© The Rockefeller University Press,
0021-9525/1999//1075 $5.00
The Journal of Cell Biology, Volume 146, Number 5,
, 1999 1075-1086
Apical Spectrin Is Essential for Epithelial Morphogenesis but Not Apicobasal Polarity in Drosophila
Daniela C. Zarnescua,b and
Graham H. Thomasa,b
a Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802
b Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802
Departments of Biology and of Biochemistry and Molecular Biology, The Pennsylvania State University, 208 Erwin W. Mueller Laboratory, University Park, PA 16802.(814) 865-9131(814) 863-0716
gxt5{at}psu.edu
Changes in cell shape and position drive morphogenesis in epithelia and depend on the polarized nature of its constituent cells. The spectrin-based membrane skeleton is thought to be a key player in the establishment and/or maintenance of cell shape and polarity. We report that apical βHeavy-spectrin (βH), a terminal web protein that is also associated with the zonula adherens, is essential for normal epithelial morphogenesis of the Drosophila follicle cell epithelium during oogenesis. Elimination of βH by the karst mutation prevents apical constriction of the follicle cells during mid-oogenesis, and is accompanied by a gross breakup of the zonula adherens. We also report that the integrity of the migratory border cell cluster, a group of anterior follicle cells that delaminates from the follicle epithelium, is disrupted.
Elimination of βH prevents the stable recruitment of
-spectrin to the apical domain, but does not result in a loss of apicobasal polarity, as would be predicted from current models describing the role of spectrin in the establishment of cell polarity. These results demonstrate a direct role for apical (
βH)2-spectrin in epithelial morphogenesis driven by apical contraction, and suggest that apical and basolateral spectrin do not play identical roles in the generation of apicobasal polarity.
Key Words: spectrin oogenesis cell polarity zonula adherens morphogenesis
© 1999 The Rockefeller University Press
1.used in this paper: βH, βHeavy-spectrin; SBMS, spectrin-based membrane skeleton; ZA, zonula adherens

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Weber, K. L., Fischer, R. S., Fowler, V. M.
(2007). Tmod3 regulates polarized epithelial cell morphology. J. Cell Sci.
120: 3625-3632
[Abstract]
[Full Text]
-
Grammont, M.
(2007). Adherens junction remodeling by the Notch pathway in Drosophila melanogaster oogenesis. JCB
177: 139-150
[Abstract]
[Full Text]
-
Hulsmeier, J., Pielage, J., Rickert, C., Technau, G. M., Klambt, C., Stork, T.
(2007). Distinct functions of {alpha}-Spectrin and {beta}-Spectrin during axonal pathfinding. Development
134: 713-722
[Abstract]
[Full Text]
-
Tian, E, Hagen, K. G. T.
(2007). A UDP-GalNAc:Polypeptide N-Acetylgalactosaminyltransferase Is Required for Epithelial Tube Formation. J. Biol. Chem.
282: 606-614
[Abstract]
[Full Text]
-
Phillips, M. D., Thomas, G. H.
(2006). Brush border spectrin is required for early endosome recycling in Drosophila. J. Cell Sci.
119: 1361-1370
[Abstract]
[Full Text]
-
Szafranski, P., Goode, S.
(2004). A Fasciclin 2 morphogenetic switch organizes epithelial cell cluster polarity and motility. Development
131: 2023-2036
[Abstract]
[Full Text]
-
Ghosh-Roy, A., Kulkarni, M., Kumar, V., Shirolikar, S., Ray, K.
(2004). Cytoplasmic Dynein-Dynactin Complex Is Required for Spermatid Growth but Not Axoneme Assembly in Drosophila. Mol. Biol. Cell
15: 2470-2483
[Abstract]
[Full Text]
-
Kroschewski, R.
(2004). Molecular Mechanisms of Epithelial Polarity: About Shapes, Forces, and Orientation Problems. Physiology
19: 61-66
[Abstract]
[Full Text]
-
Williams, J. A., MacIver, B., Klipfell, E. A., Thomas, G. H.
(2004). The C-terminal domain of Drosophila {beta}Heavy-spectrin exhibits autonomous membrane association and modulates membrane area. J. Cell Sci.
117: 771-782
[Abstract]
[Full Text]
-
Szuplewski, S., Kottler, B., Terracol, R.
(2003). The Drosophila bZIP transcription factor Vrille is involved in hair and cell growth. Development
130: 3651-3662
[Abstract]
[Full Text]
-
Hemphala, J., Uv, A., Cantera, R., Bray, S., Samakovlis, C.
(2003). Grainy head controls apical membrane growth and tube elongation in response to Branchless/FGF signalling. Development
130: 249-258
[Abstract]
[Full Text]
-
Roper, K., Gregory, S. L., Brown, N. H.
(2002). The `Spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J. Cell Sci.
115: 4215-4225
[Abstract]
[Full Text]
-
Medina, E., Williams, J., Klipfell, E., Zarnescu, D., Thomas, G., Le Bivic, A.
(2002). Crumbs interacts with moesin and {beta}Heavy-spectrin in the apical membrane skeleton of Drosophila. JCB
158: 941-951
[Abstract]
[Full Text]
-
Besse, F., Busson, D., Pret, A.-M.
(2002). Fused-dependent Hedgehog signal transduction is required for somatic cell differentiation during Drosophila egg chamber formation. Development
129: 4111-4124
[Abstract]
[Full Text]
-
Harden, N., Ricos, M., Yee, K., Sanny, J., Langmann, C., Yu, H., Chia, W., Lim, L.
(2002). Drac1 and Crumbs participate in amnioserosa morphogenesis during dorsal closure in Drosophila. J. Cell Sci.
115: 2119-2129
[Abstract]
[Full Text]
-
Norman, K. R., Moerman, D. G.
(2002). {alpha} spectrin is essential for morphogenesis and body wall muscle formation in Caenorhabditis elegans. JCB
157: 665-677
[Abstract]
[Full Text]
-
Bennett, V., Baines, A. J.
(2001). Spectrin and Ankyrin-Based Pathways: Metazoan Inventions for Integrating Cells Into Tissues. Physiol. Rev.
81: 1353-1392
[Abstract]
[Full Text]
-
MacDougall, N, Lad, Y, Wilkie, G., Francis-Lang, H, Sullivan, W, Davis, I
(2001). Merlin, the Drosophila homologue of neurofibromatosis-2, is specifically required in posterior follicle cells for axis formation in the oocyte. Development
128: 665-673
[Abstract]
-
Tanentzapf, G., Smith, C., McGlade, J., Tepass, U.
(2000). Apical, Lateral, and Basal Polarization Cues Contribute to the Development of the Follicular Epithelium during Drosophila Oogenesis. JCB
151: 891-904
[Abstract]
[Full Text]
-
Sisson, J. C., Field, C., Ventura, R., Royou, A., Sullivan, W.
(2000). Lava Lamp, a Novel Peripheral Golgi Protein, Is Required for Drosophila melanogaster Cellularization. JCB
151: 905-918
[Abstract]
[Full Text]
-
Hunter, C., Wieschaus, E.
(2000). Regulated Expression of nullo Is Required for the Formation of Distinct Apical and Basal Adherens Junctions in the Drosophila Blastoderm. JCB
150: 391-402
[Abstract]
[Full Text]
-
Moorthy, S., Chen, L., Bennett, V.
(2000). Caenorhabditis elegans {beta}-G Spectrin Is Dispensable for Establishment of Epithelial Polarity, but Essential for Muscular and Neuronal Function. JCB
149: 915-930
[Abstract]
[Full Text]