Biochemistry (Moscow)

, Volume 81, Issue 9, pp 941–950 | Cite as

Nucleolar methyltransferase fibrillarin: Evolution of structure and functions

  • M. Y. Shubina
  • Y. R. Musinova
  • E. V. ShevalEmail author


Fibrillarin is one of the most studied nucleolar proteins. Its main functions are methylation and processing of pre-rRNA. Fibrillarin is a highly conserved protein; however, in the course of evolution from archaea to eukaryotes, it acquired an additional N-terminal glycine and arginine-rich (GAR) domain. In this review, we discuss the evolution of fibrillarin structure and its relation to the functions of the protein in prokaryotes and eukaryotes.


fibrillarin nucleolus methyltransferase GAR domain 



amino acid residue


asymmetrical dimethylarginine




nucleolar dense fibrillar component

GAR domain

glycine and arginine-rich domain






preribosomal RNA


protein arginine methyltransferase


symmetrical dimethylarginine


archaeal small ribonucleoprotein


small nucleolar RNA


small nucleolar ribonucleoprotein


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  1. 1.
    Rodriguez-Corona, U., Sobol, M., Rodriguez-Zapata, L. C., Hozak, P., and Castano, E. (2015) Fibrillarin from Archaea to human, Biol. Cell, 107, 159–174.CrossRefPubMedGoogle Scholar
  2. 2.
    Tollervey, D., Lehtonen, H., Jansen, R., Kern, H., and Hurt, E. C. (1993) Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly, Cell, 72, 443–457.PubMedGoogle Scholar
  3. 3.
    Eichler, D. C., and Craig, N. (1994) Processing of eukaryotic ribosomal RNA, Prog. Nucleic Acid Res. Mol. Biol., 49, 197–239.CrossRefPubMedGoogle Scholar
  4. 4.
    Aris, J. P., and Blobel, G. (1991) cDNA cloning and sequencing of human fibrillarin, a conserved nucleolar protein recognized by autoimmune antisera, Proc. Natl. Acad. Sci. USA, 88, 931–935.CrossRefPubMedGoogle Scholar
  5. 5.
    Turley, S. J., Tan, E. M., and Pollard, K. M. (1993) Molecular cloning and sequence analysis of U3 snoRNAassociated mouse fibrillarin, Biochim. Biophys. Acta, 1216, 119–122.CrossRefPubMedGoogle Scholar
  6. 6.
    Henriquez, R., Blobel, G., and Aris, J. P. (1990) Isolation and sequencing of NOP1. A yeast gene encoding a nucleolar protein homologous to a human autoimmune antigen, J. Biol. Chem., 265, 2209–2215.Google Scholar
  7. 7.
    Lapeyre, B., Mariottini, P., Mathieu, C., Ferrer, P., Amaldi, F., Amalric, F., and Caizergues-Ferrer, M. (1990) Molecular cloning of Xenopus fibrillarin, a conserved U3 small nuclear ribonucleoprotein recognized by antisera from humans with autoimmune disease, Mol. Cell. Biol., 10, 430–434.PubMedGoogle Scholar
  8. 8.
    Schimmang, T., Tollervey, D., Kern, H., Frank, R., and Hurt, E. C. (1989) A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability, EMBO J., 8, 4015–4024.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Amiri, K. A. (1994) Fibrillarin-like proteins occur in the domain Archaea, J. Bacteriol., 176, 2124–2127.Google Scholar
  10. 10.
    Wang, H., Boisver, D., Kim, K. K., Kim, R., and Kim, S. H. (2000) Crystal structure of a fibrillarin homologue from Methanococcus jannaschii, a hyperthermophile, at 16 Å resolution, EMBO J., 19, 317–323.Google Scholar
  11. 11.
    Tycowski, K. T., Smith, C. M., Shu, M. D., and Steitz, J. A. (1996) A small nucleolar RNA requirement for site-specific ribose methylation of rRNA in Xenopus, Proc. Natl. Acad. Sci. USA, 93, 14480–14485.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Kiss-Laszlo, Z., Henry, Y., Bachellerie, J. P., CaizerguesFerrer, M., and Kiss, T. (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs, Cell, 85, 1077–1088.CrossRefPubMedGoogle Scholar
