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Structure paper

TitleMechanism of AAA+ ATPase-mediated RuvAB-Holliday junction branch migration.
Journal, issue, pagesNature, Vol. 609, Issue 7927, Page 630-639, Year 2022
Publish dateAug 24, 2022
AuthorsJiri Wald / Dirk Fahrenkamp / Nikolaus Goessweiner-Mohr / Wolfgang Lugmayr / Luciano Ciccarelli / Oliver Vesper / Thomas C Marlovits /
PubMed AbstractThe Holliday junction is a key intermediate formed during DNA recombination across all kingdoms of life. In bacteria, the Holliday junction is processed by two homo-hexameric AAA+ ATPase RuvB motors, ...The Holliday junction is a key intermediate formed during DNA recombination across all kingdoms of life. In bacteria, the Holliday junction is processed by two homo-hexameric AAA+ ATPase RuvB motors, which assemble together with the RuvA-Holliday junction complex to energize the strand-exchange reaction. Despite its importance for chromosome maintenance, the structure and mechanism by which this complex facilitates branch migration are unknown. Here, using time-resolved cryo-electron microscopy, we obtained structures of the ATP-hydrolysing RuvAB complex in seven distinct conformational states, captured during assembly and processing of a Holliday junction. Five structures together resolve the complete nucleotide cycle and reveal the spatiotemporal relationship between ATP hydrolysis, nucleotide exchange and context-specific conformational changes in RuvB. Coordinated motions in a converter formed by DNA-disengaged RuvB subunits stimulate hydrolysis and nucleotide exchange. Immobilization of the converter enables RuvB to convert the ATP-contained energy into a lever motion, which generates the pulling force driving the branch migration. We show that RuvB motors rotate together with the DNA substrate, which, together with a progressing nucleotide cycle, forms the mechanistic basis for DNA recombination by continuous branch migration. Together, our data decipher the molecular principles of homologous recombination by the RuvAB complex, elucidate discrete and sequential transition-state intermediates for chemo-mechanical coupling of hexameric AAA+ motors and provide a blueprint for the design of state-specific compounds targeting AAA+ motors.
External linksNature / PubMed:36002576 / PubMed Central
MethodsEM (single particle)
Resolution2.9 - 8.0 Å
Structure data

13294

7pbl

EMDB-13294, PDB-7pbl:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s1 [t2 dataset]
Method: EM (single particle) / Resolution: 3.2 Å

13295

7pbm

EMDB-13295, PDB-7pbm:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s2 [t2 dataset]
Method: EM (single particle) / Resolution: 3.2 Å

13296

7pbn

EMDB-13296, PDB-7pbn:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s3 [t2 dataset]
Method: EM (single particle) / Resolution: 3.2 Å

13297

7pbo

EMDB-13297, PDB-7pbo:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s4 [t2 dataset]
Method: EM (single particle) / Resolution: 2.9 Å

13298

7pbp

EMDB-13298, PDB-7pbp:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s5 [t2 dataset]
Method: EM (single particle) / Resolution: 3.2 Å

13299

7pbq

EMDB-13299, PDB-7pbq:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s0+A [t2 dataset]
Method: EM (single particle) / Resolution: 3.1 Å

13300

7pbr

EMDB-13300, PDB-7pbr:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s0-A [t2 dataset]
Method: EM (single particle) / Resolution: 3.0 Å

13301

7pbs

EMDB-13301, PDB-7pbs:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s0+A [t1 dataset]
Method: EM (single particle) / Resolution: 3.3 Å

13302

7pbt

EMDB-13302, PDB-7pbt:
RuvAB branch migration motor complexed to the Holliday junction - RuvB AAA+ state s1 [t1 dataset]
Method: EM (single particle) / Resolution: 3.3 Å

13303

7pbu

EMDB-13303, PDB-7pbu:
RuvAB branch migration motor complexed to the Holliday junction - RuvA-HJ core [t2 dataset]
Method: EM (single particle) / Resolution: 3.3 Å

EMDB-13304: RuvAB branch migration motor complexed to the Holliday junction - RuvAB-HJ half [dataset t2]
Method: EM (single particle) / Resolution: 3.9 Å

EMDB-13305: RuvAB branch migration motor complexed to the Holliday junction - RuvAB-HJ pseudo half [dataset t2]
Method: EM (single particle) / Resolution: 4.4 Å

EMDB-15085: RuvAB branch migration motor complexed to the Holliday junction - composite map 1 and 2
Method: EM (single particle) / Resolution: 8.0 Å

EMDB-15126: RuvAB branch migration motor complexed to the Holliday junction - full tripartite particle [dataset t2]
Method: EM (single particle) / Resolution: 8.0 Å

Chemicals

ChemComp-AGS:
PHOSPHOTHIOPHOSPHORIC ACID-ADENYLATE ESTER / ATP-gamma-S, energy-carrying molecule analogue*YM

ChemComp-MG:
Unknown entry

ChemComp-ADP:
ADENOSINE-5'-DIPHOSPHATE / ADP, energy-carrying molecule*YM

Source
  • streptococcus thermophilus (bacteria)
  • salmonella typhimurium (bacteria)
  • synthetic construct (others)
KeywordsHYDROLASE / DNA recombination / DNA repair / branch migration / Holliday junction / helicase

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