A novel histone H4 arginine 3 methylation-sensitive histone H4 binding activity and transcriptional regulatory function for signal recognition particle subunits SRP68 and SRP72

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40641-40651

  Li, Jingjing ^a   Zhou, Fan ^b   Zhan, Deguo ^a   Gao, Qinqin ^a   Cui, Nan ^a   Li, Jiwen ^a   Iakhiaeva, Elena ^c,d   Zwieb, Christian ^c   Lin, Biaoyang ^b   Wong, Jiemin ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c Mays Cancer Center at UT Health San Antonio   (United States)

^d UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ACTIVITIES; DNA BINDING DOMAIN; HETERODIMERS; HISTONE H4; IN-VITRO; IN-VIVO; NUCLEAR PROTEINS; PROTEOMIC APPROACHES; REGULATORY FUNCTIONS; SIGNAL RECOGNITION PARTICLES; TARGET GENES; TRANSCRIPTIONAL REGULATION;

ALKYLATION; ARGININE; CHROMOSOMES; PEPTIDES; TRANSCRIPTION;

METHYLATION;

ARGININE; DNA; HETERODIMER; HISTONE H4; NUCLEAR PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 1; PROTEIN ARGININE METHYLTRANSFERASE 5; SIGNAL RECOGNITION PARTICLE; SIGNAL RECOGNITION PARTICLE 68; SIGNAL RECOGNITION PARTICLE 72; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA BINDING; GENE CONTROL; GENE IDENTIFICATION; GENE TARGETING; HISTONE METHYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEOMICS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

AMINO ACID MOTIFS; ARGININE; BINDING SITES; DIMERIZATION; HELA CELLS; HISTONES; HUMANS; METHYLATION; PROTEIN BINDING; SIGNAL RECOGNITION PARTICLE; TRANSCRIPTION, GENETIC;

EID: 84869992761     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.414284     Document Type: Article

References (47)

