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Quantitative Biology

, Volume 6, Issue 3, pp 239–252 | Cite as

Advances and challenges towards the study of RNA-RNA interactions in a transcriptome-wide scale

  • Jing Gong
  • Yanyan Ju
  • Di Shao
  • Qiangfeng Cliff Zhang
Review
  • 209 Downloads

Abstract

Background

RNA molecules play crucial roles in various biological processes. Their regulation and function are mediated by interacting with other molecules. Among them RNA-RNA interactions (RRIs) are important in many basic cellular activities including transcription, RNA processing, localization, and translation. However, we just start to unveil the complexity of the knowledge and underlying mechanisms of RRIs.

Results

In this review, we will summarize approaches for RRI identifications, including both conventional, focused biophysical and biochemical methods and recently developed large scale sequencing-based techniques. We will also discuss discoveries per RRI type revealed by using these technologies, as well as challenges towards a systematic and functional understanding of RRIs.

Conclusions

The development of sequencing-based techniques has revolutionized the study of RRIs. Applying these techniques in multiple organisms has identified thousands of RRIs, many of which could potentially regulate multiple aspects of gene expression. However, despite the great breakthrough, the RNA-RNA interactome of any species remains far from complete due to intrinsic complex nature of RRI and limitations in current techniques. More efficient experimental methods and computational framework are needed to obtain the full image of RRI networks, and their possible regulatory roles in biology and medicine.

Keywords

RNA-RNA interactions PARIS SPLASH LIGR-seq next generation sequencing 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 31671355, 91740204 and 31761163007) and the National Thousand Young Talents Program of China to Qiangfeng Cliff Zhang. We thank Jinsong Zhang, Meiling Piao, Lei Tang and Yifan Wei for discussion.

