Cadherin 99C regulates apical expansion and cell rearrangement during epithelial tube elongation

Development (Cambridge)

Volumn 141, Issue 9, 2014, Pages 1950-1960

  Chung, SeYeon ^a   Andrew, Deborah J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apicobasal polarity; Drosophila; Epithelial organ development; Salivary gland; Tubulogenesis

Indexed keywords

CADHERIN; CADHERIN 99C PROTEIN; MEMBRANE PROTEIN; STRANDED AT SECOND PROTEIN; UNCLASSIFIED DRUG;

APICAL MEMBRANE; ARTICLE; CELL ACTIVITY; CELL EXPANSION; CELL REARRANGEMENT; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EPITHELIAL TUBE ELONGATION; LOSS OF FUNCTION MUTATION; NONHUMAN; ORGANOGENESIS; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; USHER SYNDROME;

APICOBASAL POLARITY; DROSOPHILA; EPITHELIAL ORGAN DEVELOPMENT; SALIVARY GLAND; TUBULOGENESIS;

ANIMALS; CADHERINS; CELL MEMBRANE; CELL NUCLEUS; CELL POLARITY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EPITHELIAL CELLS; EPITHELIUM; EXTRACELLULAR MATRIX; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SALIVARY GLANDS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84899647270     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.104166     Document Type: Article

References (56)

