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Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps

Cell emergence onto damaged or organized fibrous extracellular matrix (ECM) is a crucial precursor to collective cell migration in wound closure and cancer metastasis, respectively. However, there is a fundamental gap in our quantitative understanding of the role of local ECM size and arrangement in...

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Autores principales: Sharma, Puja, Ng, Colin, Jana, Aniket, Padhi, Abinash, Szymanski, Paige, Lee, Jerry S. H., Behkam, Bahareh, Nain, Amrinder S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5597329/
https://www.ncbi.nlm.nih.gov/pubmed/28747440
http://dx.doi.org/10.1091/mbc.E17-05-0305
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author Sharma, Puja
Ng, Colin
Jana, Aniket
Padhi, Abinash
Szymanski, Paige
Lee, Jerry S. H.
Behkam, Bahareh
Nain, Amrinder S.
author_facet Sharma, Puja
Ng, Colin
Jana, Aniket
Padhi, Abinash
Szymanski, Paige
Lee, Jerry S. H.
Behkam, Bahareh
Nain, Amrinder S.
author_sort Sharma, Puja
collection PubMed
description Cell emergence onto damaged or organized fibrous extracellular matrix (ECM) is a crucial precursor to collective cell migration in wound closure and cancer metastasis, respectively. However, there is a fundamental gap in our quantitative understanding of the role of local ECM size and arrangement in cell emergence–based migration and local gap closure. Here, using ECM-mimicking nanofibers bridging cell monolayers, we describe a method to recapitulate and quantitatively describe these in vivo behaviors over multispatial (single cell to cell sheets) and temporal (minutes to weeks) scales. On fiber arrays with large interfiber spacing, cells emerge (invade) either singularly by breaking cell–cell junctions analogous to release of a stretched rubber band (recoil), or in groups of few cells (chains), whereas on closely spaced fibers, multiple chains emerge collectively. Advancing cells on fibers form cell streams, which support suspended cell sheets (SCS) of various sizes and curvatures. SCS converge to form local gaps that close based on both the gap size and shape. We document that cell stream spacing of 375 µm and larger hinders SCS advancement, thus providing abilities to engineer closing and nonclosing gaps. Altogether we highlight the importance of studying cell-fiber interactions and matrix structural remodeling in fundamental and translational cell biology.
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spelling pubmed-55973292017-11-30 Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps Sharma, Puja Ng, Colin Jana, Aniket Padhi, Abinash Szymanski, Paige Lee, Jerry S. H. Behkam, Bahareh Nain, Amrinder S. Mol Biol Cell Articles Cell emergence onto damaged or organized fibrous extracellular matrix (ECM) is a crucial precursor to collective cell migration in wound closure and cancer metastasis, respectively. However, there is a fundamental gap in our quantitative understanding of the role of local ECM size and arrangement in cell emergence–based migration and local gap closure. Here, using ECM-mimicking nanofibers bridging cell monolayers, we describe a method to recapitulate and quantitatively describe these in vivo behaviors over multispatial (single cell to cell sheets) and temporal (minutes to weeks) scales. On fiber arrays with large interfiber spacing, cells emerge (invade) either singularly by breaking cell–cell junctions analogous to release of a stretched rubber band (recoil), or in groups of few cells (chains), whereas on closely spaced fibers, multiple chains emerge collectively. Advancing cells on fibers form cell streams, which support suspended cell sheets (SCS) of various sizes and curvatures. SCS converge to form local gaps that close based on both the gap size and shape. We document that cell stream spacing of 375 µm and larger hinders SCS advancement, thus providing abilities to engineer closing and nonclosing gaps. Altogether we highlight the importance of studying cell-fiber interactions and matrix structural remodeling in fundamental and translational cell biology. The American Society for Cell Biology 2017-09-15 /pmc/articles/PMC5597329/ /pubmed/28747440 http://dx.doi.org/10.1091/mbc.E17-05-0305 Text en © 2017 Sharma 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 for Cell Biology.
spellingShingle Articles
Sharma, Puja
Ng, Colin
Jana, Aniket
Padhi, Abinash
Szymanski, Paige
Lee, Jerry S. H.
Behkam, Bahareh
Nain, Amrinder S.
Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps
title Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps
title_full Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps
title_fullStr Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps
title_full_unstemmed Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps
title_short Aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps
title_sort aligned fibers direct collective cell migration to engineer closing and nonclosing wound gaps
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5597329/
https://www.ncbi.nlm.nih.gov/pubmed/28747440
http://dx.doi.org/10.1091/mbc.E17-05-0305
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