References

  1. 1.
    Gilbert, W. (1986) Origin of life: the RNA world. Nature, 319, 618CrossRefGoogle Scholar
  2. 2.
    Mattick, J. S. (2004) RNA regulation: a new genetics? Nat. Rev. Genet., 5, 316–323CrossRefGoogle Scholar
  3. 3.
    Waters, L. S. and Storz, G. (2009) Regulatory RNAs in bacteria. Cell, 136, 615–628CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Licatalosi, D. D. and Darnell, R. B. (2010) RNA processing and its regulation: global insights into biological networks. Nat. Rev. Genet., 11, 75–87CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Cech, T. R. (2012) The RNA worlds in context. Cold Spring Harb. Perspect. Biol., 4, a006742CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Morris, K. V. and Mattick, J. S. (2014) The rise of regulatory RNA. Nat. Rev. Genet., 15, 423–437CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    The ENCODE Project Consortium. (2004) The ENCODE (ENCyclopedia Of DNA Elements) Project. Science, 306, 636–640CrossRefPubMedGoogle Scholar
  8. 8.
    Iyer, M. K., Niknafs, Y. S., Malik, R., Singhal, U., Sahu, A., Hosono, Y., Barrette, T. R., Prensner, J. R., Evans, J. R., Zhao, S., et al. (2015) The landscape of long noncoding RNAs in the human transcriptome. Nat. Genet., 47, 199–208CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Lunde, B. M., Moore, C. and Varani, G. (2007) RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol., 8, 479–490CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Gerstberger, S., Hafner, M. and Tuschl, T. (2014) A census of human RNA-binding proteins. Nat. Rev. Genet., 15, 829–845CrossRefPubMedGoogle Scholar
  11. 11.
    Rinn, J. L. and Chang, H. Y. (2012) Genome regulation by long noncoding RNAs. Annu. Rev. Biochem., 81, 145–166CrossRefPubMedGoogle Scholar
  12. 12.
    Quinn, J. J. and Chang, H. Y. (2016) Unique features of long noncoding RNA biogenesis and function. Nat. Rev. Genet., 17, 47–62CrossRefPubMedGoogle Scholar
  13. 13.
    Guil, S. and Esteller, M. (2015) RNA-RNA interactions in gene regulation: the coding and noncoding players. Trends Biochem. Sci., 40, 248–256CrossRefPubMedGoogle Scholar
  14. 14.
    Modrek, B. and Lee, C. (2002) A genomic view of alternative splicing. Nat. Genet., 30, 13–19CrossRefPubMedGoogle Scholar
  15. 15.
    Matlin, A. J., Clark, F. and Smith, C. W. J. (2005) Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol., 6, 386–398CrossRefPubMedGoogle Scholar
  16. 16.
    Ibba, M. and Soll, D. (2000) Aminoacyl-tRNA synthesis. Annu. Rev. Biochem., 69, 617–650CrossRefPubMedGoogle Scholar
  17. 17.
    Selmer, M., Dunham, C. M., Murphy IV, F. V. Weixlbaumer, A., Petry, S., Kelley, A. C., Weir, J. R. and Ramakrishnan, V. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science, 313, 1935–1942CrossRefPubMedGoogle Scholar
  18. 18.
    Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Krol, J., Loedige, I. and Filipowicz, W. (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet., 11, 597–610CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Kiss, T. (2002) Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell, 109, 145–148CrossRefPubMedGoogle Scholar
  21. 21.
    Watkins, N. J. and Bohnsack, M. T. (2012) The box C/D and H/ ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip. Rev. RNA, 3, 397–414CrossRefPubMedGoogle Scholar
  22. 22.
    Morita, T., Maki, K. and Aiba, H. (2012) Detection of sRNAmRNA interactions by electrophoretic mobility shift assay. Methods Mol. Biol., 905, 235–244PubMedGoogle Scholar
  23. 23.
    Bak, G., Han, K., Kim, K. S. and Lee, Y. (2015) Electrophoretic mobility shift assay of RNA-RNA complexes. Methods Mol. Biol., 1240, 153–163CrossRefPubMedGoogle Scholar
  24. 24.
    Li, X., Nishizuka, H., Tsutsumi, K., Imai, Y., Kurihara, Y. and Uesugi, S. (2007) Structure, interactions and effects on activity of the 5′-terminal region of human telomerase RNA. J. Biochem., 141, 755–765CrossRefPubMedGoogle Scholar
  25. 25.
