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Contractile forces regulate cell division in three-dimensional environments

Lesman, Ayelet and Notbohm, Jacob and Tirrell, David A. and Ravichandran, Guruswami (2014) Contractile forces regulate cell division in three-dimensional environments. Journal of Cell Biology, 205 (2). pp. 155-162. ISSN 0021-9525. PMCID PMC4003238. http://resolver.caltech.edu/CaltechAUTHORS:20140604-075231845

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[img] Video (MPEG) (Video 1. Maximum intensity projections of a 3D image of a 3T3 fibroblast (expressing actin-GFP, shown in Fig. 1) before, during, and after division in a 3D fibrin matrix. ) - Supplemental Material
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[img] Video (MPEG) (Video 2. Representative maximum intensity projections of dividing cells embedded in 3D fibrin matrices (3T3 actin-GFP fibroblast cells). ) - Supplemental Material
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[img] Video (MPEG) (Video 3. Representative maximum intensity projections of dividing 3T3 fibroblast cells stably expressing LifeAct-mRuby.) - Supplemental Material
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[img] Video (MPEG) (Video 4. Maximum intensity projections of a 3T3 actin-GFP cell dividing on an uncoated glass substrate (on the left) or on top of a thick (∼200 µm) fibrin gel (on the right), collected with a confocal microscope (Swept Field; Nikon) every 5 min for 150 mi) - Supplemental Material
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[img] Video (MPEG) (Video 5. Examples of dividing 3T3 fibroblast cells (labeled with actin-GFP) embedded in 3D fibrin matrices in the presence of blebbistatin (50 µM).) - Supplemental Material
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[img] Video (MPEG) (Video 6. 3D maximum intensity projection of fluorescent particles (red; Invitrogen) surrounding a 3T3 dividing fibroblast cell (actin-GFP, green). ) - Supplemental Material
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[img] Video (MPEG) (Video 7. Vector plots of matrix displacements and 3D isosurface renderings of a 3T3 fibroblast cell during and after division.) - Supplemental Material
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[img] Video (MPEG) (Video 8. Multi-angle view of Fig. 3 C, t = 0, showing vector plots of matrix displacements during mitotic rounding of a 3T3 fibroblast cell labeled with GFP-actin. ) - Supplemental Material
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[img] Video (MPEG) (Video 9. Multi-angle view of Fig. 3 C, t = 210 min, showing vector plots of matrix displacements around spreading 3T3 fibroblast daughter cells labeled with GFP-actin.) - Supplemental Material
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[img] Video (MPEG) (Video 10. Time-lapse series of a single confocal plane of a 3T3 dividing fibroblast cell (actin-GFP, green) embedded in a fibrin matrix (labeled with Alexa Fluor 546, gray).) - Supplemental Material
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Abstract

Physical forces direct the orientation of the cell division axis for cells cultured on rigid, two-dimensional (2D) substrates. The extent to which physical forces regulate cell division in three-dimensional (3D) environments is not known. Here, we combine live-cell imaging with digital volume correlation to map 3D matrix displacements and identify sites at which cells apply contractile force to the matrix as they divide. Dividing cells embedded in fibrous matrices remained anchored to the matrix by long, thin protrusions. During cell rounding, the cells released adhesive contacts near the cell body while applying tensile forces at the tips of the protrusions to direct the orientation of the cell division axis. After cytokinesis, the daughter cells respread into matrix voids and invaded the matrix while maintaining traction forces at the tips of persistent and newly formed protrusions. Mechanical interactions between cells and the extracellular matrix constitute an important mechanism for regulation of cell division in 3D environments.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1083/jcb.201309029DOIArticle
http://jcb.rupress.org/content/205/2/155PublisherArticle
http://jcb.rupress.org/content/205/2/155/suppl/DC1Related ItemSupplemental Material
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4003238/PubMed CentralArticle
ORCID:
AuthorORCID
Tirrell, David A.0000-0003-3175-4596
Additional Information:© 2014 Lesman et al. 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 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/). Submitted: 6 September 2013 Accepted: 25 March 2014. We thank Scott Fraser for providing the transfected fibroblasts. We thank the Biological Imaging Center at Caltech for use of the two-photon microscope. This research was supported by grants from the National Science Foundation (Division of Materials Research No. 0520565 and 1206121). J. Notbohm was supported by the Department of Defense through the National Defense Science and Engineering Graduate Fellowship Program. A. Lesman was supported in part by the Rothschild fellowship foundation. The authors declare no competing financial interests.
Group:GALCIT
Funders:
Funding AgencyGrant Number
NSFDMR-0520565
NSFDMR-1206121
National Defense Science and Engineering Graduate (NDSEG) FellowshipUNSPECIFIED
Rothschild FoundationUNSPECIFIED
PubMed Central ID:PMC4003238
Record Number:CaltechAUTHORS:20140604-075231845
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20140604-075231845
Official Citation:Contractile forces regulate cell division in three-dimensional environments Ayelet Lesman, Jacob Notbohm, David A. Tirrell, and Guruswami Ravichandran J Cell Biol 2014 205:155-162. Published April 28, 2014, doi:10.1083/jcb.201309029
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:46067
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:04 Jun 2014 22:24
Last Modified:21 Jul 2017 22:04

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