Chapter 9 Protein Arginine Methyltransferases. Nuclear Receptor Coregulators and Beyond

Progress in Molecular Biology and Translational Science

Volumn 87, Issue C, 2009, Pages 299-342

  Kuhn, Peter ^a   Xu, Wei ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; ENZYME INHIBITOR; PROTEIN ARGININE METHYLTRANSFERASE;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; METABOLISM; MOLECULAR GENETICS; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN-ARGININE N-METHYLTRANSFERASES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTION, GENETIC;

EID: 77957036307     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1877-1173(09)87009-9     Document Type: Review

References (187)

1. Martin J.L., and McMillan F.M. SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold. Curr Opin Struct Biol 12 (2002) 783 93
2. Bedford M.T. Arginine methylation at a glance. J Cell Sci 120 (2007) 4243 6
3. Katz J.E., Dlakic M., and Clarke S. Automated identification of putative methyltransferases from genomic open reading frames. Mol Cell Proteomics 2 (2003) 525 40
4. Schubert H.L., Blumenthal R.M., and Cheng X. Many paths to methyltransfer: a chronicle of convergence. Trends Biochem Sci 28 (2003) 329 35
5. Kagan R.M., and Clarke S. Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch Biochem Biophys 310 (1994) 417 27
6. 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
7. Paik W.K., and Kim S. Enzymatic methylation of protein fractions from calf thymus nuclei. Biochem Biophys Res Commun 29 (1967) 14-20
8. 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 44
9. Bachand F. Protein arginine methyltransferases: from unicellular eukaryotes to humans. Eukaryot Cell 6 (2007) 889 98
10. Niewmierzycka A., and Clarke S. S-Adenosylmethionine-dependent methylation in Saccharomyces cerevisiae Identification of a novel protein arginine methyltransferase. J Biol Chem 274 (1999) 814 24
11. Scebba F., De Bastiani M., Bernacchia G., Andreucci A., Galli A., and Pitto L. PRMT11: a new Arabidopsis MBD7 protein partner with arginine methyltransferase activity. Plant J 52 (2007) 210 22
12. Boulanger M.C., Miranda T.B., Clarke S., Di Fruscio M., Suter B., Lasko P., et al. Characterization of the Drosophila protein arginine methyltransferases DART1 and DART4. Biochem J 379 (2004) 283 9
13. 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
14. 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 43
15. 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 9
16. Kiledjian M., and Dreyfuss G. Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J 11 (1992) 2655 64
17. Wooderchak W.L., Zang T., Zhou Z.S., Acuna M., Tahara S.M., and Hevel J.M. Substrate profiling of PRMT1 reveals amino acid sequences that extend beyond the "RGG" paradigm. Biochemistry 47 (2008) 9456 66
18. Smith J.J., Rucknagel K.P., Schierhorn A., Tang J., Nemeth A., Linder M., et al. Unusual sites of arginine methylation in Poly(A)-binding protein II and in vitro methylation by protein arginine methyltransferases PRMT1 and PRMT3. J Biol Chem 274 (1999) 13229 34
19. Zhao X., Jankovic V., Gural A., Huang G., Pardanani A., Menendez S., et al. Methylation of RUNX1 by PRMT1 abrogates SIN3A binding and potentiates its transcriptional activity. Genes Dev 22 (2008) 640 53
20. Mowen K.A., Tang J., Zhu W., Schurter B.T., Shuai K., Herschman H.R., et al. Arginine methylation of STAT1 modulates IFNalpha/beta-induced transcription. Cell 104 (2001) 731 41
21. Teyssier C., Ma H., Emter R., Kralli A., and Stallcup M.R. Activation of nuclear receptor coactivator PGC-1alpha by arginine methylation. Genes Dev 19 (2005) 1466 73
22. Tang J., Frankel A., Cook R.J., Kim S., Paik W.K., Williams K.R., et al. PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J Biol Chem 275 (2000) 7723 30