    Hahn, D., Kudla, G., Tollervey, D. and Beggs, J. D. (2012) Brr2pmediated conformational rearrangements in the spliceosome during activation and substrate repositioning. Genes Dev., 26, 2408–2421CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Di Primo, C., Dausse, E. and Toulmé, J. J. (2011) Surface plasmon resonance investigation of RNA aptamer-RNA ligand interactions. Methods Mol. Biol., 764, 279–300CrossRefPubMedGoogle Scholar
  27. 27.
    Palau, W., Masante, C., Ventura, M. and Di Primo, C. (2013) Direct evidence for RNA-RNA interactions at the 3′ end of the Hepatitis C virus genome using surface plasmon resonance. RNA, 19, 982–991CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Yu, D., Qin, P. and Cornish, P. V. (2015) Single molecule studies of RNA-RNA interactions. Methods Mol. Biol., 1240, 97–112CrossRefPubMedGoogle Scholar
  29. 29.
    Hardin, J. W., Warnasooriya, C., Kondo, Y., Nagai, K. and Rueda, D. (2015) Assembly and dynamics of the U4/U6 di-snRNP by single-molecule FRET. Nucleic Acids Res., 43, 10963–10974CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Liang, X. H. and Fournier, M. J. (2006) The helicase Has1p is required for snoRNA release from pre-rRNA. Mol. Cell. Biol., 26, 7437–7450CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Fayet-Lebaron, E., Atzorn, V., Henry, Y. and Kiss, T. (2009) 18S rRNA processing requires base pairings of snR30 H/ACA snoRNA to eukaryote-specific 18S sequences. EMBO J., 28, 1260–1270CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Piganeau, N., Schauer, U. E. and Schroeder, R. (2006) A yeast RNA-hybrid system for the detection of RNA-RNA interactions in vivo. RNA, 12, 177–184CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Piganeau, N. and Schroeder, R. (2006) Identification and detection of RNA-RNA interactions using the yeast RNA hybrid system. Nat. Protoc., 1, 689–694CrossRefPubMedGoogle Scholar
  34. 34.
    Kudla, G., Granneman, S., Hahn, D., Beggs, J. D. and Tollervey, D. (2011) Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc. Natl. Acad. Sci. USA, 108, 10010–10015CrossRefPubMedGoogle Scholar
  35. 35.
    Helwak, A., Kudla, G., Dudnakova, T. and Tollervey, D. (2013) Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell, 153, 654–665CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Waters, S. A., McAteer, S. P., Kudla, G., Pang, I., Deshpande, N. P., Amos, T. G., Leong, K.W., Wilkins, M. R., Strugnell, R., Gally, D. L., et al. (2017) Small RNA interactome of pathogenic E. coli revealed through crosslinking of RNase E. EMBO J., 36, 374–387CrossRefPubMedGoogle Scholar
  37. 37.
    Liu, T., Zhang, K., Xu, S., Wang, Z., Fu, H., Tian, B., Zheng, X. and Li, W. (2017) Detecting RNA-RNA interactions in E. coli using a modified CLASH method. BMC Genomics, 18, 343CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Kretz, M., Siprashvili, Z., Chu, C., Webster, D. E., Zehnder, A., Qu, K., Lee, C. S., Flockhart, R. J., Groff, A. F., Chow, J., et al. (2013) Control of somatic tissue differentiation by the long noncoding RNA TINCR. Nature, 493, 231–235CrossRefPubMedGoogle Scholar
  39. 39.
    Engreitz, J. M., Sirokman, K., McDonel, P., Shishkin, A. A., Surka, C., Russell, P., Grossman, S. R., Chow, A. Y., Guttman, M. and Lander, E. S. (2014) RNA-RNA interactions enable specific targeting of noncoding RNAs to nascent Pre-mRNAs and chromatin sites. Cell, 159, 188–199CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Engreitz, J., Lander, E. S. and Guttman, M. (2015) RNA antisense purification (RAP) for mapping RNA interactions with chromatin. Methods Mol. Biol., 1262, 183–197CrossRefPubMedGoogle Scholar
  41. 41.
