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Protein Arginine Methylation: A New Frontier in T Cell Signal Transduction

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Lymphocyte Signal Transduction

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10. References

  1. T. Pawson, Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191–203 (2004).

    Article  PubMed  CAS  Google Scholar 

  2. A.J. Bannister, R. Schneider, and T. Kouzarides, Histone methylation: dynamic or static? Cell 109, 801–806 (2002).

    Article  PubMed  CAS  Google Scholar 

  3. M. T. Bedford and S. Richard, Arginine methylation an emerging regulator of protein function. Mol Cell 18, 263–272 (2005).

    Article  PubMed  CAS  Google Scholar 

  4. M. R. Stallcup, Role of protein methylation in chromatin remodeling and transcriptional regulation. Oncogene 20, 3014–3020 (2001).

    Article  PubMed  CAS  Google Scholar 

  5. J. D. Gary and S. Clarke, RNA and protein interactions modulated by protein arginine methylation. Prog Nucleic Acid Res Mol Biol 61, 65–131 (1998).

    Article  PubMed  CAS  Google Scholar 

  6. A. E. McBride and P. A. Silver, State of the arg: protein methylation at arginine comes of age. Cell 106, 5–8 (2001).

    Article  PubMed  CAS  Google Scholar 

  7. A. Lanzavecchia and F. Sallusto, Progressive differentiation and selection of the fittest in the immune response. Nat Rev Immunol 2, 982–987 (2002).

    Article  PubMed  CAS  Google Scholar 

  8. V. G. Allfrey, R. Faulkner, and A. E. Mirsky, Acetylation And Methylation Of Histones And Their Possible Role In The Regulation Of Rna Synthesis. Proc Natl Acad. Sci U S A 51, 786–794 (1964).

    Article  PubMed  CAS  Google Scholar 

  9. W. K. Paik and S. Kim, Enzymatic methylation of protein fractions from calf thymus nuclei. Biochem Biophys Res Commun 29, 14–20 (1967).

    Article  PubMed  CAS  Google Scholar 

  10. D. Wu and L. B. Hersh, Identification of an active site arginine in rat choline acetyl-transferase by alanine scanning mutagenesis. J Biol Chem 270, 29111–29116 (1995).

    Article  PubMed  CAS  Google Scholar 

  11. P. D. Cary, T. Moss, and E. M. Bradbury, High-resolution proton-magnetic-resonance studies of chromatin core particles. Eur J Biochem 89, 475–482 (1978).

    Article  PubMed  CAS  Google Scholar 

  12. J. E. Katz, M. Dlakic, and S. Clarke, Automated identification of putative methyltransferases from genomic open reading frames. Mol Cell Proteomics 2, 525–540 (2003).

    PubMed  CAS  Google Scholar 

  13. T. B. Miranda, M. Miranda, A. Frankel, and S. Clarke, PRMT7 is a member of the protein arginine methyltransferase family with a distinct substrate specificity. J Biol. Chem 279, 22902–22907 (2004).

    Article  PubMed  CAS  Google Scholar 

  14. V. H. Weiss, A. E. McBride, M. A. Soriano, D. J. Filman, P. A. Silver, and J. M. Hogle, The structure and oligomerization of the yeast arginine methyltransferase, Hmt1. Nat Struct Biol 7, 1165–1171 (2000).

    Article  PubMed  CAS  Google Scholar 

  15. X. Zhang and X. Cheng, Structure of the predominant protein arginine methyltransferase PRMT1 and analysis of its binding to substrate peptides. Structure (Camb) 11, 509–520 (2003).

    Article  CAS  Google Scholar 

  16. X. Zhang, L. Zhou, and X. Cheng, Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. Embo J 19, 3509–3519 (2000).

    Article  PubMed  CAS  Google Scholar 

  17. F. M. Boisvert, J. Cote, M. C. Boulanger, and S. Richard, A proteomic analysis of arginine-methylated protein complexes. Mol Cell Proteomics 2, 1319–1330 (2003).

    Article  PubMed  CAS  Google Scholar 

  18. J. Tang, A. Frankel, R. J. Cook, S. Kim, W. K. Paik, K. R. Williams, S. Clarke, and H. R. Herschman, PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J Biol Chem 275, 7723–7730 (2000).

