Snf2 family ATPases and DExx box helicases: differences and unifying concepts from high-resolution crystal structures

Proteins with sequence similarity to the yeast Snf2 protein form a large family of ATPases that act to alter the structure of a diverse range of DNA–protein structures including chromatin. Snf2 family enzymes are related in sequence to DExx box helicases, yet they do not possess helicase activity. Recent biochemical and structural studies suggest that the mechanism by which these enzymes act involves ATP-dependent translocation on DNA. Crystal structures suggest that these enzymes travel along the minor groove, a process that can generate the torque or energy in remodelling processes. We review the recent structural and biochemical findings which suggest a common mechanistic basis underlies the action of many of both Snf2 family and DExx box helicases.

[1]  PhD Anthony Oro MD,et al.  Molecular Analysis , 2020, Definitions.

[2]  Geoffrey J. Barton,et al.  Identification of multiple distinct Snf2 subfamilies with conserved structural motifs , 2006, Nucleic acids research.

[3]  Cees Dekker,et al.  When a helicase is not a helicase: dsDNA tracking by the motor protein EcoR124I , 2006, The EMBO journal.

[4]  O. Nureki,et al.  Structural Basis for RNA Unwinding by the DEAD-Box Protein Drosophila Vasa , 2006, Cell.

[5]  D. Auble,et al.  Snf2/Swi2‐related ATPase Mot1 drives displacement of TATA‐binding protein by gripping DNA , 2006, The EMBO journal.

[6]  M. Zofall,et al.  Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome , 2006, Nature Structural &Molecular Biology.

[7]  N. Savery,et al.  Structural Basis for Bacterial Transcription-Coupled DNA Repair , 2006, Cell.

[8]  D. Dunlap,et al.  Direct observation of DNA distortion by the RSC complex. , 2006, Molecular cell.

[9]  I. Tinoco,et al.  RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP , 2006, Nature.

[10]  Danny Reinberg,et al.  Human but Not Yeast CHD1 Binds Directly and Selectively to Histone H3 Methylated at Lysine 4 via Its Tandem Chromodomains* , 2005, Journal of Biological Chemistry.

[11]  Taekjip Ha,et al.  Repetitive shuttling of a motor protein on DNA , 2005, Nature.

[12]  Anjanabha Saha,et al.  Chromatin remodeling through directional DNA translocation from an internal nucleosomal site , 2005, Nature Structural &Molecular Biology.

[13]  C. Körner,et al.  X-Ray Structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase Core and Its Complex with DNA , 2005, Cell.

[14]  D. Auble,et al.  Mot1‐mediated control of transcription complex assembly and activity , 2005, The EMBO journal.

[15]  R. G. Lloyd,et al.  DNA Binding by the Substrate Specificity (Wedge) Domain of RecG Helicase Suggests a Role in Processivity* , 2005, Journal of Biological Chemistry.

[16]  Smita S. Patel,et al.  A Brownian motor mechanism of translocation and strand separation by hepatitis C virus helicase , 2005, Nature Structural &Molecular Biology.

[17]  A. Alexeev,et al.  Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54 , 2005, Nature Structural &Molecular Biology.

[18]  R. Kingston,et al.  Swapping function of two chromatin remodeling complexes. , 2005, Molecular cell.

[19]  J. Hoeijmakers,et al.  The CSB Protein Actively Wraps DNA* , 2005, Journal of Biological Chemistry.

[20]  John R. Yates,et al.  Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation , 2005, Nature.

[21]  Dale B. Wigley,et al.  Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks , 2004, Nature.

[22]  Imre Berger,et al.  Reaction cycle of the yeast Isw2 chromatin remodeling complex , 2004, The EMBO journal.

[23]  V. Serebrov,et al.  Periodic cycles of RNA unwinding and pausing by hepatitis C virus NS3 helicase , 2004, Nature.

[24]  H. Shinagawa,et al.  Direct evidence that a conserved arginine in RuvB AAA+ ATPase acts as an allosteric effector for the ATPase activity of the adjacent subunit in a hexamer. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Zofall,et al.  Topography of the ISW2–nucleosome complex: insights into nucleosome spacing and chromatin remodeling , 2004, The EMBO journal.

[26]  A. Pyle,et al.  Backbone tracking by the SF2 helicase NPH-II , 2004, Nature Structural &Molecular Biology.

[27]  Errol C Friedberg,et al.  The yeast Rad7/Rad16/Abf1 complex generates superhelical torsion in DNA that is required for nucleotide excision repair. , 2004, DNA repair.

[28]  C. Peterson,et al.  The SANT domain: a unique histone-tail-binding module? , 2004, Nature Reviews Molecular Cell Biology.

