Control of Directed Cell Migration In Vivo by Membrane-to-Cortex Attachment
Open accessAbstract
Cell shape and motility are primarily controlled by cellular mechanics. The attachment of the plasma membrane to the underlying actomyosin cortex has been proposed to be important for cellular processes involving membrane deformation. However, little is known about the actual function of membrane-to-cortex attachment (MCA) in cell protrusion formation and migration, in particular in the context of the developing embryo. Here, we use a multidisciplinary approach to study MCA in zebrafish mesoderm and endoderm (mesendoderm) germ layer progenitor cells, which migrate using a combination of different protrusion types, namely, lamellipodia, filopodia, and blebs, during zebrafish gastrulation. By interfering with the activity of molecules linking the cortex to the membrane and measuring resulting changes in MCA by atomic force microscopy, we show that reducing MCA in mesendoderm progenitors increases the proportion of cellular blebs and reduces the directionality of cell migration. We propose that MCA is a key parameter controlling the relative proportions of different cell protrusion types in mesendoderm progenitors, and thus is key in controlling directed migration during gastrulation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Alternative perturbations such as mechanical stretching, RhoA-ROCK activation, or modification of lipid composition can induce significant disruption ranging from membrane-cytoskeleton decoupling, contractility-induced retraction to altered lipid composition and gene expression.
“Alternative perturbations such as mechanical stretching73, RhoA-ROCK activation74–76, or the modification of lipid composition77 can induce significant disruption ranging from membrane-cytoskeleton decoupling, contractility-induced retraction to altered lipid composition and gene expression.”
From Ghost Neuron preparation unlocks high-resolution structural mapping of intracellular architecture in axons (2026) · cites this paper as [75]
Split into 2 atoms — 0 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
No references could be resolved yet.
Research works printed but not linked: 52
- [1]Thompson D. A. W 1917 On growth and form Cambridge Cambridge University Press
- [2]Fletcher D. A Mullins R. D 2010 Cell mechanics and the cytoskeleton. Nature 463 485 492 20110992 PMC2851742
- [3]Bereiter-Hahn J 2005 Mechanics of crawling cells. Med Eng Phys 27 743 753 15963752
- [4]Keren K Pincus Z Allen G. M Barnhart E. L Marriott G 2008 Mechanism of shape determination in motile cells. Nature 453 475 480 18497816 PMC2877812
- [5]Insall R. H Machesky L. M 2009 Actin dynamics at the leading edge: from simple machinery to complex networks. Dev Cell 17 310 322 19758556
- [6]Sheetz M. P 2001 Cell control by membrane-cytoskeleton adhesion. Nat Rev Mol Cell Biol 2 392 396 11331914
- [7]Raucher D Sheetz M. P 2000 Cell spreading and lamellipodial extension rate is regulated by membrane tension. J Cell Biol 148 127 136 10629223 PMC2156205
- [8]Fehon R. G McClatchey A. I Bretscher A 2010 Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 11 276 287 20308985 PMC2871950
- [9]Nambiar R McConnell R. E Tyska M. J 2009 Control of cell membrane tension by myosin-I. Proc Natl Acad Sci U S A 106 11972 11977 19574460 PMC2715533
- [10]Cao X Ding X Guo Z Zhou R Wang F 2005 PALS1 specifies the localization of ezrin to the apical membrane of gastric parietal cells. J Biol Chem 280 13584 13592 15677456
- [11]Molnar C de Celis J. F 2006 Independent roles of Drosophila Moesin in imaginal disc morphogenesis and hedgehog signalling. Mech Dev 123 337 351 16682173
- [12]Van Furden D Johnson K Segbert C Bossinger O 2004 The C. elegans ezrin-radixin-moesin protein ERM-1 is necessary for apical junction remodelling and tubulogenesis in the intestine. Dev Biol 272 262 276 15242805
- [13]Kunda P Pelling A. E Liu T Baum B 2008 Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr Biol 18 91 101 18207738
- [14]Carreno S Kouranti I Glusman E. S Fuller M. T Echard A 2008 Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. J Cell Biol 180 739 746 18283112 PMC2265583
