Flexibility in mua transposase family protein structures: Functional mapping with scanning mutagenesis and sequence alignment of protein homologues

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Rasila, Tiina S ^a   Vihinen, Mauno ^b,c,d   Paulin, Lars ^a   Haapa Paananen, Saija ^a,f   Savilahti, Harri ^a,e  

^a UNIVERSITY OF HELSINKI   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^d LUND UNIVERSITY   (Sweden)

^e UNIVERSITY OF TURKU   (Finland)

^f VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MUA; TRANSPOSASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; DNA TRANSPOSITION; ESCHERICHIA COLI; MUTAGENESIS; NONHUMAN; PLASMID; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURE ACTIVITY RELATION; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTAGENESIS, INSERTIONAL; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSPOSASES;

EID: 84861559424     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037922     Document Type: Article

References (84)

1. Craig NL, Craigie R, Gellert M, Lambowitz AM, eds. (2002) Mobile DNA II. Washington, DC ASM Press.
2. Feschotte C, Pritham EJ, (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41: 331-368.
3. Kazazian HH Jr, (2004) Mobile elements: Drivers of genome evolution. Science 303: 1626-1632.
4. Muotri AR, Marchetto MC, Coufal NG, Gage FH, (2007) The necessary junk: New functions for transposable elements. Hum Mol Genet 16 Spec No. 2: R159-167.
5. Feschotte C, (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9: 397-405.
6. Sinzelle L, Izsvák Z, Ivics Z, (2009) Molecular domestication of transposable elements: From detrimental parasites to useful host genes. Cell Mol Life Sci 66: 1073-1093.
7. Boeke JD, (2002) Putting mobile DNA to work: The toolbox. In: Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Mobile DNA II Washington, DC ASM Press pp. 24-37.
8. Hayes F, (2003) Transposon-based strategies for microbial functional genomics and proteomics. Annu Rev Genet 37: 3-29.
9. Ivics Z, Izsvák Z, (2010) The expanding universe of transposon technologies for gene and cell engineering. Mob DNA 1: 25.
10. Katayanagi K, Miyagawa M, Matsushima M, Ishikawa M, Kanaya S, et al. (1990) Three-dimensional structure of ribonuclease H from E. coli. Nature 347: 306-309.
11. Yang W, Hendrickson WA, Crouch RJ, Satow Y, (1990) Structure of ribonuclease H phased at 2 Å resolution by MAD analysis of the selenomethionyl protein. Science 249: 1398-1405.
12. Rice PA, Baker TA, (2001) Comparative architecture of transposase and integrase complexes. Nat Struct Biol 8: 302-307.
13. Nowotny M, (2009) Retroviral integrase superfamily: The structural perspective. EMBO Rep 10: 144-151.
14. Haren L, Ton-Hoang B, Chandler M, (1999) Integrating DNA: Transposases and retroviral integrases. Annu Rev Microbiol 53: 245-281.
15. Zhou L, Mitra R, Atkinson PW, Hickman AB, Dyda F, et al. (2004) Transposition of hAT elements links transposable elements and V(D)J recombination. Nature 432: 995-1001.
16. Gellert M, (2002) V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 71: 101-132.
17. Rivas FV, Tolia NH, Song JJ, Aragon JP, Liu J, et al. (2005) Purified Argonaute2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol 12: 340-349.
18. Howe MM, Bade EG, (1975) Molecular biology of bacteriophage Mu. Science 190: 624-632.
19. Mizuuchi K, (1983) In vitro transposition of bacteriophage Mu: A biochemical approach to a novel replication reaction. Cell 35: 785-794.
20. Mizuuchi K, (1992) Transpositional recombination: Mechanistic insights from studies of Mu and other elements. Annu Rev Biochem 61: 1011-1051.
21. Rice P, Craigie R, Davies DR, (1996) Retroviral integrases and their cousins. Curr Opin Struct Biol 6: 76-83.
