Cadherin Cad99C is required for normal microvilli morphology in Drosophila follicle cells

Journal of Cell Science

Volumn 119, Issue 6, 2006, Pages 1184-1195

  Schlichting, Karin ^a   Wilsch Bräuninger, Michaela ^a   Demontis, Fabio ^a   Dahmann, Christian ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Cad99C; Cadherin; Drosophila; Microvilli; Protocadherin 15; Vitelline membrane

Indexed keywords

CADHERIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORRELATION ANALYSIS; DROSOPHILA; GENE MUTATION; GENE OVEREXPRESSION; HAIR CELL; HEARING IMPAIRMENT; IMMUNOELECTRON MICROSCOPY; INSECT CELL; MICROVILLUS; MORPHOGENESIS; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STEREOCILIUM; USHER SYNDROME; VITELLINE MEMBRANE;

ANIMALS; CADHERINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; MICROSCOPY, ELECTRON; MICROVILLI; MODELS, MOLECULAR; MUTATION; OVARY;

ANIMALIA; HEXAPODA; INSECTA; VERTEBRATA;

EID: 33645736042     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02831     Document Type: Article

References (63)

1. Ahmed, Z. M., Riazuddin, S., Bernstein, S. L., Ahmed, Z., Khan, S., Griffith, A. J., Morell, R. J., Friedman, T. B. and Wilcox, E. R. (2001). Mutations of the protocadherin gene PCDH15 cause Usher syndrome type 1F. Am. J. Hum. Genet. 69, 25-34.
2. Ahmed, Z. M., Riazuddin, S., Ahmad, J., Bernstein, S. L., Guo, Y., Sabar, M. F., Sieving, P., Griffith, A. J., Friedman, T. B., Belyantseva, I. A. et al. (2003). PCDH15 is expressed in the neurosensory epithelium of the eye and ear and mutant alleles are responsible for both USH1F and DFNB23. Hum. Mol. Genet. 12, 3215-3223.
3. Alagramam, K. N., Murcia, C. L., Kwon, H. Y., Pawlowski, K. S., Wright, C. G. and Woychik, R. P. (2001a). The mouse Ames waltzer hearing-loss mutant is caused by mutation of Pcdh15, a novel protocadherin gene. Nat. Genet. 27, 99-102.
4. Alagramam, K. N., Yuan, H., Kuehn, M. H., Murcia, C. L., Wayne, S., Srisailpathy, C. R., Lowry, R. B., Knaus, R., Van Laer, L., Bernier, F. P. et al. (2001b). Mutations in the novel protocadherin PCDH15 cause Usher syndrome type 1F. Hum. Mol. Genet. 10, 1709-1718.
5. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
6. Angst, B. D., Marcozzi, C. and Magee, A. I. (2001). The cadherin superfamily: diversity in form and function. J. Cell Sci. 114, 629-641.
7. Bartles, J. R., Zheng, L., Li, A., Wierda, A. and Chen, B. (1998). Small espin: a third actin-bundling protein and potential forked protein ortholog in brush border microvilli. J. Cell Biol. 143, 107-119.
8. Boeda, B., El-Amraoui, A., Bahloul, A., Goodyear, R., Daviet, L., Blanchard, S., Perfettini, I., Fath, K. R., Shorte, S., Reiners, J. et al. (2002). Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. EMBO J. 21, 6689-6699.
9. Bolz, H., von Brederlow, B., Ramirez, A., Bryda, E. C., Kutsche, K., Nothwang, H. G., Seeliger, M., del, C.-Salcado Cabrera, M., Vila, M. C., Molina, O. P. et al. (2001). Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat. Genet. 27, 108-112.
10. Bork, J. M., Peters, L. M., Riazuddin, S., Bernstein, S. L., Ahmed, Z. M., Ness, S. L., Polomeno, R., Ramesh, A., Schloss, M., Srisailpathy, C. R. et al. (2001). Usher syndrome 1D and nonsyndromic autosomal recessive deafness DFNB12 are caused by allelic mutations of the novel cadherin-like gene CDH23. Am. J. Hum. Genet. 68, 26-37.
11. 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.
12. Bretscher, A. and Weber, K. (1978). Purification of microvilli and an analysis of the protein components of the microfilament core bundle. Exp. Cell Res. 116, 397-407.
13. Bretscher, A. and Weber, K. (1980). Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures. J. Cell Biol. 86, 335-340.
14. 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.
15. Degelmann, A., Hardy, P. A. and Mahowald, A. P. (1990). Genetic analysis of two female-sterile loci affecting eggshell integrity and embryonic pattern formation in Drosophila melanogaster. Genetics 126, 427-434.