  13. 13.
    Tessarz, P., Santos-Rosa, H., Robson, S. C., Sylvestersen, K. B., Nelson, C. J., Nielsen, M. L., and Kouzarides, T. (2014) Glutamine methylation in histone H2A is an RNApolymerase-I-dedicated modification, Nature, 505, 564568.Google Scholar
  14. 14.
    Loza-Muller, L., Rodriguez-Corona, U., Sobol, M., Rodriguez-Zapata, L. C., Hozak, P., and Castano, E. (2015) Fibrillarin methylates H2A in RNA polymerase I trans-active promoters in Brassica oleracea, Front. Plant Sci., 6, 976.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Vanyushin, B. F., and Ashapkin, V. V. (2009) DNA Methylation in Plants, Nova Science Publishers Inc., N. Y.Google Scholar
  16. 16.
    Cheng, X., and Roberts, R. J. (2001) AdoMet-dependent methylation, DNA methyltransferases and base flipping, Nucleic Acids Res., 29, 3784–3795.CrossRefPubMedGoogle Scholar
  17. 17.
    Barneche, F., Steinmetz, F., and Echeverria, M. (2000) Fibrillarin genes encode both a conserved nucleolar protein and a novel small nucleolar RNA involved in ribosomal RNA methylation in Arabidopsis thaliana, J. Biol. Chem., 275, 27212–27220.PubMedGoogle Scholar
  18. 18.
    Aittaleb, M., Rashid, R., Chen, Q., Palmer, J. R., Daniels, C. J., and Li, H. (2003) Structure and function of archaeal box C/D sRNP core proteins, Nat. Struct. Biol., 10, 256–263.CrossRefPubMedGoogle Scholar
  19. 19.
    Deng, L., Starostina, N. G., Liu, Z.-J., Rose, J. P., Terns, R. M., Terns, M. P., and Wang, B.-C. (2004) Structure determination of fibrillarin from the hyperthermophilic archaeon Pyrococcus furiosus, Biochem. Biophys. Res. Commun., 315, 726–732.CrossRefPubMedGoogle Scholar
  20. 20.
    De Silva, U., Zhou, Z., and Brown, B. A. (2012) Structure of Aeropyrum pernix fibrillarin in complex with natively bound S-adenosyl-L-methionine at 1.7 Å resolution, Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 68, 854859.CrossRefGoogle Scholar
  21. 21.
    Oruganti, S., Zhang, Y., Li, H., Robinson, H., Terns, M. P., Terns, R. M., Yang, W., and Li, H. (2007) Alternative conformations of the archaeal Nop56/58-fibrillarin complex imply flexibility in box C/D RNPs, J. Mol. Biol., 371, 1141–1150.CrossRefPubMedGoogle Scholar
  22. 22.
    Ye, K., Jia, R., Lin, J., Ju, M., Peng, J., Xu, A., and Zhang, L. (2009) Structural organization of box C/D RNA-guided RNA methyltransferase, Proc. Natl. Acad. Sci. USA, 106, 13808–13813.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Lin, J., Lai, S., Jia, R., Xu, A., Zhang, L., Lu, J., and Ye, K. (2011) Structural basis for site-specific ribose methylation by box C/D RNA protein complexes, Nature, 469, 559–563.CrossRefPubMedGoogle Scholar
  24. 24.
    Lapinaite, A., Simon, B., Skjaerven, L., Rakwalska-Bange, M., Gabel, F., and Carlomagno, T. (2013) The structure of the box C/D enzyme reveals regulation of RNA methylation, Nature, 502, 519–523.CrossRefPubMedGoogle Scholar
  25. 25.
    Ofengand, J. (2002) Ribosomal RNA pseudouridines and pseudouridine synthases, FEBS Lett., 514, 17–25.CrossRefPubMedGoogle Scholar
  26. 26.
    King, T. H., Liu, B., McCully, R. R., and Fournier, M. J. (2003) Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center, Mol. Cell, 11, 425–435.CrossRefPubMedGoogle Scholar
  27. 27.
    Omer, A. D., Lowe, T. M., Russell, A. G., Ebhardt, H., Eddy, S. R., and Dennis, P. P. (2000) Homologs of small nucleolar RNAs in Archaea, Science, 288, 517–522.CrossRefPubMedGoogle Scholar
  28. 28.
    Dennis, P. P., and Omer, A. (2005) Small non-coding RNAs in Archaea, Curr. Opin. Microbiol., 8, 685–694.CrossRefPubMedGoogle Scholar
  29. 29.
