MuB is an AAA+ ATPase that forms helical filaments to control target selection for DNA transposition

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 27, 2013, Pages

  Mizuno, Naoko ^a,b   Dramicánin, Marija ^c   Mizuuchi, Michiyo ^d   Adam, Julia ^b   Wang, Yi ^d,e   Han, Yong Woon ^d,f   Yang, Wei ^d   Steven, Alasdair C ^a   Mizuuchi, Kiyoshi ^d   Ramoń Maiques, Santiago ^c,d  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c Structural Biology and Biocomputing Programme   (Spain)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f KYOTO UNIVERSITY   (Japan)

Author keywords

Nucleoprotein filament; Phage Mu

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA BINDING PROTEIN; DNA FRAGMENT; DOUBLE STRANDED DNA; MUB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; DNA BINDING; DNA FRAGMENTATION; DNA TRANSPOSITION; ELECTRON MICROSCOPY; MOLECULAR DOCKING; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN INTERACTION; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS;

NUCLEOPROTEIN FILAMENT; PHAGE MU;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BACTERIOPHAGE MU; BINDING SITES; DNA, VIRAL; DNA-BINDING PROTEINS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY, AMINO ACID; TRANSPOSASES; VIRAL PROTEINS;

ENTEROBACTERIA PHAGE MU;

EID: 84879705192     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1309499110     Document Type: Article

References (53)