    Article  PubMed  CAS  Google Scholar 

  19. S. Klein, J. A. Carroll, Y. Chen, M. F. Henry, P. A. Henry, I. E. Ortonowski, G. Pintucci, R. C. Beavis, W. H. Burgess, and D. B. Rifkin, Biochemical analysis of the arginine methylation of high molecular weight fibroblast growth factor-2. J Biol. Chem 275, 3150–3157 (2000).

    Article  PubMed  CAS  Google Scholar 

  20. H. Li, S. Park, B. Kilburn, M. A. Jelinek, A. Henschen-Edman, D. W. Aswad, M. R. Stallcup, and I. A. Laird-Offringa, Lipopolysaccharide-induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. Coactivator-associated arginine methyltransferase. J Biol Chem 277, 44623–44630 (2002).

    Article  PubMed  CAS  Google Scholar 

  21. K. A. Mowen and M. David, Analysis of protein arginine methylation and protein arginine-methyltransferase activity. Sci STKE 2001, PL1 (2001).

    Article  PubMed  CAS  Google Scholar 

  22. W. A. Smith, B. T. Schurter, F. Wong-Staal, and M. David, Arginine methylation of RNA helicase a determines its subcellular localization. J Biol Chem 279, 22795–22798 (2004).

    Article  PubMed  CAS  Google Scholar 

  23. K. A. Mowen, B. T. Schurter, J. W. Fathman, M. David, and L. H. Glimcher, Arginine methylation of NIP45 modulates cytokine gene expression in effector T lymphocytes. Mol Cell 15, 559–571 (2004).

    Article  PubMed  CAS  Google Scholar 

  24. J. Lee and M. T. Bedford, PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays. EMBO Rep 3, 268–273 (2002).

    Article  PubMed  CAS  Google Scholar 

  25. W. J. Lin, J. D. Gary, M. C. Yang, S. Clarke, and H. R. Herschman, The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J Biol Chem 271, 15034–15044 (1996).

    Article  PubMed  CAS  Google Scholar 

  26. J. Tang, P. N. Kao, and H. R. Herschman, Protein-arginine methyltransferase I, the predominant protein-arginine methyltransferase in cells, interacts with and is regulated by interleukin enhancer-binding factor 3. J Biol Chem 275, 19866–19876 (2000).

    Article  PubMed  CAS  Google Scholar 

  27. M. R. Pawlak, C. A. Scherer, J. Chen, M. J. Roshon, and H. E. Ruley, Arginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol Cell Biol 20, 4859–4869 (2000).

    Article  PubMed  CAS  Google Scholar 

  28. J. Najbauer, B. A. Johnson, A. L. Young, and D. W. Aswad, 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, 10501–10509 (1993).

    PubMed  CAS  Google Scholar 

  29. F. Herrmann, J. Lee, M. T. Bedford, and F. O. Fackelmayer, Dynamics of human protein arginine methyltransferase 1 (PRMT1) in vivo. J Biol Chem (2005).

    Google Scholar 

  30. H. S. Scott, S. E. Antonarakis, M. D. Lalioti, C. Rossier, P. A. Silver, and M. F. Henry, Identification and characterization of two putative human arginine methyltransferases (HRMT1L1 and HRMT1L2). Genomics 48, 330–340 (1998).

    Article  PubMed  CAS  Google Scholar 

  31. C. Qi, J. Chang, Y. Zhu, A. V. Yeldandi, S. M. Rao, and Y. J. Zhu, Identification of protein arginine methyltransferase 2 as a coactivator for estrogen receptor alpha. J. Biol Chem 277, 28624–28630 (2002).

    Article  PubMed  CAS  Google Scholar 

  32. J. Kzhyshkowska, H. Schutt, M. Liss, E. Kremmer, R. Stauber, H. Wolf, and T. Dobner, Heterogeneous nuclear ribonucleoprotein E1B-AP5 is methylated in its Arg-Gly-Gly (RGG) box and interacts with human arginine methyltransferase HRMT1L1. Biochem J 358, 305–314 (2001).

