Rax homeoprotein regulates photoreceptor cell maturation and survival in association with crx in the postnatal mouse retina

Molecular and Cellular Biology

Volumn 35, Issue 15, 2015, Pages 2583-2596

  Irie, Shoichi ^a,b,c   Sanuki, Rikako ^a,b   Muranishi, Yuki ^a,b   Kato, Kimiko ^a,b   Chaya, Taro ^a,b   Furukawa, Takahisa ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CONE OPSIN; CRX PROTEIN; HOMEODOMAIN PROTEIN; MESSENGER RNA; OPSIN; RAX PROTEIN; RHODOPSIN; TAMOXIFEN; UNCLASSIFIED DRUG; CONE ROD HOMEOBOX PROTEIN; EYE PROTEIN; RAX PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GLIA CELL; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; LUCIFERASE ASSAY; MOUSE; MUELLER CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RETINA CONE; RETINA DEVELOPMENT; RETINA ROD; TRANSACTIVATION; 3T3 CELL LINE; ANIMAL; BIOSYNTHESIS; CELL LINE; GENETICS; GLIA; HEK293 CELL LINE; HUMAN; METABOLISM; TRANSCRIPTION INITIATION;

MUS; VERTEBRATA;

3T3 CELLS; ANIMALS; CELL LINE; CELL SURVIVAL; CONE OPSINS; EYE PROTEINS; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; NEUROGLIA; PROMOTER REGIONS, GENETIC; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; RHODOPSIN; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84936102343     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00048-15     Document Type: Article

References (47)

