A novel RNA binding surface of the TAM domain of TIP5/BAZ2A mediates epigenetic regulation of rRNA genes

Nucleic Acids Research

Volumn 43, Issue 10, 2015, Pages 5208-5220

  Anosova, Irina ^a,b   Melnik, Svitlana ^c   Tripsianes, Konstantinos ^a,b,d   Kateb, Fatiha ^a,b   Grummt, Ingrid ^c   Sattler, Michael ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ARBP PROTEIN; MBD PROTEIN; METHYL CPG BINDING PROTEIN; NUCLEAR PROTEIN; RIBOSOME RNA; TAM PROTEIN; TIP5 PROTEIN; UNCLASSIFIED DRUG; BAZ2A PROTEIN, HUMAN; NONHISTONE PROTEIN; PROTEIN BINDING; RNA; RNA BINDING PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GENE LOCUS; GENOMICS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MUTATIONAL ANALYSIS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA BINDING; RRNA GENE; TRANSCRIPTION REGULATION; CHEMICAL STRUCTURE; CHEMISTRY; GENETIC EPIGENESIS; GENETICS; HEK293 CELL LINE; METABOLISM; POINT MUTATION; PROTEIN TERTIARY STRUCTURE; RNA GENE;

CHROMOSOMAL PROTEINS, NON-HISTONE; EPIGENESIS, GENETIC; GENES, RRNA; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; POINT MUTATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RNA; RNA-BINDING PROTEINS;

EID: 84931287861     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv365     Document Type: Article

References (58)

