The Chromodomains of the Chd1 Chromatin Remodeler Regulate DNA Access to the ATPase Motor

Molecular Cell

Volumn 39, Issue 5, 2010, Pages 711-723

  Hauk, Glenn ^a   McKnight, Jeffrey N ^a   Nodelman, Ilana M ^a   Bowman, Gregory D ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

DNA

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA; CHD1 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; FUNGAL DNA; HISTONE; NUCLEOSOME; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHANNEL GATING; CHROMATIN; CHROMATIN CHD1; CRYSTAL STRUCTURE; DNA BINDING; NONHUMAN; NUCLEOSOME; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATASES; CHROMATIN ASSEMBLY AND DISASSEMBLY; CRYSTALLOGRAPHY, X-RAY; DNA, FUNGAL; DNA-BINDING PROTEINS; HISTONES; NUCLEOSOMES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 77956522905     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.08.012     Document Type: Article

References (49)

1. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W., Read R.J., Sacchettini J.C., Sauter N.K., Terwilliger T.C. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1948-1954.
2. Alexiadis V., Lusser A., Kadonaga J.T. A conserved N-terminal motif in Rad54 is important for chromatin remodeling and homologous strand pairing. J. Biol. Chem. 2004, 279:27824-27829.
3. Baker N.A., Sept D., Joseph S., Holst M.J., McCammon J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 2001, 98:10037-10041.
4. Beitz E. TEXshade: shading and labeling of multiple sequence alignments using LATEX2 epsilon. Bioinformatics 2000, 16:135-139.
5. Büttner K., Nehring S., Hopfner K.P. Structural basis for DNA duplex separation by a superfamily-2 helicase. Nat. Struct. Mol. Biol. 2007, 14:647-652.
6. The CCP4 suite programs for protein crystallography. Acta Crystallogr. D 1994, 59:760-763. CCP4 (Collaborative Computational Project Number 4).
7. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78:273-304.
8. Clapier C.R., Längst G., Corona D.F., Becker P.B., Nightingale K.P. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 2001, 21:875-883.
9. Dang W., Kagalwala M.N., Bartholomew B. Regulation of ISW2 by concerted action of histone H4 tail and extranucleosomal DNA. Mol. Cell. Biol. 2006, 26:7388-7396.
10. Delmas V., Stokes D.G., Perry R.P. A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain. Proc. Natl. Acad. Sci. USA 1993, 90:2414-2418.
11. Dueber J.E., Yeh B.J., Bhattacharyya R.P., Lim W.A. Rewiring cell signaling: the logic and plasticity of eukaryotic protein circuitry. Curr. Opin. Struct. Biol. 2004, 14:690-699.
12. Dürr H., Korner C., Muller M., Hickmann V., Hopfner K.P. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 2005, 121:363-373.
13. Ferreira H., Flaus A., Owen-Hughes T. Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J. Mol. Biol. 2007, 374:563-579.
14. Flanagan J.F., Mi L.Z., Chruszcz M., Cymborowski M., Clines K.L., Kim Y., Minor W., Rastinejad F., Khorasanizadeh S. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 2005, 438:1181-1185.
15. Flanagan J.F., Blus B.J., Kim D., Clines K.L., Rastinejad F., Khorasanizadeh S. Molecular implications of evolutionary differences in CHD double chromodomains. J. Mol. Biol. 2007, 369:334-342.
16. Gangaraju V.K., Prasad P., Srour A., Kagalwala M.N., Bartholomew B. Conformational changes associated with template commitment in ATP-dependent chromatin remodeling by ISW2. Mol. Cell 2009, 35:58-69.
17. Hamiche A., Kang J.G., Dennis C., Xiao H., Wu C. Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proc. Natl. Acad. Sci. USA 2001, 98:14316-14321.
18. Kiianitsa K., Solinger J.A., Heyer W.D. NADH-coupled microplate photometric assay for kinetic studies of ATP-hydrolyzing enzymes with low and high specific activities. Anal. Biochem. 2003, 321:266-271.
19. Kim J.L., Morgenstern K.A., Griffith J.P., Dwyer M.D., Thomson J.A., Murcko M.A., Lin C., Caron P.R. Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure 1998, 6:89-100.
20. Kleywegt G.J., Jones T.A. Efficient rebuilding of protein structures. Acta Crystallogr. D Biol. Crystallogr. 1996, 52:829-832.
