Protein Arginine Methylation in Mammals: Who, What, and Why

Molecular Cell

Volumn 33, Issue 1, 2009, Pages 1-13

  Bedford, Mark T ^a   Clarke, Steven G ^b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; F BOX PROTEIN; GENE PRODUCT; LYSINE; PROTEIN;

CARDIOVASCULAR DISEASE; CELLULAR DISTRIBUTION; DEMETHYLATION; DNA REPAIR; ENZYME ACTIVITY; EUKARYOTE; GENETIC TRANSCRIPTION; MAMMAL; MOLECULAR RECOGNITION; NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; REVIEW; RNA SPLICING; SIGNAL TRANSDUCTION; SPINAL MUSCULAR ATROPHY; VIRUS INFECTION;

AMINO ACID SEQUENCE; ANIMALS; ARGININE; MAMMALS; METHYLATION; MOLECULAR SEQUENCE DATA; PROTEIN-ARGININE N-METHYLTRANSFERASE; PROTEINS; SUBSTRATE SPECIFICITY;

EUKARYOTA; MAMMALIA;

EID: 58149295717     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.12.013     Document Type: Review

References (120)

1. Adams M.M., Wang B., Xia Z., Morales J.C., Lu X., Donehower L.A., Bochar D.A., Elledge S.J., and Carpenter P.B. 53BP1 oligomerization is independent of its methylation by PRMT1. Cell Cycle 4 (2005) 1854-1861
2. Ancelin K., Lange U.C., Hajkova P., Schneider R., Bannister A.J., Kouzarides T., and Surani M.A. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat. Cell Biol. 8 (2006) 623-630
3. Aoki K., Ishii Y., Matsumoto K., and Tsujimoto M. Methylation of Xenopus CIRP2 regulates its arginine- and glycine-rich region-mediated nucleocytoplasmic distribution. Nucleic Acids Res. 30 (2002) 5182-5192
4. Bedford M.T. Arginine methylation at a glance. J. Cell Sci. 120 (2007) 4243-4246
5. Bedford M.T., Frankel A., Yaffe M.B., Clarke S., Leder P., and Richard S. Arginine methylation inhibits the binding of proline-rich ligands to Src homology 3, but not WW, domains. J. Biol. Chem. 275 (2000) 16030-16036
6. Bedford M.T., and Richard S. Arginine methylation an emerging regulator of protein function. Mol. Cell 18 (2005) 263-272
7. Blanchet F., Cardona A., Letimier F.A., Hershfield M.S., and Acuto O. CD28 costimulatory signal induces protein arginine methylation in T cells. J. Exp. Med. 202 (2005) 371-377
8. Boisvert F.M., Cote J., Boulanger M.C., Cleroux P., Bachand F., Autexier C., and Richard S. Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing. J. Cell Biol. 159 (2002) 957-969
9. Boisvert F.M., Cote J., Boulanger M.C., and Richard S. A Proteomic Analysis of Arginine-methylated Protein Complexes. Mol. Cell. Proteomics 2 (2003) 1319-1330
10. Boisvert F.M., Dery U., Masson J.Y., and Richard S. Arginine methylation of MRE11 by PRMT1 is required for DNA damage checkpoint control. Genes Dev. 19 (2005) 671-676
11. Boisvert F.M., Hendzel M.J., Masson J.Y., and Richard S. Methylation of MRE11 regulates its nuclear compartmentalization. Cell Cycle 4 (2005) 981-989
12. Boisvert F.M., Rhie A., Richard S., and Doherty A.J. The GAR motif of 53BP1 is arginine methylated by PRMT1 and is necessary for 53BP1 DNA binding activity. Cell Cycle 4 (2005) 1834-1841
13. Boulanger M.C., Liang C., Russell R.S., Lin R., Bedford M.T., Wainberg M.A., and Richard S. Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. J. Virol. 79 (2005) 124-131
14. Brame C.J., Moran M.F., and McBroom-Cerajewski L.D. A mass spectrometry based method for distinguishing between symmetrically and asymmetrically dimethylated arginine residues. Rapid Commun. Mass Spectrom. 18 (2004) 877-881
15. Branscombe T.L., Frankel A., Lee J.H., Cook J.R., Yang Z., Pestka S., and Clarke S. Prmt5 (janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J. Biol. Chem. 276 (2001) 32971-32976
