Fgf8 Expression and Degradation of Retinoic Acid Are Required for Patterning a High-Acuity Area in the Retina

Developmental Cell

Volumn 42, Issue 1, 2017, Pages 68-81.e6

  da Silva, Susana ^a   Cepko, Constance L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

chick; development; Fgf8; fovea; HAA; high acuity area; human; photoreceptor; RA; retinoic acid

Indexed keywords

FIBROBLAST GROWTH FACTOR 8; RETINOIC ACID; RNA;

ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELLULAR DISTRIBUTION; CHICK; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; HUMAN; HUMAN TISSUE; INTERNEURON; NERVE CELL; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RETINA; RETINA ROD; SIGNAL TRANSDUCTION; VISUAL ACUITY; ANIMAL; CHICK EMBRYO; CHICKEN; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; ORGANOGENESIS;

ANIMALS; BODY PATTERNING; CHICK EMBRYO; CHICKENS; DOWN-REGULATION; FIBROBLAST GROWTH FACTOR 8; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; ORGANOGENESIS; RETINA; RNA; SIGNAL TRANSDUCTION; TRETINOIN; VISUAL ACUITY;

EID: 85021166979     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2017.05.024     Document Type: Article

References (78)

1. Abramov, I., Gordon, J., Hendrickson, A., Hainline, L., Dobson, V., LaBossiere, E., The retina of the newborn human infant. Science 217 (1982), 265–267.
2. Abzhanov, A., Cordero, D.R., Sen, J., Tabin, C.J., Helms, J.A., Cross-regulatory interactions between Fgf8 and Shh in the avian frontonasal prominence. Congenit. Anom. (Kyoto) 47 (2007), 136–148.
3. Belecky-Adams, T., Briggs, C., Adler, R., Correlations between terminal mitosis and differentiated fate of retinal precursor cells in vivo and in vitro: analysis with the “‘window-labeling ’” technique. Dev. Biol. 315 (1996), 304–315.
4. Billings, N.A., Emerson, M.M., Cepko, C.L., Analysis of thyroid response element activity during retinal development. PLoS One, 5, 2010, e13739.
5. Bruhn, S.L., Cepko, C., Development of the pattern of photoreceptors in the chick retina. J. Neurosci. 16 (1996), 1430–1439.
6. Burmeister, M., Novak, J., Liang, M.Y., Basu, S., Ploder, L., Hawes, N.L., Vidgen, D., Hoover, F., Goldman, D., Kalnins, V.I., et al. Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat. Genet. 12 (1996), 376–384.
7. Cepko, C., Intrinsically different retinal progenitor cells produce specific types of progeny. Nat. Rev. Neurosci. 15 (2014), 615–627.
8. Cepko, C., The determination of rod and cone photoreceptor fate. Annu. Rev. Vis. 1 (2015), 211–234.
9. Chen, C.-M.A., Cepko, C.L., The chicken RaxL gene plays a role in the initiation of photoreceptor differentiation. Development 129 (2002), 5363–5375.
10. Cicconet, M., Geiger, D. & Gunsalus, K. (2013). Wavelet-based circular hough transform and its application in embryo developmental analysis. VISAPP 2013 – Proceedings of the International Conference on Computer Vision Theory and Applications, 1, 669–674.
11. Crossley, P.H., Martin, G.R., The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121 (1995), 439–451.
12. Crossley, P.H., Martinez, S., Ohkubo, Y., Rubenstein, J.L., Coordinate expression of Fgf8, Otx2, BMP4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience 108 (2001), 183–206.
13. Cunningham, T.J., Duester, G., Mechanisms of retinoic acid signalling and its roles in organ and limb development. Nat. Rev. 16 (2015), 110–123.
14. Dacey, D.M., The mosaic of midget ganglion cells in the human retina. J. Neurosci. 13 (1993), 5334–5355.
15. de Thé H., Vivanco-Ruiz, M.M., Tiollais, P., Stunnenberg, H., Dejean, A., Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature 343 (1990), 177–180.