1. Baumgartner, S., Littleton, J. T., Broadie, K., Bhat, M. A., Harbecke, R., Lengyel, J. A., Chiquet-Ehrismann, R., Prokop, A. and Bellen, H. J. (1996). A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87, 1059-1068.
2. Bilder, D. and Perrimon, N. (2000). Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403, 676-680.
3. Bökel, C., Prokop, A. and Brown, N. H. (2005). Papillote and Piopio: drosophila ZP-domain proteins required for cell adhesion to the apical extracellular matrix and microtubule organization. J. Cell Sci. 118, 633-642.
4. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
5. Broadie, K., Baumgartner, S. and Prokop, A. (2011). Extracellular matrix and its receptors in Drosophila neural development. Dev. Neurobiol. 71, 1102-1130.
6. Coutelis, J.-B. and Ephrussi, A. (2007). Rab6 mediates membrane organization and determinant localization during Drosophila oogenesis. Development 134, 1419-1430.
7. D'Alterio, C., Tran, D. D. D., Au Yeung, M. W. Y., Hwang, M. S. H., Li, M. A., Arana, C. J., Mulligan, V. K., Kubesh, M., Sharma, P., Chase, M. et al. (2005). Drosophila melanogaster Cad99C, the orthologue of human Usher cadherin PCDH15, regulates the length of microvilli. J. Cell Biol. 171, 549-558.
8. Del Nery, E., Miserey-Lenkei, S., Falguières, T., Nizak, C., Johannes, L., Perez, F. and Goud, B. (2006). Rab6A and Rab6A' GTPases play non-overlapping roles in membrane trafficking. Traffic 7, 394-407.
9. Godyna, S., Liau, G., Popa, I., Stefansson, S. and Argraves, W. S. (1995). Identification of the low density lipoprotein receptor-related protein (LRP) as an endocytic receptor for thrombospondin-1. J. Cell Biol. 129, 1403-1410.
10. Henderson, K. D. and Andrew, D. J. (2000). Regulation and function of Scr, exd, and hth in the Drosophila salivary gland. Dev. Biol. 217, 362-374.
11. Hynes, R. O. and Zhao, Q. (2000). The evolution of cell adhesion. J. Cell Biol. 150, F89-F96.
12. Ismat, A., Cheshire, A. M. and Andrew, D. J. (2013). The secreted AdamTS-A metalloprotease is required for collective cell migration. Development 140, 1981-1993.
13. Januschke, J., Nicolas, E., Compagnon, J., Formstecher, E., Goud, B. and Guichet, A. (2007). Rab6 and the secretory pathway affect oocyte polarity in Drosophila. Development 134, 3419-3425.
14. Jaźwińska, A., Ribeiro, C. and Affolter, M. (2003). Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat. Cell Biol. 5, 895-901.
15. Kerman, B. E., Cheshire, A. M., Myat, M. M. and Andrew, D. J. (2008). Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. Dev. Biol. 320, 278-288.
16. Lamb, R. S., Ward, R. E., Schweizer, L. and Fehon, R. G. (1998). Drosophila coracle, a member of the protein 4. 1 superfamily, has essential structural functions in the septate junctions and developmental functions in embryonic and adult epithelial cells. Mol. Biol. Cell 9, 3505-3519.
17. Laprise, P. and Tepass, U. (2011). Novel insights into epithelial polarity proteins in Drosophila. Trends Cell Biol. 21, 401-408.
18. Laval, M., Bel, C. and Faivre-Sarrailh, C. (2008). The lateral mobility of cell adhesion molecules is highly restricted at septate junctions in Drosophila. BMC Cell Biol. 9, 38.
19. Lee, H.-K., Cording, A., Vielmetter, J. and Zinn, K. (2013). Interactions between a receptor tyrosine phosphatase and a cell surface ligand regulate axon guidance and glial-neuronal communication. Neuron 78, 813-826.
20. Lehmann, R. and Tautz, D. (1994). In situ hybridization to RNA. Methods Cell Biol. 44, 575-598.
21. Lewis, R., Kaufman, T., Denell, R. and Tallerico, P. (1980). Genetic analysis of the Antennapedia gene complex (ANT-C) and adjacent chromosomal regions of Drosophila melanogaster. Genetics 95, 367-381.
22. Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B. and Johannes, L. (2002). Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156, 653-664.
23. Martinez, O., Schmidt, A., Salaméro, J., Hoflack, B., Roa, M. and Goud, B. (1994). The small GTP-binding protein rab6 functions in intra-Golgi transport. J. Cell Biol. 127, 1575-1588.
24. Martinez, O., Antony, C., Pehau-Arnaudet, G., Berger, E. G., Salamero, J. and Goud, B. (1997). GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 94, 1828-1833.
25. Maruyama, R. and Andrew, D. J. (2012). Drosophila as a model for epithelial tube formation. Dev. Dyn. 241, 119-135.
26. McDonald, K. L. and Auer, M. (2006). High-pressure freezing, cellular tomography, and structural cell biology. Biotechniques 41, 137-143.
27. McDonald, K. and Morphew, M. K. (1993). Improved preservation of ultrastructure in difficult-to-fix organisms by high pressure freezing and freeze substitution: I. Drosophila melanogaster and Strongylocentrotus purpuratus embryos. Microsc. Res. Tech. 24, 465-473.
