Table of Contents
Molecular Biology International
Volume 2011, Article ID 163827, 10 pages
http://dx.doi.org/10.4061/2011/163827
Review Article

The Role of Protein Arginine Methylation in mRNP Dynamics

Department of Biological Sciences, State University of New York at Buffalo, 109 Cooke Hall, Buffalo, NY 14260, USA

Received 14 January 2011; Accepted 12 February 2011

Academic Editor: Robert B. Denman

Copyright © 2011 Michael C. Yu. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. Maniatis and R. Reed, “An extensive network of coupling among gene expression machines,” Nature, vol. 416, no. 6880, pp. 499–506, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. M. J. Moore and N. J. Proudfoot, “Pre-mRNA processing reaches back to transcription and ahead to translation,” Cell, vol. 136, no. 4, pp. 688–700, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Buratowski, “Progression through the RNA polymerase II CTD Cycle,” Molecular Cell, vol. 36, no. 4, pp. 541–546, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Pandit, D. Wang, and X. D. Fu, “Functional integration of transcriptional and RNA processing machineries,” Current Opinion in Cell Biology, vol. 20, no. 3, pp. 260–265, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. S. P. Han, Y. H. Tang, and R. Smith, “Functional diversity of the hnRNPs: past, present and perspectives,” Biochemical Journal, vol. 430, no. 3, pp. 379–392, 2010. View at Publisher · View at Google Scholar
  6. X. Y. Zhong, P. Wang, J. Han, M. G. Rosenfeld, and X. D. Fu, “SR proteins in vertical integration of gene expression from transcription to RNA processing to translation,” Molecular Cell, vol. 35, no. 1, pp. 1–10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. Y.-F. Chang, J. S. Imam, and M. F. Wilkinson, “The Nonsense-mediated decay RNA surveillance pathway,” Annual Review of Biochemistry, vol. 76, pp. 51–74, 2007. View at Publisher · View at Google Scholar
  8. L. E. Maquat, “Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics,” Nature Reviews Molecular Cell Biology, vol. 5, no. 2, pp. 89–99, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. M. T. Bedford and S. G. Clarke, “Protein arginine methylation in mammals: who, what, and why,” Molecular Cell, vol. 33, no. 1, pp. 1–13, 2009. View at Publisher · View at Google Scholar
  10. K. S. Godin and G. Varani, “How arginine-rich domains coordinate mRNA maturation events,” RNA Biology, vol. 4, no. 2, pp. 69–75, 2007. View at Google Scholar · View at Scopus
  11. J. D. Gary and S. Clarke, “RNA and protein interactions modulated by protein arginine methylation,” Progress in Nucleic Acid Research and Molecular Biology, vol. 61, pp. 65–131, 1998. View at Google Scholar · View at Scopus
  12. J. Lee and M. T. Bedford, “PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays,” EMBO Reports, vol. 3, no. 3, pp. 268–273, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. W. L. Wooderchak, T. Zang, Z. S. Zhou, M. Acuña, S. M. Tahara, and J. M. Hevel, “Substrate profiling of PRMT1 reveals amino acid sequences that extend beyond the "RGG" paradigm,” Biochemistry, vol. 47, no. 36, pp. 9456–9466, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Singh and J. Valcárcel, “Building specificity with nonspecific RNA-binding proteins,” Nature Structural and Molecular Biology, vol. 12, no. 8, pp. 645–653, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. F. M. Boisvert, J. Cote, M. C. Boulanger, and S. Richard, “A proteomic analysis of arginine-methylated protein complexes,” Molecular & Cellular Proteomics, vol. 2, no. 12, pp. 1319–1330, 2003. View at Google Scholar · View at Scopus
  16. S. E. Ong, G. Mittler, and M. Mann, “Identifying and quantifying in vivo methylation sites by heavy methyl SILAC,” Nat Methods, vol. 1, no. 2, pp. 119–126, 2004. View at Google Scholar · View at Scopus
