Outline

Disclaimer: this translation is made available to the public with the aim of broadening the scientific dissemination of the original article, but has not been verified by either the authors (unless their names appear among those of the authors of the translation) or the journal's editorial team. This version does not engage the scientific responsibility of the editors. The original version remains the only scientific reference.

Organizing collective cell migration through guidance by followers
Translated by:

Abstract translation

Translation posted on:
DOI: 10.5802/crbiol.145-fr
Keywords: Collective cell migration, Embryonic development, Mechanosensation, Cell polarization, Zebrafish, Mesenchymal cell, Mesoderm
Mots-clés : Migration cellulaire collective, Développement embryonnaire, Mécanoperception, Polarisation cellulaire, Poisson zèbre, Cellule mésenchymateuse, Mésoderme
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
Arthur Boutillon.  Organiser la migration cellulaire collective via le guidage par les suiveuses
 (2024) doi : 10.5802/crbiol.145-fr (Arthur Boutillon. Organizing collective cell migration through guidance by followers. Comptes Rendus. Biologies, Volume 346 (2023), pp. 117-126. doi: 10.5802/crbiol.14)
@article{CRBIOL_2023__346_G2_117_0,
     author = {Arthur Boutillon},
     title = {Organizing collective cell migration through guidance by followers
},
     journal = {Comptes Rendus. Biologies},
     pages = {117--126},
     year = {2023},
     publisher = {Acad\'emie des sciences, Paris},
     volume = {346},
     doi = {10.5802/crbiol.145},
     language = {en},
}
TY  - JOUR
AU  - Arthur Boutillon
TI  - Organizing collective cell migration through guidance by followers

JO  - Comptes Rendus. Biologies
PY  - 2023
SP  - 117
EP  - 126
VL  - 346
PB  - Académie des sciences, Paris
DO  - 10.5802/crbiol.145
LA  - en
ID  - CRBIOL_2023__346_G2_117_0
ER  - 
%0 Journal Article
%A Arthur Boutillon
%T Organizing collective cell migration through guidance by followers

%J Comptes Rendus. Biologies
%D 2023
%P 117-126
%V 346
%I Académie des sciences, Paris
%R 10.5802/crbiol.145
%G en
%F CRBIOL_2023__346_G2_117_0

[1] C. De Pascalis; S. Etienne-Manneville Single and collective cell migration: the mechanics of adhesions, Mol. Biol. Cell, Volume 28 (2017) no. 14, pp. 1833-1846 | DOI

[2] P. Rosen; D. S. Misfeldt Cell density determines epithelial migration in culture, Proc. Natl. Acad. Sci. USA, Volume 77 (1980) no. 8, pp. 4760-4763 | DOI

[3] S. R. K. Vedula; A. Ravasio; C. T. Lim; B. Ladoux Collective cell migration: a mechanistic perspective, Physiology, Volume 28 (2013) no. 6, pp. 370-379 | DOI

[4] E. Theveneau; R. Mayor Collective cell migration of epithelial and mesenchymal cells, Cell. Mol. Life Sci., Volume 70 (2013) no. 19, pp. 3481-3492 | DOI

[5] G. J. Todaro; G. K. Lazar; H. Green The initiation of cell division in a contact-inhibited mammalian cell line, J. Cell. Physiol., Volume 66 (1965) no. 3, pp. 325-333 | DOI

[6] M. Poujade; E. Grasland-Mongrain; A. Hertzog; J. Jouanneau; P. Chavrier; B. Ladoux; A. Buguin; P. Silberzan Collective migration of an epithelial monolayer in response to a model wound, Proc. Natl. Acad. Sci. USA, Volume 104 (2007) no. 41, pp. 15988-15993 | DOI

[7] P. Rørth Collective cell migration, Annu. Rev. Cell Dev. Biol., Volume 25 (2009) no. 1, pp. 407-429 | DOI

