Reprogramming amacrine and photoreceptor progenitors into retinal ganglion cells by replacing Neurod1 with Atoh7

Development (Cambridge)

Volumn 140, Issue 3, 2013, Pages 541-551

  Mao, Chai An ^a   Cho, Jang Hyeon ^a   Wang, Jing ^b   Gao, Zhiguang ^a   Pan, Ping ^a   Tsai, Wen Wei ^a,c   Frishman, Laura J ^b   Klein, William H ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Atoh7 Math5; bHLH genes; Mouse; Neurod1; Retinal ganglion cells; Retinal progenitor cells

Indexed keywords

ATOH7 PROTEIN; NEUROGENIC DIFFERENTIATION FACTOR; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL FATE; CELL FUNCTION; CELL SUBPOPULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ELECTRORETINOGRAM; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; GENE EXPRESSION; GENE LOCUS; INTRON; LATERAL GENICULATE BODY; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PHENOTYPE; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA AMACRINE CELL; RETINA GANGLION CELL; SEQUENCE ANALYSIS; SUPERIOR COLLICULUS;

AMACRINE CELLS; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; ELECTRORETINOGRAPHY; EMBRYO, MAMMALIAN; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; IMMUNOHISTOCHEMISTRY; INTRONS; MICE; NERVE TISSUE PROTEINS; NUCLEAR REPROGRAMMING; PHOTORECEPTOR CELLS; PROTEIN BINDING; RETINA; RETINAL GANGLION CELLS; STEM CELLS;

EID: 84872127923     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.085886     Document Type: Article

References (56)

