Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina

Development

Volumn 133, Issue 7, 2006, Pages 1367-1378

  Yaron, Orly ^a   Farhy, Chen ^a   Marquardt, Till ^b   Applebury, Meredithe ^c   Ashery Padan, Ruth ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cre loxp; Lineage tracing; Mouse; Notch1; Photoreceptors; Retina development; Retinal progenitor cells

Indexed keywords

ALKALINE PHOSPHATASE; CRE RECOMBINASE; HELIX LOOP HELIX PROTEIN; NEUROGENIC DIFFERENTIATION FACTOR; NOTCH1 RECEPTOR; RECOVERIN; RHODOPSIN; THYROID HORMONE RECEPTOR BETA; THYROID HORMONE RECEPTOR BETA2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BHLH; TRANSCRIPTION FACTOR CRX; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR HES 5; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR MATH3; TRANSCRIPTION FACTOR MATH5; TRANSCRIPTION FACTOR NGN2; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMPOSITION; CELL FATE; CELL LINEAGE; CELL MATURATION; CELL SPECIFICITY; CELL TYPE; CHRONOSEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INACTIVATION; LOXP SITE; MICROPHTHALMIA; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; RETINA CELL; RETINA CONE; RETINA DEVELOPMENT; RETINA MALFORMATION; RETINA NERVE CELL;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINEAGE; CONES (RETINA); DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; RECEPTOR, NOTCH1; RETINA; TRANSCRIPTION FACTORS;

INVERTEBRATA; VERTEBRATA;

EID: 33646133654     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02311     Document Type: Article

References (87)

