Linear Z-line-like alignment of capping protein in obliquely striated muscle of the nematode <i>C. elegans</i> suggests that dense bodies are not equivalent to Z-lines

Many invertebrates have obliquely striated muscles, in which neighboring thin and thick filaments are staggered and aligned obliquely. This type of muscle allows force production over a wide range of lengths and is beneficial for soft-bodied animals. Unlike vertebrate cross-striated muscles, most of the obliquely striated muscles lack distinct Z-lines and, instead, have dense bodies. Because the dense bodies are located in the middle of the I-bands and contain α-actinin, the dogma is that dense bodies are equivalent to the Z-lines anchoring the actin barbed ends. However, we show that the barbed ends of sarcomeric actin filaments in the nematode <i>Caenorhabditis elegans</i> body wall muscle are aligned linearly without converging at the dense bodies. Colocalization of F-actin and ATN-1/α-actinin was negatively correlated. CAP-1, an α-subunit of capping protein/CapZ, was linearly aligned without concentration at the dense bodies independently of ATN-1. Depletion of the capping protein subunit, CAP-1 or CAP-2, caused embryonic or larval lethality with severe actin disorganization in muscle, indicating that barbed-end regulation by capping protein is essential for sarcomere assembly. These results contradict the current view of the sarcomere organization in <i>C. elegans</i> muscle and suggest a new model of a linear Z-line-like arrangement of actin barbed ends.

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Publication Details

Journal
Molecular Biology of the Cell
Published
2026-03-04
DOI
https://doi.org/10.1091/mbc.e25-11-0569
Primary Topic
Cardiomyopathy and Myosin Studies
Type
article
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article

Linear Z-line-like alignment of capping protein in obliquely striated muscle of the nematode C. elegans suggests that dense bodies are not equivalent to Z-lines

Shoichiro Ono, Kanako Ono, Kennosuke Kurimaru, Emily Nickoloff-Bybel
Molecular Biology of the Cell
Cardiomyopathy and Myosin Studies
article

Linear Z-line-like alignment of capping protein in obliquely striated muscle of the nematode C. elegans suggests that dense bodies are not equivalent to Z-lines

Shoichiro Ono, Kanako Ono, Kennosuke Kurimaru, Emily Nickoloff-Bybel
article en

Abstract

Many invertebrates have obliquely striated muscles, in which neighboring thin and thick filaments are staggered and aligned obliquely. This type of muscle allows force production over a wide range of lengths and is beneficial for soft-bodied animals. Unlike vertebrate cross-striated muscles, most of the obliquely striated muscles lack distinct Z-lines and, instead, have dense bodies. Because the dense bodies are located in the middle of the I-bands and contain α-actinin, the dogma is that dense bodies are equivalent to the Z-lines anchoring the actin barbed ends. However, we show that the barbed ends of sarcomeric actin filaments in the nematode <i>Caenorhabditis elegans</i> body wall muscle are aligned linearly without converging at the dense bodies. Colocalization of F-actin and ATN-1/α-actinin was negatively correlated. CAP-1, an α-subunit of capping protein/CapZ, was linearly aligned without concentration at the dense bodies independently of ATN-1. Depletion of the capping protein subunit, CAP-1 or CAP-2, caused embryonic or larval lethality with severe actin disorganization in muscle, indicating that barbed-end regulation by capping protein is essential for sarcomere assembly. These results contradict the current view of the sarcomere organization in <i>C. elegans</i> muscle and suggest a new model of a linear Z-line-like arrangement of actin barbed ends.

Molecular Biology of the CellVol. 37(4)
Emory University (US)
Openalex Percentile: Top 41%
Cardiomyopathy and Myosin Studies
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