1. Agathocleous, M. and Harris, W. A. (2009). From progenitors to differentiated cells in the vertebrate retina. Annu. Rev. Cell Dev. Biol. 25, 45-69.
2. 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.
3. Alarcón-Martínez, L., Avilés-Trigueros, M., Galindo-Romero, C., Valiente-Soriano, J., Agudo-Barriuso, M., Villa, P. L., Villegas-Pérez, M. P. and Vidal-Sanz, M. (2010). ERG changes in albino and pigmented mice after optic nerve transection. Vision Res. 50, 2176-2187.
4. 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.
5. Brown, N. L., Patel, S., Brzezinski, J. and Glaser, T. (2001). Math5 is required for retinal ganglion cell and optic nerve formation. Development 128, 2497-2508.
6. Brzezinski, J. A., 4th, Brown, N. L., Tanikawa, A., Bush, R. A., Sieving, P. A., Vitaterna, M. H., Takahashi, J. S. and Glaser, T. (2005). Loss of circadian photoentrainment and abnormal retinal electrophysiology in Math5 mutant mice. Invest. Ophthalmol. Vis. Sci. 46, 2540-2551.
7. Brzezinski, J. A., 4th, Prasov, L. and Glaser, T. (2012). Math5 defines the ganglion cell competence state in a subpopulation of retinal progenitor cells exiting the cell cycle. Dev. Biol. 365, 395-413.
8. 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.
9. De Masi, F., Grove, C. A., Vedenko, A., Alibés, A., Gisselbrecht, S. S., Serrano, L., Bulyk, M. L. and Walhout, A. J. (2011). Using a structural and logics systems approach to infer bHLH-DNA binding specificity determinants. Nucleic Acids Res. 39, 4553-4563.
10. Elshatory, Y., Deng, M., Xie, X. and Gan, L. (2007). Expression of the LIM-homeodomain protein Isl1 in the developing and mature mouse retina. J. Comp. Neurol. 503, 182-197.
11. Feng, L., Xie, X., Joshi, P. S., Yang, Z., Shibasaki, K., Chow, R. L. and Gan, L. (2006). Requirement for Bhlhb5 in the specification of amacrine and cone bipolar subtypes in mouse retina. Development 133, 4815-4825.
12. Fu, X., Kiyama, T., Li, R., Russell, M., Klein, W. H. and Mu, X. (2009). Epitope-tagging Math5 and Pou4f2: new tools to study retinal ganglion cell development in the mouse. Dev. Dyn. 238, 2309-2317.
13. Fujitani, Y., Fujitani, S., Luo, H., Qiu, F., Burlison, J., Long, Q., Kawaguchi, Y., Edlund, H., MacDonald, R. J., Furukawa, T. et al. (2006). Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development 133, 4439-4450.
14. 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.
15. Ghiasvand, N. M., Rudolph, D. D., Mashayekhi, M., Brzezinski, J. A., 4th, Goldman, D. and Glaser, T. (2011). Deletion of a remote enhancer near ATOH7 disrupts retinal neurogenesis, causing NCRNA disease. Nat. Neurosci. 14, 578-586.
16. Gomes, F. L., Zhang, G., Carbonell, F., Correa, J. A., Harris, W. A., Simons, B. D. and Cayouette, M. (2011). Reconstruction of rat retinal progenitor cell lineages in vitro reveals a surprising degree of stochasticity in cell fate decisions. Development 138, 227-235.
17. Hatakeyama, J. and Kageyama, R. (2004). Retinal cell fate determination and bHLH factors. Semin. Cell Dev. Biol. 15, 83-89.
18. Hinds, J. W. and Hinds, P. L. (1974). Early ganglion cell differentiation in the mouse retina: an electron microscopic analysis utilizing serial sections. Dev. Biol. 37, 381-416.
19. Hood, D. C. and Birch, D. G. (1990). A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Vis. Neurosci. 5, 379-387.
20. Hufnagel, R. B., Le, T. T., Riesenberg, A. L. and Brown, N. L. (2010). Neurog2 controls the leading edge of neurogenesis in the mammalian retina. Dev. Biol. 340, 490-503.
21. Inoue, T., Hojo, M., Bessho, Y., Tano, Y., Lee, J. E. and Kageyama, R. (2002). Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development 129, 831-842.
22. Jamison, J. A., Bush, R. A., Lei, B. and Sieving, P. A. (2001). Characterization of the rod photoresponse isolated from the dark-adapted primate ERG. Vis. Neurosci. 18, 445-455.
23. Kay, J. N., Voinescu, P. E., Chu, M. W. and Sanes, J. R. (2011). Neurod6 expression defines new retinal amacrine cell subtypes and regulates their fate. Nat. Neurosci. 14, 965-972.
24. Kim, J. W. and Lemke, G. (2006). Hedgehog-regulated localization of Vax2 controls eye development. Genes Dev. 20, 2833-2847.
25. Kothary, R., Clapoff, S., Darling, S., Perry, M. D., Moran, L. A. and Rossant, J. (1989). Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105, 707-714.
26. Le, T. T., Wroblewski, E., Patel, S., Riesenberg, A. N. and Brown, N. L. (2006). Math5 is required for both early retinal neuron differentiation and cell cycle progression. Dev. Biol. 295, 764-778.
27. Liu, M., Pereira, F. A., Price, S. D., Chu, M.-J., Shope, C., Himes, D., Eatock, R. A., Brownell, W. E., Lysakowski, A. and Tsai, M. J. (2000). Essential role of BETA2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev. 14, 2839-2854.