1. Cayouette M, Poggi L, Harris WA. 2006. Lineage in the vertebrate retina. Trends Neurosci 29:563-570. http://dx.doi.org/10.1016/j.tins.2006.08.003.
2. Livesey FJ, Cepko CL. 2001. Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2:109-118. http://dx.doi.org/10.1038/35053522.
3. Marquardt T, Gruss P. 2002. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci 25:32-38. http://dx.doi.org/10.1016/S0166-2236(00)02028-2.
4. Morrow EM, Furukawa T, Cepko CL. 1998. Vertebrate photoreceptor cell development and disease. Trends Cell Biol 8:353-358.
5. Muranishi Y, Terada K, Furukawa T. 2012. An essential role for Rax in retina and neuroendocrine system development. Dev Growth Differ 54: 341-348. http://dx.doi.org/10.1111/j.1440-169X.2012.01337.x.
6. Furukawa T, Kozak CA, Cepko CL. 1997. rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc Natl Acad Sci USA 94:3088-3093. http://dx.doi.org/10.1073/pnas.94.7.3088.
7. Mathers PH, Grinberg A, Mahon KA, Jamrich M. 1997. The Rx homeobox gene is essential for vertebrate eye development. Nature 387:603-607. http://dx.doi.org/10.1038/42475.
8. Bailey TJ, El-Hodiri H, Zhang L, Shah R, Mathers PH, Jamrich M. 2004. Regulation of vertebrate eye development by Rx genes. Int J Dev Biol 48:761-770. http://dx.doi.org/10.1387/ijdb.041878tb.
9. Voronina VA, Kozhemyakina EA, O'Kernick CM, Kahn ND, Wenger SL, Linberg JV, Schneider AS, Mathers PH. 2004. Mutations in the human RAX homeobox gene in a patient with anophthalmia and sclerocornea. Hum Mol Genet 13:315-322. http://dx.doi.org/10.1093/hmg/ddh025.
10. Andreazzoli M, Gestri G, Angeloni D, Menna E, Barsacchi G. 1999. Role of Xrx1 in Xenopus eye and anterior brain development. Development 126:2451-2460.
11. Chuang JC, Raymond PA. 2001. Zebrafish genes rx1 and rx2 help define the region of forebrain that gives rise to retina. Dev Biol 231:13-30. http://dx.doi.org/10.1006/dbio.2000.0125.
12. Terada K, Furukawa T. 2010. Sumoylation controls retinal progenitor proliferation by repressing cell cycle exit in Xenopus laevis. Dev Biol 347: 180-194. http://dx.doi.org/10.1016/j.ydbio.2010.08.023.
13. Terada K, Kitayama A, Kanamoto T, Ueno N, Furukawa T. 2006. Nucleosome regulator Xhmgb3 is required for cell proliferation of the eye and brain as a downstream target of Xenopus rax/Rx1. Dev Biol 291:398-412. http://dx.doi.org/10.1016/j.ydbio.2005.12.029.
14. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL. 2000. rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26:383-394. http://dx.doi.org/10.1016/S0896-6273(00)81171-X.
15. Kimura A, Singh D, Wawrousek EF, Kikuchi M, Nakamura M, Shinohara T. 2000. Both PCE-1/RX and OTX/CRX interactions are necessary for photoreceptor-specific gene expression. J Biol Chem 275:1152-1160. http://dx.doi.org/10.1074/jbc.275.2.1152.
16. Muranishi Y, Terada K, Inoue T, Katoh K, Tsujii T, Sanuki R, Kurokawa D, Aizawa S, Tamaki Y, Furukawa T. 2011. An essential role for RAX homeoprotein and NOTCH-HES signaling in Otx2 expression in embryonic retinal photoreceptor cell fate determination. J Neurosci 31: 16792-16807. http://dx.doi.org/10.1523/JNEUROSCI.3109-11.2011.
17. Nelson SM, Park L, Stenkamp DL. 2009. Retinal homeobox 1 is required for retinal neurogenesis and photoreceptor differentiation in embryonic zebrafish. Dev Biol 328:24-39. http://dx.doi.org/10.1016/j.ydbio.2008.12.040.
18. Pan Y, Martinez-De Luna RI, Lou CH, Nekkalapudi S, Kelly LE, Sater AK, El-Hodiri HM. 2010. Regulation of photoreceptor gene expression by the retinal homeobox (Rx) gene product. Dev Biol 339:494-506. http://dx.doi.org/10.1016/j.ydbio.2009.12.032.
19. Reks SE, McIlvain V, Zhuo X, Knox BE. 2014. Cooperative activation of Xenopus rhodopsin transcription by paired-like transcription factors. BMC Mol Biol 15:4. http://dx.doi.org/10.1186/1471-2199-15-4.
20. Chen CM, Cepko CL. 2002. The chicken RaxL gene plays a role in the initiation of photoreceptor differentiation. Development 129:5363-5375. http://dx.doi.org/10.1242/dev.00114.
21. Pan Y, Nekkalapudi S, Kelly LE, El-Hodiri HM. 2006. The Rx-like homeobox gene (Rx-L) is necessary for normal photoreceptor development. Invest Ophthalmol Vis Sci 47:4245-4253. http://dx.doi.org/10.1167/iovs.06-0167.
22. Wang QL, Chen S, Esumi N, Swain PK, Haines HS, Peng G, Melia BM, McIntosh I, Heckenlively JR, Jacobson SG, Stone EM, Swaroop A, Zack DJ. 2004. QRX, a novel homeobox gene, modulates photoreceptor gene expression. HumMol Genet 13:1025-1040. http://dx.doi.org/10.1093/hmg/ddh117.
23. Rojas-Munoz A, Dahm R, Nusslein-Volhard C. 2005. chokh/rx3 specifies the retinal pigment epithelium fate independently of eye morphogenesis. Dev Biol 288:348-362. http://dx.doi.org/10.1016/j.ydbio.2005.08.046.
24. Katoh K, Omori Y, Onishi A, Sato S, Kondo M, Furukawa T. 2010. Blimp1 suppresses Chx10 expression in differentiating retinal photoreceptor precursors to ensure proper photoreceptor development. J Neurosci 30:6515-6526. http://dx.doi.org/10.1523/JNEUROSCI.0771-10.2010.
25. Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M, Miyata K, Funabiki K, Koyasu T, Kajimura N, Miyoshi T, Sawai H, Kobayashi K, Tani A, Toda T, Usukura J, Tano Y, Fujikado T, Furukawa T. 2008. Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11:923-931. http://dx.doi.org/10.1038/nn.2160.
