Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity
Planar cell polarity (PCP) information is a critical determinant of organ morphogenesis. While PCP in bounded epithelial sheets is increasingly well understood, how PCP is organized in tubular and acinar tissues is not. Drosophila egg chambers (follicles) are an acinus-like “edgeless epithelium” and...
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| Format: | Article |
| Language: | English |
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Elsevier
2016-05-01
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| Series: | Cell Reports |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124716304272 |
| _version_ | 1818938669750288384 |
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| author | Dong-Yuan Chen Katherine R. Lipari Yalda Dehghan Sebastian J. Streichan David Bilder |
| author_facet | Dong-Yuan Chen Katherine R. Lipari Yalda Dehghan Sebastian J. Streichan David Bilder |
| author_sort | Dong-Yuan Chen |
| collection | DOAJ |
| description | Planar cell polarity (PCP) information is a critical determinant of organ morphogenesis. While PCP in bounded epithelial sheets is increasingly well understood, how PCP is organized in tubular and acinar tissues is not. Drosophila egg chambers (follicles) are an acinus-like “edgeless epithelium” and exhibit a continuous, circumferential PCP that does not depend on pathways active in bounded epithelia; this follicle PCP directs formation of an ellipsoid rather than a spherical egg. Here, we apply an imaging algorithm to “unroll” the entire 3D tissue surface and comprehensively analyze PCP onset. This approach traces chiral symmetry breaking to plus-end polarity of microtubules in the germarium, well before follicles form and rotate. PCP germarial microtubules provide chiral information that predicts the direction of whole-tissue rotation as soon as independent follicles form. Concordant microtubule polarity, but not microtubule alignment, requires the atypical cadherin Fat2, which acts at an early stage to translate plus-end bias into coordinated actin-mediated collective cell migration. Because microtubules are not required for PCP or migration after follicle rotation initiates, while dynamic actin and extracellular matrix are, polarized microtubules lie at the beginning of a handoff mechanism that passes early chiral PCP of the cytoskeleton to a supracellular planar polarized extracellular matrix and elongates the organ. |
| first_indexed | 2024-12-20T06:11:32Z |
| format | Article |
| id | doaj.art-d32e1f27cd6b4b2abe34c90b1b9c078f |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-12-20T06:11:32Z |
| publishDate | 2016-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-d32e1f27cd6b4b2abe34c90b1b9c078f2022-12-21T19:50:41ZengElsevierCell Reports2211-12472016-05-011561125113310.1016/j.celrep.2016.04.014Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule PolarityDong-Yuan Chen0Katherine R. Lipari1Yalda Dehghan2Sebastian J. Streichan3David Bilder4Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720-3200, USADepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720-3200, USADepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720-3200, USAKavli Institute of Theoretical Physics, University of California, Santa Barbara, Santa Barbara, CA 93106, USADepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720-3200, USAPlanar cell polarity (PCP) information is a critical determinant of organ morphogenesis. While PCP in bounded epithelial sheets is increasingly well understood, how PCP is organized in tubular and acinar tissues is not. Drosophila egg chambers (follicles) are an acinus-like “edgeless epithelium” and exhibit a continuous, circumferential PCP that does not depend on pathways active in bounded epithelia; this follicle PCP directs formation of an ellipsoid rather than a spherical egg. Here, we apply an imaging algorithm to “unroll” the entire 3D tissue surface and comprehensively analyze PCP onset. This approach traces chiral symmetry breaking to plus-end polarity of microtubules in the germarium, well before follicles form and rotate. PCP germarial microtubules provide chiral information that predicts the direction of whole-tissue rotation as soon as independent follicles form. Concordant microtubule polarity, but not microtubule alignment, requires the atypical cadherin Fat2, which acts at an early stage to translate plus-end bias into coordinated actin-mediated collective cell migration. Because microtubules are not required for PCP or migration after follicle rotation initiates, while dynamic actin and extracellular matrix are, polarized microtubules lie at the beginning of a handoff mechanism that passes early chiral PCP of the cytoskeleton to a supracellular planar polarized extracellular matrix and elongates the organ.http://www.sciencedirect.com/science/article/pii/S2211124716304272 |
| spellingShingle | Dong-Yuan Chen Katherine R. Lipari Yalda Dehghan Sebastian J. Streichan David Bilder Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity Cell Reports |
| title | Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity |
| title_full | Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity |
| title_fullStr | Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity |
| title_full_unstemmed | Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity |
| title_short | Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity |
| title_sort | symmetry breaking in an edgeless epithelium by fat2 regulated microtubule polarity |
| url | http://www.sciencedirect.com/science/article/pii/S2211124716304272 |
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