  17. M. S. Jurica and M. J. Moore, “Pre-mRNA splicing: awash in a sea of proteins,” Molecular Cell, vol. 12, no. 1, pp. 5–14, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. J. P. Staley and J. L. Woolford, “Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines,” Current Opinion in Cell Biology, vol. 21, no. 1, pp. 109–118, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. M. C. Wahl, C. L. Will, and R. Luhrmann, “The spliceosome: design principles of a dynamic RNP machine,” Cell, vol. 136, no. 4, pp. 701–718, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Yong, L. Wan, and G. Dreyfuss, “Why do cells need an assembly machine for RNA-protein complexes?” Trends in Cell Biology, vol. 14, no. 5, pp. 226–232, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Staněk and K. M. Neugebauer, “The Cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze,” Chromosoma, vol. 115, no. 5, pp. 343–354, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Brahms, J. Raymackers, A. Union, F. De Keyser, L. Meheus, and R. Luhrmann, “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,” Journal of Biological Chemistry, vol. 275, no. 22, pp. 17122–17129, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Chari, E. Paknia, and U. Fischer, “The role of RNP biogenesis in spinal muscular atrophy,” Current Opinion in Cell Biology, vol. 21, no. 3, pp. 387–393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Paushkin, A. K. Gubitz, S. Massenet, and G. Dreyfuss, “The SMN complex, an assemblyosome of ribonucleoproteins,” Current Opinion in Cell Biology, vol. 14, no. 3, pp. 305–312, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. W. J. Friesen, S. Massenet, S. Paushkin, A. Wyce, and G. Dreyfuss, “SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets,” Molecular Cell, vol. 7, no. 5, pp. 1111–1117, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Brahms, L. Meheus, V. De Brabandere, U. Fischer, and R. Luhrmann, “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, vol. 7, no. 11, pp. 1531–1542, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Selenko, R. Sprangers, G. Stier, D. Bühler, U. Fischer, and M. Sattler, “SMN tudor domain structure and its interaction with the Sm proteins,” Nature Structural Biology, vol. 8, no. 1, pp. 27–31, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Cote and S. Richard, “Tudor domains bind symmetrical dimethylated arginines,” Journal of Biological Chemistry, vol. 280, no. 31, pp. 28476–28483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Kim, J. Daniel, A. Espejo et al., “Tudor, MBT and chromo domains gauge the degree of lysine methylation,” EMBO Reports, vol. 7, no. 4, pp. 397–403, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. F. M. Boisvert, J. Cote, M. C. Boulanger et al., “Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing,” Journal of Cell Biology, vol. 159, no. 6, pp. 957–969, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. W. J. Friesen, S. Paushkin, A. Wyce et al., “The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins,” Molecular and Cellular Biology, vol. 21, no. 24, pp. 8289–8300, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Meister, C. Eggert, D. Bühler, H. Brahms, C. Kambach, and U. Fischer, “Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln,” Current Biology, vol. 11, no. 24, pp. 1990–1994, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. W. T. Pu, G. B. Krapivinsky, L. Krapivinsky, and D. E. Clapham, “pICln inhibits snRNP biogenesis by binding core spliceosomal proteins,” Molecular and Cellular Biology, vol. 19, no. 6, pp. 4113–4120, 1999. View at Google Scholar · View at Scopus
  34. G. Meister and U. Fischer, “Assisted RNP assembly: SMN and PRMT5 complexes cooperate in the formation of spliceosomal UsnRNPs,” EMBO Journal, vol. 21, no. 21, pp. 5853–5863, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. X. Deng, L. Gu, C. Liu et al., “Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 44, pp. 19114–19119, 2010. View at Publisher · View at Google Scholar
  36. S. E. Sanchez, E. Petrillo, E. J. Beckwith et al., “A methyl transferase links the circadian clock to the regulation of alternative splicing,” Nature, vol. 468, no. 7320, pp. 112–116, 2010. View at Publisher · View at Google Scholar
