Notch1 is required in newly postmitotic cells to inhibit the rod photoreceptor fate

Development (Cambridge)

Volumn 140, Issue 15, 2013, Pages 3188-3197

  Mizeracka, Karolina ^a   Demaso, Christina R ^a,b   Cepko, Constance L ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Cell fate; Id; Mouse; Notch; Nrarp; Postmitotic; Retina

Indexed keywords

ANKYRIN; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 3; NOTCH REGULATED ANKYRIN REPEAT PROTEIN; NOTCH1 RECEPTOR; UNCLASSIFIED DRUG;

ALLELE; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; DAUGHTER CELL; DNA BINDING; GENE EXPRESSION; GLIA CELL; MITOSIS; MOUSE; MUELLER CELL; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RETINA CELL; RETINA DEVELOPMENT; RETINA ROD; RETINAL PROGENITOR CELL; STEM CELL; VIRUS GENOME; WILD TYPE;

CELL FATE; ID; MOUSE; NOTCH; NRARP; POSTMITOTIC; RETINA;

ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEINS; MICE; MICE, KNOCKOUT; MITOSIS; MODELS, BIOLOGICAL; NEURAL STEM CELLS; PROTEINS; RECEPTOR, NOTCH1; RETINA; RETINAL ROD PHOTORECEPTOR CELLS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84880251625     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.090696     Document Type: Article

References (59)

