Evolutionarily conserved long intergenic non-coding RNAs in the eye

Human Molecular Genetics

Volumn 22, Issue 15, 2013, Pages

  Mustafi, Debarshi ^a   Kevany, Brian M ^a   Bai, Xiaodong ^b   Maeda, Tadao ^a   Sears, Jonathan E ^b   Khalil, Ahmad M ^a,b   Palczewski, Krzysztof ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; EYE; GENE EXPRESSION; GENE LOCUS; GENETIC ANALYSIS; GENETIC CONSERVATION; GENOMIC IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; MAMMAL; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROMOTER REGION; RETINA NERVE CELL; RETINA ROD; RNA SEQUENCE; SEQUENCE ANALYSIS; ANIMAL; ANTIBODY SPECIFICITY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR CELL; RETINA;

ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; EYE; GENE EXPRESSION; GENETIC LOCI; HUMANS; MAMMALS; MICE; NUCLEOTIDE MOTIFS; ORGAN SPECIFICITY; PHOTORECEPTOR CELLS; PROMOTER REGIONS, GENETIC; RETINA; RNA, LONG NONCODING; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC;

EID: 84880306247     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt156     Document Type: Article

References (77)

1. Siegert, S., Cabuy, E., Scherf, B.G., Kohler, H., Panda, S., Le, Y.Z., Fehling, H.J., Gaidatzis, D., Stadler, M.B. and Roska, B. (2012) Transcriptional code and disease map for adult retinal cell types. Nat. Neurosci., 15, 487-495.
2. Palczewski, K. (2012) Chemistry and biology of vision. J. Biol. Chem., 287, 1612-1619.
3. Lee, R.C., Feinbaum, R.L. and Ambros, V. (1993) The C-elegans heterochronic gene Lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843-854.
4. Pasquinelli, A.E., Reinhart, B.J., Slack, F., Martindale, M.Q., Kuroda, M.I., Maller, B., Hayward, D.C., Ball, E.E., Degnan, B., Muller, P. et al. (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature, 408, 86-89.
5. He, L. and Hannon, G.J. (2004) Micrornas: small RNAs with a big role in gene regulation. Nat. Rev. Genet., 5, 522-531.
6. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W. et al. (2001) Initial sequencing and analysis of the human genome. Nature, 409, 860-921.
7. Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J., Sutton, G.G., Smith, H.O., Yandell, M., Evans, C.A., Holt, R.A. et al. (2001) The sequence of the human genome. Science, 291, 1304-1351.
8. Waterston, R.H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J.F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P. et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature, 420, 520-562.
9. Mercer, T.R., Dinger, M.E. and Mattick, J.S. (2009) Long non-coding RNAs: insights into functions. Nat. Rev. Genet., 10, 155-159.
10. Moran, V.A., Perera, R.J. and Khalil, A.M. (2012) Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res., 40, 6391-6400.
11. Cabili, M.N., Trapnell, C., Goff, L., Koziol, M., Tazon-Vega, B., Regev, A. and Rinn, J.L. (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Gene. Dev., 25, 1915-1927.
12. Guttman, M., Amit, I., Garber, M., French, C., Lin, M.F., Feldser, D., Huarte, M., Zuk, O., Carey, B.W., Cassady, J.P. et al. (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature, 458, 223-227.
13. Khalil, A.M., Guttman, M., Huarte, M., Garber, M., Raj, A., Morales, D.R., Thomas, K., Presser, A., Bernstein, B.E., van Oudenaarden, A. et al. (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl Acad. Sci. USA, 106, 11667-11672.
14. Rinn, J.L., Kertesz, M., Wang, J.K., Squazzo, S.L., Xu, X., Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E. et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell, 129, 1311-1323.
15. Guttman, M., Donaghey, J., Carey, B.W., Garber, M., Grenier, J.K., Munson, G., Young, G., Lucas, A.B., Ach, R., Bruhn, L. et al. (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature, 477, 295-300.