- [15]Kim S. V Flavell R. A 2008 Myosin I: from yeast to human. Cell Mol Life Sci 65 2128 2137 18344022 PMC11131817
- [16]Link V Carvalho L Castanon I Stockinger P Shevchenko A 2006 Identification of regulators of germ layer morphogenesis using proteomics in zebrafish. J Cell Sci 119 2073 2083 16638810
- [17]Bretscher A Edwards K Fehon R. G 2002 ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3 586 599 12154370
- [18]Ulrich F Concha M. L Heid P. J Voss E Witzel S 2003 Slb/Wnt11 controls hypoblast cell migration and morphogenesis at the onset of zebrafish gastrulation. Development 16 16 PMC1414802 13129848
- [19]Montero J. A Kilian B Chan J Bayliss P. E Heisenberg C. P 2003 Phosphoinositide 3-kinase is required for process outgrowth and cell polarization of gastrulating mesendodermal cells. Curr Biol 13 1279 1289 12906787
- [20]Schier A. F 2003 Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol 19 589 621 14570583
- [21]Gautreau A Louvard D Arpin M 2000 Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane. J Cell Biol 150 193 203 10893267 PMC2185562
- [22]Hochmuth F. M Shao J. Y Dai J Sheetz M. P 1996 Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys J 70 358 369 8770212 PMC1224934
- [23]Brochard-Wyart F Borghi N Cuvelier D Nassoy P 2006 Hydrodynamic narrowing of tubes extruded from cells. Proc Natl Acad Sci U S A 103 7660 7663 16679410 PMC1472501
- [24]Krieg M Helenius J Heisenberg C. P Muller D. J 2008 A bond for a lifetime: employing membrane nanotubes from living cells to determine receptor-ligand kinetics. Angew Chem Int Ed Engl 47 9775 9777 19035533
- [25]Song J Waugh R. E 1993 Bending rigidity of SOPC membranes containing cholesterol. Biophys J 64 1967 1970 8369417 PMC1262529
- [26]Sun M Northup N Marga F Huber T Byfield F. J 2007 The effect of cellular cholesterol on membrane-cytoskeleton adhesion. J Cell Sci 120 2223 2231 17550968
- [27]Heinrich V Leung A Evans E 2005 Nano- to microscale dynamics of P-selectin detachment from leukocyte interfaces. II. Tether flow terminated by P-selectin dissociation from PSGL-1. Biophys J 88 2299 2308 15653735 PMC1305279
- [28]Day C. A Kenworthy A. K 2009 Tracking microdomain dynamics in cell membranes. Biochim Biophys Acta 1788 245 253 19041847 PMC2792115
- [29]Charras G. T Hu C. K Coughlin M Mitchison T. J 2006 Reassembly of contractile actin cortex in cell blebs. J Cell Biol 175 477 490 17088428 PMC2064524
- [30]Charras G Paluch E 2008 Blebs lead the way: how to migrate without lamellipodia. Nat Rev Mol Cell Biol 9 730 736 18628785
- [31]Fackler O. T Grosse R 2008 Cell motility through plasma membrane blebbing. J Cell Biol 181 879 884 18541702 PMC2426937
- [32]Riedl J Crevenna A. H Kessenbrock K Yu J. H Neukirchen D 2008 Lifeact: a versatile marker to visualize F-actin. Nat Methods 5 605 607 18536722 PMC2814344
- [34]Blaser H Reichman-Fried M Castanon I Dumstrei K Marlow F. L 2006 Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev Cell 11 613 627 17084355
- [35]Tinevez J. Y Schulze U Salbreux G Roensch J Joanny J. F 2009 Role of cortical tension in bleb growth. Proc Natl Acad Sci U S A 106 18581 18586 19846787 PMC2765453
- [36]Charras G. T Coughlin M Mitchison T. J Mahadevan L 2008 Life and times of a cellular bleb. Biophys J 94 1836 1853 17921219 PMC2242777
- [37]Krieg M Arboleda-Estudillo Y Puech P. H Kafer J Graner F 2008 Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10 429 436 18364700
- [38]Gritsman K Zhang J Cheng S Heckscher E Talbot W. S 1999 The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 97 121 132 10199408
- [39]Arboleda-Estudillo Y Krieg M Stuhmer J Licata N. A Muller D. J 2010 Movement directionality in collective migration of germ layer progenitors. Curr Biol 20 161 169 20079641
- [40]Weiser D. C Row R. H Kimelman D 2009 Rho-regulated myosin phosphatase establishes the level of protrusive activity required for cell movements during zebrafish gastrulation. Development 136 2375 2384 19515695 PMC2729349
- [41]Sahai E Marshall C. J 2003 Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5 711 719 12844144
