwold, N. et al. (2021) Mutants of the white ABCG transporter in Drosophila melanogaster have deficient olfactory learning and cholesterol homeostasis. International Journal of Molecular Sciences, vol. 22, article 12967. https://doi.org/10.3390/ijms222312967 (In English)
Nikitina, E. A. (2023) Obuchenie i pamyat’ u drozofily: Rol’ mutatsii white [Learning and memory in Drosophila: role of white mutation]. Integrativnaya fiziologiya — Integrative Physiology, vol. 4, no. 1, pp. 91–102. https://doi.org/10.33910/2687-1270-2023-4-1-91-102 (In Russian)
Nikitina, E. A., Kaminskaya, A. N., Molotkov, D. A. et al. (2014) Effect of heat shock on courtship behavior, sound production, and learning in comparison with the brain content of LIMK1 in Drosophila melanogaster males with altered structure of the limk1 gene. Journal of Evolutionary Biochemistry and Physiology, vol. 50, no. 2, pp. 154–166. https://doi.org/10.1134/S0022093014020082 (In English)
Nikitina, E. A., Komarova, A. V., Golubkova, E. V. et al. (2003a) SemidDominant effects of the l(1)ts403 (sbr10) mutation at the disjunction ofon sex chromosome nondsjunctions in meiosis inof Drosophila melanogaster females exposed to heatafter heat shock. Russian Journal of Genetics, vol. 39, no. 3, pp. 269–2756. https://doi.org/10.1023/A:1023208725228 (In English)
Nikitina, E. A., Medvedeva, A. V., Dolgaya, Yu. F. et al. (2012) Involvement of GDNF and LIMK1 and heat shock proteins in Drosophila learning and memory formation. Journal of Evolutionary Biochemistry and Physiology, vol. 48, no. 5–6, pp. 529–539. https://doi.org/10.1134/S0022093012050076 (In English)
Nikitina, E. A., Tokmatcheva, E. V., Savvateeva-Popova, E. V. (2003b) 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, vol. 39, no. 1, pp. 25–31. https://doi.org/10.1023/A:1022062609102 (In English)
Nikitina, E. A., Zhuravlev, A. V., Savvateeva-Popova, E. V. (2021) Vliyanie narusheniya sinteza kinureninov na pamyat’ u drozofily [Effect of impaired kynurenine synthesis on memory in Drosophila]. Integrativnaya fiziologiya — Integrative Physiology, vol. 2, no. 1, pp. 49–60. https://doi.org/10.33910/2687-1270-2021-2-1-49-60 (In Russian)
Rubin, G. M., Spradling, A. C. (1982) Genetic transformation of Drosophila with transposable element vectors. Science, vol. 218 no. 4570, pp. 348–353. https://doi.org/10.1126/science.6289436 (In English)
Sakai, T., Kitamoto, T. (2006) Differential roles of two major brain structures, mushroom bodies and central complex, for Drosophila male courtship behavior. Journal of Neurobiology, vol. 66, no. 8, pp. 821–834. https://doi.org/10.1002/neu.20262 (In English)
Savvateeva-Popova, E. V., Popov, A. V., Grossman, A. I. et al. (2007) Pathogenic chaperone-like RNA induces congophilic aggregates and facilitates neurodegeneration in Drosophila. Cell Stress & Chaperones, vol. 12, no. 1, pp. 9–19. https://doi.org/10.1379/csc-222r.1 (In English)
Savvateeva-Popova, E. V., Popov, A. V., Grossman, A. et al. (2008) Non-coding RNA as a trigger of neuropathologic disorder phenotypes in transgenic Drosophila. Journal of Neuronal Transmission, vol. 115, no. 12, pp. 1629–1642. https://doi.org/10.1007/s00702-008-0078-8 (In English)
Sitaraman, D., Zars, M., LaFerriere, H. et al. (2008) Serotonin is necessary for place memory in Drosophila. Proceedings of the National Academy of Sciences USA, vol. 105, no. 14, pp. 5579–5584. https://doi.org/10.1073/pnas.0710168105 (In English)
Snijder, P. M., Baratashvili, M., Grzeschik, N. A. et al. (2015) Overexpression of cystathionine γ-lyase suppresses detrimental effects of spinocerebellar ataxia type 3. Molecular Medicine, vol. 21, no. 1, pp. 758–768. https://doi.org/10.2119/molmed.2015.00221 (In English)
Sokal, R. R., Rohlf, F. J. (1995) Biometry: The principles and practice of statistics in biological research. 3rd ed. New York: W. H. Freeman Publ., 887 р. (In English)
Solanki, N., Wolf, R., Heisenberg, M. (2015) Central complex and mushroom bodies mediate novelty choice behavior in Drosophila. Journal of Neurogenetics, vol. 29, no. 1, pp. 30–37. https://doi.org/10.3109/01677063.2014.1002661 (In English)
Strauss, R., Heisenberg, M. (1993) A higher control center of locomotor behavior in the Drosophila brain. Journal of Neuroscience, vol. 13, no. 5, pp. 1852–1861. https://doi.org/10.1523/JNEUROSCI.13-05-01852.1993 (In English)
Sturtevant, A. H. (1915) Experiments on sex recognition and the problem of sexual selection in Drosophila. Journal of Animal Behavior, vol. 5, pp. 351–366. https://doi.org/10.1037/h0074109 (In English)
Sun, Y., Qiu, R., Li, X. et al. (2020) Social attraction in Drosophila is regulated by the mushroom body and serotonergic system. Nature Communications, vol. 11, no. 1, article 5350. https://doi.org/10.1038/s41467-020-19102-3 (In English)