16. Ponjavic, J., Oliver, P.L., Lunter, G. and Ponting, C.P. (2009) Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet., 5, e1000617.
17. Mercer, T.R., Dinger, M.E., Sunkin, S.M., Mehler, M.F. and Mattick, J.S. (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl Acad. Sci. USA, 105, 716-721.
18. Kapranov, P., Cheng, J., Dike, S., Nix, D.A., Duttagupta, R., Willingham, A.T., Stadler, P.F., Hertel, J., Hackermuller, J., Hofacker, I.L. et al. (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science, 316, 1484-1488.
19. Martin, L. and Chang, H.Y. (2012) Uncovering the role of genomic 'dark matter' in human disease. J. Clin. Invest., 122, 1589-1595.
20. Maass, P.G., Rump, A., Schultz, H., Stricker, S., Schulze, L., Platzer, K., Aydin, A., Tinschert, S., Goldring, M.B., Luft, F.C. et al. (2012) A misplaced lncRNA causes bracydactyly in humans. J. Clin. Invest., 122, 3990-4002.
21. Kumar, V., Westra, H.J., Karjalainen, J., Zhernakova, D.V., Esko, T., Hrdlickova, B., Almeida, R., Zhernakova, A., Reinmaa, E., Vosa, U. et al. (2013) Human disease-associated genetic variation impacts large intergenic non-coding RNA expression. PLoS Genet., 9, e1003201.
22. Talkowski, M.E., Maussion, G., Crapper, L., Rosemfeld, J.A., Blumenthal, I., Hanscom, C., Chiang, C., Lindgren, A., Pereira, S., Ruderfer, D. et al. (2012) Disruption of large intergenic noncoding RNA in subjects with neurodevelopmental disabilities. Am. J. Hum. Genet., 91, 1128-1134.
23. Guttman, M., Garber, M., Levin, J.Z., Donaghey, J., Robinson, J., Adiconis, X., Fan, L., Koziol, M.J., Gnirke, A., Nusbaum, C. et al. (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat. Biotechnol., 28, 503-510.
24. Ulitsky, I., Shkumatava, A., Jan, C.H., Sive, H. and Bartel, D.P. (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell, 147, 1537-1550.
25. Young, R.S., Marques, A.C., Tibbit, C., Haerty, W., Bassett, A.R., Liu, J.L. and Ponting, C.P. (2012) Identification and properties of 1,119 candidate lincRNA loci in the Drosophila melanogaster Genome. Genome Biol. Evol., 4, 427-442.
26. Chakraborty, D., Kappei, D., Theis, M., Nitzsche, A., Ding, L., Paszkowski-Rogacz, M., Surendranath, V., Berger, N., Schulz, H., Saar, K. et al. (2012) Combined RNAi and localization for functionally dissecting long noncoding RNAs. Nat. Methods, 9, 360-362.
27. Guo, X., Gao, L., Liao, Q., Xiao, H., Ma, X., Yang, X., Luo, H., Zhao, G., Bu, D., Jiao, F. et al. (2013) Long non-coding RNAs function annotation: a global prediction method based on bi-colored networks. Nucleic Acids Res., 41, e35
28. Liao, Q., Liu, C., Yuan, X., Kang, S., Miao, R., Xiao, H., Zhao, G., Luo, H., Bu, D., Zhao, H. et al. (2011) Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res., 39, 3864-3878.
29. Washietl, S., Hofacker, I.L., Lukasser, M., Huttenhofer, A. and Stadler, P.F. (2005) Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome. Nat. Biotechnol., 23, 1383-1390.
30. Coon, S.L., Munson, P.J., Cherukuri, P.F., Sugden, D., Rath, M.F., Moller, M., Clokie, S.J.H., Fu, C., Olanich, M.E., Rangel, Z. et al. (2012) Circadian changes in long noncoding RNAs in the pineal gland. Proc. Natl Acad. Sci. USA, 109, 13319-13324.
