Histone H2A and H4 N-terminal tails are positioned by the MEP50 WD repeat protein for efficient methylation by the PRMT5 arginine methyltransferase

Journal of Biological Chemistry

Volumn 290, Issue 15, 2015, Pages 9674-9689

  Burgos, Emmanuel S ^a   Wilczek, Carola ^a,c   Onikubo, Takashi ^a   Bonanno, Jeffrey B ^a   Jansong, Janina ^b   Reime, Ulf ^b   Shechter, David ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b JPT Peptide Technologies GmbH   (Germany)

^c Erdmann Technologies GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; AMINO ACIDS; ARGININE; ASSAYS; DIMERS; ENZYME KINETICS; METHYLATION; PEPTIDES; SUBSTRATES;

CAENORHABDITIS ELEGANS; ENZYMATIC EFFICIENCY; HISTONE METHYLATION; INTERACTION STUDIES; METHYLTRANSFERASE ACTIVITY; METHYLTRANSFERASES; PROTEIN SUBSTRATE; PROTEIN-ARGININE METHYLTRANSFERASE;

PROTEINS;

ARGININE; HISTONE H2A; HISTONE H4; HISTONE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE; CAENORHABDITIS ELEGANS PROTEIN; HISTONE; HSL7 PROTEIN, XENOPUS; MEP50 PROTEIN, HUMAN; METHYLOSOME PROTEIN 50, XENOPUS; NONHISTONE PROTEIN; PRMT5 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN; XENOPUS PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CAENORHABDITIS ELEGANS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; HISTONE METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; SEQUENCE ALIGNMENT; XENOPUS LAEVIS; ALGORITHM; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; KINETICS; METABOLISM; METHYLATION; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

CAENORHABDITIS ELEGANS; VERTEBRATA; XENOPUS LAEVIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALGORITHMS; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CATALYTIC DOMAIN; CHROMOSOMAL PROTEINS, NON-HISTONE; HISTONES; HUMANS; KINETICS; METHYLATION; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-ARGININE N-METHYLTRANSFERASES; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84927145268     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.636894     Document Type: Article

References (50)