16. Buhr N., Carapito C., Schaeffer C., Kieffer E., Van Dorsselaer A., and Viville S. Nuclear proteome analysis of undifferentiated mouse embryonic stem and germ cells. Electrophoresis 29 (2008) 2381-2390
17. Calnan B.J., Tidor B., Biancalana S., Hudson D., and Frankel A.D. Arginine-mediated RNA recognition: the arginine fork. Science 252 (1991) 1167-1171
18. Chang B., Chen Y., Zhao Y., and Bruick R.K. JMJD6 is a histone arginine demethylase. Science 318 (2007) 444-447
19. Chen D., Ma H., Hong H., Koh S.S., Huang S.M., Schurter B.T., Aswad D.W., and Stallcup M.R. Regulation of transcription by a protein methyltransferase. Science 284 (1999) 2174-2177
20. Cheng D., Cote J., Shaaban S., and Bedford M.T. The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol. Cell 25 (2007) 71-83
21. Cheng X., Collins R.E., and Zhang X. Structural and sequence motifs of protein (histone) methylation enzymes. Annu. Rev. Biophys. Biomol. Struct. 34 (2005) 267-294
22. Cheung N., Chan L.C., Thompson A., Cleary M.L., and So C.W. Protein arginine-methyltransferase-dependent oncogenesis. Nat. Cell Biol. 9 (2007) 1208-1215
23. In: Clarke S.G., and Tamanoi F. (Eds). Protein Methyltransferases. The Enzymes, Third Edition Volume XXIV (2006), Academic Press, San Diego, CA
24. Cook J.R., Lee J.H., Yang Z.H., Krause C.D., Herth N., Hoffmann R., and Pestka S. FBXO11/PRMT9, a new protein arginine methyltransferase, symmetrically dimethylates arginine residues. Biochem. Biophys. Res. Commun. 342 (2006) 472-481
25. Cote J., and Richard S. Tudor domains bind symmetrical dimethylated arginines. J. Biol. Chem. 280 (2005) 28476-28483
26. Couture J.F., Collazo E., and Trievel R.C. Molecular recognition of histone H3 by the WD40 protein WDR5. Nat. Struct. Mol. Biol. 13 (2006) 698-703
27. Cusco I., Barcelo M.J., del Rio E., Baiget M., and Tizzano E.F. Detection of novel mutations in the SMN Tudor domain in type I SMA patients. Neurology 63 (2004) 146-149
28. Dacwag C.S., Ohkawa Y., Pal S., Sif S., and Imbalzano A.N. The protein arginine methyltransferase Prmt5 is required for myogenesis because it facilitates ATP-dependent chromatin remodeling. Mol. Cell. Biol. 27 (2007) 384-394
29. Dery U., Coulombe Y., Rodrigue A., Stasiak A., Richard S., and Masson J.Y. A glycine-arginine domain in control of the human MRE11 DNA repair protein. Mol. Cell Biol. 28 (2008) 3058-3069
30. El Messaoudi S., Fabbrizio E., Rodriguez C., Chuchana P., Fauquier L., Cheng D., Theillet C., Vandel L., Bedford M.T., and Sardet C. Coactivator-associated arginine methyltransferase 1 (CARM1) is a positive regulator of the Cyclin E1 gene. Proc. Natl. Acad. Sci. USA 103 (2006) 13351-13356
31. El-Andaloussi N., Valovka T., Toueille M., Hassa P.O., Gehrig P., Covic M., Hubscher U., and Hottiger M.O. Methylation of DNA polymerase beta by protein arginine methyltransferase 1 regulates its binding to proliferating cell nuclear antigen. FASEB J. 21 (2007) 26-34
32. El-Andaloussi N., Valovka T., Toueille M., Steinacher R., Focke F., Gehrig P., Covic M., Hassa P.O., Schar P., Hubscher U., and Hottiger M.O. Arginine methylation regulates DNA polymerase Beta. Mol. Cell 22 (2006) 51-62
33. Fabbrizio E., El Messaoudi S., Polanowska J., Paul C., Cook J.R., Lee J.H., Negre V., Rousset M., Pestka S., Le Cam A., and Sardet C. Negative regulation of transcription by the type II arginine methyltransferase PRMT5. EMBO Rep. 3 (2002) 641-645