[8] E. Caussinus; J. Colombelli; M. Affolter Tip-cell migration controls stalk-cell intercalation during drosophila tracheal tube elongation, Curr. Biol., Volume 18 (2008) no. 22, pp. 1727-1734 | DOI

[9] P. Haas; D. Gilmour Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line, Dev. Cell, Volume 10 (2006) no. 5, pp. 673-680 | DOI

[10] A. K. Mishra; J. A. Mondo; J. P. Campanale; D. J. Montell Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II, Mol. Biol. Cell, Volume 30 (2019) no. 19, pp. 2490-2502 | DOI

[11] C. Dambly-Chaudière; N. Cubedo; A. Ghysen Control of cell migration in the development of the posterior lateral line: antagonistic interactions between the chemokine receptors CXCR4 and CXCR7/RDC1, BMC Dev. Biol., Volume 7 (2007), 23 | DOI

[12] N. B. David; D. Sapède; L. Saint-Etienne; C. Thisse; B. Thisse; C. Dambly-Chaudière; F. M. Rosa; A. Ghysen Molecular basis of cell migration in the fish lateral line: role of the chemokine receptor CXCR4 and of its ligand, SDF1, Proc. Natl. Acad. Sci. USA, Volume 99 (2002) no. 25, pp. 16297-16302 | DOI

[13] E. Donà; J. D. Barry; G. Valentin; C. Quirin; A. Khmelinskii; A. Kunze; S. Durdu; L. R. Newton; A. Fernandez-Minan; W. Huber; M. Knop; D. Gilmour Directional tissue migration through a self-generated chemokine gradient, Nature, Volume 503 (2013), pp. 285-289 | DOI

[14] G. Venkiteswaran; S. W. Lewellis; J. Wang; E. Reynolds; C. Nicholson; H. Knaut Generation and dynamics of an endogenous, self-generated signaling gradient across a migrating tissue, Cell, Volume 155 (2013) no. 3, pp. 674-687 | DOI

[15] D. D. Nogare; K. Somers; S. Rao; M. Matsuda; M. Reichman-Fried; E. Raz; A. B. Chitnis Leading and trailing cells cooperate in collective migration of the zebrafish posterior lateral line primordium, Development (Cambridge), Volume 141 (2014) no. 16, pp. 3188-3196 | DOI

[16] J. M. Burns; B. C. Summers; Y. Wang; A. Melikian; R. Berahovich; Z. Miao; M. E. T. Penfold; M. J. Sunshine; D. R. Littman; C. J. Kuo; K. Wei; B. E. McMaster; K. Wright; M. C. Howard; T. J. Schall A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development, J. Exp. Med., Volume 203 (2006) no. 9, pp. 2201-2213 | DOI

[17] G. Valentin; P. Haas; D. Gilmour The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b, Curr. Biol., Volume 17 (2007) no. 12, pp. 1026-1031 | DOI

[18] A. Aalto; A. Olguin-Olguin; E. Raz Zebrafish primordial germ cell migration, Front. Cell Dev. Biol., Volume 9 (2021), 684460 | DOI

[19] V. Miskolci; J. Squirrell; J. Rindy; W. Vincent; J. D. Sauer; A. Gibson; K. W. Eliceiri; A. Huttenlocher Distinct inflammatory and wound healing responses to complex caudal fin injuries of larval zebrafish, ELife, Volume 8 (2019), pp. 1-18 | DOI

[20] J. Stock; T. Kazmar; F. Schlumm; E. Hannezo; A. Pauli A self-generated toddler gradient guides mesodermal cell migration, Sci. Adv., Volume 8 (2022) no. 37, pp. 1-15 | DOI

[21] E. Theveneau; R. Mayor Can mesenchymal cells undergo collective cell migration? The case of the neural crest, Cell Adh. Migr., Volume 5 (2011) no. 6, pp. 490-498 | DOI

