The BEN domain protein LIN-14 coordinates neuromuscular positioning during epidermal maturation

Development and function of an organism depend on coordinated inter-tissue interaction. How such interactions are maintained during tissue renewal and reorganization remains poorly understood. Here, we find that <i>Caenorhabditis elegans</i> BEN domain transcription factor LIN-14 is required in epidermis for maintaining the position of motor neurons and muscles during developmental tissue reorganization. <i>lin-14</i> loss of function <i>(lf)</i> mutants display highly penetrant ventral neuromuscular mispositioning. These defects arise post-embryonically during first larval (L1) stage as the maturing epidermis replaces the embryonic ventral epidermis. Tissue-specific and temporally controlled depletion experiments indicate LIN-14 acts within the epidermis for ventral neuromuscular positioning. <i>lin-14(lf)</i> mutants show defects in formation of epidermis-muscle attachment complex hemidesmosomes in the maturing ventral epidermis, leading to detachment of muscles and motor neurons as well as movement defects. Our findings reveal a cell non-autonomous role for LIN-14 in coordinating inter-tissue interaction and neuromuscular positioning during epidermal maturation.

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Journal
iScience
Published
2024-12-12
DOI
https://doi.org/10.1016/j.isci.2024.111577
Primary Topic
Hereditary Neurological Disorders
Type
article
Field-Weighted Citation Impact
0.00

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article

The BEN domain protein LIN-14 coordinates neuromuscular positioning during epidermal maturation

Andrew D. Chisholm, Yishi Jin, Yingchuan Qi, Eugene Jennifer Jin
iScience
Hereditary Neurological Disorders
article

The BEN domain protein LIN-14 coordinates neuromuscular positioning during epidermal maturation

Andrew D. Chisholm, Yishi Jin, Yingchuan Qi, Eugene Jennifer Jin
article en

Abstract

Development and function of an organism depend on coordinated inter-tissue interaction. How such interactions are maintained during tissue renewal and reorganization remains poorly understood. Here, we find that <i>Caenorhabditis elegans</i> BEN domain transcription factor LIN-14 is required in epidermis for maintaining the position of motor neurons and muscles during developmental tissue reorganization. <i>lin-14</i> loss of function <i>(lf)</i> mutants display highly penetrant ventral neuromuscular mispositioning. These defects arise post-embryonically during first larval (L1) stage as the maturing epidermis replaces the embryonic ventral epidermis. Tissue-specific and temporally controlled depletion experiments indicate LIN-14 acts within the epidermis for ventral neuromuscular positioning. <i>lin-14(lf)</i> mutants show defects in formation of epidermis-muscle attachment complex hemidesmosomes in the maturing ventral epidermis, leading to detachment of muscles and motor neurons as well as movement defects. Our findings reveal a cell non-autonomous role for LIN-14 in coordinating inter-tissue interaction and neuromuscular positioning during epidermal maturation.

iScienceVol. 28(1)
ShanghaiTech University (CN), University of California San Diego (US)
A.P. Giannini Foundation, Giannini Foundation of Agricultural Economics, National Institutes of Health, University of California, San Diego
Zero hunger
Openalex Percentile: Top 75%
Hereditary Neurological Disorders
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