Learning and forgetting in Drosophila melanogaster in limk1 gene polymorphism

Authors

  • Ekaterina S. Zalomaeva Pavlov Institute of Physiology, Russian Academy of Sciences; Herzen State Pedagogical University of Russia https://orcid.org/0000-0002-6005-3433
  • Varvara S. Falina Herzen State Pedagogical University of Russia
  • Anna V. Medvedeva Pavlov Institute of Physiology, Russian Academy of Sciences https://orcid.org/0000-0001-7989-8746
  • Ekaterina A. Nikitina Pavlov Institute of Physiology, Russian Academy of Sciences; Herzen State Pedagogical University of Russia https://orcid.org/0000-0003-1897-8392
  • Elena V. Savvateeva-Popova Pavlov Institute of Physiology, Russian Academy of Sciences

DOI:

https://doi.org/10.33910/2687-1270-2021-2-3-318-327

Keywords:

limk1, memory, learning, actin remodeling, cytoskeleton, Drosophila

Abstract

Currently, neurodegenerative diseases (NDD) are very widespread. According to the World Health Organization (WHO), dementia affected 47 million people worldwide in 2015, and is projected to reach 75 million by 2030 and 132 million by 2050. Neurophysiologists around the world seek to know the etiology and pathogenesis of NDD. It is known that one of the causes of neurocognitive pathologies is impaired expression of the limk1 gene. In addition, according to modern ideas, the basis of intellectual problems in neurological brain injuries is active forgetting, regulated by the signaling cascade of actin remodeling, the key enzyme of which is LIMK1. The work analyzed the formation and dynamics of short and medium-term memory change in Drosophila melanogaster stocks polymorphic for the limk1 gene (Canton-S, Oregon-R and agnts3). Polymorphism on the limk1 gene of Drosophila affects the content of its product (mutant agnts3 is characterized by a 2.5-fold increase in LIMK1 content compared to CS) and leads to violations of courtship and training behavior. The results of the present study of two wild-type stocks and agnts3 mutant with altered limk1 gene structure indicate that disruptions in the structure of this gene can cause disturbance of learning and forgetting processes.

References

Asok, A., Leroy, F., Rayman, J. B., Kandel, E. R. (2019) Molecular mechanisms of the memory trace. Trends in Neurosciences, vol. 42, no. 1, pp. 14–22. https://www.doi.org/10.1016/j.tins.2018.10.005 (In English)

Brown, R. E. (2020) Donald O. Hebb and the organization of behavior: 17 years in the writing. Molecular Brain, vol. 13, no. 1, article 55. https://www.doi.org/10.1186/s13041-020-00567-8 (In English)

Cervantes-Sandoval, I., Chakraborty, M., MacMullen, C., Davic, R. L. (2016) Scribble scaffolds a signalosome for active forgetting. Neuron, vol. 90, no. 6, pp. 1230–1242. https://www.doi.org/10.1016/j.neuron.2016.05.010 (In English)

Davis, R. L., Zhong, Y. (2017) The biology of forgetting — a perspective. Neuron, vol. 95, no. 3, pp. 490–503. https://www.doi.org/10.1016/j.neuron.2017.05.039 (In English)

Gao, T.-T., Wang, Y., Liu, L. et al. (2020) LIMK1/2 in the mPFC plays a role in chronic stress-induced depressive-like effects in mice. The International Journal of Neuropsychopharmacology, vol. 23, no. 12, pp. 821–836. https://www.doi.org/10.1093/ijnp/pyaa067 (In English)

Griffith, L. C., Ejima, A. (2009) Courtship learning in Drosophila melanogaster: Diverse plasticity of a reproductive behavior. Learning & Memory, vol. 16, no. 12, pp. 743–750. https://www.doi.org/10.1101/lm.956309 (In English)

Gu, J., Lee, C. W., Fan, Y. et al. (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nature Neuroscience, vol. 13, no. 10, pp. 1208–1215. https://www.doi.org/10.1038/nn.2634 (In English)

Honjo, K., Furukubo-Tokunaga, K. (2005) Induction of cAMP response element-binding protein-dependent medium-term memory by appetitive gustatory reinforcement in Drosophila larvae. The Journal of Neuroscience, vol. 25, no. 35, pp. 7905–7913. https://www.doi.org/10.1523/JNEUROSCI.2135-05.2005 (In English)

Huang, J., Sun, W., Ren, J. et al. (2020) Genome-Wide Identification and characterization of actin-depolymerizing factor (ADF) family genes and expression analysis of responses to various stresses in Zea Mays L. International Journal of Molecular Sciences, vol. 21, no. 5, article 1751. https://www.doi.org/10.3390/ijms21051751 (In English)

Jonides, J., Lewis, R. L., Nee, D. E. et al. (2008) The mind and brain of short-term memory. Annual Review of Psychology, vol. 59, pp. 193–224. https://www.doi.org/10.1146/annurev.psych.59.103006.093615 (In English)

Kaminskaya, A. N., Nikitina, E. A., Payalina, T. L. et al. (2012) Effect of the LIM kinase 1 isoform ratio on Drosophila melanogaster courtship behavior: A complex approach. Russian Journal of Genetics: Applied Research, vol. 2, no. 5, pp. 367–377. https://www.doi.org/10.1134/S2079059712050024 (In English)