  37. G. B. Gonsalvez, L. Tian, J. K. Ospina, F. M. Boisvert, A. I. Lamond, and A. G. Matera, “Two distinct arginine methyltransferases are required for biogenesis of Sm-class ribonucleoproteins,” Journal of Cell Biology, vol. 178, no. 5, pp. 733–740, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. G. B. Gonsalvez, K. Praveen, A. J. Hicks, L. Tian, and A. G. Matera, “Sm protein methylation is dispensable for snRNP assembly in Drosophila melanogaster,” RNA, vol. 14, no. 5, pp. 878–887, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. G. B. Gonsalvez, T. K. Rajendra, L. Tian, and A. G. Matera, “The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance,” Current Biology, vol. 16, no. 11, pp. 1077–1089, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. T. B. Miranda, P. Khusial, J. R. Cook et al., “Spliceosome Sm proteins D1, D3, and B/B′ are asymmetrically dimethylated at arginine residues in the nucleus,” Biochemical and Biophysical Research Communications, vol. 323, no. 2, pp. 382–387, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. M. C. Boulanger, T. B. Miranda, S. Clarke et al., “Characterization of the Drosophila protein arginine methyltransferases DART1 and DART4,” Biochemical Journal, vol. 379, no. 2, pp. 283–289, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Cheng, J. Cote, S. Shaaban, and M. T. Bedford, “The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing,” Molecular Cell, vol. 25, no. 1, pp. 71–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. A. L. Beyer, M. E. Christensen, B. W. Walker, and W. M. LeStourgeon, “Identification and characterization of the packaging proteins of core 40S hnRNP particles,” Cell, vol. 11, no. 1, pp. 127–138, 1977. View at Google Scholar · View at Scopus
  44. H. E. Wilk, H. Werr, D. Friedrich, H. H. Kiltz, and K. P. Schäfer, “The core proteins of 35S hnRNP complexes. Characterization of nine different species,” European Journal of Biochemistry, vol. 146, no. 1, pp. 71–81, 1985. View at Google Scholar · View at Scopus
  45. Q. Liu and G. Dreyfuss, “In vivo and in vitro arginine methylation of RNA-binding proteins,” Molecular and Cellular Biology, vol. 15, no. 5, pp. 2800–2808, 1995. View at Google Scholar · View at Scopus
  46. R. C. Nichols, X. W. Wang, J. Tang et al., “The RGG domain in hnRNP A2 affects subcellular localization,” Experimental Cell Research, vol. 256, no. 2, pp. 522–532, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. D. O. Passos, A. J. C. Quaresma, and J. Kobarg, “The methylation of the C-terminal region of hnRNPQ (NSAP1) is important for its nuclear localization,” Biochemical and Biophysical Research Communications, vol. 346, no. 2, pp. 517–525, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Wada, K. Inoue, and M. Hagiwara, “Identification of methylated proteins by protein arginine N-methyltransferase 1, PRMT1, with a new expression cloning strategy,” Biochimica et Biophysica Acta, vol. 1591, no. 1-3, pp. 1–10, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Kzhyshkowska, H. Schütt, M. Liss et al., “Heterogeneous nuclear ribonucleoprotein E1B-AP5 is methylated in its Arg-Gly-Gly (RGG) box and interacts with human arginine methyltransferase HRMT1L1,” Biochemical Journal, vol. 358, no. 2, pp. 305–314, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Herrmann, M. Bossert, A. Schwander, E. Akgün, and F. O. Fackelmayer, “Arginine methylation of scaffold attachment factor A by heterogeneous nuclear ribonucleoprotein particle-associated PRMT1,” Journal of Biological Chemistry, vol. 279, no. 47, pp. 48774–48779, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Kukalev, Y. Nord, C. Palmberg, T. Bergman, and P. Percipalle, “Actin and hnRNP U cooperate for productive transcription by RNA polymerase II,” Nature Structural and Molecular Biology, vol. 12, no. 3, pp. 238–244, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Yugami, Y. Kabe, Y. Yamaguchi, T. Wada, and H. Handa, “hnRNP-U enhances the expression of specific genes by stabilizing mRNA,” FEBS Letters, vol. 581, no. 1, pp. 1–7, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Maggipinto, C. Rabiner, G. J. Kidd, A. J. Hawkins, R. Smith, and E. Barbarese, “Increased expression of the MBP mRNA binding protein HnRNP A2 during oligodendrocyte differentiation,” Journal of Neuroscience Research, vol. 75, no. 5, pp. 614–623, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Cote, F. M. Boisvert, M. C. Boulanger, M. T. Bedford, and S. Richard, “Sam68 RNA binding protein is an in vivo substrate for protein arginine N-methyltransferase 1,” Molecular Biology of the Cell, vol. 14, no. 1, pp. 274–287, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. D. M. Green, K. A. Marfatia, E. B. Crafton, X. Zhang, X. Cheng, and A. H. Corbett, “Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p,” Journal of Biological Chemistry, vol. 277, no. 10, pp. 7752–7760, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. E. C. Shen, M. F. Henry, V. H. Weiss, S. R. Valentini, P. A. Silver, and M. S. Lee, “Arginine methylation facilitates the nuclear export of hnRNP proteins,” Genes and Development, vol. 12, no. 5, pp. 679–691, 1998. View at Google Scholar · View at Scopus