23. Tang J., Gary J.D., Clarke S., and Herschman H.R. 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 (1998) 16935 45
24. 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 82
25. Bachand F., and Silver P.A. PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. EMBO J 23 (2004) 2641 50
26. 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 23
27. Singh V., Miranda T.B., Jiang W., Frankel A., Roemer M.E., Robb V.A., et al. 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 71
28. Chen D., Ma H., Hong H., Koh S.S., Huang S.M., Schurter B.T., et al. Regulation of transcription by a protein methyltransferase. Science 284 (1999) 2174 7
29. Schurter B.T., Koh S.S., Chen D., Bunick G.J., Harp J.M., Hanson B.L., et al. Methylation of histone H3 by coactivator-associated arginine methyltransferase 1. Biochemistry 40 (2001) 5747 56
30. Hong H., Kao C., Jeng M.H., Eble J.N., Koch M.O., Gardner T.A., 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 9
31. Guccione E., Bassi C., Casadio F., Martinato F., Cesaroni M., Schuchlautz H., et al. Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449 (2007) 933 7
32. Sgarra R., Lee J., Tessari M.A., Altamura S., Spolaore B., Giancotti V., et al. 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 72
33. Invernizzi C.F., Xie B., Richard S., and Wainberg M.A. PRMT6 diminishes HIV-1 Rev binding to and export of viral RNA. Retrovirology 3 (2006) 93
34. Aubert J., Stavridis M.P., Tweedie S., O'Reilly M., Vierlinger K., Li M., et al. Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc Natl Acad Sci USA 100 Suppl 1 (2003) 11836 41
35. 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 6
36. Taneda T., Miyata S., Kousaka A., Inoue K., Koyama Y., Mori Y., et al. Specific regional distribution of protein arginine methyltransferase 8 (PRMT8) in the mouse brain. Brain Res 1155 (2007) 1-9
37. 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 53
38. 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 37
39. Pollack B.P., Kotenko S.V., He W., Izotova L.S., Barnoski B.L., and Pestka S. The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J Biol Chem 274 (1999) 31531 42
40. Branscombe T.L., Frankel A., Lee J.H., Cook J.R., Yang Z., Pestka S., et al. PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J Biol Chem 276 (2001) 32971 6
41. Teng Y., Girvan A.C., Casson L.K., Pierce Jr. W.M., Qian M., Thomas S.D., et al. AS1411 alters the localization of a complex containing protein arginine methyltransferase 5 and nucleolin. Cancer Res 67 (2007) 10491 500
42. Liang J.J., Wang Z., Chiriboga L., Greco M.A., Shapiro E., Huang H., et al. The expression and function of androgen receptor coactivator p44 and protein arginine methyltransferase 5 in the developing testis and testicular tumors. J Urol 177 (2007) 1918 22
43. Friesen W.J., Wyce A., Paushkin S., Abel L., Rappsilber J., Mann M., et al. A novel WD repeat protein component of the methylosome binds Sm proteins. J Biol Chem 277 (2002) 8243 7
44. Pal S., Yun R., Datta A., Lacomis L., Erdjument-Bromage H., Kumar J., et al. 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 87
45. 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 45
46. Kwak Y.T., Guo J., Prajapati S., Park K.J., Surabhi R.M., Miller B., et al. Methylation of SPT5 regulates its interaction with RNA polymerase II and transcriptional elongation properties. Mol Cell 11 (2003) 1055 66
47. 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 7
48. Lee J.H., Cook J.R., Yang Z.H., Mirochnitchenko O., Gunderson S.I., Felix A.M., et al. PRMT7, a new protein arginine methyltransferase that synthesizes symmetric dimethylarginine. J Biol Chem 280 (2005) 3656 64
49. Sayegh J., and Clarke S.G. Hsl7 is a substrate-specific type II protein arginine methyltransferase in yeast. Biochem Biophys Res Commun 372 (2008) 811 5
