Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

ELife
Csaba VerasztóGáspár Jékely

Abstract

Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.

References

Jun 1, 1989·Biology of Reproduction·S A HalbertS E Szal
Oct 1, 1972·The Journal of Cell Biology·S L Tamm
Oct 27, 1999·Proceedings of the National Academy of Sciences of the United States of America·S Gueron, K Levit-Gurevich
Jul 8, 2000·Proceedings. Biological Sciences·A Hay-Schmidt
Dec 17, 2002·The Journal of Comparative Neurology·Elena E VoronezhskayaLeonid P Nezlin
Nov 21, 2008·Nature·Gáspár JékelyDetlev Arendt
Apr 21, 2009·Bioinformatics·Stephan SaalfeldPavel Tomancak
May 12, 2009·Current Biology : CB·Brian MitchellChris Kintner
Mar 23, 2010·Nature Cell Biology·Boris GuiraoNathalie Spassky
Dec 3, 2010·Proceedings. Biological Sciences·Gáspár Jékely
Jan 5, 2011·Frontiers in Zoology·Antje Hl FischerDetlev Arendt
Jan 8, 2011·Evolution & Development·Patrick R H SteinmetzDetlev Arendt
Jun 30, 2011·The Biological Bulletin·Bruno Pernet, Richard R Strathmann
Sep 8, 2011·Proceedings of the National Academy of Sciences of the United States of America·Natan Osterman, Andrej Vilfan
Oct 19, 2011·Proceedings of the National Academy of Sciences of the United States of America·Markus ConzelmannGáspár Jékely
Mar 1, 2012·The Journal of Cell Biology·Luis AlvarezU Benjamin Kaupp
Jun 30, 2012·Nature Methods·Johannes SchindelinAlbert Cardona
Nov 6, 2012·Current Biology : CB·Eszter K VladarJeffrey D Axelrod
Dec 4, 2012·EvoDevo·Albina AsadulinaGáspár Jékely
Feb 2, 2013·Physical Review Letters·Douglas R BrumleyRaymond E Goldstein
Mar 15, 2013·Proceedings of the National Academy of Sciences of the United States of America·Jens Elgeti, Gerhard Gompper
Apr 10, 2013·Proceedings of the National Academy of Sciences of the United States of America·Markus ConzelmannGáspár Jékely
May 15, 2013·Integrative and Comparative Biology·Nadine RandelGáspár Jékely
May 28, 2013·Nature Neuroscience·Grégory ConductierAlice Guyon
Jul 23, 2013·Nature·Tsai-Wen ChenDouglas S Kim
Jan 31, 2014·BMC Biology·Heather MarlowDetlev Arendt
May 29, 2014·ELife·Nadine RandelGáspár Jékely
Jul 31, 2014·ELife·Douglas R BrumleyRaymond E Goldstein
Sep 7, 2014·Proceedings of the National Academy of Sciences of the United States of America·Orr H ShapiroRoman Stocker
Sep 27, 2014·Cell·Maria Antonietta ToschesDetlev Arendt
Apr 17, 2015·BMC Evolutionary Biology·Viktor V StarunovGuillaume Balavoine
Jun 5, 2015·Journal of the Royal Society, Interface·Douglas R BrumleyRaymond E Goldstein
Jun 11, 2015·ELife·Nadine RandelGáspár Jékely
Jul 21, 2015·Cell Reports·Philipp Bauknecht, Gáspár Jékely

