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Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage

Basement membrane (BM) matrices surround and separate most tissues. However, through poorly understood mechanisms, BMs of adjacent tissue can also stably link to support organ structure and function. Using endogenous knock-in fluorescent proteins, conditional RNAi, optogenetics, and quantitative liv...

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Autores principales: Gianakas, Claire A., Keeley, Daniel P., Ramos-Lewis, William, Park, Kieop, Jayadev, Ranjay, Kenny, Isabel W., Chi, Qiuyi, Sherwood, David R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9597354/
https://www.ncbi.nlm.nih.gov/pubmed/36282214
http://dx.doi.org/10.1083/jcb.202112096
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author Gianakas, Claire A.
Keeley, Daniel P.
Ramos-Lewis, William
Park, Kieop
Jayadev, Ranjay
Kenny, Isabel W.
Chi, Qiuyi
Sherwood, David R.
author_facet Gianakas, Claire A.
Keeley, Daniel P.
Ramos-Lewis, William
Park, Kieop
Jayadev, Ranjay
Kenny, Isabel W.
Chi, Qiuyi
Sherwood, David R.
author_sort Gianakas, Claire A.
collection PubMed
description Basement membrane (BM) matrices surround and separate most tissues. However, through poorly understood mechanisms, BMs of adjacent tissue can also stably link to support organ structure and function. Using endogenous knock-in fluorescent proteins, conditional RNAi, optogenetics, and quantitative live imaging, we identified extracellular matrix proteins mediating a BM linkage (B-LINK) between the uterine utse and epidermal seam cell BMs in Caenorhabditis elegans that supports the uterus during egg-laying. We found that hemicentin is secreted by the utse and promotes fibulin-1 assembly to jointly initiate the B-LINK. During egg-laying, however, both proteins’ levels decline and are not required for B-LINK maintenance. Instead, we discovered that hemicentin recruits ADAMTS9/20, which facilitates the assembly of high levels of type IV collagen that sustains the B-LINK during the mechanically active egg-laying period. This work reveals mechanisms underlying BM–BM linkage maturation and identifies a crucial function for hemicentin and fibulin-1 in initiating attachment and type IV collagen in strengthening this specialized form of tissue linkage.
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spelling pubmed-95973542023-04-25 Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage Gianakas, Claire A. Keeley, Daniel P. Ramos-Lewis, William Park, Kieop Jayadev, Ranjay Kenny, Isabel W. Chi, Qiuyi Sherwood, David R. J Cell Biol Article Basement membrane (BM) matrices surround and separate most tissues. However, through poorly understood mechanisms, BMs of adjacent tissue can also stably link to support organ structure and function. Using endogenous knock-in fluorescent proteins, conditional RNAi, optogenetics, and quantitative live imaging, we identified extracellular matrix proteins mediating a BM linkage (B-LINK) between the uterine utse and epidermal seam cell BMs in Caenorhabditis elegans that supports the uterus during egg-laying. We found that hemicentin is secreted by the utse and promotes fibulin-1 assembly to jointly initiate the B-LINK. During egg-laying, however, both proteins’ levels decline and are not required for B-LINK maintenance. Instead, we discovered that hemicentin recruits ADAMTS9/20, which facilitates the assembly of high levels of type IV collagen that sustains the B-LINK during the mechanically active egg-laying period. This work reveals mechanisms underlying BM–BM linkage maturation and identifies a crucial function for hemicentin and fibulin-1 in initiating attachment and type IV collagen in strengthening this specialized form of tissue linkage. Rockefeller University Press 2022-10-25 /pmc/articles/PMC9597354/ /pubmed/36282214 http://dx.doi.org/10.1083/jcb.202112096 Text en © 2022 Gianakas et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Article
Gianakas, Claire A.
Keeley, Daniel P.
Ramos-Lewis, William
Park, Kieop
Jayadev, Ranjay
Kenny, Isabel W.
Chi, Qiuyi
Sherwood, David R.
Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage
title Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage
title_full Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage
title_fullStr Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage
title_full_unstemmed Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage
title_short Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage
title_sort hemicentin-mediated type iv collagen assembly strengthens juxtaposed basement membrane linkage
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9597354/
https://www.ncbi.nlm.nih.gov/pubmed/36282214
http://dx.doi.org/10.1083/jcb.202112096
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