1. Wysocka, J., Allis, C. D., and Coonrod, S. (2006) Histone arginine methylation and its dynamic regulation. Front Biosci. 11, 344-355 (Pubitemid 43253497)
2. Lee, Y. H., and Stallcup, M. R. (2009) Minireview. Protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol. Endocrinol. 23, 425-433
3. Bedford, M. T., and Clarke, S. G. (2009) Protein arginine methylation in mammals. Who, what, and why. Mol. Cell 33, 1-13
4. Bedford, M. T., and Richard, S. (2005) Arginine methylation an emerging regulator of protein function. Mol. Cell 18, 263-272 (Pubitemid 41350532)
5. Pollack, B. P., Kotenko, S. V., He, W., Izotova, L. S., Barnoski, B. L., and Pestka, S. (1999) The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J. Biol. Chem. 274, 31531-31542
6. Branscombe, T. L., Frankel, A., Lee, J. H., Cook, J. R., Yang, Z., Pestka, S., and Clarke, S. (2001) PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J. Biol. Chem. 276, 32971-32976
7. Wang, H., Huang, Z. Q., Xia, L., Feng, Q., Erdjument-Bromage, H., Strahl, B. D., Briggs, S. D., Allis, C. D., Wong, J., Tempst, P., and Zhang, Y. (2001) Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 293, 853-857 (Pubitemid 32743973)
8. Pal, S., Vishwanath, S. N., Erdjument-Bromage, H., Tempst, P., and Sif, S. (2004) 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, 9630-9645 (Pubitemid 39391698)
9. Pal, S., Yun, R., Datta, A., Lacomis, L., Erdjument-Bromage, H., Kumar, J., Tempst, P., and Sif, S. (2003) mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol. 23, 7475-7487 (Pubitemid 37271449)
10. Xu, X., Hoang, S., Mayo, M. W., and Bekiranov, S. (2010) Application of machine learning methods to histone methylation ChIP-Seq data reveals H4R3me2 globally represses gene expression.BMCBioinformatics 11, 396
11. 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 (Pubitemid 38748890)
12. Jenuwein, T., and Allis, C. D. (2001) Translating the histone code. Science 293, 1074-1080 (Pubitemid 32758077)
13. Martin, C., and Zhang, Y. (2005) The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6, 838-849 (Pubitemid 41568733)
14. Ruthenburg, A. J., Li, H., Patel, D. J., and Allis, C. D. (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cell Biol. 8, 983-994 (Pubitemid 350174643)
15. Huang, S., Litt, M., and Felsenfeld, G. (2005) Methylation of histone H4 by arginine methyltransferase PRMT1 is essential in vivo for many subsequent histone modifications. Genes Dev. 19, 1885-1893 (Pubitemid 41186989)
16. Yap, K. L., and Zhou, M. M. (2011) Structure and mechanisms of lysine methylation recognition by the chromodomain in gene transcription. Biochemistry 50, 1966-1980
17. Yap, K. L., and Zhou, M. M. (2010) Keeping it in the family. Diverse histone recognition by conserved structural folds. Crit. Rev. Biochem. Mol. Biol. 45, 488-505
18. Yang, Y., Lu, Y., Espejo, A., Wu, J., Xu, W., Liang, S., and Bedford, M. T. (2010) TDRD3 is an effector molecule for arginine-methylated histone marks. Mol. Cell 40, 1016-1023
19. 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 and DNA methylation in gene silencing. Nat. Struct. Mol. Biol. 16, 304-311
20. Li, X., Hu, X., Patel, B., Zhou, Z., Liang, S., Ybarra, R., Qiu, Y., Felsenfeld, G., Bungert, J., and Huang, S. (2010) H4R3 methylation facilitates β-globin transcription by regulating histone acetyltransferase binding and H3 acetylation. Blood 115, 2028-2037
21. Wu, J., and Xu, W. (2012) Histone H3R17me2a mark recruits humanRNA polymerase-associated factor 1 complex to activate transcription. Proc. Natl. Acad. Sci. U.S.A. 109, 5675-5680
22. Liu, K., Guo, Y., Liu, H., Bian, C., Lam, R., Liu, Y., Mackenzie, F., Rojas, L. A., Reinberg, D., Bedford, M. T., Xu, R. M., and Min, J. (2012) Crystal structure of TDRD3 and methyl-arginine binding characterization of TDRD3, SMN, and SPF30. PloS One 7, e30375
23. Côté, J., and Richard, S. (2005) Tudor domains bind symmetrical dimethylated arginines. J. Biol. Chem. 280, 28476-28483 (Pubitemid 41105747)
24. Doudna, J. A., and Batey, R. T. (2004) Structural insights into the signal recognition particle. Annu. Rev. Biochem. 73, 539-557 (Pubitemid 39050379)
25. Leung, E., and Brown, J. D. (2010) Biogenesis of the signal recognition particle. Biochem. Soc. Trans. 38, 1093-1098
26. Egea, P. F., Stroud, R. M., and Walter, P. (2005) Targeting proteins to membranes. Structure of the signal recognition particle. Curr. Opin. Struct. Biol. 15, 213-220
27. Iakhiaeva, E., Hinck, C. S., Hinck, A. P., and Zwieb, C. (2009) Characterization of the SRP68/72 interface of human signal recognition particle by systematic site-directed mutagenesis. Protein Sci. 18, 2183-2195