  57. W. Gilbert, C. W. Siebel, and C. Guthrie, “Phosphorylation by Sky1p promotes Npl3p shuttling and mRNA dissociation,” RNA, vol. 7, no. 2, pp. 302–313, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. M. S. Lee, M. Henry, and P. A. Silver, “A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export,” Genes and Development, vol. 10, no. 10, pp. 1233–1246, 1996. View at Google Scholar · View at Scopus
  59. S. M. Wilson, K. V. Datar, M. R. Paddy, J. R. Swedlow, and M. S. Swanson, “Characterization of nuclear polyadenylated RNA-binding proteins in Saccharomyces cerevisiae,” Journal of Cell Biology, vol. 127, no. 5, pp. 1173–1184, 1994. View at Publisher · View at Google Scholar · View at Scopus
  60. M. F. Henry and P. A. Silver, “A novel methyltransferase (Hmt1p) modifies poly(A)-RNA-binding proteins,” Molecular and Cellular Biology, vol. 16, no. 7, pp. 3668–3678, 1996. View at Google Scholar · View at Scopus
  61. M. M. Kessler, M. F. Henry, E. Shen et al., “Hrp1, a sequence-specific RNA-binding protein that shuttles between the nucleus and the cytoplasm, is required for mRNA 3'-end formation in yeast,” Genes and Development, vol. 11, no. 19, pp. 2545–2556, 1997. View at Google Scholar · View at Scopus
  62. J. T. Anderson, S. M. Wilson, K. V. Datar, and M. S. Swanson, “NAB2: a yeast nuclear polyadenylated RNA-binding protein essential for cell viability,” Molecular and Cellular Biology, vol. 13, no. 5, pp. 2730–2741, 1993. View at Google Scholar · View at Scopus
  63. A. E. McBride, J. T. Cook, E. A. Stemmler, K. L. Rutledge, K. A. McGrath, and J. A. Rubens, “Arginine methylation of yeast mRNA-binding protein Npl3 directly affects its function, nuclear export, and intranuclear protein interactions,” Journal of Biological Chemistry, vol. 280, no. 35, pp. 30888–30898, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Xu and M. F. Henry, “Nuclear export of hnRNP Hrp1p and nuclear export of hnRNP Npl3p are linked and influenced by the methylation state of Npl3p,” Molecular and Cellular Biology, vol. 24, no. 24, pp. 10742–10756, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Y. Yun and X. D. Fu, “Conserved SR protein kinase functions in nuclear import and its action is counteracted by arginine methylation in Saccharomyces cerevisiae,” Journal of Cell Biology, vol. 150, no. 4, pp. 707–717, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. R. Rajpurohit, S. O. Lee, J. O. Park, W. K. Paik, and S. Kim, “Enzymatic methylation of recombinant heterogeneous nuclear RNP protein A1. Dual substrate specificity for S-adenosylmethionine:histone-arginine N- methyltransferase,” Journal of Biological Chemistry, vol. 269, no. 2, pp. 1075–1082, 1994. View at Google Scholar · View at Scopus
  67. J. Rho, S. Choi, C. R. Jung, and D. S. Im, “Arginine methylation of Sam68 and SLM proteins negatively regulates their poly(U) RNA binding activity,” Archives of Biochemistry and Biophysics, vol. 466, no. 1, pp. 49–57, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. M. L. Hung, G. M. Hautbergue, A. P. L. Snijders, M. J. Dickman, and S. A. Wilson, “Arginine methylation of REF/ALY promotes efficient handover of mRNA to TAP/NXF1,” Nucleic Acids Research, vol. 38, no. 10, pp. 3351–3361, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Ostareck-Lederer, D. H. Ostareck, K. P. Rucknagel et al., “Asymmetric arginine dimethylation of heterogeneous nuclear ribonucleoprotein K by protein-arginine methyltransferase 1 inhibits its interaction with c-Src,” Journal of Biological Chemistry, vol. 281, no. 16, pp. 11115–11125, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. B. Raman, C. Guarnaccia, K. Nadassy et al., “N-arginine dimethylation modulates the interaction between a gly/arg-rich peptide from human nucleolin and nucleic acids,” Nucleic Acids Research, vol. 29, no. 16, pp. 3377–3384, 2001. View at Google Scholar · View at Scopus