[22] E. Scarpa; R. Mayor Collective cell migration in development, J. Cell Biol., Volume 212 (2016) no. 2, pp. 143-155 | DOI

[23] E. Theveneau; R. Mayor Neural crest migration: interplay between chemorepellents, chemoattractants, contact inhibition, epithelial–mesenchymal transition, and collective cell migration, Wiley Interdiscip. Rev. Dev. Biol., Volume 1 (2012) no. 3, pp. 435-445 | DOI

[24] E. H. Barriga; R. Mayor Adjustable viscoelasticity allows for efficient collective cell migration, Semin. Cell Dev. Biol., Volume 93 (2019), pp. 55-68 | DOI

[25] E. H. Barriga; E. Theveneau In vivo neural crest cell migration is controlled by ‘Mixotaxis’, Front. Physiol., Volume 11 (2020), pp. 1-9 | DOI

[26] F. Ferreira; Sofia Moreira; E. H. Barriga Stretch-induced endogenous electric fields drive neural crest directed collective cell migration in vivo, 2021 (BioRxiv, https://doi.org/10.1101/2021.10.11.463916)

[27] A. Shellard; R. Mayor Collective durotaxis along a self-generated stiffness gradient in vivo, Nature, Volume 600 (2021) no. 7890, pp. 690-694 | DOI

[28] E. Theveneau; L. Marchant; S. Kuriyama; M. Gull; B. Moepps; M. Parsons; R. Mayor Collective chemotaxis requires contact-dependent cell polarity, Dev. Cell, Volume 19 (2010) no. 1, pp. 39-53 | DOI

[29] C. Carmona-Fontaine; H. K. Matthews; S. Kuriyama; M. Moreno; G. A. Dunn; M. Parsons; C. D. Stern; R. Mayor Contact inhibition of locomotion in vivo controls neural crest directional migration, Nature, Volume 456 (2008) no. 7224, pp. 957-961 | DOI

[30] C. Carmona-Fontaine; E. Theveneau; A. Tzekou; M. Tada; M. Woods; K. M. Page; M. Parsons; J. D. Lambris; R. Mayor Complement fragment C3a controls mutual cell attraction during collective cell migration, Dev. Cell, Volume 21 (2011) no. 6, pp. 1026-1037 | DOI

[31] A. Shellard; R. Mayor Chemotaxis during neural crest migration, Semin. Cell Dev. Biol., Volume 55 (2016), pp. 111-118 | DOI

[32] L. Loeb Amœboid movement, tissue formation and consistency of protoplasm, Science, Volume 53 (1921) no. 1368, pp. 261-262 | DOI

[33] M. Abercrombie; J. E. M. Heaysman Observations on the social behaviour of cells in tissue culture: II. ‘Monolayering’ of fibroblasts, Exp. Cell Res., Volume 6 (1954) no. 2, pp. 293-306 | DOI

[34] B. Stramer; R. Mayor Mechanisms and in vivo functions of contact inhibition of locomotion, Nat. Rev. Mol. Cell Biol., Volume 18 (2016) no. 1, pp. 43-55 | DOI

[35] A. Szabó; M. Melchionda; G. Nastasi; M. L. Woods; S. Campo; R. Perris; R. Mayor In vivo confinement promotes collective migration of neural crest cells, J. Cell Biol., Volume 213 (2016) no. 5, pp. 543-555 | DOI

[36] D. Li; Y.-L. Wang Coordination of cell migration mediated by site-dependent cell–cell contact, Proc. Natl. Acad. Sci. USA, Volume 115 (2018), pp. 10678-10683 | DOI

[37] M. Hayakawa; T. Hiraiwa; Y. Wada; H. Kuwayama; T. Shibata Polar pattern formation induced by contact following locomotion in a multicellular system, ELife, Volume 9 (2020), pp. 1-18 | DOI