    Article  PubMed  CAS  Google Scholar 

  33. J. Tang, J. D. Gary, S. Clarke, and H. R. Herschman, PRMT 3, 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 (1998).

    Article  PubMed  CAS  Google Scholar 

  34. A. Frankel and S. Clarke, PRMT3 is a distinct member of the protein arginine N-methyltransferase family. Conferral of substrate specificity by a zinc-finger domain. J Biol Chem 275, 32974–32982 (2000).

    Article  PubMed  CAS  Google Scholar 

  35. S. Pahlich, K. Bschir, C. Chiavi, L. Belyanskaya, and H. Gehring, Different methylation characteristics of protein arginine methyltransferase 1 and 3 toward the Ewing Sarcoma protein and a peptide. Proteins 61, 164–175 (2005).

    Article  PubMed  CAS  Google Scholar 

  36. R. Swiercz, M. D. Person, and M. T. Bedford, Ribosomal protein S2 is a substrate for mammalian protein arginine methyltransferase 3 (PRMT3). Biochem J (2004).

    Google Scholar 

  37. D. Chen, H. Ma, H. Hong, S. S. Koh, S. M. Huang, B. T. Schurter, D. W. Aswad, and M. R. Stallcup, Regulation of transcription by a protein methyltransferase. Science 284, 2174–2177 (1999).

    Article  PubMed  CAS  Google Scholar 

  38. B. T. Schurter, S. S. Koh, D. Chen, G. J. Bunick, J. M. Harp, B. L. Hanson, A. Henschen-Edman, D. R. Mackay, M. R. Stallcup, and D. W. Aswad, Methylation of histone H3 by coactivator-associated arginine methyltransferase 1. Biochemistry 40, 5747–5756 (2001).

    Article  PubMed  CAS  Google Scholar 

  39. D. Y. Lee, C. Teyssier, B. D. Strahl, and M. R. Stallcup, Role of protein methylation in regulation of transcription. Endocr Rev 26, 147–170 (2005).

    Article  PubMed  CAS  Google Scholar 

  40. N. Yadav, J. Lee, J. Kim, J. Shen, M. C. Hu, C. M. Aldaz, and M. T. Bedford, Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice. Proc Natl Acad Sci U S A 100, 6464–6468 (2003).

    Article  PubMed  CAS  Google Scholar 

  41. B. P. Pollack, S. V. Kotenko, W. He, L. S. Izotova, B. L. Barnoski, and S. Pestka, The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J Biol Chem 274, 31531–31542 (1999).

    Article  PubMed  CAS  Google Scholar 

  42. W. J. Friesen, S. Paushkin, A. Wyce, S. Massenet, G. S. Pesiridis, G. Van Duyne, J. Rappsilber, M. Mann, and G. Dreyfuss, The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol Cell Biol 21, 8289–8300 (2001).

    Article  PubMed  CAS  Google Scholar 

  43. M. C. Boulanger, C. Liang, R. S. Russell, R. Lin, M. T. Bedford, M. A. Wainberg, and S. Richard, Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. J Virol 79, 124–131 (2005).

    Article  PubMed  CAS  Google Scholar 

  44. A. Frankel, N. Yadav, J. Lee, T. L. Branscombe, S. Clarke, and M. T. Bedford, The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J Biol Chem 277, 3537–3543 (2002).

    Article  PubMed  CAS  Google Scholar 

  45. T. B. Miranda, K. J. Webb, D. D. Edberg, R. Reeves, and S. Clarke, Protein arginine methyltransferase 6 specifically methylates the nonhistone chromatin protein HMGA1a. Biochem Biophys Res Commun 336, 831–835 (2005).

    Article  PubMed  CAS  Google Scholar 

  46. J. Lee, J. Sayegh, J. Daniel, S. Clarke, and M. T. Bedford, PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J Biol Chem 280, 32890–32896 (2005).

    Article  PubMed  CAS  Google Scholar 

  47. T. R. Cimato, J. Tang, Y. Xu, C. Guarnaccia, H. R. Herschman, S. Pongor, and J. M. Aletta, Nerve growth factor-mediated increases in protein methylation occur predominantly at type I arginine methylation sites and involve protein arginine methyltransferase 1. J Neurosci Res 67, 435–442 (2002).