  71. S. R. Valentini, V. H. Weiss, and P. A. Silver, “Arginine methylation and binding of Hrp1p to the efficiency element for mRNA 3'-end formation,” RNA, vol. 5, no. 2, pp. 272–280, 1999. View at Publisher · View at Google Scholar · View at Scopus
  72. J. R. Sanford, J. Ellis, and J. F. Càceres, “Multiple roles of arginine/serine-rich splicing factors in RNA processing,” Biochemical Society Transactions, vol. 33, no. 3, pp. 443–446, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. G. C. Bressan, E. C. Moraes, A. O. Manfiolli et al., “Arginine methylation analysis of the splicing-associated SR protein SFRS9/SRp30C,” Cellular and Molecular Biology Letters, vol. 14, no. 4, pp. 657–669, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. R. Sinha, E. Allemand, Z. Zhang, R. Karni, M. P. Myers, and A. R. Krainer, “Arginine methylation controls the subcellular localization and functions of the oncoprotein splicing factor SF2/ASF,” Molecular and Cellular Biology, vol. 30, no. 11, pp. 2762–2774, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. E. Park, J. Han, H. S. Gi et al., “Cooperative actions of Tra2α with 9G8 and SRp30c in the RNA splicing of the gonadotropin-releasing hormone gene transcript,” Journal of Biological Chemistry, vol. 281, no. 1, pp. 401–409, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. P. Cloutier, J. Toutant, L. Shkreta, S. Goekjian, T. Revil, and B. Chabot, “Antagonistic effects of the SRp30c protein and cryptic 5′ splice sites on the alternative splicing of the apoptotic regulator Bcl-x,” Journal of Biological Chemistry, vol. 283, no. 31, pp. 21315–21324, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. Z. Zhang and A. R. Krainer, “Involvement of SR proteins in mRNA surveillance,” Molecular Cell, vol. 16, no. 4, pp. 597–607, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. Huang, T. A. Yario, and J. A. Steitz, “A molecular link between SR protein dephosphorylation and mRNA export,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 26, pp. 9666–9670, 2004. View at Publisher · View at Google Scholar · View at Scopus
  79. J. R. Sanford, N. K. Gray, K. Beckmann, and J. F. Cáceres, “A novel role for shuttling SR proteins in mRNA translation,” Genes and Development, vol. 18, no. 7, pp. 755–768, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Koizumi, Y. Okamoto, H. Onogi, A. Mayeda, A. R. Krainer, and M. Hagiwara, “The subcellular localization of SF2/ASF is regulated by direct interaction with SR protein kinases (SRPKs),” Journal of Biological Chemistry, vol. 274, no. 16, pp. 11125–11131, 1999. View at Publisher · View at Google Scholar · View at Scopus
  81. L. Cartegni, S. L. Chew, and A. R. Krainer, “Listening to silence and understanding nonsense: exonic mutations that affect splicing,” Nature Reviews Genetics, vol. 3, no. 4, pp. 285–298, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Reed, “Coupling transcription, splicing and mRNA export,” Current Opinion in Cell Biology, vol. 15, no. 3, pp. 326–331, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. A. C. Goldstrohm, T. R. Albrecht, C. Sune, M. T. Bedford, and M. A. Garcia-Blanco, “The transcription elongation factor CA150 interacts with RNA polymerase II and the pre-mRNA splicing factor SF1,” Molecular and Cellular Biology, vol. 21, no. 22, pp. 7617–7628, 2001. View at Publisher · View at Google Scholar · View at Scopus
  84. L. Pellizzoni, N. Kataoka, B. Charroux, and G. Dreyfuss, “A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing,” Cell, vol. 95, no. 5, pp. 615–624, 1998. View at Google Scholar · View at Scopus
  85. N. Ohkura, M. Takahashi, H. Yaguchi, Y. Nagamura, and T. Tsukada, “Coactivator-associated arginine methyltransferase 1, CARM1, affects pre-mRNA splicing in an isoform-specific manner,” Journal of Biological Chemistry, vol. 280, no. 32, pp. 28927–28935, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. P. Kuhn, R. Chumanov, Y. Wang, Y. Ge, R. R. Burgess, and W. Xu, “Automethylation of CARM1 allows coupling of transcription and mRNA splicing,” Nucleic Acids Research. In press.
