Stress influences and cognitive activity: search for targets and general mechanisms using Drosophila mutants

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

According to modern concepts, biochemical cascades activated in response to stress impacts also contribute to cognitive functions, such as learning and memory formation. Considering a conditioned reflex as an adaptation to the external environment, one can assume its occurrence as a reaction to external challenges, which, when reinforced, contribute to the formation of a conditioned connection, and in the absence, cause the development of a stress response. The metabolic activity of the body is inextricably linked with circadian rhythms, which determine the daily fluctuations in light, temperature, oxygen content and magnetic field. The integration of these timers is carried out by a protein of the cryptochrome family (CRY), which functions as a blue light receptor and is known as a repressor of the main circadian transcription complex CLOCK/BMAL1. In order to develop methods for non-invasive correction of pathologies of the nervous system on a model object of genetics – Drosophila using mutant lines, the relationship between adaptive mechanisms for the formation of a conditioned connection and the development of a stress response to a weakening of the magnetic field, hypoxic and temperature effects is studied. The data are discussed in light of the role of the CRY/CLOCK/BMAL1 system as a link in magnetoreception, hypoxia, circadian rhythm regulation, cognitive functions, and DNA double-strand breaks in nerve ganglia (an indicator of the physiological activity of neurons).

Full Text

Restricted Access

About the authors

D. M. Karovetskaya

Russian State Pedagogical University named after A. I. Herzen; Pavlov Institute of Physiology of Russian Academy of Sciences

Email: 21074@mail.ru
Russian Federation, St. Petersburg; St. Petersburg

A. V. Medvedeva

Pavlov Institute of Physiology of Russian Academy of Sciences

Email: 21074@mail.ru
Russian Federation, St. Petersburg

E. V. Tokmacheva

Pavlov Institute of Physiology of Russian Academy of Sciences

Email: 21074@mail.ru
Russian Federation, St. Petersburg

S. A. Vasilyeva

Russian State Pedagogical University named after A. I. Herzen; Pavlov Institute of Physiology of Russian Academy of Sciences

Email: 21074@mail.ru
Russian Federation, St. Petersburg; St. Petersburg

A. V. Rebrova

Russian State Pedagogical University named after A. I. Herzen

Email: 21074@mail.ru
Russian Federation, St. Petersburg

E. A. Nikitina

Russian State Pedagogical University named after A. I. Herzen; Pavlov Institute of Physiology of Russian Academy of Sciences

Author for correspondence.
Email: 21074@mail.ru
Russian Federation, St. Petersburg; St. Petersburg

