O-GlcNAcylation of co-activator-associated arginine methyltransferase 1 regulates its protein substrate specificity

Biochemical Journal

Volumn 466, Issue 3, 2015, Pages 587-599

  Charoensuksai, Purin ^a   Kuhn, Peter ^a,b   Wang, Lu ^a   Sherer, Nathan ^a   Xu, Wei ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b EDGEWOOD COLLEGE   (United States)

Author keywords

Co activator mass spectrometry (MS); Co activator associated arginine methyltransferase 1 (CARM1); O linked N acetylglucosaminidation (O GlcNAcylation); Proteinmethylation; Transcription

Indexed keywords

CO ACTIVATOR ASSOCIATED ARGININE METHYLTRANSFERASE 1; LENTIVIRUS VECTOR; METHYLTRANSFERASE; N ACETYLGLUCOSAMINE; O LINKED BETA N ACETYLGLUCOSAMINIDATION; PROTEIN PS2; RECOMBINANT PROTEIN; SERINE; THREONINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WHEAT GERM AGGLUTININ; COACTIVATOR-ASSOCIATED ARGININE METHYLTRANSFERASE 1; PROTEIN ARGININE METHYLTRANSFERASE;

ACYLATION; AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRESS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME STABILITY; EXON SKIPPING; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; LIMIT OF QUANTITATION; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SUBSTRATE SPECIFICITY; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; RADIOISOTOPE DISTRIBUTION; REPORTER GENE; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY; TRANSCRIPTION INITIATION; TRIPLE NEGATIVE BREAST CANCER; WESTERN BLOTTING; WILD TYPE; ANIMAL; GENETICS; HEK293 CELL LINE; MCF 7 CELL LINE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY;

TRITICUM AESTIVUM;

ACETYLGLUCOSAMINE; AMINO ACID SEQUENCE; ANIMALS; HEK293 CELLS; HUMANS; MCF-7 CELLS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN-ARGININE N-METHYLTRANSFERASES; SUBSTRATE SPECIFICITY;

EID: 84928231343     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20141072     Document Type: Article

References (69)

