Effects of the dynamics of noise-induced calcium signals in a biophysical model of the astrocytic process

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Abstract

The purpose of this work is to study the effects of spatio-temporal dynamics of spontaneous calcium signaling in the morphological structure of an astrocyte at the subcellular level using biophysical mathematical modeling methods. Methods. This work proposes a biophysical multicompartmental model of noise-induced calcium dynamics in the astrocytic process. The model describes the process of generation of spontaneous Ca2+ signals induced by the stochastic activation of voltage-dependent Ca2+ channels on the plasma membrane of the astrocyte. The model allows us to study the dynamics of the propagation of spontaneous local Ca2+ signals and the mechanisms of formation of spatial Ca2+ patterns in the astrocytic process. Results. The developed model enables studying the influence of morphology and intracellular biophysical mechanisms on the characteristics of spontaneous noise-induced Ca2+ signaling in the astrocytic process. The parameter ranges at which the model qualitatively reproduces the spontaneous Ca2+ activity at the subcellular level observed in experimental studies have been specified. The characteristics of noise-induced Ca2+ patterns propagating along the process were investigated, depending on the internal structure of the process, its geometry, and the steady state concentration of inositol 1,4,5-triphosphate molecules.

About the authors

Anastasia Viktorovna Ermolaeva

Lobachevsky State University of Nizhny Novgorod

ORCID iD: 0000-0002-9513-7434
SPIN-code: 4135-8585
Scopus Author ID: 57205610474
ResearcherId: AAI-2314-2021
603950 Nizhny Novgorod, Gagarin Avenue, 23

Innokentiy A. Kastalskiy

Lobachevsky State University of Nizhny Novgorod

ORCID iD: 0000-0001-6050-4356
Scopus Author ID: 55314345300
ResearcherId: A-6923-2014
603950 Nizhny Novgorod, Gagarin Avenue, 23

Viktor Borisovich Kazantsev

Institute of Applied Physics of the Russian Academy of Sciences

ORCID iD: 0000-0002-2881-6648
ResearcherId: L-1424-2013
ul. Ul'yanova, 46, Nizhny Novgorod , 603950, Russia

