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Macropinocytosis-mediated membrane recycling drives neural crest migration by delivering F-actin to the lamellipodium

Li, Yuwei and Gonzalez, Walter G. and Andreev, Andrey and Tang, Weiyi and Gandhi, Shashank and Cunha, Alexandre and Prober, David and Lois, Carlos and Bronner, Marianne E. (2020) Macropinocytosis-mediated membrane recycling drives neural crest migration by delivering F-actin to the lamellipodium. Proceedings of the National Academy of Sciences of the United States of America, 117 (44). pp. 27400-27411. ISSN 0027-8424. https://resolver.caltech.edu/CaltechAUTHORS:20201022-090820908

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[img] Video (AVI) (Movie S1. Neural Crest cells (Membrane-YFP) migrate with lamellipodial extension in the anterior and cell body retraction in the posterior) - Supplemental Material
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[img] Video (AVI) (Movie S2. Photo-conversion to show membrane flow in basal (left) and apical (right) region) - Supplemental Material
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[img] Video (AVI) (Movie S3. A segmented view of vesicle movement after computational motion correction) - Supplemental Material
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[img] Video (AVI) (Movie S4. Vesicles move along MTs) - Supplemental Material
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[img] Video (AVI) (Movie S5. Vesicle motion in cell body (left) and front (right)) - Supplemental Material
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[img] Video (AVI) (Movie S6. The dynamics of MTs) - Supplemental Material
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[img] Video (AVI) (Movie S7. Infrequent Phagocytosis) - Supplemental Material
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[img] Video (AVI) (Movie S8. The cellular process of non-canonical macropinocytosis (Membrane-YFP), during which the cell extends its protrusion and then retracts and degrades into vesicles (arrows)) - Supplemental Material
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[img] Video (AVI) (Movie S9. Dextran (red) is engulfed by the cell (Membrane-YFP, green), rapped by a vesicle (spot segmented) and transported to the front) - Supplemental Material
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[img] Video (AVI) (Movie S10. Type I Vesicles Transport F-actin) - Supplemental Material
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[img] Video (AVI) (Movie S11. As the lipid potion integrates into the membrane (Membrane-YFP, green), F-actin (Utrophin-scarlet, red) released from the same vesicle (arrows) merges with the actin brunches in the lamellipodium) - Supplemental Material
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[img] Video (AVI) (Movie S12. F-actin (Utrophin-scarlet, red) is enriched in the vesicle (Membrane-YFP, green) (left movie); in contrast, total actin (Actin-scarlet, red) (middle movie) and cortactin (Cortactin-scarlet, red) (right movie) is expressed in a low level ...) - Supplemental Material
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[img] Video (AVI) (Movie S13. During canonical macropinocytosis, the folding membrane (Membrane-YFP, green) is transiently bound by F-actin (Utrophin-scarlet, red)) - Supplemental Material
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[img] Video (AVI) (Movie S14. Photo-conversion on the nocodazole treated cells expressing Farnesylated-Dendra2 shows opposite directions of membrane flow in basal (left) and apical (right) region) - Supplemental Material
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[img] Video (AVI) (Movie S15. A migrating cell (Membrane-YFP) in the presence of nocodazole) - Supplemental Material
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[img] Video (AVI) (Movie S16. A segmented view of vesicle movement inside the nocodazole treated cell) - Supplemental Material
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[img] Video (AVI) (Movie S17. Bleb expansion (actin absence) and retraction (actin presence) in the Nocodazole treated cells (pointed by arrows)) - Supplemental Material
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[img] Video (AVI) (Movie S18. A migrating cell (Membrane-YFP, green) expressing DN-Rab11-2A-mCherry (Red)) - Supplemental Material
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Abstract

Individual cell migration requires front-to-back polarity manifested by lamellipodial extension. At present, it remains debated whether and how membrane motility mediates this cell morphological change. To gain insights into these processes, we perform live imaging and molecular perturbation of migrating chick neural crest cells in vivo. Our results reveal an endocytic loop formed by circular membrane flow and anterograde movement of lipid vesicles, resulting in cell polarization and locomotion. Rather than clathrin-mediated endocytosis, macropinosomes encapsulate F-actin in the cell body, forming vesicles that translocate via microtubules to deliver actin to the anterior. In addition to previously proposed local conversion of actin monomers to polymers, we demonstrate a surprising role for shuttling of F-actin across cells for lamellipodial expansion. Thus, the membrane and cytoskeleton act in concert in distinct subcellular compartments to drive forward cell migration.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2007229117DOIArticle
https://www.pnas.org/content/suppl/2020/10/21/2007229117.DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Li, Yuwei0000-0001-7753-4869
Gonzalez, Walter G.0000-0003-1310-9323
Andreev, Andrey0000-0002-7833-1390
Tang, Weiyi0000-0002-1279-1001
Gandhi, Shashank0000-0002-4081-4338
Cunha, Alexandre0000-0002-2541-6024
Prober, David0000-0002-7371-4675
Lois, Carlos0000-0002-7305-2317
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2020 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Contributed by Marianne E. Bronner, September 22, 2020 (sent for review June 8, 2020; reviewed by Angela Nieto and Tatjana Piotrowski) We thank Pierre Martineau for sharing reagents and Beckman Institute Biological Imaging Facility at Caltech for sharing equipment. We thank the Beckman Institute at Caltech for financial support to the Center for Advanced Methods in Biological Image Analysis (A.C.). W.G.G. is supported by the Della Martin Foundation, the American Heart Association, and the Burroughs Wellcome Fund. S.G. is supported by the American Heart Association. This project is supported by DE024157 and R35NS111564 (to M.E.B.). Data Availability. All study data are included in the article and supporting information. Author contributions: Y.L. and W.G.G. designed research; Y.L., W.T., and S.G. performed research; Y.L., W.G.G., and A.A. contributed new reagents/analytic tools; Y.L., W.G.G., A.A., A.C., D.P., and C.L. analyzed data; and Y.L., W.G.G., and M.E.B. wrote the paper. Reviewers: A.N., Instituto de Neurociencias de Alicante, Consejo Superior de Investigaciones Científicas–Universidad Miguel Hernández; and T.P., Stowers Institute for Medical Research. Competing interest statement: M.E.B. and A.N. are listed as coauthors on a 2020 Consensus Statement. They did not collaborate directly on the paper. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2007229117/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Caltech Beckman InstituteUNSPECIFIED
Della Martin FoundationUNSPECIFIED
American Heart AssociationUNSPECIFIED
Burroughs Wellcome FundUNSPECIFIED
NIHDE024157
NIHR35NS111564
Subject Keywords:membrane recycling | actin turnover | macropinocytosis | cell migration | neural crests
Issue or Number:44
Record Number:CaltechAUTHORS:20201022-090820908
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201022-090820908
Official Citation:Macropinocytosis-mediated membrane recycling drives neural crest migration by delivering F-actin to the lamellipodium. Yuwei Li, Walter G. Gonzalez, Andrey Andreev, Weiyi Tang, Shashank Gandhi, Alexandre Cunha, David Prober, Carlos Lois, Marianne E. Bronner. Proceedings of the National Academy of Sciences Nov 2020, 117 (44) 27400-27411; DOI: 10.1073/pnas.2007229117
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:106204
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:22 Oct 2020 17:06
Last Modified:04 Nov 2020 18:48

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