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Origin and Evolution of the Nervous System: New Data from Comparative Whole Genome Studies of Multicellular Animals

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Abstract

For evolutionary neuroscience, 2021 is associated with great research achievements based on cell whole genome sequencing methods. These studies have made significant progress in understanding several fundamental issues. How and when did the first neurons appear in animal evolution? What were the first nervous systems of basal Metazoa, and what could be inherited by the modern vertebrate brain from their ancient organization? Why has glutamate become the dominant neurotransmitter in the mammalian brain? What genes and how do they determine the differences between the human brain and the brain of other vertebrates? How often is cotransmission (the use of several classical neurotransmitters by the same neuron) observed in the nervous system of different types of multicellular animals? This review is devoted to the analysis of revisions in the theoretical statements of evolutionary neuroscience, which are associated with the summarization of the results of recent years.

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REFERENCES

  1. Bayramov, A.V., Ermakova, G.V., Kuchryavyy, A.V., et al., Genome duplications as the basis of vertebrates’ evolutionary success, Russ. J. Dev. Biol., 2021, vol. 52, pp. 141–163. https://doi.org/10.1134/S1062360421030024

    Article  Google Scholar 

  2. Brodsky, V.Y., Direct cell-cell communications and social behavior of cells in mammals, protists, and bacteria. possible causes of multicellularity, Russ. J. Dev. Biol., 2009, vol. 40, pp. 69–82. https://doi.org/10.1134/S1062360409020027

    Article  Google Scholar 

  3. Brodskii, V.Ya., Okolochasovye signaly, metabolizm, funktsii. Pryamye mezhkletochnye vzaimodeistviya (Circahoralian Signals, Metabolism, and Functions. Direct Cell–Cell Communications), Vasil’ev, A.V., Ed., Moscow: Nauchnyi Mir, 2021. ISBN: 978-5-91522-505-2.

  4. Brunet, C. and Sprecher, S.G., Single-cell transcriptomic reveals dual and multi-transmitter use in neurons across metazoans, Front. Mol. Neurosci., 2021, vol. 14, art. 623148. https://doi.org/10.3389/fnmol.2021.623148

    Article  CAS  Google Scholar 

  5. Buznikov, G.A., Preneural transmitters as regulators of embryogenesis. Current state of problem, Russ. J. Dev. Biol., 2007, vol. 38, pp. 213–220. https://doi.org/10.1134/S1062360407040042

    Article  CAS  Google Scholar 

  6. D’iakonova, T.L. and D’iakonova, V.E., Participation of receptors of the NMDA type in regulation by glutamate of alimentary motor program of the freshwater mollusc Lymnaea stagnalis, Zh. Evol. Biokhim. Fiziol., 2010, vol. 46, no. 1, pp. 45–51.

    PubMed  Google Scholar 

  7. Dyakonova, T.L., Rearrangement of neuronal interactions upon activation of different glutamate receptors, Dokl. Biol. Sci, 2003, vol. 388, pp. 21–27. https://doi.org/10.1023/a:1022435607789

    Article  CAS  PubMed  Google Scholar 

  8. Dyakonova, V.E., Neuronal counter of the life span: does it exist?, Russ. J. Dev. Biol., 2020, vol. 51, pp. 197–200. https://doi.org/10.1134/S1062360420030066

    Article  Google Scholar 

  9. Dyakonova, V.E. and Sakharov, D.A., Postreflektoraya neirobiologiya povedeniya (Post-Reflex Neurobiology of Behavior), Ser. Razumnoe povedenie i yazyk (Reasonable Behavior and Language), Moscow: Yazyki Slavyanskikh Kul’tur, 2019. ISBN 978-5-907117-52-5

  10. Evrony, G.D., Cai, X., Lee, E., et al., Single-neuron sequencing analysis of l1 retrotransposition and somatic mutation in the human brain, Cell, 2012, vol. 151, no. 3, pp. 483–496.

    Article  CAS  Google Scholar 

  11. Fiddes, I.T., Lodewijk, G.A., Mooring, M., Bosworth, C.M., Ewing, A.D., et al., Human-specific NOTCH2NL genes affect notch signaling and cortical neurogenesis, Cell, 2018, vol. 173, no. 6, pp. 1356–1369, article e22. https://doi.org/10.1016/j.cell.2018.03.051

  12. Girskis, K.M., Stergachis, A.B., DeGennaro, E.M., Doan, R.N., Qian, X., et al., Rewiring of human neurodevelopmental gene regulatory programs by human accelerated regions, Neuron, 2021, S0896-6273(21)00580-8. https://doi.org/10.1016/j.neuron.2021.08.005

  13. Grassi, D., Franz, H., Vezzali, R., et al., Neuronal activity, TGFβ-signaling and unpredictable chronic stress modulate transcription of Gadd45 family members and DNA methylation in the hippocampus, Cereb. Cortex, 2017, vol. 27, no. 8, pp. 4166–4181. https://doi.org/10.1093/cercor/bhx095

    Article  PubMed  Google Scholar 

  14. Hazen, J.L., Faust, G.G., Rodriguez, A.R., et al., The complete genome sequences, unique mutational spectra, and developmental potency of adult neurons revealed by cloning, Neuron, 2016, vol. 89, no. 6, pp. 1223–1236.https://doi.org/10.1016/j.neuron.2016.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Jékely, G., The chemical brain hypothesis for the origin of nervous systems, Philos. Trans. R. Soc., B, 2021, vol. 376, article 20190761. https://doi.org/10.1098/rstb.2019.0761

  16. Krushinskii, A.L., Cost of solving the problem: biophysical prerequisites and possible evolutionary consequences, Ross. Zh. Kogn. Nauki, 2015, vol. 2, no. 1, pp. 52–61.

