MEF2D drives photoreceptor development through a genome-wide competition for tissue-specific enhancers

Neuron

Volumn 86, Issue 1, 2015, Pages 247-263

  Andzelm, Milena M ^a   Cherry, Timothy J ^a   Harmin, David A ^a   Boeke, Annabel C ^a   Lee, Charlotte ^a   Hemberg, Martin ^b   Pawlyk, Basil ^a   Malik, Athar N ^a   Flavell, Steven W ^a   Sandberg, Michael A ^a   Raviola, Elio ^a   Greenberg, Michael E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOCYTE ENHANCER FACTOR 2D; PROTEIN CRX; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CONE ROD HOMEOBOX PROTEIN; EYE PROTEIN; GREEN FLUORESCENT PROTEIN; HOMEODOMAIN PROTEIN; MEF2D PROTEIN, MOUSE; MYOCYTE ENHANCER FACTOR 2; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL SPECIFICITY; CONSENSUS SEQUENCE; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; GENE CONTROL; GENE EXPRESSION; IN VITRO STUDY; MOUSE; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RETINA; TISSUE SPECIFICITY; AGE; ANIMAL; C57BL MOUSE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; ELECTRORETINOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; MAMMALIAN EMBRYO; METABOLISM; MUTATION; NEWBORN; PHYSIOLOGY; VISUAL ADAPTATION;

ADAPTATION, OCULAR; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CHROMATIN IMMUNOPRECIPITATION; ELECTRORETINOGRAPHY; EMBRYO, MAMMALIAN; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; MEF2 TRANSCRIPTION FACTORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; PHOTORECEPTOR CELLS; RETINA; TRANS-ACTIVATORS;

EID: 84930339882     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.02.038     Document Type: Article

References (53)