34. Feng Q., Yi P., Wong J., and O'Malley B.W. Signaling within a coactivator complex: methylation of SRC-3/AIB1 is a molecular switch for complex disassembly. Mol. Cell. Biol. 26 (2006) 7846-7857
35. Fielenbach N., Guardavaccaro D., Neubert K., Chan T., Li D., Feng Q., Hutter H., Pagano M., and Antebi A. DRE-1: an evolutionarily conserved F box protein that regulates C. elegans developmental age. Dev. Cell 12 (2007) 443-455
36. Flanagan J.F., Mi L.Z., Chruszcz M., Cymborowski M., Clines K.L., Kim Y., Minor W., Rastinejad F., and Khorasanizadeh S. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438 (2005) 1181-1185
37. Frankel A., and Clarke S. 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 (2000) 32974-32982
38. Frankel A., Yadav N., Lee J., Branscombe T.L., Clarke S., and Bedford M.T. The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J. Biol. Chem. 277 (2002) 3537-3543
39. Frietze S., Lupien M., Silver P.A., and Brown M. CARM1 regulates estrogen-stimulated breast cancer growth through up-regulation of E2F1. Cancer Res. 68 (2008) 301-306
40. Ganesh L., Yoshimoto T., Moorthy N.C., Akahata W., Boehm M., Nabel E.G., and Nabel G.J. Protein methyltransferase 2 inhibits NF-kappaB function and promotes apoptosis. Mol. Cell. Biol. 26 (2006) 3864-3874
41. Gary J.D., and Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog. Nucleic Acid Res. Mol. Biol. 61 (1998) 65-131
42. Gehrig P.M., Hunziker P.E., Zahariev S., and Pongor S. Fragmentation pathways of N(G)-methylated and unmodified arginine residues in peptides studied by ESI-MS/MS and MALDI-MS. J. Am. Soc. Mass Spectrom. 15 (2004) 142-149
43. Gonsalvez G.B., Tian L., Ospina J.K., Boisvert F.M., Lamond A.I., and Matera A.G. Two distinct arginine methyltransferases are required for biogenesis of Sm-class ribonucleoproteins. J. Cell Biol. 178 (2007) 733-740
44. Goulet I., Gauvin G., Boisvenue S., and Cote J. Alternative splicing yields protein arginine methyltransferase 1 isoforms with distinct activity, substrate specificity, and subcellular localization. J. Biol. Chem. 282 (2007) 33009-33021
45. Gros L., Renodon-Corniere A., de Saint Vincent B.R., Feder M., Bujnicki J.M., and Jacquemin-Sablon A. Characterization of prmt7alpha and beta isozymes from Chinese hamster cells sensitive and resistant to topoisomerase II inhibitors. Biochim. Biophys. Acta 1760 (2006) 1646-1656
46. Guccione E., Bassi C., Casadio F., Martinato F., Cesaroni M., Schuchlautz H., Luscher B., and Amati B. Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449 (2007) 933-937
47. Higashimoto K., Kuhn P., Desai D., Cheng X., and Xu W. Phosphorylation-mediated inactivation of coactivator-associated arginine methyltransferase 1. Proc. Natl. Acad. Sci. USA 104 (2007) 12318-12323
48. Hong H., Kao C., Jeng M.H., Eble J.N., Koch M.O., Gardner T.A., Zhang S., Li L., Pan C.X., Hu Z., et al. Aberrant expression of CARM1, a transcriptional coactivator of androgen receptor, in the development of prostate carcinoma and androgen-independent status. Cancer 101 (2004) 83-89
49. Hou Z., Peng H., Ayyanathan K., Yan K.P., Langer E.M., Longmore G.D., and Rauscher III F.J. The LIM protein AJUBA recruits protein arginine methyltransferase 5 to mediate SNAIL-dependent transcriptional repression. Mol. Cell. Biol. 28 (2008) 3198-3207
50. Hsieh C.H., and Tam M.F. Detection of dimethylarginines in protein hydrolysates by matrix-assisted laser desorption/ionization mass spectrometry. Anal. Biochem. 350 (2006) 151-155
51. Hughes R.M., and Waters M.L. Arginine methylation in a beta-hairpin peptide: implications for Arg-pi interactions, DeltaCp(o), and the cold denatured state. J. Am. Chem. Soc. 128 (2006) 12735-12742
