A Nucleotide-Driven Switch Regulates Flanking DNA Length Sensing by a Dimeric Chromatin Remodeler

Molecular Cell

Volumn 57, Issue 5, 2015, Pages 850-859

  Leonard, John D ^a,b   Narlikar, Geeta J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; DIMER; MONOMER; NUCLEOTIDE; PROTEIN; SNF2H PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BAZ1A PROTEIN, HUMAN; CHROMATIN; DNA; FLUORESCENT DYE; NONHISTONE PROTEIN; NUCLEOSOME; PROTEIN BINDING; SMARCA5 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATIONAL TRANSITION; COVALENT BOND; DIMERIZATION; DNA BINDING; DNA FLANKING REGION; DNA STRUCTURE; ELECTROPHORETIC MOBILITY; FLANKING DNA LENGTH; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL MOBILITY SHIFT ASSAY; HAND SANT SLIDE DOMAIN; HUMAN; HYDROLYSIS; NUCLEOSOME; PROTEIN STRUCTURE; PROTOMER; THERMODYNAMICS; WILD TYPE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CHROMATIN; CONFORMATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; NUCLEOTIDES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS; TRANSCRIPTION FACTORS;

EID: 84924041052     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.01.008     Document Type: Article

References (43)

1. Blosser T.R., Yang J.G., Stone M.D., Narlikar G.J., Zhuang X. Dynamics of nucleosome remodelling by individual ACF complexes. Nature 2009, 462:1022-1027.
2. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78:273-304.
3. Clapier C.R., Cairns B.R. Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 2012, 492:280-284.
4. Clapier C.R., Längst G., Corona D.F., Becker P.B., Nightingale K.P. Critical role for the histone H4N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 2001, 21:875-883.
5. Collins N., Poot R.A., Kukimoto I., García-Jiménez C., Dellaire G., Varga-Weisz P.D. An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat. Genet. 2002, 32:627-632.
6. Dang W., Bartholomew B. Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol. Cell. Biol. 2007, 27:8306-8317.
7. Davey C.A., Sargent D.F., Luger K., Maeder A.W., Richmond T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J.Mol. Biol. 2002, 319:1097-1113.
8. Deindl S., Hwang W.L., Hota S.K., Blosser T.R., Prasad P., Bartholomew B., Zhuang X. ISWI remodelers slide nucleosomes with coordinated multi-base-pair entry steps and single-base-pair exit steps. Cell 2013, 152:442-452.
9. Del Campo M., Lambowitz A.M. Structure of the Yeast DEAD box protein Mss116p reveals two wedges that crimp RNA. Mol. Cell 2009, 35:598-609.
10. Deuring R., Fanti L., Armstrong J.A., Sarte M., Papoulas O., Prestel M., Daubresse G., Verardo M., Moseley S.L., Berloco M., et al. The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure invivo. Mol. Cell 2000, 5:355-365.
11. Fan H.Y., Narlikar G.J., Kingston R.E. Noncovalent modification of chromatin: different remodeled products with different ATPase domains. Cold Spring Harb. Symp. Quant. Biol. 2004, 69:183-192.
12. Fyodorov D.V., Blower M.D., Karpen G.H., Kadonaga J.T. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin invivo. Genes Dev. 2004, 18:170-183.
13. 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.
14. Grüne T., Brzeski J., Eberharter A., Clapier C.R., Corona D.F.V., Becker P.B., Müller C.W. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 2003, 12:449-460.
15. 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.
16. He X., Fan H.-Y., Narlikar G.J., Kingston R.E. Human ACF1 alters the remodeling strategy of SNF2h. J.Biol. Chem. 2006, 281:28636-28647.
17. He X., Fan H.-Y., Garlick J.D., Kingston R.E. Diverse regulation of SNF2h chromatin remodeling by noncatalytic subunits. Biochemistry 2008, 47:7025-7033.