[38] J. D’alessandro; A. P. Solon; Y. Hayakawa; C. Anjard; F. Detcheverry; J. P. Rieu; C. Rivière Contact enhancement of locomotion in spreading cell colonies, Nat. Phys., Volume 13 (2017) no. 10, pp. 999-1005 | DOI

[39] R. Alert; X. Trepat Physical models of collective cell migration, Annu. Rev. Condens. Matter Phys., Volume 11 (2020), pp. 77-101 | DOI

[40] D. T. Tambe; C. C. Hardin; T. E. Angelini; K. Rajendran; C. Y. Park; X. Serra-Picamal; E. H. Zhou; M. H. Zaman; J. P. Butler; D. A. Weitz; J. J. Fredberg; X. Trepat Collective cell guidance by cooperative intercellular forces, Nat. Mater., Volume 10 (2011) no. 6, pp. 469-475 | DOI

[41] A. Boutillon; S. Escot; A. Elouin; D. Jahn; S. González-Tirado; J. Starruß; L. Brusch; N. B. David Guidance by followers ensures long-range coordination of cell migration through α-catenin mechanoperception, Dev. Cell, Volume 57 (2022) no. 12, p. 1529-1544.e5 | DOI

[42] A. E. E. Bruce Zebrafish epiboly: spreading thin over the yolk, Dev. Dyn., Volume 245 (2016) no. 3, pp. 244-258 | DOI

[43] R. M. Warga; C. B. Kimmel Cell movements during epiboly and gastrulation in zebrafish, Development, Volume 108 (1990) no. 4, pp. 569-580 | DOI

[44] J.-A. Montero; L. Carvalho; M. Wilsch-Bräuninger; B. Kilian; C. Mustafa; C.-P. Heisenberg Shield formation at the onset of zebrafish gastrulation, Development (Cambridge, England), Volume 132 (2005) no. 6, pp. 1187-1198 | DOI

[45] D. Pinheiro; R. Kardos; É. Hannezo; C.-P. Heisenberg Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming, Nat. Phys., Volume 18 (2022), pp. 1482-1493 | DOI

[46] D. Pinheiro; C. P. Heisenberg Zebrafish gastrulation: putting fate in motion, Curr. Top. Dev. Biol., Volume 136 (2020), pp. 343-375 | DOI

[47] M. L. K. Williams; L. Solnica-Krezel Regulation of gastrulation movements by emergent cell and tissue interactions, Curr. Opin. Cell Biol., Volume 48 (2017), pp. 33-39 | DOI

[48] A. Souchaud; A. Boutillon; G. Charron; A. Asnacios; C. Noûs; N. B. David; F. Graner; F. Gallet Live 3D imaging and mapping of shear stresses within tissues using incompressible elastic beads, Development, Volume 149 (2022) no. 4, dev199765 | DOI

[49] J. G. Dumortier; S. Martin; D. Meyer; F. M. Rosa; N. B. David Collective mesendoderm migration relies on an intrinsic directionality signal transmitted through cell contacts, Proc. Natl. Acad. Sci. USA, Volume 109 (2012) no. 42, pp. 16945-16950 | DOI

[50] C. B. Kimmel; W. W. Ballard; S. R. Kimmel; B. Ullmann; T. F. Schilling Stages of embryonic development of the zebrafish, Dev. Dyn., Volume 203 (1995), pp. 253-310 | DOI

[51] J.-A. Montero; B. Kilian; J. Chan; P. E. Bayliss; C.-P. Heisenberg Phosphoinositide 3-kinase is required for process outgrowth and cell polarization of gastrulating mesendodermal cells, Curr. Biol., Volume 13 (2003), pp. 1279-1289 | DOI

[52] N. S. Glickman; C. B. Kimmel; M. A. Jones; R. J. Adams Shaping the zebrafish notochord, Development, Volume 130 (2003) no. 5, pp. 873-887 | DOI