50. Cook J.R., Lee J.H., Yang Z.H., Krause C.D., Herth N., Hoffmann R., et al. FBXO11/PRMT9, a new protein arginine methyltransferase, symmetrically dimethylates arginine residues. Biochem Biophys Res Commun 342 (2006) 472 81
51. Katsanis N., Yaspo M.L., and Fisher E.M. Identification and mapping of a novel human gene, HRMT1L1, homologous to the rat protein arginine N-methyltransferase 1 (PRMT1) gene. Mamm Genome 8 (1997) 526 9
52. Scott H.S., Antonarakis S.E., Lalioti M.D., Rossier C., Silver P.A., and Henry M.F. Identification and characterization of two putative human arginine methyltransferases (HRMT1L1 and HRMT1L2). Genomics 48 (1998) 330 40
53. Qi C., Chang J., Zhu Y., Yeldandi A.V., Rao S.M., and Zhu Y.J. Identification of protein arginine methyltransferase 2 as a coactivator for estrogen receptor alpha. J Biol Chem 277 (2002) 28624 30
54. 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
55. Bedford M.T. The family of protein arginine methyltransferases (2006), Academic Press, Amsterdam
56. 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 81
57. Obianyo O., Osborne T.C., and Thompson P.R. Kinetic mechanism of protein arginine methyltransferase 1. Biochemistry 47 (2008) 10420 7
58. 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 25
59. Osborne T., Roska R.L., Rajski S.R., and Thompson P.R. In situ generation of a bisubstrate analogue for protein arginine methyltransferase 1. J Am Chem Soc 130 (2008) 4574 5
60. 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 93
61. 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 12
62. Rho J., Choi S., Seong Y.R., Cho W.K., Kim S.H., and Im D.S. Prmt5, which forms distinct homo-oligomers, is a member of the protein-arginine methyltransferase family. J Biol Chem 276 (2001) 11393 401
63. 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 69
64. Wang H., Huang Z.Q., Xia L., Feng Q., Erdjument-Bromage H., Strahl B.D., et al. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 293 (2001) 853 7
65. Pahlich S., Bschir K., Chiavi C., Belyanskaya L., and Gehring H. Different methylation characteristics of protein arginine methyltransferase 1 and 3 toward the Ewing Sarcoma protein and a peptide. Proteins 61 (2005) 164 75
66. Fronz K., Otto S., Kolbel K., Kuhn U., Friedrich H., Schierhorn A., et al. Promiscuous modification of the nuclear poly(A)-binding protein by multiple protein-arginine methyltransferases does not affect the aggregation behavior. J Biol Chem 283 (2008) 20408 20
67. 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 47
68. Miyata S., Mori Y., and Tohyama M. PRMT1 and Btg2 regulates neurite outgrowth of Neuro2a cells. Neurosci Lett 445 (2008) 162 5
69. Choi S., Jung C.R., Kim J.Y., and Im D.S. PRMT3 inhibits ubiquitination of ribosomal protein S2 and together forms an active enzyme complex. Biochim Biophys Acta 1780 (2008) 1062 9
70. 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
71. Xu W., Chen H., Du K., Asahara H., Tini M., Emerson B.M., et al. A transcriptional switch mediated by cofactor methylation. Science 294 (2001) 2507 11
72. 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 23
73. Allfrey V.G., Faulkner R., and Mirsky A.E. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 51 (1964) 786 94
74. Berger S.L. The complex language of chromatin regulation during transcription. Nature 447 (2007) 407 12
75. Sims III R.J., and Reinberg D. Is there a code embedded in proteins that is based on post-translational modifications?. Nat Rev Mol Cell Biol 9 (2008) 815 20
76. Stallcup M.R. Role of protein methylation in chromatin remodeling and transcriptional regulation. Oncogene 20 (2001) 3014 20
77. Wysocka J., Allis C.D., and Coonrod S. Histone arginine methylation and its dynamic regulation. Front Biosci 11 (2006) 344 55
78. Strahl B.D., Briggs S.D., Brame C.J., Caldwell J.A., Koh S.S., Ma H., et al. Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr Biol 11 (2001) 996-1000