    Lu, Z., Zhang, Q. C., Lee, B., Flynn, R. A., Smith, M. A., Robinson, J. T., Davidovich, C., Gooding, A. R., Goodrich, K. J., Mattick, J. S., et al. (2016) RNA duplex map in living cells reveals higher-order transcriptome structure. Cell, 165, 1267–1279CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Lu, Z., Gong, J. and Zhang, Q. C. (2018) PARIS: psoralen analysis of RNA interactions and structures with high throughput and resolution. Methods Mol. Biol., 1649, 59–84CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Aw, J. G., Shen, Y., Wilm, A., Sun, M., Lim, X. N., Boon, K. L., Tapsin, S., Chan, Y. S., Tan, C. P., Sim, A. Y., et al. (2016) In vivo mapping of eukaryotic RNA interactomes reveals principles of higher-order organization and regulation. Mol. Cell, 62, 603–617CrossRefPubMedGoogle Scholar
  44. 44.
    Aw, J. G. A., Shen, Y., Nagarajan, N. and Wan, Y. (2017) Mapping RNA-RNA interactions globally using biotinylated psoralen. J. Vis. Exp., 123Google Scholar
  45. 45.
    Sharma, E., Sterne-Weiler, T., O’Hanlon, D. and Blencowe, B. J. (2016) Global mapping of human RNA-RNA interactions. Mol. Cell, 62, 618–626CrossRefPubMedGoogle Scholar
  46. 46.
    Nguyen, T. C., Cao, X., Yu, P., Xiao, S., Lu, J., Biase, F. H., Sridhar, B., Huang, N., Zhang, K. and Zhong, S. (2016) Mapping RNA-RNA interactome and RNA structure in vivo. by MARIO. Nat. Commun., 7, 12023CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kertesz, M., Wan, Y., Mazor, E., Rinn, J. L., Nutter, R. C., Chang, H. Y. and Segal, E. (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature, 467, 103–107CrossRefPubMedGoogle Scholar
  48. 48.
    Wan, Y., Qu, K., Zhang, Q. C., Flynn, R. A., Manor, O., Ouyang, Z., Zhang, J., Spitale, R. C., Snyder, M. P., Segal, E., et al. (2014) Landscape and variation of RNA secondary structure across the human transcriptome. Nature, 505, 706–709CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Underwood, J. G., Uzilov, A. V., Katzman, S., Onodera, C. S., Mainzer, J. E., Mathews, D. H., Lowe, T. M., Salama, S. R. and Haussler, D. (2010) FragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing. Nat. Methods, 7, 995–1001CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Rouskin, S., Zubradt, M., Washietl, S., Kellis, M. and Weissman, J. S. (2014) Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature, 505, 701–705CrossRefPubMedGoogle Scholar
  51. 51.
    Ding, Y., Tang, Y., Kwok, C. K., Zhang, Y., Bevilacqua, P. C. and Assmann, S. M. (2014) In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature, 505, 696–700CrossRefPubMedGoogle Scholar
  52. 52.
    Spitale, R. C., Flynn, R. A., Zhang, Q. C., Crisalli, P., Lee, B., Jung, J. W., Kuchelmeister, H. Y., Batista, P. J., Torre, E. A., Kool, E. T., et al. (2015) Structural imprints in vivo. decode RNA regulatory mechanisms. Nature, 519, 486–490CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Wan, Y., Kertesz, M., Spitale, R. C., Segal, E. and Chang, H. Y. (2011) Understanding the transcriptome through RNA structure. Nat. Rev. Genet., 12, 641–655CrossRefPubMedGoogle Scholar
  54. 54.
    Mortimer, S. A., Kidwell, M. A. and Doudna, J. A. (2014) Insights into RNA structure and function from genome-wide studies. Nat. Rev. Genet., 15, 469–479CrossRefPubMedGoogle Scholar
  55. 55.
    Kwok, C. K., Tang, Y., Assmann, S. M. and Bevilacqua, P. C. (2015) The RNA structurome: transcriptome-wide structure probing with next-generation sequencing. Trends Biochem. Sci., 40, 221–232CrossRefPubMedGoogle Scholar
  56. 56.
    Kwok, C. K. (2016) Dawn of the in vivo. RNA structurome and interactome. Biochem. Soc. Trans., 44, 1395–1410CrossRefPubMedGoogle Scholar
  57. 57.
    Bai, Y., Dai, X., Harrison, A., Johnston, C. and Chen, M. (2016) Toward a next-generation atlas of RNA secondary structure. Brief. Bioinform., 17, 63–77CrossRefPubMedGoogle Scholar
  58. 58.
    Bevilacqua, P. C., Ritchey, L. E., Su, Z. and Assmann, S. M. (2016) Genome-wide analysis of RNA secondary structure. Annu. Rev. Genet., 50, 235–266CrossRefPubMedGoogle Scholar
  59. 59.
    Piao, M., Sun, L. and Zhang, Q. C. (2017) RNA regulations and functions decoded by transcriptome-wide RNA structure probing. Genom. Proteom. Bioinform., 15, 267–278CrossRefGoogle Scholar
  60. 60.
    Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406–3415CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    DiChiacchio, L. and Mathews, D. H. (2016) Predicting RNA-RNA interactions using RNA structure. Methods Mol. Biol., 1490, 51–62CrossRefPubMedGoogle Scholar
  62. 62.
    Morozova, O., Hirst, M. and Marra, M. A. (2009) Applications of new sequencing technologies for transcriptome analysis. Annu. Rev. Genomics Hum. Genet., 10, 135–151CrossRefPubMedGoogle Scholar
  63. 63.
    Melamed, S., Peer, A., Faigenbaum-Romm, R., Gatt, Y. E., Reiss, N., Bar, A., Altuvia, Y., Argaman, L. and Margalit, H. (2016) Global mapping of small RNA-target interactions in bacteria. Mol. Cell, 63, 884–897CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Sugimoto, Y., Vigilante, A., Darbo, E., Zirra, A., Militti, C., D’Ambrogio, A., Luscombe, N. M. and Ule, J. (2015) hiCLIP reveals the in vivo. atlas of mRNA secondary structures recognized by Staufen 1. Nature, 519, 491–494CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Sugimoto, Y., Chakrabarti, A. M., Luscombe, N. M. and Ule, J. (2017) Using hiCLIP to identify RNA duplexes that interact with a specific RNA-binding protein. Nat. Protoc., 12, 611–637CrossRefPubMedGoogle Scholar
  66. 66.
    Lustig, Y., Wachtel, C., Safro, M., Liu, L. and Michaeli, S. (2010) “RNA walk” a novel approach to study RNA-RNA interactions between a small RNA and its target. Nucleic Acids Res., 38, e5CrossRefPubMedGoogle Scholar
  67. 67.
    Wachtel, C. and Michaeli, S. (2011) Functional analysis of noncoding RNAs in trypanosomes: RNA walk, a novel approach to study RNA-RNA interactions between small RNA and its target. Methods Mol. Biol., 718, 245–257CrossRefPubMedGoogle Scholar
  68. 68.
    Ramani, V., Qiu, R. and Shendure, J. (2015) High-throughput determination of RNA structure by proximity ligation. Nat. Biotechnol., 33, 980–984CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Bushati, N. and Cohen, S. M. (2007) microRNA functions. Annu. Rev. Cell Dev. Biol., 23, 175–205CrossRefPubMedGoogle Scholar
  70. 70.
    Hutvágner, G. and Zamore, P. D. (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science, 297, 2056–2060CrossRefPubMedGoogle Scholar
  71. 71.
    Brodersen, P. and Voinnet, O. (2009) Revisiting the principles of microRNA target recognition and mode of action. Nat. Rev. Mol. Cell Biol., 10, 141–148CrossRefPubMedGoogle Scholar
  72. 72.
    John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C. and Marks, D. S. (2004) Human microRNA targets. PLoS Biol., 2, e363CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Kiss, T. (2001) Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J., 20, 3617–3622CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Bachellerie, J. P., Cavaillé, J. and Hüttenhofer, A. (2002) The expanding snoRNA world. Biochimie, 84, 775–790CrossRefPubMedGoogle Scholar
  75. 75.
    Tanner, N. K. and Linder, P. (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol. Cell, 8, 251–262CrossRefPubMedGoogle Scholar
  76. 76.
    Bleichert, F. and Baserga, S. J. (2007) The long unwinding road of RNA helicases. Mol. Cell, 27, 339–352CrossRefPubMedGoogle Scholar
  77. 77.
    Leeds, N. B., Small, E. C., Hiley, S. L., Hughes, T. R. and Staley, J. P. (2006) The splicing factor Prp43p, a DEAH box ATPase, functions in ribosome biogenesis. Mol. Cell. Biol., 26, 513–522CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Bohnsack, M. T., Martin, R., Granneman, S., Ruprecht, M., Schleiff, E. and Tollervey, D. (2009) Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol. Cell, 36, 583–592CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Ponting, C. P., Oliver, P. L. and Reik, W. (2009) Evolution and functions of long noncoding RNAs. Cell, 136, 629–641CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Geisler, S. and Coller, J. (2013) RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nat. Rev. Mol. Cell Biol., 14, 699–712CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Wang, G. Q., Wang, Y., Xiong, Y., Chen, X. C., Ma, M. L., Cai, R., Gao, Y., Sun, Y. M., Yang, G. S. and Pang, W. J. (2016) Sirt1 AS lncRNA interacts with its mRNA to inhibit muscle formation by attenuating function of miR-34a. Sci. Rep., 6, 21865CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Gong, C. and Maquat, L. E. (2011) lncRNAs transactivate STAU1- mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature, 470, 284–288CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Berk, V., Zhang, W., Pai, R. D. and Cate, J. H. (2006) Structural basis for mRNA and tRNA positioning on the ribosome. Proc. Natl. Acad. Sci. USA, 103, 15830–15834CrossRefPubMedGoogle Scholar
