Functional roles of non-coding Y RNAs

International Journal of Biochemistry and Cell Biology

Volumn 66, Issue , 2015, Pages 20-29

  Kowalski, Madzia P ^a,b   Krude, Torsten ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA replication; Non coding RNA; RNA domains; RNA stability; Y RNA

Indexed keywords

NON CODING Y RNA; RNA BINDING PROTEIN; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA; RIBONUCLEOPROTEIN;

ARTICLE; BIOCHEMISTRY; CELLULAR STRESS RESPONSE; DNA REPLICATION; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; RNA STABILITY; RNA STRUCTURE; ANIMAL; CHEMISTRY; CONFORMATION; GENETICS; MOLECULAR GENETICS; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE;

EUKARYOTA; MAMMALIA; NEMATODA; PROKARYOTA; VERTEBRATA;

ANIMALS; BASE SEQUENCE; DNA REPLICATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RIBONUCLEOPROTEINS; RNA, UNTRANSLATED;

EID: 84937209030     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2015.07.003     Document Type: Review

References (104)

1. M.N. Aftab, H. He, G. Skogerbo, and R. Chen Microarray analysis of ncRNA expression patterns in Caenorhabditis elegans after RNAi against snoRNA associated proteins BMC Genomics 9 2008 278
2. A. Belisova, K. Semrad, O. Mayer, G. Kocian, E. Waigmann, R. Schroeder, and G. Steiner RNA chaperone activity of protein components of human Ro RNPs RNA 11 2005 1084 1094
3. J.J. Blow, S.M. Dilworth, C. Dingwall, A.D. Mills, and R.A. Laskey Chromosome replication in cell-free systems from Xenopus eggs Philos. Trans. R. Soc. Lond. B: Biol. Sci. 317 1987 483 494
4. I. Boria, A.R. Gruber, A. Tanzer, S.H. Bernhart, R. Lorenz, M.M. Mueller, I.L. Hofacker, and P.F. Stadler Nematode sbRNAs: homologs of vertebrate Y RNAs J. Mol. Evol. 70 2010 346 358
5. P. Bouffard, E. Barbar, F. Briere, and G. Boire Interaction cloning and characterization of RoBPI, a novel protein binding to human Ro ribonucleoproteins RNA 6 2000 66 78
6. C.J. Chen, and E. Heard Small RNAs derived from structural non-coding RNAs Methods 63 2013 76 84
7. X. Chen, H. Liang, J. Zhang, K. Zen, and C.Y. Zhang Horizontal transfer of microRNAs: molecular mechanisms and clinical applications Protein Cell 3 2012 28 37
8. X. Chen, A.M. Quinn, and S.L. Wolin Ro ribonucleoproteins contribute to the resistance of Deinococcus radiodurans to ultraviolet irradiation Genes Dev. 14 2000 777 782
9. X. Chen, S. Sim, E.J. Wurtmann, A. Feke, and S.L. Wolin Bacterial noncoding Y RNAs are widespread and mimic tRNAs RNA 20 2014 1715 1724
10. X. Chen, J.D. Smith, H. Shi, D.D. Yang, R.A. Flavell, and S.L. Wolin The Ro autoantigen binds misfolded U2 small nuclear RNAs and assists mammalian cell survival after UV irradiation Curr. Biol. 13 2003 2206 2211
11. X. Chen, D.W. Taylor, C.C. Fowler, J.E. Galan, H.W. Wang, and S.L. Wolin An RNA degradation machine sculpted by Ro autoantigen and noncoding RNA Cell 153 2013 166 177
12. X. Chen, and S.L. Wolin The Ro 60 kDa autoantigen: insights into cellular function and role in autoimmunity J. Mol. Med. (Berl.) 82 2004 232 239
13. X. Chen, E.J. Wurtmann, J. Van Batavia, B. Zybailov, M.P. Washburn, and S.L. Wolin An ortholog of the Ro autoantigen functions in 23S rRNA maturation in D. radiodurans Genes Dev. 21 2007 1328 1339
14. Y.L. Chiu, H.E. Witkowska, S.C. Hall, M. Santiago, V.B. Soros, C. Esnault, T. Heidmann, and W.C. Greene High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition Proc. Natl. Acad. Sci. U. S. A. 103 2006 15588 15593