Titlow, J. S., Rice, J., Majeed, Z. R. et al. (2014). Anatomical and genotype-specific mechanosensory responses in Drosophila melanogaster larvae. Neuroscience Research, vol. 83, pp. 54–63. https://doi.org/10.1016/j.neures.2014.04.003 (In English)
Tsao, C.-H., Chen, C.-C., Lin, C.-H. et al. (2018) Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior. eLife, vol. 7, article e35264. https://doi.org/10.7554/eLife.35264 (In English)
Van Swinderen, B., Andretic, R. (2011) Dopamine in Drosophila: Setting arousal thresholds in a miniature brain. Proceedings of the Royal Society B. Biological Sciences, vol. 278, no. 1707, pp. 906–913. https://doi.org/10.1098/rspb.2010.2564 (In English)
Wang, J., Wu, C., Zhang, X. et al. (2023) Developmental neurotoxic effects of bisphenol A and its derivatives in Drosophila melanogaster. Ecotoxicology and Environmental Safety, vol. 260, article 115098. https://doi.org/10.1016/j.ecoenv.2023.115098 (In English)
Warren, T. L., Giraldo, Y. M., Dickinson, M. H. (2019) Celestial navigation in Drosophila. Journal of Experimental Biology, vol. 222, no. 1, article jeb186148. https://doi.org/10.1242/jeb.186148 (In English)
Weiss, J. T., Donlea, J. M. (2021) Sleep deprivation results in diverse patterns of synaptic scaling across the Drosophila mushroom bodies. Current Biology, vol. 31, no. 15, pp. 3248–3261. https://doi.org/10.1016/j.cub.2021.05.018 (In English)
West, R. J., Elliott, C. J., Wade, A. R. (2015). Classification of Parkinson’s disease genotypes in Drosophila using spatiotemporal profiling of vision. Scientific Reports, vol. 5, article 16933. https://doi.org/10.1038/srep16933 (In English)
Wolf, R., Wittig, T., Liu L. et al. (1998) Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. Learning & Memory, vol. 5, no. 1–2, pp. 166–178. https://pubmed.ncbi.nlm.nih.gov/10454381 (In English)
Xiao, C., Qiu, S. (2020) Frequency-specific modification of locomotor components by the white gene in Drosophila melanogaster adult flies. Genes, Brain and Behavior, vol. 20, no. 2, article e12703. https://doi.org/10.1111/gbb.12703 (In English)
Xiao, C., Qiu, S., Robertson, R. M. (2017) The white gene controls copulation success in Drosophila melanogaster. Scientific Reports, vol. 7, article 7712. https://doi.org/10.1038/s41598-017-08155-y (In English)
Xiao, C., Robertson, R. M. (2016) Timing of locomotor recovery from anoxia modulated by the white gene in Drosophila. Genetics, vol. 203, no. 2, pp. 787–797. https://doi.org/10.1534/genetics.115.185066 (In English)
Xiao, C., Robertson, R. M. (2017) White — cGMP interaction promotes fast locomotor recovery from anoxia in adult Drosophila. PLoS One, vol. 12, no. 1, article e0168361. https://doi.org/10.1371/journal.pone.0168361 (In English)
Zalucki, O., Day, R., Kottler, B. et al. (2015) Behavioral and electrophysiological analysis of general anesthesia in 3 background strains of Drosophila melanogaster. Fly, vol. 9, no. 1, pp. 7–15. https://doi.org/10.1080/19336934.2015.1072663 (In English)
Zatsepina, O. G., Chuvakova, L. N., Nikitina E. A. et al. (2022) Genes responsible for H2S production and metabolism are involved in learning and memory in Drosophila melanogaster. Biomolecules, vol. 12, no. 6, article 751. https://doi.org/10.3390/biom12060751 (In English)
Zatsepina, O. G., Nikitina, E. A., Shilova, V. Y. et al. (2021) Hsp70 affects memory formation and behaviorally relevant gene expression in Drosophila melanogaster. Cell Stress and Chaperones, vol. 26, no. 3, pp. 575–594. https://doi.org/10.1007/s12192-021-01203-7 (In English)
Zhuravlev, A. V., Nikitina, E. A., Savvateeva-Popova, E. V. (2015) Obuchenie i pamyat’ u drozofily: Ffiziologo-geneticheskie osnovy [Learning and memory in Drosophila: Physiologic and genetic bases]. Uspekhi fiziologicheskikh nauk, vol. 46, no. 1, pp. 76–92. (In Russian)
Zhuravlev, A. V., Shchegolev, B. F., Zakharov, G. A. et al. (2022) 3-hydroxykynurenine as a potential ligand for hsp70 proteins and its effects on Drosophila memory after heat shock. Molecular Neurobiology, vol. 59, pp. 1862–1871. https://doi.org/10.1007/s12035-021-02704-3 (In English)
Zimmerman, J. E., Chan, M. T., Jackson, N. et al. (2012) Genetic background has a major impact on differences in sleep resulting from environmental influences in Drosophila. SLEEP, vol. 35, no. 4, pp. 545–557. http://dx.doi.org/10.5665/sleep.1744 (In English)
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Ekaterina A. Nikitina
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The work is provided under the terms of the Public Offer and of Creative Commons public license Attribution-NonCommercial 4.0 International (CC BY-NC 4.0). This license allows an unlimited number of persons to reproduce and share the Licensed Material in all media and formats. Any use of the Licensed Material shall contain an identification of its Creator(s) and must be for non-commercial purposes only.