1. Adler, R., Tamres, A., Bradford, R. L. and Belecky-Adams, T. L. (2001). Microenvironmental regulation of visual pigment expression in the chick retina. Dev. Biol. 236, 454-464.
2. Ahmad, I., Dooley, C. M. and Polk, D. L. (1997). Delta-1 is a regulator of neurogenesis in the vertebrate retina. Dev. Biol. 185, 92-103.
3. Akagi, T., Inoue, T., Miyoshi, G., Bessho, Y., Takahashi, M., Lee, J. E., Guillemot, F. and Kageyama, R. (2004). Requirement of multiple basic helix-loop-helix genes for retinal neuronal subtype specification. J. Biol. Chem. 279, 28492-28498.
4. Applebury, M. L., Antoch, M. P., Baxter, L. C., Chun, L. L., Falk, J. D., Farhangfar, F., Kage, K., Krzystolik, M. G., Lyass, L. A. and Robbins, J. T. (2000). The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513-523.
5. 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.
6. Ashery-Padan, R. (2002). Somatic gene targeting in the developing and adult mouse retina. Methods 28, 457-464.
7. Ashery-Padan, R., Marquardt, T, Zhou, X. and Gruss, P. (2000). Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev. 14, 2701-2711.
8. Austin, C. P., Feldman, D. E., Ida, J. A., Jr and Cepko, C. L (1995). Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637-3650.
9. Bao, Z. Z. and Cepko, C. L. (1997). The expression and function of Notch pathway genes in the developing rat eye. J. Neurosci. 17, 1425-1434.
10. Bernardos, R. L., Lentz, S. I., Wolfe, M. S. and Raymond, P. A. (2005). Notch-Delta signaling is required for spatial patterning and Muller glia differentiation in the zebrafish retina. Dev. Biol. 278, 381-395.
11. Blanks, J. C. and Johnson, L. V. (1983). Selective lectin binding of the developing mouse retina. J. Comp. Neurol. 221, 31-41.
12. Bray, S. (1998). Notch signalling in Drosophila: three ways to use a pathway. Semin. Cell Dev. Biol. 9, 591-597.
13. Brown, N. L., Kanekar, S., Vetter, M. L., Tucker, P. K., Gemza, D. L. and Glaser, T. (1998). Math5 encodes a murine basic helix-loop-helix transcription factor expressed during early stages of retinal neurogenesis. Development 125, 4821-4833.
14. Cepko, C. L., Austin, C. P, Yang, X., Alexiades, M. and Ezzeddine, D. (1996). Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. USA 93, 589-595.
15. Chambers, C. B., Peng, Y., Nguyen, H., Gaiano, N., Fishell, G. and Nye, J. S. (2001). Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128, 689-702.
16. Chen, J., Rattner, A. and Nathans, J. (2005). The rod photoreceptor-specific nuclear receptor Nr2e3 represses transcription of multiple cone-specific genes. J. Neurosci. 25, 118-129.
17. Chen, S., Wang, Q. L., Nie, Z., Sun, H., Lennon, G., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. and Zack, D. J. (1997). Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19,1017-1030.
18. Cheng, H., Khanna, H., Oh, E. C., Hicks, D., Mitton, K. P. and Swaroop, A. (2004). Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum. Mol. Genet. 13, 1563-1575.
19. Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D. and Kintner, C. (1995). Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761-766.
20. Conlon, R. A., Reaume, A. G. and Rossant J. (1995). Notch1 is required for the coordinate segmentation of somites. Development 121, 1533-1545.
21. de la Pompa, J. L., Wakeham, A., Correia, K. M., Samper, E., Brown, S., Aguilera, R. J., Nakano, T., Honjo, T., Mak, T. W., Rossant, J. et al. (1997). Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124, 1139-1148.
22. del Amo, F. F., Gendron-Maguire, M., Swiatek, P. J., Jenkins, N. A., Copeland, N. G. and Gridley, T. (1993). Cloning, analysis, and chromosomal localization of Notch-1, a mouse homolog of Drosophila Notch. Genomics 15, 259-264.
23. Dorsky, R. I., Rapaport, D. H. and Harris, W. A. (1995). Xotch inhibits cell differentiation in the Xenopus retina. Neuron 14, 487-496.
24. Dorsky, R. I., Chang, W. S., Rapaport, D. H. and Harris, W. A. (1997). Regulation of neuronal diversity in the Xenopus retina by Delta signalling. Nature 385,67-70.
25. Furukawa, T., Morrow, E. M. and Cepko, C. L. (1997). Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91, 531-541.
26. Furukawa, T., Morrow, E. M., Li, T., Davis, F. C. and Cepko, C. L. (1999). Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat. Genet. 23, 466-470.
27. Furukawa, T., Mukherjee, S., Bao, Z. Z., Morrow, E. M. and Cepko, C. L. (2000). rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26, 383-394.
28. Gaiano, N. and Fishell, G. (2002). The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25, 471-490.
29. Gan, L., Xiang, M., Zhou, L., Wagner, D. S., Klein, W. H. and Nathans, J. (1996). POU domain factor Brn-3b is required for the development of a large set of retinal ganglion cells. Proc. Natl. Acad. Sci. USA 93, 3920-3925.