15. C.P. Christov, T.J. Gardiner, D. Szüts, and T. Krude Functional requirement of noncoding Y RNAs for human chromosomal DNA replication Mol. Cell. Biol. 26 2006 6993 7004
16. C.P. Christov, E. Trivier, and T. Krude Noncoding human Y RNAs are overexpressed in tumours and required for cell proliferation Br. J. Cancer 98 2008 981 988
17. M.B. Clark, P.P. Amaral, F.J. Schlesinger, M.E. Dinger, R.J. Taft, J.L. Rinn, C.P. Ponting, P.F. Stadler, K.V. Morris, A. Morillon, J.S. Rozowsky, M.B. Gerstein, C. Wahlestedt, Y. Hayashizaki, P. Carninci, T.R. Gingeras, and J.S. Mattick The reality of pervasive transcription PLoS Biol. 9 2011 e1000625 discussion e1001102
18. C. Collart, C.P. Christov, J.C. Smith, and T. Krude The midblastula transition defines the onset of Y RNA-dependent DNA replication in Xenopus laevis Mol. Cell. Biol. 31 2011 3857 3870
19. W. Deng, X. Zhu, G. Skogerbo, Y. Zhao, Z. Fu, Y. Wang, H. He, L. Cai, H. Sun, C. Liu, B. Li, B. Bai, J. Wang, D. Jia, S. Sun, H. He, Y. Cui, Y. Wang, D. Bu, and R. Chen Organization of the Caenorhabditis elegans small non-coding transcriptome: genomic features, biogenesis, and expression Genome Res. 16 2006 20 29
20. J.M. Dhahbi Circulating small noncoding RNAs as biomarkers of aging Ageing Res. Rev. 17 2014 86 98
21. J.M. Dhahbi, S.R. Spindler, H. Atamna, D. Boffelli, and D.I. Martin Deep sequencing of serum small RNAs identifies patterns of 5′ tRNA half and YRNA fragment expression associated with breast cancer Biomark. Cancer 6 2014 37 47
22. J.M. Dhahbi, S.R. Spindler, H. Atamna, D. Boffelli, P. Mote, and D.I. Martin 5′-YRNA fragments derived by processing of transcripts from specific YRNA genes and pseudogenes are abundant in human serum and plasma Physiol. Genomics 45 2013 990 998
23. F.F. Duarte Jr., Q.A. de Lima Neto, S. Rando Fdos, D.V. de Freitas, J.R. Pattaro Junior, L.G. Polizelli, R.E. Munhoz, F.A. Seixas, and M.A. Fernandez Identification and molecular structure analysis of a new noncoding RNA, a sbRNA homolog, in the silkworm Bombyx mori genome Mol. BioSyst. 11 2015 801 808
24. G. Fabini, R. Raijmakers, S. Hayer, M.A. Fouraux, G.J. Pruijn, and G. Steiner The heterogeneous nuclear ribonucleoproteins I and K interact with a subset of the Ro ribonucleoprotein-associated Y RNAs in vitro and in vivo J. Biol. Chem. 276 2001 20711 20718
25. G. Fabini, S.A. Rutjes, C. Zimmermann, G.J. Pruijn, and G. Steiner Analysis of the molecular composition of Ro ribonucleoprotein complexes. Identification of novel Y RNA-binding proteins Eur. J. Biochem. 267 2000 2778 2789
26. A.D. Farris, J.K. Gross, J.S. Hanas, and J.B. Harley Genes for murine Y1 and Y3 Ro RNAs have class 3 RNA polymerase III promoter structures and are unlinked on mouse chromosome 6 Gene 174 1996 35 42
27. A.D. Farris, G. Koelsch, G.J. Pruijn, W.J. van Venrooij, and J.B. Harley Conserved features of Y RNAs revealed by automated phylogenetic secondary structure analysis Nucleic Acids Res. 27 1999 1070 1078
28. A.D. Farris, F. Puvion-Dutilleul, E. Puvion, J.B. Harley, and L.A. Lee The ultrastructural localization of 60-kDa Ro protein and human cytoplasmic RNAs: association with novel electron-dense bodies Proc. Natl. Acad. Sci. U. S. A. 94 1997 3040 3045
