Transcriptional Activity of Neural Retina Leucine Zipper (Nrl) Is Regulated by c-Jun N-Terminal Kinase and Tip60 during Retina Development

REFERENCES

• Akimoto M, et al. 2006. Targeting of GFP to newborn rods by Nrl promoter and temporal expression profiling of flow-sorted photoreceptors. Proc. Natl. Acad. Sci. U. S. A. 103:3890–3895.
   PubMed Web of Science ®Google Scholar
• Brady ME, et al. 1999. Tip60 is a nuclear hormone receptor coactivator. J. Biol. Chem. 274:17599–17604.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Carter-Dawson LD, LaVail MM. 1979. Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritiated thymidine. J. Comp. Neurol. 188:263–272.
   PubMed Web of Science ®Google Scholar
• Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D. 1996. Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. U. S. A. 93:589–595.
   PubMed Web of Science ®Google Scholar
• Cheng H, et al. 2004. Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum. Mol. Genet. 13:1563–1575.
   PubMedGoogle Scholar
• Cvekl A, Mitton KP. 2010. Epigenetic regulatory mechanisms in vertebrate eye development and disease. Heredity 105:135–151.
   PubMedGoogle Scholar
• Davis RJ. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103:239–252.
   PubMed Web of Science ®Google Scholar
• DeAngelis MM, Grimsby JL, Sandberg MA, Berson EL, Dryja TP. 2002. Novel mutations in the NRL gene and associated clinical findings in patients with dominant retinitis pigmentosa. Arch. Ophthalmol. 120:369–375.
   PubMedGoogle Scholar
• Derijard B, et al. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025–1037.
   PubMed Web of Science ®Google Scholar
• Dong C, et al. 1998. Defective T cell differentiation in the absence of Jnk1. Science 282:2092–2095.
   PubMed Web of Science ®Google Scholar
• Donovan SL, Dyer MA. 2006. Preparation and square wave electroporation of retinal explant cultures. Nat. Protoc. 1:2710–2718.
   PubMed Web of Science ®Google Scholar
• Dyer MA, Cepko CL. 2001. Regulating proliferation during retinal development. Nat. Rev. Neurosci. 2:333–342.
   PubMedGoogle Scholar
• Friedman JS, et al. 2004. The minimal transactivation domain of the basic motif-leucine zipper transcription factor NRL interacts with TATA-binding protein. J. Biol. Chem. 279:47233–47241.
   PubMedGoogle Scholar
• Gaughan L, Brady ME, Cook S, Neal DE, Robson CN. 2001. Tip60 is a co-activator specific for class I nuclear hormone receptors. J. Biol. Chem. 276:46841–46848.
   PubMedGoogle Scholar
• Gavaravarapu S, Kamine J. 2000. Tip60 inhibits activation of CREB protein by protein kinase A. Biochem. Biophys. Res. Commun. 269:758–766.
   PubMedGoogle Scholar
• Guccione E, et al. 2006. Myc-binding-site recognition in the human genome is determined by chromatin context. Nat. Cell Biol. 8:764–770.
   PubMedGoogle Scholar
• Hellman LM, Fried MG. 2007. Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. Nat. Protoc. 2:1849–1861.
   PubMed Web of Science ®Google Scholar
• Hennig AK, Peng GH, Chen S. 2008. Regulation of photoreceptor gene expression by Crx-associated transcription factor network. Brain Res. 1192:114–133.
   PubMed Web of Science ®Google Scholar
• Heo YS, et al. 2004. Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125. EMBO J. 23:2185–2195.
   PubMed Web of Science ®Google Scholar
• Hibi M, Lin A, Smeal T, Minden A, Karin M. 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7:2135–2148.
   PubMed Web of Science ®Google Scholar
• Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293:1074–1080.
   PubMed Web of Science ®Google Scholar
• Jones DO, Cowell IG, Singh PB. 2000. Mammalian chromodomain proteins: their role in genome organisation and expression. Bioessays 22:124–137.