21. Konev A.Y., Tribus M., Park S.Y., Podhraski V., Lim C.Y., Emelyanov A.V., Vershilova E., Pirrotta V., Kadonaga J.T., Lusser A., Fyodorov D.V. CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 2007, 317:1087-1090.
22. La Fortelle E.D., Bricogne G. Maximum-likelihood heavy-atom parameter refinement in the MIR and MAD methods. Methods in Enzymology 1997, 476-494. Academic Press, New York. C.W. Carter, R.M. Sweet (Eds.).
23. Lake R.J., Geyko A., Hemashettar G., Zhao Y., Fan H.Y. UV-induced association of the CSB remodeling protein with chromatin requires ATP-dependent relief of N-terminal autorepression. Mol. Cell 2010, 37:235-246.
24. Längst G., Bonte E.J., Corona D.F., Becker P.B. Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell 1999, 97:843-852.
25. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
26. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993, 26:283-291.
27. Lowary P.T., Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 1998, 276:19-42.
28. Luger K., Rechsteiner T.J., Richmond T.J. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 1999, 304:3-19.
29. Lusser A., Urwin D.L., Kadonaga J.T. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat. Struct. Mol. Biol. 2005, 12:160-166.
30. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 1997, 53:240-255.
31. Okada M., Okawa K., Isobe T., Fukagawa T. CENP-H-containing complex facilitates centromere deposition of CENP-A in cooperation with FACT and CHD1. Mol. Biol. Cell 2009, 20:3986-3995.
32. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology 1997, 307-326. Academic Press, New York. C.W. Carter, R.M. Sweet (Eds.).
33. Pufall M.A., Graves B.J. Autoinhibitory domains: modular effectors of cellular regulation. Annu. Rev. Cell Dev. Biol. 2002, 18:421-462.
34. Saha A., Wittmeyer J., Cairns B.R. Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat. Struct. Mol. Biol. 2005, 12:747-755.
35. Schwanbeck R., Xiao H., Wu C. Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J. Biol. Chem. 2004, 279:39933-39941.
36. Sengoku T., Nureki O., Nakamura A., Kobayashi S., Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 2006, 125:287-300.
37. Shaw G., Gan J., Zhou Y.N., Zhi H., Subburaman P., Zhang R., Joachimiak A., Jin D.J., Ji X. Structure of RapA, a Swi2/Snf2 protein that recycles RNA polymerase during transcription. Structure 2008, 16:1417-1427.
38. Sigurdsson S., Van Komen S., Petukhova G., Sung P. Homologous DNA pairing by human recombination factors Rad51 and Rad54. J. Biol. Chem. 2002, 277:42790-42794.
39. Simic R., Lindstrom D.L., Tran H.G., Roinick K.L., Costa P.J., Johnson A.D., Hartzog G.A., Arndt K.M. Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J. 2003, 22:1846-1856.
40. Sims R.J., Chen C.F., Santos-Rosa H., Kouzarides T., Patel S.S., Reinberg D. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem. 2005, 280:41789-41792.
41. Singleton M.R., Dillingham M.S., Wigley D.B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 2007, 76:23-50.
42. Stockdale C., Flaus A., Ferreira H., Owen-Hughes T. Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J. Biol. Chem. 2006, 281:16279-16288.
43. Stokes D.G., Perry R.P. DNA-binding and chromatin localization properties of CHD1. Mol. Cell. Biol. 1995, 15:2745-2753.
44. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 1999, 55:849-861.
45. Thoma N.H., Czyzewski B.K., Alexeev A.A., Mazin A.V., Kowalczykowski S.C., Pavletich N.P. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat. Struct. Mol. Biol. 2005, 12:350-356.
46. Tran H.G., Steger D.J., Iyer V.R., Johnson A.D. The chromo domain protein chd1p from budding yeast is an ATP-dependent chromatin-modifying factor. EMBO J. 2000, 19:2323-2331.
47. Tsukiyama T., Palmer J., Landel C.C., Shiloach J., Wu C. Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev. 1999, 13:686-697.
48. Walfridsson J., Khorosjutina O., Matikainen P., Gustafsson C.M., Ekwall K. A genome-wide role for CHD remodelling factors and Nap1 in nucleosome disassembly. EMBO J. 2007, 26:2868-2879.
49. Zofall M., Persinger J., Kassabov S.R., Bartholomew B. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat. Struct. Mol. Biol. 2006, 13:339-346.