1. McStay, B. and Grummt, I. (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol., 24, 131-157.
2. Strohner, R., Nemeth, A., Jansa, P., Hofmann-Rohrer, U., Santoro, R., Langst, G. and Grummt, I. (2001) NoRC-a novel member of mammalian ISWI-containing chromatin remodeling machines. Embo J., 20, 4892-4900.
3. Santoro, R., Li, J. and Grummt, I. (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat. Genet., 32, 393-396.
4. Zhou, Y., Santoro, R. and Grummt, I. (2002) The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J., 21, 4632-4640.
5. Li, J., Langst, G. and Grummt, I. (2006) NoRC-dependent nucleosome positioning silences rRNA genes. EMBO J., 25, 5735-5741.
6. Mayer, C., Schmitz, K.M., Li, J., Grummt, I. and Santoro, R. (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol. Cell, 22, 351-361.
7. Schmitz, K.M., Mayer, C., Postepska, A. and Grummt, I. (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev., 24, 2264-2269.
8. Zhou, Y. and Grummt, I. (2005) The PHD fnger/bromodomain of NoRC interacts with acetylated histone H4K16 and is suffcient for rDNA silencing. Curr. Biol., 15, 1434-1438.
9. Santoro, R., Schmitz, K.M., Sandoval, J. and Grummt, I. (2010) Intergenic transcripts originating from a subclass of ribosomal DNA repeats silence ribosomal RNA genes in trans. EMBO Rep., 11, 52-58.
10. Mayer, C., Neubert, M. and Grummt, I. (2008) The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep., 9, 774-780.
11. Savic, N., Bar, D., Leone, S., Frommel, S.C., Weber, F.A., Vollenweider, E., Ferrari, E., Ziegler, U., Kaech, A., Shakhova, O. et al. (2014) lncRNA maturation to initiate heterochromatin formation in the nucleolus is required for exit from pluripotency in ESCs. Cell Stem Cell, 15, 720-734.
12. Postepska-Igielska, A., Krunic, D., Schmitt, N., Greulich-Bode, K.M., Boukamp, P. and Grummt, I. (2013) The chromatin remodelling complex NoRC safeguards genome stability by heterochromatin formation at telomeres and centromeres. EMBO Rep., 14, 704-710.
13. Gu, L., Frommel, S.C., Oakes, C.C., Simon, R., Grupp, K., Gerig, C.Y., Bar, D., Robinson, M.D., Baer, C., Weiss, M. et al. (2015) BAZ2A (TIP5) is involved in epigenetic alterations in prostate cancer and its overexpression predicts disease recurrence. Nat. Genet., 47, 22-30.
14. Hendrich, B. and Tweedie, S. (2003) The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet., 19, 269-277.
15. Aravind, L. and Landsman, D. (1998) AT-hook motifs identifed in a wide variety of DNA-binding proteins. Nucleic Acids Res., 26, 4413-4421.
16. Jeffery, L. and Nakielny, S. (2004) Components of the DNA methylation system of chromatin control are RNA-binding proteins. J. Biol. Chem., 279, 49479-49487.
17. Lukavsky, P.J. and Puglisi, J.D. (2004) Large-scale preparation and purifcation of polyacrylamide-free RNA oligonucleotides. RNA, 10, 889-893.
18. Wyatt, J.R., Chastain, M. and Puglisi, J.D. (1991) Synthesis and purifcation of large amounts of RNA oligonucleotides. Biotechniques, 11, 764-769.
19. Kao, C., Zheng, M. and Rudisser, S. (1999) A simple and effcient method to reduce nontemplated nucleotide addition at the 3 terminus of RNAs transcribed by T7 RNA polymerase. RNA, 5, 1268-1272.
20. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
21. Sattler, M., Schleucher, J. and Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed feld gradients. Prog. Nucl. Magn. Reson. Spectrosc., 34, 93-158.
22. Pastore, A. and Saudek, V. (1990) The relationship between chemical shift and secondary structure in proteins. J. Magn. Reson., 90, 165-176.
23. Spera, S. and Bax, A. (1991) Empirical correlation between protein backbone conformation and C.alpha. and C.beta. 13C nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc., 113, 5490-5492.
24. Yamazaki, T., Forman-Kay, J.D. and Kay, L.E. (1993) Two-dimensional NMR experiments for correlating carbon-13.beta. and proton.delta./.epsilon. chemical shifts of aromatic residues in 13C-labeled proteins via scalar couplings. J. Am. Chem. Soc., 115, 11054-11055.
25. Pelton, J.G., Torchia, D.A., Meadow, N.D. and Roseman, S. (1993) Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci., 2, 543-558.
26. Senn, H., Werner, B., Messerle, B.A., Weber, C., Traber, R. and Wuethrich, K. (1989) Stereospecifc assignment of the methyl 1H NMR lines of valine and leucine in polypeptides by nonrandom 13C labelling FEBS Lett., 249, 113-118.
27. Neri, D., Szyperski, T., Otting, G., Senn, H. and Wüthrich, K. (1989) Stereospecifc nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional 13C labeling. Biochemistry, 28, 7510-7516.
28. Jung, Y.S. and Zweckstetter, M. (2004) Mars-robust automatic backbone assignment of proteins. J. Biomol. NMR, 30, 11-23.
29. Guntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol., 278, 353-378.