30. Gan, L., Wang, S. W., Huang, Z. and Klein, W. H. (1999). POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Dev. Biol. 210, 469-480.
31. Genoud, S., Lappe-Siefke, C., Goebbels, S., Radtke, F., Aguet, M., Scherer, S. S., Suter, U., Nave, K. A. and Mantei, N. (2002). Notch1 control of oligodendrocyte differentiation in the spinal cord. J. Cell Biol. 158, 709-718.
32. Hatakeyama, J. and Kageyama, R. (2004). Retinal cell fate determination and bHLH factors. Semin. Cell Dev. Biol. 15, 83-89.
33. Haverkamp, S. and Wassle, H. (2000). Immunocytochemical analysis of the mouse retina. J. Comp. Neurol. 424,1-23.
34. 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.
35. Henrique, D., Hirsinger, E., Adam, J., Le, Roux, I., Pourquie, 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.
36. Hojo, M., Ohtsuka, T., Hashimoto, N., Gradwohl, G., Guillemot F. and Kageyama, R. (2000). Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127, 2515-2522.
37. Jones, I., Srinivas, M., Ng, L. and Forrest, D. (2003). The thyroid hormone receptor beta gene: structure and functions in the brain and sensory systems. Thyroid 13, 1057-1068.
38. Kageyama, R., Ishibashi, M., Takebayashi, K. and Tomita, K. (1997). bHLH transcription factors and mammalian neuronal differentiation. Int. J. Biochem. Cell Biol. 29, 1389-1399.
39. Kammandel, B., Chowdhury, K., Stoykova, A., Aparicio, S., Brenner, S. and Gruss, P. (1999). Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity Dev. Biol. 205, 79-97.
40. Kim, J., Wu, H. H., Lander, A. D., Lyons, K. M., Matzuk, M. M. and Calof, A. L. (2005). GDF11 controls the timing of progenitor cell competence in developing retina. Science 308, 1927-1930.
41. Knight, J. K. and Raymond, P. A. (1990). Time course of opsin expression in developing rod photoreceptors. Development 110, 1115-1120.
42. Kopan, R. and Cagan, R. (1997). Notch on the cutting edge. Trends Genet. 13, 465-467.
43. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development 131, 965-973.
44. Lee, H. Y., Wroblewski, E., Philips, G. T., Stair, C. N., Conley, K., Reedy, M., Mastick, G. S. and Brown, N. L. (2005). Multiple requirements for Hes 1 during early eye formation. Dev. Biol. 284, 464-478.
45. Lee, J. E., Hollenberg, S. M., Snider, L., Turner, D. L., Lipnick, N. and Weintraub, H. (1995). Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836-844.
46. Levine, E. M., Fuhrmann, S. and Reh, T. A. (2000). Soluble factors and the development of rod photoreceptors. Cell Mol. Life Sci. 57, 224-234.
47. Livesey, F J. and Cepko, C. L. (2001). Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2, 109-118.
48. Lo, L., Sommer, L. and Anderson, D. J. (1997). MASH1 maintains competence for BMP2-induced neuronal differentiation in post-migratory neural crest cells. Curr. Biol. 7, 440-450.
49. Lobe, C. G., Koop, K. E., Kreppner, W., Lomeli, H., Gertsenstein, M. and Nagy, A. (1999). Z/AP, a double reporter for cre-mediated recombination. Dev. Biol. 208, 281-292.
50. Lutolf, S., Radtke, F., Aguet, M., Suter, U. and Taylor, V. (2002). Notch1 is required for neuronal and glial differentiation in the cerebellum. Development 129, 373-385.
51. Ma, W., Yan, R. T., Xie, W. and Wang, S. Z. (2004). A role of ath5 in inducing neuroD and the photoreceptor pathway. J. Neurosci. 24, 7150-7158.
52. Marquardt, T. (2003). Transcriptional control of neuronal diversification in the retina. Prog. Retin. Eye Res. 22, 567-577.
53. Marquardt, T., Ashery-Padan, R., Andrejewski, N., Scardigli, R., Guillemot F. and Gruss, P. (2001). Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105, 43-55.
54. Martinez-Morales, J. R., Signore, M., Acampora, D., Simeone, A. and Bovolenta, P. (2001). Otx genes are required for tissue specification in the developing eye. Development 128, 2019-2030.
55. Morrow, E. M., Belliveau, M. J. and Cepko, C. L. (1998a). Two phases of rod photoreceptor differentiation during rat retinal development. J. Neurosci. 18, 3738-3748.
56. Morrow, E. M., Furukawa, T. and Cepko, C. L. (1998b). Vertebrate photoreceptor cell development and disease. Trends Cell. Biol. 8, 353-358.
57. Morrow, E. M., Furukawa, T., Lee, J. E. and Cepko, C. L. (1999). NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126, 23-36.
58. Mu, X., Fu, X., Sun, H., Beremand, P. D., Thomas, T. L. and Klein, W. H. (2005). A gene network downstream of transcription factor Math5 regulates retinal progenitor cell competence and ganglion cell fate. Dev. Biol. 280, 467-481.
59. Neumann, C. J. and Nuesslein-Volhard, C. (2000). Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289, 2137-2139.