1. Di Lorenzo, A., and Bedford, M. T. (2011) Histone arginine methylation. FEBS Lett. 585, 2024-2031
2. Wolf, S. S. (2009) The protein arginine methyltransferase family: an update about function, new perspectives and the physiological role in humans. Cell Mol. Life Sci. 66, 2109-2121
3. Wysocka, J., Allis, C. D., and Coonrod, S. (2006) Histone arginine methylation and its dynamic regulation. Front. Biosci. 11, 344-355
4. Lee, Y. H., and Stallcup, M. R. (2009) Minireview: protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol. Endocrinol. 23, 425-433
5. Wilczek, C., Chitta, R., Woo, E., Shabanowitz, J., Chait, B. T., Hunt, D. F., and Shechter, D. (2011) Protein arginine methyltransferase Prmt5-Mep50 methylates histones H2A and H4 and the histone chaperone nucleoplasmin in Xenopus laevis eggs. J. Biol. Chem. 286, 42221-42231
6. Bezzi, M., Teo, S. X., Muller, J., Mok, W. C., Sahu, S. K., Vardy, L. A., Bonday, Z. Q., and Guccione, E. (2013) Regulation of constitutive and alternative splicing by PRMT5 reveals a role for Mdm4 pre-mRNA in sensing defects in the spliceosomal machinery. Genes Dev. 27, 1903-1916
7. Scoumanne, A., Zhang, J., and Chen, X. (2009) PRMT5 is required for cell-cycle progression and p53 tumor suppressor function. Nucleic Acids Res. 37, 4965-4976
8. Friesen, W. J., Wyce, A., Paushkin, S., Abel, L., Rappsilber, J., Mann, M., and Dreyfuss, G. (2002) A novel WD repeat protein component of the methylosome binds Sm proteins. J. Biol. Chem. 277, 8243-8247
9. Furuno, K., Masatsugu, T., Sonoda, M., Sasazuki, T., and Yamamoto, K. (2006) Association of Polycomb group SUZ12 with WD-repeat protein MEP50 that binds to histone H2A selectively in vitro. Biochem. Biophys. Res. Commun. 345, 1051-1058
10. Le Guezennec, X., Vermeulen, M., Brinkman, A. B., Hoeijmakers, W. A., Cohen, A., Lasonder, E., and Stunnenberg, H. G. (2006) MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol. Cell Biol. 26, 843-851
11. Aggarwal, P., Vaites, L. P., Kim, J. K., Mellert, H., Gurung, B., Nakagawa, H., Herlyn, M., Hua, X., Rustgi, A. K., McMahon, S. B., and Diehl, J. A. (2010) Nuclear cyclin D1/CDK4 kinase regulates CUL4 expression and triggers neoplastic growth via activation of the PRMT5 methyltransferase. Cancer Cell 18, 329-340
12. Guderian, G., Peter, C., Wiesner, J., Sickmann, A., Schulze-Osthoff, K., Fischer, U., and Grimmler, M. (2011) RioK1, a new interactor of protein arginine methyltransferase 5 (PRMT5), competes with pICln for binding and modulates PRMT5 complex composition and substrate specificity. J. Biol. Chem. 286, 1976-1986
13. Ancelin, K., Lange, U. C., Hajkova, P., Schneider, R., Bannister, A. J., Kouzarides, T., and Surani, M. A. (2006) Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat. Cell Biol. 8, 623-630
14. Friesen, W. J., Paushkin, S., Wyce, A., Massenet, S., Pesiridis, G. S., Van Duyne, G., Rappsilber, J., Mann, M., and Dreyfuss, G. (2001) The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylargi-nine- modified Sm proteins. Mol. Cell Biol. 21, 8289-8300
15. Lacroix, M., El Messaoudi, S., Rodier, G., Le Cam, A., Sardet, C., and Fabbrizio, E. (2008) The histone-binding protein COPR5 is required for nuclear functions of the protein arginine methyltransferase PRMT5. EMBO Rep. 9, 452-458
16. Gurung, B., Feng, Z., Iwamoto, D. V., Thiel, A., Jin, G., Fan, C. M., Ng, J. M., Curran, T., and Hua, X. (2013) Menin epigenetically represses Hedgehog signaling in MEN1 tumor syndrome. Cancer Res. 73, 2650-2658
17. Karkhanis, V., Hu, Y.-J., Baiocchi, R. A., Imbalzano, A. N., and Sif, S. (2011) Versatility of PRMT5-induced methylation in growth control and development. Trends Biochem. Sci. 36, 633-641