16. Dyer, M.A., Martins, R., da Silva Filho, M., Muniz, J.A., Silveira, L.C., Cepko, C.L., Finlay, B.L., Developmental sources of conservation and variation in the evolution of the primate eye. Proc. Natl. Acad. Sci. USA 106 (2009), 8963–8968.
17. Ehrlich, D., Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer. J. Comp. Neurol. 195 (1981), 643–657.
18. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., Sasai, Y., Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472 (2011), 51–56.
19. Fite, K.V., Rosenfield-Wessels, S., A comparative study of deep avian foveas. Brain Behav. Evol. 12 (1975), 97–115.
20. Gierut, J.J., Jacks, T.E., Haigis, K.M., Whole-mount X-gal staining of mouse tissues. Cold Spring Harb. Protoc. 2014 (2014), 417–419.
21. Gonzalez-Cordero, A., West, E.L., Pearson, R.A., Duran, Y., Carvalho, L.S., Chu, C.J., Naeem, A., Blackford, S.J., Georgiadis, A., Lakowski, J., et al. Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat. Biotechnol. 31 (2013), 741–747.
22. Hamburger, V., Hamilton, H.L., A series of normal stages in the development of the chick embryo. J. Morphol. 88 (1951), 49–92.
23. Harpavart, S., Cepko, C.L., RCAS-RNAi: a loss-of-function method for the developing chick retina. BMC Dev. Biol., 6, 2006, 10.1186/1471-213X-6-2.
24. Hendrickson, A., A morphological comparison of foveal development in man and monkey. Eye 6 (1992), 136–144.
25. Hendrickson, A., Development of retinal layers in prenatal human retina. Am. J. Ophthalmol. 161 (2016), 29–35.e1.
26. Hendrickson, A., Kupfer, C., The histogenesis of the fovea in the macaque monkey. Invest. Ophthalmol. Vis. Sci. 15 (1976), 746–756.
27. Hendrickson, A.E., Yuodelis, C., The morphological development of the human fovea. Ophthalmology 91 (1984), 603–612.
28. Hendrickson, A., Zhang, C., Development of cone photoreceptors and their synapses in the human and monkey fovea. J. Comp. Neurol., 2017 http://doi.wiley.com/10.1002/cne.24170.
29. Hendrickson, A., Bumsted-O'Brien, K., Natoli, R., Ramamurthy, V., Possin, D., Provis, J., Rod photoreceptor differentiation in fetal and infant human retina. Exp. Eye Res. 87 (2008), 415–426.
30. Hughes, A., The topography of vision in mammals of contrasting life styles: comparative optics and retinal organization. Crescitelli, F., (eds.) Handbook of Sensory Physiology, 1977, Springer-Verlag, 613–756.
31. Hyatt, G.A., Schmitt, E.A., Marsh-Armstrong, N.R., Dowling, J.E., Retinoic acid-induced duplication of the zebrafish retina. Proc. Natl. Acad. Sci. USA 89 (1992), 8293–8297.
32. Hyatt, G.A., Schmitt, E.A., Fadool, J.M., Dowling, J.E., Retinoic acid alters photoreceptor development in vivo. Proc. Natl. Acad. Sci. USA 93 (1996), 13298–13303.
33. Inzunza, O., Bravo, H., Smith, R.L., Foveal regions of bird retinas correlate with the aster of the inner nuclear layer. Anat. Rec. 223 (1989), 342–346.
34. Jacob, M., Unser, M., Design of steerable filters for feature detection using canny-like criteria. IEEE Trans. Pattern Anal. Mach. Intell. 26 (2004), 1007–1019.
35. Kelley, M.W., Turner, J.K., Reh, T.A., Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120 (1994), 2091–2102.
36. Khanna, H., Akimoto, M., Siffroi-Fernandez, S., Friedman, J.S., Hicks, D., Swaroop, A., Retinoic acid regulates the expression of photoreceptor transcription factor NRL. J. Biol. Chem. 281 (2006), 27327–27334.
37. Kim, J.-W., Yang, H.J., Oel, A.P., Brooks, M.J., Jia, L., Plachetzki, D.C., Li, W., Allison, W.T., Swaroop, A., Recruitment of rod photoreceptors from short-wavelength-sensitive cones during the evolution of nocturnal vision in mammals. Dev. Cell 37 (2016), 520–532.