29. M.A. Fouraux, P. Bouvet, S. Verkaart, W.J. van Venrooij, and G.J. Pruijn Nucleolin associates with a subset of the human Ro ribonucleoprotein complexes J. Mol. Biol. 320 2002 475 488
30. G. Fuchs, A.J. Stein, C. Fu, K.M. Reinisch, and S.L. Wolin Structural and biochemical basis for misfolded RNA recognition by the Ro autoantigen Nat. Struct. Mol. Biol. 13 2006 1002 1009
31. S. Gallois-Montbrun, R.K. Holmes, C.M. Swanson, M. Fernandez-Ocana, H.L. Byers, M.A. Ward, and M.H. Malim Comparison of cellular ribonucleoprotein complexes associated with the APOBEC3F and APOBEC3G antiviral proteins J. Virol. 82 2008 5636 5642
32. E.L. Garcia, A. Onafuwa-Nuga, S. Sim, S.R. King, S.L. Wolin, and A. Telesnitsky Packaging of host mY RNAs by murine leukemia virus may occur early in Y RNA biogenesis J. Virol. 83 2009 12526 12534
33. T.J. Gardiner, C.P. Christov, A.R. Langley, and T. Krude A conserved motif of vertebrate Y RNAs essential for chromosomal DNA replication RNA 15 2009 1375 1385
34. M. Gendron, D. Roberge, and G. Boire Heterogeneity of human Ro ribonucleoproteins (RNPS): nuclear retention of Ro RNPS containing the human hY5 RNA in human and mouse cells Clin. Exp. Immunol. 125 2001 162 168
35. H. Ginisty, H. Sicard, B. Roger, and P. Bouvet Structure and functions of nucleolin J. Cell Sci. 112 Pt 6 1999 761 772
36. C.D. Green, K.S. Long, H. Shi, and S.L. Wolin Binding of the 60-kDa Ro autoantigen to Y RNAs: evidence for recognition in the major groove of a conserved helix RNA 4 1998 750 765
37. C. Gwizdek, E. Bertrand, C. Dargemont, J.C. Lefebvre, J.M. Blanchard, R.H. Singer, and A. Doglio Terminal minihelix, a novel RNA motif that directs polymerase III transcripts to the cell cytoplasm. Terminal minihelix and RNA export J. Biol. Chem. 276 2001 25910 25918
38. C. Gwizdek, B. Ossareh-Nazari, A.M. Brownawell, A. Doglio, E. Bertrand, I.G. Macara, and C. Dargemont Exportin-5 mediates nuclear export of minihelix-containing RNAs J. Biol. Chem. 278 2003 5505 5508
39. A.E. Hall, and T. Dalmay Discovery of novel small RNAs in the quest to unravel genome complexity Biochem. Soc. Trans. 41 2013 866 870
40. A.E. Hall, C. Turnbull, and T. Dalmay Y RNAs: recent developments Biomol. Concepts 4 2013 103 110
41. J.P. Hendrick, S.L. Wolin, J. Rinke, M.R. Lerner, and J.A. Steitz Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells Mol. Cell. Biol. 1 1981 1138 1149
42. J.R. Hogg, and K. Collins Human Y5 RNA specializes a Ro ribonucleoprotein for 5S ribosomal RNA quality control Genes Dev. 21 2007 3067 3072
43. A.M. Hoy, and A.H. Buck Extracellular small RNAs: what, where, why? Biochem. Soc. Trans. 40 2012 886 890
44. M.K. Iyer, Y.S. Niknafs, R. Malik, U. Singhal, A. Sahu, Y. Hosono, T.R. Barrette, J.R. Prensner, J.R. Evans, S. Zhao, A. Poliakov, X. Cao, S.M. Dhanasekaran, Y.M. Wu, D.R. Robinson, D.G. Beer, F.Y. Feng, H.K. Iyer, and A.M. Chinnaiyan The landscape of long noncoding RNAs in the human transcriptome Nat. Genet. 47 2015 199 208
45. M. Köhn, N. Pazaitis, and S. Huttelmaier Why YRNAs? About versatile RNAs and their functions Biomolecules 3 2013 143 156
46. M.P. Kowalski, H.A. Baylis, and T. Krude Non-coding stem-bulge RNAs are required for cell proliferation and embryonic development in C. elegans J. Cell Sci. 128 2015 2118 2129
47. A.M. Krecic, and M.S. Swanson hnRNP complexes: composition, structure, and function Curr. Opin. Cell Biol. 11 1999 363 371