B. F. Shchegolev

Pavlov Institute of Physiology of Russian Academy of Sciences

Email: 21074@mail.ru
Russian Federation, St. Petersburg

E. V. Savvateeva-Popova

Pavlov Institute of Physiology of Russian Academy of Sciences

Email: 21074@mail.ru
Russian Federation, St. Petersburg

References

  1. Лобашев М.Е., Савватеев В.Б. Физиология суточного ритма животных. М., Л.: Изд-во АН СССР, 1959. 259 с.
  2. Zatsepina O.G., Nikitina E.A., Shilova V.Y., Chuvakova L.N., Sorokina S., Vorontsova Yu.E., Tokmacheva E.V., Funikov S. Yu., Rezvykh A.P., Evgeniev M.B.// Cell Stress and Chaperones. 2021. V. 26. № 3. P. 575–594.
  3. Damulewicz M., Mazzotta G.M. // Front Physiol. 2020. V. 11. Art. 99.
  4. Agrawal P., Houl J.H., Gunawardhana K.L., Liu T., Zhou J., Zoran M.J., Hardin P.E. // Сurr Biol. 2017. V. 16. P. 2431–2441.
  5. Karki N., Vergish S., Zoltovski B.D. // Protein Science. 2021. V. 30. № 8. P. 1521–1534.
  6. Cusumano P., Damulewicz M., Carbognin E., Caccin L., Puricella V., Specchia M., Bozzetti P., Costa R., Mazzotta G.M. // Front Physiol. 2019. V. 10. Art. 133.
  7. Helfrich-Förster C. // Genes Brain Behav. 2005. V. 4. P. 65–76.
  8. Hermann-Luibl C., Helfrich-Förster C. // Curr. Opin. Insect Sci. 2015. V. 7. P. 65–70.
  9. Yoshii T., Ahmad M., Helfrich-Förster C. // PLoS Biol. 2009. V. 7. Art. 1000086.
  10. Shang Y., Haynes P., Pírez N., Harrington K.I., Guo F., Pollack J., Hong P., Griffith L.C., Rosbash M. // Nat Neurosci. 2011. V. 14. № 7. P. 889–895.
  11. Yamamoto Sh., Seto E.S. // Exp Anim. 2014. V. 63. № 2. P. 107–119.
  12. Tabuch M., Coates K.E., Bautista O.B., Zukowski L.H. // Front Neurol. 2021. V. 12. Art. 625369.
  13. Sitaraman D., Aso Y., Jin X. // Сurr Biol. 2015. V. 25. № 22. P. 2915–2927.
  14. Flyer-Adams J., Rivera-Rodriguez E.J., Yu J. Junwei Yu, Jacob D. Mardovin, Martha L. Reed, Leslie C. Griffith // J Neurosci. 2020. V. 40. P. 9066–9077.
  15. Fogle K., Parson K.G., Dahm N.A., Holmes T.C. // Science. 2011. V. 331. P. 1409–1413.
  16. Sitaraman D., Aso Y., Jin X. Rubin G.M.,Nitabach M.N. // Сurr Biol. 2015. V. 25. P. 2915–2927.
  17. Pokorny R., Klar T., Hennecke U., Carell T. // Proc Natl Acad Sci. 2008. V. 105. № 52. P. 21023–21027.
  18. Romero-Franco A., Checa-Rodríguez C., Maikel Castellano-Pozo M., Miras H., Wals A., Huertas P. // 22.01.2023 on bioRxiv preprint.
  19. Boutros S.W., Krenik D., Holden S., Vivek K. Unni, Raber J. // Oncotarget. 2022. V. 13. Р. 198–213.
  20. Никитина Е.А., Васильева С.А., Щеголев Б.Ф., Савватеева-Попова Е.В. // Журнал высшей нервной деятельности им. И.П. Павлова. 2022. Т. 72. № 6. С. 783–799.
  21. Eichwald C., Walleczek J. // Biophysical Journal. 1996. V. 71. № 2. P. 623–631.
  22. Izmaylov A.F., Tully J.C., Frisch M.J. // Journal of Physical Chemistry A. 2009. V. 113. № 44. P. 12276–12284.
  23. Rodgers C.T., Hore P.J. // Proceedings of the National Academy of Sciences of USA. 2009. V. 106. № 2. P. 353–360.
  24. Kaushik R., Nawathean P., Busza A., Murad A., Emery P., Rosbash M. // PLoS Biology. 2007. V. 5. № 6. P. 1257–1266.
  25. Solov’yov I.A., Schulten K. // Biophys. J. 2009. V. 96. № 12. P. 4804–4813.
  26. Nikitina E.A., Medvedeva A.V., Gerasimenko M.S., Pronikov V.S., Surma S.V., Shchegolev B.F., Savvateeva-Popova E.V. // Neuroscience and Behavioral Physiology. 2018. V. 48. № 7. P. 796–803.
  27. Nikitina E.A., Medvedeva A.V., Zakharov G.A., Savvateeva-Popova E.V. // Acta Naturae. 2014. V. 6. № 2. P. 53–61.
  28. Borovac J., Bosch M., Okamoto K. // Mol Cell Neurosci. 2018. V. 91. P. 122–130.
  29. Misu S., Takebayashi M., Kei M. // Frontiers in Genetics. 2017. V. 8. Art. 27.
  30. Kamyshev N.G., Iliadi K.G., Bragina J.V. // Learning & Memory. 1999. V. 6. № 1. P. 1–20.
  31. Vasilieva S.A., Tokmacheva E.V., Medvedeva A.V., Ermilova A.A., Nikitina E.A., Shchegolev B.F., Surma S.V., Savvateeva-Popova E.V. // Cell and Tissue Biology. 2020. V. 14. № 3. P. 178–189.
  32. Mehta N., Cheng H.Y.M. // J. Mol. Biol. 2012. V. 425. № 19. P. 3609–3624.