31. Meola, N., Pizzo, M., Alfano, G., Surace, E.M. and Banfi, S. (2012) The long noncoding RNA Vax2os1 controls the cell cycle progression of photoreceptor progenitors in the mouse retina. RNA, 18, 111-123.
32. Rapicavoli, N.A., Poth, E.M. and Blackshaw, S. (2010) The long noncoding RNA RNCR2 directs mouse retinal cell specification. BMC Dev. Biol., 10, 49.
33. Rapicavoli, N.A., Poth, E.M., Zhu, H. and Blackshaw, S. (2011) The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity. Neural Dev., 6, 32.
34. Sone, M., Hayashi, T., Tarui, H., Agata, K., Takeichi, M. and Nakagawa, S. (2007) The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J. Cell Sci., 120, 2498-2506.
35. Young, T.L., Matsuda, T. and Cepko, C.L. (2005) The noncoding RNA taurine upregulated gene 1 is required for differentiation of the murine retina. Curr. Biol., 15, 501-512.
36. Blackshaw, S., Harpavat, S., Trimarchi, J., Cai, L., Huang, H.Y., Kuo, W.P., Weber, G., Lee, K., Fraioli, R.E., Cho, S.H. et al. (2004) Genomic analysis of mouse retinal development. PLoS Biol., 2, 1411-1431.
37. Mustafi, D., Maeda, T., Kohno, H., Nadeau, J.H. and Palczewski, K. (2012) Inflammatory priming predisposes to age-related retinal degeneration in mice. J. Clin. Invest., 122, 2989-3001.
38. Mustafi, D., Kevany, B.M., Genoud, C., Okano, K., Cideciyan, A.V., Sumaroka, A., Roman, A.J., Jacobson, S.G., Engel, A., Adams, M.D. et al. (2011) Defective photoreceptor phagocytosis in a mouse model of enhanced S-cone syndrome causes progressive retinal degeneration. FASEB J., 25, 3157-3176.
39. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621-628.
40. Curcio, C.A., Sloan, K.R., Kalina, R.E. and Hendrickson, A.E. (1990) Human photoreceptor topography. J. Comp. Neurol., 292, 497-523.
41. Provis, J.M., Penfold, P.L., Cornish, E.E., Sandercoe, T.M. and Madigan, M.C. (2005) Anatomy and development of the macula: specialisation and the vulnerability to macular degeneration. Clin. Exp. Optom., 88, 269-281.
42. Zhu, Q.B., Sun, W.Y., Okano, K., Chen, Y., Zhang, N., Maeda, T. and Palczewski, K. (2011) Sponge transgenic mouse model reveals important roles for the MicroRNA-183 (miR-183)/96/182 cluster in postmitotic photoreceptors of the retina. J. Biol. Chem., 286, 31749-31760.
43. Soucy, E., Wang, Y.S., Nirenberg, S., Nathans, J. and Meister, M. (1998) A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron, 21, 481-493.
44. Mears, A.J., Kondo, M., Swain, P.K., Takada, Y., Bush, R.A., Saunders, T.L., Sieving, P.A. and Swaroop, A. (2001) Nrl is required for rod photoreceptor development. Nat. Genet., 29, 447-452.
45. Sakami, S., Maeda, T., Bereta, G., Okano, K., Golczak, M., Sumaroka, A., Roman, A.J., Cideciyan, A.V., Jacobson, S.G. and Palczewski, K. (2011) Probing mechanisms of photoreceptor degeneration in a new mouse model of the common form of autosomal dominant retinitis pigmentosa due to P23H opsin mutations. J. Biol. Chem., 286, 10551-10567.
46. Sun, H. and Nathans, J. (1997) Stargardt's ABCR is localized to the disc membrane of retinal rod outer segments. Nat. Genet., 17, 15-16.
47. Lerner, L.E., Peng, G.H., Gribanova, Y.E., Chen, S.M. and Farber, D.B. (2005) Sp4 is expressed in retinal neurons, activates transcription of photoreceptor-specific genes, and synergizes with Crx. J. Biol. Chem., 280, 20642-20650.