1. Chen, D., Ma, H., Hong, H., Koh, S.S., Huang, S.M., Schurter, B.T., Aswad, D.W. and Stallcup, M.R. (1999) Regulation of transcription by a protein methyltransferase. Science 284, 2174-2177 CrossRef PubMed
2. Miao, F., Li, S., Chavez, V., Lanting, L. and Natarajan, R. (2006) Coactivator-associated arginine methyltransferase-1 enhances nuclear factor-kappaB-mediated gene transcription through methylation of histone H3 at arginine 17. Mol. Endocrinol. 20, 1562-1573 CrossRef PubMed
3. An, W., Kim, J. and Roeder, R.G. (2004) Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117, 735-748 CrossRef PubMed
4. Koh, S.S., Chen, D., Lee, Y.H. and Stallcup, M.R. (2001) Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities. J. Biol. Chem. 276, 1089-1098 CrossRef PubMed
5. Yadav, N., Cheng, D., Richard, S., Morel, M., Iyer, V.R., Aldaz, C.M. and Bedford, M.T. (2008) CARM1 promotes adipocyte differentiation by coactivating PPARgamma. EMBO Rep. 9, 193-198 CrossRef PubMed
6. Bauer, U.M., Daujat, S., Nielsen, S.J., Nightingale, K. and Kouzarides, T. (2002) Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep. 3, 39-44 CrossRef PubMed
7. Cheng, D., C ?ot é, J., Shaaban, S. and Bedford, M.T. (2007) The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol. Cell 25, 71-83 CrossRef PubMed
8. Lee, J. and Bedford, M.T. (2002) PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays. EMBO Rep. 3, 268-273 CrossRef PubMed
9. Teyssier, C., Chen, D. and Stallcup, M.R. (2002) Requirement for multiple domains of the protein arginine methyltransferase CARM1 in its transcriptional coactivator function. J. Biol. Chem. 277, 46066-46072 CrossRef PubMed
10. Teyssier, C., Ou, C.Y., Khetchoumian, K., Losson, R. and Stallcup, M.R. (2006) 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, 1276-1286 CrossRef PubMed
11. Nandi, A., Sprung, R., Barma, D.K., Zhao, Y., Kim, S.C. and Falck, J.R. (2006) Global identification of O-GlcNAc-modified proteins. Anal. Chem. 78, 452-458 CrossRef PubMed
12. Copeland, R.J., Han, G. and Hart, G.W. (2013) O-GlcNAcomics-revealing roles of O-GlcNAcylation in disease mechanisms and development of potential diagnostics. Proteomics Clin. Appl., doi: 10.1002/prca.201300001
13. Hahne, H., Sobotzki, N., Nyberg, T., Helm, D., Borodkin, V.S., van Aalten, D.M., Agnew, B. and Kuster, B. (2013) Proteome wide purification and identification of O-GlcNAc-modified proteins using click chemistry and mass spectrometry. J. Proteome Res. 12, 927-936 CrossRef PubMed
14. Trinidad, J.C., Barkan, D.T., Gulledge, B.F., Thalhammer, A., Sali, A., Schoepfer, R. and Burlingame, A.L. (2012) Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol. Cell. Proteomics 11, 215-229 CrossRef PubMed
15. Haltiwanger, R.S., Blomberg, M.A. and Hart, G.W. (1992) Glycosylation of nuclear and cytoplasmic proteins. Purification and characterization of a uridine diphospho-N-acetylglucosamine: polypeptide beta-N-acetylglucosaminyltransferase. J. Biol. Chem. 267, 9005-9013 PubMed
16. Kreppel, L.K., Blomberg, M.A. and Hart, G.W. (1997) Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J. Biol. Chem. 272, 9308-9315 CrossRef PubMed
17. Gao, Y., Wells, L., Comer, F.I., Parker, G.J. and Hart, G.W. (2001) Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276, 9838-9845 CrossRef PubMed
18. Zachara, N.E. and Hart, G.W. (2006) Cell signaling, the essential role of O-GlcNAc!. Biochim. Biophys. Acta 1761, 599-617 CrossRef PubMed
19. Zachara, N.E. and Hart, G.W. (2004) O-GlcNAc a sensor of cellular state: the role of nucleocytoplasmic glycosylation in modulating cellular function in response to nutrition and stress. Biochim. Biophys. Acta 1673, 13-28 CrossRef PubMed