1. Akagi, T., Inoue, T., Miyoshi, G., Bessho, Y., Takahashi, M., Lee, J. E., Guillemot, F. and Kageyama, R. (2004). Requirement of multiple basic helixloop-helix genes for retinal neuronal subtype specification. J. Biol. Chem. 279, 28492-28498.
2. Alexiades, M. R. and Cepko, C. (1996). Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev. Dyn. 205, 293-307.
3. Bai, G., Sheng, N., Xie, Z., Bian, W., Yokota, Y., Benezra, R., Kageyama, R., Guillemot, F. and Jing, N. (2007). Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev. Cell 13, 283-297.
4. 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.
5. Belliveau, M. J. and Cepko, C. L. (1999). Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. Development 126, 555-566.
6. Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L. and Weintraub, H. (1990). The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49-59.
7. Cai, L., Morrow, E. M. and Cepko, C. L. (2000). Misexpression of basic helixloop-helix genes in the murine cerebral cortex affects cell fate choices and neuronal survival. Development 127, 3021-3030.
8. Cau, E. and Blader, P. (2009). Notch activity in the nervous system: to switch or not switch? Neural Dev. 4, 36.
9. Cherry, T. J., Wang, S., Bormuth, I., Schwab, M., Olson, J. and Cepko, C. L. (2011). NeuroD factors regulate cell fate and neurite stratification in the developing retina. J. Neurosci. 31, 7365-7379.
10. Ezzeddine, Z. D., Yang, X., DeChiara, T., Yancopoulos, G. and Cepko, C. L. (1997). Postmitotic cells fated to become rod photoreceptors can be respecified by CNTF treatment of the retina. Development 124, 1055-1067.
11. Fekete, D. M., Perez-Miguelsanz, J., Ryder, E. F. and Cepko, C. L. (1994). Clonal analysis in the chicken retina reveals tangential dispersion of clonally related cells. Dev. Biol. 166, 666-682.
12. Fields-Berry, S. C., Halliday, A. L. and Cepko, C. L. (1992). A recombinant retrovirus encoding alkaline phosphatase confirms clonal boundary assignment in lineage analysis of murine retina. Proc. Natl. Acad. Sci. USA 89, 693-697.
13. 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.
14. Godinho, L., Williams, P. R., Claassen, Y., Provost, E., Leach, S. D., Kamermans, M. and Wong, R. O. L. (2007). Nonapical symmetric divisions underlie horizontal cell layer formation in the developing retina in vivo. Neuron 56, 597-603.
15. Hafler, B. P., Surzenko, N., Beier, K. T., Punzo, C., Trimarchi, J. M., Kong, J. H. and Cepko, C. L. (2012). Transcription factor Olig2 defines subpopulations of retinal progenitor cells biased toward specific cell fates. Proc. Natl. Acad. Sci. USA 109, 7882-7887.
16. Holt, C. E., Bertsch, T. W., Ellis, H. M. and Harris, W. A. (1988). Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1, 15-26.
17. Jadhav, A. P., Mason, H. A. and Cepko, C. L. (2006). Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 133, 913-923.
18. Kageyama, R., Ohtsuka, T. and Kobayashi, T. (2007). The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134, 1243-1251.
19. Kim, D. S., Matsuda, T. and Cepko, C. L. (2008). A core paired-type and POU homeodomain-containing transcription factor program drives retinal bipolar cell gene expression. J. Neurosci. 28, 7748-7764.
20. Krebs, L. T., Deftos, M. L., Bevan, M. J. and Gridley, T. (2001). The Nrarp gene encodes an ankyrin-repeat protein that is transcriptionally regulated by the notch signaling pathway. Dev. Biol. 238, 110-119.
21. Krebs, L. T., Bradley, C. K., Norton, C. R., Xu, J., Oram, K. F., Starling, C., Deftos, M. L., Bevan, M. J. and Gridley, T. (2012). The Notch-regulated ankyrin repeat protein is required for proper anterior-posterior somite patterning in mice. Genesis 50, 366-374.
22. Lamar, E., Deblandre, G., Wettstein, D., Gawantka, V., Pollet, N., Niehrs, C. and Kintner, C. (2001). Nrarp is a novel intracellular component of the Notch signaling pathway. Genes Dev. 15, 1885-1899.
23. Livesey, F. J. and Cepko, C. L. (2001). Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2, 109-118.
24. Lyden, D., Young, A. Z., Zagzag, D., Yan, W., Gerald, W., O'Reilly, R., Bader, B. L., Hynes, R. O., Zhuang, Y., Manova, K. et al. (1999). Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401, 670-677.
25. Matsuda, T. and Cepko, C. L. (2004). Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl. Acad. Sci. USA 101, 16-22.
26. Matsuda, T. and Cepko, C. L. (2007). Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA 104, 1027-1032.
27. McConnell, S. K. and Kaznowski, C. E. (1991). Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282-285.
28. Meier-Stiegen, F., Schwanbeck, R., Bernoth, K., Martini, S., Hieronymus, T., Ruau, D., Zenke, M. and Just, U. (2010). Activated Notch1 target genes during embryonic cell differentiation depend on the cellular context and include lineage determinants and inhibitors. PLoS ONE 5, e11481.
29. Mizeracka, K., Trimarchi, J. M., Stadler, M.B. and Cepko, C.L. (2013) Analysis of gene expression in wild type and Notch1 mutant retinal cells by single cell profiling. Dev. Dyn. (in press).
30. 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.
31. Nelson, B. R., Hartman, B. H., Georgi, S. A., Lan, M. S. and Reh, T. A. (2007). Transient inactivation of Notch signaling synchronizes differentiation of neural progenitor cells. Dev. Biol. 304, 479-498.
32. Pirot, P., van Grunsven, L. A., Marine, J.-C., Huylebroeck, D. and Bellefroid, E. J. (2004). Direct regulation of the Nrarp gene promoter by the Notch signaling pathway. Biochem. Biophys. Res. Commun. 322, 526-534.
33. Price, J., Turner, D. and Cepko, C. (1987). Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc. Natl. Acad. Sci. USA 84, 156-160.
34. 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.
35. Rapaport, D. H., Wong, L. L., Wood, E. D., Yasumura, D. and LaVail, M. M. (2004). Timing and topography of cell genesis in the rat retina. J. Comp. Neurol. 474, 304-324.
36. Reynaud-Deonauth, S., Zhang, H., Afouda, A., Taillefert, S., Beatus, P., Kloc, M., Etkin, L. D., Fischer-Lougheed, J. and Spohr, G. (2002). Notch signaling is involved in the regulation of Id3 gene transcription during Xenopus embryogenesis. Differentiation 69, 198-208.
37. Riesenberg, A. N., Liu, Z., Kopan, R. and Brown, N. L. (2009). Rbpj cell autonomous regulation of retinal ganglion cell and cone photoreceptor fates in the mouse retina. J. Neurosci. 29, 12865-12877.
38. Roe, T., Chow, S. A. and Brown, P. O. (1997). 3'-end processing and kinetics of 5'-end joining during retroviral integration in vivo. J. Virol. 71, 1334-1340.
39. Rompani, S. B. and Cepko, C. L. (2008). Retinal progenitor cells can produce restricted subsets of horizontal cells. Proc. Natl. Acad. Sci. USA 105, 192-197.
40. Ruzinova, M. B. and Benezra, R. (2003). Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13, 410-418.
41. Salic, A. and Mitchison, T. J. (2008). A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA 105, 2415-2420.
42. Sidman, R. (1961). Histogenesis of the mouse retina studied with thymidine-3H. In The Structure of the Eye, pp. 487-506. New York, NY: Academic Press.
43. Skeath, J. B. and Doe, C. Q. (1998). Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. Development 125, 1857-1865.
44. Spana, E. P. and Doe, C. Q. (1996). Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17, 21-26.
45. 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.
46. Trimarchi, J. M., Stadler, M. B., Roska, B., Billings, N., Sun, B., Bartch, B. and Cepko, C. L. (2007). Molecular heterogeneity of developing retinal ganglion and amacrine cells revealed through single cell gene expression profiling. J. Comp. Neurol. 502, 1047-1065.
47. Trimarchi, J.M., Stadler, M.B., and Cepko, C.L. (2008). Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLoS ONE 3, e1588.
48. Truman, J. W., Moats, W., Altman, J., Marin, E. C. and Williams, D. W. (2010). Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster. Development 137, 53-61.
49. 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.
50. Turner, D. L., Snyder, E. Y. and Cepko, C. L. (1990). Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4, 833-845.
51. 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.
52. Wong, L. L. and Rapaport, D. H. (2009). Defining retinal progenitor cell competence in Xenopus laevis by clonal analysis. Development 136, 1707-1715.
53. Yamamoto, N., Tanigaki, K., Tsuji, M., Yabe, D., Ito, J. and Honjo, T. (2006). Inhibition of Notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J. Mol. Med. 84, 37-45.
54. Yaron, O., Farhy, C., Marquardt, T., Applebury, M. and Ashery-Padan, R. (2006). Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133, 1367-1378.
55. Yokota, Y. (2001). Id and development. Oncogene 20, 8290-8298.
56. Young, R. W. (1985a). Cell differentiation in the retina of the mouse. Anat. Rec. 212, 199-205.
57. Young, R. W. (1985b). Cell proliferation during postnatal development of the retina in the mouse. Brain Res. 353, 229-239.
58. Yun, T. J. and Bevan, M. J. (2003). Notch-regulated ankyrin-repeat protein inhibits Notch1 signaling: multiple Notch1 signaling pathways involved in T cell development. J. Immunol. 170, 5834-5841.
59. Zheng, M.-H., Shi, M., Pei, Z., Gao, F., Han, H. and Ding, Y.-Q. (2009). The transcription factor RBP-J is essential for retinal cell differentiation and lamination. Mol. Brain 2, 38.