    Google Scholar 

  17. Moroz, L.L., Multiple origins of neurons from secretory cells, Front. Cell. Dev. Biol., 2021, vol. 9, article 669087. https://doi.org/10.3389/fcell.2021.669087

    Article  PubMed  PubMed Central  Google Scholar 

  18. Moroz, L.L. and Romanova, D.Y., Selective advantages of synapses in evolution, Front. Cell Dev. Biol., 2021. https://doi.org/10.3389/fcell.2021.726563

  19. Moroz, L.L., Romanova, D.Y., and Kohn, A.B., Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters, Philos. Trans. R. Soc., B, 2021a, vol. 376, no. 1821, article 20190762. https://doi.org/10.1098/rstb.2019.0762

  20. Moroz, L.L., Nikitin, M.A., Poličar, P.G., Kohn, A.B., and Romanova, D.Y., Evolution of glutamatergic signaling and synapses, Neuropharmacology, 2021b, article 108740. https://doi.org/10.1016/j.neuropharm.2021.108740

  21. Nezlin, L.P. and Voronezhskaya, E.E., Early peripheral sensory neurons in the development of trochozoan animals, Russ. J. Dev. Biol., 2017, vol. 48, pp. 130–143.https://doi.org/10.1134/S1062360417020060

  22. Romanova, D.Y., Heyland, A., Sohn, D., Kohn, A.B., Fasshauer, D., Varoqueaux, F., and Moroz, L.L., Glycine as a signaling molecule and chemoattractant in Trichoplax (Placozoa): insights into the early evolution of neurotransmitters, Neuroreport, 2020, vol. 31, no. 6, pp. 490–497. https://doi.org/10.1097/WNR.0000000000001436

    Article  CAS  PubMed  Google Scholar 

  23. Romanova, D.Y., Varoqueaux, F., Daraspe, J., Nikitin, M.A., Eitel, M., Fasshauer, D., and Moroz, L.L., Hidden cell diversity in Placozoa: ultrastructural insights from Hoilungia hongkongensis, Cell Tissue Res., 2021 (in press). PMID: 33876313.https://doi.org/10.1007/s00441-021-03459-y

  24. Rosenegger, D. and Lukowiak, K., The participation of NMDA receptors, PKC, and MAPK in the formation of memory following operant conditioning in Lymnaea, Mol. Brain, 2010, vol. 3. https://doi.org/10.1186/1756-6606-3-24

  25. Ryan, J.F., Pang, K., Schnitzler, C.E., Nguyen, A.D., et al., The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution, Science, 2013, vol. 342, no. 6164, article 1242592. https://doi.org/10.1126/science.1242592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sakharov, D.A., Evolutionary aspects of transmitter heterogeneity, J. Neural Transm., 1974, suppl. 11, pp. 43–59.

  27. Sakharov, D.A., Genealogiya neironov (Genealogy of Neurons), Moscow: Nauka, 1974.

  28. Shibata, M., et al., Hominini-specific regulation of CBLN2 increases prefrontal spinogenesis, Nature, 2021a. https://doi.org/10.1038/s41586-021-03952-y

  29. Shibata, M., Pattabiraman, K., Lorente-Galdos, B., et al., Regulation of prefrontal patterning and connectivity by retinoic acid, Nature, 2021b. https://doi.org/10.1038/s41586-021-03953-x

  30. Sukhinich, K.K., Shakirova, K.M., Dashinimaev, E.B., et al., Development of 3D cerebral aggregates in the brain ventricles of adult mice, Russ. J. Dev. Biol., 2021, vol. 52, pp. 164–175. https://doi.org/10.1134/S1062360421030061

    Article  CAS  Google Scholar 

  31. Sultan F.A. and Sweatt J.D. The role of the gadd45 family in the nervous system: a focus on neurodevelopment, neuronal injury, and cognitive neuroepigenetics, in Gadd45. Stress Sensor Genes, Liebermann, D.A. and Hoffman, B., Eds., Springer, 2013, pp. 81–121.

    Google Scholar 

  32. Wu, W., Hill, S.E., Nathan, W.J., et al., Neuronal enhancers are hotspots for DNA single-strand break repair, Nature, 2021, vol. 593, pp. 440–444. https://doi.org/10.1038/s41586-021-03468-5

    Article  CAS  PubMed  Google Scholar 

  33. ** Neocortex, Neuron, 2020. S0896-6273(20)30758-3. https://doi.org/10.1016/j.neuron.2020.09.034

  34. Zullo, J.M., Drake, D., Aron, L., et al., Regulation of lifespan by neural excitation and rest, Nature, 2019, vol. 574, no. 7778, pp. 359–364. https://doi.org/10.1038/s41586-019-1647-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

I am grateful to Yu.A. Kraus for valuable advice and editing of the manuscript.

Funding

The work was performed within the framework of State Assignment 0108-2019-0002 and with the financial support of the grant of the Russian Foundation for Basic Research 19-04-00628.

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Authors and Affiliations

  1. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, 119334, Moscow, Russia

    V. E. Dyakonova

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  1. V. E. Dyakonova
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Correspondence to V. E. Dyakonova.

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The author declares that she has no conflict of interests. This article does not contain any studies involving human participants or laboratory animals as experimental models performed by the author.

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Translated by A. Ermakov

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Dyakonova, V.E. Origin and Evolution of the Nervous System: New Data from Comparative Whole Genome Studies of Multicellular Animals. Russ J Dev Biol 53, 55–64 (2022). https://doi.org/10.1134/S1062360422010088

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