Literature DB >> 31916933

Origin and role of the cerebrospinal fluid bidirectional flow in the central canal.

Olivier Thouvenin1,2, Ludovic Keiser3, Yasmine Cantaut-Belarif1, Martin Carbo-Tano1, Frederik Verweij4, Nathalie Jurisch-Yaksi5,6, Pierre-Luc Bardet1, Guillaume van Niel4, Francois Gallaire3, Claire Wyart1.   

Abstract

Circulation of the cerebrospinal fluid (CSF) contributes to body axis formation and brain development. Here, we investigated the unexplained origins of the CSF flow bidirectionality in the central canal of the spinal cord of 30 hpf zebrafish embryos and its impact on development. Experiments combined with modeling and simulations demonstrate that the CSF flow is generated locally by caudally-polarized motile cilia along the ventral wall of the central canal. The closed geometry of the canal imposes the average flow rate to be null, explaining the reported bidirectionality. We also demonstrate that at this early stage, motile cilia ensure the proper formation of the central canal. Furthermore, we demonstrate that the bidirectional flow accelerates the transport of particles in the CSF via a coupled convective-diffusive transport process. Our study demonstrates that cilia activity combined with muscle contractions sustain the long-range transport of extracellular lipidic particles, enabling embryonic growth.
© 2020, Thouvenin et al.

Entities:  

Keywords:  central canal; cerebrospinal fluid; cilia dynamics; embryogenesis; fluid dynamics; long range transport; physics of living systems; zebrafish

Mesh:

Substances:

Year:  2020        PMID: 31916933      PMCID: PMC6989091          DOI: 10.7554/eLife.47699

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.713


  63 in total

1.  Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia.

Authors:  Antonia Borovina; Simone Superina; Daniel Voskas; Brian Ciruna
Journal:  Nat Cell Biol       Date:  2010-03-21       Impact factor: 28.824

2.  Biomimetic cilia arrays generate simultaneous pumping and mixing regimes.

Authors:  A R Shields; B L Fiser; B A Evans; M R Falvo; S Washburn; R Superfine
Journal:  Proc Natl Acad Sci U S A       Date:  2010-08-26       Impact factor: 11.205

3.  Polycystin-2 immunolocalization and function in zebrafish.

Authors:  Tomoko Obara; Steven Mangos; Yan Liu; Jinhua Zhao; Stephanie Wiessner; Albrecht G Kramer-Zucker; Felix Olale; Alexander F Schier; Iain A Drummond
Journal:  J Am Soc Nephrol       Date:  2006-08-30       Impact factor: 10.121

4.  c21orf59/kurly Controls Both Cilia Motility and Polarization.

Authors:  Kimberly M Jaffe; Daniel T Grimes; Jodi Schottenfeld-Roames; Michael E Werner; Tse-Shuen J Ku; Sun K Kim; Jose L Pelliccia; Nicholas F C Morante; Brian J Mitchell; Rebecca D Burdine
Journal:  Cell Rep       Date:  2016-02-18       Impact factor: 9.423

5.  LRRC50, a conserved ciliary protein implicated in polycystic kidney disease.

Authors:  Ellen van Rooijen; Rachel H Giles; Emile E Voest; Carina van Rooijen; Stefan Schulte-Merker; Freek J van Eeden
Journal:  J Am Soc Nephrol       Date:  2008-04-02       Impact factor: 10.121

Review 6.  Making sense of cilia in disease: the human ciliopathies.

Authors:  Kate Baker; Philip L Beales
Journal:  Am J Med Genet C Semin Med Genet       Date:  2009-11-15       Impact factor: 3.908

7.  The cerebrospinal fluid provides a proliferative niche for neural progenitor cells.

Authors:  Maria K Lehtinen; Mauro W Zappaterra; Xi Chen; Yawei J Yang; Anthony D Hill; Melody Lun; Thomas Maynard; Dilenny Gonzalez; Seonhee Kim; Ping Ye; A Joseph D'Ercole; Eric T Wong; Anthony S LaMantia; Christopher A Walsh
Journal:  Neuron       Date:  2011-03-10       Impact factor: 17.173