16. Di Palma, F., Holme, R. H., Bryda, E. C., Belyantseva, I. A., Pellegrino, R., Kachar, B., Steel, K. P. and Noben-Trauth, K. (2001). Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat. Genet. 27, 103-107.
17. 2+-dependent F-actin disruption in intestinal brush borders. J. Cell Biol. 146, 819-830.
18. Franck, Z., Footer, M. and Bretscher, A. (1990). Microinjection of villin into cultured cells induces rapid and long-lasting changes in cell morphology but does not inhibit cytokinesis, cell motility, or membrane ruffling. J. Cell Biol. 111, 2475-2485.
19. Friederich, E., Huet, C., Arpin, M. and Louvard, D. (1989). Villin induces microvilli growth and actin redistribution in transfected fibroblasts. Cell 59, 461-475.
20. Frolenkov, G. I., Belyantseva, I. A., Friedman, T. B. and Griffith, A. J. (2004). Genetic insights into the morphogenesis of inner ear hair cells. Nat. Rev. Genet. 5, 489-498.
21. Golic, K. G. and Lindquist, S. (1989). The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509.
22. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell. Biol. 6, 622-634.
23. Heintzelman, M. B. and Mooseker, M. S. (1992). Assembly of the intestinal brush border cytoskeleton. Curr. Top. Dev. Biol. 26, 93-122.
24. Hill, E., Broadbent, I. D., Chothia, C. and Pettitt, J. (2001). Cadherin superfamily proteins in Caenorhabditis elegans and Drosophila melanogaster. J. Mol. Biol. 305, 1011-1124.
25. Hynes, R. O. and Zhao, Q. (2000). The evolution of cell adhesion. J. Cell Biol. 150, F89-F96.
26. Jimenez, G., Gonzalez-Reyes, A. and Casanova, J. (2002). Cell surface proteins Nasrat and Polehole stabilize the Torso-like extracellular determinant in Drosophila oogenesis. Genes Dev. 16, 913-918.
27. King, R. C. (1970). Ovarian development in Drosophila melanogaster. New York: Academic Press.
28. Lagziel, A., Ahmed, Z. M., Schultz, J. M., Morell, R. J., Belyantseva, I. A. and Friedman, T. B. (2005). Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development. Dev. Biol. 280, 295-306.
29. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
30. LeMosy, E. K. and Hashimoto, C. (2000). The nudel protease of Drosophila is required for eggshell biogenesis in addition to embryonic patterning. Dev. Biol. 217, 352-361.
31. Loomis, P. A., Zheng, L., Sekerkova, G., Changyaleket, B., Mugnaini, E. and Bartles, J. R. (2003). Espin cross-links cause the elongation of microvillus-type parallel actin bundles in vivo. J. Cell Biol. 163, 1045-1055.
32. Mahowald, A. P. (1972). Ultrastructural observations on oogenesis in Drosophila. J. Morphol. 137, 29-48.
33. Mahowald, A. P. and Kambysellis, M. P. (1980). Oogenesis. In The Genetics and Biology of Drosophila (ed. M. Ashburner and T. R. F. Wright), pp. 141-224. New York: Academic Press.
34. Margaritis, L. H., Kafatos, F. C. and Petri, W. H. (1980). The eggshell of Drosophila melanogaster. I. Fine structure of the layers and regions of the wild-type eggshell. J. Cell Sci. 43, 1-35.
35. Matsudaira, P. T. and Burgess, D. R. (1979). Identification and organization of the components in the isolated microvillus cytoskeleton. J. Cell Biol. 83, 667-673.
36. Michel, V., Goodyear, R. J., Weil, D., Marcotti, W., Perfettini, I., Wolfrum, U., Kros, C. J., Richardson, G. P. and Petit, C. (2005). Cadherin 23 is a component of the transient lateral links in the developing hair bundles of cochlear sensory cells. Dev. Biol. 280, 281-294.
37. Mooseker, M. S., Graves, T. A., Wharton, K. A., Falco, N. and Howe, C. L. (1980). Regulation of microvillus structure: calcium-dependent isolation and cross-linking of actin filaments in the microvilli of intestinal epithelial cells. J. Cell Biol. 87, 809-822.
38. Oda, H., Uemura, T., Harada, Y., Iwai, Y. and Takeichi, M. (1994). A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 165, 716-726.