38. Kumar, S., Duester, G., Retinoic acid controls body axis extension by directly repressing Fgf8 transcription. Development 141 (2014), 2972–2977.
39. Lovicu, F.J., Overbeek, P.A., Overlapping effects of different FGF family members on lens fiber differentiation in transgenic mice. Invest. Ophthalmol. Vis. Sci. 38 (1997), 3365–3377.
40. Loy, G., Zelinsky, A., Fast radial symmetry for detecting points of interest. IEEE Trans. Pattern Anal. Mach. Intell. 25 (2003), 959–973.
41. Luo, T., Sakai, Y., Wagner, E., Dräger, U.C., Retinoids, eye development, and maturation of visual function. J. Neurobiol. 66 (2006), 677–686.
42. Maden, M., Retinoid signalling in the development of the central nervous system. Nat. Rev. 3 (2002), 843–853.
43. Mann, I.C., The process of differentiation of the retinal layers in vertebrates. Br. J. Ophthalmol. 12 (1928), 449–478.
44. Mann, I., The development of the human eye. The Development of the Human Eye, 1964, Grune & Stratton, 69–150.
45. Mark, M., Ghyselinck, N.B., Chambon, P., Function of retinoic acid receptors during embryonic development. Nucl. Recept. Signal., 7, 2009, e002.
46. Martinez-Morales, J.R., Del Bene, F., Nica, G., Hammerschmidt, M., Bovolenta, P., Wittbrodt, J., Differentiation of the vertebrate retina is coordinated by an FGF signaling center. Dev. Cell 8 (2005), 565–574.
47. Matt, N., Dupé V., Garnier, J.M., Dennefeld, C., Chambon, P., Mark, M., Ghyselinck, N.B., Retinoic acid-dependent eye morphogenesis is orchestrated by neural crest cells. Development 132 (2005), 4789–4800.
48. McCaffery, P., Lee, M.O., Wagner, M.A., Sladek, N.E., Dräger, U.C., Asymmetrical retinoic acid synthesis in the dorsoventral axis of the retina. Development 115 (1992), 371–382.
49. Mears, A.J., Kondo, M., Swain, P.K., Takada, Y., Bush, R.A., Saunders, T.L., Sieving, P.A., Swaroop, A., Nrl is required for rod photoreceptor development. Nat. Genet. 29 (2001), 447–452.
50. Mey, J., McCaffery, P., Klemeit, M., Sources and sink of retinoic acid in the embryonic chick retina: distribution of aldehyde dehydrogenase activities, CRABP-I, and sites of retinoic acid inactivation. Dev. Brain Res. 127 (2001), 135–148.
51. Mitchell, D.M., Stevens, C.B., Frey, R.A., Hunter, S.S., Ashino, R., Kawamura, S., Stenkamp, D.L., Retinoic acid signaling regulates differential expression of the tandemly-duplicated long wavelength-sensitive cone opsin genes in zebrafish. PLoS Genet., 11, 2015, e1005483.
52. Moore, B.A., Kamilar, J.M., Collin, S.P., Bininda-Emonds, O.R., Dominy, N.J., Hall, M.I., Heesy, C.P., Johnsen, S., Lisney, T.J., Loew, E.R., et al. A novel method for comparative analysis of retinal specialization traits from topographic maps. J. Vis. 12 (2012), 1–24.
53. Morris, V.B., An afoveate area centralis in the chick retina. J. Comp. Neurol. 210 (1982), 198–203.
54. Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M., Sasai, Y., Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10 (2012), 771–785.
55. Nelson, D.R., Goldstone, J.V., Stegeman, J.J., The cytochrome P450 genesis locus: the origin and evolution of animal cytochrome P450s. Philos. Trans. R. Soc. Lond. B Biol. Sci., 368, 2013, 20120474.
56. Osakada, F., Ikeda, H., Mandai, M., Wataya, T., Watanabe, K., Yoshimura, N., Akaike, A., Sasai, Y., Takahashi, M., Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat. Biotechnol. 26 (2008), 215–224.
57. Perz-Edwards, A., Hardison, N.L., Linney, E., Retinoic acid-mediated gene expression in transgenic reporter zebrafish. Dev. Biol. 229 (2001), 89–101.
58. Peters, M.A., Cepko, C.L., The dorsal – ventral axis of the neural retina is divided into multiple domains of restricted gene expression which exhibit features of lineage compartments. Dev. Biol. 251 (2002), 59–73.