20. Hanover, J.A., Krause, M.W. and Love, D.C. (2010) The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine. Biochim. Biophys. Acta 1800, 80-95 CrossRef PubMed
21. Hart, G.W., Slawson, C., Ramirez-Correa, G. and Lagerlof, O. (2011) Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80, 825-858 CrossRef PubMed
22. Hart, G.W., Housley, M.P. and Slawson, C. (2007) Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022 CrossRef PubMed
23. O'Donnell, N. (2002) Intracellular glycosylation and development. Biochim. Biophys. Acta 1573, 336-345 CrossRef PubMed
24. Ozcan, S., Andrali, S.S. and Cantrell, J.E. (2010) Modulation of transcription factor function by O-GlcNAc modification. Biochim. Biophys. Acta 1799, 353-364 CrossRef PubMed
25. Chumanov, R.S., Kuhn, P.A., Xu, W. and Burgess, R.R. (2011) Expression and purification of full-length mouse CARM1 from transiently transfected HEK293T cells using HaloTag technology. Protein. Expr. Purif. 76, 145-153 CrossRef PubMed
26. Kuhn, P., Xu, Q., Cline, E., Zhang, D., Ge, Y. and Xu, W. (2009) Delineating Anopheles gambiae coactivator associated arginine methyltransferase 1 automethylation using top-down high resolution tandem mass spectrometry. Protein Sci. 18, 1272-1280 CrossRef PubMed
27. Zachara, N.E., Vosseller, K. and Hart, G.W. (2011) Detection and analysis of proteins modified by O-linked N-acetylglucosamine. Curr. Protoc. Protein Sci. Chapter 12, Unit12.18
28. Wang, L., Zhao, Z., Meyer, M.B., Saha, S., Yu, M., Guo, A., Wisinski, K.B., Huang, W., Cai, W., Pike, J.W. et al. (2014) CARM1 methylates chromatin remodeling factor BAF155 to enhance tumor progression and metastasis. Cancer Cell 25, 21-36 CrossRef PubMed
29. Wang, L., Charoensuksai, P., Watson, N.J., Wang, X., Zhao, Z., Coriano, C.G., Kerr, L.R. and Xu, W. (2013) CARM1 automethylation is controlled at the level of alternative splicing. Nucleic Acids Res 41, 6870-6880 CrossRef PubMed
30. Cheung, W.D., Sakabe, K., Housley, M.P., Dias, W.B. and Hart, G.W. (2008) O-linked beta-N-acetylglucosaminyltransferase substrate specificity is regulated by myosin phosphatase targeting and other interacting proteins. J. Biol. Chem. 283, 33935-33941 CrossRef PubMed
31. Kuhn, P., Chumanov, R., Wang, Y., Ge, Y., Burgess, R.R. and Xu, W. (2011) Automethylation of CARM1 allows coupling of transcription and mRNA splicing. Nucleic Acids Res 39, 2717-2726 CrossRef PubMed
32. Troffer-Charlier, N., Cura, V., Hassenboehler, P., Moras, D. and Cavarelli, J. (2007) Functional insights from structures of coactivator-associated arginine methyltransferase 1 domains. EMBO J. 26, 4391-4401 CrossRef PubMed
33. Xue, B., Dunbrack, R.L., Williams, R.W., Dunker, A.K. and Uversky, V.N. (2010) PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochim. Biophys. Acta 1804, 996-1010 CrossRef PubMed
34. Yue, W.W., Hassler, M., Roe, S.M., Thompson-Vale, V. and Pearl, L.H. (2007) Insights into histone code syntax from structural and biochemical studies of CARM1 methyltransferase. EMBO J. 26, 4402-4412 CrossRef PubMed
35. Wu, J. and Xu, W. (2012) Histone H3R17me2a mark recruits human RNA polymerase-associated factor 1 complex to activate transcription. Proc. Natl. Acad. Sci. U.S.A. 109, 5675-5680 CrossRef PubMed
36. Myers, S.A., Panning, B. and Burlingame, A.L. (2011) Polycomb repressive complex 2 is necessary for the normal site-specific O-GlcNAc distribution in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 108, 9490-9495 CrossRef PubMed
