The role of the Rx homeobox gene in retinal progenitor proliferation and cell fate specification

Mechanisms of Development

Volumn 151, Issue , 2018, Pages 18-29

  Rodgers, H M ^a,d   Huffman, V J ^a,b   Voronina, V A ^a,c,e   Lewandoski, M ^c   Mathers, P H ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d EAST CAROLINA UNIVERSITY   (United States)

^e REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL FATE; CELL LABELING; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENETIC ANALYSIS; MOUSE; MUELLER CELL; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; RETINA CELL; RETINA CONE; RETINA DEVELOPMENT; RETINA NERVE CELL; RETINAL PROGENITOR CELL; RX GENE; ANIMAL; ANOPHTHALMIA; CELL DIFFERENTIATION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; RETINA; STEM CELL;

EYE PROTEIN; HOMEODOMAIN PROTEIN; RX PROTEIN, MOUSE;

ANIMALS; ANOPHTHALMOS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; STEM CELLS;

EID: 85046042089     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2018.04.003     Document Type: Article

References (43)

1. Abouzeid, H., Youssef, M.A., Bayoumi, N., ElShakankiri, N., Marzouk, I., Hauser, P., Schorderet, D.F., RAX and anophthalmia in humans: evidence of brain anomalies. Mol. Vis. 18 (2012), 1449–1456.
2. Andreazzoli, M., Gestri, G., Cremisi, F., Casarosa, S., Dawid, I.B., Barsacchi, G., Xrx1 controls proliferation and neurogenesis in Xenopus anterior neural plate. Development 130 (2003), 5143–5154.
3. Bailey, T.J., El-Hodiri, H., Zhang, L., Shah, R., Mathers, P.H., Jamrich, M., Regulation of vertebrate eye development by Rx genes. Int. J. Dev. Biol. 48 (2004), 761–770.
4. Burmeister, M., Novak, J., Liang, M.-Y., Basu, S., Ploder, L., Hawes, N.L., Vidgen, D., Hoover, F., Goldman, D., Kalnins, V.I., Roderick, T.H., Taylor, B.A., Hankin, M.H., Mclnnes, R.R., Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat. Genet. 12 (1996), 376–384.
5. Carter-Dawson, L.D., LaVail, M.M., Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritiated thymidine. J. Comp. Neurol. 188 (1979), 263–272.
6. Casarosa, S., Amato, M.A., Andreazzoli, M., Gestri, G., Barsacchi, G., Cremisi, F., Xrx1 controls proliferation and multipotency of retinal progenitors. Mol. Cell. Neurosci. 22 (2003), 25–36.
7. Chassaing, N. et al., Molecular findings and clinical data in a cohort of 150 patients with anophthalmia/microphthalmia. Clin. Genet. 86 (2014), 326–334.
8. 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.
9. Cwinn, M.A., Mazerolle, C., McNeill, B., Ringuette, R., Thurig, S., Hui, C., Wallace, V.A., Suppressor of fused is required to maintain the multipotency of neural progenitor cells in the retina. J. Neurosci. 31 (2011), 5169–5180.
10. de Melo, J., Zibetti, C., Clark, B.S., Hwang, W., Miranda-Angulo, A.L., Qian, J., Blackshaw, S., Lhx2 is an essential factor for retinal gliogenesis and notch signaling. J. Neurosci., 36, 2016.
11. Dyer, M.A., Cepko, C.L., Regulating proliferation during retinal development. Nat. Rev. Neurosci. 2 (2001), 333–342.
12. Furukawa, T., Kozak, C.A., Cepko, C.L., Rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 3088–3093.
13. Gonzalez-Rodriguez, J., Pelcastre, E.L., Tovilla-Canales, J.L., Garcia-Ortiz, J.E., Amato-Almanza, M., Villanueva-Mendoza, C., Espinosa-Mattar, Z., Zenteno, J.C., Mutational screening of CHX10, GDF6, OTX2, RAX and SOX2 genes in 50 unrelated microphthalmia-anophthalmia-coloboma (MAC) spectrum cases. Br. J. Ophthalmol. 94 (2010), 1100–1104.
14. Gordon, P.J., Yun, S., Clark, A.M., Monuki, E.S., Murtaugh, L.C., Levine, E.M., Lhx2 balances progenitor maintenance with neurogenic output and promotes competence state progression in the developing retina. J. Neurosci. 33 (2013), 12197–12207.
15. Gueta, K., David, A., Cohen, T., Menuchin-Lasowski, Y., Nobel, H., Narkis, G., Li, L., Love, P., de Melo, J., Blackshaw, S., Westphal, H., Ashery-Padan, R., The stage-dependent roles of Ldb1 and functional redundancy with Ldb2 in mammalian retinogenesis. Development 143 (2016), 4182–4192.
16. Howell, D.M., Morgan, W.J., Jarjour, A.A., Spirou, G.A., Berrebi, A.S., Kennedy, T.E., Mathers, P.H., Molecular guidance cues necessary for axon pathfinding from the ventral cochlear nucleus. J. Comp. Neurol. 504 (2007), 533–549.
17. Irie, S., Sanuki, R., Muranishi, Y., Kato, K., Chaya, T., Furukawa, T., Rax homeoprotein regulates photoreceptor cell maturation and survival in association with Crx in the postnatal mouse retina. Mol. Cell. Biol. 35 (2015), 2583–2596.
18. Jadhav, A.P., Mason, H.A., Cepko, C.L., Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development, 133, 2006.