52. Hung C.J., Chen D.H., Shen Y.T., Li Y.C., Lin Y.W., Hsieh M., and Li C. Characterization of protein arginine methyltransferases in porcine brain. J. Biochem. Mol. Biol. 40 (2007) 617-624
53. Hyllus D., Stein C., Schnabel K., Schiltz E., Imhof A., Dou Y., Hsieh J., and Bauer U.M. PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev. 21 (2007) 3369-3380
54. Iacovides D.C., O'Shea C.C., Oses-Prieto J., Burlingame A., and McCormick F. Critical role for arginine methylation in adenovirus-infected cells. J. Virol. 81 (2007) 13209-13217
55. Iberg A.N., Espejo A., Cheng D., Kim D., Michaud-Levesque J., Richard S., and Bedford M.T. Arginine methylation of the histone h3 tail impedes effector binding. J. Biol. Chem. 283 (2008) 3006-3010
56. Iwasaki H., and Yada T. Protein arginine methylation regulates insulin signaling in L6 skeletal muscle cells. Biochem. Biophys. Res. Commun. 364 (2007) 1015-1021
57. Jelinic P., Stehle J.C., and Shaw P. The testis-specific factor CTCFL cooperates with the protein methyltransferase PRMT7 in H19 imprinting control region methylation. PLoS Biol. 4 (2006) e355 10.1371/journal.pbio.0040355
58. Katz J.E., Dlakic M., and Clarke S. Automated identification of putative methyltransferases from genomic open reading frames. Mol. Cell. Proteomics 2 (2003) 525-540
59. Kim J., Daniel J., Espejo A., Lake A., Krishna M., Xia L., Zhang Y., and Bedford M.T. Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep. 7 (2006) 397-403
60. Kim J.M., Sohn H.Y., Yoon S.Y., Oh J.H., Yang J.O., Kim J.H., Song K.S., Rho S.M., Yoo H.S., Kim Y.S., et al. Identification of gastric cancer-related genes using a cDNA microarray containing novel expressed sequence tags expressed in gastric cancer cells. Clin. Cancer Res. 11 (2005) 473-482
61. Kleinschmidt M.A., Streubel G., Samans B., Krause M., and Bauer U.M. The protein arginine methyltransferases CARM1 and PRMT1 cooperate in gene regulation. Nucleic Acids Res. 36 (2008) 3202-3213
62. Krause C.D., Yang Z.H., Kim Y.S., Lee J.H., Cook J.R., and Pestka S. Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol. Ther. 113 (2007) 50-87
63. Lacroix M., Messaoudi S.E., Rodier G., Le Cam A., Sardet C., and Fabbrizio E. The histone-binding protein COPR5 is required for nuclear functions of the protein arginine methyltransferase PRMT5. EMBO Rep. 9 (2008) 452-458
64. Lakowski T.M., and Frankel A. A kinetic study of human protein arginine N-methyltransferase 6 reveals a distributive mechanism. J. Biol. Chem. 283 (2008) 10015-10025
65. Le Romancer M., Treilleux I., Leconte N., Robin-Lespinasse Y., Sentis S., Bouchekioua-Bouzaghou K., Goddard S., Gobert-Gosse S., and Corbo L. Regulation of estrogen rapid signaling through arginine methylation by PRMT1. Mol. Cell 31 (2008) 212-221
66. Lee D.Y., Ianculescu I., Purcell D., Zhang X., Cheng X., and Stallcup M.R. Surface-scanning mutational analysis of protein arginine methyltransferase 1: roles of specific amino acids in methyltransferase substrate specificity, oligomerization, and coactivator function. Mol. Endocrinol. 21 (2007) 1381-1393
67. Lee J., and Bedford M.T. PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays. EMBO Rep. 3 (2002) 268-273
68. Lee J., Sayegh J., Daniel J., Clarke S., and Bedford M.T. PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J. Biol. Chem. 280 (2005) 32890-32896