37. Alfaro, J.F., Gong, C.X., Monroe, M.E., Aldrich, J.T., Clauss, T.R., Purvine, S.O., Wang, Z., Camp, D.G., Shabanowitz, J., Stanley, P. et al. (2012) Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc. Natl. Acad. Sci. U.S.A. 109, 7280-7285 CrossRef PubMed
38. Gawlowski, T., Suarez, J., Scott, B., Torres-Gonzalez, M., Wang, H., Schwappacher, R., Han, X., Yates, J.R., Hoshijima, M. and Dillmann, W. (2012) Modulation of dynamin-related protein 1 (DRP1) function by increased O-linked-β -N-acetylglucosamine modification (O-GlcNAc) in cardiac myocytes. J. Biol. Chem. 287, 30024-30034 CrossRef PubMed
39. Ranuncolo, S.M., Ghosh, S., Hanover, J.A., Hart, G.W. and Lewis, B.A. (2012) Evidence of the involvement of O-GlcNAc-modified human RNA polymerase II CTD in transcription in vitro and in vivo. J. Biol. Chem. 287, 23549-23561 CrossRef PubMed
40. Li, X., Molina, H., Huang, H., Zhang, Y.Y., Liu, M., Qian, S.W., Slawson, C., Dias, W.B., Pandey, A., Hart, G.W. et al. (2009) O-linked N-acetylglucosamine modification on CCAAT enhancer-binding protein beta: role during adipocyte differentiation. J. Biol. Chem. 284, 19248-19254 CrossRef PubMed
41. Jochmann, R., Holz, P., Sticht, H. and St?urzl, M. (2014) Validation of the reliability of computational O-GlcNAc prediction. Biochim. Biophys. Acta 1844, 416-421 CrossRef PubMed
42. Park, S.Y., Kim, H.S., Kim, N.H., Ji, S., Cha, S.Y., Kang, J.G., Ota, I., Shimada, K., Konishi, N., Nam, H.W. et al. (2010) Snail1 is stabilized by O-GlcNAc modification in hyperglycaemic condition. EMBO J. 29, 3787-3796 CrossRef PubMed
43. Hu, P., Berkowitz, P., Madden, V.J. and Rubenstein, D.S. (2006) Stabilization of plakoglobin and enhanced keratinocyte cell-cell adhesion by intracellular O-glycosylation. J. Biol. Chem. 281, 12786-12791 CrossRef PubMed
44. Yang, W.H., Kim, J.E., Nam, H.W., Ju, J.W., Kim, H.S., Kim, Y.S. and Cho, J.W. (2006) Modification of p53 with O-linked N-acetylglucosamine regulates p53 activity and stability. Nat. Cell Biol. 8, 1074-1083 CrossRef PubMed
45. Huang, X., Pan, Q., Sun, D., Chen, W., Shen, A., Huang, M., Ding, J. and Geng, M. (2013) O-GlcNAcylation of cofilin promotes breast cancer cell invasion. J. Biol. Chem. 288, 36418-36425 CrossRef PubMed
46. Dauphinee, S.M., Ma, M. and Too, C.K. (2005) Role of O-linked beta-N-acetylglucosamine modification in the subcellular distribution of alpha4 phosphoprotein and Sp1 in rat lymphoma cells. J. Cell Biochem. 96, 579-588 CrossRef PubMed
47. Andrali, S.S., Qian, Q. and Ozcan, S. (2007) Glucose mediates the translocation of NeuroD1 by O-linked glycosylation. J. Biol. Chem. 282, 15589-15596 CrossRef PubMed
48. Herrmann, F., Pably, P., Eckerich, C., Bedford, M.T. and Fackelmayer, F.O. (2009) Human protein arginine methyltransferases in vivo-distinct properties of eight canonical members of the PRMT family. J. Cell Sci. 122, 667-677 CrossRef PubMed
49. Tarrant, M.K., Rho, H.S., Xie, Z., Jiang, Y.L., Gross, C., Culhane, J.C., Yan, G., Qian, J., Ichikawa, Y., Matsuoka, T. et al. (2012) Regulation of CK2 by phosphorylation and O-GlcNAcylation revealed by semisynthesis. Nat. Chem. Biol. 8, 262-269 CrossRef PubMed
50. Higashimoto, K., Kuhn, P., Desai, D., Cheng, X. and Xu, W. (2007) Phosphorylation-mediated inactivation of coactivator-associated arginine methyltransferase 1. Proc. Natl. Acad. Sci. U.S.A. 104, 12318-12323 CrossRef PubMed
51. Feng, Q., He, B., Jung, S.Y., Song, Y., Qin, J., Tsai, S.Y., Tsai, M.J. and O'Malley, B.W. (2009) Biochemical control of CARM1 enzymatic activity by phosphorylation. J. Biol. Chem. 284, 36167-36174 CrossRef PubMed