  84. 84.
    Salmena, L., Poliseno, L., Tay, Y., Kats, L. and Pandolfi, P. P. (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell, 146, 353–358CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Qi, X., Zhang, D. H., Wu, N., Xiao, J. H., Wang, X. and Ma, W. (2015) ceRNA in cancer: possible functions and clinical implications. J. Med. Genet., 52, 710–718CrossRefPubMedGoogle Scholar
  86. 86.
    An, Y., Furber, K. L. and Ji, S. (2017) Pseudogenes regulate parental gene expression via ceRNA network. J. Cell. Mol. Med., 21, 185–192CrossRefPubMedGoogle Scholar
  87. 87.
    Chiu, H. S., Martínez, M. R., Bansal, M., Subramanian, A., Golub, T. R., Yang, X., Sumazin, P. and Califano, A. (2017) Highthroughput validation of ceRNA regulatory networks. BMC Genomics, 18, 418CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Gong, J., Shao, D., Xu, K., Lu, Z., Lu, Z. J., Yang, Y. T. and Zhang, Q. C. (2017) RISE: a database of RNA interactome from sequencing experiments. Nucleic Acids Res., 46, D194–D201PubMedCentralGoogle Scholar
  89. 89.
    Barabási, A. L. and Oltvai, Z. N. (2004) Network biology: understanding the cell’s functional organization. Nat. Rev. Genet., 5, 101–113CrossRefPubMedGoogle Scholar
  90. 90.
    Panni, S., Prakash, A., Bateman, A. and Orchard, S. (2017) The yeast noncoding RNA interaction network. RNA, 23, 1479–1492CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Albert, R. (2005) Scale-free networks in cell biology. J. Cell Sci., 118, 4947–4957CrossRefPubMedGoogle Scholar
  92. 92.
    Albert, R. and Barabasi, A. L. (2002) Statistical mechanics of complex networks. Rev. Mod. Phys., 74, 47–97CrossRefGoogle Scholar
  93. 93.
    Garrett-Wheeler, E., Lockard, R. E. and Kumar, A. (1984) Mapping of psoralen cross-linked nucleotides in RNA. Nucleic Acids Res., 12, 3405–3424CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Harris, M. E. and Christian, E. L. (2009) RNA Crosslinking Methods. In Methods in Enzymology, Vol 468: Biophysical, Chemical, and Functional Probes of RNA Structure, Interactions and Folding: Part A, pp. 127–146. ElsevierCrossRefGoogle Scholar
  95. 95.
    Graveley, B. R. (2016) RNA matchmaking: finding cellular pairing partners. Mol. Cell, 63, 186–189CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Hao, Y., Wu, W., Li, H., Yuan, J., Luo, J., Zhao, Y. and Chen, R. (2016) NPInter v3.0: an upgraded database of noncoding RNAassociated interactions. Database (Oxford), 2016, baw057CrossRefGoogle Scholar
  97. 97.
    Yi, Y., Zhao, Y., Li, C., Zhang, L., Huang, H., Li, Y., Liu, L., Hou, P., Cui, T., Tan, P., et al. (2017) RAID v2.0: an updated resource of RNA-associated interactions across organisms. Nucleic Acids Res., 45, D115–D118CrossRefPubMedGoogle Scholar
  98. 98.
    Junge, A., Refsgaard, J. C., Garde, C., Pan, X., Santos, A., Alkan, F., Anthon, C., von Mering, C., Workman, C. T., Jensen, L. J., et al. (2017) RAIN: RNA-protein association and interaction networks. Database (Oxford), 2017, baw167CrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jing Gong
    • 1
  • Yanyan Ju
    • 1
  • Di Shao
    • 1
  • Qiangfeng Cliff Zhang
    • 1
  1. 1.MOE Key Laboratory of Bioinformatics, Beijing Advanced Innovation Center for Structural Biology, Center for Synthetic and Systems Biology, Tsinghua-Peking Joint Center for Life Sciences, School of Life SciencesTsinghua UniversityBeijingChina

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