69. Lee J.H., Cook J.R., Yang Z.H., Mirochnitchenko O., Gunderson S.I., Felix A.M., Herth N., Hoffmann R., and Pestka S. PRMT7, a new protein arginine methyltransferase that synthesizes symmetric dimethylarginine. J. Biol. Chem. 280 (2005) 3656-3664
70. Lee Y.H., Coonrod S.A., Kraus W.L., Jelinek M.A., and Stallcup M.R. Regulation of coactivator complex assembly and function by protein arginine methylation and demethylimination. Proc. Natl. Acad. Sci. USA 102 (2005) 3611-3616
71. Leiper J., Nandi M., Torondel B., Murray-Rust J., Malaki M., O'Hara B., Rossiter S., Anthony S., Madhani M., Selwood D., et al. Disruption of methylarginine metabolism impairs vascular homeostasis. Nat. Med. 13 (2007) 198-203
72. Lin W.J., Gary J.D., Yang M.C., Clarke S., and Herschman H.R. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J. Biol. Chem. 271 (1996) 15034-15044
73. Liu Z., Zhou Z., Chen G., and Bao S. A putative transcriptional elongation factor hIws1 is essential for mammalian cell proliferation. Biochem. Biophys. Res. Commun. 353 (2007) 47-53
74. Luscombe N.M., Laskowski R.A., and Thornton J.M. Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res. 29 (2001) 2860-2874
75. Majumder S., Liu Y., Ford III O.H., Mohler J.L., and Whang Y.E. Involvement of arginine methyltransferase CARM1 in androgen receptor function and prostate cancer cell viability. Prostate 66 (2006) 1292-1301
76. Meyer R., Wolf S.S., and Obendorf M. PRMT2, a member of the protein arginine methyltransferase family, is a coactivator of the androgen receptor. J. Steroid Biochem. Mol. Biol. 107 (2007) 1-14
77. Miranda T.B., Miranda M., Frankel A., and Clarke S. PRMT7 is a member of the protein arginine methyltransferase family with a distinct substrate specificity. J. Biol. Chem. 279 (2004) 22902-22907
78. Miranda T.B., Webb K.J., Edberg D.D., Reeves R., and Clarke S. Protein arginine methyltransferase 6 specifically methylates the nonhistone chromatin protein HMGA1a. Biochem. Biophys. Res. Commun. 336 (2005) 831-835
79. Mitchell J.B., Thornton J.M., Singh J., and Price S.L. Towards an understanding of the arginine-aspartate interaction. J. Mol. Biol. 226 (1992) 251-262
80. Naeem H., Cheng D., Zhao Q., Underhill C., Tini M., Bedford M.T., and Torchia J. The activity and stability of the transcriptional coactivator p/CIP/SRC-3 are regulated by CARM1-dependent methylation. Mol. Cell. Biol. 27 (2007) 120-134
81. Najbauer J., Johnson B.A., Young A.L., and Aswad D.W. 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 (1993) 10501-10509
82. Nakashima K., Hagiwara T., and Yamada M. Nuclear localization of peptidylarginine deiminase V and histone deimination in granulocytes. J. Biol. Chem. 277 (2002) 49562-49568
83. Neuenkirchen N., Chari A., and Fischer U. Deciphering the assembly pathway of Sm-class U snRNPs. FEBS Lett. 582 (2008) 1997-2003
84. Nishioka K., and Reinberg D. Methods and tips for the purification of human histone methyltransferases. Methods 31 (2003) 49-58
85. Ohkura N., Takahashi M., Yaguchi H., Nagamura Y., and Tsukada T. Coactivator-associated arginine methyltransferase 1, CARM1, affects pre-mRNA splicing in an isoform-specific manner. J. Biol. Chem. 280 (2005) 28927-28935
86. Osborne T.C., Obianyo O., Zhang X., Cheng X., and Thompson P.R. Protein arginine methyltransferase 1: positively charged residues in substrate peptides distal to the site of methylation are important for substrate binding and catalysis. Biochemistry 46 (2007) 13370-13381
87. Pahlich S., Zakaryan R.P., and Gehring H. Protein arginine methylation: Cellular functions and methods of analysis. Biochim. Biophys. Acta 1764 (2006) 1890-1903