Kaminskaya, A. N., Nikitina, E. A., Medvedeva, А. V. et al. (2015) The influence of gene limk1 polymorphism on learning and memory and distribution pCREB and aggregates formation in neuromuscular junctions of Drosophila melanogaster. Russian Journal of Genetics, vol. 51, no. 6, pp. 582–590. https://www.doi.org/10.1134/S1022795415060071 (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. PMID: 10355520. (In English)

Masse, N. Y., Rosen, M. C., Freedman, D. J. (2020) Reevaluating the role of persistent neural activity in short-term memory. Trends in Cognitive Sciences, vol. 24, no. 3, pp. 242–258. https://www.doi.org/10.1016/j.tics.2019.12.014 (In English)

Medina, J. H. (2018) Neural, cellular and molecular mechanisms of active forgetting. Frontiers in Systems Neuroscience, vol. 12, article 3. https://www.doi.org/10.3389/fnsys.2018.00003 (In English)

Medvedeva, A. V., Molotkov, D. A., Nikitina, E. A. et al. (2008) Systemic regulation of genetic and cytogenetic processes by a signal cascade of actin remodeling: Locus agnostic in Drosophila. Russian Journal of Genetics, vol. 44, no. 6, pp. 669–681. https://www.doi.org/10.1134/S1022795408060069 (In English)

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://www.doi.org/10.1134/S0022093014020082 (In English)

Nikitina, E. A., Medvedeva, A. V., Gerasimenko, M. S. et al. (2017) Oslablennoe magnitnoe pole Zemli: vliyanie na transkriptsionnuyu aktivnost’ genoma, obuchenie i pamyat’ u Dr. melanogaster [Weakened geomagnetic field: Effects on genomic transcriptional activity, learning, and memory in Drosophila melanogaster]. Zhurnal vysshej nervnoj deyatelnosti im. I. P. Pavlova — I.P. Pavlov Journal of Higher Nervous Activity, vol. 67, no. 2, pp. 246–256. https://www.doi.org/10.7868/S0044467717020101 (In Russian)

Reiter, L. T., Potocki, L., Chien, S. et al. (2001) A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Research, vol. 11, no. 6, pp. 1114–1125. https://www.doi.org/10.1101/gr.169101 (In English)

Savvateeva-Popova, E. V., Zhuravlev, A. V., Brázda, V. et al. (2017) Drosophila model for the analysis of genesis of LIM-kinase 1-Dependent Williams-Beuren syndrome cognitive phenotypes: INDELs, transposable elements of the Tc1/Mariner superfamily and microRNAs. Frontiers in Genetics, vol. 8, article 123. https://www.doi.org/10.3389/fgene.2017.00123 (In English)

Siegel, R. W., Hall, J. C. (1979) Conditioned responses in courtship behavior of normal and mutant Drosophila. Proceedings of the National Academy of Sciences of the USA, vol. 76, no. 7, pp. 3430–3434. https://www.doi.org/10.1073/pnas.76.7.3430 (In English)

Smirnov, V. M. (2000) Nejrofiziologiya i vysshaya nervnaya deyatel’nost’ detej i podrostkov [Neurophysiology and higher nervous activity of children and adolescents]. Moscow: Academia Publ., 400 p. (In Russian)

Tully, T. (1996) Discovery of genes involved with learning and memory: An experimental synthesis of Hirschian and Benzerian perspectives. Proceedings of the National Academy of Sciences of the USA, vol. 93, no. 24, pp. 13460–13467. https://doi.org/10.1073/pnas.93.24.13460 (In English)

Zamboni, F., Vieira, S., Reis, R. L. et al. (2018) The potential of hyaluronic acid in immunoprotection and immunomodulation: Chemistry, processing and function. Progress in Materials Science, vol. 97, pp. 97–122. https://www.doi.org/10.1016/j.pmatsci.2018.04.003 (In English)

Zefirov, T. L., Ziyatdinova, N. I., Kyptsova, A. M. (2015) Fiziologicheskie osnovy pamyati. Razvitie pamyati u detej i podrostkov [Physiological bases of memory. Memory development in children and adolescents]. Kazan: Kazan Federal University, 40 p. (In Russian)

Zhuravlev, A. V., Nikitina, E. A., Savvateeva-Popova, E. V. (2015) Obuchenie i pamyat’ u drozofily: fiziologo-geneticheskie osnovy [Education and memory in drosophila: Physiological and genetic bases]. Uspekhi fiziologicheskikh nauk, vol. 46, no. 1, pp. 76–92. (In Russian)

Zhuravlev, A. V., Nikitina, E. A., Savvateeva-Popova, E. V. (2020) Rol’ kinureninov v regulyatsii povedeniya i protsessov pamyati u drozofily [Role of kynurenines in regulation of behavior and memory processes in Drosophila]. Integrativnaya fiziologiya — Integrative Physiology, vol. 1, no. 1, pp. 40–50. https://www.doi.org/10.33910/2687-1270-2020-1-1-40-50 (In Russian)

Published

2021-12-03

Issue

Section

Experimental articles