48. Chau, K.Y., Munshi, N., Keane-Myers, A., Cheung-Chau, K.W., Tai, A.K.F., Manfioletti, G., Dorey, C.K., Thanos, D., Zack, D.J. and Ono, S.J. (2000) The architectural transcription factor high mobility group I(Y) participates in photoreceptor-specific gene expression. J. Neurosci., 20, 7317-7324.
49. Ruan, G.X., Zhang, D.Q., Zhou, T.R., Yamazaki, S. and McMahon, D.G. (2006) Circadian organization of the mammalian retina. Proc. Natl Acad. Sci. USA, 103, 9703-9708.
50. Rath, M.F., Bailey, M.J., Kim, J.S., Coon, S.L., Klein, D.C. and Moller, M. (2009) Developmental and daily expression of the Pax4 and Pax6 homeobox genes in the rat retina: localization of Pax4 in photoreceptor cells. J. Neurochem., 108, 285-294.
51. Li, T., Lu, Z.Y. and Lu, L. (2004) Regulation of eye development by transcription control of CCCTC binding factor (CTCF). J. Biol. Chem., 279, 27575-27583.
52. Canto-Soler, M.V., Huang, H., Romero, M.S. and Adler, R. (2008) Transcription factors CTCF and Pax6 are segregated to different cell types during retinal cell differentiation. Dev. Dynam., 237, 758-767.
53. Sopher, B.L., Ladd, P.D., Pineda, V.V., Libby, R.T., Sunkin, S.M., Hurley, J.B., Thienes, C.P., Gaasterland, T., Filippova, G.N. and La Spada, A.R. (2011) CTCF regulates ataxin-7 expression through promotion of a convergently transcribed, antisense noncoding RNA. Neuron, 70, 1071-1084.
54. Ponting, C.P., Oliver, P.L. and Reik, W. (2009) Evolution and functions of long noncoding RNAs. Cell, 136, 629-641.
55. Taft, R.J., Pang, K.C., Mercer, T.R., Dinger, M. and Mattick, J.S. (2010) Non-coding RNAs: regulators of disease. J. Pathol., 220, 126-139.
56. Kutter, C., Watt, S., Stefflova, K., Wilson, M.D., Goncalves, A., Ponting, C.P., Odom, D.T. and Marques, A.C. (2012) Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet., 8, e1002841.
57. Chodroff, R.A., Goodstadt, L., Sirey, T.M., Oliver, P.L., Davies, K.E., Green, E.D., Molnar, Z. and Ponting, C.P. (2010) Long noncoding RNA genes: conservation of sequence and brain expression among diverse amniotes. Genome Biol., 11, R72.
58. Quazi, F., Lenevich, S. and Molday, R.S. (2012) ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer. Nat. Commun., 3, 1-9.
59. Allikmets, R., Singh, N., Sun, H., Shroyer, N.E., Hutchinson, A., Chidambaram, A., Gerrard, B., Baird, L., Stauffer, D., Peiffer, A. et al. (1997) A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat. Genet., 15, 236-246.
60. Cremers, F.P.M., van De Pol, D.J.R., van Driel, M., den Hollander, A.I., van Haren, F.J.J., Knoers, N.V.A.M., Tijmes, N., Bergen, A.A.B., Rohrschneider, K., Blankenagel, A. et al. (1998) Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt's disease gene ABCR. Hum. Mol. Genet., 7, 355-362.
61. Hoppe, G., Rayborn, M.E. and Sears, J.E. (2007) Diurnal rhythm of the chromatin protein Hmgb1 in rat photoreceptors is under circadian regulation. J. Comp. Neurol., 501, 219-230.