18. Pal, S., Vishwanath, S. N., Erdjument-Bromage, H., Tempst, P., and Sif, S. (2004) Human SWI/SNF-associated PRMT5 methylates histone H3 arginine8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol. Cell Biol. 24, 9630-9645
19. Yan, F., Alinari, L., Lustberg, M. E., Martin, L. K., Cordero-Nieves, H. M., Banasavadi-Siddegowda, Y., Virk, S., Barnholtz-Sloan, J., Bell, E. H., Wojton, J., Jacob, N. K., Chakravarti, A., Nowicki, M. O., Wu, X., Lapalombella, R., Datta, J., Yu, B., Gordon, K., Haseley, A., Patton, J. T., Smith, P. L., Ryu, J., Zhang, X., Mo, X., Marcucci, G., Nuovo, G., Kwon, C. H., Byrd, J. C., Chiocca, E. A., Li, C., Sif, S., Jacob, S., Lawler, S., Kaur, B., and Baiocchi, R. A. (2014) Genetic validation of the protein arginine methyltransferase PRMT5 as a candidate therapeutic target in glioblastoma. Cancer Res. 74, 1752-1765
20. Bao, X., Zhao, S., Liu, T., Liu, Y., Liu, Y., and Yang, X. (2013) Overexpression of PRMT5 promotes tumor cell growth and is associated with poor disease prognosis in epithelial ovarian cancer. J. Histochem. Cytochem. 61, 206-217
21. Gu, Z., Gao, S., Zhang, F., Wang, Z., Ma, W., Davis, R. E., and Wang, Z. (2012) Protein arginine methyltransferase 5 is essential for growth of lung cancer cells. Biochem. J. 446, 235-241
22. Ho, M.-C., Wilczek, C., Bonanno, J. B., Xing, L., Seznec, J., Matsui, T., Carter, L. G., Onikubo, T., Kumar, P. R., Chan, M. K., Brenowitz, M., Cheng, R. H., Reimer, U., Almo, S. C., and Shechter, D. (2013) Structure of the arginine methyltransferase PRMT5-MEP50 reveals a mechanism for substrate specificity. PLoS One 8, e57008
23. Antonysamy, S., Bonday, Z., Campbell, R. M., Doyle, B., Druzina, Z., Gheyi, T., Han, B., Jungheim, L. N., Qian, Y., Rauch, C., Russell, M., Sauder, J. M., Wasserman, S. R., Weichert, K., Willard, F. S., Zhang, A., and Emtage, S. (2012) Crystal structure of the human PRMT5:MEP50 complex. Proc. Natl. Acad. Sci. U.S.A. 109, 17960-17965
24. Ruthenburg, A. J., Wang, W., Graybosch, D. M., Li, H., Allis, C. D., Patel, D. J., and Verdine, G. L. (2006) Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex. Nat. Struct. Mol. Biol. 13, 704-712
25. Murzina, N. V., Pei, X. Y., Zhang, W., Sparkes, M., Vicente-Garcia, J., Pratap, J. V., McLaughlin, S. H., Ben-Shahar, T. R., Verreault, A., Luisi, B. F., and Laue, E. D. (2008) Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16, 1077-1085
26. Hemeon, I., Gutierrez, J. A., Ho, M. C., and Schramm, V. L. (2011) Characterizing DNA methyltransferases with an ultrasensitive luciferaselinked continuous assay. Anal. Chem. 83, 4996-5004
27. Sturm, M. B., and Schramm, V. L. (2009) Detecting ricin: sensitive luminescent assay for ricin A-chain ribosome depurination kinetics. Anal. Chem. 81, 2847-2853
28. Wang, H. C., Ciskanik, L., Dunaway-Mariano, D., von der Saal, W., and Villafranca, J. J. (1988) Investigations of the partial reactions catalyzed by pyruvate phosphate dikinase. Biochemistry 27, 625-633
29. Morrison, J. F. (1969) Kinetics of the reversible inhibition of enzymecatalysed reactions by tight-binding inhibitors. Biochim. Biophys. Acta 185, 269-286
30. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-28
31. Russell, R. B., and Barton, G. J. (1992) Multiple protein sequence alignment from tertiary structure comparison: assignment of global and residue confidence levels. Proteins 14, 309-323
32. Roberts, E., Eargle, J., Wright, D., and Luthey-Schulten, Z. (2006) Multi- Seq: unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics 7, 382
33. Comeau, S. R., Gatchell, D. W., Vajda, S., and Camacho, C. J. (2004) Clus- Pro: a fully automated algorithm for protein-protein docking. Nucleic Acids Res. 32, W96-W99