  87. K. M. Neugebauer, “On the importance of being co-transcriptional,” Journal of Cell Science, vol. 115, no. 20, pp. 3865–3871, 2002. View at Publisher · View at Google Scholar · View at Scopus
  88. C. L. Will and R. Luhrmann, “Spliceosomal UsnRNP biogenesis, structure and function,” Current Opinion in Cell Biology, vol. 13, no. 3, pp. 290–301, 2001. View at Publisher · View at Google Scholar · View at Scopus
  89. Y. C. Chen, E. J. Milliman, I. Goulet et al., “Protein arginine methylation facilitates Co-transcriptional recruitment of pre-mRNA splicing factors,” Molecular and Cellular Biology, vol. 30, no. 21, pp. 5245–5256, 2010. View at Google Scholar
  90. T. Ito, T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, and Y. Sakaki, “A comprehensive two-hybrid analysis to explore the yeast protein interactome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 8, pp. 4569–4574, 2001. View at Publisher · View at Google Scholar · View at Scopus
  91. G. Dreyfuss, V. N. Kim, and N. Kataoka, “Messenger-RNA-binding proteins and the messages they carry,” Nature Reviews Molecular Cell Biology, vol. 3, no. 3, pp. 195–205, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. H. Le Hir and B. Séraphin, “EJCs at the heart of translational control,” Cell, vol. 133, no. 2, pp. 213–216, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. I. W. Hsu, M. Hsu, C. Li, T. W. Chuang, R. I. Un, and W. Y. Tarn, “Phosphorylation of Y14 modulates its interaction with proteins involved in mRNA metabolism and influences its methylation,” Journal of Biological Chemistry, vol. 280, no. 41, pp. 34507–34512, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. T. W. Chuang, P. J. Peng, and W. Y. Tarn, “The exon junction complex component Y14 modulates the activity of the methylosome in biogenesis of spliceosomal snRNPs,” The Journal of Biological Chemistry, vol. 286, no. 11, pp. 8722–8728, 2011. View at Publisher · View at Google Scholar
  95. M. C. Yu, F. Bachand, A. E. McBride, S. Komili, J. M. Casolari, and P. A. Silver, “Arginine methyltransferase affects interactions and recruitment of mRNA processing and export factors,” Genes and Development, vol. 18, no. 16, pp. 2024–2035, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. B. J. Calnan, B. Tidor, S. Biancalana, D. Hudson, and A. D. Frankel, “Arginine-mediated RNA recognition: the arginine fork,” Science, vol. 252, no. 5010, pp. 1167–1171, 1991. View at Google Scholar · View at Scopus
  97. S. Hyun, S. Jeong, and J. Yu, “Effects of asymmetric arginine dimethylation on RNA-binding peptides,” Chembiochem, vol. 9, no. 17, pp. 2790–2792, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. R. B. Denman, “Methylation of the arginine-glycine-rich region in the fragile X mental retardation protein FMRP differentially affects RNA binding,” Cellular and Molecular Biology Letters, vol. 7, no. 3, pp. 877–883, 2002. View at Google Scholar · View at Scopus
  99. Y. Chen, X. Zhou, N. Liu et al., “Arginine methylation of hnRNP K enhances p53 transcriptional activity,” FEBS Letters, vol. 582, no. 12, pp. 1761–1765, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. C. M. Wong, H. M. V. Tang, K. Y. E. Kong et al., “Yeast arginine methyltransferase Hmt1p regulates transcription elongation and termination by methylating Npl3p,” Nucleic Acids Research, vol. 38, no. 7, pp. 2217–2228, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. R. F. Luco, Q. Pan, K. Tominaga, B. J. Blencowe, O. M. Pereira-Smith, and T. Misteli, “Regulation of alternative splicing by histone modifications,” Science, vol. 327, no. 5968, pp. 996–1000, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. R. P. Zakaryan and H. Gehring, “Identification and characterization of the nuclear localization/retention signal in the EWS proto-oncoprotein,” Journal of Molecular Biology, vol. 363, no. 1, pp. 27–38, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. K. Aoki, Y. Ishii, K. Matsumoto, and M. Tsujimoto, “Methylation of Xenopus CIRP2 regulates its arginine- and glycine-rich region-mediated nucleocytoplasmic distribution,” Nucleic Acids Research, vol. 30, no. 23, pp. 5182–5192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  104. J. Li, H. Tang, T. M. Mullen et al., “A role for RNA helicase A in post-transcriptional regulation of HIV type 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 2, pp. 709–714, 1999. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Zhang, C. Herrmann, and F. Grosse, “Pre-mRNA and mRNA binding of human nuclear DNA helicase II (RNA helicase A),” Journal of Cell Science, vol. 112, no. 7, pp. 1055–1064, 1999. View at Google Scholar · View at Scopus
  106. W. A. Smith, B. T. Schurter, F. Wong-Staal, and M. David, “Arginine methylation of RNA helicase A determines its subcellular localization,” Journal of Biological Chemistry, vol. 279, no. 22, pp. 22795–22798, 2004. View at Publisher · View at Google Scholar · View at Scopus
  107. G. Martin, A. Ostareck-Lederer, A. Chari et al., “Arginine methylation in subunits of mammalian pre-mRNA cleavage factor I,” RNA, vol. 16, no. 8, pp. 1646–1659, 2010. View at Publisher · View at Google Scholar
  108. J. J. Smith, K. P. Rücknagel, A. Schierhorn et al., “Unusual sites of arginine methylation in poly(A)-binding protein II and in vitro methylation by protein arginine methyltransferases PRMT1 and PRMT3,” Journal of Biological Chemistry, vol. 274, no. 19, pp. 13229–13234, 1999. View at Publisher · View at Google Scholar · View at Scopus
  109. U. Kühn and E. Wahle, “Structure and function of poly(A) binding proteins,” Biochimica et Biophysica Acta, vol. 1678, no. 2-3, pp. 67–84, 2004. View at Publisher · View at Google Scholar · View at Scopus
  110. K. Fronz, S. Otto, K. Kölbel et al., “Promiscuous modification of the nuclear poly(A)-binding protein by multiple protein-arginine methyltransferases does not affect the aggregation behavior,” Journal of Biological Chemistry, vol. 283, no. 29, pp. 20408–20420, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. A. Perreault, C. Lemieux, and F. Bachand, “Regulation of the nuclear poly(A)-binding protein by arginine methylation in fission yeast,” Journal of Biological Chemistry, vol. 282, no. 10, pp. 7552–7562, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. C. M. Brennan and J. A. Steitz, “HuR and mRNA stability,” Cellular and Molecular Life Sciences, vol. 58, no. 2, pp. 266–277, 2001. View at Google Scholar · View at Scopus
  113. T. Fujiwara, Y. Mori, D. L. Chu et al., “CARM1 regulates proliferation of PC12 cells by methylating HuD,” Molecular and Cellular Biology, vol. 26, no. 6, pp. 2273–2285, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. H. Li, S. Park, B. Kilburn et al., “Lipopolysaccharide-induced methylation of HuR, an mRNA-stabilizing protein, by CARM1,” Journal of Biological Chemistry, vol. 277, no. 47, pp. 44623–44630, 2002. View at Publisher · View at Google Scholar
  115. V. Calvanese, E. Lara, B. Suárez-Álvarez et al., “Sirtuin 1 regulation of developmental genes during differentiation of stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 31, pp. 13736–13741, 2010. View at Publisher · View at Google Scholar
  116. L. Hubers, H. Valderrama-Carvajal, J. Laframboise, J. Timbers, G. Sanchez, and J. Côté, “HuD interacts with survival motor neuron protein and can rescue spinal muscular atrophy-like neuronal defects,” Human Molecular Genetics, vol. 20, no. 3, pp. 553–579, 2011. View at Publisher · View at Google Scholar
  117. D. Chen, M. Ma, H. Hong et al., “Regulation of transcription by a protein methyltransferase,” Science, vol. 284, no. 5423, pp. 2174–2177, 1999. View at Publisher · View at Google Scholar · View at Scopus
  118. B. T. Schurter, S. S. Koh, D. Chen et al., “Methylation of histone H3 by coactivator-associated arginine methyltransferase 1,” Biochemistry, vol. 40, no. 19, pp. 5747–5756, 2001. View at Publisher · View at Google Scholar · View at Scopus