62. Gehring, W.J. (1996) The master control gene for morphogenesis and evolution of the eye. Genes Cells, 1, 11-15.
63. Reichman, S., Kalathur, R.K., Lambard, S., Ait-Ali, N., Yang, Y., Lardenois, A., Ripp, R., Poch, O., Zack, D.J., Sahel, J.A. et al. (2010) The homeobox gene CHX10/VSX2 regulates RdCVF promoter activity in the inner retina. Hum. Mol. Genet., 19, 250-261.
64. Leveillard, T., Mohand-Said, S., Lorentz, O., Hicks, D., Fintz, A.C., Clerin, E., Simonutti, M., Forster, V., Cavusoglu, N., Chalmel, F. et al. (2004) Identification and characterization of rod-derived cone viability factor. Nat. Genet., 36, 755-759.
65. Yang, Y., Mohand-Said, S., Danan, A., Simonutti, M., Fontaine, V., Clerin, E., Picaud, S., Leveillard, T. and Sahel, J.A. (2009) Functional cone rescue by RdCVF protein in a dominant model of retinitis pigmentosa. Mol. Ther., 17, 787-795.
66. Yanicostas, C., Barbieri, E., Hibi, M., Brice, A., Stevanin, G. and Soussi-Yanicostas, N. (2012) Requirement for zebrafish ataxin-7 in differentiation of photoreceptors and cerebellar neurons. PLoS ONE, 7, e50705.
67. Helmlinger, D., Hardy, S., Abou-Sleymane, G., Eberlin, A., Bowman, A.B., Gansmuller, A., Picaud, S., Zoghbi, H.Y., Trottier, Y., Tora, L. et al. (2006) Glutamine-expanded ataxin-7 alters TFTC/STAGA recruitment and chromatin structure leading to photoreceptor dysfunction. PLoS Biol., 4, e67.
68. Palhan, V.B., Chen, S., Peng, G.H., Tjernberg, A., Gamper, A.M., Fan, Y., Chait, B.T., La Spada, A.R. and Roeder, R.G. (2005) Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc. Natl Acad. Sci. USA, 102, 8472-8477.
69. Kahle, J.J., Gulbahce, N., Shaw, C.A., Lim, J., Hill, D.E., Barabasi, A.L. and Zoghbi, H.Y. (2011) Comparison of an expanded ataxia interactome with patient medical records reveals a relationship between macular degeneration and ataxia. Hum. Mol. Genet., 20, 510-527.
70. Orom, U.A., Derrien, T., Beringer, M., Gumireddy, K., Gardini, A., Bussotti, G., Lai, F., Zytnicki, M., Notredame, C., Huang, Q.H. et al. (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell, 143, 46-58.
71. Djebali, S., Davis, C.A., Merkel, A., Dobin, A., Lassmann, T., Mortazavi, A., Tanzer, A., Lagarde, J., Lin, W., Schlesinger, F. et al. (2012) Landscape of transcription in human cells. Nature, 489, 101-108.
72. Burd, C.E., Jeck, W.R., Liu, Y., Sanoff, H.K., Wang, Z. and Sharpless, N.E. (2010) Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk. PLoS Genet., 6, e1001233.
73. Gupta, R.A., Shah, N., Wang, K.C., Kim, J., Horlings, H.M., Wong, D.J., Tsai, M.C., Hung, T., Argani, P., Rinn, J.L. et al. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature, 464, 1071-1076.
74. Wheeler, T.M., Leger, A.J., Pandey, S.K., MacLeod, A.R., Nakamori, M., Cheng, S.H., Wentworth, B.M., Bennett, C.F. and Thornton, C.A. (2012) Targeting nuclear RNA for in vivo correction of myotonic dystrophy. Nature, 488, 111-115.
75. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
76. Grant, C.E., Bailey, T.L. and Noble, W.S. (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics, 27, 1017-1018.
77. Maeda, A., Maeda, T., Imanishi, Y., Kuksa, V., Alekseev, A., Bronson, J.D., Zhang, H.B., Zhu, L., Sun, W.Y., Saperstein, D.A. et al. (2005) Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J. Biol. Chem., 280, 18822-18832.