22. Nesmelova IV, Hackett PB, (2010) DDE transposases: Structural similarity and diversity. Adv Drug Deliv Rev 62: 1187-1195.
23. Surette MG, Buch SJ, Chaconas G, (1987) Transpososomes: Stable protein-DNA complexes involved in the in vitro transposition of bacteriophage Mu DNA. Cell 49: 253-262.
24. Craigie R, Mizuuchi K, (1987) Transposition of Mu DNA: Joining of Mu to target DNA can be uncoupled from cleavage at the ends of Mu. Cell 51: 493-501.
25. Lavoie BD, Chan BS, Allison RG, Chaconas G, (1991) Structural aspects of a higher order nucleoprotein complex: Induction of an altered DNA structure at the Mu-host junction of the Mu type 1 transpososome. EMBO J 10: 3051-3059.
26. Baker TA, Mizuuchi M, Savilahti H, Mizuuchi K, (1993) Division of labor among monomers within the Mu transposase tetramer. Cell 74: 723-733.
27. Savilahti H, Rice PA, Mizuuchi K, (1995) The phage Mu transpososome core: DNA requirements for assembly and function. EMBO J 14: 4893-4903.
28. Chaconas G, Harshey RM, (2002) Transposition of phage Mu DNA. In: Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Mobile DNA II Washington, DC ASM Press pp. 384-402.
29. Haapa S, Taira S, Heikkinen E, Savilahti H, (1999) An efficient and accurate integration of mini-Mu transposons in vitro: A general methodology for functional genetic analysis and molecular biology applications. Nucleic Acids Res 27: 2777-2784.
30. Aldaz H, Schuster E, Baker TA, (1996) The interwoven architecture of the Mu transposase couples DNA synapsis to catalysis. Cell 85: 257-269.
31. Savilahti H, Mizuuchi K, (1996) Mu transpositional recombination: Donor DNA cleavage and strand transfer in trans by the Mu transposase. Cell 85: 271-280.
32. Yang J-Y, Jayaram M, Harshey RM, (1996) Positional information within the Mu transposase tetramer: Catalytic contributions of individual monomers. Cell 85: 447-455.
33. Haapa S, Suomalainen S, Eerikäinen S, Airaksinen M, Paulin L, et al. (1999) An efficient DNA sequencing strategy based on the bacteriophage Mu in vitro DNA transposition reaction. Genome Res 9: 308-315.
34. Orsini L, Pajunen M, Hanski I, Savilahti H, (2007) SNP discovery by mismatch-targeting of Mu transposition. Nucleic Acids Res 35: e44.
35. Pajunen M, Turakainen H, Poussu E, Peränen J, Vihinen M, et al. (2007) High-precision mapping of protein-protein interfaces: An integrated genetic strategy combining en masse mutagenesis and DNA-level parallel analysis on a yeast two-hybrid platform. Nucleic Acids Res 35: e103.
36. Poussu E, Jäntti J, Savilahti H, (2005) A gene truncation strategy generating N- and C-terminal deletion variants of proteins for functional studies: Mapping of the Sec1p binding domain in yeast Mso1p by a Mu in vitro transposition-based approach. Nucleic Acids Res 33: e104.
37. Poussu E, Vihinen M, Paulin L, Savilahti H, (2004) Probing the α-complementing domain of E. coli β-galactosidase with use of an insertional pentapeptide mutagenesis strategy based on Mu in vitro DNA transposition. Proteins 54: 681-692.
38. Brady T, Roth SL, Malani N, Wang GP, Berry CC, et al. (2011) A method to sequence and quantify DNA integration for monitoring outcome in gene therapy. Nucleic Acids Res 39: e72.
39. Krupovič M, Vilen H, Bamford JKH, Kivelä HM, Aalto J-M, et al. (2006) Genome characterization of lipid-containing marine bacteriophage PM2 by transposon insertion mutagenesis. J Virol 80: 9270-9278.
40. Pajunen MI, Pulliainen AT, Finne J, Savilahti H, (2005) Generation of transposon insertion mutant libraries for Gram-positive bacteria by electroporation of phage Mu DNA transposition complexes. Microbiology 151: 1209-1218.