39. Papassideri, I. S., Margaritis, L. H. and Gulik-Krzywicki, T. (1993). The eggshell of Drosophila melanogaster. VIII. Morphogenesis of the wax layer during oogenesis. Tissue Cell 25, 929-936.
40. Pascucci, T., Perrino, J., Mahowald, A. P. and Waring, G. L. (1996). Eggshell assembly in Drosophila: processing and localization of vitelline membrane and chorion proteins. Dev. Biol. 177, 590-598.
41. Patel, S. D., Chen, C. P., Bahna, F., Honig, B. and Shapiro, L. (2003). Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13, 690-698.
42. Pignoni, F. and Zipursky, S. L. (1997). Induction of Drosophila eye development by decapentaplegic. Development 124, 271-278.
43. Pinson, K. I., Dunbar, L., Samuelson, L. and Gumucio, D. L. (1998). Targeted disruption of the mouse villin gene does not impair the morphogenesis of microvilli. Dev. Dyn. 211, 109-121.
44. Queenan, A. M., Ghabrial, A. and Schüpbach, T. (1997). Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development 124, 3871-3880.
45. Rzadzinska, A. K., Derr, A., Kachar, B. and Noben-Trauth, K. (2005). Sustained cadherin 23 expression in young and adult cochlea of normal and hearing-impaired mice. Hear. Res. 208, 114-121.
46. Salinas, P. C. and Price, S. R. (2005). Cadherins and catenins in synapse development. Curr. Opin. Neurobiol. 15, 73-80.
47. Savant, S. S. and Waring, G. L. (1989). Molecular analysis and rescue of a vitelline membrane mutant in Drosophila. Dev. Biol. 135, 43-52.
48. Schlichting, K., Demontis, F. and Dahmann, C. (2005). Cadherin Cad99C is regulated by Hedgehog signaling in Drosophila. Dev. Biol. 279, 142-154.
49. Schultz, J., Milpetz, F., Bork, P. and Ponting, C. P. (1998). SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 95, 5857-5864.
50. Seiler, C., Finger-Baier, K. C., Rinner, O., Makhankov, Y. V., Schwarz, H., Neuhauss, S. C. and Nicolson, T. (2005). Duplicated genes with split functions: independent roles of protocadherin 15 orthologues in zebrafish hearing and vision. Development 132, 615-623.
51. Senzaki, K., Ogawa, M. and Yagi, T. (1999). Proteins of the CNR family are multiple receptors for Reelin. Cell 99, 635-647.
52. Sheng, M. and Sala, C. (2001). PDZ domains and the organization of supramolecular complexes. Annu. Rev. Neurosci. 24, 1-29.
53. Siemens, J., Lillo, C., Dumont, R. A., Reynolds, A., Williams, D. S., Gillespie, P. G. and Muller, U. (2004). Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428, 950-955.
54. Spradling, A. C. (1993). Developmental Genetics of Oogenesis. In The Development of Drosophila melanogaster. Vol. 1 (ed. M. Bate and A. Martinez Arias), pp. 1-70. New York: Cold Spring Harbor Laboratory Press.
55. Tepass, U., Truong, K., Godt, D., Ikura, M. and Peifer, M. (2000). Cadherins in embryonic and neural morphogenesis. Nat. Rev. Mol. Cell. Biol. 1, 91-100.
56. Trougakos, I. P., Papassideri, I. S., Waring, G. L. and Margaritis, L. H. (2001). Differential sorting of constitutively co-secreted proteins in the ovarian follicle cells of Drosophila. Eur. J. Cell Biol. 80, 271-284.
57. Tyska, M. J., Mackey, A. T., Huang, J. D., Copeland, N. G., Jenkins, N. A. and Mooseker, M. S. (2005). Myosin-1a is critical for normal brush border structure and composition. Mol. Biol. Cell 16, 2443-2457.
58. Waring, G. L. (2000). Morphogenesis of the eggshell in Drosophila. Int. Rev. Cytol. 198, 67-108.
59. Wheelock, M. J. and Johnson, K. R. (2003). Cadherin-mediated cellular signaling. Curr. Opin. Cell Biol. 15, 509-514.
60. Wilsch-Bräuninger, M., Schwarz, H. and Nüsslein-Volhard, C. (1997). A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis. J. Cell Biol. 139, 817-829.
61. Wilson, I. A., Niman, H. L., Houghten, R. A., Cherenson, A. R., Connolly, M. L. and Lerner, R. A. (1984). The structure of an antigenic determinant in a protein. Cell 37, 767-778.
62. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
63. Yagi, T. and Takeichi, M. (2000). Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev. 14, 1169-1180.