Abstract

Organisms generate shapes across size scales. Whereas patterning and morphogenesis of macroscopic tissues has been extensively studied, the principles underlying the formation of micrometric and submicrometric structures remain largely enigmatic. Individual cells of polychaete annelids, so-called chaetoblasts, are associated with the generation of chitinous bristles of highly stereotypic geometry. Here we show that bristle formation requires a chitin-producing enzyme specifically expressed in the chaetoblasts. Chaetoblasts exhibit dynamic cell surfaces with stereotypical patterns of actin-rich microvilli. These microvilli can be matched with internal and external structures of bristles reconstructed from serial block-face electron micrographs. Individual chitin teeth are deposited by microvilli in an extension-disassembly cycle resembling a biological 3D printer. Consistently, pharmacological interference with actin dynamics leads to defects in tooth formation. Our study reveals that both material and shape of bristles are encoded by the same cell, and that microvilli play a role in micro- to submicrometric sculpting of biomaterials.

Bristleworms possess dedicated cells that can synthesize highly stereotypical bristles with sub-micrometric precision. Here, Ikeda and colleagues shed light on the underlying dynamics of cellular protrusions, revealing an extension-disassembly cycle that resembles a 3D printer.

Details

Title
Dynamic microvilli sculpt bristles at nanometric scale
Author
Ikeda, Kyojiro N. 1   VIAFID ORCID Logo  ; Belevich, Ilya 2   VIAFID ORCID Logo  ; Zelaya-Lainez, Luis 3 ; Orel, Lukas 1   VIAFID ORCID Logo  ; Füssl, Josef 3 ; Gumulec, Jaromír 4   VIAFID ORCID Logo  ; Hellmich, Christian 3 ; Jokitalo, Eija 2   VIAFID ORCID Logo  ; Raible, Florian 5   VIAFID ORCID Logo 

 Max Perutz Labs; University of Vienna, Vienna, Austria (GRID:grid.465536.7) (ISNI:0000 0000 9805 9959) 
 University of Helsinki, Institute of Biotechnology, Helsinki Institute of Life Science, Helsinki, Finland (GRID:grid.7737.4) (ISNI:0000 0004 0410 2071) 
 TU Wien-Vienna University of Technology, Institute for Mechanics of Materials and Structures, Vienna, Austria (GRID:grid.5329.d) (ISNI:0000 0004 1937 0669) 
 Masaryk University, Department of Pathophysiology, Faculty of Medicine, Brno, Czech Republic (GRID:grid.10267.32) (ISNI:0000 0001 2194 0956) 
 Max Perutz Labs; University of Vienna, Vienna, Austria (GRID:grid.465536.7) (ISNI:0000 0000 9805 9959); University of Vienna, Research Platform “Single-Cell Regulation of Stem Cells”, Vienna, Austria (GRID:grid.10420.37) (ISNI:0000 0001 2286 1424) 
Pages
3733
Publication year
2024
Publication date
2024
Publisher
Nature Publishing Group
e-ISSN
20411723
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
3054303454
Copyright
© The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.