Susanna Yurevna Gordleeva

Lobachevsky State University of Nizhny Novgorod; Innopolis University

ORCID iD: 0000-0002-7687-3065
603950 Nizhny Novgorod, Gagarin Avenue, 23

References

  1. Semyanov A. Spatiotemporal pattern of calcium activity in astrocytic network // Cell calcium. 2019. Vol. 78. P. 15–25. doi: 10.1016/j.ceca.2018.12.007.
  2. Li Y. X, Rinzel J. Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism // Journal of theoretical Biology. 1994. Vol. 166, no. 4. P. 461–73. doi: 10.1006/jtbi.1994.1041.
  3. Ullah G., Jung P., Cornell-Bell A. H. Anti-phase calcium oscillations in astrocytes via inositol (1, 4, 5)-trisphosphate regeneration // Cell calcium. 2006. Vol. 39, no. 3. P. 197–208. DOI: 10.1016/ j.ceca.2005.10.009.
  4. Nett W. J., Oloff S. H., Mccarthy K. D. Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity // Journal of neurophysiology. 2002. Vol. 87, no. 1. P. 528–37. doi: 10.1152/jn.00268.2001.
  5. Volterra A., Liaudet N., Savtchouk I. Astrocyte Ca2+ signalling: an unexpected complexity // Nature Reviews Neuroscience. 2014. Vol. 15, no. 5. P. 327–35. doi: 10.1038/nrn3725.
  6. Skupin A., Kettenmann H., Falcke M. Calcium signals driven by single channel noise // PLoS computational biology. 2010. Vol. 6, no. 8. P. e1000870. doi: 10.1371/journal.pcbi.1000870.
  7. Oschmann F., Mergenthaler K., Jungnickel E., Obermayer K. Spatial separation of two different pathways accounting for the generation of calcium signals in astrocytes // PLoS computational biology. 2017. Vol. 13, no. 2. P. e1005377. doi: 10.1371/journal.pcbi.1005377.
  8. De Pitta M., Goldberg M., Volman V., Berry H., Ben-Jacob E. Glutamate regulation of calcium and IP3 oscillating and pulsating dynamics in astrocytes // Journal of biological physics. 2009. Vol. 35. P. 383–411. doi: 10.1007/s10867-009-9155-y.
  9. Matrosov V. V, Kazantsev V. B. Bifurcation mechanisms of regular and chaotic network signaling in brain astrocytes // Chaos: An Interdisciplinary Journal of Nonlinear Science. 2011. Vol. 21, no. 2. doi: 10.1063/1.3574031.
  10. Kang M., Othmer H. G. Spatiotemporal characteristics of calcium dynamics in astrocytes // Chaos: An Interdisciplinary Journal of Nonlinear Science. 2009. Vol. 19, no. 3. doi: 10.1063/1.3206698.
  11. Kazantsev V. B. Spontaneous calcium signals induced by gap junctions in a network model of astrocytes //Physical Review E. 2009. Vol. 79, no. 1. P. 010901. doi: 10.1103/PhysRevE.79.010901.
  12. Gordleeva S. Y., Stasenko S. V., Semyanov A. V., Dityatev A. E., Kazantsev V. B. Bi-directional astrocytic regulation of neuronal activity within a network // Frontiers in computational neuroscience. 2012. Vol. 6. P. 92. doi: 10.3389/fncom.2012.00092.
  13. De Pitta M., Volman V., Berry H., Ben-Jacob E. A tale of two stories: astrocyte regulation of synaptic depression and facilitation // PLoS computational biology. 2011. Vol. 7, no. 12. P. e1002293. doi: 10.1371/journal.pcbi.1002293.
  14. Volman V., Ben-Jacob E., Levine H. The astrocyte as a gatekeeper of synaptic information transfer // Neural computation. 2007. Vol. 19, no. 2. P. 303–26. doi: 10.1162/neco.2007.19.2.303.
  15. Postnov D. E., Koreshkov R. N., Brazhe N. A., Brazhe A. R., Sosnovtseva O. V. Dynamical patterns of calcium signaling in a functional model of neuron–astrocyte networks // Journal of biological physics. 2009. Vol. 35. P. 425–45. doi: 10.1007/s10867-009-9156-x.
  16. Bindocci E., Savtchouk I., Liaudet N., Becker D., Carriero G., Volterra A. Three-dimensional Ca2+ imaging advances understanding of astrocyte biology // Science. 2017. Vol. 356, no. 6339. P. eaai8185. doi: 10.1126/science.aai8185.
  17. Brazhe A., Verisokin A., Verveyko D., Postnov D. Astrocytes: new evidence, new models, new roles // Biophysical Reviews. 2023. P. 1–31. doi: 10.1007/s12551-023-01145-7.
  18. Wu Y. W., Gordleeva S., Tang X., Shih P. Y., Dembitskaya Y., Semyanov A. Morphological profile determines the frequency of spontaneous calcium events in astrocytic processes // Glia. 2019. Vol. 67, no. 2. P. 246-62. doi: 10.1002/glia.23537.