    Clouet d’Orval, B., Bortolin, M. L., Gaspin, C., and Bachellerie, J. P. (2001) Box C/D RNA guides for the ribose methylation of archaeal tRNAs. The tRNATrp intron guides the formation of two ribose-methylated nucleosides in the mature tRNATrp, Nucleic Acids Res., 29, 4518–4529.CrossRefPubMedGoogle Scholar
  30. 30.
    Kiss-Laszla, Z., Henry, Y., and Kiss, T. (1998) Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA, EMBO J., 17, 797–807.CrossRefGoogle Scholar
  31. 31.
    Dunbar, D. A., Wormsley, S., Lowe, T. M., and Baserga, S. J. (2000) Fibrillarin-associated box C/D small nucleolar RNAs in Trypanosoma brucei. Sequence conservation and implications for 2’-O-ribose methylation of rRNA, J. Biol. Chem., 275, 14767–14776.CrossRefPubMedGoogle Scholar
  32. 32.
    Nolivos, S., Carpousis, A. J., and Clouet-d’Orval, B. (2005) The K-loop, a general feature of the Pyrococcus C/D guide RNAs, is an RNA structural motif related to the K-turn, Nucleic Acids Res., 33, 6507–6514.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Samarsky, D. A., Fournier, M. J., Singer, R. H., and Bertrand, E. (1998) The snoRNA box C/D motif directs nucleolar targeting and also couples snoRNA synthesis and localization, EMBO J., 17, 3747–3757.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Gautier, T., Berges, T., Tollervey, D., and Hurt, E. (1997) Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis, Mol. Cell. Biol., 17, 7088–7098.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Filipowicz, W., and Pogacic, V. (2002) Biogenesis of small nucleolar ribonucleoproteins, Curr. Opin. Cell Biol., 14, 319–327.CrossRefPubMedGoogle Scholar
  36. 36.
    Kiss, T. (2004) Biogenesis of small nuclear RNPs, J. Cell Sci., 117, 5949–5951.CrossRefPubMedGoogle Scholar
  37. 37.
    Tollervey, D. (1996) Small nucleolar RNAs guide ribosomal RNA methylation, Science, 273, 1056–1057.CrossRefPubMedGoogle Scholar
  38. 38.
    Hirose, T., Shu, M.-D., and Steitz, J. A. (2003) Splicingdependent and -independent modes of assembly for intronencoded box C/D snoRNPs in mammalian cells, Mol. Cell, 12, 113–123.CrossRefPubMedGoogle Scholar
  39. 39.
    Morlando, M., Ballarino, M., Greco, P., Caffarelli, E., Dichtl, B., and Bozzoni, I. (2004) Coupling between snoRNP assembly and 3’ processing controls box C/D snoRNA biosynthesis in yeast, EMBO J., 23, 2392–2401.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Tollervey, D., and Kiss, T. (1997) Function and synthesis of small nucleolar RNAs, Curr. Opin. Cell Biol., 9, 337–342.CrossRefPubMedGoogle Scholar
  41. 41.
    Omer, A. D., Ziesche, S., Decatur, W. A., Fournier, M. J., and Dennis, P. P. (2003) RNA-modifying machines in Archaea, Mol. Microbiol., 48, 617–629.CrossRefPubMedGoogle Scholar
  42. 42.
    Omer, A. D., Ziesche, S., Ebhardt, H., and Dennis, P. P. (2002) In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex, Proc. Natl. Acad. Sci. USA, 99, 5289–5294.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Klein, D. J., Schmeing, T. M., Moore, P. B., and Steitz, T. A. (2001) The kink-turn: a new RNA secondary structure motif, EMBO J., 20, 4214–4221.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Charron, C., Manival, X., Clery, A., Senty-Segault, V., Charpentier, B., Marmier-Gourrier, N., Branlant, C., and Aubry, A. (2004) The archaeal sRNA binding protein L7Ae has a 3D structure very similar to that of its eukaryal counterpart while having a broader RNA-binding specificity, J. Mol. Biol., 342, 757–773.CrossRefPubMedGoogle Scholar
  45. 45.
    Rashid, R., Aittaleb, M., Chen, Q., Spiegel, K., Demeler, B., and Li, H. (2003) Functional requirement for symmetric assembly of archaeal box C/D small ribonucleoprotein particles, J. Mol. Biol., 333, 295–306.CrossRefPubMedGoogle Scholar