48. T. Krude Initiation of human DNA replication in vitro using nuclei from cells arrested at an initiation-competent state J. Biol. Chem. 275 2000 13699 13707
49. T. Krude Non-coding RNAs: new players in the field of eukaryotic DNA replication Subcell Biochem. 50 2010 105 118
50. T. Krude, C.P. Christov, O. Hyrien, and K. Marheineke Y RNA functions at the initiation step of mammalian chromosomal DNA replication J. Cell Sci. 122 2009 2836 2845
51. T. Krude, M. Jackman, J. Pines, and R.A. Laskey Cyclin/Cdk-dependent initiation of DNA replication in a human cell-free system Cell 88 1997 109 119
52. J.C. Labbe, J. Burgess, L.A. Rokeach, and S. Hekimi ROP-1, an RNA quality-control pathway component, affects Caenorhabditis elegans dauer formation Proc. Natl. Acad. Sci. U. S. A. 97 2000 13233 13238
53. J.C. Labbe, S. Hekimi, and L.A. Rokeach Assessing the function of the Ro ribonucleoprotein complex using Caenorhabditis elegans as a biological tool Biochem. Cell Biol. 77 1999 349 354
54. J.C. Labbe, S. Hekimi, and L.A. Rokeach The levels of the RoRNP-associated Y RNA are dependent upon the presence of ROP-1, the Caenorhabditis elegans Ro60 protein Genetics 151 1999 143 150
55. D. Langenberger, M.V. Cakir, S. Hoffmann, and P.F. Stadler Dicer-processed small RNAs: rules and exceptions J. Exp. Zool. B: Mol. Dev. Evol. 320 2013 35 46
56. A.R. Langley, H. Chambers, C.P. Christov, and T. Krude Ribonucleoprotein particles containing non-coding Y RNAs, Ro60, La and nucleolin are not required for Y RNA function in DNA replication PLoS ONE 5 2010 e13673
57. A.R. Langley, J.C. Smith, D.L. Stemple, and S.A. Harvey New insights into the maternal to zygotic transition Development 141 2014 3834 3841
58. R.A. Laskey, R.M. Harland, W.C. Earnshaw, and C. Dingwall Chromatin assembly and the co-ordination of DNA replication in the eukaryotic chromosome H.G. Schweiger, International Cell Biology 1980-1981 1981 Springer Verlag Berlin 162 167
59. M.R. Lerner, J.A. Boyle, J.A. Hardin, and J.A. Steitz Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus Science 211 1981 400 402
60. R. Maraia, A.L. Sakulich, E. Brinkmann, and E.D. Green Gene encoding human Ro-associated autoantigen Y5 RNA Nucleic Acids Res. 24 1996 3552 3559
61. R.J. Maraia, N. Sasaki-Tozawa, C.T. Driscoll, E.D. Green, and G.J. Darlington The human Y4 small cytoplasmic RNA gene is controlled by upstream elements and resides on chromosome 7 with all other hY scRNA genes Nucleic Acids Res. 22 1994 3045 3052
62. A.G. Matera, M.R. Frey, K. Margelot, and S.L. Wolin A perinucleolar compartment contains several RNA polymerase III transcripts as well as the polypyrimidine tract-binding protein, hnRNP I J. Cell Biol. 129 1995 1181 1193
63. E. Meiri, A. Levy, H. Benjamin, M. Ben-David, L. Cohen, A. Dov, N. Dromi, E. Elyakim, N. Yerushalmi, O. Zion, G. Lithwick-Yanai, and E. Sitbon Discovery of microRNAs and other small RNAs in solid tumors Nucleic Acids Res. 38 2010 6234 6246
64. A. Mosig, M. Guofeng, B.M.R. Stadler, and P.F. Stadler Evolution of the vertebrate Y RNA cluster Theory Biosci. 129 2007 9 14
65. F.E. Nicolas, A.E. Hall, T. Csorba, C. Turnbull, and T. Dalmay Biogenesis of Y RNA-derived small RNAs is independent of the microRNA pathway FEBS Lett. 586 2012 1226 1230
66. E.N. Nolte-'t Hoen, H.P. Buermans, M. Waasdorp, W. Stoorvogel, M.H. Wauben, and P.A. 't Hoen Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions Nucleic Acids Res. 40 2012 9272 9285