88. Pahlich S., Zakaryan R.P., and Gehring H. Identification of proteins interacting with protein arginine methyltransferase 8: the Ewing sarcoma (EWS) protein binds independent of its methylation state. Proteins 72 (2008) 1125-1137
89. Paik W.K., and Kim S. Natural occurrence of various methylated amino acid derivatives. In: Meister A. (Ed). Protein Methylation (1980), John Wiley & Sons, New York 8-25
90. Pal S., Baiocchi R.A., Byrd J.C., Grever M.R., Jacob S.T., and Sif S. Low levels of miR-92b/96 induce PRMT5 translation and H3R8/H4R3 methylation in mantle cell lymphoma. EMBO J. 26 (2007) 3558-3569
91. Pal S., Vishwanath S.N., Erdjument-Bromage H., Tempst P., and Sif S. Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol. Cell. Biol. 24 (2004) 9630-9645
92. Pal S., Yun R., Datta A., Lacomis L., Erdjument-Bromage H., Kumar J., Tempst P., and Sif S. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol. 23 (2003) 7475-7487
93. Pesavento J.J., Bullock C.R., LeDuc R.D., Mizzen C.A., and Kelleher N.L. Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J. Biol. Chem. 283 (2008) 14927-14937
94. Pintucci G., Quarto N., and Rifkin D.B. Methylation of high molecular weight fibroblast growth factor-2 determines post-translational increases in molecular weight and affects its intracellular distribution. Mol. Biol. Cell 7 (1996) 1249-1258
95. Raijmakers R., Zendman A.J., Egberts W.V., Vossenaar E.R., Raats J., Soede-Huijbregts C., Rutjes F.P., van Veelen P.A., Drijfhout J.W., and Pruijn G.J. Methylation of arginine residues interferes with citrullination by peptidylarginine deiminases in vitro. J. Mol. Biol. 367 (2007) 1118-1129
96. Ramon-Maiques S., Kuo A.J., Carney D., Matthews A.G., Oettinger M.A., Gozani O., and Yang W. The plant homeodomain finger of RAG2 recognizes histone H3 methylated at both lysine-4 and arginine-2. Proc. Natl. Acad. Sci. USA 104 (2007) 18993-18998
97. Rathert P., Dhayalan A., Murakami M., Zhang X., Tamas R., Jurkowska R., Komatsu Y., Shinkai Y., Cheng X., and Jeltsch A. Protein lysine methyltransferase G9a acts on non-histone targets. Nat. Chem. Biol. 4 (2008) 344-346
98. Richard S., Morel M., and Cleroux P. Arginine methylation regulates IL-2 gene expression: a role for protein arginine methyltransferase 5 (PRMT5). Biochem. J. 388 (2005) 379-386
99. Robin-Lespinasse Y., Sentis S., Kolytcheff C., Rostan M.C., Corbo L., and Le Romancer M. hCAF1, a new regulator of PRMT1-dependent arginine methylation. J. Cell Sci. 120 (2007) 638-647
100. Sayegh J., Webb K., Cheng D., Bedford M.T., and Clarke S.G. Regulation of protein arginine methyltransferase 8 (PRMT8) activity by its N-terminal domain. J. Biol. Chem. 282 (2007) 36444-36453
101. Sgarra R., Lee J., Tessari M.A., Altamura S., Spolaore B., Giancotti V., Bedford M.T., and Manfioletti G. The AT-hook of the chromatin architectural transcription factor high mobility group A1a is arginine-methylated by protein arginine methyltransferase 6. J. Biol. Chem. 281 (2006) 3764-3772
102. Shen E.C., Henry M.F., Weiss V.H., Valentini S.R., Silver P.A., and Lee M.S. Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev. 12 (1998) 679-691
103. Singh V., Miranda T.B., Jiang W., Frankel A., Roemer M.E., Robb V.A., Gutmann D.H., Herschman H.R., Clarke S., and Newsham I.F. DAL-1/4.1B tumor suppressor interacts with protein arginine N-methyltransferase 3 (PRMT3) and inhibits its ability to methylate substrates in vitro and in vivo. Oncogene 23 (2004) 7761-7771
