Ligand-dependent Notch signaling strength orchestrates lateral induction and lateral inhibition in the developing inner ear

Development (Cambridge)

Volumn 141, Issue 11, 2014, Pages 2313-2324

  Petrovic, Jelena ^a   Formosa Jordan, Pau ^b   Luna Escalante, Juan C ^b   Abelló, Gina ^a   Ibañes, Marta ^b   Neves, Joana ^a,c   Giraldez, Fernando ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

Atoh1; Hair cells; Mathematical modeling; Sensory development; Signal competition; Systems biology

Indexed keywords

DELTA1 PROTEIN; HEY1 PROTEIN; JAGGED1; NOTCH RECEPTOR; PROTEIN; TRANSCRIPTION FACTOR HES 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; EMBRYO; GENE INDUCTION; GENE REPRESSION; HAIR CELL; INNER EAR; LATERAL INDUCTION; LATERAL INHIBITION; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ATOH1; HAIR CELLS; MATHEMATICAL MODELING; SENSORY DEVELOPMENT; SIGNAL COMPETITION; SYSTEMS BIOLOGY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM-BINDING PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CHICK EMBRYO; EAR, INNER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY, INNER; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MEMBRANE PROTEINS; MODELS, THEORETICAL; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84901387665     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.108100     Document Type: Article

References (70)