1. Amiel J., Rio M., de Pontual L., Redon R., Malan V., Boddaert N., Plouin P., Carter N.P., Lyonnet S., Munnich A., Colleaux L. Mutations in TCF4, encoding a class I basic helix-loop-helix transcription factor, are responsible for Pitt-Hopkins syndrome, a severe epileptic encephalopathy associated with autonomic dysfunction. Am. J. Hum. Genet. 2007, 80:988-993.
2. Barbosa A.C., Kim M.S., Ertunc M., Adachi M., Nelson E.D., McAnally J., Richardson J.A., Kavalali E.T., Monteggia L.M., Bassel-Duby R., Olson E.N. MEF2C, a transcription factor that facilitates learning and memory by negative regulation of synapse numbers and function. Proc. Natl. Acad. Sci. USA 2008, 105:9391-9396.
3. Bienvenu T., Diebold B., Chelly J., Isidor B. Refining the phenotype associated with MEF2C point mutations. Neurogenetics 2013, 14:71-75.
4. Black B.L., Ligon K.L., Zhang Y., Olson E.N. Cooperative transcriptional activation by the neurogenic basic helix-loop-helix protein MASH1 and members of the myocyte enhancer factor-2 (MEF2) family. J.Biol. Chem. 1996, 271:26659-26663.
5. Chen S., Wang Q.L., Nie Z., Sun H., Lennon G., Copeland N.G., Gilbert D.J., Jenkins N.A., Zack D.J. Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 1997, 19:1017-1030.
6. Cole C.J., Mercaldo V., Restivo L., Yiu A.P., Sekeres M.J., Han J.H., Vetere G., Pekar T., Ross P.J., Neve R.L., et al. MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat. Neurosci. 2012, 15:1255-1264.
7. Corbo J.C., Lawrence K.A., Karlstetter M., Myers C.A., Abdelaziz M., Dirkes W., Weigelt K., Seifert M., Benes V., Fritsche L.G., et al. CRX ChIP-seq reveals the cis-regulatory architecture of mouse photoreceptors. Genome Res. 2010, 20:1512-1525.
8. Cosgrove D., Zallocchi M. Usher protein functions in hair cells and photoreceptors. Int. J. Biochem. Cell Biol. 2014, 46:80-89.
9. Creyghton M.P., Cheng A.W., Welstead G.G., Kooistra T., Carey B.W., Steine E.J., Hanna J., Lodato M.A., Frampton G.M., Sharp P.A., et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA 2010, 107:21931-21936.
10. Edmondson D.G., Cheng T.C., Cserjesi P., Chakraborty T., Olson E.N. Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2. Mol. Cell. Biol. 1992, 12:3665-3677.
11. Escher P., Schorderet D.F., Cottet S. Altered expression of the transcription factor Mef2c during retinal degeneration in Rpe65-/- mice. Invest. Ophthalmol. Vis. Sci. 2011, 52:5933-5940.
12. Flavell S.W., Cowan C.W., Kim T.K., Greer P.L., Lin Y., Paradis S., Griffith E.C., Hu L.S., Chen C., Greenberg M.E. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 2006, 311:1008-1012.
13. Flavell S.W., Kim T.K., Gray J.M., Harmin D.A., Hemberg M., Hong E.J., Markenscoff-Papadimitriou E., Bear D.M., Greenberg M.E. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 2008, 60:1022-1038.
14. Freund C.L., Gregory-Evans C.Y., Furukawa T., Papaioannou M., Looser J., Ploder L., Bellingham J., Ng D., Herbrick J.A., Duncan A., et al. Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell 1997, 91:543-553.
15. Fuchs S., Nakazawa M., Maw M., Tamai M., Oguchi Y., Gal A. A homozygous 1-base pair deletion in the arrestin gene is a frequent cause of Oguchi disease in Japanese. Nat. Genet. 1995, 10:360-362.
16. Furukawa T., Morrow E.M., Cepko C.L. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 1997, 91:531-541.
17. Furukawa T., Morrow E.M., Li T., Davis F.C., Cepko C.L. Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat. Genet. 1999, 23:466-470.
18. Hao H., Tummala P., Guzman E., Mali R.S., Gregorski J., Swaroop A., Mitton K.P. The transcription factor neural retina leucine zipper (NRL) controls photoreceptor-specific expression of myocyte enhancer factor Mef2c from an alternative promoter. J.Biol. Chem. 2011, 286:34893-34902.
19. Hao H., Kim D.S., Klocke B., Johnson K.R., Cui K., Gotoh N., Zang C., Gregorski J., Gieser L., Peng W., et al. Transcriptional regulation of rod photoreceptor homeostasis revealed by invivo NRL targetome analysis. PLoS Genet. 2012, 8:e1002649.
20. Heinz S., Benner C., Spann N., Bertolino E., Lin Y.C., Laslo P., Cheng J.X., Murre C., Singh H., Glass C.K. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 2010, 38:576-589.
21. Hong E.J., McCord A.E., Greenberg M.E. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 2008, 60:610-624.
22. Hsiau T.H., Diaconu C., Myers C.A., Lee J., Cepko C.L., Corbo J.C. The cis-regulatory logic of the mammalian photoreceptor transcriptional network. PLoS ONE 2007, 2:e643.
23. Huang W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
24. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
25. Jeon C.J., Strettoi E., Masland R.H. The major cell populations of the mouse retina. J.Neurosci. 1998, 18:8936-8946.
26. Johnson D.S., Mortazavi A., Myers R.M., Wold B. Genome-wide mapping of invivo protein-DNA interactions. Science 2007, 316:1497-1502.
27. Kim Y., Phan D., van Rooij E., Wang D.Z., McAnally J., Qi X., Richardson J.A., Hill J.A., Bassel-Duby R., Olson E.N. The MEF2D transcription factor mediates stress-dependent cardiac remodeling in mice. J.Clin. Invest. 2008, 118:124-132.
