Unveiling the hidden function of long non-coding RNA by identifying its major partner-protein

Cell and Bioscience

Volumn 5, Issue 1, 2015, Pages

  Yang, Yongfang ^a   Wen, Liwei ^a   Zhu, Hongliang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Biochemistry approaches; Function; Interaction; Long non coding RNA; Protein

Indexed keywords

EID: 84945188157     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/s13578-015-0050-x     Document Type: Review

References (85)

1. Johnson JM, Edwards S, Shoemaker D, Schadt EE. Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments. Trends Genet. 2005;21:93-102.
2. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511-5.
3. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F. Landscape of transcription in human cells. Nature. 2012;489:101-8.
4. Novikova IV, Hennelly SP, Sanbonmats KY. Sizing up long non-coding RNAs: do lncRNAs have secondary and tertiary structure? Bioarchitecture. 2012;2:189-99.
5. Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Gene Dev. 2009;23:1494-504.
6. Yoon J, Abdelmohsen K, Gorospe M. Functional interactions among microRNAs and long noncoding RNAs. Seminars in cell and developmental biology. Elsevier; 2014. p. 9-14.
7. Chu C, Spitale RC, Chang HY. Technologies to probe functions and mechanisms of long noncoding RNAs. Nat Struct Mol Biol. 2015;22:29-35.
8. Rinn JL, Ule J. Oming in on RNA-protein interactions. Genome Biol. 2014;15:401.
9. Buenrostro JD, Araya CL, Chircus LM, Layton CJ, Chang HY, Snyder MP, Greenleaf WJ. Quantitative analysis of RNA-protein interactions on a massively parallel array reveals biophysical and evolutionary landscapes. Nat Biotechnol. 2014;32:562-8.
10. Tome JM, Ozer A, Pagano JM, Gheba D, Schroth GP, Lis JT. Comprehensive analysis of RNA-protein interactions by high-throughput sequencing-RNA affinity profiling. Nat Methods. 2014;11:683-8.
11. Wang S, Tran E. Unexpected functions of lncRNAs in gene regulation. Commun Integr Biol. 2013; 6.
12. Zhu B, Yang Y, Li R, Fu D, Wen L, Luo Y, Zhu H. RNA sequencing and functional analysis implicate the regulatory role of long non-coding RNAs in tomato fruit ripening. J Exp Bot. 2015;66:4483-95.
13. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012;22:1775-89.
14. Zhao J, Sun BK, Erwin JA, Song J, Lee JT. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science. 2008;322:750-6.
15. Ilik IA, Quinn JJ, Georgiev P, Tavares-Cadete F, Maticzka D, Toscano S, Wan Y, Spitale RC, Luscombe N, Backofen R. Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. Mol Cell. 2013;51:156-73.
16. Lee JT. Epigenetic regulation by long noncoding RNAs. Science. 2012;338:1435-9.
17. Yoon J, Abdelmohsen K, Gorospe M. Posttranscriptional gene regulation by long noncoding RNA. J Mol Biol. 2013;425:3723-30.
18. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136:629-41.
19. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 2007;129:1311-23.
20. Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, Orkin SH, Peters AH. Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev Cell. 2008;15:668-79.
21. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-DiNardo D, Kanduri C. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell. 2008;32:232-46.
22. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature. 2008;454:126-30.
23. Feng J, Bi C, Clark BS, Mady R, Shah P, Kohtz JD. The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Gene Dev. 2006;20:1470-84.
24. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell. 2010;39:925-38.
25. Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature. 2012;491:454-7.
26. Lin D, Pestova TV, Hellen CU, Tiedge H. Translational control by a small RNA: dendritic BC1 RNA targets the eukaryotic initiation factor 4A helicase mechanism. Mol Cell Biol. 2008;28:3008-19.
27. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell. 2011;43:904-14.
28. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145-66.
29. Grote P, Wittler L, Hendrix D, Koch F, Währisch S, Beisaw A, Macura K, Bläss G, Kellis M, Werber M. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell. 2013;24:206-14.
30. Heo JB, Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science. 2011;331:76-9.
31. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell. 2010;142:409-19.
32. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA. The sequence of the human genome. Science. 2001;291:1304-51.
33. Zappulla DC, Cech TR. RNA as a flexible scaffold for proteins: yeast telomerase and beyond. Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press; 2006. p. 217-24.
34. Cech TR. Life at the end of the chromosome: telomeres and telomerase. Angew Chem Int Ed. 2000;39:34-43.
35. Bilaud T, Brun C, Ancelin K, Koering CE, Laroche T, Gilson E. Telomeric localization of TRF2, a novel human telobox protein. Nat Genet. 1997;17:236-9.
36. Jeon Y, Lee JT. YY1 tethers Xist RNA to the inactive X nucleation center. Cell. 2011;146:119-33.
37. Tsai M, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010;329:689-93.
38. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature. 2004;431:873-8.
39. Maenner S, Müller M, Fröhlich J, Langer D, Becker PB. ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol Cell. 2013;51:174-84.
40. Yang L, Lin C, Liu W, Zhang J, Ohgi KA, Grinstein JD, Dorrestein PC, Rosenfeld MG. ncRNA-and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell. 2011;147:773-88.
41. Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD, Horlings HM, Shah N, Umbricht C, Wang P. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet. 2011;43:621-9.
42. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP. Noncoding RNA Gas5 is a growth arrest and starvation-associated repressor of the glucocorticoid receptor. Sci Signal. 2010;3:a8.
43. Gong C, Popp MW, Maquat LE. Biochemical analysis of long non-coding RNA-containing ribonucleoprotein complexes. Methods. 2012;58:88-93.
44. Darnell R. CLIP (cross-linking and immunoprecipitation) identification of RNAs bound by a specific protein. Cold Spring Harb Protoc. 2012;2012:t72132.
45. Feng Y, Hu X, Zhang Y, Zhang D, Li C, Zhang L. Methods for the Study of Long Noncoding RNA in Cancer Cell Signaling. Cancer Cell Signaling. Springer; 2014. p. 115-43.
46. Chu C, Quinn J.Chang HY. Chromatin isolation by RNA purification (ChIRP). J Vis Exp. 2012;61. doi: 10.3791/3912.
47. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell. 2011;44:667-78.
48. Engreitz J, Lander ES, Guttman M. RNA antisense purification (RAP) for mapping rna interactions with chromatin. Nuclear bodies and noncoding RNAs. Springer; 2015. p. 183-97.
49. Bellucci M, Agostini F, Masin M, Tartaglia GG. Predicting protein associations with long noncoding RNAs. Nat Methods. 2011;8:444-5.
50. Lu Q, Ren S, Lu M, Zhang Y, Zhu D, Zhang X, Li T. Computational prediction of associations between long non-coding RNAs and proteins. BMC Genom. 2013;14:651.
51. Selth LA, Close P, Svejstrup JQ. Studying RNA-protein interactions in vivo by RNA immunoprecipitation. Epigenetics protocols. Springer; 2011. p. 253-64.
52. Niranjanakumari S, Lasda E, Brazas R, Garcia-Blanco MA. Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods. 2002;26:182-90.
53. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Morales DR, Thomas K, Presser A, Bernstein BE, van Oudenaarden A. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci. 2009;106:11667-72.
54. Keene JD, Komisarow JM, Friedersdorf MB. RIP-Chip: the isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat Protoc Electron Ed. 2006;1:302.
55. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods. 2008;5:613-9.
56. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT. Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell. 2010;40:939-53.
57. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, Fraser P. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science. 2008;322:1717-20.
58. Hacisuleyman E, Goff LA, Trapnell C, Williams A, Henao-Mejia J, Sun L, McClanahan P, Hendrickson DG, Sauvageau M, Kelley DR. Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat Struct Mol Biol. 2014;21:198-206.
59. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature. 2011;472:120-4.
60. West JA, Davis CP, Sunwoo H, Simon MD, Sadreyev RI, Wang PI, Tolstorukov MY, Kingston RE. The long noncoding RNAs Neat1 and Malat1 bind active chromatin sites. Mol Cell. 2014;55:791-802.
61. Quinn JJ, Chang HY. In situ dissection of RNA functional subunits by domain-specific chromatin isolation by RNA purification (dChIRP). Nuclear bodies and noncoding RNAs. Springer; 2015. p. 199-213.