104. Sprangers R., Groves M.R., Sinning I., and Sattler M. High-resolution X-ray and NMR structures of the SMN Tudor domain: conformational variation in the binding site for symmetrically dimethylated arginine residues. J. Mol. Biol. 327 (2003) 507-520
105. Swiercz R., Cheng D., Kim D., and Bedford M.T. Ribosomal protein rpS2 is hypomethylated in PRMT3-deficient mice. J. Biol. Chem. 282 (2007) 16917-16923
106. Tadesse H., Deschenes-Furry J., Boisvenue S., and Cote J. KH-type splicing regulatory protein interacts with survival motor neuron protein and is misregulated in spinal muscular atrophy. Hum. Mol. Genet. 17 (2008) 506-524
107. Tang J., Frankel A., Cook R.J., Kim S., Paik W.K., Williams K.R., Clarke S., and Herschman H.R. PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J. Biol. Chem. 275 (2000) 7723-7730
108. Taverna S.D., Li H., Ruthenburg A.J., Allis C.D., and Patel D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14 (2007) 1025-1040
109. Thompson P.R., and Fast W. Histone citrullination by protein arginine deiminase: is arginine methylation a green light or a roadblock?. ACS Chem. Biol. 1 (2006) 433-441
110. Troffer-Charlier N., Cura V., Hassenboehler P., Moras D., and Cavarelli J. Functional insights from structures of coactivator-associated arginine methyltransferase 1 domains. EMBO J. 26 (2007) 4391-4401
111. Verbiest V., Montaudon D., Tautu M.T., Moukarzel J., Portail J.P., Markovits J., Robert J., Ichas F., and Pourquier P. Protein arginine (N)-methyl transferase 7 (PRMT7) as a potential target for the sensitization of tumor cells to camptothecins. FEBS Lett. 582 (2008) 1483-1489
112. Willemsen N.M., Hitchen E.M., Bodetti T.J., Apolloni A., Warrilow D., Piller S.C., and Harrich D. Protein methylation is required to maintain optimal HIV-1 infectivity. Retrovirology 3 (2006) 92
113. Xu W., Cho H., Kadam S., Banayo E.M., Anderson S., Yates III J.R., Emerson B.M., and Evans R.M. A methylation-mediator complex in hormone signaling. Genes Dev. 18 (2004) 144-156
114. Yadav N., Cheng D., Richard S., Morel M., Iyer V.R., Aldaz C.M., and Bedford M.T. CARM1 promotes adipocyte differentiation by coactivating PPARgamma. EMBO Rep. 9 (2008) 193-198
115. Yadav N., Lee J., Kim J., Shen J., Hu M.C., Aldaz C.M., and Bedford M.T. Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice. Proc. Natl. Acad. Sci. USA 100 (2003) 6464-6468
116. Yamagata K., Daitoku H., Takahashi Y., Namiki K., Hisatake K., Kako K., Mukai H., Kasuya Y., and Fukamizu A. Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol. Cell 32 (2008) 221-231
117. Yue W.W., Hassler M., Roe S.M., Thompson-Vale V., and Pearl L.H. Insights into histone code syntax from structural and biochemical studies of CARM1 methyltransferase. EMBO J. 26 (2007) 4402-4412
118. Zhang X., and Cheng X. Structure of the Predominant Protein Arginine Methyltransferase PRMT1 and Analysis of Its Binding to Substrate Peptides. Structure 11 (2003) 509-520
119. Zhao X., Jankovic V., Gural A., Huang G., Pardanani A., Menendez S., Zhang J., Dunne R., Xiao A., Erdjument-Bromage H., et al. Methylation of RUNX1 by PRMT1 abrogates SIN3A binding and potentiates its transcriptional activity. Genes Dev. 22 (2008) 640-653
120. Zheng Z., Schmidt-Ott K.M., Chua S., Foster K.A., Frankel R.Z., Pavlidis P., Barasch J., D'Agati V.D., and Gharavi A.G. A Mendelian locus on chromosome 16 determines susceptibility to doxorubicin nephropathy in the mouse. Proc. Natl. Acad. Sci. USA 102 (2005) 2502-2507