[29]  Wei-Hua Wu,et al.  ATP-Driven Exchange of Histone H2AZ Variant Catalyzed by SWR1 Chromatin Remodeling Complex , 2004, Science.

[30]  Nicholas Proudfoot,et al.  Isw1 Chromatin Remodeling ATPase Coordinates Transcription Elongation and Termination by RNA Polymerase II , 2003, Cell.

[31]  C. Müller,et al.  Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. , 2003, Molecular cell.

[32]  M. Guenther,et al.  A SANT motif in the SMRT corepressor interprets the histone code and promotes histone deacetylation , 2003, The EMBO journal.

[33]  Smita S. Patel,et al.  ATP Binding Modulates the Nucleic Acid Affinity of Hepatitis C Virus Helicase* , 2003, Journal of Biological Chemistry.

[34]  Hien G. Tran,et al.  Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes , 2003, The EMBO journal.

[35]  T. Owen-Hughes,et al.  Evidence for DNA Translocation by the ISWI Chromatin-Remodeling Enzyme , 2003, Molecular and Cellular Biology.

[36]  P. Sung,et al.  Rad54p Is a Chromatin Remodeling Enzyme Required for Heteroduplex DNA Joint Formation with Chromatin* , 2003, The Journal of Biological Chemistry.

[37]  R. G. Lloyd,et al.  A model for dsDNA translocation revealed by a structural motif common to RecG and Mfd proteins , 2003, The EMBO journal.

[38]  J. Svejstrup.  Rescue of arrested RNA polymerase II complexes , 2003, Journal of Cell Science.

[39]  C. Peterson,et al.  Structural analysis of the yeast SWI/SNF chromatin remodeling complex , 2003, Nature Structural Biology.

[40]  C. Peterson,et al.  Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. , 2002, Molecular cell.

[41]  W. Vermeulen,et al.  When machines get stuck--obstructed RNA polymerase II: displacement, degradation or suicide. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[42]  Anjanabha Saha,et al.  Chromatin remodeling by RSC involves ATP-dependent DNA translocation. , 2002, Genes & development.

[43]  G. Längst,et al.  The dMi‐2 chromodomains are DNA binding modules important for ATP‐dependent nucleosome mobilization , 2002, The EMBO journal.

[44]  D. Wigley,et al.  Modularity and Specialization in Superfamily 1 and 2 Helicases , 2002, Journal of bacteriology.

[45]  H. Erdjument-Bromage,et al.  A Rad26–Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage , 2002, Nature.

[46]  D. Mckay,et al.  Helicase structure and mechanism. , 2002, Current opinion in structural biology.

[47]  J. E. Cabrera,et al.  RapA, a bacterial homolog of SWI2/SNF2, stimulates RNA polymerase recycling in transcription. , 2001, Genes & development.

[48]  D. Wigley,et al.  Structural Analysis of DNA Replication Fork Reversal by RecG , 2001, Cell.

[49]  Ding‐Shinn Chen,et al.  Structure-Based Mutational Analysis of the Hepatitis C Virus NS3 Helicase , 2001, Journal of Virology.

[50]  R. Kanaar,et al.  The architecture of the human Rad54–DNA complex provides evidence for protein translocation along DNA , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[51]  D. Lilley,et al.  Generation of Superhelical Torsion by ATP-Dependent Chromatin Remodeling Activities , 2000, Cell.

[52]  George M Church,et al.  The Isw2 Chromatin Remodeling Complex Represses Early Meiotic Genes upon Recruitment by Ume6p , 2000, Cell.

[53]  P. Sung,et al.  Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. , 2000, Molecular cell.

[54]  Ali Hamiche,et al.  A chromatin remodelling complex involved in transcription and DNA processing , 2000, Nature.

[55]  T. Owen-Hughes,et al.  Mechanisms for ATP-dependent chromatin remodelling. , 2000, Current opinion in genetics & development.

[56]  D. Wigley,et al.  Uncoupling DNA translocation and helicase activity in PcrA: direct evidence for an active mechanism , 2000, The EMBO journal.

[57]  V. Iyer,et al.  The chromo domain protein Chd1p from budding yeast is an ATP‐dependent chromatin‐modifying factor , 2000, The EMBO journal.

[58]  P. Becker,et al.  Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. , 2000, Molecular cell.

[59]  P. Sung,et al.  Yeast Rad54 Promotes Rad51-dependent Homologous DNA Pairing via ATP Hydrolysis-driven Change in DNA Double Helix Conformation* , 1999, The Journal of Biological Chemistry.

[60]  Lei Zeng,et al.  Structure and ligand of a histone acetyltransferase bromodomain , 1999, Nature.

