Piccolo NuA4-catalyzed acetylation of nucleosomal histones: Criticalroles of an Esa1 tudor/chromo barrel loop and an Epl1 enhancer of polycomb A (EPcA) basic region

Molecular and Cellular Biology

Volumn 33, Issue 1, 2013, Pages 159-169

  Huang, Jiehuan ^a   Tan, Song ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPL1 PROTEIN; ESA1 PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE H2A; HISTONE H2B; HISTONE H4; PICCOLO NUA4 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CATALYSIS; ENHANCER REGION; ENZYME ACTIVITY; ESCHERICHIA COLI; MICROBIAL VIABILITY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; XENOPUS;

ACETYLATION; AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; DNA; HISTONE ACETYLTRANSFERASES; HISTONES; MULTIPROTEIN COMPLEXES; MUTATION; NUCLEOSOMES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; XENOPUS;

EID: 84871864815     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01131-12     Document Type: Article

References (41)

1. Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Res. 21:381-395.
2. Rando OJ, Winston F. 2012. Chromatin and transcription in yeast. Genetics 190:351-387.
3. Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, Allis CD. 1996. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843-851.
4. Grant PA, Duggan L, Côté J, Roberts SM, Brownell JE, Candau R, Ohba R, Owen-Hughes T, Allis CD, Winston F, Berger SL, Workman JL. 1997. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 11:1640-1650.
5. Marmorstein R. 2001. Structure of histone acetyltransferases. J. Mol. Biol. 311:433-444.
6. Rojas JR, Trievel RC, Zhou J, Mo Y, Li X, Berger SL, Allis CD, Marmorstein R. 1999. Structure of Tetrahymena GCN5 bound to coenzyme A and a histone H3 peptide. Nature 401:93-98.
7. Trievel RC, Rojas JR, Sterner DE, Venkataramani RN, Wang L, Zhou J, Allis CD, Berger SL, Marmorstein R. 1999. Crystal structure and mechanism of histone acetylation of the yeast GCN5 transcriptional coactivator. Proc. Natl. Acad. Sci. U. S. A. 96:8931-8936.
8. Yan Y, Barlev NA, Haley RH, Berger SL, Marmorstein R. 2000. Crystal structure of yeast Esa1 suggests a unified mechanism for catalysis and substrate binding by histone acetyltransferases. Mol. Cell 6:1195-1205.
9. Clements A, Poux AN, Lo Pillus W-SL, Berger SL, Marmorstein R. 2003. Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol. Cell 12:461-473.
10. Lee J-S, Smith E, Shilatifard A. 2010. The language of histone crosstalk. Cell 142:682-685.
11. Boudreault AA, Cronier D, Selleck W, Lacoste N, Utley RT, Allard S, Savard J, Lane WS, Tan S, Côté J. 2003. Yeast enhancer of polycomb defines global Esa1-dependent acetylation of chromatin. Genes Dev. 17: 1415-1428.
12. Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197-208.
13. Patel A, Vought VE, Dharmarajan V, Cosgrove MS. 2011. A novel non-SET domain multi-subunit methyltransferase required for sequential nucleosomal histone H3 methylation by the mixed lineage leukemia protein- 1 (MLL1) core complex. J. Biol. Chem. 286:3359-3369.
14. Balasubramanian R, Pray-Grant MG, Selleck W, Grant PA, Tan S. 2002. Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation. J. Biol. Chem. 277:7989-7995.
15. Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, Verdine GL, Allis CD, Roeder RG. 2006. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat. Struct. Mol. Biol. 13:713-719.
16. Lee MG, Wynder C, Cooch N, Shiekhattar R. 2005. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437: 432-435.
17. Selleck W, Fortin I, Sermwittayawong D, Côté J, Tan S. 2005. The Saccharomyces cerevisiae Piccolo NuA4 histone acetyltransferase complex requires the Enhancer of Polycomb A domain and chromodomain to acetylate nucleosomes. Mol. Cell. Biol. 25:5535-5542.
18. Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CP. 2003. The Tudor domain "Royal Family": Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci. 28:69-74.
19. Eissenberg JC. 2012. Structural biology of the chromodomain: form and function. Gene 496:69-78.