   PubMed Web of Science ®Google Scholar
• Kamine J, Elangovan B, Subramanian T, Coleman D, Chinnadurai G. 1996. Identification of a cellular protein that specifically interacts with the essential cysteine region of the HIV-1 Tat transactivator. Virology 216:357–366.
   PubMed Web of Science ®Google Scholar
• Kanda A, Friedman JS, Nishiguchi KM, Swaroop A. 2007. Retinopathy mutations in the bZIP protein NRL alter phosphorylation and transcriptional activity. Hum. Mutat. 28:589–598.
   PubMedGoogle Scholar
• Karin M. 1994. Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr. Opin. Cell Biol. 6:415–424.
   PubMed Web of Science ®Google Scholar
• Kim JW, et al. 2010. Neural retina leucine-zipper regulates the expression of Ppp2r5c, the regulatory subunit of protein phosphatase 2A, in photoreceptor development. FEBS J. 277:5051–5060.
   PubMedGoogle Scholar
• Kim JW, et al. 2008. TIP60 represses transcriptional activity of p73beta via an MDM2-bridged ternary complex. J. Biol. Chem. 283:20077–20086.
   PubMedGoogle Scholar
• Kobayashi M, Shimomura A, Hagiwara M, Kawakami K. 1997. Phosphorylation of ATF-1 enhances its DNA binding and transcription of the Na,K-ATPase alpha 1 subunit gene promoter. Nucleic Acids Res. 25:877–882.
   PubMedGoogle Scholar
• Kuan CY, et al. 1999. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22:667–676.
   PubMed Web of Science ®Google Scholar
• Li B, Carey M, Workman JL. 2007. The role of chromatin during transcription. Cell 128:707–719.
   PubMed Web of Science ®Google Scholar
• Liu J, et al. 2005. Distinct gene expression profiles and reduced JNK signaling in retinitis pigmentosa caused by RP1 mutations. Hum. Mol. Genet. 14:2945–2958.
   PubMedGoogle Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408.
   PubMed Web of Science ®Google Scholar
• Livesey FJ, Cepko CL. 2001. Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2:109–118.
   PubMed Web of Science ®Google Scholar
• MacLaren RE, et al. 2006. Retinal repair by transplantation of photoreceptor precursors. Nature 444:203–207.
   PubMed Web of Science ®Google Scholar
• Mears AJ, et al. 2001. Nrl is required for rod photoreceptor development. Nat. Genet. 29:447–452.
   PubMed Web of Science ®Google Scholar
• Mitton KP, et al. 2000. The leucine zipper of NRL interacts with the CRX homeodomain. A possible mechanism of transcriptional synergy in rhodopsin regulation. J. Biol. Chem. 275:29794–29799.
   PubMed Web of Science ®Google Scholar
• Mitton KP, et al. 2003. Interaction of retinal bZIP transcription factor NRL with Flt3-interacting zinc-finger protein Fiz1: possible role of Fiz1 as a transcriptional repressor. Hum. Mol. Genet. 12:365–373.
   PubMed Web of Science ®Google Scholar
• Nielsen PR, et al. 2002. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416:103–107.
   PubMed Web of Science ®Google Scholar
• Nishida A, et al. 2003. Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat. Neurosci. 6:1255–1263.
   PubMed Web of Science ®Google Scholar
• Oh EC, et al. 2008. Rod differentiation factor NRL activates the expression of nuclear receptor NR2E3 to suppress the development of cone photoreceptors. Brain Res. 1236:16–29.
   PubMed Web of Science ®Google Scholar
• Partington GA, Patient RK. 1999. Phosphorylation of GATA-1 increases its DNA-binding affinity and is correlated with induction of human K562 erythroleukaemia cells. Nucleic Acids Res. 27:1168–1175.
   PubMedGoogle Scholar
• Peng GH, Chen S. 2007. Crx activates opsin transcription by recruiting HAT-containing co-activators and promoting histone acetylation. Hum. Mol. Genet. 16:2433–2452.
   PubMedGoogle Scholar
• Roberts MR, Srinivas M, Forrest D, Morreale de Escobar G, Reh TA. 2006. Making the gradient: thyroid hormone regulates cone opsin expression in the developing mouse retina. Proc. Natl. Acad. Sci. U. S. A. 103:6218–6223.