[53] M. Kai; C. P. Heisenberg; M. Tada Sphingosine-1-phosphate receptors regulate individual cell behaviours underlying the directed migration of prechordal plate progenitor cells during zebrafish gastrulation, Development, Volume 135 (2008) no. 18, pp. 3043-3051 | DOI

[54] A. Boutillon; S. Escot; N. B. David Deep and spatially controlled volume ablations using a two-photon microscope in the zebrafish gastrula, J. Vis. Exp. (2021) no. 173, e62815 | DOI

[55] J. Richardson; A. Gauert; L. B. Montecinos; L. Fanlo; Z. M. Alhashem; R. Assar; E. Marti; A. Kabla; S. Härtel; C. Linker Leader cells define directionality of trunk, but not cranial, neural crest cell migration, Cell Rep., Volume 15 (2016) no. 9, pp. 2076-2088 | DOI

[56] A. Boutillon; F. A. Giger; N. B. David Analysis of in vivo cell migration in mosaic zebrafish embryos, Methods in Molecular Biology (A. Gautreau, ed.), Volume 1749, Springer, New York, 2018, pp. 213-226 | DOI

[57] M. K. L. Han; G. N. M. Van Der Krogt; Johan De Rooij Zygotic vinculin is not essential for embryonic development in zebrafish, PLoS ONE, Volume 12 (2017) no. 8, pp. 1-22 | DOI

[58] J. Jurado; J. de Navascués; N. Gorfinkiel α-catenin stabilises cadherin-catenin complexes and modulates actomyosin dynamics to allow pulsatile apical contraction, J. Cell Sci., Volume 129 (2016) no. 24, pp. 4496-4508 | DOI

[59] M. Yao; W. Qiu; R. Liu; A. K. Efremov; P. Cong; R. Seddiki; M. Payre; C. T. Lim; B. Ladoux; R. M. Mège; J. Yan Force-dependent conformational switch of α-catenin controls vinculin binding, Nat. Commun., Volume 5 (2014), 4525 | DOI

[60] S. Yonemura; Y. Wada; T. Watanabe; A. Nagafuchi; M. Shibata α-catenin as a tension transducer that induces adherens junction development, Nat. Cell Biol., Volume 12 (2010) no. 6, pp. 533-542 | DOI

[61] R. Müller; A. Boutillon; D. Jahn; J. Starruß; N. B. David; L. Brusch Collective cell migration due to guidance-by-followers is robust to multiple stimuli, Front. Appl. Math. Stat., Volume 9 (2023), 1163583 | DOI

[62] C. Grashoff; B. D. Hoffman; M. D. Brenner; R. Zhou; M. Parsons; M. T. Yang; M. A. McLean; S. G. Sligar; C. S. Chen; T. Ha; M. A. Schwartz Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics, Nature, Volume 466 (2010) no. 7303, pp. 263-266 | DOI

[63] B. Kilian; H. Mansukoski; F. C. Barbosa; F. Ulrich; M. Tada; C. P. Heisenberg The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation, Mech. Dev., Volume 120 (2003) no. 4, pp. 467-476 | DOI

[64] F. Ulrich; M. L. Concha; P. J. Heid; E. Voss; S. Witzel; H. Roehl; M. Tada; S. W. Wilson; R. J. Adams; D. R. Soll; C.-P. Heisenberg Slb/Wnt11 controls hypoblast cell migration and morphogenesis at the onset of zebrafish gastrulation, Development, Volume 130 (2003) no. 22, pp. 5375-5384 | DOI

[65] A. Shimada; M. Yabusaki; H. Niwa; H. Yokoi; K. Hatta; D. Kobayashi; H. Takeda Maternal-zygotic medaka mutants for Fgfr1 reveal its essential role in the migration of the axial mesoderm but not the lateral mesoderm, Development (Cambridge, England), Volume 135 (2008) no. 2, pp. 281-290 | DOI

Cited by Sources:

Comments - Policy