  33. Savvateeva-Popova E.V., Zhuravlev A.V., Brázda V., Zakharov G.A., Kaminskaya A.N., Medvedeva A.V., Nikitina E.A., Tokmatcheva E.V., Dolgaya J.F., Kulikova D.A., Zatsepina O.G., Funikov S.Y., Ryazansky S.S., Evgen’ev M.B.// Front. Genet. 2017. V. 8. Art. 123.
  34. Sempere L.F., Sokol N.S., Dubrovsky E.B., Berger EM, Ambros V. // Dev. Biol. 2003. V. 259. № 1. P. 9–18.
  35. Weng R., Chin J.S.R, Yew J.Y. // eLife. 2013. V. 2. Art. e00640.
  36. Xue Y., Zhang Y. // BMC Neurosci. 2018. V. 19. № 1. https://doi.org/10.1186/s12868–018–0401–8
  37. Медведева А.В., Реброва А.В., Заломаева Е.С. // Журнал эволюционной биохимии и физиологии. 2022. T. 58. № 1. C. 34–42.
  38. Adel M., Griffith L.C. // Neuroscience Bulletin. 2021. V. 37. № 6. P. 831–852.
  39. Davis R.L., Zhong Y. // Neuron. 2017. V. 95. P. 490–503.
  40. Kasture A.S., Hummel T., Sucic S., Freissmuth M. // International Journal of Molecular Sciences. 2018. V. 19. Art. 1788.
  41. Suberbielle E., Sanchez P.E., Kravitz A.V. // Nature Neuroscience. 2013. V. 16. № 5. P. 613–621.
  42. Verheijen B.M., Vermulst M., van Leeuwen F.W. // Acta Neuropathologica. 2018. V. 135. № 6. P. 811–826.
  43. Ishikawa T., Matsumoto A., Kato T. Jr., Togashi S., Ryo H., Ikenaga M., Todo T., Ueda R., Tanimura T. // Genes Cells. 1999. V. 4. № 1. P. 57–65.
  44. Smith K.D., Fu M.A., Brown E.J. // Journal of Cell Biology. 2009. V. 187. № 1. P. 15–23.
  45. Thöni V., Oliva R., Mauracher D., Egg M. // Chronobiology International. 2021. V. 38. № 8. P. 1120–1134.
  46. Bozek K., Kiełbasa S.M., Kramer A., Herzel H. // Genomics & Informatics. 2007. V. 18. P. 65–74.
  47. Peek C., Levine D.C., Cedernaes J., Taguchi A., Kobayashi Y., Tsai S.J., Bonar N.A., McNulty M.R., Ramsey K.M., Bass J. // Cell Metab. 2017. V. 25. № 1. P. 86–92.
  48. Elhalel G., Price C., Fixler D., Shainberg A. // Scientific Reports. 2019. V. 9. № 1. Art. 1645.
  49. Vaughan M.E., Wallace M., Handzlik M.K. // Science. 2020. V. 23. № 7. Art. 101338.
  50. Hernansanz-Agustín P., Enríquez J.A. // Antioxidants. 2021. V. 10. № 3. Art. 415.
  51. Бучаченко А.Л. // Усп. химии. 2014. Т. 83. № 1. С. 1–12.
  52. Srinivas U.S., Tan B.W.Q., Vellayappan B.A., Jeyasekharan A.D. // Redox Biology. 2019. V. 25. Art. 101084.
  53. Caldecott K.W., Ward M.E., Nussenzweig A. // Nature Genetics. 2022. V. 54. P. 115–120.
  54. Caridi C.P., Plessner М., Grosse R., Chiolo I. // Nat Cell Biol. 2019. V. 21. № 9. P. 1068–1077.
  55. Xu Q., Huff L., Fujii M., Griendling K. // Free Radic Biol Med. 2017. V. 109. P. 84–107.
  56. Медведева А.В., Токмачева Е.В., Никитина Е.А., Васильева С.А., Заломаева Е.С., Савватеева-Попова Е.В. // Медицинский академический журнал. 2020. T. 20. № 4. C. 45–54.
  57. Movafagh Sh., Crooc S., Vo K. // J Cell Biochem. 2015. V. 116. № 5. P. 696–703.
  58. Wozny A.-S., Gauthier A., Alphonse G. // Cancers. 2021. V. 13. № 15. Art. 3833.
  59. Cheng L., Yu H., Yan N., Lai K., Xiang M. // Front. Cell. Neurosci. 2017. V. 11. Art. 20.
  60. Bellemer A. // Temperature (Austin). 2015. V. 16. P. 2227–2243.
  61. Gentile C., Sehodova H., Chen Ch., Stanewsky R. // Сurr Biol. 2013. V. 23. P. 185–195.
  62. Yoshii T., Hermann Ch., Helfrich-Forster Ch. // J Biol Rhithms. 2010. V. 25. № 6. P. 387–398.
  63. D’Amico-Damião V., Carvalho R F. // Front. Plant Sci. 2018. V. 9. Art. 1897.
  64. Kidd P B., Young M V., Siggia E D. // PNAS. 2015. V. 112. № 46. Р. 6284–6292.
  65. Москалев А.А., Малышева О.А. // Экологическая генетика. 2010. Т. 8. С. 67–80.
  66. Никитина Е.А., Комарова А.В., Голубкова Е.В. // Генетика. 2003. Т. 39. № 3. С. 341–348.
  67. Nikitina E.A., Kaminskaya A.N., Molotkov D.A., Popov A.V., Savvateeva-Popova E.V. // Journal of Evolutionary Biochemistry and Physiology. 2014. V. 50. № 2. P. 154–166.
  68. Никитина Е.А., Медведева А.В., Долгая Ю.Ф. // Журнал эволюционной биохимии и физиологии. 2012. Т. 48. № 6. С. 588–596.
  69. Doshi B., Hightower L.E., Lee J. // Cell Stress Chaperones. 2009. V. 14. P. 445–457.

