Notch/Her12 signalling modulates motile/immotile cilia ratio downstream of Foxj1a in zebrafish left-right organizer
- CEDOC, Chronic Diseases Research Centre, NOVA Medical School, Universidade Nova de Lisboa, Portugal
- Instituto de Medicina Molecular, Centro Académico de Medicina de Lisboa, Portugal
- Instituto Gulbenkian de Ciencia, Portugal
- Max Planck Institute of Molecular Cell Biology and Genetics, Germany
- Instituto de Medicina Molecular, Portugal
Abstract
Foxj1a is necessary and sufficient to specify motile cilia. Using transcriptional studies and slow-scan two-photon live imaging capable of identifying the number of motile and immotile cilia, we now established that the final number of motile cilia depends on Notch signalling (NS). We found that despite all left-right organizer (LRO) cells express foxj1a and the ciliary axonemes of these cells have dynein arms some cilia remain immotile. We identified that this decision is taken early in development in the Kupffer’s Vesicle (KV) precursors the readout being her12 transcription. We demonstrate that overexpression of either her12 or Notch intracellular domain (NICD) increases the number of immotile cilia at the expense of motile cilia, and leads to an accumulation of immotile cilia at the anterior half of the KV. This disrupts the normal fluid flow intensity and pattern, with consequent impact on dand5 expression pattern and left-right (L-R) axis establishment.
Article and author information
Author details
Susana Santos Lopes
Funding
Fundação para a Ciência e a Tecnologia (PTDC/BEX-BID/1411/2014)
- Susana Santos Lopes
Fundação para a Ciência e a Tecnologia (FCT-ANR/BEX-BID/0153/2012)
- Sara Pestana
Fundação para a Ciência e a Tecnologia (PTDC/SAU-OBD/103981/2008)
- Andreia Vaz
Fundação para a Ciência e a Tecnologia (PD/BD/52420/2013)
- Raquel Jacinto
Fundação para a Ciência e a Tecnologia (SFRH/BPD/77258/2011)
- Barbara Tavares
Fundação para a Ciência e a Tecnologia (SFRH/BD/111611/2015)
- Pedro Sampaio
Fundação para a Ciência e a Tecnologia (IF/00951/2012)
- Susana Santos Lopes
The funders had no role in study design, data collection and interpretation, or the on the decision to submit the work for publication.
Reviewing Editor
- Jeremy F Reiter, University of California, San Francisco, United States
Version history
- Received: January 16, 2017
- Accepted: September 3, 2017
- Accepted Manuscript published: September 6, 2017 (version 1)
- Version of Record published: September 21, 2017 (version 2)
Copyright
© 2017, Tavares et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Notch/Her12 signalling modulates motile/immotile cilia ratio downstream of Foxj1a in zebrafish left-right organizer
eLife 6:e25165.
https://doi.org/10.7554/eLife.25165
Further reading
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- Developmental Biology
Large-scale cell flow characterizes gastrulation in animal development. In amniote gastrulation, particularly in avian gastrula, a bilateral vortex-like counter-rotating cell flow, called ‘polonaise movements’, appears along the midline. Here, through experimental manipulations, we addressed relationships between the polonaise movements and morphogenesis of the primitive streak, the earliest midline structure in amniotes. Suppression of the Wnt/planar cell polarity (PCP) signaling pathway maintains the polonaise movements along a deformed primitive streak. Mitotic arrest leads to diminished extension and development of the primitive streak and maintains the early phase of the polonaise movements. Ectopically induced Vg1, an axis-inducing morphogen, generates the polonaise movements, aligned to the induced midline, but disturbs the stereotypical cell flow pattern at the authentic midline. Despite the altered cell flow, induction and extension of the primitive streak are preserved along both authentic and induced midlines. Finally, we show that ectopic axis-inducing morphogen, Vg1, is capable of initiating the polonaise movements without concomitant PS extension under mitotic arrest conditions. These results are consistent with a model wherein primitive streak morphogenesis is required for the maintenance of the polonaise movements, but the polonaise movements are not necessarily responsible for primitive streak morphogenesis. Our data describe a previously undefined relationship between the large-scale cell flow and midline morphogenesis in gastrulation.
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- Developmental Biology
- Physics of Living Systems
Geometric criteria can be used to assess whether cell intercalation is active or passive during the convergent extension of tissue.