79. Ma H., Baumann C.T., Li H., Strahl B.D., Rice R., Jelinek M.A., et al. Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter. Curr Biol 11 (2001) 1981 5
80. Huang S., Litt M., and Felsenfeld G. Methylation of histone H4 by arginine methyltransferase PRMT1 is essential in vivo for many subsequent histone modifications. Genes Dev 19 (2005) 1885 93
81. Wagner S., Weber S., Kleinschmidt M.A., Nagata K., and Bauer U.M. SET-mediated promoter hypoacetylation is a prerequisite for coactivation of the estrogen-responsive pS2 gene by PRMT1. J Biol Chem 281 (2006) 27242 50
82. Miao F., Li S., Chavez V., Lanting L., and Natarajan R. Coactivator-associated arginine methyltransferase-1 enhances nuclear factor-kappaB-mediated gene transcription through methylation of histone H3 at arginine 17. Mol Endocrinol 20 (2006) 1562 73
83. El Messaoudi S., Fabbrizio E., Rodriguez C., Chuchana P., Fauquier L., Cheng D., et al. Coactivator-associated arginine methyltransferase 1 (CARM1) is a positive regulator of the Cyclin E1 gene. Proc Natl Acad Sci USA 103 (2006) 13351 6
84. Daujat S., Bauer U.M., Shah V., Turner B., Berger S., and Kouzarides T. Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr Biol 12 (2002) 2090 7
85. An W., Kim J., and Roeder R.G. Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117 (2004) 735 48
86. Hyllus D., Stein C., Schnabel K., Schiltz E., Imhof A., Dou Y., et al. PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev 21 (2007) 3369 80
87. Iberg A.N., Espejo A., Cheng D., Kim D., Michaud-Levesque J., Richard S., et al. Arginine methylation of the histone H3 tail impedes effector binding. J Biol Chem 283 (2008) 3006 10
88. Fabbrizio E., El Messaoudi S., Polanowska J., Paul C., Cook J.R., Lee J.H., et al. Negative regulation of transcription by the type II arginine methyltransferase PRMT5. EMBO Rep 3 (2002) 641 5
89. 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 94
90. Hosohata K., Li P., Hosohata Y., Qin J., Roeder R.G., and Wang Z. Purification and identification of a novel complex which is involved in androgen receptor-dependent transcription. Mol Cell Biol 23 (2003) 7019 29
91. 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 86
92. Ancelin K., Lange U.C., Hajkova P., Schneider R., Bannister A.J., Kouzarides T., et al. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8 (2006) 623 30
93. Wang Y., Wysocka J., Sayegh J., Lee Y.H., Perlin J.R., Leonelli L., et al. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306 (2004) 279 83
94. Cuthbert G.L., Daujat S., Snowden A.W., Erdjument-Bromage H., Hagiwara T., Yamada M., et al. Histone deimination antagonizes arginine methylation. Cell 118 (2004) 545 53
95. 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 6
96. Chang B., Chen Y., Zhao Y., and Bruick R.K. JMJD6 is a histone arginine demethylase. Science 318 (2007) 444 7
97. Garcia B.A., Pesavento J.J., Mizzen C.A., and Kelleher N.L. Pervasive combinatorial modification of histone H3 in human cells. Nat Methods 4 (2007) 487 9
98. Xu W., Cho H., and Evans R.M. Acetylation and methylation in nuclear receptor gene activation. Methods Enzymol 364 (2003) 205 23
99. Koh S.S., Chen D., Lee Y.H., and Stallcup M.R. Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities. J Biol Chem 276 (2001) 1089 98
100. Lee Y.H., Koh S.S., Zhang X., Cheng X., and Stallcup M.R. Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol Cell Biol 22 (2002) 3621 32
101. Zhao X., and Benveniste E.N. Transcriptional activation of human matrix metalloproteinase-9 gene expression by multiple co-activators. J Mol Biol 383 (2008) 945 56
102. Teyssier C., Chen D., and Stallcup M.R. Requirement for multiple domains of the protein arginine methyltransferase CARM1 in its transcriptional coactivator function. J Biol Chem 277 (2002) 46066 72