20. Nielsen PR, Nietlispach D, Buscaino A, Warner RJ, Akhtar A, Murzin AG, Murzina NV, Laue ED. 2005. Structure of the chromo barrel domain from the MOF acetyltransferase. J. Biol. Chem. 280:32326-32331.
21. Shimojo H, Sano N, Moriwaki Y, Okuda M, Horikoshi M, Nishimura Y. 2008. Novel structural and functional mode of a knot essential for RNA binding activity of the Esa1 presumed chromodomain. J. Mol. Biol. 378: 987-1001.
22. Akhtar A, Zink D, Becker PB. 2000. Chromodomains are protein-RNA interaction modules. Nature 407:405-409.
23. Tan S, Kern RC, Selleck W. 2005. The pST44 polycistronic expression system for producing protein complexes in Escherichia coli. Protein Expr. Purif. 40:385-395.
24. Barrios A, Selleck W, Hnatkovich B, Kramer R, Sermwittayawong D, Tan S. 2007. Expression and purification of recombinant yeast Ada2/ Ada3/Gcn5 and Piccolo NuA4 histone acetyltransferase complexes. Methods 41:271-277.
25. Luger K, Rechsteiner TJ, Richmond TJ. 1999. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304:3-19.
26. Chin JW, Martin AB, King DS, Wang L, Schultz PG. 2002. Addition of a photocrosslinking amino acid to the genetic code of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99:11020-11024.
27. Ryu Y, Schultz PG. 2006. Efficient incorporation of unnatural amino acids into proteins in Escherichia coli. Nat. Methods 3:263-265.
28. Gietz D, St Jean A, Woods RA, Schiestl RH. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
29. Sharma VM, Tomar RS, Dempsey AE, Reese JC. 2007. Histone deacetylases RPD3 and HOS2 regulate the transcriptional activation of DNA damage-inducible genes. Mol. Cell. Biol. 27:3199-3210.
30. Gao YG, Su SY, Robinson H, Padmanabhan S, Lim L, McCrary BS, Edmondson SP, Shriver JW, Wang AH. 1998. The crystal structure of the hyperthermophile chromosomal protein Sso7d bound to DNA. Nat. Struct. Biol. 5:782-786.
31. Cobb CE, Beth AH. 1990. Identification of the eosinyl-5-maleimide reaction site on the human erythrocyte anion-exchange protein: overlap with the reaction sites of other chemical probes. Biochemistry 29:8283-8290.
32. Smyth DG, Blumenfeld OO, Konigsberg W. 1964. Reactions of Nethylmaleimide with peptides and amino acids. Biochem. J. 91:589-595.
33. Chahal HK, Dai Y, Saini A, Ayala-Castro C, Outten FW. 2009. The SufBCD Fe-S scaffold complex interacts with SufA for Fe-S cluster transfer. Biochemistry 48:10644-10653.
34. Layer G, Gaddam SA, Ayala-Castro CN, Ollagnier-de Choudens S, Lascoux D, Fontecave M, Outten FW. 2007. SufE transfers sulfur from SufS to SufB for iron-sulfur cluster assembly. J. Biol. Chem. 282:13342-13350.
35. Padrick SB, Doolittle LK, Brautigam CA, King DS, Rosen MK. 2011. Arp2/3 complex is bound and activated by twoWASPproteins. Proc. Natl. Acad. Sci. U. S. A. 108:E472-E479.
36. Conrad T, Cavalli FMG, Holz H, Hallacli E, Kind J, Ilik I, Vaquerizas JM, Luscombe NM, Akhtar A. 2012. The MOF chromobarrel domain controls genome-wide H4K16 acetylation and spreading of the MSL complex. Dev. Cell 22:610-624.
37. Decker PV, Yu DY, Iizuka M, Qiu Q, Smith MM. 2008. Catalytic-site mutations in the MYST family histone acetyltransferase Esa1. Genetics 178:1209-1220.
38. Chittuluru JR, Chaban Y, Monnet-Saksouk J, Carrozza MJ, Sapountzi V, Selleck W, Huang J, Utley RT, Cramet M, Allard S, Cai G, Workman JL, Fried MG, Tan S, Côté J, Asturias FJ. 2011. Structure and nucleosome interaction of the yeast NuA4 and Piccolo-NuA4 histone acetyltransferase complexes. Nat. Struct. Mol. Biol. 18:1196-1203.
39. Berndsen CE, Selleck W, McBryant SJ, Hansen JC, Tan S, Denu JM. 2007. Nucleosome recognition by the Piccolo NuA4 histone acetyltransferase complex. Biochemistry 46:2091-2099.
40. Makde RD, England JR, Yennawar HP, Tan S. 2010. Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467:562-566.
41. White CL, Suto RK, Luger K. 2001. Structure of the yeast nucleosome particle reveals fundamental changes in internucleosome interactions. EMBO J. 20:5207-5218.