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. Acloque, H., Wilkinson, D. G. and Nieto, M. A. (2008). In situ hybridization analysis of chick embryos in whole-mount and tissue sections. Methods Cell Biol. 87, 169-185.
3. 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.
4. Benedito, R., Roca, C., Sörensen, I., Adams, S., Gossler, A., Fruttiger, M. and Adams, R. H. (2009). The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137, 1124-1135.
5. Bray, S. J. (2006). Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689.
6. 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.
7. Brückner, K., Perez, L., Clausen, H. and Cohen, S. (2000). Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 406, 411-415.
8. Buchler, N. E., Gerland, U. and Hwa, T. (2003). On schemes of combinatorial transcription logic. Proc. Natl. Acad. Sci. U.S.A. 100, 5136-5141.
9. Chen, P. and Segil, N. (1999). p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126, 1581-1590.
10. Chiang, M. Y., Xu, L., Shestova, O., Histen, G., L'Heureux, S., Romany, C., Childs, M. E., Gimotty, P. A., Aster, J. C. and Pear, W. S. (2008). Leukemiaassociated NOTCH1 alleles are weak tumor initiators but accelerate K-rasinitiated leukemia. J. Clin. Invest. 118, 3181-3194.
11. Chrysostomou, E., Gale, J. E. and Daudet, N. (2012). Delta-like 1 and lateral inhibition during hair cell formation in the chicken inner ear: evidence against cisinhibition. Development 139, 3764-3774.
12. Cole, L. K., Le Roux, I., Nunes, F., Laufer, E., Lewis, J. and Wu, D. K. (2000). Sensory organ generation in the chicken inner ear: contributions of bone morphogenetic protein 4, serrate1, and lunatic fringe. J. Comp. Neurol. 424, 509-520.
13. Collier, J. R., Monk, N. A. M., 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.
14. 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.
15. 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.
16. Doetzlhofer, A., Basch, M. L., Ohyama, T., Gessler, M., Groves, A. K. and Segil, N. (2009). Hey2 regulation by FGF provides a Notch-independent mechanism for maintaining pillar cell fate in the organ of Corti. Dev. Cell 16, 58-69.
17. Driver, E. C., Sillers, L., Coate, T. M., Rose, M. F. and Kelley, M. W. (2013). The Atoh1-lineage gives rise to hair cells and supporting cells within the mammalian cochlea. Dev. Biol. 376, 86-98.
18. Du, X., Li, W., Gao, X., West, M. B., Saltzman, W. M., Cheng, C. J., Stewart, C., Zheng, J., Cheng, W. and Kopke, R. D. (2013). Regeneration of mammalian cochlear and vestibular hair cells through Hes1/Hes5 modulation with siRNA. Hear. Res. 304, 91-110.
19. 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. U.S.A. 97, 11692-11699.
20. Ferjentsik, Z., Hayashi, S., Dale, J. K., Bessho, Y., Herreman, A., De Strooper, B., del Monte, G., de la Pompa, J. L. and Maroto, M. (2009). Notch is a critical component of the mouse somitogenesis oscillator and is essential for the formation of the somites. PLoS Genet. 5, e1000662.
21. Fischer, A. and Gessler, M. (2007). Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res. 35, 4583-4596.
22. Formosa-Jordan, P. and Ibañes, M. (2009). Diffusible ligand and lateral inhibition dynamics for pattern formation. J. Stat. Mech. 2009, P03019.
23. Formosa-Jordan, P. and Ibañes, M. (2014). Competition in Notch signaling with cis enriches cell fate decisions. PLoS ONE 9, p. e95744.
24. Formosa-Jordan, P., Ibañes, M., Ares, S. and Frade, J. M. (2012). Regulation of neuronal differentiation at the neurogenic wavefront. Development 139, 2321-2329.
25. Golson, M. L., Le Lay, J., Gao, N., Brämswig, N., Loomes, K. M., Oakey, R., May, C. L., White, P. and Kaestner, K. H. (2009). Jagged1 is a competitive inhibitor of Notch signaling in the embryonic pancreas. Mech. Dev. 126, 687-699.
26. 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.
27. Haines, N. and Irvine, K. D. (2003). Glycosylation regulates Notch signalling. Nat. Rev. Mol. Cell Biol. 4, 786-797.
28. Hansson, E. M., Teixeira, A. I., Gustafsson, M. V., Dohda, T., Chapman, G., Meletis, K., Muhr, J. and Lendahl, U. (2006). Recording Notch signaling in real time. Dev. Neurosci. 28, 118-127.
29. Hartman, B. H., Reh, T. A. and Bermingham-McDonogh, O. (2010). Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc. Natl. Acad. Sci. U.S.A. 107, 15792-15797.
30. Hayashi, T., Kokubo, H., Hartman, B. H., Ray, C. A., Reh, T. A. and Bermingham-McDonogh, O. (2008). Hesr1 and Hesr2 may act as early effectors of Notch signaling in the developing cochlea. Dev. Biol. 316, 87-99.
31. Helms, A.W., Abney, A. L., Ben-Arie, N., Zoghbi, H. Y. and Johnson, J. E. (2000). Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. Development 127, 1185-1196.
32. Henrique, D., Adam, J., Myat, A., Chitnis, A., Lewis, J. and Ish-Horowicz, D. (1995). Expression of a Delta homologue in prospective neurons in the chick. Nature 375, 787-790.
33. Iso, T., Kedes, L. and Hamamori, Y. (2003). HES and HERP families: multiple effectors of the Notch signaling pathway. J. Cell. Physiol. 194, 237-255.
34. Jeffries, S., Robbins, D. J. and Capobianco, A. J. (2002). Characterization of a high-molecular-weight Notch complex in the nucleus of Notch(ic)-transformed RKE cells and in a human T-cell leukemia cell line. Mol. Cell. Biol. 22, 3927-3941.
35. Kageyama, R., Niwa, Y., Shimojo, H., Kobayashi, T. and Ohtsuka, T. (2010). Ultradian oscillations in Notch signaling regulate dynamic biological events. Curr. Top. Dev. Biol. 92, 311-331.
36. Kamaid, A., Neves, J. and Giraldez, F. (2010). Id gene regulation and function in the prosensory domains of the chicken inner ear: a link between Bmp signaling and Atoh1. J. Neurosci. 30, 11426-11434.