❮ Previous
Next ❯

Citations

Jul 6, 2017·ELife·Yee Lian Chew, William R Schafer
Dec 5, 2017·ELife·Elizabeth A WilliamsGáspár Jékely
Nov 23, 2018·Essays in Biochemistry·Kirsty Y Wan
Dec 12, 2018·Genome Biology and Evolution·Patricia Álvarez-CamposAna Riesgo
Dec 31, 2019·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Kirsty Y Wan, Gáspár Jékely
Dec 31, 2019·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Kirsty Y WanWallace F Marshall
Dec 31, 2019·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Kirsty Y Wan
Dec 31, 2019·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Milena MarinkovićGáspár Jékely
May 1, 2020·The Journal of Comparative Neurology·Steven J CookOliver Hobert
Mar 16, 2019·EvoDevo·F Javier Bernardo-GarciaSimon G Sprecher
Jan 4, 2020·Development·José M Martín-Durán, Ferdinand Marlétaz
Mar 4, 2020·International Journal of Molecular Sciences·Julien Bacqué-CazenavePhilippe De Deurwaerdère
Sep 16, 2020·BMC Evolutionary Biology·Suman KumarHarald Hausen
Dec 6, 2019·PloS One·Emily KuehnB Duygu Özpolat
Dec 14, 2018·Frontiers in Neural Circuits·Ben MulcahyMei Zhen
Aug 12, 2021·Cell·Hernando M VergaraDetlev Arendt
Sep 29, 2021·EvoDevo·B Duygu ÖzpolatDetlev Arendt
Sep 24, 2021·The Journal of Experimental Biology·Brian T NedvedMichael G Hadfield
Sep 4, 2020·Developmental Biology·Johanna BischofMichael Levin

❮ Previous
Next ❯

Methods Mentioned

BETA
transgenic
transmission electron microscopy

Software Mentioned

Gephi
Imaris
ssTEM
Catmaid
FIJI
siGOLD
Force Atlas 2 Plugin

Related Concepts

Trending Feeds

COVID-19

Coronaviruses encompass a large family of viruses that cause the common cold as well as more serious diseases, such as the ongoing outbreak of coronavirus disease 2019 (COVID-19; formally known as 2019-nCoV). Coronaviruses can spread from animals to humans; symptoms include fever, cough, shortness of breath, and breathing difficulties; in more severe cases, infection can lead to death. This feed covers recent research on COVID-19.

Blastomycosis

Blastomycosis fungal infections spread through inhaling Blastomyces dermatitidis spores. Discover the latest research on blastomycosis fungal infections here.

Nuclear Pore Complex in ALS/FTD

Alterations in nucleocytoplasmic transport, controlled by the nuclear pore complex, may be involved in the pathomechanism underlying multiple neurodegenerative diseases including Amyotrophic Lateral Sclerosis and Frontotemporal Dementia. Here is the latest research on the nuclear pore complex in ALS and FTD.

Applications of Molecular Barcoding

The concept of molecular barcoding is that each original DNA or RNA molecule is attached to a unique sequence barcode. Sequence reads having different barcodes represent different original molecules, while sequence reads having the same barcode are results of PCR duplication from one original molecule. Discover the latest research on molecular barcoding here.

Chronic Fatigue Syndrome

Chronic fatigue syndrome is a disease characterized by unexplained disabling fatigue; the pathology of which is incompletely understood. Discover the latest research on chronic fatigue syndrome here.

Evolution of Pluripotency

Pluripotency refers to the ability of a cell to develop into three primary germ cell layers of the embryo. This feed focuses on the mechanisms that underlie the evolution of pluripotency. Here is the latest research.

Position Effect Variegation

Position Effect Variagation occurs when a gene is inactivated due to its positioning near heterochromatic regions within a chromosome. Discover the latest research on Position Effect Variagation here.

STING Receptor Agonists

Stimulator of IFN genes (STING) are a group of transmembrane proteins that are involved in the induction of type I interferon that is important in the innate immune response. The stimulation of STING has been an active area of research in the treatment of cancer and infectious diseases. Here is the latest research on STING receptor agonists.

Microbicide

Microbicides are products that can be applied to vaginal or rectal mucosal surfaces with the goal of preventing, or at least significantly reducing, the transmission of sexually transmitted infections. Here is the latest research on microbicides.

Related Papers

Proceedings of the National Academy of Sciences of the United States of America
Markus ConzelmannGáspár Jékely
Current Biology : CB
Florian Raible, Kristin Tessmar-Raible
© 2022 Meta ULC. All rights reserved