30. Shen, Y, Delaglio, F., Cornilescu, G. and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR, 44, 213-223.
31. Cordier, F., Dingley, A.J. and Grzesiek, S. (1999) A doublet-separated sensitivity-enhanced HSQC for the determination of scalar and dipolar one-bond J-couplings. J. Biomol. NMR, 13, 175-180.
32. Ishii, Y, Markus, M.A. and Tycko, R. (2001) Controlling residual dipolar couplings in high-resolution NMR of proteins by strain induced alignment in a gel. J. Biomol. NMR, 21, 141-151.
33. Ottiger, M. and Bax, A. (1999) Bicelle-based liquid crystals for NMR-measurement of dipolar couplings at acidic and basic pH values. J. Biomol. NMR, 13, 187-191.
34. Farrow, NA., Muhandiram, R., Singer, A.U., Pascal, S.M., Kay, C.M., Gish, G., Shoelson, S.E., Pawson, T., Forman-Kay, J.D. and Kay, L.E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry, 33, 5984-6003.
35. Akke, M. and Palmer, A.G (1996) Monitoring macromolecular motions on microsecond to millisecond time scales by R1p -R1 constant relaxation time NMR spectroscopy. J. Am. Chem. Soc, 118, 911-912.
36. Kay, L.E., Torchia, D.A. and Bax, A. (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry, 28, 8972-8979.
37. Bruschweiler, R., Liao, X. andWright, P. (1995) Long-range motional restrictions in a multidomain zinc-fnger protein from anisotropic tumbling. Science, 268, 886-889.
38. Daragan, V.A. and Mayo, K.H. (1997) Motional model analyses of protein and peptide dynamics using 13C and 15N NMR relaxation. Prog. Nucl. Magn. Reson. Spectrosc, 31, 63-105.
39. Schanda, P and Brutscher, B. (2005) Very fast two-dimensional NMR spectroscopy for real-time investigation of dynamic events in proteins on the time scale of seconds. J. Am. Chem. Soc, 127, 8014-8015.
40. Linge, J.P, Habeck, M., Rieping, W. andNilges, M. (2003) ARIA: automated NOE assignment and NMR structure calculation. Bioinformatics, 19, 315-316.
41. Linge, J.P, Williams, M.A., Spronk, C.A., Bonvin, A.M. and Nilges, M. (2003) Refnement of protein structures in explicit solvent. Proteins, 50, 496-506.
42. Doreleijers, J.F., Sousa da Silva, A.W., Krieger, E., Nabuurs, S.B., Spronk, C.A., Stevens, T.J., Vranken, W.F., Vriend, G. and Vuister, GW. (2012) CING: an integrated residue-based structure validation program suite. J. Biomol. NMR, 54, 267-283.
43. Laskowski, R.A., Macarthur, M.W., Moss, D.S. andThornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst., 26, 283-291.
44. Vriend, G and Sander, C (1993) Quality control of protein models: directional atomic contact analysis. J. Appl. Crystallogr., 26, 47-60.
45. Cornilescu, G, Marquardt, J.L., Ottiger, M. and Bax, A. (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J. Am. Chem. Soc, 120, 6836-6837.
46. Stepanov, A.S., Voronina, A.S., Ovchinnikov, L.P and Spirin, A.S. (1971) RNA-binding protein factor of animal cell extracts. FEBS Lett., 18, 13-18.
47. Edgar, R.C (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
48. Larkin, M.A., Blackshields, G, Brown, NP, Chenna, R., McGettigan, PA., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
49. Letunic, I., Doerks, T. andBork, P (2009) SMART 6: recent updates and new developments. Nucleic Acids Res, 37, D229-D232.
50. Schultz, J., Milpetz, F., Bork, P and Ponting, CP (1998) SMART, a simple modular architecture research tool: identifcation of signaling domains. Proc Natl. Acad. Sci. U.S.A., 95, 5857-5864.
51. Finn, R.D., Mistry, J., Tate, J., Coggill, P, Heger, A., Pollington, J.E., Gavin, O.L., Gunasekaran, P, Ceric, G, Forslund, K. et al. (2010) The Pfam protein families database. Nucleic Acids Res., 38, D211-D222.
52. Ohki, I., Shimotake, N, Fujita, N, Jee, J., Ikegami, T, Nakao, M. and Shirakawa, M. (2001) Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell, 105, 487-497.
53. Ho, K.L., McNae, I.W., Schmiedeberg, L., Klose, R.J., Bird, A.P. and Walkinshaw, M.D. (2008) MeCP2 binding to DNA depends upon hydration at methyl-CpG. Mol. Cell, 29, 525-531.
54. Scarsdale, J.N., Webb, H.D., Ginder, G.D. and Williams, D.C. Jr (2011) Solution structure and dynamic analysis of chicken MBD2 methyl binding domain bound to a target-methylated DNA sequence. Nucleic Acids Res., 39, 6741-6752.
55. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
56. Gobl, C., Madl, T., Simon, B. and Sattler, M. (2014) NMR approaches for structural analysis of multidomain proteins and complexes in solution. Prog. Nucl. Magn. Reson. Spectrosc., 80C, 26-63.
57. Postepska-Igielska, A. and Grummt, I. (2014) NoRC silences rRNA genes, telomeres, and centromeres. Cell Cycle, 13, 493-494.
58. Bierhoff, H., Postepska-Igielska, A. and Grummt, I. (2014) Noisy silence: non-coding RNA and heterochromatin formation at repetitive elements. Epigenetics, 9, 53-61.