Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea

Development

Volumn 130, Issue 11, 2003, Pages 2375-2384

  Dabdoub, Alain ^a   Donohue, Maura J ^a   Brennan, Angela ^b   Wolf, Vladimir ^a   Montcouquiol, Mireille ^a   Sassoon, David A ^c   Hseih, Jen Chih ^d   Rubin, Jeffrey S ^a   Salinas, Patricia C ^b   Kelley, Matthew W ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

Mechanosensory hair cells; Mouse; Organ of Corti; Planar polarity; Sensory epithelium

Indexed keywords

MEMBRANE PROTEIN; MUTANT PROTEIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; CELL MATURATION; CELL POLARITY; CILIATED EPITHELIUM; COCHLEA; CONTROLLED STUDY; EMBRYO; HAIR CELL; IN VITRO STUDY; MAMMAL; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; CARRIER PROTEINS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; HAIR CELLS, OUTER; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED ICR; MUTATION; PROTEINS; PROTO-ONCOGENE PROTEINS; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; WNT PROTEINS; ZEBRAFISH PROTEINS;

ANIMALIA; MAMMALIA;

EID: 12444329708     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00448     Document Type: Review

References (70)

1. Adler, P. N. (2002). Planar signaling and morphogenesis in Drosophila. Dev. Cell 2, 525-535.
2. Adler, P. N. and Lee, H. (2001). Frizzled signaling and cell-cell interactions in planar polarity. Curr. Opin. Cell Biol. 13, 635-640.
3. Baeg, G. H., Lin, X., Khare, N., Baumgartner, S. and Perrimon, N. (2001). Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development 128, 87-94.
4. Bafico, A., Gazit, A., Pramila, T., Finch, P. W., Yaniv, A. and Aaronson, S. A. (1999). Interaction of frizzled related protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling. J. Biol. Chem. 274, 16180-16187.
5. Bejsovec, A. (2000). Wnt signaling: an embarrassment of receptors. Curr. Biol. 10, R919-R922.
6. Belyantseva, I. A., Adler, H. I., Curi, R., Frolenkov, G. I. and Kachar, B. (2000). Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J. Neurosci. 20, RC116 (1-5).
7. Bergwitz, C., Wendlandt, T., Kispert, A. and Brabant, G. (2001). Wnts differentially regulate colony growth and differentiation of chondrogenic rat calvaria cells. Biochim. Biophys. Acta 1538, 129-140.
8. Blanton, S. H., Liang, C. Y., Cai, M. W., Pandya, A., Du, L. L., Landa, B., Mummalanni, S., Li, K. S., Chen, Z. Y., Qin, X. N. et al. (2002). A novel locus for autosomal dominant non-syndromic deafness (DFNA41) maps to chromosome 12q24-qter. J. Med. Genet. 39, 567-570.
9. Bolz, H., von Brederlow, B., Ramirez, A., Bryda, E. C., Kutsche, K., Nothwang, H. G., Seeliger, M., del Salcedo Cabrera, M., Vila, M. C., Molina, O. P., Gal, A. and Kubisch, C. (2001). Mutation of CDH 23, 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. Comis, S. D., Pickles, J. O., Osborne, M. P. and Pepper, C. B. (1989). Tiplink organization in anomalously-oriented hair cells of the guinea pig cochlea. Hear. Res. 40, 205-211.
12. Cotanche, D. A. and Corwin, J. T. (1991). Stereociliary bundles reorient during hair cell development and regeneration in the chick cochlea. Hear. Res. 52, 379-402.
13. Daudet, N., Ripoll, C., Moles, J. P. and Rebillard, G. (2002). Expression of Wnt and Frizzled gene families in the postnatal rat cochlea. Mol. Brain Res. 105, 98-107.
14. Denman-Johnson, K. and Forge, A. (1999). Establishment of hair bundle polarity and orientation in the developing vestibular system of the mouse. J. Neurocytol. 28, 821-835.
15. Dhoot, G. K., Gustafsson, M. K., Ai, X., Sun, W., Standiford, D. M. and Emerson, C. P., Jr (2001). Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293, 1663-1666.
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. Finch, P. W., He, X., Kelley, M. J., Uren, A., Schaudies, R. P., Popescu, N. C., Rudikoff, S., Aaronson, S. A., Varmus, H. E. and Rubin, J. S. (1997). Purification and molecular cloning of a secreted, Frizzled-related antagonist of Wnt action. Proc. Natl. Acad. Sci. USA 94, 6770-6775.
18. Fujita, H. (1990). Mutant golden hamsters with an abnormal outer hair cell stereociliary arrangement. Hear. Res. 44, 63-69.
19. Fujita, H. and Orita, Y. (1988). An inner ear anomaly in golden hamsters. Am. J. Otolaryngol. 9, 224-231.
20. Furness, D. N., Hackney, C. M. and Hynd, A. N. (1990). Rotated stereociliary bundles and their relationship with the tectorial membrane in the guinea pig cochlea. Acta Otolaryngol. 109, 66-75.