103. Chevillard-Briet M., Trouche D., and Vandel L. Control of CBP co-activating activity by arginine methylation. EMBO J 21 (2002) 5457 66
104. Demarest S.J., Martinez-Yamout M., Chung J., Chen H., Xu W., Dyson H.J., et al. Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415 (2002) 549 53
105. Koh S.S., Li H., Lee Y.H., Widelitz R.B., Chuong C.M., and Stallcup M.R. Synergistic coactivator function by coactivator-associated arginine methyltransferase (CARM) 1 and beta-catenin with two different classes of DNA-binding transcriptional activators. J Biol Chem 277 (2002) 26031 5
106. 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 57
107. Naeem H., Cheng D., Zhao Q., Underhill C., Tini M., Bedford M.T., et al. The activity and stability of the transcriptional coactivator p/CIP/SRC-3 are regulated by CARM1-dependent methylation. Mol Cell Biol 27 (2007) 120 34
108. Xu W., Cho H., Kadam S., Banayo E.M., Anderson S., Yates III J.R., et al. A methylation-mediator complex in hormone signaling. Genes Dev 18 (2004) 144 56
109. Teyssier C., Ou C.Y., Khetchoumian K., Losson R., and Stallcup M.R. Transcriptional intermediary factor 1alpha mediates physical interaction and functional synergy between the coactivator-associated arginine methyltransferase 1 and glucocorticoid receptor-interacting protein 1 nuclear receptor coactivators. Mol Endocrinol 20 (2006) 1276 86
110. Lee Y.H., Campbell H.D., and Stallcup M.R. Developmentally essential protein flightless I is a nuclear receptor coactivator with actin binding activity. Mol Cell Biol 24 (2004) 2103 17
111. Thompson M. Polybromo-1: The chromatin targeting subunit of the PBAF complex. Biochimie 31 (2008) 309 19
112. Chen Y.H., Kim J.H., and Stallcup M.R. GAC63, a GRIP1-dependent nuclear receptor coactivator. Mol Cell Biol 25 (2005) 5965 72
113. Kim J.H., Li H., and Stallcup M.R. CoCoA, a nuclear receptor coactivator which acts through an N-terminal activation domain of p160 coactivators. Mol Cell 12 (2003) 1537 49
114. Kim J.H., Yang C.K., and Stallcup M.R. Downstream signaling mechanism of the C-terminal activation domain of transcriptional coactivator CoCoA. Nucleic Acids Res 34 (2006) 2736 50
115. Lee D.Y., Northrop J.P., Kuo M.H., and Stallcup M.R. Histone H3 lysine 9 methyltransferase G9a is a transcriptional coactivator for nuclear receptors. J Biol Chem 281 (2006) 8476 85
116. Choi H.K., Choi K.C., Oh S.Y., Kang H.B., Lee Y.H., Haam S., et al. The functional role of the CARM1-SNF5 complex and its associated HMT activity in transcriptional activation by thyroid hormone receptor. Exp Mol Med 39 (2007) 544 55
117. Barrero M.J., and Malik S. Two functional modes of a nuclear receptor-recruited arginine methyltransferase in transcriptional activation. Mol Cell 24 (2006) 233 43
118. Rizzo G., Renga B., Antonelli E., Passeri D., Pellicciari R., and Fiorucci S. The methyl transferase PRMT1 functions as co-activator of farnesoid X receptor (FXR)/9-cis retinoid X receptor and regulates transcription of FXR responsive genes. Mol Pharmacol 68 (2005) 551 8
119. Ananthanarayanan M., Li S., Balasubramaniyan N., Suchy F.J., and Walsh M.J. Ligand-dependent activation of the farnesoid X-receptor directs arginine methylation of histone H3 by CARM1. J Biol Chem 279 (2004) 54348 57
120. Le Romancer M., Treilleux I., Leconte N., Robin-Lespinasse Y., Sentis S., Bouchekioua-Bouzaghou K., et al. Regulation of estrogen rapid signaling through arginine methylation by PRMT1. Mol Cell 31 (2008) 212 21
121. Yamagata K., Daitoku H., Takahashi Y., Namiki K., Hisatake K., Kako K., et al. Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol Cell 32 (2008) 221 31
122. Chen S.L., Loffler K.A., Chen D., Stallcup M.R., and Muscat G.E. The coactivator-associated arginine methyltransferase is necessary for muscle differentiation: CARM1 coactivates myocyte enhancer factor-2. J Biol Chem 277 (2002) 4324 33