  46. 46.
    Zhang, X., Champion, E. A., Tran, E. J., Brown, B. A., Baserga, S. J., and Maxwell, E. S. (2006) The coiled-coil domain of the Nop56/58 core protein is dispensable for sRNP assembly but is critical for archaeal box C/D sRNPguided nucleotide methylation, RNA, 12, 1092–1103.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Cahill, N. M., Friend, K., Speckmann, W., Li, Z.-H., Terns, R. M., Terns, M. P., and Steitz, J. A. (2002) Sitespecific cross-linking analyses reveal an asymmetric protein distribution for a box C/D snoRNP, EMBO J., 21, 38163828.CrossRefGoogle Scholar
  48. 48.
    Maxwell, E. S., and Fournier, M. J. (1995) The small nucleolar RNAs, Annu. Rev. Biochem., 64, 897–934.CrossRefPubMedGoogle Scholar
  49. 49.
    Tyc, K., and Steitz, J. A. (1989) U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus, EMBO J., 8, 3113–3119.PubMedGoogle Scholar
  50. 50.
    Craig, N., Kass, S., and Sollner-Webb, B. (1987) Nucleotide sequence determining the first cleavage site in the processing of mouse precursor rRNA, Proc. Natl. Acad. Sci. USA, 84, 629–633.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Kass, S., Tyc, K., Steitz, J. A., and Sollner-Webb, B. (1990) The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing, Cell, 60, 897908.CrossRefGoogle Scholar
  52. 52.
    Yoshikawa, H., Komatsu, W., Hayano, T., Miura, Y., Homma, K., Izumikawa, K., Ishikawa, H., Miyazawa, N., Tachikawa, H., Yamauchi, Y., Isobe, T., and Takahashi, N. (2011) Splicing factor 2-associated protein p32 participates in ribosome biogenesis by regulating the binding of Nop52 and fibrillarin to preribosome particles, Mol. Cell. Proteom., 10, M110.006148.CrossRefGoogle Scholar
  53. 53.
    Lischwe, M. A., Ochs, R. L., Reddy, R., Cook, R. G., Yeoman, L. C., Tan, E. M., Reichlin, M., and Busch, H. (1985) Purification and partial characterization of a nucleolar scleroderma antigen (Mr = 34,000; pI, 85) rich in NG, NGdimethylarginine, J. Biol. Chem., 260, 14304–14310.Google Scholar
  54. 54.
    Russell, A. G., Watanabe, Y., Charette, J. M., and Gray, M. W. (2005) Unusual features of fibrillarin cDNA and gene structure in Euglena gracilis: evolutionary conservation of core proteins and structural predictions for methylationguide box C/D snoRNPs throughout the domain Eucarya, Nucleic Acids Res., 33, 2781–2791.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    David, E., McNeil, J. B., Basile, V., and Pearlman, R. E. (1997) An unusual fibrillarin gene and protein: structure and functional implications, Mol. Biol. Cell, 8, 10511061.CrossRefGoogle Scholar
  56. 56.
    Narcisi, E. M., Glover, C. V., and Fechheimer, M. (1998) Fibrillarin, a conserved pre-ribosomal RNA processing protein of Giardia, J. Eukaryot. Microbiol., 45, 105111.Google Scholar
  57. 57.
    Sobol, M., Yildirim, S., Philimonenko, V. V., Marasek, P., Castano, E., and Hozak, P. (2013) UBF complexes with phosphatidylinositol 4,5-bisphosphate in nucleolar organizer regions regardless of ongoing RNA polymerase I activity, Nucleus, 4, 478–486.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Ochs, R. L., Lischwe, M. A., Spohn, W. H., and Busch, H. (1985) Fibrillarin: a new protein of the nucleolus identified by autoimmune sera, Biol. Cell, 54, 123–133.CrossRefPubMedGoogle Scholar
  59. 59.
    De Carcer, G., and Medina, F. J. (1999) Simultaneous localization of transcription and early processing markers allows dissection of functional domains in the plant cell nucleolus, J. Struct. Biol., 128, 139–151.CrossRefPubMedGoogle Scholar
  60. 60.