   PubMedGoogle Scholar
• Roger JE, Nellissery J, Kim DS, Swaroop A. 2010. Sumoylation of bZIP transcription factor NRL modulates target gene expression during photoreceptor differentiation. J. Biol. Chem. 285:25637–25644.
   PubMedGoogle Scholar
• Sapountzi V, Logan IR, Robson CN. 2006. Cellular functions of TIP60. Int. J. Biochem. Cell Biol. 38:1496–1509.
   PubMedGoogle Scholar
• Sharrocks AD, Yang SH, Galanis A. 2000. Docking domains and substrate-specificity determination for MAP kinases. Trends Biochem. Sci. 25:448–453.
   PubMed Web of Science ®Google Scholar
• Sun Y, et al. 2009. Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol. 11:1376–1382.
   PubMed Web of Science ®Google Scholar
• Swain P, et al. 2007. Mutations associated with retinopathies alter mitogen-activated protein kinase-induced phosphorylation of neural retina leucine-zipper. Mol. Vis. 13:1114–1120.
   PubMedGoogle Scholar
• Swain PK, et al. 2001. Multiple phosphorylated isoforms of NRL are expressed in rod photoreceptors. J. Biol. Chem. 276:36824–36830.
   PubMed Web of Science ®Google Scholar
• Swaroop A, Kim D, Forrest D. 2010. Transcriptional regulation of photoreceptor development and homeostasis in the mammalian retina. Nat. Rev. Neurosci. 11:563–576.
   PubMed Web of Science ®Google Scholar
• Swaroop A, et al. 1992. A conserved retina-specific gene encodes a basic motif/leucine zipper domain. Proc. Natl. Acad. Sci. U. S. A. 89:266–270.
   PubMed Web of Science ®Google Scholar
• Sykes SM, et al. 2006. Acetylation of the p53 DNA-binding domain regulates apoptosis induction. Mol. Cell 24:841–851.
   PubMed Web of Science ®Google Scholar
• Tang Y, Luo J, Zhang W, Gu W. 2006. Tip60-dependent acetylation of p53 modulates the decision between cell-cycle arrest and apoptosis. Mol. Cell 24:827–839.
   PubMed Web of Science ®Google Scholar
• Thomas T, Loveland KL, Voss AK. 2007. The genes coding for the MYST family histone acetyltransferases, Tip60 and Mof, are expressed at high levels during sperm development. Gene Expr. Patterns 7:657–665.
   PubMedGoogle Scholar
• Turner DL, Cepko CL. 1987. A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131–136.
   PubMed Web of Science ®Google Scholar
• Weston CR, Davis RJ. 2002. The JNK signal transduction pathway. Curr. Opin. Genet. Dev. 12:14–21.
   PubMed Web of Science ®Google Scholar
• Weston CR, et al. 2003. JNK initiates a cytokine cascade that causes Pax2 expression and closure of the optic fissure. Genes Dev. 17:1271–1280.
   PubMed Web of Science ®Google Scholar
• Xia Y, Karin M. 2004. The control of cell motility and epithelial morphogenesis by Jun kinases. Trends Cell Biol. 14:94–101.
   PubMed Web of Science ®Google Scholar
• Xiao H, Chung J, Kao HY, Yang YC. 2003. Tip60 is a co-repressor for STAT3. J. Biol. Chem. 278:11197–11204.
   PubMed Web of Science ®Google Scholar
• Yang DD, et al. 1998. Differentiation of CD4+ T cells to Th1 cells requires MAP kinase JNK2. Immunity 9:575–585.
   PubMed Web of Science ®Google Scholar
• Yang DD, et al. 1997. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389:865–870.
   PubMed Web of Science ®Google Scholar
• Yang XJ. 2004. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32:959–976.
   PubMed Web of Science ®Google Scholar
• Yang XJ, Seto E. 2008. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell 31:449–461.
   PubMed Web of Science ®Google Scholar
• Young RW. 1985. Cell differentiation in the retina of the mouse. Anat. Rec. 212:199–205.
   PubMedGoogle Scholar