34. Comeau, S. R., Gatchell, D. W., Vajda, S., and Camacho, C. J. (2004) Clus- Pro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20, 45-50
35. Shechter, D., Nicklay, J. J., Chitta, R. K., Shabanowitz, J., Hunt, D. F., and Allis, C. D. (2009) Analysis of histones in Xenopus laevis. I.Adistinct index of enriched variants and modifications exists in each cell type and is remodeled during developmental transitions. J. Biol. Chem. 284, 1064-1074
36. Nicklay, J. J., Shechter, D., Chitta, R. K., Garcia, B. A., Shabanowitz, J., Allis, C. D., and Hunt, D. F. (2009) Analysis of histones in Xenopus laevis. II. Mass spectrometry reveals an index of cell type-specific modifications on H3 and H4. J. Biol. Chem. 284, 1075-1085
37. Tee, W. W., Pardo, M., Theunissen, T. W., Yu, L., Choudhary, J. S., Hajkova, P., and Surani, M. A. (2010) Prmt5 is essential for early mousedevelopment and acts in the cytoplasm to maintain ES cell pluripotency. Genes Dev. 24, 2772-2777
38. Shechter, D., Dormann, H. L., Allis, C. D., and Hake, S. B. (2007) Extraction, purification and analysis of histones. Nat. Protoc. 2, 1445-1457
39. 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. (2002)Negative regulation of transcription by the type II arginine methyltransferase PRMT5. EMBO Rep. 3, 641-645
40. Majumder, S., Alinari, L., Roy, S., Miller, T., Datta, J., Sif, S., Baiocchi, R., and Jacob, S. T. (2010) Methylation of histone H3 and H4 by PRMT5regulates ribosomal RNA gene transcription. J. Cell Biochem. 109, 553-563
41. Wang, L., Pal, S., and Sif, S. (2008) Protein arginine methyltransferase 5suppresses the transcription of the RB family of tumor suppressors in leukemia and lymphoma cells. Mol. Cell Biol. 28, 6262-6277
42. Wang, M., Fuhrmann, J., and Thompson, P. R. (2014) Protein arginine methyltransferase 5 catalyzes substrate dimethylation in a distributive fashion. Biochemistry 53, 7884-7892
43. Wang, M., Xu, R. M., and Thompson, P. R. (2013) Substrate specificity, processivity, and kinetic mechanism of protein arginine methyltransferase5. Biochemistry 52, 5430-5440
44. Gui, S., Gathiaka, S., Li, J., Qu, J., Acevedo, O., and Hevel, J. M. (2014) Aremodeled protein arginine methyltransferase 1 (PRMT1) generates symmetric dimethylarginine. J. Biol. Chem. 289, 9320-9327
45. Porollo, A., and Meller, J. (2007) Prediction-based fingerprints of proteinprotein interactions. Proteins 66, 630-645
46. Zhang, Q. C., Deng, L., Fisher, M., Guan, J., Honig, B., and Petrey, D. (2011) PredUs: a web server for predicting protein interfaces using structural neighbors. Nucleic Acids Res. 39, W283-W287
47. Wang, W.-L., Anderson, L. C., Nicklay, J. J., Chen, H., Gamble, M. J., Shabanowitz, J., Hunt, D. F., and Shechter, D. (2014) Phosphorylation and arginine methylation mark histone H2A prior to deposition during Xenopus laevis development. Epigenetics Chromatin 7, 22
48. Zhao, Q., Rank, G., Tan, Y. T., Li, H., Moritz, R. L., Simpson, R. J., Cerruti, L., Curtis, D. J., Patel, D. J., Allis, C. D., Cunningham, J. M., and Jane, S. M. (2009) PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone andDNAmethylation in gene silencing. Nat. Struct. Mol. Biol. 16, 304-311
49. Pal, S., Baiocchi, R. A., Byrd, J. C., Grever, M. R., Jacob, S. T., and Sif, S. (2007) Low levels of miR-92b/96 induce PRMT5 translation and H3R8/ H4R3 methylation in mantle cell lymphoma. EMBO J. 26, 3558-3569
50. Feng, Y., Wang, J., Asher, S., Hoang, L., Guardiani, C., Ivanov, I., and Zheng, Y. G. (2011) Histone H4 acetylation differentially modulates arginine methylation by an in cis mechanism. J. Biol. Chem. 286, 20323-20334