67. C.A. O'Brien, K. Margelot, and S.L. Wolin Xenopus Ro ribonucleoproteins: members of an evolutionarily conserved class of cytoplasmic ribonucleoproteins Proc. Natl. Acad. Sci. U. S. A. 90 1993 7250 7254
68. C.A. O'Brien, and S.L. Wolin A possible role for the 60-kD Ro autoantigen in a discard pathway for defective 5S rRNA precursors Genes Dev. 8 1994 2891 2903
69. P.S. Page-McCaw, K. Amonlirdviman, and P.A. Sharp PUF60: a novel U2AF65-related splicing activity RNA 5 1999 1548 1560
70. R. Peek, G.J. Pruijn, A.J. van der Kemp, and W.J. van Venrooij Subcellular distribution of Ro ribonucleoprotein complexes and their constituents J. Cell Sci. 106 Pt 3 1993 929 935
71. J. Perreault, J.P. Perreault, and G. Boire The Ro associated Y RNAs in metazoans: evolution and diversification Mol. Biol. Evol. 24 2007 1678 1689
72. G.J. Pruijn, F.H. Simons, and W.J. van Venrooij Intracellular localization and nucleocytoplasmic transport of Ro RNP components Eur. J. Cell Biol. 74 1997 123 132
73. G.J. Pruijn, R.L. Slobbe, and W.J. van Venrooij Analysis of protein-RNA interactions within Ro ribonucleoprotein complexes Nucleic Acids Res. 19 1991 5173 5180
74. S. Rother, and G. Meister Small RNAs derived from longer non-coding RNAs Biochimie 93 2011 1905 1915
75. S.A. Rutjes, E. Lund, A. van der Heijden, C. Grimm, W.J. van Venrooij, and G.J. Pruijn Identification of a novel cis-acting RNA element involved in nuclear export of hY RNAs RNA 7 2001 741 752
76. S.A. Rutjes, A. van der Heijden, P.J. Utz, W.J. van Venrooij, and G.J. Pruijn Rapid nucleolytic degradation of the small cytoplasmic Y RNAs during apoptosis J. Biol. Chem. 274 1999 24799 24807
77. P. Sarkies, and E.A. Miska Small RNAs break out: the molecular cell biology of mobile small RNAs Nat Rev. Mol. Cell Biol. 15 2014 525 535
78. S. Sim, D.E. Weinberg, G. Fuchs, K. Choi, J. Chung, and S.L. Wolin The subcellular distribution of an RNA quality control protein, the Ro autoantigen, is regulated by noncoding Y RNA binding Mol. Biol. Cell 20 2009 1555 1564
79. S. Sim, and S.L. Wolin Emerging roles for the Ro 60-kDa autoantigen in noncoding RNA metabolism Wiley Interdiscip. Rev. RNA 2 2011 686 699
80. S. Sim, J. Yao, D.E. Weinberg, S. Niessen, J.R. Yates 3rd, and S.L. Wolin The zipcode-binding protein ZBP1 influences the subcellular location of the Ro 60-kDa autoantigen and the noncoding Y3 RNA RNA 18 2012 100 110
81. F.H. Simons, G.J. Pruijn, and W.J. van Venrooij Analysis of the intracellular localization and assembly of Ro ribonucleoprotein particles by microinjection into Xenopus laevis oocytes J. Cell Biol. 125 1994 981 988
82. F.H. Simons, S.A. Rutjes, W.J. van Venrooij, and G.J. Pruijn The interactions with Ro60 and La differentially affect nuclear export of hY1 RNA RNA 2 1996 264 273
83. J.E. Stefano Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts Cell 36 1984 145 154
84. A.J. Stein, G. Fuchs, C. Fu, S.L. Wolin, and K.M. Reinisch Structural insights into RNA quality control: the Ro autoantigen binds misfolded RNAs via its central cavity Cell 121 2005 529 539
85. J.A. Steitz, C. Berg, J.P. Hendrick, H. La Branche-Chabot, A. Metspalu, J. Rinke, and T. Yario A 5S rRNA/L5 complex is a precursor to ribosome assembly in mammalian cells J. Cell Biol. 106 1988 545 556