41. Vilen H, Aalto J-M, Kassinen A, Paulin L, Savilahti H, (2003) A direct transposon insertion tool for modification and functional analysis of viral genomes. J Virol 77: 123-134.
42. Lamberg A, Nieminen S, Qiao M, Savilahti H, (2002) Efficient insertion mutagenesis strategy for bacterial genomes involving electroporation of in vitro-assembled DNA transposition complexes of bacteriophage Mu. Appl Environ Microbiol 68: 705-712.
43. Paatero AO, Turakainen H, Happonen LJ, Olsson C, Palomäki T, et al. (2008) Bacteriophage Mu integration in yeast and mammalian genomes. Nucleic Acids Res 36: e148.
44. Nakayama C, Teplow DB, Harshey RM, (1987) Structural domains in phage Mu transposase: Identification of the site-specific DNA-binding domain. Proc Natl Acad Sci U S A 84: 1809-1813.
45. Clubb RT, Omichinski JG, Savilahti H, Mizuuchi K, Gronenborn AM, et al. (1994) A novel class of winged helix-turn-helix protein: The DNA-binding domain of Mu transposase. Structure 2: 1041-1048.
46. Clubb RT, Schumacher S, Mizuuchi K, Gronenborn AM, Clore GM, (1997) Solution structure of the Iγ subdomain of the Mu end DNA-binding domain of phage Mu transposase. J Mol Biol 273: 19-25.
47. Schumacher S, Clubb RT, Cai M, Mizuuchi K, Clore GM, et al. (1997) Solution structure of the Mu end DNA-binding Iβ subdomain of phage Mu transposase: Modular DNA recognition by two tethered domains. EMBO J 16: 7532-7541.
48. Rice P, Mizuuchi K, (1995) Structure of the bacteriophage Mu transposase core: A common structural motif for DNA transposition and retroviral integration. Cell 82: 209-220.
49. Leung PC, Teplow DB, Harshey RM, (1989) Interaction of distinct domains in Mu transposase with Mu DNA ends and an internal transpositional enhancer. Nature 338: 656-658.
50. Mizuuchi M, Mizuuchi K, (1989) Efficient Mu transposition requires interaction of transposase with a DNA sequence at the Mu operator: Implications for regulation. Cell 58: 399-408.
51. Baker TA, Luo L, (1994) Identification of residues in the Mu transposase essential for catalysis. Proc Natl Acad Sci U S A 91: 6654-6658.
52. Krementsova E, Giffin MJ, Pincus D, Baker TA, (1998) Mutational analysis of the Mu transposase: Contributions of two distinct regions of domain II to recombination. J Biol Chem 273: 31358-31365.
53. Wu Z, Chaconas G, (1995) A novel DNA binding and nuclease activity in domain III of Mu transposase: Evidence for a catalytic region involved in donor cleavage. EMBO J 14: 3835-3843.
54. Choi W, Harshey RM, (2010) DNA repair by the cryptic endonuclease activity of Mu transposase. Proc Natl Acad Sci U S A 107: 10014-10019.
55. Harshey RM, Cuneo SD, (1986) Carboxyl-terminal mutants of phage Mu transposase. J Genet 65: 159-174.
56. Baker TA, Mizuuchi M, Mizuuchi K, (1991) MuB protein allosterically activates strand transfer by the transposase of phage Mu. Cell 65: 1003-1013.
57. Leung PC, Harshey RM, (1991) Two mutations of phage Mu transposase that affect strand transfer or interactions with B protein lie in distinct polypeptide domains. J Mol Biol 219: 189-199.
58. Wu Z, Chaconas G, (1992) Flanking host sequences can exert an inhibitory effect on the cleavage step of the in vitro Mu DNA strand transfer reaction. J Biol Chem 267: 9552-9558.
59. Levchenko I, Luo L, Baker TA, (1995) Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev 9: 2399-2408.
60. Pajunen MI, Rasila TS, Happonen LJ, Lamberg A, Haapa-Paananen S, et al. (2010) Universal platform for quantitative analysis of DNA transposition. Mob DNA 1: 24.
61. Kim YC, Morrison SL, (2009) N-terminal domain-deleted Mu transposase exhibits increased transposition activity with low target site preference in modified buffers. J Mol Microbiol Biotechnol 17: 30-40.