52. Carascossa, S., Dudek, P., Cenni, B., Briand, P.A. and Picard, D. (2010) CARM1 mediates the ligand-independent and tamoxifen-resistant activation of the estrogen receptor alpha by cAMP. Genes Dev. 24, 708-719 CrossRef PubMed
53. Chou, T.Y., Hart, G.W. and Dang, C.V. (1995) c-Myc is glycosylated at threonine 58, a known phosphorylation site and a mutational hot spot in lymphomas. J. Biol. Chem. 270, 18961-18965 CrossRef PubMed
54. Cheng, X., Cole, R.N., Zaia, J. and Hart, G.W. (2000) Alternative O-glycosylation/O-phosphorylation of the murine estrogen receptor beta. Biochemistry 39, 11609-11620 CrossRef PubMed
55. Overath, T., Kuckelkorn, U., Henklein, P., Strehl, B., Bonar, D., Kloss, A., Siele, D., Kloetzel, P.M. and Janek, K. (2012) Mapping of O-GlcNAc sites of 20 S proteasome subunits and Hsp90 by a novel biotin-cystamine tag. Mol. Cell. Proteomics 11, 467-477 CrossRef PubMed
56. Kawauchi, K., Araki, K., Tobiume, K. and Tanaka, N. (2009) Loss of p53 enhances catalytic activity of IKKbeta through O-linked beta-N-acetyl glucosamine modification. Proc. Natl. Acad. Sci. U.S.A. 106, 3431-3436 CrossRef PubMed
57. Sakabe, K. and Hart, G.W. (2010) O-GlcNAc transferase regulates mitotic chromatin dynamics. J. Biol. Chem. 285, 34460-34468 CrossRef PubMed
58. Lim, K. and Chang, H.I. (2009) O-GlcNAc modification of Sp1 inhibits the functional interaction between Sp1 and Oct1. FEBS Lett. 583, 512-520 CrossRef PubMed
59. Lim, K. and Chang, H.I. (2009) O-GlcNAc inhibits interaction between Sp1 and Elf-1 transcription factors. Biochem. Biophys. Res. Commun. 380, 569-574 CrossRef PubMed
60. Gewinner, C., Hart, G., Zachara, N., Cole, R., Beisenherz-Huss, C. and Groner, B. (2004) The coactivator of transcription CREB-binding protein interacts preferentially with the glycosylated form of Stat5. J. Biol. Chem. 279, 3563-3572 CrossRef PubMed
61. Zeng, H., Wu, J., Bedford, M.T., Sbardella, G., Hoffmann, F.M., Bi, K. and Xu, W. (2013) A TR-FRET-based functional assay for screening activators of CARM1. Chembiochem 14, 827-835 CrossRef PubMed
62. Slawson, C., Copeland, R.J. and Hart, G.W. (2010) O-GlcNAc signaling: a metabolic link between diabetes and cancer? Trends Biochem. Sci. 35, 547-555 CrossRef PubMed
63. Slawson, C. and Hart, G.W. (2011) O-GlcNAc signalling: implications for cancer cell biology. Nat. Rev. Cancer 11, 678-684 CrossRef PubMed
64. Lynch, T.P. and Reginato, M.J. (2011) O-GlcNAc transferase: a sweet new cancer target. Cell Cycle 10, 1712-1713 CrossRef PubMed
65. Fardini, Y., Dehennaut, V., Lefebvre, T. and Issad, T. (2013) O-GlcNAcylation: a new cancer hallmark? Front Endocrinol. 4, 99 CrossRef
66. Akbar, H., Schmitt, E., Ballou, M.A., Corrêa, M.N., Depeters, E.J. and Loor, J.J. (2013) Dietary lipid during late-pregnancy and early-lactation to manipulate metabolic and inflammatory gene network expression in dairy cattle liver with a focus on PPARs. Gene Regul. Syst. Bio. 7, 103-123 PubMed
67. Schmitt, E., Ballou, M.A., Correa, M.N., DePeters, E.J., Drackley, J.K. and Loor, J.J. (2011) Dietary lipid during the transition period to manipulate subcutaneous adipose tissue peroxisome proliferator-activated receptor-γ co-regulator and target gene expression. J. Dairy Sci. 94, 5913-5925 CrossRef PubMed
68. Krones-Herzig, A., Mesaros, A., Metzger, D., Ziegler, A., Lemke, U., Brüning, J.C. and Herzig, S. (2006) Signal-dependent control of gluconeogenic key enzyme genes through coactivator-associated arginine methyltransferase 1. J. Biol. Chem. 281, 3025-3029 CrossRef PubMed
69. Wang, S.C., Dowhan, D.H., Eriksson, N.A. and Muscat, G.E. (2012) CARM1/PRMT4 is necessary for the glycogen gene expression programme in skeletal muscle cells. Biochem. J. 444, 323-331 CrossRef PubMed