Cadherin preserves cohesion across involuting tissues during C. elegans neurulation

Author:

Barnes Kristopher M12ORCID,Fan Li1ORCID,Moyle Mark W3,Brittin Christopher A1ORCID,Xu Yichi1,Colón-Ramos Daniel A34ORCID,Santella Anthony15,Bao Zhirong1ORCID

Affiliation:

1. Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York, United States

2. Graduate Program in Neuroscience, Weill Cornell Medicine, New York, United States

3. Department of Neuroscience and Department of Cell Biology, Yale University School of Medicine, New Haven, United States

4. Instituto de Neurobiología, Recinto de Ciencias Médicas, Universidad de Puerto Rico, San Juan, United States

5. Molecular Cytology Core, Memorial Sloan Kettering Cancer Center, New York, United States

Abstract

The internalization of the central nervous system, termed neurulation in vertebrates, is a critical step in embryogenesis. Open questions remain regarding how force propels coordinated tissue movement during the process, and little is known as to how internalization happens in invertebrates. We show that inC. elegansmorphogenesis, apical constriction in the retracting pharynx drives involution of the adjacent neuroectoderm. HMR-1/cadherin mediates this process via inter-tissue attachment, as well as cohesion within the neuroectoderm. Our results demonstrate that HMR-1 is capable of mediating embryo-wide reorganization driven by a centrally located force generator, and indicate a non-canonical use of cadherin on the basal side of an epithelium that may apply to vertebrate neurulation. Additionally, we highlight shared morphology and gene expression in tissues driving involution, which suggests that neuroectoderm involution inC. elegansis potentially homologous with vertebrate neurulation and thus may help elucidate the evolutionary origin of the brain.

Funder

National Institute of General Medical Sciences

Office of the Director

National Cancer Institute

Chan Zuckerberg Initiative

Howard Hughes Medical Institute

National Institute of Neurological Disorders and Stroke

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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