28. Memmo, L. M. and McKeown-Longo, P. (1998). The alpha v beta 5 integrin functions as an endocytic receptor for vitronectin. J. Cell Sci. 111, 425-433.
29. Nelson, K. S., Furuse, M. and Beitel, G. J. (2010). The Drosophila Claudin Kunekune is required for septate junction organization and tracheal tube size control. Genetics 185, 831-839.
30. Opdam, F. J., Echard, A., Croes, H. J., van den Hurk, J. A., van de Vorstenbosch, R. A., Ginsel, L. A., Goud, B. and Fransen, J. A. (2000). The small GTPase Rab6B, a novel Rab6 subfamily member, is cell-type specifically expressed and localised to the Golgi apparatus. J. Cell Sci. 113, 2725-2735.
31. Paul, S. M., Ternet, M., Salvaterra, P. M. and Beitel, G. J. (2003). The Na+/K+ ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 130, 4963-4974.
32. Peifer, M., Orsulic, S., Sweeton, D. and Wieschaus, E. (1993). A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 118, 1191-1207.
33. Pelissier, A., Chauvin, J.-P. and Lecuit, T. (2003). Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr. Biol. 13, 1848-1857.
34. Rousso, T., Shewan, A. M., Mostov, K. E., Schejter, E. D. and Shilo, B.-Z. (2013). Apical targeting of the formin Diaphanous in Drosophila tubular epithelia. Elife 2, e00666.
35. Saraste, J. and Goud, B. (2007). Functional symmetry of endomembranes. Mol. Biol. Cell 18, 1430-1436.
36. Satoh, A. K., O'Tousa, J. E., Ozaki, K. and Ready, D. F. (2005). Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132, 1487-1497.
37. Schlichting, K., Demontis, F. and Dahmann, C. (2005). Cadherin Cad99C is regulated by Hedgehog signaling in Drosophila. Dev. Biol. 279, 142-154.
38. Schlichting, K., Wilsch-Bräuninger, M., Demontis, F. and Dahmann, C. (2006). Cadherin Cad99C is required for normal microvilli morphology in Drosophila follicle cells. J. Cell Sci. 119, 1184-1195.
39. Schonbaum, C. P., Organ, E. L., Qu, S. and Cavener, D. R. (1992). The Drosophila melanogaster stranded at second (sas) gene encodes a putative epidermal cell surface receptor required for larval development. Dev. Biol. 151, 431-445.
40. Shiga, Y., Tanaka-Matakatsu, M. and Hayashi, S. (1996). A nuclear GFP/betagalactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ. 38, 99-106.
41. St. Johnston, D. and Ahringer, J. (2010). Cell polarity in eggs and epithelia: parallels and diversity. Cell 141, 757-774.
42. St. Pierre, S. E., Ponting, L., Stefancsik, R. and McQuilton, P.; the FlyBase Consortium (2014). FlyBase 102-advanced approaches to interrogating FlyBase. Nucleic Acids Res. 42, D780-D788.
43. Strand, D., Raska, I. and Mechler, B. M. (1994). The Drosophila lethal(2)giant larvae tumor suppressor protein is a component of the cytoskeleton. J. Cell Biol. 127, 1345-1360.
44. Strickland, L. I. and Burgess, D. R. (2004). Pathways for membrane trafficking during cytokinesis. Trends Cell Biol. 14, 115-118.
45. Tanentzapf, G., Smith, C., McGlade, J. and Tepass, U. (2000). Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis. J. Cell Biol. 151, 891-904.
46. Tepass, U. (1996). Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev. Biol. 177, 217-225.
47. Tepass, U. (2012). The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu. Rev. Cell Dev. Biol. 28, 655-685.
48. von Stein, W., Ramrath, A., Grimm, A., Müller-Borg, M. and Wodarz, A. (2005). Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling. Development 132, 1675-1686.
49. Walther, P. and Ziegler, A. (2002). Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J. Microsc. 208, 3-10.
50. Wienke, D., MacFadyen, J. R. and Isacke, C. M. (2003). Identification and characterization of the endocytic transmembrane glycoprotein Endo180 as a novel collagen receptor. Mol. Biol. Cell 14, 3592-3604.
51. Wodarz, A., Hinz, U., Engelbert, M. and Knust, E. (1995). Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67-76.
52. Wodarz, A., Ramrath, A., Grimm, A. and Knust, E. (2000). Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150, 1361-1374.
53. Wolfstetter, G. and Holz, A. (2012). The role of LamininB2 (LanB2) during mesoderm differentiation in Drosophila. Cell Mol. Life Sci. 69, 267-282.
54. Woods, D. F. and Bryant, P. J. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451-464.
55. Wu, V. M., Schulte, J., Hirschi, A., Tepass, U. and Beitel, G. J. (2004). Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J. Cell Biol. 164, 313-323.
56. Zhang, L. and Ward, R. E. (2009). uninflatable encodes a novel ectodermal apical surface protein required for tracheal inflation in Drosophila. Dev. Biol. 336, 201-212.