86. S.W. Teunissen, M.J. Kruithof, A.D. Farris, J.B. Harley, W.J. van Venrooij, and G.J. Pruijn Conserved features of Y RNAs: a comparison of experimentally derived secondary structures Nucleic Acids Res. 28 2000 610 619
87. A.C. Tuck, and D. Tollervey RNA in pieces Trends Genet. 27 2011 422 432
88. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J.J. Lee, and J.O. Lotvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat. Cell Biol. 9 2007 654 659
89. C.W. van Gelder, J.P. Thijssen, E.C. Klaassen, C. Sturchler, A. Krol, W.J. van Venrooij, and G.J. Pruijn Common structural features of the Ro RNP associated hY1 and hY5 RNAs Nucleic Acids Res. 22 1994 2498 2506
90. D.J. Van Horn, D. Eisenberg, C.A. O'Brien, and S.L. Wolin Caenorhabditis elegans embryos contain only one major species of Ro RNP RNA 1 1995 293 303
91. A.P. Verhagen, and G.J. Pruijn Are the Ro RNP-associated Y RNAs concealing microRNAs? Y RNA-derived miRNAs may be involved in autoimmunity Bioessays 33 2011 674 682
92. L. Vojtech, S. Woo, S. Hughes, C. Levy, L. Ballweber, R.P. Sauteraud, J. Strobl, K. Westerberg, R. Gottardo, M. Tewari, and F. Hladik Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions Nucleic Acids Res. 42 2014 7290 7304
93. I. Wang, M.P. Kowalski, A.R. Langley, R. Rodriguez, S. Balasubramanian, S.T. Hsu, and T. Krude Nucleotide contributions to the structural integrity and DNA replication initiation activity of noncoding y RNA Biochemistry 53 2014 5848 5863
94. T. Wang, C. Tian, W. Zhang, K. Luo, P.T. Sarkis, L. Yu, B. Liu, Y. Yu, and X.F. Yu 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G J. Virol. 81 2007 13112 13124
95. S.L. Wolin, C. Belair, M. Boccitto, X. Chen, S. Sim, D.W. Taylor, and H.W. Wang Non-coding Y RNAs as tethers and gates: insights from bacteria RNA Biol. 10 2013 1602 1608
96. S.L. Wolin, and T. Cedervall The La protein Annu. Rev. Biochem. 71 2002 375 403
97. S.L. Wolin, S. Sim, and X. Chen Nuclear noncoding RNA surveillance: is the end in sight? Trends Genet. 28 2012 306 313
98. S.L. Wolin, and J.A. Steitz Genes for two small cytoplasmic Ro RNAs are adjacent and appear to be single-copy in the human genome Cell 32 1983 735 744
99. S.L. Wolin, and J.A. Steitz The Ro small cytoplasmic ribonucleoproteins: identification of the antigenic protein and its binding site on the Ro RNAs Proc. Natl. Acad. Sci. U. S. A. 81 1984 1996 2000
100. E.J. Wurtmann, and S.L. Wolin A role for a bacterial ortholog of the Ro autoantigen in starvation-induced rRNA degradation Proc. Natl. Acad. Sci. U. S. A. 107 2010 4022 4027
101. T. Xiao, Y. Wang, H. Luo, L. Liu, G. Wei, X. Chen, Y. Sun, X. Chen, G. Skogerbo, and R. Chen A differential sequencing-based analysis of the C. elegans noncoding transcriptome RNA 18 2012 626 639
102. D. Xue, H. Shi, J.D. Smith, X. Chen, D.A. Noe, T. Cedervall, D.D. Yang, E. Eynon, D.E. Brash, M. Kashgarian, R.A. Flavell, and S.L. Wolin A lupus-like syndrome develops in mice lacking the Ro 60-kDa protein, a major lupus autoantigen Proc. Natl. Acad. Sci. U. S. A. 100 2003 7503 7508
103. F. Yamazaki, H.H. Kim, P. Lau, C.K. Hwang, P.M. Iuvone, D. Klein, and S.J. Clokie pY RNA1-s2: a highly retina-enriched small RNA that selectively binds to Matrin 3 (Matr3) PLoS ONE 9 2014 e88217
104. A.T. Zhang, A.R. Langley, C.P. Christov, E. Kheir, T. Shafee, T.J. Gardiner, and T. Krude Dynamic interaction of Y RNAs with chromatin and initiation proteins during human DNA replication J. Cell Sci. 124 2011 2058 2069