Mechanosensitive adaptation of E-cadherin turnover across adherens junctions

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  De Beco, Simon ^a,b,c   Perney, Jean Baptiste ^a,b,c   Coscoy, Sylvie ^a,b,c   Amblard, François ^a,b,c  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; UVOMORULIN; CADHERIN; HYBRID PROTEIN;

ADAPTATION; ANIMAL CELL; ARTICLE; BIOCHEMISTRY; BIOMECHANICS; CELL INTERACTION; CELL JUNCTION; CONTROLLED STUDY; EPITHELIUM; FORCE TRANSDUCER; HOMEOSTASIS; NONHUMAN; REGULATORY MECHANISM; STEADY STATE; ADHERENS JUNCTION; ANIMAL; BIOSYNTHESIS; CYTOSKELETON; DOG; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETICS; MDCK CELL LINE; METABOLISM; TIME FACTOR;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CYTOSKELETON; DOGS; ENDOCYTOSIS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; MADIN DARBY CANINE KIDNEY CELLS; MICROSCOPY, FLUORESCENCE; RECOMBINANT FUSION PROTEINS; TIME FACTORS;

EID: 84935034911     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128281     Document Type: Article

References (33)

1. Benazeraf B, Pourquie O. Formation and segmentation of the vertebrate body axis. Annu Rev Cell Dev Biol. 2013; 29:1-26. Epub 2013/07/03. doi: 10.1146/annurev-cellbio-101011-155703 PMID: 23808844.
2. Kourakis MJ, Reeves W, Newman-Smith E, Maury B, Abdul-Wajid S, Smith WC. A one-dimensional model of PCP signaling: Polarized cell behavior in the notochord of the ascidian Ciona. Dev Biol. 2014; 395(1):120-30. Epub 2014/09/01. doi: S0012-1606(14)00414-X [pii] doi: 10.1016/j.ydbio.2014.08.023 PMID: 25173874; PubMed Central PMCID: PMC4190077.
3. Iruela-Arispe ML, Beitel GJ. Tubulogenesis. Development. 2013; 140(14):2851-5. Epub 2013/07/04. doi: 140/14/2851 [pii] doi: 10.1242/dev.070680 PMID: 23821032; PubMed Central PMCID: PMC3699276.
4. Reffay M, Parrini MC, Cochet-Escartin O, Ladoux B, Buguin A, Coscoy S, et al. Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells. Nat Cell Biol. 2014; 16(3):217-23. Epub 2014/02/25. doi: ncb2917 [pii] doi: 10.1038/ncb2917 PMID: 24561621.
5. Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol. 2009; 10(7):445-57. Epub 2009/06/24. doi: nrm2720 [pii] doi: 10.1038/nrm2720 PMID: 19546857.
6. Wu SK, Yap AS. Patterns in space: coordinating adhesion and actomyosin contractility at E-cadherin junctions. Cell Commun Adhes. 2013; 20(6):201-12. Epub 2013/11/12. doi: 10.3109/15419061.2013.856889 PMID: 24205985.
7. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ. Deconstructing the cadherin-catenin-actin complex. Cell. 2005; 123(5):889-901. PMID: 16325582.
8. Truong Quang BA, Mani M, Markova O, Lecuit T, Lenne PF. Principles of E-cadherin supramolecular organization in vivo. Curr Biol. 2013; 23(22):2197-207. Epub 2013/11/05. doi: S0960-9822(13)01131-7 [pii] doi: 10.1016/j.cub.2013.09.015 PMID: 24184100.
9. Coscoy S, Waharte F, Gautreau A, Martin M, Louvard D, Mangeat P, et al. Molecular analysis of microscopic ezrin dynamics by two-photon FRAP. Proc Natl Acad Sci U S A. 2002; 99(20):12813-8. PMID: 12271120.
10. Waharte F, Brown CM, Coscoy S, Coudrier E, Amblard F. A two-photon FRAP analysis of the cytoskeleton dynamics in the microvilli of intestinal cells. Biophys J. 2005; 88(2):1467-78. PMID: 15596489.
11. de Beco S, Gueudry C, Amblard F, Coscoy S. Endocytosis is required for E-cadherin redistribution at mature adherens junctions. Proc Natl Acad Sci U S A. 2009; 106(17):7010-5. PMID: 19372377. doi: 10.1073/pnas.0811253106
12. de Beco S, Amblard F, Coscoy S. New insights into the regulation of E-cadherin distribution by endocytosis. Int Rev Cell Mol Biol. 2012; 295:63-108. Epub 2012/03/28. doi: B978-0-12-394306-4.00008-3 [pii] doi: 10.1016/B978-0-12-394306-4.00008-3. PMID: 22449487.
13. Smutny M, Wu SK, Gomez GA, Mangold S, Yap AS, Hamilton NA. Multicomponent Analysis of Junctional Movements Regulated by Myosin II Isoforms at the Epithelial Zonula Adherens. PLoS One. 2011; 6(7):e22458. Epub 2011/07/30. doi: 10.1371/journal.pone.0022458PONE-D-11-04153 [pii]. PMID: 21799860; PubMed Central PMCID: PMC3142163.
14. Martin AC, Kaschube M, Wieschaus EF. Pulsed contractions of an actin-myosin network drive apical constriction. Nature. 2009; 457(7228):495-9. Epub 2008/11/26. doi: nature07522 [pii] doi: 10.1038/nature07522 PMID: 19029882; PubMed Central PMCID: PMC2822715.
15. Solon J, Kaya-Copur A, Colombelli J, Brunner D. Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell. 2009; 137(7):1331-42. Epub 2009/07/01. doi: S0092-8674(09)00394-8 [pii] doi: 10.1016/j.cell.2009.03.050 PMID: 19563762.