18. Hota S.K., Bhardwaj S.K., Deindl S., Lin Y.-C., Zhuang X., Bartholomew B. Nucleosome mobilization by ISW2 requires the concerted action of the ATPase and SLIDE domains. Nat. Struct. Mol. Biol. 2013, 20:222-229.
19. Hwang W.L., Deindl S., Harada B.T., Zhuang X. Histone H4 tail mediates allosteric regulation of nucleosome remodelling by linker DNA. Nature 2014, 512:213-217.
20. Ito T., Bulger M., Pazin M.J., Kobayashi R., Kadonaga J.T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 1997, 90:145-155.
21. Kagalwala M.N., Glaus B.J., Dang W., Zofall M., Bartholomew B. Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodeling. EMBO J. 2004, 23:2092-2104.
22. Kelley L.A., Sternberg M.J.E. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
23. 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.
24. 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.
25. Ludwigsen J., Klinker H., Mueller-Planitz F. No need for a power stroke in ISWI-mediated nucleosome sliding. EMBO Rep. 2013, 14:1092-1097.
26. Mueller-Planitz F., Klinker H., Ludwigsen J., Becker P.B. The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat. Struct. Mol. Biol. 2013, 20:82-89.
27. Narlikar G.J., Phelan M.L., Kingston R.E. Generation and interconversion of multiple distinct nucleosomal states as a mechanism for catalyzing chromatin fluidity. Mol. Cell 2001, 8:1219-1230.
28. Narlikar G.J., Sundaramoorthy R., Owen-Hughes T. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 2013, 154:490-503.
29. Nodelman I.M., Bowman G.D. Nucleosome sliding by Chd1 does not require rigid coupling between DNA-binding and ATPase domains. EMBO Rep. 2013, 14:1098-1103.
30. Popp M.W., Antos J.M., Grotenbreg G.M., Spooner E., Ploegh H.L. Sortagging: a versatile method for protein labeling. Nat. Chem. Biol. 2007, 3:707-708.
31. Popp M.W.-L., Antos J.M., Ploegh H.L. Site-specific protein labeling via sortase-mediated transpeptidation. Curr. Protoc. Protein Sci. 2009, Chapter 15. Unit 15.3.
32. Racki L.R., Yang J.G., Naber N., Partensky P.D., Acevedo A., Purcell T.J., Cooke R., Cheng Y., Narlikar G.J. The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 2009, 462:1016-1021.
33. Racki L.R., Naber N., Pate E., Leonard J.D., Cooke R., Narlikar G.J. The histone H4 tail regulates the conformation of the ATP-binding pocket in the SNF2h chromatin remodeling enzyme. J.Mol. Biol. 2014, 426:2034-2044.
34. Rayment I., Smith C., Yount R.G. The active site of myosin. Annu. Rev. Physiol. 1996, 58:671-702.
35. Shahian T., Narlikar G.J. Analysis of changes in nucleosome conformation using fluorescence resonance energy transfer. Methods Mol. Biol. 2012, 833:337-349.
36. 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.
37. Thomsen N.D., Berger J.M. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 2009, 139:523-534.
38. Whitehouse I., Stockdale C., Flaus A., Szczelkun M.D., Owen-Hughes T. Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme. Mol. Cell. Biol. 2003, 23:1935-1945.
39. Yamada K., Frouws T.D., Angst B., Fitzgerald D.J., DeLuca C., Schimmele K., Sargent D.F., Richmond T.J. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 2011, 472:448-453.
40. Yang J.G., Narlikar G.J. FRET-based methods to study ATP-dependent changes in chromatin structure. Methods 2007, 41:291-295.
41. Yang J.G., Madrid T.S., Sevastopoulos E., Narlikar G.J. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat. Struct. Mol. Biol. 2006, 13:1078-1083.
42. Zakeri B., Fierer J.O., Celik E., Chittock E.C., Schwarz-Linek U., Moy V.T., Howarth M. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc. Natl. Acad. Sci. USA 2012, 109:E690-E697.
43. Zofall M., Persinger J., Bartholomew B. Functional role of extranucleosomal DNA and the entry site of the nucleosome in chromatin remodeling by ISW2. Mol. Cell. Biol. 2004, 24:10047-10057.