26. Sanuki R, Omori Y, Koike C, Sato S, Furukawa T. 2010. Panky, a novel photoreceptor-specific ankyrin repeat protein, is a transcriptional cofactor that suppresses CRX-regulated photoreceptor genes. FEBS Lett 584: 753-758. http://dx.doi.org/10.1016/j.febslet.2009.12.030.
27. Carter-Dawson LD, LaVail MM. 1979. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 188:245-262.
28. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D. 1996. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 93:589-595. http://dx.doi.org/10.1073/pnas.93.2.589.
29. Rapaport DH, Wong LL, Wood ED, Yasumura D, LaVail MM. 2004. Timing and topography of cell genesis in the rat retina. J Comp Neurol 474:304-324. http://dx.doi.org/10.1002/cne.20134.
30. Sherry DM, Wang MM, Bates J, Frishman LJ. 2003. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465:480-498. http://dx.doi.org/10.1002/cne.10838.
31. Furukawa T, Morrow EM, Li T, Davis FC, Cepko CL. 1999. Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat Genet 23:466-470. http://dx.doi.org/10.1038/70591.
32. Hsiau TH, Diaconu C, Myers CA, Lee J, Cepko CL, Corbo JC. 2007. The cis-regulatory logic of the mammalian photoreceptor transcriptional network. PLoS One 2:e643. http://dx.doi.org/10.1371/journal.pone.0000643.
33. Sanuki R, Onishi A, Koike C, Muramatsu R, Watanabe S, Muranishi Y, Irie S, Uneo S, Koyasu T, Matsui R, Chérasse Y, Urade Y, Watanabe D, Kondo M, Yamashita T, Furukawa T. 2011. miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat Neurosci 14:1125-1134. http://dx.doi.org/10.1038/nn.2897.
34. Trifunovic D, Dengler K, Michalakis S, Zrenner E, Wissinger B, Paquet-Durand F. 2010. cGMP-dependent cone photoreceptor degeneration in the cpfl1 mouse retina. J Comp Neurol 518:3604-3617. http://dx.doi.org/10.1002/cne.22416.
35. Robson JG, Frishman LJ. 1995. Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis Neurosci 12:837-850. http://dx.doi.org/10.1017/S0952523800009408.
36. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, Farhangfar F, Kage K, Krzystolik MG, Lyass LA, Robbins JT. 2000. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27:513-523. http://dx.doi.org/10.1016/S0896-6273(00)00062-3.
37. Szel A, Rohlich P, Caffe AR, van Veen T. 1996. Distribution of cone photoreceptors in the mammalian retina. Microsc Res Tech 35:445-462. http://dx.doi.org/10.1002/(SICI)1097-0029(19961215)35:6<445::AID-JEMT4>3.0.CO;2-H.
38. Chen S, Wang QL, Nie Z, Sun H, Lennon G, Copeland NG, Gilbert DJ, Jenkins NA, Zack DJ. 1997. Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19:1017-1030. http://dx.doi.org/10.1016/S0896-6273(00)80394-3.
39. Cheng H, Khanna H, Oh EC, Hicks D, Mitton KP, Swaroop A. 2004. Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum Mol Genet 13:1563-1575. http://dx.doi.org/10.1093/hmg/ddh173.
40. Lerner LE, Gribanova YE, Ji M, Knox BE, Farber DB. 2001. Nrl and Sp nuclear proteins mediate transcription of rod-specific cGMPphosphodiesterase beta-subunit gene: involvement of multiple response elements. J Biol Chem 276:34999-35007. http://dx.doi.org/10.1074/jbc.M103301200.
41. Pittler SJ, Zhang Y, Chen S, Mears AJ, Zack DJ, Ren Z, Swain PK, Yao S, Swaroop A, White JB. 2004. Functional analysis of the rod photoreceptor cGMP phosphodiesterase alpha-subunit gene promoter: Nrl and Crx are required for full transcriptional activity. J Biol Chem 279:19800-19807. http://dx.doi.org/10.1074/jbc.M401864200.
42. Rehemtulla A, Warwar R, Kumar R, Ji X, Zack DJ, Swaroop A. 1996. The basic motif-leucine zipper transcription factor Nrl can positively regulate rhodopsin gene expression. Proc Natl Acad Sci USA 93:191-195. http://dx.doi.org/10.1073/pnas.93.1.191.
43. Schulte JE, O'Brien CS, Conte MA, O'Quin KE, Carleton KL. 2014. Interspecific variation in Rx1 expression controls opsin expression and causes visual system diversity in African cichlid fishes. Mol Biol Evol 31: 2297-2308. http://dx.doi.org/10.1093/molbev/msu172.
44. Calvert PD, Krasnoperova NV, Lyubarsky AL, Isayama T, Nicolo M, Kosaras B, Wong G, Gannon KS, Margolskee RF, Sidman RL, Pugh EN, Jr, Makino CL, Lem J. 2000. Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proc Natl Acad Sci USA 97:13913-13918. http://dx.doi.org/10.1073/pnas.250478897.
45. Lem J, Krasnoperova NV, Calvert PD, Kosaras B, Cameron DA, Nicolo M, Makino CL, Sidman RL. 1999. Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc Natl Acad Sci USA 96:736-741. http://dx.doi.org/10.1073/pnas.96.2.736.
46. Tsang SH, Gouras P, Yamashita CK, Kjeldbye H, Fisher J, Farber DB, Goff SP. 1996. Retinal degeneration in mice lacking the gamma subunit of the rod cGMP phosphodiesterase. Science 272:1026-1029. http://dx.doi.org/10.1126/science.272.5264.1026.
47. Chang B, Grau T, Dangel S, Hurd R, Jurklies B, Sener EC, Andreasson S, Dollfus H, Baumann B, Bolz S, Artemyev N, Kohl S, Heckenlively J, Wissinger B. 2009. A homologous genetic basis of the murine cpfl1 mutant and human achromatopsia linked to mutations in the PDE6C gene. Proc Natl Acad Sci USA 106:19581-19586. http://dx.doi.org/10.1073/pnas.0907720106.