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Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells

Intestinal epithelial cells have unique apical membrane structures, known as microvilli, that contain bundles of actin microfilaments. In this study, we report that Caenorhabditis elegans cytosolic chaperonin containing TCP-1 (CCT) is essential for proper formation of microvilli in intestinal cells....

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Autores principales: Saegusa, Keiko, Sato, Miyuki, Sato, Katsuya, Nakajima-Shimada, Junko, Harada, Akihiro, Sato, Ken
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4196862/
https://www.ncbi.nlm.nih.gov/pubmed/25143409
http://dx.doi.org/10.1091/mbc.E13-09-0530
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author Saegusa, Keiko
Sato, Miyuki
Sato, Katsuya
Nakajima-Shimada, Junko
Harada, Akihiro
Sato, Ken
author_facet Saegusa, Keiko
Sato, Miyuki
Sato, Katsuya
Nakajima-Shimada, Junko
Harada, Akihiro
Sato, Ken
author_sort Saegusa, Keiko
collection PubMed
description Intestinal epithelial cells have unique apical membrane structures, known as microvilli, that contain bundles of actin microfilaments. In this study, we report that Caenorhabditis elegans cytosolic chaperonin containing TCP-1 (CCT) is essential for proper formation of microvilli in intestinal cells. In intestinal cells of cct-5(RNAi) animals, a substantial amount of actin is lost from the apical area, forming large aggregates in the cytoplasm, and the apical membrane is deformed into abnormal, bubble-like structures. The length of the intestinal microvilli is decreased in these animals. However, the overall actin protein levels remain relatively unchanged when CCT is depleted. We also found that CCT depletion causes a reduction in the tubulin levels and disorganization of the microtubule network. In contrast, the stability and localization of intermediate filament protein IFB-2, which forms a dense filamentous network underneath the apical surface, appears to be superficially normal in CCT-deficient cells, suggesting substrate specificity of CCT in the folding of filamentous cytoskeletons in vivo. Our findings demonstrate physiological functions of CCT in epithelial cell morphogenesis using whole animals.
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spelling pubmed-41968622014-12-30 Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells Saegusa, Keiko Sato, Miyuki Sato, Katsuya Nakajima-Shimada, Junko Harada, Akihiro Sato, Ken Mol Biol Cell Articles Intestinal epithelial cells have unique apical membrane structures, known as microvilli, that contain bundles of actin microfilaments. In this study, we report that Caenorhabditis elegans cytosolic chaperonin containing TCP-1 (CCT) is essential for proper formation of microvilli in intestinal cells. In intestinal cells of cct-5(RNAi) animals, a substantial amount of actin is lost from the apical area, forming large aggregates in the cytoplasm, and the apical membrane is deformed into abnormal, bubble-like structures. The length of the intestinal microvilli is decreased in these animals. However, the overall actin protein levels remain relatively unchanged when CCT is depleted. We also found that CCT depletion causes a reduction in the tubulin levels and disorganization of the microtubule network. In contrast, the stability and localization of intermediate filament protein IFB-2, which forms a dense filamentous network underneath the apical surface, appears to be superficially normal in CCT-deficient cells, suggesting substrate specificity of CCT in the folding of filamentous cytoskeletons in vivo. Our findings demonstrate physiological functions of CCT in epithelial cell morphogenesis using whole animals. The American Society for Cell Biology 2014-10-15 /pmc/articles/PMC4196862/ /pubmed/25143409 http://dx.doi.org/10.1091/mbc.E13-09-0530 Text en © 2014 Saegusa, Sato, et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Saegusa, Keiko
Sato, Miyuki
Sato, Katsuya
Nakajima-Shimada, Junko
Harada, Akihiro
Sato, Ken
Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells
title Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells
title_full Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells
title_fullStr Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells
title_full_unstemmed Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells
title_short Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells
title_sort caenorhabditis elegans chaperonin cct/tric is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4196862/
https://www.ncbi.nlm.nih.gov/pubmed/25143409
http://dx.doi.org/10.1091/mbc.E13-09-0530
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