28. Yin, J., Iakhiaeva, E., Menichelli, E., and Zwieb, C. (2007) Identification of the RNA binding regions of SRP68/72 and SRP72 by systematic mutagenesis of human SRP RNA. RNA Biol. 4, 154-159 (Pubitemid 351237916)
29. Iakhiaeva, E., Bhuiyan, S. H., Yin, J., and Zwieb, C. (2006) Protein SRP68 of human signal recognition particle. Identification of the RNA and SRP72 binding domains. Protein Sci. 15, 1290-1302 (Pubitemid 43800002)
30. Zhang, D., Yoon, H. G., and Wong, J. (2005) JMJD2A is a novel N-CoR-interacting protein and is involved in repression of the human transcription factor achaete scute-like homologue 2 (ASCL2/Hash2). Mol. Cell. Biol. 25, 6404-6414 (Pubitemid 41023217)
31. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. (1983) Accurate transcription initiation byRNApolymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489
32. Karagianni, P., Amazit, L., Qin, J., and Wong, J. (2008) ICBP90, a novel methyl K9 H3-binding protein linking protein ubiquitination with heterochromatin formation. Mol. Cell. Biol. 28, 705-717
33. Zhang, J., Gao, Q., Li, P., Liu, X., Jia, Y., Wu, W., Li, J., Dong, S., Koseki, H., and Wong, J. (2011) S phase-dependent interaction with DNMT1 dictates the role of UHRF1 but not UHRF2 inDNAmethylation maintenance. Cell Res. 21, 1723-1739
34. Nye, A. C., Rajendran, R. R., Stenoien, D. L., Mancini, M. A., Katzenellenbogen, B. S., and Belmont, A. S. (2002) Alteration of large-scale chromatin structure by estrogen receptor. Mol. Cell. Biol. 22, 3437-3449 (Pubitemid 34453983)
35. Chan, D. W., Wang, Y., Wu, M., Wong, J., Qin, J., and Zhao, Y. (2009) Unbiased proteomic screen for binding proteins to modified lysines on histone H3. Proteomics 9, 2343-2354
36. Li, J., Chu, M., Wang, S., Chan, D., Qi, S., Wu, M., Zhou, Z., Li, J., Nishi, E., Qin, J., and Wong, J. (2012) Identification and characterization of nardilysin as a novel dimethyl H3K4-binding protein involved in transcriptional regulation. J. Biol. Chem. 287, 10089-10098
37. Grosshans, H., Deinert, K., Hurt, E., and Simos, G. (2001) Biogenesis of the signal recognition particle (SRP) involves import of SRP proteins into the nucleolus, assembly with the SRP-RNA, and Xpo1p-mediated export. J. Cell Biol. 153, 745-762
38. Politz, J. C., Lewandowski, L. B., and Pederson, T. (2002) Signal recognition particle RNA localization within the nucleolus differs from the classical sites of ribosome synthesis. J. Cell Biol. 159, 411-418 (Pubitemid 35332828)
39. Stenoien, D. L., Nye, A. C., Mancini, M. G., Patel, K., Dutertre, M., O'Malley, B. W., Smith, C. L., Belmont, A. S., and Mancini, M. A. (2001) Ligand-mediated assembly and real-time cellular dynamics of estrogen receptor α-coactivator complexes in living cells. Mol. Cell. Biol. 21, 4404-4412 (Pubitemid 32565321)
40. Guccione, E., Bassi, C., Casadio, F., Martinato, F., Cesaroni, M., Schuchlautz, H., Lüscher, B., and Amati, B. (2007) Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449, 933-937 (Pubitemid 47598605)
41. Kirmizis, A., Santos-Rosa, H., Penkett, C. J., Singer, M. A., Vermeulen, M., Mann, M., Bähler, J., Green, R. D., and Kouzarides, T. (2007) Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449, 928-932 (Pubitemid 47598603)
42. Iberg, A. N., Espejo, A., Cheng, D., Kim, D., Michaud-Levesque, J., Richard, S., and Bedford, M. T. (2008) Arginine methylation of the histone H3 tail impedes effector binding. J. Biol. Chem. 283, 3006-3010
43. Rajakumara, E., Wang, Z., Ma, H., Hu, L., Chen, H., Lin, Y., Guo, R., Wu, F., Li, H., Lan, F., Shi, Y. G., Xu, Y., Patel, D. J., and Shi, Y. (2011) PHD finger recognition of unmodified histone H3R2 links UHRF1 to regulation of euchromatic gene expression. Mol. Cell 43, 275-284
44. Wu, J., Cui, N., Wang, R., Li, J., and Wong, J. (2012) A role for CARM1-mediated histone H3 arginine methylation in protecting histone acetylation by releasing corepressors from chromatin. PloS One 7, e34692
45. Pan, G. J., Chang, Z. Y., Schöler, H. R., and Pei, D. (2002) Stem cell pluripotency and transcription factor Oct4. Cell Res. 12, 321-329 (Pubitemid 135708344)
46. Yuan, P., Han, J., Guo, G., Orlov, Y. L., Huss, M., Loh, Y. H., Yaw, L. P., Robson, P., Lim, B., and Ng, H. H. (2009) Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23, 2507-2520
47. Ang, Y. S., Tsai, S. Y., Lee, D. F., Monk, J., Su, J., Ratnakumar, K., Ding, J., Ge, Y., Darr, H., Chang, B., Wang, J., Rendl, M., Bernstein, E., Schaniel, C., and Lemischka, I. R. (2011) Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145, 183-197