    Article  PubMed  CAS  Google Scholar 

  48. T. R. Cimato, M. J. Ettinger, X. Zhou, and J. M. Aletta, Nerve growth factor-specific regulation of protein methylation during neuronal differentiation of PC12 cells. J Cell Biol 138, 1089–1103 (1997).

    Article  PubMed  CAS  Google Scholar 

  49. C. Abramovich, B. Yakobson, J. Chebath, and M. Revel, A protein-arginine methyltransferase binds to the intracytoplasmic domain of the IFNAR1 chain in the type I interferon receptor. Embo J 16, 260–266 (1997).

    Article  PubMed  CAS  Google Scholar 

  50. M. Chevillard-Briet, D. Trouche, and L. Vandel, Control of CBP co-activating activity by arginine methylation. Embo J 21, 5457–5466 (2002).

    Article  PubMed  CAS  Google Scholar 

  51. M. Covic, P. O. Hassa, S. Saccani, C. Buerki, N. I. Meier, C. Lombardi, R. Imhof, M. T. Bedford, G. Natoli, and M. O. Hottiger, Arginine methyltransferase CARM1 is a promoter-specific regulator of NF-kappaB-dependent gene expression. Embo J (2004).

    Google Scholar 

  52. K. A. Mowen, J. Tang, W. Zhu, B. T. Schurter, K. Shuai, H. R. Herschman, and M. David, Arginine methylation of STAT1 modulates IFNalpha/beta-induced transcription. Cell 104, 731–741 (2001).

    Article  PubMed  CAS  Google Scholar 

  53. W. Chen, M. O. Daines, and G. K. Hershey, Methylation of STAT6 modulates STAT6 phosphorylation, nuclear translocation, and DNA-binding activity. J Immunol 172, 6744–6750 (2004).

    PubMed  CAS  Google Scholar 

  54. W. Komyod, U. M. Bauer, P. C. Heinrich, S. Haan, and I. Behrmann, Are STATS arginine-methylated? J Biol Chem 280, 21700–21705 (2005).

    Article  PubMed  CAS  Google Scholar 

  55. J. A. Wolos, K. A. Frondorf, G. F. Davis, E. T. Jarvi, J. R. McCarthy, and T. L. Bowlin, Selective inhibition of T cell activation by an inhibitor of S-adenosyl-L-homocysteine hydrolase. J Immunol 150, 3264–3273 (1993).

    PubMed  CAS  Google Scholar 

  56. J. A. Wolos, K. A. Frondorf, and R. E. Esser, Immunosuppression mediated by an inhibitor of S-adenosyl-L-homocysteine hydrolase. Prevention and treatment of collagen-induced arthritis. J Immunol 151, 526–534 (1993).

    PubMed  CAS  Google Scholar 

  57. J. Kim, J. Lee, N. Yadav, Q. Wu, C. Carter, S. Richard, E. Richie, and M. T. Bedford, Loss of CARM1 results in hypomethylation of thymocyte cyclic AMP-regulated phosphoprotein and deregulated early T cell development. J Biol Chem 279, 25339–25344 (2004).

    Article  PubMed  CAS  Google Scholar 

  58. G. R. Crabtree and E. N. Olson, NFAT signaling: choreographing the social lives of cells. Cell 109, S67–79 (2002).

    Article  PubMed  CAS  Google Scholar 

  59. M. Diehn, A. A. Alizadeh, O. J. Rando, C. L. Liu, K. Stankunas, D. Botstein, G. R. Crabtree, and P. O. Brown, Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc Natl Acad Sci U S A 99, 11796–11801 (2002).

    Article  PubMed  CAS  Google Scholar 

  60. O. Acuto and F. Michel, CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 3, 939–951 (2003).

    Article  PubMed  CAS  Google Scholar 

  61. M. R. Hodge, H. J. Chun, J. Rengarajan, A. Alt, R. Lieberson, and L. H. Glimcher, NF-AT-driven interleukin-4 transcription potentiated by NIP45. Science 274, 1903–1905 (1996).