28. Liu, H., Etter, P., Hayes, S., Jones, I., Nelson, B., Hartman, B., Forrest, D. and Reh, T. A. (2008). NeuroD1 regulates expression of thyroid hormone receptor 2 and cone opsins in the developing mouse retina. J. Neurosci. 28, 749-756.
29. Livesey, F. J. and Cepko, C. L. (2001). Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2, 109-118.
30. Mao, C. A., Kiyama, T., Pan, P., Furuta, Y., Hadjantonakis, A. K. and Klein, W. H. (2008a). Eomesodermin, a target gene of Pou4f2, is required for retinal ganglion cell and optic nerve development in the mouse. Development 135, 271-280.
31. Mao, C. A., Wang, S. W., Pan, P. and Klein, W. H. (2008b). Rewiring the retinal ganglion cell gene regulatory network: Neurod1 promotes retinal ganglion cell fate in the absence of Math5. Development 135, 3379-3388.
32. Moore, K. B., Schneider, M. L. and Vetter, M. L. (2002). Posttranslational mechanisms control the timing of bHLH function and regulate retinal cell fate. Neuron 34, 183-195.
33. Moshiri, A., Gonzalez, E., Tagawa, K., Maeda, H., Wang, M., Frishman, L. J. and Wang, S. W. (2008). Near complete loss of retinal ganglion cells in the math5/brn3b double knockout elicits severe reductions of other cell types during retinal development. Dev. Biol. 316, 214-227.
34. Mu, X., Fu, X., Beremand, P. D., Thomas, T. L. and Klein, W. H. (2008). Gene regulation logic in retinal ganglion cell development: Isl1 defines a critical branch distinct from but overlapping with Pou4f2. Proc. Natl. Acad. Sci. USA 105, 6942-6947.
35. Mullen, A. C., Orlando, D. A., Newman, J. J., Lovén, J., Kumar, R. M., Bilodeau, S., Reddy, J., Guenther, M. G., DeKoter, R. P. and Young, R. A. (2011). Master transcription factors determine cell-type-specific responses to TGF-β signaling. Cell 147, 565-576.
36. Ohsawa, R. and Kageyama, R. (2008). Regulation of retinal cell fate specification by multiple transcription factors. Brain Res. 1192, 90-98.
37. Onishi, A., Peng, G. H., Chen, S. and Blackshaw, S. (2010). Pias3-dependent SUMOylation controls mammalian cone photoreceptor differentiation. Nat. Neurosci. 13, 1059-1065.
38. Oster, S. F., Deiner, M., Birgbauer, E. and Sretavan, D. W. (2004). Ganglion cell axon pathfinding in the retina and optic nerve. Semin. Cell Dev. Biol. 15, 125-136.
39. 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.
40. 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.
41. Prasov, L., Nagy, M., Rudolph, D. D. and Glaser, T. (2012). Math5 (Atoh7) gene dosage limits retinal ganglion cell genesis. Neuroreport 23, 631-634.
42. Püschel, A. W. and Betz, H. (1995). Neurexins are differentially expressed in the embryonic nervous system of mice. J. Neurosci. 15, 2849-2856.
43. Raper, J. and Mason, C. (2010). Cellular strategies of axonal pathfinding. Cold Spring Harb. Perspect. Biol. 2, a001933.
44. Robson, J. G. and Frishman, L. J. (1995). Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis. Neurosci. 12, 837-850.
45. Robson, J. G., Maeda, H., Saszik, S. M. and Frishman, L. J. (2004). In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Res. 44, 3253-3268.
46. Rodieck, R. W. (1998). The First Steps in Seeing. Sunderland, MA: Sinauer Associates.
47. Roger, J. E., Nellissery, J., Kim, D. S. and Swaroop, A. (2010). Sumoylation of bZIP transcription factor NRL modulates target gene expression during photoreceptor differentiation. J. Biol. Chem. 285, 25637-25644.
48. Saszik, S. M., Robson, J. G. and Frishman, L. J. (2002). The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J. Physiol. 543, 899-916.
49. 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.
50. Trompouki, E., Bowman, T. V., Lawton, L. N., Fan, Z. P., Wu, D. C., DiBiase, A., Martin, C. S., Cech, J. N., Sessa, A. K., Leblanc, J. L. et al. (2011). Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 147, 577-589.
51. Tsai, W. W., Wang, Z., Yiu, T. T., Akdemir, K. C., Xia, W., Winter, S., Tsai, C. Y., Shi, X., Schwarzer, D., Plunkett, W. et al. (2010). TRIM24 links a non-canonical histone signature to breast cancer. Nature 468, 927-932.
52. Vetter, M. L. and Brown, N. L. (2001). The role of basic helix-loop-helix genes in vertebrate retinogenesis. Semin. Cell Dev. Biol. 12, 491-498.
53. Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F. et al. (2009). ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858.
54. Wallace, V. A. (2011). Making a retina-from the building blocks to clinical application. Stem Cells 29, 412-417.
55. Wang, S. W., Kim, B. S., Ding, K., Wang, H., Sun, D., Johnson, R. L., Klein, W. H. and Gan, L. (2001). Requirement for math5 in the development of retinal ganglion cells. Genes Dev. 15, 24-29.
56. Yang, Z., Ding, K., Pan, L., Deng, M. and Gan, L. (2003). Math5 determines the competence state of retinal ganglion cell progenitors. Dev. Biol. 264, 240-254.