Delta-like 1 and lateral inhibition during hair cell formation in the chicken inner ear: Evidence against cis-inhibition

Development (Cambridge)

Volumn 139, Issue 20, 2012, Pages 3764-3774

  Chrysostomou, Elena ^a   Gale, Jonathan E ^a   Daudet, Nicolas ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cis inhibition; Delta like 1; Inner ear; Lateral inhibition; Notch; Pattern formation

Indexed keywords

DELTA LIKE 1 PROTEIN; DOXYCYCLINE; NOTCH RECEPTOR; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CHICK EMBRYO; CHICKEN; EMBRYO; EMBRYO DEVELOPMENT; FLUORESCENCE; HAIR CELL; INNER EAR; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPORTER GENE; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; DOXYCYCLINE; EAR, INNER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HAIR CELLS, AUDITORY, INNER; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 84866486422     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.074476     Document Type: Article

References (56)

1. Abelló, G., Khatri, S., Giráldez, F. and Alsina, B. (2007). Early regionalization of the otic placode and its regulation by the Notch signaling pathway. Mech. Dev. 124, 631-645.
2. Adam, J., Myat, A., Le Roux, I., Eddison, M., Henrique, D., Ish-Horowicz, D. and Lewis, J. (1998). Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development 125, 4645-4654.
3. Artavanis-Tsakonas, S., Rand, M. D. and Lake, R. J. (1999). Notch signaling: cell fate control and signal integration in development. Science 284, 770-776.
4. Barad, O., Rosin, D., Hornstein, E. and Barkai, N. (2010). Error minimization in lateral inhibition circuits. Sci. Signal. 3, ra51.
5. Bartolami, S., Goodyear, R. and Richardson, G. (1991). Appearance and distribution of the 275 kD hair-cell antigen during development of the avian inner ear. J. Comp. Neurol. 314, 777-788.
6. Bermingham, N. A., Hassan, B. A., Price, S. D., Vollrath, M. A., Ben-Arie, N., Eatock, R. A., Bellen, H. J., Lysakowski, A. and Zoghbi, H. Y. (1999). Math1: an essential gene for the generation of inner ear hair cells. Science 284, 1837-1841.
7. Bray, S. J. (2006). Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689.
8. Brooker, R., Hozumi, K. and Lewis, J. (2006). Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133, 1277-1286.
9. Chitnis, A. (1995). The role of Notch in lateral inhibition and cell fate specification. Mol. Cell. Neurosci. 6, 311-321.
10. Collier, J. R., Monk, N. A., Maini, P. K. and Lewis, J. H. (1996). Pattern formation by lateral inhibition with feedback: a mathematical model of delta-notch intercellular signalling. J. Theor. Biol. 183, 429-446.
11. Collins, R. T., Linker, C. and Lewis, J. (2010). MAZe: a tool for mosaic analysis of gene function in zebrafish. Nat. Methods 7, 219-223.
12. Daudet, N. and Lewis, J. (2005). Two contrasting roles for Notch activity in chick inner ear development: specification of prosensory patches and lateral inhibition of hair-cell differentiation. Development 132, 541-551.
13. Daudet, N., Ariza-McNaughton, L. and Lewis, J. (2007). Notch signalling is needed to maintain, but not to initiate, the formation of prosensory patches in the chick inner ear. Development 134, 2369-2378.
14. Daudet, N., Gibson, R., Shang, J., Bernard, A., Lewis, J. and Stone, J. (2009). Notch regulation of progenitor cell behavior in quiescent and regenerating auditory epithelium of mature birds. Dev. Biol. 326, 86-100.
15. de Celis, J. F. and Bray, S. (1997). Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124, 3241-3251.
16. Deblandre, G. A., Wettstein, D. A., Koyano-Nakagawa, N. and Kintner, C. (1999). A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. Development 126, 4715-4728.
17. del Álamo, D., Rouault, H. and Schweisguth, F. (2011). Mechanism and significance of cis-inhibition in Notch signalling. Curr. Biol. 21, R40-R47.
18. Eddison, M., Le Roux, I. and Lewis, J. (2000). Notch signaling in the development of the inner ear: lessons from Drosophila. Proc. Natl. Acad. Sci. USA 97, 11692-11699.
19. Fior, R. and Henrique, D. (2005). A novel hes5/hes6 circuitry of negative regulation controls Notch activity during neurogenesis. Dev. Biol. 281, 318-333.
20. Goodyear, R. and Richardson, G. (1997). Pattern formation in the basilar papilla: evidence for cell rearrangement. J. Neurosci. 17, 6289-6301.
21. Goodyear, R. J., Gates, R., Lukashkin, A. N. and Richardson, G. P. (1999). Hair-cell numbers continue to increase in the utricular macula of the early posthatch chick. J. Neurocytol. 28, 851-861.
22. Goodyear, R. J., Legan, P. K., Christiansen, J. R., Xia, B., Korchagina, J., Gale, J. E., Warchol, M. E., Corwin, J. T. and Richardson, G. P. (2010). Identification of the hair cell soma-1 antigen, HCS-1, as otoferlin. J. Assoc. Res. Otolaryngol. 11, 573-586.
23. Haddon, C., Jiang, Y. J., Smithers, L. and Lewis, J. (1998). Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development 125, 4637-4644.
24. Hamburger, V. and Hamilton, H. L. (1992). A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 195, 231-272.
25. Hartman, B. H., Hayashi, T., Nelson, B. R., Bermingham-McDonogh, O. and Reh, T. A. (2007). Dll3 is expressed in developing hair cells in the mammalian cochlea. Dev. Dyn. 236, 2875-2883.