62. Chu C, Zhang QC, Da Rocha ST, Flynn RA, Bharadwaj M, Calabrese JM, Magnuson T, Heard E, Chang HY. Systematic discovery of Xist RNA binding proteins. Cell. 2015;161:404-16.
63. McHugh CA, Chen C, Chow A, Surka CF, Tran C. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature. 2015;521:232-6.
64. Ule J, Jensen K, Mele A, Darnell RB. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods. 2005;37:376-86.
65. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature. 2008;456:464-9.
66. Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature. 2009;460:479-86.
67. Lagier-Tourenne C, Polymenidou M, Hutt KR, Vu AQ, Baughn M, Huelga SC, Clutario KM, Ling S, Liang TY, Mazur C. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat Neurosci. 2012;15:1488-97.
68. Li Q, Uemura Y, Kawahara Y. Cross-linking and immunoprecipitation of nuclear RNA-binding proteins. nuclear bodies and noncoding RNAs. Springer; 2015. p. 247-63.
69. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp A, Munschauer M. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell. 2010;141:129-41.
70. König J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, Turner DJ, Luscombe NM, Ule J. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol. 2010;17:909-15.
71. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp A, Munschauer M. PAR-CliP-a method to identify transcriptome-wide the binding sites of RNA binding proteins. J Vis Exp. 2010;41. doi: 10.3791/2034.
72. Ascano M, Mukherjee N, Bandaru P, Miller JB, Nusbaum JD, Corcoran DL, Langlois C, Munschauer M, Dewell S, Hafner M. FMRP targets distinct mRNA sequence elements to regulate protein expression. Nature. 2012;492:382-6.
73. Lebedeva S, Jens M, Theil K, Schwanhäusser B, Selbach M, Landthaler M, Rajewsky N. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell. 2011;43:340-52.
74. Yokoshi M, Li Q, Yamamoto M, Okada H, Suzuki Y, Kawahara Y. Direct binding of Ataxin-2 to distinct elements in 3' UTRs promotes mRNA stability and protein expression. Mol Cell. 2014;55:186-98.
75. Rossbach O, Hung L, Khrameeva E, Schreiner S, König J, Curk T, Zupan B, Ule J, Gelfand MS, Bindereif A. Crosslinking-immunoprecipitation (iCLIP) analysis reveals global regulatory roles of hnRNP L. RNA Biol. 2014;11:146-55.
76. Lau E. Non-coding RNA: zooming in on lncRNA functions. Nat Rev Genet. 2014;15:574-5.
77. Quinn JJ, Ilik IA, Qu K, Georgiev P, Chu C, Akhtar A, Chang HY. Revealing long noncoding RNA architecture and functions using domain-specific chromatin isolation by RNA purification. Nat Biotechnol. 2014;32:933-40.
78. Baltz AG, Munschauer M, Schwanhäusser B, Vasile A, Murakawa Y, Schueler M, Youngs N, Penfold-Brown D, Drew K, Milek M. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell. 2012;46:674-90.
79. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, Davey NE, Humphreys DT, Preiss T, Steinmetz LM. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell. 2012;149:1393-406.
80. Klass DM, Scheibe M, Butter F, Hogan GJ, Mann M, Brown PO. Quantitative proteomic analysis reveals concurrent RNA-protein interactions and identifies new RNA-binding proteins in Saccharomyces cerevisiae. Genome Res. 2013;23:1028-38.
81. Kramer K, Sachsenberg T, Beckmann BM, Qamar S, Boon K, Hentze MW, Kohlbacher O, Urlaub H. Photo-cross-linking and high-resolution mass spectrometry for assignment of RNA-binding sites in RNA-binding proteins. Nat Methods. 2014;11:1064-70.
82. Simon MD, Wang CI, Kharchenko PV, West JA, Chapman BA, Alekseyenko AA, Borowsky ML, Kuroda MI, Kingston RE. The genomic binding sites of a noncoding RNA. Proc Natl Acad Sci. 2011;108:20497-502.
83. Cirillo D, Agostini F, Klus P, Marchese D, Rodriguez S, Bolognesi B, Tartaglia GG. Neurodegenerative diseases: quantitative predictions of protein-RNA interactions. RNA. 2013;19:129-40.
84. Agostini F, Cirillo D, Bolognesi B, Tartaglia GG. X-inactivation: quantitative predictions of protein interactions in the Xist network. Nucleic Acids Res. 2013;41:e31.
85. Shang D, Yang H, Xu Y, Yao Q, Zhou W, Shi X, Han J, Su F, Su B, Zhang C. A global view of network of lncRNAs and their binding proteins. Mol Biosyst. 2015;11:656-63.