123. Fauquier L., Duboe C., Jore C., Trouche D., and Vandel L. Dual role of the arginine methyltransferase CARM1 in the regulation of c-Fos target genes. FASEB J 22 (2008) 3337 47
124. Tabata T., Kokura K., Ten Dijke P., and Ishii S. Ski co-repressor complexes maintain the basal repressed state of the TGF-beta target gene, SMAD7, via HDAC3 and PRMT5. Genes Cells (2008)
125. Furuno K., Masatsugu T., Sonoda M., Sasazuki T., and Yamamoto K. Association of Polycomb group SUZ12 with WD-repeat protein MEP50 that binds to histone H2A selectively in vitro. Biochem Biophys Res Commun 345 (2006) 1051 8
126. Hou Z., Peng H., Ayyanathan K., Yan K.P., Langer E.M., Longmore G.D., et al. The LIM protein AJUBA recruits protein arginine methyltransferase 5 to mediate SNAIL-dependent transcriptional repression. Mol Cell Biol 28 (2008) 3198 207
127. Langer E.M., Feng Y., Zhaoyuan H., Rauscher III F.J., Kroll K.L., and Longmore G.D. Ajuba LIM proteins are snail/slug corepressors required for neural crest development in Xenopus. Dev Cell 14 (2008) 424 36
128. 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 8
129. Jansson M., Durant S.T., Cho E.C., Sheahan S., Edelmann M., Kessler B., et al. Arginine methylation regulates the p53 response. Nat Cell Biol 10 (2008) 1431 9
130. Covic M., Hassa P.O., Saccani S., Buerki C., Meier N.I., Lombardi C., et al. Arginine methyltransferase CARM1 is a promoter-specific regulator of NF-kappaB-dependent gene expression. EMBO J 24 (2005) 85-96
131. Hassa P.O., Covic M., Bedford M.T., and Hottiger M.O. Protein arginine methyltransferase 1 coactivates NF-kappaB-dependent gene expression synergistically with CARM1 and PARP1. J Mol Biol 377 (2008) 668 78
132. Ganesh L., Yoshimoto T., Moorthy N.C., Akahata W., Boehm M., Nabel E.G., et al. Protein methyltransferase 2 inhibits NF-kappaB function and promotes apoptosis. Mol Cell Biol 26 (2006) 3864 74
133. Yoshimoto T., Boehm M., Olive M., Crook M.F., San H., Langenickel T., et al. The arginine methyltransferase PRMT2 binds RB and regulates E2F function. Exp Cell Res 312 (2006) 2040 53
134. 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 6
135. Bres V., Yoh S.M., and Jones K.A. The multi-tasking P-TEFb complex. Curr Opin Cell Biol 20 (2008) 334 40
136. Amente S., Napolitano G., Licciardo P., Monti M., Pucci P., Lania L., et al. Identification of proteins interacting with the RNAPII FCP1 phosphatase: FCP1 forms a complex with arginine methyltransferase PRMT5 and it is a substrate for PRMT5-mediated methylation. FEBS Lett 579 (2005) 683 9
137. Boffa L.C., Karn J., Vidali G., and Allfrey V.G. Distribution of NG, NG,-dimethylarginine in nuclear protein fractions. Biochem Biophys Res Commun 74 (1977) 969 76
138. Liu Q., and Dreyfuss G. In vivo and in vitro arginine methylation of RNA-binding proteins. Mol Cell Biol 15 (1995) 2800 8
139. Rho J., Choi S., Jung C.R., and Im D.S. Arginine methylation of Sam68 and SLM proteins negatively regulates their poly(U) RNA binding activity. Arch Biochem Biophys 466 (2007) 49-57
140. Cote J., Boisvert F.M., Boulanger M.C., Bedford M.T., and Richard S. Sam68 RNA binding protein is an in vivo substrate for protein arginine N-methyltransferase 1. Mol Biol Cell 14 (2003) 274 87
141. Iwasaki H. Involvement of PRMT1 in hnRNPQ activation and internalization of insulin receptor. Biochem Biophys Res Commun 372 (2008) 314 9
142. Swiercz R., Person M.D., and Bedford M.T. Ribosomal protein S2 is a substrate for mammalian PRMT3 (protein arginine methyltransferase 3). Biochem J 386 (2005) 85-91
143. 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
144. Fujiwara T., Mori Y., Chu D.L., Koyama Y., Miyata S., Tanaka H., et al. CARM1 regulates proliferation of PC12 cells by methylating HuD. Mol Cell Biol 26 (2006) 2273 85