8.  Analysis of Urine Flow in Three Different Ureter Models.

Authors:  Kyung-Wuk Kim; Young Ho Choi; Seung Bae Lee; Yasutaka Baba; Hyoung-Ho Kim; Sang-Ho Suh
Journal:  Comput Math Methods Med       Date:  2017-06-04       Impact factor: 2.238

9.  Neuroinflammatory signals drive spinal curve formation in zebrafish models of idiopathic scoliosis.

Authors:  J L M Van Gennip; C W Boswell; B Ciruna
Journal:  Sci Adv       Date:  2018-12-12       Impact factor: 14.136

10.  Ciliogenesis and cerebrospinal fluid flow in the developing Xenopus brain are regulated by foxj1.

Authors:  Cathrin Hagenlocher; Peter Walentek; Christina M Ller; Thomas Thumberger; Kerstin Feistel
Journal:  Cilia       Date:  2013-09-24
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  20 in total

Review 1.  Development of a straight vertebrate body axis.

Authors:  Michel Bagnat; Ryan S Gray
Journal:  Development       Date:  2020-10-06       Impact factor: 6.868

2.  Daw1 regulates the timely onset of cilia motility during development.

Authors:  Elizabeth A Bearce; Zoe H Irons; Samuel B Craig; Colin J Kuhns; Cynthia Sabazali; Dylan R Farnsworth; Adam C Miller; Daniel T Grimes
Journal:  Development       Date:  2022-06-16       Impact factor: 6.862

Review 3.  Mechanics of Development.

Authors:  Katharine Goodwin; Celeste M Nelson
Journal:  Dev Cell       Date:  2020-12-14       Impact factor: 12.270

Review 4.  Choroid Plexus: The Orchestrator of Long-Range Signalling Within the CNS.

Authors:  Karol Kaiser; Vitezslav Bryja
Journal:  Int J Mol Sci       Date:  2020-07-04       Impact factor: 5.923

5.  Adrenergic activation modulates the signal from the Reissner fiber to cerebrospinal fluid-contacting neurons during development.

Authors:  Yasmine Cantaut-Belarif; Adeline Orts Del'Immagine; Margot Penru; Guillaume Pézeron; Claire Wyart; Pierre-Luc Bardet
Journal:  Elife       Date:  2020-10-13       Impact factor: 8.140

6.  The Spatial and Cell-Type Distribution of SARS-CoV-2 Receptor ACE2 in the Human and Mouse Brains.

Authors:  Rongrong Chen; Keer Wang; Jie Yu; Derek Howard; Leon French; Zhong Chen; Chengping Wen; Zhenghao Xu
Journal:  Front Neurol       Date:  2021-01-20       Impact factor: 4.003

7.  SARS-CoV-2 invasion of the central nervous: a brief review.

Authors:  Ruqaiyyah Siddiqui; Mohammad Ridwane Mungroo; Naveed Ahmed Khan
Journal:  Hosp Pract (1995)       Date:  2021-03-01

8.  Variations in the cerebrospinal fluid dynamics of the American alligator (Alligator mississippiensis).

Authors:  Bruce A Young; James Adams; Jonathan M Beary; Kent-Andre Mardal; Robert Schneider; Tatyana Kondrashova
Journal:  Fluids Barriers CNS       Date:  2021-03-12

9.  CiliaQ: a simple, open-source software for automated quantification of ciliary morphology and fluorescence in 2D, 3D, and 4D images.

Authors:  Nathalie Jurisch-Yaksi; Dagmar Wachten; Jan Niklas Hansen; Sebastian Rassmann; Birthe Stüven
Journal:  Eur Phys J E Soft Matter       Date:  2021-03-08       Impact factor: 1.890

10.  Automated Analysis of Cerebrospinal Fluid Flow and Motile Cilia Properties in The Central Canal of Zebrafish Embryos.

Authors:  Olivier Thouvenin; Yasmine Cantaut-Belarif; Ludovic Keiser; François Gallaire; Claire Wyart
Journal:  Bio Protoc       Date:  2021-03-05
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