19. Kimura, A., Singh, D., Wawrousek, E.F., Kikuchi, M., Nakamura, M., Shinohara, T., Both PCE-1/RX and OTX/CRX interactions are necessary for photoreceptor-specific gene expression. J. Biol. Chem. 275 (2000), 1152–1160.
20. Koike, C., Nishida, A., Akimoto, K., Nakaya, M., Noda, T., Ohno, S., Furukawa, T., Function of atypical protein kinase C in differentiating photoreceptors is required for proper lamination of mouse retina. J. Neurosci. 25 (2005), 10290–10298.
21. Lequeux, L., Rio, M., Vigouroux, A., Titeux, M., Etchevers, H., Malecaze, F., Chassaing, N., Calvas, P., Confirmation of RAX gene involvement in human anophthalmia. Clin. Genet. 74 (2008), 392–395.
22. London, N.J.S., Kessler, P., Williams, B., Pauer, G.J., Hagstrom, S.A., Traboulsi, E.I., Sequence alterations in RX in patients with microphthalmia, anophthalmia, and coloboma. Mol. Vis. 15 (2009), 162–167.
23. Mao, X., Fujiwara, Y., Chapdelaine, A., Yang, H., Orkin, S.H., Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood 97 (2001), 324–326.
24. Marquardt, T., Ashery-Padan, R., Andrejewski, N., Scardigli, R., Guillemot, F., Gruss, P., Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105 (2001), 43–55.
25. Marrs, G.S., Morgan, W.J., Howell, D.M., Spirou, G.A., Mathers, P.H., Embryonic origins of the mouse superior olivary complex. Dev. Neurobiol. 73 (2013), 384–398.
26. Mathers, P.H., Grinberg, A., Mahon, K.A., Jamrich, M., The Rx homeobox gene is essential for vertebrate eye development. Nature 387 (1997), 603–607.
27. Muranishi, Y., Terada, K., Inoue, T., Katoh, K., Tsujii, T., Sanuki, R., Kurokawa, D., Aizawa, S., Tamaki, Y., Furukawa, T., An essential role for RAX homeoprotein and NOTCH-HES signaling in Otx2 expression in embryonic retinal photoreceptor cell fate determination. J. Neurosci. 31 (2011), 16792–16807.
28. Nishida, A., Furukawa, A., Koike, C., Tano, Y., Aizawa, S., Matsuo, I., Furukawa, T., Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat. Neurosci. 6 (2003), 1255–1263.
29. Pan, Y., Nekkalapudi, S., Kelly, L.E., El-Hodiri, H.M., The Rx-like homeobox gene (Rx-L) is necessary for normal photoreceptor development. Invest. Ophthalmol. Vis. Sci. 47 (2006), 4245–4253.
30. Pan, Y., Martinez-De Luna, R.I., Lou, C.-H., Nekkalapudi, S., Kelly, L.E., Sater, A.K., El-Hodiri, H.M., Regulation of photoreceptor gene expression by the retinal homeobox (Rx) gene product. Dev. Biol. 339 (2010), 494–506.
31. Rapaport, D.H., Wong, L.L., Wood, E.D., Yasumura, D., LaVail, M.M., Timing and topography of cell genesis in the rat retina. J. Comp. Neurol. 474 (2004), 304–324.
32. Rodgers, H.M., Belcastro, M., Sokolov, M., Mathers, P.H., Embryonic markers of cone differentiation. Mol. Vis. 22 (2016), 1455–1467.
33. Rohde, K., Klein, D.C., Møller, M., Rath, M.F., Rax : developmental and daily expression patterns in the rat pineal gland and retina. J. Neurochem. 118 (2011), 999–1007.
34. Sakagami, K., Gan, L., Yang, X.-J., Distinct effects of hedgehog signaling on neuronal fate specification and cell cycle progression in the embryonic mouse retina. J. Neurosci. 29 (2009), 6932–6944.
35. Sokolov, M., Strissel, K.J., Leskov, I.B., Michaud, N.A., Govardovskii, V.I., Arshavsky, V.Y., Phosducin facilitates light-driven transducin translocation in rod photoreceptors. Evidence from the phosducin knockout mouse. J. Biol. Chem. 279 (2004), 19149–19156.
36. Soriano, P., Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999), 70–71.
37. Voronina, V.A., Kozhemyakina, E.A., O'Kernick, C.M., Kahn, N.D., Wenger, S.L., Linberg, J.V., Schneider, A.S., Mathers, P.H., Mutations in the human RAX homeobox gene in a patient with anophthalmia and sclerocornea. Hum. Mol. Genet. 13 (2004), 315–322.
38. Voronina, V.A., Kozlov, S., Mathers, P.H., Lewandoski, M., Conditional alleles for activation and inactivation of the mouse Rx homeobox gene. Genesis 41 (2005), 160–164.
39. Wang, Q., Chen, S., Esumi, N., Swain, P.K., Haines, H.S., Peng, G., Melia, B.M., McIntosh, I., Heckenlively, J.R., Jacobson, S.G., Stone, E.M., Swaroop, A., Zack, D.J., QRX, a novel homeobox gene, modulates photoreceptor gene expression. Hum. Mol. Genet. 13 (2004), 1025–1040.
40. Yaron, O., Farhy, C., Marquardt, T., Applebury, M., Ashery-Padan, R., Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133 (2006), 1367–1378.
41. Young, R.W., Cell differentiation in the retina of the mouse. Anat. Rec. 212 (1985), 199–205.
42. Zagozewski, J.L., Zhang, Q., Eisenstat, D.D., Genetic regulation of vertebrate eye development. Clin. Genet. 86 (2014), 453–460.
43. Zhang, L., Mathers, P.H., Jamrich, M., Function of Rx, but not Pax6, is essential for the formation of retinal progenitor cells in mice. Genesis 28 (2000), 135–142.