Polarizing cytoskeletal tension to induce leader cell formation during collective cell migration

Biointerphases

Volumn 8, Issue 1, 2013, Pages

  Rausch, Sebastian ^a,b   Das, Tamal ^a,b   Soiné, Jérôme R D ^b,c   Hofmann, Tobias W ^a,b   Boehm, Christian H J ^a,b   Schwarz, Ulrich S ^b,c   Boehm, Heike ^a,b   Spatz, Joachim P ^a,b  

^a MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c INSTITUT FÜR THEORETISCHE PHYSIK   (Germany)

Author keywords

Collective migration; Geometric constraint; Leader cell; MDCK cells; Traction force

Indexed keywords

CELLULAR MANUFACTURING; CYTOLOGY; GEOMETRY; MORPHOLOGY; REDUCING AGENTS; SHEAR STRESS; TISSUE REGENERATION; TRACTION (FRICTION);

CELL-SUBSTRATE INTERACTIONS; COLLECTIVE CELL MIGRATIONS; COLLECTIVE MIGRATION; EPITHELIAL CELL SHEETS; GEOMETRIC CONSTRAINT; MDCK CELLS; TRACTION FORCE MICROSCOPIES; TRACTION FORCES;

CELLS;

ANIMAL; CELL CULTURE; CELL MOTION; CYTOSKELETON; METABOLISM; PHYSIOLOGY; RAT;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; RATS;

EID: 84891442243     PISSN: 19348630     EISSN: 15594106     Source Type: Journal    
DOI: 10.1186/1559-4106-8-32     Document Type: Article

References (41)