145. Meister G., Eggert C., Buhler D., Brahms H., Kambach C., and Fischer U. Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr Biol 11 (2001) 1990 4
146. Weiss V.H., McBride A.E., Soriano M.A., Filman D.J., Silver P.A., and Hogle J.M. The structure and oligomerization of the yeast arginine methyltransferase, Hmt1. Nat Struct Biol 7 (2000) 1165 71
147. 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 401
148. Troffer-Charlier N., Cura V., Hassenboehler P., Moras D., and Cavarelli J. Expression, purification, crystallization and preliminary crystallographic study of isolated modules of the mouse coactivator-associated arginine methyltransferase 1. Acta Crystallogr Sect F Struct Biol Cryst Commun 63 (2007) 330 3
149. 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 20
150. Zhang X., Zhou L., and Cheng X. Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J 19 (2000) 3509 19
151. Min J.R., Wu H., Zeng H., Loppnau P., Sundstrom M., Arrowsmith C.H., et al. Human HMT1 hnRNP methyltransferase-like 3 (S. cerevisiae) protein. Structural Genomics Consortium PDB ID: 2FYT ed (2006)
152. Lin Q., Jiang F., Schultz P.G., and Gray N.S. Design of allele-specific protein methyltransferase inhibitors. J Am Chem Soc 123 (2001) 11608 13
153. Cheng D., Yadav N., King R.W., Swanson M.S., Weinstein E.J., and Bedford M.T. Small molecule regulators of protein arginine methyltransferases. J Biol Chem 279 (2004) 23892 9
154. Spannhoff A., Heinke R., Bauer I., Trojer P., Metzger E., Gust R., et al. Target-based approach to inhibitors of histone arginine methyltransferases. J Med Chem 50 (2007) 2319 25
155. Ragno R., Simeoni S., Castellano S., Vicidomini C., Mai A., Caroli A., et al. Small molecule inhibitors of histone arginine methyltransferases: homology modeling, molecular docking, binding mode analysis, and biological evaluations. J Med Chem 50 (2007) 1241 53
156. Mai A., Cheng D., Bedford M.T., Valente S., Nebbioso A., Perrone A., et al. epigenetic multiple ligands: mixed histone/protein methyltransferase, acetyltransferase, and class III deacetylase (sirtuin) inhibitors. J Med Chem 51 (2008) 2279 90
157. Spannhoff A., Machmur R., Heinke R., Trojer P., Bauer I., Brosch G., et al. A novel arginine methyltransferase inhibitor with cellular activity. Bioorg Med Chem Lett 17 (2007) 4150 3
158. Purandare A.V., Chen Z., Huynh T., Pang S., Geng J., Vaccaro W., et al. Pyrazole inhibitors of coactivator associated arginine methyltransferase 1 (CARM1). Bioorg Med Chem Lett 18 (2008) 4438 41
159. Torres-Padilla M.E., Parfitt D.E., Kouzarides T., and Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445 (2007) 214 8
160. Durcova-Hills G., Tang F., Doody G., Tooze R., and Surani M.A. Reprogramming primordial germ cells into pluripotent stem cells. PLoS ONE 3 (2008) e3531
161. Pawlak M.R., Scherer C.A., Chen J., Roshon M.J., and Ruley H.E. Arginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol Cell Biol 20 (2000) 4859 69
162. Yadav N., Lee J., Kim J., Shen J., Hu M.C., Aldaz C.M., et al. Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice. Proc Natl Acad Sci USA 100 (2003) 6464 8
163. 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 15
164. Kim J., Lee J., Yadav N., Wu Q., Carter C., Richard S., et al. Loss of CARM1 results in hypomethylation of thymocyte cyclic AMP-regulated phosphoprotein and deregulated early T cell development. J Biol Chem 279 (2004) 25339 44
165. Wang L., Pal S., and Sif S. Protein arginine methyltransferase 5 suppresses the transcription of the RB family of tumor suppressors in leukemia and lymphoma cells. Mol Cell Biol 28 (2008) 6262 77
166. Jiang W., Roemer M.E., and Newsham I.F. The tumor suppressor DAL-1/4.1B modulates protein arginine N-methyltransferase 5 activity in a substrate-specific manner. Biochem Biophys Res Commun 329 (2005) 522 30