1. Shapiro JA (2010) Mobile DNA and evolution in the 21st century. Mob DNA 1(1):4-18.
2. Craig NL (1997) Target site selection in transposition. Annu Rev Biochem 66:437-474.
3. Mizuuchi K (1992) Transpositional recombination: Mechanistic insights from studies of mu and other elements. Annu Rev Biochem 61:1011-1051.
4. Chaconas G, Harshey RM (2002) Mobile DNA II, eds Craig NL, Craigie R, Gellert M, Lambowitz A (ASM Press, Washington, DC), pp 384-402.
5. Robinson MK, Bennett PM, Richmond MH (1977) Inhibition of TnA translocation by TnA. J Bacteriol 129(1):407-414. (Pubitemid 8018609)
6. Lee CH, Bhagwat A, Heffron F (1983) Identification of a transposon Tn3 sequence required for transposition immunity. Proc Natl Acad Sci USA 80(22):6765-6769. (Pubitemid 14243228)
7. Hauer B, Shapiro JA (1984) Control of Tn7 transposition. Mol Gen Genet 194(1-2):149-158.
8. Goto N, et al. (1987) Identification of the DNA sequence required for transposition immunity of the gamma delta sequence. J Bacteriol 169(9):4388-4390.
9. Craigie R, Arndt-Jovin DJ, Mizuuchi K (1985) A defined system for the DNA strand-transfer reaction at the initiation of bacteriophage Mu transposition: Protein and DNA substrate requirements. Proc Natl Acad Sci USA 82(22):7570-7574. (Pubitemid 16204389)
10. Maxwell A, Craigie R, Mizuuchi K (1987) B protein of bacteriophage mu is an ATPase that preferentially stimulates intermolecular DNA strand transfer. Proc Natl Acad Sci USA 84(3):699-703. (Pubitemid 17033882)
11. Adzuma K, Mizuuchi K (1988) Target immunity of Mu transposition reflects a differential distribution of Mu B protein. Cell 53(2):257-266.
12. Miller JL, et al. (1984) The nucleotide sequence of the B gene of bacteriophage Mu. Nucleic Acids Res 12(22):8627-8638.
13. Chaconas G, Gloor G, Miller JL (1985) Ampli fi cation and purifi cation of the bacteriophage Mu encoded B transposition protein. J Biol Chem 260(5):2662-2669. (Pubitemid 15139318)
14. Adzuma K, Mizuuchi K (1991) Steady-state kinetic analysis of ATP hydrolysis by the B protein of bacteriophage mu. Involvement of protein oligomerization in the ATPase cycle. J Biol Chem 266(10):6159-6167. (Pubitemid 21906198)
15. Greene EC, Mizuuchi K (2002) Dynamics of a protein polymer: The assembly and disassembly pathways of the MuB transposition target complex. EMBO J 21(6):1477-1486. (Pubitemid 34246526)
16. Greene EC, Mizuuchi K (2004) Visualizing the assembly and disassembly mechanisms of the MuB transposition targeting complex. J Biol Chem 279(16):16736-16743. (Pubitemid 38509376)
17. Greene EC, Mizuuchi K (2002) Direct observation of single MuB polymers: Evidence for a DNA-dependent conformational change for generating an active target complex. Mol Cell 9(5):1079-1089. (Pubitemid 34626676)
18. Greene EC, Mizuuchi K (2002) Target immunity during Mu DNA transposition. Transpososome assembly and DNA looping enhance MuA-mediated disassembly of the MuB target complex. Mol Cell 10(6):1367-1378. (Pubitemid 36050878)
19. Baker TA, Mizuuchi M, Mizuuchi K (1991) MuB protein allosterically activates strand transfer by the transposase of phage Mu. Cell 65(6):1003-1013. (Pubitemid 121001688)
20. Surette MG, Harkness T, Chaconas G (1991) Stimulation of the Mu A protein-mediated strand cleavage reaction by the Mu B protein, and the requirement of DNA nicking for stable type 1 transpososome formation. In vitro transposition characteristics of mini-Mu plasmids carrying terminal base pair mutations. J Biol Chem 266(5):3118-3124. (Pubitemid 21909182)
21. Han YW, Mizuuchi K (2010) Phage Mu transposition immunity: Protein pattern formation along DNA by a diffusion-ratchet mechanism. Mol Cell 39(1):48-58.
22. Manna D, Higgins NP (1999) Phage Mu transposition immunity reflects supercoil domain structure of the chromosome. Mol Microbiol 32(3):595-606. (Pubitemid 29233903)
23. Teplow DB, Nakayama C, Leung PC, Harshey RM (1988) Structure-function relationships in the transposition protein B of bacteriophage Mu. J Biol Chem 263(22):10851-10857.
24. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha-and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1(8):945-951.
25. Hung LH, Chaconas G, Shaw GS (2000) The solution structure of the C-terminal domain of the Mu B transposition protein. EMBO J 19(21):5625-5634.
26. Yamauchi M, Baker TA (1998) An ATP-ADP switch in MuB controls progression of the Mu transposition pathway. EMBO J 17(18):5509-5518. (Pubitemid 28427064)
27. Erzberger JP, Berger JM (2006) Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu Rev Biophys Biomol Struct 35:93-114. (Pubitemid 43877371)
28. Wendler P, Ciniawsky S, Kock M, Kube S (2012) Structure and function of the AAA+ nucleotide binding pocket. Biochim Biophys Acta 1823(1):2-14.
29. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat Protoc 4(3):363-371.
30. Söding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33(Web Server issue): W244-W248.
31. Penefsky HS (1977) Reversible binding of Pi by beef heart mitochondrial adenosine triphosphatase. J Biol Chem 252(9):2891-2899.
32. Ramón-Maiques S, Britton HG, Rubio V (2002) Molecular physiology of phosphoryl group transfer from carbamoyl phosphate by a hyperthermophilic enzyme at low temperature. Biochemistry 41(12):3916-3924. (Pubitemid 34251030)
33. Egelman EH (2007) The iterative helical real space reconstruction method: Surmounting the problems posed by real polymers. J Struct Biol 157(1):83-94.
34. Ishikawa T, Maurizi MR, Steven AC (2004) The N-terminal substrate-binding domain of ClpA unfoldase is highly mobile and extends axially from the distal surface of ClpAP protease. J Struct Biol 146(1-2):180-188. (Pubitemid 38369030)
35. Effantin G, Ishikawa T, De Donatis GM, Maurizi MR, Steven AC (2010) Local and global mobility in the ClpA AAA+ chaperone detected by cryo-electron microscopy: Functional connotations. Structure 18(5):553-562.
36. Coros CJ, Sekino Y, Baker TA, Chaconas G (2003) Effect of mutations in the C-terminal domain of Mu B on DNA binding and interactions with Mu A transposase. J Biol Chem 278(33):31210-31217. (Pubitemid 36994637)
37. Rappas M, Schumacher J, Niwa H, Buck M, Zhang X (2006) Structural basis of the nucleotide driven conformational changes in the AAA+ domain of transcription activator PspF. J Mol Biol 357(2):481-492. (Pubitemid 43290749)
38. Ammelburg M, Frickey T, Lupas AN (2006) Classification of AAA+ proteins. J Struct Biol 156(1):2-11. (Pubitemid 44486070)
39. Rappas M, et al. (2005) Structural insights into the activity of enhancer-binding proteins. Science 307(5717):1972-1975. (Pubitemid 40404708)
40. Chen Z, Yang H, Pavletich NP (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453(7194):489-494. (Pubitemid 351733325)
41. Duderstadt KE, Chuang K, Berger JM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478(7368):209-213.
42. Bowman GD, O'Donnell M, Kuriyan J (2004) Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature 429(6993):724-730. (Pubitemid 38833117)
43. Hui MP, et al. (2010) ParA2, a Vibrio cholerae chromosome partitioning protein, forms left-handed helical filaments on DNA. Proc Natl Acad Sci USA 107(10):4590-4595.
44. Vecchiarelli AG, et al. (2010) ATP control of dynamic P1 ParA-DNA interactions: A key role for the nucleoid in plasmid partition. Mol Microbiol 78(1):78-91.
45. Yanagihara K, Mizuuchi K (2002) Mismatch-targeted transposition of Mu: A new strategy to map genetic polymorphism. Proc Natl Acad Sci USA 99(17):11317-11321. (Pubitemid 34920923)
46. Montaño SP, Pigli YZ, Rice PA (2012) The μ transpososome structure sheds light on DDE recombinase evolution. Nature 491(7424):413-417.
47. Baker TA, Mizuuchi M, Savilahti H, Mizuuchi K (1993) Division of labor among monomers within the Mu transposase tetramer. Cell 74(4):723-733. (Pubitemid 23259752)
48. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
49. Shaikh TR, et al. (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3(12):1941-1974.
50. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: Semiautomated software for highresolution single-particle reconstructions. J Struct Biol 128(1):82-97. (Pubitemid 30013436)
51. Sorzano CO, et al. (2004) XMIPP: A new generation of an open-source image processing package for electron microscopy. J Struct Biol 148(2):194-204. (Pubitemid 39346008)
52. Scheres SH, Núñez-Ramírez R, Sorzano CO, Carazo JM, Marabini R (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat Protoc 3(6):977-990. (Pubitemid 351818686)
53. Heymann JB, Belnap DM (2007) Bsoft: Image processing and molecular modeling for electron microscopy. J Struct Biol 157(1):3-18. (Pubitemid 44880789) Diseases, National Institute of Arthritis, Musculoskeletal and Skin Diseases, National Institutes of Health