[61]  S. Velankar,et al.  Crystal Structures of Complexes of PcrA DNA Helicase with a DNA Substrate Indicate an Inchworm Mechanism , 1999, Cell.

[62]  R. Kingston,et al.  Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. , 1999, Molecular cell.

[63]  J. Workman,et al.  The SWI/SNF Complex Creates Loop Domains in DNA and Polynucleosome Arrays and Can Disrupt DNA-Histone Contacts within These Domains , 1999, Molecular and Cellular Biology.

[64]  G. Längst,et al.  ISWI is an ATP-dependent nucleosome remodeling factor. , 1999, Molecular cell.

[65]  D. Auble,et al.  Testing for DNA Tracking by MOT1, a SNF2/SWI2 Protein Family Member , 1999, Molecular and Cellular Biology.

[66]  J. Hoeijmakers,et al.  The Human Rad54 Recombinational DNA Repair Protein Is a Double-stranded DNA-dependent ATPase* , 1998, The Journal of Biological Chemistry.

[67]  P. Sung,et al.  Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins , 1998, Nature.

[68]  J P Griffith,et al.  Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. , 1998, Structure.

[69]  J. Buerstedde,et al.  Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. , 1997, Genetics.

[70]  A. Buchman,et al.  Identification of a member of a DNA-dependent ATPase family that causes interference with silencing , 1997, Molecular and cellular biology.

[71]  D. Auble,et al.  Molecular analysis of the SNF2/SWI2 protein family member MOT1, an ATP-driven enzyme that dissociates TATA-binding protein from DNA , 1997, Molecular and cellular biology.

[72]  Ryuji Kobayashi,et al.  ACF, an ISWI-Containing and ATP-Utilizing Chromatin Assembly and Remodeling Factor , 1997, Cell.

[73]  F. Ahne,et al.  The RAD5 gene product is involved in the avoidance of non-homologous end-joining of DNA double strand breaks in the yeast Saccharomyces cerevisiae. , 1997, Nucleic acids research.

[74]  L. Bird,et al.  Crystal structure of a DExx box DNA helicase , 1996, Nature.

[75]  C. Peterson,et al.  Functional analysis of the DNA-stimulated ATPase domain of yeast SWI2/SNF2. , 1996, Nucleic acids research.

[76]  G. Crabtree,et al.  Diversity and specialization of mammalian SWI/SNF complexes. , 1996, Genes & development.

[77]  T. Gibson,et al.  The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB. , 1996, Trends in biochemical sciences.

[78]  Craig L. Peterson,et al.  DNA-binding properties of the yeast SWI/SNF complex , 1996, Nature.

[79]  Carl Wu,et al.  Purification and properties of an ATP-dependent nucleosome remodeling factor , 1995, Cell.

[80]  Vasily M. Studitsky,et al.  Overcoming a nucleosomal barrier to transcription , 1995, Cell.

[81]  J A Eisen,et al.  Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. , 1995, Nucleic acids research.

[82]  Jaap,et al.  RAD26, the functional S. cerevisiae homolog of the Cockayne syndrome B gene ERCC6. , 1994, The EMBO journal.

[83]  J. Thorner,et al.  Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. , 1994, Genes & development.

[84]  J. Workman,et al.  Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. , 1994, Science.

[85]  M. Carlson,et al.  The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. , 1993, Genes & development.

[86]  H. Feldmann,et al.  Molecular analysis of yeast chromosome II between CMD1 and LYS2: The excision repair gene RAD16 located in this region belongs to a novel group of double‐finger proteins , 1992, Yeast.

[87]  M. Carlson,et al.  An essential Saccharomyces cerevisiae gene homologous to SNF2 encodes a helicase-related protein in a new family , 1992, Molecular and cellular biology.

[88]  J. Thorner,et al.  A presumptive helicase (MOT1 gene product) affects gene expression and is required for viability in the yeast Saccharomyces cerevisiae , 1992, Molecular and cellular biology.

[89]  I. Herskowitz,et al.  Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription , 1992, Cell.

[90]  E. Koonin,et al.  Superfamily of UvrA-related NTP-binding proteins. Implications for rational classification of recombination/repair systems. , 1990, Journal of molecular biology.

[91]  A. Alexeev,et al.  Thoma, N.H. et al. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat. Struct. Mol. Biol. 12, 350-356 , 2005 .

[92]  R. Kornberg,et al.  Electron microscopic analysis of the RSC chromatin remodeling complex. , 2004, Methods in enzymology.

[93]  W. Hörz,et al.  ATP-dependent nucleosome remodeling. , 2002, Annual review of biochemistry.