Shootins mediate collective cell migration and organogenesis of the zebrafish posterior lateral line system

Urasaki, Akihiro; Morishita, Seiya; Naka, Kosuke; Uozumi, Minato; Abe, Kouki; Huang, Liguo; Watase, Emiko; Nakagawa, Osamu; Kawakami, Koichi; Matsui, Takaaki; Bessho, Yasumasa; Inagaki, Naoyuki

doi:10.1038/s41598-019-48585-4

Cited by 5 publications

(2 citation statements)

References 59 publications

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“…Recent studies have reported that the molecular clutch system involving shootin1a, cortactin, and L1 mediates axon guidance in response to the diffusible chemotactic ligand netrin-1 ( 34 ) and the substrate-bound haptotactic ligand laminin ( 31 ). The clutch molecule shootin1 is also involved in the generation of force for neuronal migration ( 77 , 78 ) and required for axon pathfinding and cell migration in vivo in three-dimensional environments ( 34 , 77 , 79 ). Netrin-1 signals promote Pak1-mediated shootin1a phosphorylation in axonal growth cones under the activation of Cdc42 and Rac1 ( 12 ).…”

Section: Discussionmentioning

confidence: 99%

Mechanosensitive axon outgrowth mediated by L1-laminin clutch interface

Abe

Baba

Huang

et al. 2021

Biophysical Journal

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Mechanical properties of the extracellular environment modulate axon outgrowth. Growth cones at the tip of extending axons generate traction force for axon outgrowth by transmitting the force of actin filament retrograde flow, produced by actomyosin contraction and F-actin polymerization, to adhesive substrates through clutch and cell adhesion molecules. A molecular clutch between the actin filament flow and substrate is proposed to contribute to cellular mechanosensing. However, the molecular identity of the clutch interface responsible for mechanosensitive growth cone advance is unknown. We previously reported that mechanical coupling between actin filament retrograde flow and adhesive substrates through the clutch molecule shootin1a and the cell adhesion molecule L1 generates traction force for axon outgrowth and guidance. Here, we show that cultured mouse hippocampal neurons extend longer axons on stiffer substrates under elastic conditions that correspond to the soft brain environments. We demonstrate that this stiffness-dependent axon outgrowth requires actin-adhesion coupling mediated by shootin1a, L1, and laminin on the substrate. Speckle imaging analyses showed that L1 at the growth cone membrane switches between two adhesive states: L1 that is immobilized and that undergoes retrograde movement on the substrate. The duration of the immobilized phase was longer on stiffer substrates; this was accompanied by increases in actin-adhesion coupling and in the traction force exerted on the substrate. These data suggest that the interaction between L1 and laminin is enhanced on stiffer substrates, thereby promoting force generation for axon outgrowth.

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Section: Discussionmentioning

confidence: 99%

Mechanosensitive axon outgrowth mediated by L1-laminin clutch interface

Abe

Baba

Huang

et al. 2021

Biophysical Journal

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“…In addition, shootin1 KO results in ectopic accumulation of mitral cells ( Minegishi et al, 2018 ), olfactory excitatory neurons that undergo radial migration ( Hinds, 1968 ; Blanchart et al, 2006 ). Recent studies also reported that shootin1 knockdown inhibits the radial migration of cortical neurons ( Sapir et al, 2013 ) and that shootin1 KO delays the collective cell migration of zebrafish posterior lateral line primordium (PLLP), a cluster of progenitor cells destined to form a mechanosensory organ called the neuromast ( Urasaki et al, 2019 ). These data suggest that traction force generated by shootin1-mediated actin–adhesion coupling may propel the migration of multiple types of neurons.…”

Section: Forces For Leading Process Extensionmentioning

confidence: 99%

Forces to Drive Neuronal Migration Steps

Minegishi

Inagaki

2020

Front. Cell Dev. Biol.

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To establish and maintain proper brain architecture and elaborate neural networks, neurons undergo massive migration. As a unique feature of their migration, neurons move in a saltatory manner by repeating two distinct steps: extension of the leading process and translocation of the cell body. Neurons must therefore generate forces to extend the leading process as well as to translocate the cell body. In addition, neurons need to switch these forces alternately in order to orchestrate their saltatory movement. Recent studies with mechanobiological analyses, including traction force microscopy, cell detachment analyses, live-cell imaging, and loss-of-function analyses, have begun to reveal the forces required for these steps and the molecular mechanics underlying them. Spatiotemporally organized forces produced between cells and their extracellular environment, as well as forces produced within cells, play pivotal roles to drive these neuronal migration steps. Traction force produced by the leading process growth cone extends the leading processes. On the other hand, mechanical tension of the leading process, together with reduction in the adhesion force at the rear and the forces to drive nucleokinesis, translocates the cell body. Traction forces are generated by mechanical coupling between actin filament retrograde flow and the extracellular environment through clutch and adhesion molecules. Forces generated by actomyosin and dynein contribute to the nucleokinesis. In addition to the forces generated in cell-intrinsic manners, external forces provided by neighboring migratory cells coordinate cell movement during collective migration. Here, we review our current understanding of the forces that drive neuronal migration steps and describe the molecular machineries that generate these forces for neuronal migration.

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Research progress on the pathogenesis of CDKL5 pathogenic variants and related encephalopathy

Sun

Wang

2023

Eur J Pediatr

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Shootins mediate collective cell migration and organogenesis of the zebrafish posterior lateral line system

Cited by 5 publications

References 59 publications

Mechanosensitive axon outgrowth mediated by L1-laminin clutch interface

Mechanosensitive axon outgrowth mediated by L1-laminin clutch interface

Forces to Drive Neuronal Migration Steps

Research progress on the pathogenesis of CDKL5 pathogenic variants and related encephalopathy

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