26. Heitzler, P. and Simpson, P. (1991). The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083-1092.
27. Heitzler, P., Bourouis, M., Ruel, L., Carteret, C. and Simpson, P. (1996). Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila. Development 122, 161-171.
28. Henrique, D., Hirsinger, E., Adam, J., Le Roux, I., Pourquié, O., Ish-Horowicz, D. and Lewis, J. (1997). Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr. Biol. 7, 661-670.
29. Itoh, M., Kim, C. H., Palardy, G., Oda, T., Jiang, Y. J., Maust, D., Yeo, S. Y., Lorick, K., Wright, G. J., Ariza-McNaughton, L. et al. (2003). Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82.
30. Jacobsen, T. L., Brennan, K., Arias, A. M. and Muskavitch, M. A. (1998). Cis-interactions between Delta and Notch modulate neurogenic signalling in Drosophila. Development 125, 4531-4540.
31. Jørgensen, J. M. and Mathiesen, C. (1988). The avian inner ear. Continuous production of hair cells in vestibular sensory organs, but not in the auditory papilla. Naturwissenschaften 75, 319-320.
32. Katayama, A. and Corwin, J. T. (1989). Cell production in the chicken cochlea. J. Comp. Neurol. 281, 129-135.
33. Kiernan, A. E., Cordes, R., Kopan, R., Gossler, A. and Gridley, T. (2005). The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 132, 4353-4362.
34. Klein, T., Brennan, K. and Arias, A. M. (1997). An intrinsic dominant negative activity of serrate that is modulated during wing development in Drosophila. Dev. Biol. 189, 123-134.
35. 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.
36. Lewis, J. (1998). Notch signalling and the control of cell fate choices in vertebrates. Semin. Cell Dev. Biol. 9, 583-589.
37. Liu, Y., Pathak, N., Kramer-Zucker, A. and Drummond, I. A. (2007). Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134, 1111-1122.
38. Matsuda, M. and Chitnis, A. B. (2009). Interaction with Notch determines endocytosis of specific Delta ligands in zebrafish neural tissue. Development 136, 197-206.
39. Micchelli, C. A., Rulifson, E. J. and Blair, S. S. (1997). The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124, 1485-1495.
40. Morimoto, M., Liu, Z., Cheng, H.-T., Winters, N., Bader, D. and Kopan, R. (2010). Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate. J. Cell Sci. 123, 213-224.
41. Petropoulos, C. J. and Hughes, S. H. (1991). Replication-competent retrovirus vectors for the transfer and expression of gene cassettes in avian cells. J. Virol. 65, 3728-3737.
42. Podgorski, G. J., Bansal, M. and Flann, N. S. (2007). Regular mosaic pattern development: a study of the interplay between lateral inhibition, apoptosis and differential adhesion. Theor. Biol. Med. Model. 4, 43.
43. Salazar-Ciudad, I., Jernvall, J. and Newman, S. A. (2003). Mechanisms of pattern formation in development and evolution. Development 130, 2027-2037.
44. Sato, Y., Kasai, T., Nakagawa, S., Tanabe, K., Watanabe, T., Kawakami, K. and Takahashi, Y. (2007). Stable integration and conditional expression of electroporated transgenes in chicken embryos. Dev. Biol. 305, 616-624.
45. Schweisguth, F. (2004). Regulation of notch signaling activity. Curr. Biol. 14, R129-R138.
46. Sprinzak, D., Lakhanpal, A., Lebon, L., Santat, L. A., Fontes, M. E., Anderson, G. A., Garcia-Ojalvo, J. and Elowitz, M. B. (2010). Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 465, 86-90.
47. Steinberg, M. S. and Takeichi, M. (1994). Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc. Natl. Acad. Sci. USA 91, 206-209.
48. Stone, J. S. and Rubel, E. W. (1999). Delta1 expression during avian hair cell regeneration. Development 126, 961-973.
49. Takebayashi, K., Akazawa, C., Nakanishi, S. and Kageyama, R. (1995). Structure and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-5. Identification of the neural precursor cell-specific promoter element. J. Biol. Chem. 270, 1342-1349.
50. Togashi, H., Kominami, K., Waseda, M., Komura, H., Miyoshi, J., Takeichi, M. and Takai, Y. (2011). Nectins establish a checkerboard-like cellular pattern in the auditory epithelium. Science 333, 1144-1147.
51. Warchol, M. E. (2007). Characterization of supporting cell phenotype in the avian inner ear: implications for sensory regeneration. Hear. Res. 227, 11-18.
52. Watanabe, T., Saito, D., Tanabe, K., Suetsugu, R., Nakaya, Y., Nakagawa, S. and Takahashi, Y. (2007). Tet-on inducible system combined with in ovo electroporation dissects multiple roles of genes in somitogenesis of chicken embryos. Dev. Biol. 305, 625-636.
53. Webb, S. D. and Owen, M. R. (2004). Oscillations and patterns in spatially discrete models for developmental intercellular signalling. J. Math. Biol. 48, 444-476.
54. Xu, Q., Mellitzer, G., Robinson, V. and Wilkinson, D. G. (1999). In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399, 267-271.
55. Zine, A., Van De Water, T. R. and de Ribaupierre, F. (2000). Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development 127, 3373-3383.
56. Zine, A., Aubert, A., Qiu, J., Therianos, S., Guillemot, F., Kageyama, R. and de Ribaupierre, F. (2001). Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J. Neurosci. 21, 4712-4720.