  19. Savtchenko L. P., Bard L., Jensen T. P., Reynolds J. P., Kraev I., Medvedev N., Stewart M. G., Henneberger C., Rusakov D. A. Disentangling astroglial physiology with a realistic cell model in silico // Nature communications. 2018. Vol. 9, no. 1. P. 3554. doi: 10.1038/s41467-018-05896-w.
  20. Gordleeva S. Y., Lebedev S. A., Rumyantseva M. A., Kazantsev V. B. Astrocyte as a detector of synchronous events of a neural network // JETP Letters. 2018. Vol. 107. P. 440–5. DOI: 10.1134/ S0021364018070032.
  21. Gordleeva S. Y., Ermolaeva A. V., Kastalskiy I. A., Kazantsev V. B. Astrocyte as spatiotemporal integrating detector of neuronal activity // Frontiers in physiology. 2019. Vol. 10. P. 294. doi: 10.3389/fphys.2019.00294.
  22. Kastalskiy I., Ermolaeva A., Kazantsev V., Gordleeva S. Impact of the steady state IP3 level on the intracellular Ca2+ signaling in spatially distributed model of astrocyte // 2020 4th Scientific School on Dynamics of Complex Networks and their Application in Intellectual Robotics (DCNAIR). 2020. P. 120–123. doi: 10.1109/DCNAIR50402.2020.9216749.
  23. Zeng S., Li B., Zeng S., Chen S. Simulation of spontaneous Ca2+ oscillations in astrocytes mediated by voltage-gated calcium channels // Biophysical journal. 2009. Vol. 97, no. 9. P. 2429– 37. doi: 10.1016/j.bpj.2009.08.030.
  24. Yaguchi T., Nishizaki T. Extracellular high K+ stimulates vesicular glutamate release from astrocytes by activating voltage-dependent calcium channels // Journal of Cellular Physiology. 2010. Vol. 225, no. 2. P. 512-8. doi: 10.1002/jcp.22231.
  25. Letellier M., Park Y. K., Chater T. E., Chipman P. H., Gautam S. G., Oshima-Takago T., Goda Y. Astrocytes regulate heterogeneity of presynaptic strengths in hippocampal networks // Proceedings of the National Academy of Sciences. 2016. Vol. 113, no. 19. P. E2685-94. doi: 10.1073/pnas. 1523717113.
  26. Zamora N. N., Cheli V. T., Santiago Gonzalez D. A., Wan R., Paez P. M. Deletion of Voltage-Gated Calcium Channels in Astrocytes during Demyelination Reduces Brain Inflammation and Promotes Myelin Regeneration in Mice. The Journal of Neuroscience. 2020. Vol. 40, no. 17. P. 3332–3347. doi: 10.1523/JNEUROSCI.1644-19.2020.
  27. Hodgkin A. L., Huxley A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve // The Journal of physiology. 1952. Vol. 117, no. 4. P. 500–544. doi: 10.1113/jphysiol.1952.sp004764.
  28. Dupont G., Goldbeter A. One-pool model for Ca2+ oscillations involving Ca2+ and inositol 1,4,5-trisphosphate as co-agonists for Ca2+ release // Cell calcium. 1993. Vol. 14, no. 4. P. 311–22. doi: 10.1016/0143-4160(93)90052-8.
  29. Гордлеева С.Ю., Матросов В. В., Казанцев В. Б. Кальциевые колебания в астроцитах. Часть 1. Астроцит как генератор кальциевых колебаний // Известия вузов. Прикладная нелинейная динамика. 2012. Vol. 20, № 3. C. 29–39. doi: 10.3389/fphys.2019.00294.
  30. Cresswell-Clay E., Crock N., Tabak J. and Erlebacher G. A Compartmental Model to Investigate Local and Global Ca2+ Dynamics in Astrocytes // Frontiers in Computational Neuroscience. 2018. Vol. 12. P. 94. doi: 10.3389/fncom.2018.00094.
  31. Verisokin A. Y., Verveyko D. V., Postnov D. E., Brazhe A. R. Modeling of Astrocyte Networks: Toward Realistic Topology and Dynamics // Frontiers in Cellular Neuroscience. 2021. Vol. 15. P. 645068. doi: 10.3389/fncel.2021.645068.
  32. Santello M., Toni N., Volterra A. Astrocyte function from information processing to cognition and cognitive impairment // Nature neuroscience. 2019. Vol. 22, no. 2. P. 154–66. doi: 10.1038/s41593- 018-0325-8.
  33. Popov A., Brazhe A., Denisov P., Sutyagina O., Li L., Lazareva N., Verkhratsky A., Semyanov A. Astrocyte dystrophy in ageing brain parallels impaired synaptic plasticity // Aging cell. 2021. Vol. 20, no. 3. P. e13334. doi: 10.18500/0869-6632-2012-20-3-29-39.
  34. Olabarria M., Noristani H. N., Verkhratsky A., Rodrıguez J. J. Concomitant astroglial atrophy and astrogliosis in a triple transgenic animal model of Alzheimer’s disease // Glia. 2010. Vol. 58, no. 7. P. 831–8. doi: 10.1002/glia.20967.

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