59. Prada, C., Puga, J., Pérez-Méndez, L., López, R., Ramírez, G., Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci. 3 (1991), 559–569.
60. Provis, J.M., Diaz, C.M., Dreher, B., Ontogeny of the primate fovea: a central issue in retinal development. Prog. Neurobiol. 54 (1998), 549–580.
61. Provis, J.M., Dubis, A.M., Maddess, T., Carroll, J., Adaptation of the central retina for high acuity vision: cones, the fovea and the a vascular zone. Prog. Retin. Eye Res. 35 (2013), 63–81.
62. Querubin, A., Lee, H.R., Provis, J.M., O'Brien, K.M., Photoreceptor and ganglion cell topographies correlate with information convergence and high acuity regions in the adult pigeon (Columba livia) retina. J. Comp. Neurol. 517 (2009), 711–722.
63. Reijntjes, S., Gale, E., Maden, M., Expression of the retinoic acid catabolising enzyme CYP26B1 in the chick embryo and its regulation by retinoic acid. Gene Expr. Patterns 3 (2003), 621–627.
64. Rhinn, M., Dolle, P., Retinoic acid signalling during development. Development 139 (2012), 843–858.
65. Rodrigues, T., Krawczyk, M., Skowronska-Krawczyk, D., Matter-Sadzinski, L., Matter, J.M., Delayed neurogenesis with respect to eye growth shapes the pigeon retina for high visual acuity. Development 143 (2016), 4701–4712.
66. Rossant, J., Zirngibl, R., Cado, D., Shago, M., Giguere, V., Expression of retinoic acid response element-hsp lacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 5 (1991), 1333–1344.
67. Schulte, D., Peters, M.A., Sen, J., Cepko, C.L., The rod photoreceptor pattern is set at the optic vesicle stage and requires spatially restricted cvax expression. J. Neurosci. 25 (2005), 2823–2831.
68. Sen, J., Harpavat, S., Peters, M.A., Cepko, C.L., Retinoic acid regulates the expression of dorsoventral topographic guidance molecules in the chick retina. Development 23 (2005), 5147–5159.
69. Slonaker, J.R., A Comparative Study of the Area of Acute Vision in Vertebrates. 1897, The Athenaeum Press.
70. Stenkamp, D.L., Gregory, J.K., Adler, R., Retinoid effects in purified cultures of chick embryo retina neurons and photoreceptors. Invest. Ophthalmol. Vis. Sci. 34 (1993), 2425–2436.
71. Stevens, C.B., Cameron, D.A., Stenkamp, D.L., Plasticity of photoreceptor-generating retinal progenitors revealed by prolonged retinoic acid exposure. BMC Dev. Biol., 11, 2011, 51.
72. Straznicky, C., Chehade, M., The formation of the area centralis of the retinal ganglion cell layer in the chick. Development 100 (1987), 411–420.
73. Vogel-Höpker, A., Momose, T., Rohrer, H., Yasuda, K., Ishihara, L., Rapaport, D.H., Multiple functions of fibroblast growth factor-8 (FGF-8) in chick eye development. Mech. Dev. 94 (2000), 25–36.
74. Wagner, M., Han, B., Jessell, T.M., Regional differences in retinoid release from embryonic neural tissue detected by an in vitro reporter assay. Development 116 (1992), 55–66.
75. Walls, G.L., The Vertebrate Eye and Its Adaptive Radiation. 1942, Cranbrook Institute of Science.
76. Wassle, H., Boycott, B.B., Functional architecture of the mammalian retina. Physiol. Rev. 71 (1991), 447–480.
77. Van Wauwe, J., Van Nyen, G., Coene, M.C., Stoppie, P., Cools, W., Goossens, J., Borghgraef, P., Janssen, P.A., Liarozole, an inhibitor of retinoic acid metabolism, exerts retinoid-mimetic effects in vivo. J. Pharmacol. Exp. Ther. 261 (1992), 773–779.
78. Wilson, J.G., Roth, C.B., Warkany, J., An analysis of the syndrome of malformations induced by maternal vitamin a deficiency. effects of restoration of vitamin a at various times during gestation. Am. J. Anat. 92 (1953), 189–217.