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Prototypical pacemaker neurons are immunocompetent cells

View ORCID ProfileAlexander Klimovich, Stefania Giacomello, Åsa Björklund, Louis Faure, Marketa Kaucka, Christoph Giez, Andrea P. Murillo-Rincon, Ann-Sophie Matt, Gabriele Crupi, Jaime de Anda, Gerard C.L. Wong, Mauro D’Amato, Igor Adameyko, Thomas C.G. Bosch
doi: https://doi.org/10.1101/750026
Alexander Klimovich
Zoological Institute, University of Kiel, Kiel, Germany.
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  • For correspondence: tbosch@zoologie.uni-kiel.de aklimovich@zoologie.uni-kiel.de
Stefania Giacomello
Department of Biochemistry and Biophysics, National Infrastructure of Sweden, Science for Life Laboratory, Stockholm University, Solna, Sweden.
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Åsa Björklund
Department of Cell and Molecular Biology, National Infrastructure of Sweden, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
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Louis Faure
Department of Molecular Neurosciences, Center for Brain Research, Medical University Vienna, Vienna, Austria.
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Marketa Kaucka
Department of Molecular Neurosciences, Center for Brain Research, Medical University Vienna, Vienna, Austria.Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden.Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Plön, Germany.
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Christoph Giez
Zoological Institute, University of Kiel, Kiel, Germany.
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Andrea P. Murillo-Rincon
Zoological Institute, University of Kiel, Kiel, Germany.
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Ann-Sophie Matt
Zoological Institute, University of Kiel, Kiel, Germany.
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Gabriele Crupi
Zoological Institute, University of Kiel, Kiel, Germany.
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Jaime de Anda
Department of Bioengineering, Department of Chemistry and Biochemistry, and California NanoSystems Institute, University of California Los Angeles, Los Angeles, USA.
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Gerard C.L. Wong
Department of Bioengineering, Department of Chemistry and Biochemistry, and California NanoSystems Institute, University of California Los Angeles, Los Angeles, USA.
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Mauro D’Amato
School of Biological Sciences, Monash University, Clayton, Australia.
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Igor Adameyko
Department of Molecular Neurosciences, Center for Brain Research, Medical University Vienna, Vienna, Austria.Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden.
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Thomas C.G. Bosch
Zoological Institute, University of Kiel, Kiel, Germany.
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  • For correspondence: tbosch@zoologie.uni-kiel.de aklimovich@zoologie.uni-kiel.de
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Abstract

Pacemaker neurons exert control over neuronal circuit function by their intrinsic ability to generate rhythmic bursts of action potential. Recent work has identified rhythmic gut contractions in human, mice and hydra to be dependent on both neurons and the resident microbiota. However, little is known about the evolutionary origin of these neurons and their interaction with microbes. In this study, we identified and functionally characterized prototypical ANO/SCN/TRPM ion channel expressing pacemaker cells in the basal metazoan Hydra by using a combination of single-cell transcriptomics, immunochemistry, and functional experiments. Unexpectedly, these prototypical pacemaker neurons express a rich set of immune-related genes mediating their interaction with the microbial environment. Functional experiments validated a model of the evolutionary emergence of pacemaker cells as neurons using components of innate immunity to interact with the microbial environment and ion channels to generate rhythmic contractions.

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Posted August 30, 2019.
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Prototypical pacemaker neurons are immunocompetent cells
Alexander Klimovich, Stefania Giacomello, Åsa Björklund, Louis Faure, Marketa Kaucka, Christoph Giez, Andrea P. Murillo-Rincon, Ann-Sophie Matt, Gabriele Crupi, Jaime de Anda, Gerard C.L. Wong, Mauro D’Amato, Igor Adameyko, Thomas C.G. Bosch
bioRxiv 750026; doi: https://doi.org/10.1101/750026
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Prototypical pacemaker neurons are immunocompetent cells
Alexander Klimovich, Stefania Giacomello, Åsa Björklund, Louis Faure, Marketa Kaucka, Christoph Giez, Andrea P. Murillo-Rincon, Ann-Sophie Matt, Gabriele Crupi, Jaime de Anda, Gerard C.L. Wong, Mauro D’Amato, Igor Adameyko, Thomas C.G. Bosch
bioRxiv 750026; doi: https://doi.org/10.1101/750026

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