    Article  PubMed  CAS  Google Scholar 

  62. F. Blanchet, A. Cardona, F. A. Letimier, M. S. Hershfield, and O. Acuto, CD28 costimulatory signal induces protein arginine methylation in T cells. J Exp Med 202, 371–377 (2005).

    Article  PubMed  CAS  Google Scholar 

  63. M. Turner and D. D. Billadeau, VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat Rev Immunol 2, 476–486 (2002).

    Article  PubMed  CAS  Google Scholar 

  64. M. Houlard, R. Arudchandran, F. Regnier-Ricard, A. Germani, S. Gisselbrecht, U. Blank, J. Rivera, and N. Varin-Blank, Vav1 is a component of transcriptionally active complexes. J Exp Med 195, 1115–1127 (2002).

    Article  PubMed  CAS  Google Scholar 

  65. M. Lopez-Lago, H. Lee, C. Cruz, N. Movilla, and X. R. Bustelo, Tyrosine phosphorylation mediates both activation and downmodulation of the biological activity of Vav. Mol Cell Biol 20, 1678–1691 (2000).

    Article  PubMed  CAS  Google Scholar 

  66. D. Klasen, F. Pages, J.-F. Peyron, D. A. Cantrell, and D. Olive, Two distinct regions of the CD28 intracytoplasmic domain are involved in the tyrosine phosphorylation of Vav and GTPase activating protein-associated p62 protein. International Immunology 10, 481–489 (1998).

    Article  PubMed  CAS  Google Scholar 

  67. J. L. Zugaza, M. A. Lopez-Lago, M. J. Caloca, M. Dosil, N. Movilla, and X. R. Bustelo, Structural determinants for the biological activity of Vav proteins. J Biol. Chem 277, 45377–45392 (2002).

    Article  PubMed  CAS  Google Scholar 

  68. Y. Wang, J. Wysocka, J. Sayegh, Y. H. Lee, J. R. Perlin, L. Leonelli, L. S. Sonbuchner, C. H. McDonald, R. G. Cook, Y. Dou, R. G. Roeder, S. Clarke, M. R. Stallcup, C. D. Allis, and S. A. Coonrod, Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306, 279–283 (2004).

    Article  PubMed  CAS  Google Scholar 

  69. O. F. Sarmento, L. C. Digilio, Y. Wang, J. Perlin, J. C. Herr, C. D. Allis, and S. A. Coonrod, Dynamic alterations of specific histone modifications during early murine development. J Cell Sci 117, 4449–4459 (2004).

    Article  PubMed  CAS  Google Scholar 

  70. G. L. Cuthbert, S. Daujat, A. W. Snowden, H. Erdjument-Bromage, T. Hagiwara, M. Yamada, R. Schneider, P. D. Gregory, P. Tempst, A. J. Bannister, and T. Kouzarides, Histone deimination antagonizes arginine methylation. Cell 118, 545–553 (2004).

    Article  PubMed  CAS  Google Scholar 

  71. E. R. Vossenaar, A. J. Zendman, W. J. van Venrooij, and G. J. Pruijn, PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays 25, 1106–1118 (2003).

    Article  PubMed  CAS  Google Scholar 

  72. S. Kubicek and T. Jenuwein, A crack in histone lysine methylation. Cell 119, 903–906 (2004).

    Article  PubMed  CAS  Google Scholar 

  73. J. M. Aletta, T. R. Cimato, and M. J. Ettinger, Protein methylation: a signal event in post-translational modification. Trends Biochem Sci 23, 89–91 (1998).

    Article  PubMed  CAS  Google Scholar 

  74. D. Cheng, N. Yadav, R. W. King, M. S. Swanson, E. J. Weinstein, and M. T. Bedford, Small molecule regulators of protein arginine methyltransferases. J Biol Chem 279, 23892–23899 (2004).

    Article  PubMed  CAS  Google Scholar 

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Schurter, B.T., Blanchet, F., Acuto, O. (2006). Protein Arginine Methylation: A New Frontier in T Cell Signal Transduction. In: Tsoukas, C. (eds) Lymphocyte Signal Transduction. Advances in Experimental Medicine and Biology, vol 584. Springer, Boston, MA. https://doi.org/10.1007/0-387-34132-3_14

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