21. Gavin, B. J., McMahon, J. A. and McMahon, A. P. (1990). Expression of multiple novel Wnt-1/int-1-related genes during fetal and adult mouse development. Genes Dev. 4, 2319-2332.
22. Giráldez, A. J., Copley, R. R. and Cohen, S. M. (2002). HSPG modification by the secreted enzyme notum shapes the wingless morphogen gradient. Dev. Cell 2, 667-676.
23. Haddon, C., Mowbray, C., Whitfield, T., Jones, D., Gschmeissner, S. and Lewis, J. (1999). Hair cells without supporting cells: further studies in the ear of the zebrafish mind bomb mutant. J. Neurocytol. 28, 837-850.
24. Hall, A. C., Lucas, F. R. and Salinas, P. C. (2000). Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling, Cell 100, 525-535.
25. Huelsken, J. and Birchmeier, W. (2001). New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Gene. Dev. 11, 547-553.
26. Hsieh, C.-J., Kodjabachian, L., Rebbert, M. L., Rattner, A., Smallwood, P. M., Samos, C. H., Nusse, R., Dawid, I. B. and Nathans, J. (1999). A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 398, 431-436.
27. Kaufman, M. H. (1992). The Atlas of Mouse Development. San Diego, CA: Academic Press.
28. Kelley, M. W., Xu, X. M., Wagner, M. A., Warchol, M. E. and Corwin, J. T. (1993). The developing organ of Corti contains retinoic acid and forms supernumerary hair cells in response to exogenous retinoic acid in culture. Development 119, 1041-1053.
29. Kelley, M. W. and Bianchi, L. M. (2001). Development and neural innervation of the organ of Corti. In: Handbook of the Mouse Auditory Research: From Behavior to Molecular Biology (ed. J. F. Willcott), pp. 137-156. New York: CRC Press.
30. Kengaku, M., Capdevila, J., Rodriguez-Esteban, C., de la Pena, J., Johnson, R. L., Belmonte, J. C. and Tabin, C. J. (1998). Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280, 1274-1277.
31. Kispert, A., Vainio, S., Shen, L., Rowitch, D. H. and McMahon, A. P. (1996). Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. Development 122, 3627-3637.
32. Lanford, P. J., Lan, Y., Jiang, R., Lindsell, C., Weinmaster, G., Gridley, T. and Kelley, M. W. (1999). Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat. Genet. 21, 289-292.
33. Lewis, J. and Davies, A. (2002). Planar cell polarity in the inner ear: how do hair cells acquire their oriented structure? J. Neurobiol. 53, 190-201.
34. Leyns, L., Bouwmeester, T., Kim, S. H., Piccolo, S. and de Robertis, E. M. 1997). Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88, 747-756.
35. Lim, D. J. and Anniko, M. (1985). Developmental morphology of the mouse inner ear. A scanning electron microscopic observation. Acta Otolaryngol. Suppl. 422, 1-69.
36. Lin, X. and Perrimon, N. (1999). Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signaling. Nature 400, 281-284.
37. Ma, D., Yang, C.-H., McNeill, H., Simon, M. A. and Axelrod, J. D. (2003). Fidelity in planar cell polarity signaling. Nature 421, 543-547.
38. 2+ pathways. Oncogene 18, 7860-7872.
39. Mlodzik, M. (1999). Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross-talk. EMBO J. 18, 6873-6879.
40. Mlodzik, M. (2000). Spiny legs and prickled bodies: new insights and complexities in planar polarity establishment. BioEssays 22, 311-315.
41. Mlodzik, M. (2002). Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation? Trends Genet. 18, 564-571.
42. Montcouquiol, M. and Corwin, J. T. (2001). Intracellular signals that control cell proliferation in mammalian balance epithelia: key roles for phosphatidylinositol-3 kinase, mammalian target of rapamycin, and S6 kinases in preference to calcium, protein kinase C, and mitogen-activated protein kinase. J. Neurosci. 21, 570-580.
43. Monteiro, A., French, V., Smit, G., Brakefield, P. M. and Metz, J. A. (2001). Butterfly eyespot patterns: evidence for specification by a morphogen diffusion gradient. Acta Biotheor. 49, 77-88.
44. Neumann, C. J. and Cohen, S. M. (1997). Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124, 871-880.
45. Parr, B. A. and McMahon, A. P. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350-353.
46. Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J. and Skarnes, W. C. (2000). An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407, 535-538.
