Symmetry breaking during morphogenesis of a mechanosensory organ

Actively regulated symmetry breaking, which is ubiquitous in biological cells, underlies phenomena such as directed cellular movement and morphological polarization. Here we investigate how an organ-level polarity pattern emerges through symmetry breaking at the cellular level during the formation of a mechanosensory organ. Combining theory, genetic perturbations, and in vivo imaging assisted by deep learning, we study the development and regeneration of the fluid-motion sensors in the zebrafish’s lateral line. We find that two interacting symmetry-breaking events — one mediated by biochemical signaling and the other by cellular mechanics — give rise to a novel form of collective cell migration, which produces a mirror-symmetric polarity pattern in the receptor organ.

• Publication year

  2019

• Venue

  bioRxiv

• Publication date

  2019-07-30

• Fields of study

  Biology, Physics

• Identifiers
  DOI 10.1101/718502
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar

• No claims are published for this paper.

• No concepts are published for this paper.

• Live cell-lineage tracing and machine learning reveal patterns of organ regeneration

  2018cited by this paper
• Notch-Mediated Polarity Decisions in Mechanosensory Hair Cells

  2018influential reference
• Connectomics of the zebrafish's lateral-line neuromast reveals wiring and miswiring in a simple microcircuit

  2018cited by this paper
• Physical control of tissue morphogenesis across scales.

  2018cited by this paper
• Content-aware image restoration: pushing the limits of fluorescence microscopy

  2018cited by this paper
• Guiding self-organized pattern formation in cell polarity establishment

  2018cited by this paper
• Genetic evidence that Nkx2.2 acts primarily downstream of Neurog3 in pancreatic endocrine lineage development

  2017cited by this paper
• Transcription factor Emx2 controls stereociliary bundle orientation of sensory hair cells

  2017cited by this paper
• Self-organized Notch dynamics generate stereotyped sensory organ patterns in Drosophila

  2017cited by this paper
• Planar cell polarity: global inputs establishing cellular asymmetry.

  2017cited by this paper
• Asymmetric division of contractile domains couples cell positioning and fate specification

  2016cited by this paper
• Author response: Ventromedial hypothalamic neurons control a defensive emotion state

  2015cited by this paper
• Cortical Contractility Triggers a Stochastic Switch to Fast Amoeboid Cell Motility

  2015cited by this paper
• Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing

  2015cited by this paper
• Cellular projections from sensory hair cells form polarity-specific scaffolds during synaptogenesis

  2015cited by this paper
• Inexhaustible hair-cell regeneration in young and aged zebrafish

  2015cited by this paper
• Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells.

  2015cited by this paper
• Aberrant cochlear hair cell attachments caused by Nectin-3 deficiency result in hair bundle abnormalities

  2014cited by this paper
• The physics of hearing: fluid mechanics and the active process of the inner ear

  2014cited by this paper
• A Morphological Approach to Curvature-Based Evolution of Curves and Surfaces

  2014cited by this paper
• A balance of form and function: planar polarity and development of the vestibular maculae.

  2013cited by this paper
• Dispersal of grouper larvae drives local resource sharing in a coral reef fishery.

  2013cited by this paper
• Forces in tissue morphogenesis and patterning.

  2013cited by this paper
• Three Functions of Cadherins in Cell Adhesion

  2013cited by this paper
• Cell mechanics control rapid transitions between blebs and lamellipodia during migration

  2012cited by this paper
• Rearrangements between differentiating hair cells coordinate planar polarity and the establishment of mirror symmetry in lateral-line neuromasts

  2012cited by this paper
• Kinocilia mediate mechanosensitivity in developing zebrafish hair cells.

  2012cited by this paper
• Adhesion Functions in Cell Sorting by Mechanically Coupling the Cortices of Adhering Cells

  2012cited by this paper
• Planar cell polarity and the developmental control of cell behavior in vertebrate embryos.

  2012cited by this paper
• Nectins Establish a Checkerboard-Like Cellular Pattern in the Auditory Epithelium

  2011cited by this paper
• Cell flow and tissue polarity patterns.

  2011cited by this paper
• Compartmentalized Notch signaling sustains epithelial mirror symmetry

  2011cited by this paper
• Spontaneous contractility-mediated cortical flow generates cell migration in three-dimensional environments.

  2010cited by this paper
• The Origins of Lactase Persistence in Europe

  2009cited by this paper
• Asymmetric localisation of planar polarity proteins: Mechanisms and consequences.

  2009cited by this paper
• Order and Stochastic Dynamics in Drosophila Planar Cell Polarity

  2009cited by this paper
• Notch Signaling Regulates the Extent of Hair Cell Regeneration in the Zebrafish Lateral Line

  2008cited by this paper
• Active behavior of the Cytoskeleton

  2007cited by this paper
• Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis

  2007cited by this paper
• Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line.

  2006cited by this paper
• A two-step mechanism underlies the planar polarization of regenerating sensory hair cells

  2006cited by this paper
• Capillarity and Wetting Phenomena

  2004cited by this paper
• Development of the zebrafish lateral line.

  2004cited by this paper
• Zebrafish deadly seven functions in neurogenesis.

  2001cited by this paper
• Use of the Gal4-UAS technique for targeted gene expression in the zebrafish.

  1999cited by this paper
• A pyramid approach to subpixel registration based on intensity

  1998cited by this paper
• Stages of embryonic development of the zebrafish

  1995cited by this paper
• Motions of droplets on solid surfaces induced by chemical or thermal gradients

  1989cited by this paper
• Wetting: statics and dynamics

  1985cited by this paper
• DIRECTIONAL SENSITIVITY OF INDIVIDUAL VERTEBRATE HAIR CELLS TO CONTROLLED DEFLECTION OF THEIR HAIR BUNDLES *

  1981cited by this paper

• Notch-Mediated Determination of Hair-Bundle Polarity in Mechanosensory Hair Cells of the Zebrafish Lateral Line.

  2019cites this paper