1. Streichan SJ, Valentin G, Gilmour D, Hufnagel L (2011) Collective cell migration guided by dynamically maintained gradients. Phys Biol 8(4):045004
2. Friedl P, Hegerfeldt Y, Tusch M (2004) Collective cell migration in morphogenesis and cancer. Int J Dev Biol 48(5-6):441-449
3. Martin P (1997) Wound Healing-Aiming for Perfect Skin Regeneration. Science 276(5309):75-81
4. Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P, Ladoux B, Buguin A, Silberzan P (2007) Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci 104(41):15988-15993
5. Omelchenko T, Vasiliev JM, Gelfand IM, Feder HH, Bonder EM (2003) Rho-dependent formation of epithelial "leader" cells during wound healing. Proc Natl Acad Sci 100(19):10788-10793
6. Khalil AA, Friedl P (2010) Determinants of leader cells in collective cell migration. Integr Biol 2(11-12):568-574
7. Lim JI, Sabouri-Ghomi M, Machacek M, Waterman CM, Danuser G (2010) Protrusion and actin assembly are coupled to the organization of lamellar contractile structures. Exp Cell Res 316(13):2027-2041
8. Vitorino P, Meyer T (2008) Modular control of endothelial sheet migration. Genes Dev 22(23):3268-3281
9. Aigouy B, Lepelletier L, Giangrande A (2008) Glial chain migration requires pioneer cells. J Neurosci 28(45):11635-11641
10. Reffay M, Petitjean L, Coscoy S, Grasland-Mongrain E, Amblard F, Buguin A, Silberzan P (2011) Orientation and polarity in collectively migrating cell structures: statics and dynamics. Biophys J 100(11):2566-2575
11. Trepat X, Wasserman M, Angelini T, Millet E, Weitz D, Butler J, Fredberg J (2009) Physical forces during collective cell migration. Nat Phys 5(6):426-430
12. Farooqui R, Fenteany G (2005) Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J Cell Sci 118(Pt 1):51-63
13. Trepat X, Fredberg JJ (2011) Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol 11(21):638-646
14. Vedula SRK, Leong MC, Lai TL, Hersen P, Kabla AJ, Lim CT, Ladoux B (2012) Emerging modes of collective cell migration induced by geometrical constraints. Proc Natl Acad Sci 109(32):12974-12979
15. Anon E, Serra-Picamal X, Hersen P, Gauthier NC, Sheetz MP, Trepat X, Ladoux B (2012) Cell crawling mediates collective cell migration to close undamaged epithelial gaps. Proc Natl Acad Sci 109(27):10891-10896
16. Ng MR, Besser A, Danuser G, Brugge JS (2012) Substrate stiffness regulates cadherindependent collective migration through myosin-II contractility. J Cell Biol 199(3):545-563
17. Hirashima T, Hosokawa Y, Lino T, Nagayama M (2013) On fundamental cellular processes for emergence of collective epithelial movement. Biol Open 2(7):660-666
18. Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, Spector AA, Chen CS (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci 102(33):11594-11599
19. Mark S, Shlomovitz R, Gov NS, Poujade M, Grasland-Mongrain E, Silberzan P (2010) Physical model of the dynamic instability in an expanding cell culture. Biophys J 98(3):361-370
20. Rolli CG, Nakayama H, Yamaguchi K, Spatz JP, Kemkemer R, Nakanishi J (2012) Switchable adhesive substrates: revealing geometry dependence in collective cell behavior. Biomaterials 33(8):2409-2418
21. Tse JM, Cheng G, Tyrrell JA, Wilcox-Adelman SA, Boucher Y, Jain RK, Munn LL (2012) Mechanical compression drives cancer cells toward invasive phenotype. Proc Natl Acad Sci 109(3):911-916
22. Jiang X, Bruzewicz DA, Wong AP, Piel M, Whitesides GM (2005) Directing cell migration with asymmetric micropatterns. Proc Natl Acad Sci 102(4):975-978
23. Brock A, Chang E, Ho C-C, LeDuc P, Jiang X, Whitesides GM, Ingber DE (2003) Geometric determinants of directional cell motility revealed using microcontact printing. Langmuir 19(5):1611-1617
24. Duffy DC, McDonald JC, Schueller OJA, Whitesides GM (1998) Rapid Prototyping of Microfluidic Systems in Poly(dimethylsiloxane). Anal Chem 70(23):4974-4984
25. Aratyn-Schaus Y, Oakes PW, Stricker J, Winter SP, Gardel ML (2010) Preparation of complaint matrices for quantifying cellular contraction. J Vis Exp 46:2173
26. Crocker JC, Grier DG (1996) Methods of digital video microscopy for colloidal studies. J Colloid Interface Sci 179(1):298-310
27. Sabass B, Gardel ML, Waterman CM, Schwarz US (2008) High Resolution Traction Force Microscopy Based on Experimental and Computational Advances. Biophys J 94(1):207-220
28. Edwards CM, Schwarz US (2011) Force localization in contracting cell layers. Phys Rev Lett 107(12):128101
29. Weijer CJ (2009) Collective cell migration in development. J Cell Sci 122(Pt 18):3215-3223
30. Rørth P (2009) Collective Cell Migration. Annu Rev Cell Dev Biol 25(1):407-429
31. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10(7):445-457
32. Tambe DT, Hardin CC, Angelini TE, Rajendran K, Park CY, Serra-Picamal X, Zhou EH, Zaman MH, Butler JP, Weitz DA, Fredberg JJ, Trepat X (2011) Collective cell guidance by cooperative intercellular forces. Nat Mater 10(6):469-475
33. Kim JH, Serra-Picamal X, Tambe DT, Zhou EH, Park CY, Sadati M, Park J-A, Krishnan R, Gweon B, Millet E, Butler JP, Trepat X, Fredberg JJ (2013) Propulsion and navigation within the advancing monolayer sheet. Nat Mater 12(9):856-863
34. Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, Sellers JR, Mitchison TJ (2003) Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299(5613):1743-1747
35. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389(6654):990-994
36. Pelham RJ, Wang YL (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci 94(25):13661-13665
37. Butler JP, Tolić-Nørrelykke IM, Fabry B, Fredberg JJ (2002) Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol Cell Physiol 282(3):C595-C605
38. Berginski ME, Vitriol EA, Hahn KM, Gomez SM (2011) High-resolution quantification of focal adhesion spatiotemporal dynamics in living cells. PLoS ONE 6(7):e22025
39. Tojkander S, Gateva G, Lappalainen P (2012) Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci 125(8):1855-1864
40. Bement WM, Mandato CA, Kirsch MN (1999) Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes. Curr Biol 9(11):579-587
41. Martin P, Lewis J (1992) Actin cables and epidermal movement in embryonic wound healing. Nature 360(6400):179-183