37. Katoh, M. (2006). Notch ligand, JAG1, is evolutionarily conserved target of canonical WNT signaling pathway in progenitor cells. Int. J. Mol. Med. 17, 681-685.
38. 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.
39. Kiernan, A. E., Xu, J. and Gridley, T. (2006). The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet. 2, e4.
40. Le, T. T., Conley, K.W. and Brown, N. L. (2009). Jagged 1 is necessary for normal mouse lens formation. Dev. Biol. 328, 118-126.
41. Li, S., Mark, S., Radde-Gallwitz, K., Schlisner, R., Chin, M. T. and Chen, P. (2008). Hey2 functions in parallel with Hes1 and Hes5 for mammalian auditory sensory organ development. BMC Dev. Biol. 8, 20.
42. Liu, Z., Liu, Z., Walters, B. J., Owen, T., Kopan, R. and Zuo, J. (2013). In vivo visualization of Notch1 proteolysis reveals the heterogeneity of Notch1 signaling activity in the mouse cochlea. PLoS ONE 8, e64903.
43. Matsuda, M., Koga, M., Nishida, E. and Ebisuya, M. (2012). Synthetic signal propagation through direct cell-cell interaction. Sci. Signal. 5, ra31.
44. Mazzone, M., Selfors, L. M., Albeck, J., Overholtzer, M., Sale, S., Carroll, D. L., Pandya, D., Lu, Y., Mills, G. B., Aster, J. C. et al. (2010). Dose-dependent induction of distinct phenotypic responses to Notch pathway activation in mammary epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 107, 5012-5017.
45. Morrison, A., Hodgetts, C., Gossler, A., Hrabé de Angelis, M. and Lewis, J. (1999). Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech. Dev. 84, 169-172.
46. Morsli, H., Choo, D., Ryan, A., Johnson, R. and Wu, D. K. (1998). Development of the mouse inner ear and origin of its sensory organs. J. Neurosci. 18, 3327-3335.
47. Mulvaney, J. and Dabdoub, A. (2012). Atoh1, an essential transcription factor in neurogenesis and intestinal and inner ear development: function, regulation, and context dependency. J. Assoc. Res. Otolaryngol. 13, 281-293.
48. Murata, J., Ohtsuka, T., Tokunaga, A., Nishiike, S., Inohara, H., Okano, H. and Kageyama, R. (2009). Notch-Hes1 pathway contributes to the cochlear prosensory formation potentially through the transcriptional down-regulation of p27Kip1. J. Neurosci. Res. 87, 3521-3534.
49. Murray, J. D. (2002). Mathematical Biology: I. An Introduction, Vol. 1, 3rd edn. p. 576. Berlin, Heidelberg: Springer-Verlag.
50. Neves, J., Kamaid, A., Alsina, B. and Giraldez, F. (2007). Differential expression of Sox2 and Sox3 in neuronal and sensory progenitors of the developing inner ear of the chick. J. Comp. Neurol. 503, 487-500.
51. Neves, J., Parada, C., Chamizo, M. and Giraldez, F. (2011). Jagged 1 regulates the restriction of Sox2 expression in the developing chicken inner ear: a mechanism for sensory organ specification. Development 138, 735-744.
52. Neves, J., Uchikawa, M., Bigas, A. and Giraldez, F. (2012). The prosensory function of Sox2 in the chicken inner ear relies on the direct regulation of Atoh1. PLoS ONE 7, e30871.
53. Neves, J., Abelló, G., Petrovic, J. and Giraldez, F. (2013). Patterning and cell fate in the inner ear: a case for Notch in the chicken embryo. Dev. Growth Differ. 55, 96-112.
54. Ninov, N., Borius, M. and Stainier, D. Y. R. (2012). Different levels of Notch signaling regulate quiescence, renewal and differentiation in pancreatic endocrine progenitors. Development 139, 1557-1567.
55. Oesterle, E. C. and Rubel, E.W. (1993). Postnatal production of supporting cells in the chick cochlea. Hear. Res. 66, 213-224.
56. Owen, M. R., Sherratt, J. A. and Wearing, H. J. (2000). Lateral induction by juxtacrine signaling is a new mechanism for pattern formation. Dev. Biol. 217, 54-61.
57. Pan, W., Jin, Y., Stanger, B. and Kiernan, A. E. (2010). Notch signaling is required for the generation of hair cells and supporting cells in the mammalian inner ear. Proc. Natl. Acad. Sci. U.S.A. 107, 15798-15803.
58. Perdigoto, C. N., Schweisguth, F. and Bardin, A. J. (2011). Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine. Development 138, 4585-4595.
59. 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.
60. Pujades, C., Kamaid, A., Alsina, B. and Giraldez, F. (2006). BMP-signaling regulates the generation of hair-cells. Dev. Biol. 292, 55-67.
61. Ramos, C., Rocha, S., Gaspar, C. and Henrique, D. (2010). Two Notch ligands, Dll1 and Jag1, are differently restricted in their range of action to control neurogenesis in the mammalian spinal cord. PLoS ONE 5, e15515.
62. Robert-Moreno, A., Guiu, J., Ruiz-Herguido, C., López, M. E., Inglés-Esteve, J., Riera, L., Tipping, A., Enver, T., Dzierzak, E., Gridley, T. et al. (2008). Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1. EMBO J. 27, 1886-1895.
63. Savill, N. J. and Sherratt, J. A. (2003). Control of epidermal stem cell clusters by Notch-mediated lateral induction. Dev. Biol. 258, 141-153.
64. 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.
65. Takebayashi, S., Yamamoto, N., Yabe, D., Fukuda, H., Kojima, K., Ito, J. and Honjo, T. (2007). Multiple roles of Notch signaling in cochlear development. Dev. Biol. 307, 165-178.
66. Tateya, T., Imayoshi, I., Tateya, I., Ito, J. and Kageyama, R. (2011). Cooperative functions of Hes/Hey genes in auditory hair cell and supporting cell development. Dev. Biol. 352, 329-340.
67. 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.
68. Zheng, J. L., Shou, J., Guillemot, F., Kageyama, R. and Gao, W. Q. (2000). Hes1 is a negative regulator of inner ear hair cell differentiation. Development 127, 4551-4560.
69. 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.
70. 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.