16. Cavey M, Rauzi M, Lenne PF, Lecuit T. A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature. 2008; 453(7196):751-6. Epub 2008/05/16. doi: nature06953 [pii] doi: 10.1038/nature06953 PMID: 18480755.
17. Chu YS, Thomas WA, Eder O, Pincet F, Perez E, Thiery JP, et al. Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J Cell Biol. 2004; 167(6):1183-94. Epub 2004/12/15. doi: jcb.200403043 [pii] doi: 10.1083/jcb.200403043 PMID: 15596540; PubMed Central PMCID: PMC2172605.
18. Hong S, Troyanovsky RB, Troyanovsky SM. Spontaneous assembly and active disassembly balance adherens junction homeostasis. Proc Natl Acad Sci U S A. 2010; 107(8):3528-33. Epub 2010/02/06. doi: 0911027107 [pii] doi: 10.1073/pnas.0911027107 PMID: 20133579; PubMed Central PMCID: PMC2840517.
19. Nanes BA, Chiasson-MacKenzie C, Lowery AM, Ishiyama N, Faundez V, Ikura M, et al. p120-catenin binding masks an endocytic signal conserved in classical cadherins. J Cell Biol. 2012; 199(2):365-80. Epub 2012/10/17. doi: jcb.201205029 [pii] doi: 10.1083/jcb.201205029 PMID: 23071156; PubMed Central PMCID: PMC3471230.
20. Warner SJ, Longmore GD. Cdc42 antagonizes Rho1 activity at adherens junctions to limit epithelial cell apical tension. J Cell Biol. 2009; 187(1):119-33. Epub 2009/10/07. doi: jcb.200906047 [pii] doi: 10.1083/jcb.200906047 PMID: 19805632; PubMed Central PMCID: PMC2762093.
21. Yao M, Qiu W, Liu R, Efremov AK, Cong P, Seddiki R, et al. Force-dependent conformational switch of alpha-catenin controls vinculin binding. Nat Commun. 2014; 5:4525. Epub 2014/08/01. doi: ncomms5525 [pii] doi: 10.1038/ncomms5525 PMID: 25077739.
22. Leckband DE, de Rooij J. Cadherin adhesion and mechanotransduction. Annu Rev Cell Dev Biol. 2014; 30:291-315. Epub 2014/07/26. doi: 10.1146/annurev-cellbio-100913-013212 PMID: 25062360.
23. Kim TJ, Zheng S, Sun J, Muhamed I, Wu J, Lei L, et al. Dynamic Visualization of alpha-Catenin Reveals Rapid, Reversible Conformation Switching between Tension States. Curr Biol. 2015; 25(2):218-24. Epub 2014/12/30. doi: S0960-9822(14)01444-4 [pii] doi: 10.1016/j.cub.2014.11.017 PMID: 25544608; PubMed Central PMCID: PMC4302114.
24. Twiss F, Le Duc Q, Van Der Horst S, Tabdili H, Van Der Krogt G, Wang N, et al. Vinculin-dependent Cadherin mechanosensing regulates efficient epithelial barrier formation. Biol Open. 2012; 1 (11):1128-40. Epub 2012/12/06. doi: 10.1242/bio.20122428BIO20122428 [pii]. PMID: 23213393; PubMed Central PMCID: PMC3507192.
25. le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol. 2010; 189(7):1107-15. PMID: 20584916. doi: 10.1083/jcb.201001149
26. Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N, Weis WI, et al. Cell adhesion. The minimal cadherin-catenin complex binds to actin filaments under force. Science. 2014; 346(6209):1254211. Epub 2014/11/02. doi: 346/6209/1254211 [pii] doi: 10.1126/science.1254211 PMID: 25359979.
27. Borghi N, Sorokina M, Shcherbakova OG, Weis WI, Pruitt BL, Nelson WJ, et al. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc Natl Acad Sci U S A. 2012; 109(31):12568-73. Epub 2012/07/18. doi: 1204390109 [pii] doi: 10.1073/pnas.1204390109 PMID: 22802638; PubMed Central PMCID: PMC3411997.
28. Schwarz US, Gardel ML. United we stand: integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J Cell Sci. 2012; 125(Pt 13):3051-60. Epub 2012/07/17. doi: jcs.093716 [pii] doi: 10.1242/jcs.093716 PMID: 22797913; PubMed Central PMCID: PMC3434863.
29. Engl W, Arasi B, Yap LL, Thiery JP, Viasnoff V. Actin dynamics modulate mechanosensitive immobilization of E-cadherin at adherens junctions. Nat Cell Biol. 2014; 16(6):587-94. Epub 2014/05/27. doi: ncb2973 [pii] doi: 10.1038/ncb2973 PMID: 24859003.
30. Dufour S, Mege RM, Thiery JP. alpha-catenin, vinculin, and F-actin in strengthening E-cadherin cellcell adhesions and mechanosensing. Cell Adh Migr. 2013; 7(4):345-50. Epub 2013/06/07. doi: 25139 [pii] doi: 10.4161/cam.25139 PMID: 23739176; PubMed Central PMCID: PMC3739810.
31. Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M. alpha-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol. 2010; 12(6):533-42. PMID: 20453849. doi: 10.1038/ncb2055
32. Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ, Ruiz SA, et al. Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci U S A. 2010; 107(22):9944-9. PMID: 20463286. doi: 10.1073/pnas.0914547107
33. Hong S, Troyanovsky RB, Troyanovsky SM. Binding to F-actin guides cadherin cluster assembly, stability, and movement. J Cell Biol. 2013; 201(1):131-43. Epub 2013/04/03. doi: jcb.201211054 [pii] doi: 10.1083/jcb.201211054 PMID: 23547031; PubMed Central PMCID: PMC3613698.