47. Rattner, A., Hsieh, J. C., Smallwood, P. M., Gilbert, D. J., Copeland, N. G., Jenkins, N. A. and Nathans, J. (1997). A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc. Natl. Acad. Sci. USA 94, 2859-2863.
48. Self, T., Mahony, M., Fleming, J., Walsh, J., Brown, S. D. and Steel, K. P. (1998). Shaker-1 mutations reveal roles for myosin VIIA in both development and function of cochlear hair cells. Development 125, 557-566.
49. Shimizu, H., Julius, M. A., Giarre, M., Zheng, Z., Brown, A. M. and Kitajewski, J. (1997). Transformation by Wnt family proteins correlates with regulation of beta-catenin. Cell Growth Differ. 8, 1349-1358.
50. Shulman, J. M., Perrimon, N. and Axelrod, J. D. (1998). Frizzled signaling and the developmental control of cell polarity. Trends Genet. 14, 452-458.
51. Sobin, A. and Anniko, M. (1984). Early development of cochlear hair cell stereociliary surface morphology. Arch. Otorhinolaryngol. 241, 55-64.
52. Strigini, M. and Cohen, S. M. (2000). Wingless gradient formation in the Drosophila wing. Curr. Biol. 10, 293-300.
53. Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyanna, Y., Hess, F., Saint-Jeannet, J. P. and He, X. (2000). LDL-receptor-related proteins in Wnt signal transduction. Nature 407, 530-535.
54. Tomlinson, A., Strapps, W. R. and Heemskerk, J. (1997). Linking Frizzled and Wnt signaling in Drosophila development. Development 124, 4515-4521.
55. Tomlinson, A. and Struhl, G. (1999). Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye. Development 126, 5725-5738.
56. Tree, D. R. P., Shulman, J. M., Rousset, R., Scott, M. P., Gubb, D. and Axelrod, J. D. (2002). Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109, 371-381.
57. Tsuda, M., Kamimura, K., Nakato, H., Archer, M., Staatz, W., Fox, B., Humphrey, M., Olson, S., Futch, T., Kaluza, V., Siegfried, E., Stam, L. and Selleck, S. B. (1999). The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature 400, 276-280.
58. Uren, A., Reichsman, F., Anest, V., Taylor, W. G., Muraiso, K., Bottaro, D. P., Cumberledge, S. and Rubin, J. S. (2000). Secreted frizzled-related protein-1 binds directly to Wingless and is a biphasic modulator of Wnt signaling. J. Biol. Chem. 275, 4374-4382.
59. Wada, T., Wakabayashi, Y., Takahashi, S., Ushiki, T., Kikkawa, Y., Yonekawa, H. and Kominami, R. (2001). A point mutation in a cadherin gene, Cdh23, causes deafness in a novel mutant, Waltzer mouse niigata. Biochem. Biophys. Res. Commun. 283, 113-117.
60. Wang, S., Krinks, M., Lin, K, Luyten, F. P. and Moos, M., Jr (1997). Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88, 757-766.
61. Wang, Y., Huso, D., Cahill, H., Ryugo, D. and Nathans, J. (2001). Progressive cerebellar, auditory, and esophageal dysfunction caused by targeted disruption of the frizzled-4 gene. J. Neurosci. 21, 4761-4771.
62. Weil, D., Blanchard, S., Kaplan, J., Guilford, P., Gibson, F., Walsh, J., Mburu, P., Varela, A., Levilliers, J., Weston, M. D. et al. (1995). Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 374, 60-61.
63. Wilson, S. M., Householder, D. B., Coppola, V., Tessarollo, L., Fritzsch, B., Lee, E. C., Goss, D., Carlson, G. A., Copeland, N. G. and Jenkins, N. A. (2001). Mutations in Cdh23 cause nonsyndromic hearing loss in waltzer mice. Genomics 74, 228-233.
64. Winter, C. G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J. D. and Luo, L. (2001). Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91.
65. Wodarz, A. and Nusse, R. (1998). Mechanisms of Wnt signaling in development. Annu. Rev. Cell. Dev. Biol. 14, 59-88.
66. Xu, Q., D'Amore, P. A. and Sokol, S. Y. (1998). Functional and biochemical interactions of Wnts with FrzA, a secreted Wnt antagonist. Development 125, 4767-4776.
67. Yang, C.-H., Axelrod, J. D. and Simon, M. A. (2002). Regulation of frizzled by fat-like cadherins during planar polarity signaling in the Drosophila eye. Cell 108, 675-688.
68. Yoshida, N. and Liberman, M. C. (1999). Stereociliary anomaly in the guinea pig: effects of hair bundle rotation on cochlear sensitivity. Hear. Res. 131, 29-38.
69. Yoshino, K., Rubin, J. S., Higinbotham, K. G., Uren, A., Anest, V., Plisov, S. Y. and Perantoni, A. O. (2001). Secreted Frizzled-related proteins can regulate metanephric development. Mech. Dev. 102, 45-55.
70. Zecca, M., Basler, K. and Struhl, G. (1996). Direct and long-range action of a wingless morphogen gradient. Cell 87, 833-844.