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. The role of CRY in switching the molecular clock. The arrows reflect the impact on the processes described in the text (adapted from Damulewicz, Mazzotta, 2020).

Download (201KB)
3. Fig. 2. The system of circadian oscillatory neurons of the drosophila brain: AD – antennal lobes; FG – faceted eyes; L – lamina; M – medula; GT – mushroom body; CC – central complex; OC – ocelli; k-VLN – short ventro-lateral neurons; d-VLN – long ventro-lateral neurons; DLN – dorso-lateral neurons; DN – dorsal neurons; ZLN – posterolateral neurons (adapted from Helfrich-Förster, 2005).

Download (161KB)
4. Fig. 3. Diagram of the influence of the magnetic field on the radical pairs formed between FADH (reduced flavinadenine dinucleotide) and tryptophan in the active site of the CRY molecule: S1 and S2 are unpaired electron spins that precess in a local magnetic field formed by the superposition of an external magnetic field on the intrinsic magnetic fields of I1 and I2 nuclear spins. The reverse electron transfer from tryptophan to FADH quenches the active state of cryptochrome, provided that the electron spins are in the singlet state (adapted from Solov'yov, Schulten, 2009).

Download (94KB)
5. Fig. 5. A hypothetical scheme of the influence of the magnetic field through the CRY magnetosensor. The arrows reflect the impact on the processes described in the text.

Download (237KB)
6. Fig. 6. Schematic representation of the interaction of circadian rhythm systems and stress response to hypoxia: ROS are reactive oxygen species, and DCR are double–stranded breaks. The arrows reflect the impact on the processes described in the text.

Download (234KB)
7. Fig. 7. Diagram of the relationship between the circadian rhythm system and the stress response to temperature shock. BTSH are heat shock proteins. The arrows reflect the impact on the processes described in the text.

Download (132KB)
8. Fig. 8. Hypothetical diagram of the CRY role: BTSH – heat shock proteins; ROS – reactive oxygen species; DCR – double–stranded breaks; GT - mushroom bodies; CC – central complex. The arrows reflect the impact on the processes described in the text.

Download (229KB)

Copyright (c) 2024 Russian Academy of Sciences