Integrin adhesion drives the emergent polarization of active cytoskeletal stresses to pattern cell delamination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 22, 2011, Pages 9107-9112

  Meghana, C ^a   Ramdas, Nisha ^b   Hameed, Feroz Meeran ^b   Rao, Madan ^b,c   Shivashankar, G V ^b,d   Narasimha, Maithreyi ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^c RAMAN RESEARCH INSTITUTE   (India)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cell extrusion; Cell mechanics; Tissue dynamics; Wound healing

Indexed keywords

INTEGRIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; UVOMORULIN;

ANISOTROPY; ARTICLE; CELL ADHESION; CELL DELAMINATION; CELL MEMBRANE; CELL POLARITY; CELL STRESS; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; DIPOLE; DOWN REGULATION; DROSOPHILA; GENOTYPE; LAMELLIPODIUM; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL;

ACTOMYOSIN; ANIMALS; CELL ADHESION; CELL LINEAGE; CYTOPLASM; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; INTEGRINS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; TIME FACTORS; WOUND HEALING;

EID: 79959370907     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1018652108     Document Type: Article

References (41)

1. Lecuit T (2005) Adhesion remodeling underlying tissue morphogenesis. Trends Cell Biol 15:34-42.
2. Juliano RL (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: Functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42:283-323.
3. Bershadsky AD, Balaban NQ, Geiger B (2003) Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 19:677-695. (Pubitemid 37487365)
4. Vogel V, Sheetz M (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7:265-275.
5. Hutson MS, et al. (2003) Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300:145-149. (Pubitemid 36423049)
6. Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149:471-490. (Pubitemid 30227162)
7. Narasimha M, Brown NH (2004) Novel functions for integrins in epithelial morphogenesis. Curr Biol 14:381-385. (Pubitemid 38431171)
8. Peralta XG, et al. (2007) Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys J 92:2583-2596. (Pubitemid 46536438)
9. Jacinto A, Woolner S, Martin P (2002) Dynamic analysis of dorsal closure in Drosophila: From genetics to cell biology. Dev Cell 3:9-19. (Pubitemid 34778392)
10. Toyama Y, Peralta XG, Wells AR, Kiehart DP, Edwards GS (2008) Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321:1683-1686.
11. Mazumder A, Shivashankar GV (2007) Gold-nanoparticle-assisted laser perturbation of chromatin assembly reveals unusual aspects of nuclear architecture within living cells. Biophys J 93:2209-2216. (Pubitemid 47437604)
12. Kumar S, et al. (2006) Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J 90:3762-3773.
13. Farhadifar R, Röper JC, Aigouy B, Eaton S, Jülicher F (2007) The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 17:2095-2104. (Pubitemid 50014864)
14. Rauzi M, Verant P, Lecuit T, Lenne PF (2008) Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat Cell Biol 10:1401-1410.
15. Hatwalne Y, Ramaswamy S, Rao M, Simha RA (2004) Rheology of active-particle suspensions. Phys Rev Lett 92:118101-118104.
16. Lau AWC, Hoffman BD, Davies A, Crocker JC, Lubensky TCPRL (2003) Microrheology, stress fluctuations, and active behavior of living cells. Phys Rev Lett 91:198101-198104.
17. Heisterkamp A, et al. (2005) Pulse energy dependence of subcellular dissection by femtosecond laser pulses. Opt Express 13:3690-3696. (Pubitemid 40899347)
18. Clark AG, et al. (2009) Integration of single and multicellular wound responses. Curr Biol 19:1389-1395.
19. Hutson MS, et al. (2009) Combining laser microsurgery and finite element modeling to assess cell-level epithelial mechanics. Biophys J 97:3075-3085.
20. Mandato CA, Bement WM (2003) Actomyosin transports microtubules and microtubules control actomyosin recruitment during Xenopus oocyte wound healing. Curr Biol 13:1096-1105. (Pubitemid 36815257)
21. Slattum G, McGee KM, Rosenblatt J (2009) P115 RhoGEF and microtubules decide the direction apoptotic cells extrude from an epithelium. J Cell Biol 186:693-702.
22. Mazumder A, Roopa T, Basu A, Mahadevan L, Shivashankar GV (2008) Dynamics of chromatin decondensation reveals the structural integrity of a mechanically prestressed nucleus. Biophys J 95:3028-3035.
23. Mayer M, Depken M, Bois JS, Jülicher F, Grill SW (2010) Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467:617-621.
24. Kuhn SJ, Hallahan DE, Giorgio TD (2006) Characterization of superparamagnetic nanoparticle interactions with extracellular matrix in an in vitro system. Ann Biomed Eng 34:51-58.
25. Zhelev DV, Needham D, Hochmuth RM (1994) Role of the membrane cortex in neutrophil deformation in small pipets. Biophys J 67:696-705. (Pubitemid 24235398)
26. Wang N, et al. (2002) Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am J Physiol Cell Physiol 282:C606-C616. (Pubitemid 34663177)
27. Narasimha M, Brown N (2006) Integrins and associated proteins in Drosophila development. Integrins and Development, ed Danen E (Landes Bioscience, Austin, TX).
28. Giannone G, et al. (2007) Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128:561-575. (Pubitemid 46198897)
29. Rosenblatt J, Raff MC, Cramer LP (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11:1847-1857. (Pubitemid 33136524)
30. Tamada M, Perez TD, Nelson WJ, Sheetz MP (2007) Two distinct modes of myosin assembly and dynamics during epithelial wound closure. J Cell Biol 176:27-33. (Pubitemid 46041677)
31. Paluch E, van der Gucht J, Sykes C (2006) Cracking up: Symmetry breaking in cellular systems. J Cell Biol 175:687-692. (Pubitemid 44878500)
32. Fernandez-Gonzalez R, Simoes SdeM, Röper JC, Eaton S, Zallen JA (2009) Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 17:736-743.
33. Yoshigi M, Hoffman LM, Jensen CC, Yost HJ, Beckerle MC (2005) Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J Cell Biol 171:209-215. (Pubitemid 41540014)
34. Pouille PA, Ahmadi P, Brunet AC, Farge E (2009) Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci Signal 2:ra16.
35. Hirata H, Tatsumi H, Sokabe M (2008) Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J Cell Sci 121:2795-2804.
36. Jankovics F, Brunner D (2006) Transiently reorganized microtubules are essential for zippering during dorsal closure in Drosophila melanogaster. Dev Cell 11:375-385. (Pubitemid 44283946)
37. Kruse K, Joanny JF, Julicher F, Prost J (2005) Generic theory of active polar gels: A paradigm for cytoskeletal dynamics. Eur Phys J E Soft Matter 16:5-16. (Pubitemid 40226343)
38. Uemura T, et al. (1996) Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev 10:659-671. (Pubitemid 26112421)
39. Royou A, Sullivan W, Karess R (2002) Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: Its role in nuclear axial expansion and its regulation by Cdc2 activity. J Cell Biol 158:127-137.
40. Oda H, Tsukita S (1999) Dynamic features of adherens junctions during Drosophila embryonic epithelial morphogenesis revealed by a Dalpha-catenin-GFP fusion protein. Dev Genes Evol 209:218-225. (Pubitemid 29142240)
41. Morin X, Daneman R, Zavortink M, Chia W (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci USA 98:15050-15055. (Pubitemid 34013967)