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Increased Cell Bond Tension Governs Cell Sorting at the Drosophila Anteroposterior Compartment Boundary

2009; Elsevier BV; Volume: 19; Issue: 22 Linguagem: Inglês

10.1016/j.cub.2009.10.021

1879-0445

Katharina P. Landsberg, Reza Farhadifar, Jonas Ranft, Daiki Umetsu, Thomas J. Widmann, Thomas Bittig, Amani Said, Frank Jülicher, Christian Dahmann,

Hippo pathway signaling and YAP/TAZ

Subdividing proliferating tissues into compartments is an evolutionarily conserved strategy of animal development [1Blair S.S. Lineage compartments in Drosophila.Curr. Biol. 2003; 13: R548-R551Abstract Full Text Full Text PDF PubMed Google Scholar, 2Dahmann C. Basler K. Compartment boundaries: At the edge of development.Trends Genet. 1999; 15: 320-326Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar, 3Irvine K.D. Rauskolb C. Boundaries in development: Formation and function.Annu. Rev. Cell Dev. Biol. 2001; 17: 189-214Crossref PubMed Scopus (172) Google Scholar, 4McNeill H. Sticking together and sorting things out: Adhesion as a force in development.Nat. Rev. Genet. 2000; 1: 100-108Crossref PubMed Scopus (47) Google Scholar, 5Tepass U. Godt D. Winklbauer R. Cell sorting in animal development: Signalling and adhesive mechanisms in the formation of tissue boundaries.Curr. Opin. Genet. Dev. 2002; 12: 572-582Crossref PubMed Scopus (119) Google Scholar, 6Vincent J.P. Compartment boundaries: Where, why and how?.Int. J. Dev. Biol. 1998; 42: 311-315PubMed Google Scholar]. Signals across boundaries between compartments can result in local expression of secreted proteins organizing growth and patterning of tissues [1Blair S.S. Lineage compartments in Drosophila.Curr. Biol. 2003; 13: R548-R551Abstract Full Text Full Text PDF PubMed Google Scholar, 2Dahmann C. Basler K. Compartment boundaries: At the edge of development.Trends Genet. 1999; 15: 320-326Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar, 3Irvine K.D. Rauskolb C. Boundaries in development: Formation and function.Annu. Rev. Cell Dev. Biol. 2001; 17: 189-214Crossref PubMed Scopus (172) Google Scholar, 4McNeill H. Sticking together and sorting things out: Adhesion as a force in development.Nat. Rev. Genet. 2000; 1: 100-108Crossref PubMed Scopus (47) Google Scholar, 5Tepass U. Godt D. Winklbauer R. Cell sorting in animal development: Signalling and adhesive mechanisms in the formation of tissue boundaries.Curr. Opin. Genet. Dev. 2002; 12: 572-582Crossref PubMed Scopus (119) Google Scholar, 6Vincent J.P. Compartment boundaries: Where, why and how?.Int. J. Dev. Biol. 1998; 42: 311-315PubMed Google Scholar]. Sharp and straight interfaces between compartments are crucial for stabilizing the position of such organizers and therefore for precise implementation of body plans. Maintaining boundaries in proliferating tissues requires mechanisms to counteract cell rearrangements caused by cell division; however, the nature of such mechanisms remains unclear. Here we quantitatively analyzed cell morphology and the response to the laser ablation of cell bonds in the vicinity of the anteroposterior compartment boundary in developing Drosophila wings. We found that mechanical tension is approximately 2.5-fold increased on cell bonds along this compartment boundary as compared to the remaining tissue. Cell bond tension is decreased in the presence of Y-27632 [7Uehata M. Ishizaki T. Satoh H. Ono T. Kawahara T. Morishita T. Tamakawa H. Yamagami K. Inui J. Maekawa M. et al.Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension.Nature. 1997; 389: 990-994Crossref PubMed Scopus (2465) Google Scholar], an inhibitor of Rho-kinase whose main effector is Myosin II [8Winter C.G. Wang B. Ballew A. Royou A. Karess R. Axelrod J.D. Luo L. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton.Cell. 2001; 105: 81-91Abstract Full Text Full Text PDF PubMed Scopus (438) Google Scholar]. Simulations using a vertex model [9Farhadifar R. Roper J.C. Aigouy B. Eaton S. Julicher F. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing.Curr. Biol. 2007; 17: 2095-2104Abstract Full Text Full Text PDF PubMed Scopus (643) Google Scholar] demonstrate that a 2.5-fold increase in local cell bond tension suffices to guide the rearrangement of cells after cell division to maintain compartment boundaries. Our results provide a physical mechanism in which the local increase in Myosin II-dependent cell bond tension directs cell sorting at compartment boundaries.