    Snaar, S., Wiesmeijer, K., Jochemsen, A. G., Tanke, H. J., and Dirks, R. W. (2000) Mutational analysis of fibrillarin and its mobility in living human cells, J. Cell Biol., 151, 653–662.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Zheng, L., Yao, J., Gao, F., Chen, L., Zhang, C., Lian, L., Xie, L., Wu, Z., and Xie, L. (2016) The subcellular localization and functional analysis of Fibrillarin2, a nucleolar protein in Nicotiana benthamiana, Biomed. Res. Int., 2831287.Google Scholar
  62. 62.
    Creancier, L., Prats, H., Zanibellato, C., Amalric, F., and Bugler, B. (1993) Determination of the functional domains involved in nucleolar targeting of nucleolin, Mol. Biol. Cell, 4, 1239–1250.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Schmidt-Zachmann, M. S., and Nigg, E. A. (1993) Protein localization to the nucleolus: a search for targeting domains in nucleolin, J. Cell Sci., 105, 3799–3806.Google Scholar
  64. 64.
    Pih, K. T., Yi, M. J., Liang, Y. S., Shin, B. J., Cho, M. J., Hwang, I., and Son, D. (2000) Molecular cloning and targeting of a fibrillarin homolog from Arabidopsis, Plant Physiol., 123, 51–58.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Musinova, Y. R., Lisitsyna, O. M., Golyshev, S. A., Tuzhikov, A. I., Polyakov, V. Y., and Sheval, E. V. (2011) Nucleolar localization/retention signal is responsible for transient accumulation of histone H2B in the nucleolus through electrostatic interactions, Biochim. Biophys. Acta, 1813, 27–38.CrossRefPubMedGoogle Scholar
  66. 66.
    Savada, R. P., and Bonham-Smith, P. C. (2013) Charge versus sequence for nuclear/nucleolar localization of plant ribosomal proteins, Plant Mol. Biol., 81, 477–493.CrossRefPubMedGoogle Scholar
  67. 67.
    Musinova, Y. R., Kananykhina, E. Y., Potashnikova, D. M., Lisitsyna, O. M., and Sheval, E. V. (2015) A chargedependent mechanism is responsible for the dynamic accumulation of proteins inside nucleoli, Biochim. Biophys. Acta, 1853, 101–110.CrossRefPubMedGoogle Scholar
  68. 68.
    Martin, R. M., Ter-Avetisyan, G., Herce, H. D., Ludwig, A. K., Lattig-Tunnemann, G., and Cardoso, M. C. (2015) Principles of protein targeting to the nucleolus, Nucleus, 6, 314–325.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Levitskii, S. A., Mukhar’ iamova, K. S., Veiko, V. P., and Zatsepina, O. V. (2004) Identification of signal sequences determining the specific nucleolar localization of fibrillarin in HeLa cells, Mol. Biol. (Moscow), 38, 483–492.Google Scholar
  70. 70.
    Bedford, M. T., and Richard, S. (2005) Arginine methylation an emerging regulator of protein function, Mol. Cell, 18, 263–272.CrossRefPubMedGoogle Scholar
  71. 71.
    Li, C., Ai, L. S., Lin, C. H., Hsieh, M., Li, Y. C., and Li, S. Y. (1998) Protein N-arginine methylation in adenosine dialdehyde-treated lymphoblastoid cells, Arch. Biochem. Biophys., 351, 53–59.CrossRefPubMedGoogle Scholar
  72. 72.
    Lin, C. H., Hsieh, M., Li, Y. C., Li, S. Y., Pearson, D. L., Pollard, K. M., and Li, C. (2000) Protein N-arginine methylation in subcellular fractions of lymphoblastoid cells, J. Biochem., 128, 493–498.CrossRefPubMedGoogle Scholar
  73. 73.
    Najbauer, J., Johnson, B. A., Young, A. L., and Aswad, D. W. (1993) Peptides with sequences similar to glycine, arginine-rich motifs in proteins interacting with RNA are efficiently recognized by methyltransferase(s) modifying arginine in numerous proteins, J. Biol. Chem., 268, 1050110509.Google Scholar
  74. 74.
    Baldwin, G. S., and Carnegie, P. R. (1971) Specific enzymic methylation of an arginine in the experimental allergic encephalomyelitis protein from human myelin, Science, 171, 579–581.CrossRefPubMedGoogle Scholar
  75. 75.