62. Yuan JF, Beniac DR, Chaconas G, Ottensmeyer FP, (2005) 3D reconstruction of the Mu transposase and the type 1 transpososome: A structural framework for Mu DNA transposition. Genes Dev 19: 840-852.
63. Goldhaber-Gordon I, Williams TL, Baker TA, (2002) DNA recognition sites activate MuA transposase to perform transposition of non-Mu DNA. J Biol Chem 277: 7694-7702.
64. Goldhaber-Gordon I, Early MH, Gray MK, Baker TA, (2002) Sequence and positional requirements for DNA sites in a Mu transpososome. J Biol Chem 277: 7703-7712.
65. Saariaho A-H, Savilahti H, (2006) Characteristics of MuA transposase-catalyzed processing of model transposon end DNA hairpin substrates. Nucleic Acids Res 34: 3139-3149.
66. Saariaho A-H, Lamberg A, Elo S, Savilahti H, (2005) Functional comparison of the transposition core machineries of phage Mu and Haemophilus influenzae Mu-like prophage Hin-Mu reveals interchangeable components. Virology 331: 6-19.
67. Grant SGN, Jessee J, Bloom FR, Hanahan D, (1990) Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A 87: 4645-4649.
68. Sambrook J, Russell DW, (2001) Molecular cloning: A laboratory manual. In: Harbor ColdSpring, editors. N.Y.: Cold Spring Harbor Laboratory Press.
69. Hanahan D, Jessee J, Bloom FR, (1991) Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol 204: 63-113.
70. Rasila TS, Pajunen MI, Savilahti H, (2009) Critical evaluation of random mutagenesis by error-prone polymerase chain reaction protocols, Escherichia coli mutator strain, and hydroxylamine treatment. Anal Biochem 388: 71-80.
71. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
72. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38 (Database issue) pp. D211-D222.
73. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
74. Kabsch W, Sander C, (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
75. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
76. Petyuk V, McDermott J, Cook M, Sauer B, (2004) Functional mapping of Cre recombinase by pentapeptide insertional mutagenesis. J Biol Chem 279: 37040-37048.
77. Weber M, Chernov K, Turakainen H, Wohlfahrt G, Pajunen M, et al. (2010) Mso1p regulates membrane fusion through interactions with the putative N-peptide-binding area in Sec1p domain 1. Mol Biol Cell 21: 1362-1374.
78. Fransen M, Vastiau I, Brees C, Brys V, Mannaerts GP, et al. (2005) Analysis of human Pex19p's domain structure by pentapeptide scanning mutagenesis. J Mol Biol 346: 1275-1286.
79. von Nandelstadh P, Grönholm M, Moza M, Lamberg A, Savilahti H, et al. (2005) Actin-organising properties of the muscular dystrophy protein myotilin. Exp Cell Res 310: 131-139.
80. Grönholm M, Muranen T, Toby GG, Utermark T, Hanemann CO, et al. (2006) A functional association between merlin and HEI10, a cell cycle regulator. Oncogene 25: 4389-4398.
81. Baker TA, Mizuuchi K, (1992) DNA-promoted assembly of the active tetramer of the Mu transposase. Genes Dev 6: 2221-2232.
82. Richardson JM, Colloms SD, Finnegan DJ, Walkinshaw MD, (2009) Molecular architecture of the Mos1 paired-end complex: The structural basis of DNA transposition in a eukaryote. Cell 138: 1096-1108.
83. Tanaka Y, Nureki O, Kurumizaka H, Fukai S, Kawaguchi S, et al. (2001) Crystal structure of the CENP-B protein-DNA complex: The DNA-binding domains of CENP-B induce kinks in the CENP-B box DNA. EMBO J 20: 6612-6618.
84. Akhverdyan VZ, Gak ER, Tokmakova IL, Stoynova NV, Yomantas YAV, et al. (2011) Application of the bacteriophage Mu-driven system for the integration/amplification of target genes in the chromosomes of engineered Gram-negative bacteria-mini review. Appl Microbiol Biotechnol 91: 857-871.