- [42]Pinner S Sahai E 2008 Imaging amoeboid cancer cell motility in vivo. J Microsc 231 441 445 18754999
- [43]Trinkaus J. P 1973 Surface activity and locomotion of Fundulus deep cells during blastula and gastrula stages. Dev Biol 30 69 103 4735370
- [44]Fink R. D Trinkaus J. P 1988 Fundulus deep cells: directional migration in response to epithelial wounding. Dev Biol 129 179 190 3410158
- [45]Trinkaus J. P Trinkaus M Fink R. D 1992 On the convergent cell movements of gastrulation in Fundulus. J Exp Zool 261 40 61 1729385
- [46]Brambilla D Fais S 2009 The Janus-faced role of ezrin in “linking” cells to either normal or metastatic phenotype. Int J Cancer 125 2239 2245 19588507
- [47]Westerfield M 2000 The zebrafish book: A guide for the laboratory use of zebrafish (Danio rerio). 4th edition Eugene (Oregon) University of Oregon
- [48]Kimmel C. B Ballard W. W Kimmel S. R Ullmann B Schilling T. F 1995 Stages of embryonic development of the zebrafish. Dev Dyn 203 253 310 8589427
- [49]Montero J. A Carvalho L Wilsch-Brauninger M Kilian B Mustafa C 2005 Shield formation at the onset of zebrafish gastrulation. Development 132 1187 1198 15703282
- [50]Tyska M. J Mooseker M. S 2004 A role for myosin-1A in the localization of a brush border disaccharidase. J Cell Biol 165 395 405 15138292 PMC2172191
- [51]Zimmerberg J 2006 Membrane biophysics. Curr Biol 16 R272 R276 16631568
- [52]Borghi N Brochard-Wyart F 2007 Tether extrusion from red blood cells: integral proteins unbinding from cytoskeleton. Biophys J 93 1369 1379 17526591 PMC1929048
- [53]Ferrer J. M Lee H Chen J Pelz B Nakamura F 2008 Measuring molecular rupture forces between single actin filaments and actin-binding proteins. Proc Natl Acad Sci U S A 105 9221 9226 18591676 PMC2453742
Cited by
Sorted by citations
α-Catenin cytomechanics – role in cadherin-dependent adhesion and mechanotransduction
Barry, A. K., Tabdili, H., Muhamed, I., Wu, J., Shashikanth, N., Gomez, G. A., Yap, A. S., Gottardi, C. J., de Rooij, J., Wang, N., et al. (2014) · Journal of Cell Science · doi:10.1242/jcs.139014 · Cited by 119 · see citing works
Huang, B., Lu, M., Jolly, M. K., Tsarfaty, I., Onuchic, J., & Ben-Jacob, E. (2014) · Scientific Reports · doi:10.1038/srep06449 · Cited by 91 · see citing works
Bodakuntla, S., Marelli, J., Vasquez-Montes, V., Glauser, S., Biertümpfel, C., & Mizuno, N. (2026) · Nature Communications · doi:10.1038/s41467-026-77741-4
- Authors
- Diz-Muñoz, A., Krieg, M., Bergert, M., Ibarlucea-Benitez, I., Muller, D. J., Paluch, E., & Heisenberg, C.-P.
- Affiliations
- International Institute of Molecular and Cell Biology (PL)
- Biotechnologisches Zentrum (DE)
- Institute of Science and Technology Austria (AT)
- Corresponding author
- Krieg, Michael
- Paluch, Ewa
- Heisenberg, Carl-Philipp
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-11-30
- Volume
- 8
- Issue
- 11
- Pages
- e1000544
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC2994655
- OpenAlex
- W2145865462
- Cited by
- 271
- References
- 0
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 15 · 2023: 13 · 2022: 18 · 2021: 13 · 2020: 29 · 2019: 16 · 2018: 16 · 2017: 13 · 2016: 16 · 2015: 21 · 2014: 28 · 2013: 20 · 2012: 18
- FWCI
- 6.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Institute for Plasma Physics (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Qucosa (Saxon State and University Library Dresden) (submittedVersion, cc-by)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- ETH Zürich Research Collection (cc-by)
- Funders
- Institute of Science and Technology Austria
- Boehringer Ingelheim Fonds
- Deutsche Forschungsgemeinschaft (PA 1590/1-1, 1590/1-1, HE 3231/6-1)
- Max-Planck-Gesellschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- cell migration, cell protrusions, blebs, lamellipodia, filopodia, zebrafish gastrulation, actomyosin cortex, cell shape, migration directionality, atomic force microscopy
- MeSH terms
- Animals, Cell Membrane, Cell Movement, Cytoskeleton, Mesoderm, Pseudopodia, Stem Cells, Zebrafish, Microscopy, Confocal, Microscopy, Atomic Force, Gastrulation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review