167. Jiang W., and Newsham I.F. The tumor suppressor DAL-1/4.1B and protein methylation cooperate in inducing apoptosis in MCF-7 breast cancer cells. Mol Cancer 5 (2006) 4
168. 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 301
169. Jeong S.J., Lu H., Cho W.K., Park H.U., Pise-Masison C., and Brady J.N. Coactivator-associated arginine methyltransferase 1 enhances transcriptional activity of the human T-cell lymphotropic virus type 1 long terminal repeat through direct interaction with Tax. J Virol 80 (2006) 10036 44
170. Boulanger M.C., Liang C., Russell R.S., Lin R., Bedford M.T., Wainberg M.A., et al. Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. J Virol 79 (2005) 124 31
171. Xie B., Invernizzi C.F., Richard S., and Wainberg M.A. Arginine methylation of the human immunodeficiency virus type 1 Tat protein by PRMT6 negatively affects Tat Interactions with both cyclin T1 and the Tat transactivation region. J Virol 81 (2007) 4226 34
172. Invernizzi C.F., Xie B., Frankel F.A., Feldhammer M., Roy B.B., Richard S., et al. Arginine methylation of the HIV-1 nucleocapsid protein results in its diminished function. AIDS 21 (2007) 795-805
173. Altschuler L., Wook J.O., Gurari D., Chebath J., and Revel M. Involvement of receptor-bound protein methyltransferase PRMT1 in antiviral and antiproliferative effects of type I interferons. J Interferon Cytokine Res 19 (1999) 189 95
174. Zika E., Fauquier L., Vandel L., and Ting J.P. Interplay among coactivator-associated arginine methyltransferase 1, CBP, and CIITA in IFN-gamma-inducible MHC-II gene expression. Proc Natl Acad Sci USA 102 (2005) 16321 6
175. Krones-Herzig A., Mesaros A., Metzger D., Ziegler A., Lemke U., Bruning J.C., et al. Signal-dependent control of gluconeogenic key enzyme genes through coactivator-associated arginine methyltransferase 1. J Biol Chem 281 (2006) 3025 9
176. Powell E., Kuhn P., and Xu W. Nuclear receptor cofactors in PPARgamma-mediated adipogenesis and adipocyte energy metabolism. PPAR Res 2007 (2007) 53843
177. Yadav N., Cheng D., Richard S., Morel M., Iyer V.R., Aldaz C.M., et al. CARM1 promotes adipocyte differentiation by coactivating PPARgamma. EMBO Rep 9 (2008) 193 8
178. Christian M., Kiskinis E., Debevec D., Leonardsson G., White R., and Parker M.G. RIP140-targeted repression of gene expression in adipocytes. Mol Cell Biol 25 (2005) 9383 91
179. Mostaqul Huq M.D., Gupta P., Tsai N.P., White R., Parker M.G., and Wei L.N. Suppression of receptor interacting protein 140 repressive activity by protein arginine methylation. EMBO J 25 (2006) 5094 104
180. Le Guezennec X., Vermeulen M., Brinkman A.B., Hoeijmakers W.A., Cohen A., Lasonder E., et al. MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol Cell Biol 26 (2006) 843 51
181. Tan C.P., and Nakielny S. Control of the DNA methylation system component MBD2 by protein arginine methylation. Mol Cell Biol 26 (2006) 7224 35
182. Boisvert F.M., Hendzel M.J., Masson J.Y., and Richard S. Methylation of MRE11 regulates its nuclear compartmentalization. Cell Cycle 4 (2005) 981 9
183. 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 69
184. El-Andaloussi N., Valovka T., Toueille M., Steinacher R., Focke F., Gehrig P., et al. Arginine methylation regulates DNA polymerase beta. Mol Cell 22 (2006) 51-62
185. 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 5
186. Zou Y., Webb K., Perna A.D., Zhang Q., Clarke S., and Wang Y. A mass spectrometric study on the in vitro methylation of HMGA1a and HMGA1b proteins by PRMTs: methylation specificity, the effect of binding to AT-rich duplex DNA, and the effect of C-terminal phosphorylation. Biochemistry 46 (2007) 7896 906
187. Huang S., Li X., Yusufzai T.M., Qiu Y., and Felsenfeld G. USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol Cell Biol 27 (2007) 7991-8002