60. Ng, L., Hurley, J. B., Dierks, B., Srinivas, M., Salto, C., Vennstrom, B., Reh, T. A. and Forrest, D. (2001). A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet. 27, 94-98.
61. Nishida, A., Furukawa, A., Koike, C., Tano, Y., Aizawa, S., Matsuo, I. and Furukawa, T. (2003). Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat. Neurosci. 6, 1255-1263.
62. Ohnuma, S., Hopper, S., Wang, K. C., Philpott, A. and Harris, W. A. (2002). Co-ordinating retinal histogenesis: early cell cycle exit enhances early cell fate determination in the Xenopus retina. Development 129, 2435-2446.
63. Ohtsuka, T., Ishibashi, M., Gradwohl, G., Nakanishi, S., Guillemot, F. and Kageyama, R. (1999). Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J. 18, 2196-2207.
64. Oishi, K., Kamakura, S., Isazawa, Y., Yoshimatsu, T., Kuida, K., Nakafuku, M., Masuyama, N. and Gotoh, Y. (2004). Notch promotes survival of neural precursor cells via mechanisms distinct from those regulating neurogenesis. Dev. Biol. 276, 172-184.
65. Peng, G. H., Ahmad, O., Ahmad, F., Liu, J. and Chen, S. (2005). The photoreceptor-specific nuclear receptor Nr2e3 interacts with Crx and exerts opposing effects on the transcription of rod versus cone genes. Hum. Mol. Genet. 14,747-764.
66. Pennesi, M. E., Cho, J. H., Yang, Z., Wu, S. H., Zhang, J., Wu, S. M. and Tsai, M. J. (2003). BETA2/NeuroD1 null mice: a new model for transcription factor-dependent photoreceptor degeneration. J. Neurosci. 23, 453-461.
67. Perron, M. and Harris, W. A. (2000). Determination of vertebrate retinal progenitor cell fate by the Notch pathway and basic helix-loop-helix transcription factors. Cell. Mol. Life Sci. 57, 215-223.
68. Radtke, F., Wilson, A., Stark, G., Bauer, M., van Meerwijk, J., MacDonald, H. R. and Aguet, M. (1999). Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10, 547-558.
69. Rapaport, D. H. and Dorsky, R. I. (1998). Inductive competence, its significance in retinal cell fate determination and a role for Delta-Notch signaling. Semin. Cell Dev. Biol. 9, 241-247.
70. Scheer, N., Groth, A., Hans, S. and Campos-Ortega, J. A. (2001). An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 128, 1099-1107.
71. Schroder, N. and Gossler, A. (2002). Expression of Notch pathway components in fetal and adult mouse small intestine. Gene Expr. Patt. 2, 247-250.
72. 3. In The Structure of the Eye (ed. G. K. Smelser), pp. 487-505. New York: Academic Press.
73. Sharma, R. K., O'Leary, T. E., Fields, C. M. and Johnson, D. A. (2003). Development of the outer retina in the mouse. Dev. Brain Res. 145, 93-105.
74. Sidman, R. L. (1961), Histogenesis of Mouse Retina Studied with Thymidine-H3. New York: Academic Press.
75. Silva, A. O., Ercole, C. E. and McLoon, S. C. (2003). Regulation of ganglion cell production by Notch signaling during retinal development. J. Neurobiol. 54, 511-524.
76. Sommer, L., Ma, Q. and Anderson, D. J. (1996). neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 8, 221-241.
77. Swiatek, P. J., Lindsell, C. E., del Amo, F. F., Weinmaster, G. and Gridley, T. (1994). Notch1 is essential for postimplantation development in mice. Genes Dev. 8, 707-719.
78. Tomita, K., Ishibashi, M., Nakahara, K., Ang, S. L., Nakanishi, S., Guillemot, F. and Kageyama, R. (1996). Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 16, 723-734.
79. Turner, D. L. and Cepko, C. L. (1987). A common progenitor for neurons and glia persists in rat retina late in development. Nature 328, 131-136.
80. Waid, D. K. and McLoon, S. C. (1998). Ganglion cells influence the fate of dividing retinal cells in culture. Development 125, 1059-1066.
81. Wang, S., Sdrulla, A. D., diSibio, G., Bush, G., Nofziger, D., Hicks, C., Weinmaster, G. and Barres, B. A. (1998). Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 63-75.
82. Wang, S. W., Gan, L., Martin, S. E. and Klein, W. H. (2000). Abnormal polarization and axon outgrowth in retinal ganglion cells lacking the POU-domain transcription factor Brn-3b. Mol. Cell. Neurosci. 16, 141-156.
83. Watanabe, T. and Raff, M. C. (1990). Rod photoreceptor development in vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron 4, 461-467.
84. Wetts, R. and Fraser, S. E. (1988). Multipotent precursors can give rise to all major cell types of the frog retina. Science 239, 1142-1145.
85. Wood, W. M., Dowding, J. M., Haugen, B. R., Bright, T. M., Gordon, D. F. and Ridgway, E. C. (1994). Structural and functional characterization of the genomic locus encoding the murine beta 2 thyroid hormone receptor. Mol. Endocrinol. 8, 1605-1617.
86. Yan, R. T. and Wang, S. Z. (1998). neuroD induces photoreceptor cell overproduction in vivo and de novo generation in vitro. J. Neurobiol. 36, 485-496.
87. Young, R. W. (1985). Cell differentiation in the retina of the mouse. Anat. Rec. 212, 199-205.