    Brahms, H., Raymackers, J., Union, A., De Keyser, F., Meheus, L., and Luhrmann, R. (2000) The C-terminal RG dipeptide repeats of the spliceosomal Sm proteins D1 and D3 contain symmetrical dimethylarginines, which form a major B-cell epitope for anti-Sm autoantibodies, J. Biol. Chem., 275, 17122–17129.Google Scholar
  76. 76.
    Brahms, H., Meheus, L., De Brabandere, V., Fischer, U., and Luhrmann, R. (2001) Symmetrical dimethylation of arginine residues in spliceosomal Sm protein B/B’ and the Sm-like protein LSm4, and their interaction with the SMN protein, RNA, 7, 1531–1542.PubMedGoogle Scholar
  77. 77.
    Liu, Q., and Dreyfuss, G. (1995) In vivo and in vitro arginine methylation of RNA-binding proteins, Mol. Cell. Biol., 15, 2800–2808.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Ai, L. S., Lin, C. H., Hsieh, M., and Li, C. (1999) Arginine methylation of a glycine and arginine rich peptide derived from sequences of human FMRP and fibrillarin, Proc. Natl. Sci. Counc. Repub. China B, 23, 175–180.PubMedGoogle Scholar
  79. 79.
    Yagoub, D., Hart-Smith, G., Moecking, J., Erce, M. A., and Wilkins, M. R. (2015) Yeast proteins Gar1p, Nop1p, Npl3p, Nsr1p, and Rps2p are natively methylated and are substrates of the arginine methyltransferase Hmt1p, Proteomics, 15, 3209–3218.PubMedGoogle Scholar
  80. 80.
    Tang, J., Gary, J. D., Clarke, S., and Herschman, H. R. (1998) PRMT3, a type I protein arginine N-methyltransferase that differs from PRMT1 in its oligomerization, subcellular localization, substrate specificity, and regulation, J. Biol. Chem., 273, 16935–16945.CrossRefPubMedGoogle Scholar
  81. 81.
    Zurita-Lopez, C. I., Sandberg, T., Kelly, R., and Clarke, S. G. (2012) Human protein arginine methyltransferase 7 (PRMT7) is a type III enzyme forming NGmonomethylated arginine residues, J. Biol. Chem., 287, 7859–7870.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Lapeyre, B., Bourbon, H., and Amalric, F. (1987) Nucleolin, the major nucleolar protein of growing eukaryotic cells: an unusual protein structure revealed by the nucleotide sequence, Proc. Natl. Acad. Sci. USA, 84, 14721476.Google Scholar
  83. 83.
    Girard, J. P., Lehtonen, H., Caizergues-Ferrer, M., Amalric, F., Tollervey, D., and Lapeyre, B. (1992) GAR1 is an essential small nucleolar RNP protein required for prerRNA processing in yeast, EMBO J., 11, 673–682.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Lee, W. C., Xue, Z. X., and Melese, T. (1991) The NSR1 gene encodes a protein that specifically binds nuclear localization sequences and has two RNA recognition motifs, J. Cell. Biol., 113, 1–12.CrossRefPubMedGoogle Scholar
  85. 85.
    Jong, A. Y., Clark, M. W., Gilbert, M., Oehm, A., and Campbell, J. L. (1987) Saccharomyces cerevisiae SSB1 protein and its relationship to nucleolar RNA-binding proteins, Mol. Cell. Biol., 7, 2947–2955.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Russell, I. D., and Tollervey, D. (1992) NOP3 is an essential yeast protein which is required for pre-rRNA processing, J. Cell Biol., 119, 737–747.CrossRefPubMedGoogle Scholar
  87. 87.
    Ghisolfi, L., Joseph, G., Amalric, F., and Erard, M. (1992) The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties, J. Biol. Chem., 267, 2955–2959.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • M. Y. Shubina
    • 1
  • Y. R. Musinova
    • 2
  • E. V. Sheval
    • 2
    Email author
  1. 1.Lomonosov Moscow State UniversityFaculty of Bioengineering and BioinformaticsMoscowRussia
  2. 2.Lomonosov Moscow State UniversityBelozersky Institute of Physico-Chemical BiologyMoscowRussia

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