28. Kim T.K., Hemberg M., Gray J.M., Costa A.M., Bear D.M., Wu J., Harmin D.A., Laptewicz M., Barbara-Haley K., Kuersten S., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
29. Kohl S., Coppieters F., Meire F., Schaich S., Roosing S., Brennenstuhl C., Bolz S., van Genderen M.M., Riemslag F.C., Lukowski R., et al. A nonsense mutation in PDE6H causes autosomal-recessive incomplete achromatopsia. Am. J. Hum. Genet. 2012, 91:527-532. European Retinal Disease Consortium.
30. Li H., Radford J.C., Ragusa M.J., Shea K.L., McKercher S.R., Zaremba J.D., Soussou W., Nie Z., Kang Y.J., Nakanishi N., et al. Transcription factor MEF2C influences neural stem/progenitor cell differentiation and maturation invivo. Proc. Natl. Acad. Sci. USA 2008, 105:9397-9402.
31. Liu X., Wu B., Szary J., Kofoed E.M., Schaufele F. Functional sequestration of transcription factor activity by repetitive DNA. J.Biol. Chem. 2007, 282:20868-20876.
32. Molkentin J.D., Black B.L., Martin J.F., Olson E.N. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 1995, 83:1125-1136.
33. Nakagawa O., Arnold M., Nakagawa M., Hamada H., Shelton J.M., Kusano H., Harris T.M., Childs G., Campbell K.P., Richardson J.A., et al. Centronuclear myopathy in mice lacking a novel muscle-specific protein kinase transcriptionally regulated by MEF2. Genes Dev. 2005, 19:2066-2077.
34. Pan F., Ye Z., Cheng L., Liu J.O. Myocyte enhancer factor 2 mediates calcium-dependent transcription of the interleukin-2 gene in T lymphocytes: a calcium signaling module that is distinct from but collaborates with the nuclear factor of activated Tcells (NFAT). J.Biol. Chem. 2004, 279:14477-14480.
35. Payne A.M., Downes S.M., Bessant D.A., Taylor R., Holder G.E., Warren M.J., Bird A.C., Bhattacharya S.S. A mutation in guanylate cyclase activator 1A (GUCA1A) in an autosomal dominant cone dystrophy pedigree mapping to a new locus on chromosome 6p21.1. Hum. Mol. Genet. 1998, 7:273-277.
36. Pollock R., Treisman R. Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev. 1991, 5(12A):2327-2341.
37. Potthoff M.J., Olson E.N. MEF2: a central regulator of diverse developmental programs. Development 2007, 134:4131-4140.
38. Pulipparacharuvil S., Renthal W., Hale C.F., Taniguchi M., Xiao G., Kumar A., Russo S.J., Sikder D., Dewey C.M., Davis M.M., et al. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 2008, 59:621-633.
39. Rada-Iglesias A., Bajpai R., Swigut T., Brugmann S.A., Flynn R.A., Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470:279-283.
40. Sandmann T., Jensen L.J., Jakobsen J.S., Karzynski M.M., Eichenlaub M.P., Bork P., Furlong E.E. A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. Dev. Cell 2006, 10:797-807.
41. Sato M., Nakazawa M., Usui T., Tanimoto N., Abe H., Ohguro H. Mutations in the gene coding for guanylate cyclase-activating protein 2 (GUCA1B gene) in patients with autosomal dominant retinal dystrophies. Graefes Arch. Clin. Exp. Ophthalmol. 2005, 243:235-242.
42. Sebastian S., Faralli H., Yao Z., Rakopoulos P., Palii C., Cao Y., Singh K., Liu Q.C., Chu A., Aziz A., et al. Tissue-specific splicing of a ubiquitously expressed transcription factor is essential for muscle differentiation. Genes Dev. 2013, 27:1247-1259.
43. Shalizi A., Gaudillière B., Yuan Z., Stegmüller J., Shirogane T., Ge Q., Tan Y., Schulman B., Harper J.W., Bonni A. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 2006, 311:1012-1017.
44. Smith E., Shilatifard A. Enhancer biology and enhanceropathies. Nat. Struct. Mol. Biol. 2014, 21:210-219.
45. Spitz F., Furlong E.E. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13:613-626.
46. Storch K.F., Paz C., Signorovitch J., Raviola E., Pawlyk B., Li T., Weitz C.J. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 2007, 130:730-741.
47. Swain P.K., Chen S., Wang Q.L., Affatigato L.M., Coats C.L., Brady K.D., Fishman G.A., Jacobson S.G., Swaroop A., Stone E., et al. Mutations in the cone-rod homeobox gene are associated with the cone-rod dystrophy photoreceptor degeneration. Neuron 1997, 19:1329-1336.
48. Tran N.M., Zhang A., Zhang X., Huecker J.B., Hennig A.K., Chen S. Mechanistically distinct mouse models for CRX-associated retinopathy. PLoS Genet. 2014, 10:e1004111.
49. Wada Y., Abe T., Takeshita T., Sato H., Yanashima K., Tamai M. Mutation of human retinal fascin gene (FSCN2) causes autosomal dominant retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 2001, 42:2395-2400.
50. Yanagi Y., Masuhiro Y., Mori M., Yanagisawa J., Kato S. p300/CBP acts as a coactivator of the cone-rod homeobox transcription factor. Biochem. Biophys. Res. Commun. 2000, 269:410-414.
51. Yokokura S., Wada Y., Nakai S., Sato H., Yao R., Yamanaka H., Ito S., Sagara Y., Takahashi M., Nakamura Y., et al. Targeted disruption of FSCN2 gene induces retinopathy in mice. Invest. Ophthalmol. Vis. Sci. 2005, 46:2905-2915.
52. Youn H.D., Chatila T.A., Liu J.O. Integration of calcineurin and MEF2 signals by the coactivator p300 during T-cell apoptosis. EMBO J. 2000, 19:4323-4331.
53. Young R.W. Cell differentiation in the retina of the mouse. Anat. Rec. 1985, 212:199-205.