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Assembly of the Tc1 and mariner transposition initiation complexes depends on the origins of their transposase DNA binding domains

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An Erratum to this article was published on 29 June 2007

Abstract

In this review, we focus on the assembly of DNA/protein complexes that trigger transposition in eukaryotic members of the IS630–Tc1–mariner (ITm) super-family, the Tc1- and mariner-like elements (TLEs and MLEs). Elements belonging to this super-family encode transposases with DNA binding domains of different origins, and recent data indicate that the chimerization of functional domains has been an important evolutionary aspect in the generation of new transposons within the ITm super-family. These data also reveal that the inverted terminal repeats (ITRs) at the ends of transposons contain three kinds of motif within their sequences. The first two are well known and correspond to the cleavage site on the outer ITR extremities, and the transposase DNA binding site. The organization of ITRs and of the transposase DNA binding domains implies that differing pathways are used by MLEs and TLEs to regulate transposition initiation. These differences imply that the ways ITRs are recognized also differ leading to the formation of differently organized synaptic complexes. The third kind of motif is the transposition enhancers, which have been found in almost all the functional MLEs and TLEs analyzed to date. Finally, in vitro and in vivo assays of various elements all suggest that the transposition initiation complex is not formed randomly, but involves a mechanism of oriented transposon scanning.

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Abbreviations

MLE:

Mariner-like elements

TLE:

Tc1-like elements

ITR:

Inverted terminal repeats

Tnp:

Transposase

bp:

Base pairs

UTR:

Untranslated region

ORF:

Open reading frame

NLS:

Nuclear localization signal

HTH:

Helix turn helix

DR:

Direct repeat

References

  • Arkhipova IR, Meselson M (2005) Diverse DNA transposons in rotifers of the class Bdelloidea. Proc Natl Acad Sci USA 102:11781–11786

    Article  PubMed  CAS  Google Scholar 

  • Augé-Gouillou C, Bigot Y, Pollet N, Hamelin MH, Meunier-Rotival M, Periquet G (1995) Human and other mammalian genomes contain transposons of the mariner family. FEBS Lett 368:541–546

    Article  PubMed  Google Scholar 

  • Augé-Gouillou C, Notareschi-Leroy H, Abad P, Periquet G, Bigot Y (2000) Phylogenetic analysis of the functional domains of mariner-like element (MLE) transposases. Mol Genet Genomics 264:506–513

    Article  CAS  Google Scholar 

  • Augé-Gouillou C, Hamelin MH, Demattei MV, Periquet M, Bigot Y (2001a) The wild-type conformation of the Mos1 inverted terminal repeats is suboptimal for transposition in bacteria. Mol Genet Genom 265:51–57

    Article  Google Scholar 

  • Augé-Gouillou C, Hamelin MH, Demattei MV, Periquet G, Bigot Y (2001b) The ITR binding domain of the mariner Mos1 transposase. Mol Genet Genom 265:58–65

    Article  Google Scholar 

  • Augé-Gouillou C, Brillet B, Germon S, Hamelin MH, Bigot Y (2005a) Mariner Mos1 transposase dimerizes prior to ITR binding. J Mol Biol 351:117–130

    Article  CAS  Google Scholar 

  • Augé-Gouillou C, Brillet B, Hamelin MH, Bigot Y (2005b) Assembly of the mariner Mos1 synaptic complex. Mol Cell Biol 25:2861–2870

    Article  CAS  Google Scholar 

  • Bigot Y, Brillet B, Augé-Gouillou C (2005) Conservation of palindromic and mirror motifs within inverted terminal repeats of mariner-like elements. J Mol Biol 351:108–116

    Article  PubMed  CAS  Google Scholar 

  • Callebaut I, Labesse G, Durand P, Poupon A, Canard L, Chomilier J, Henrissat B, Mornon JP (1997) Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cell Mol Life Sci 53:621–645

    Article  PubMed  CAS  Google Scholar 

  • Capy P, Langin T, Bigot Y, Brunet F, Daboussi MJ, Periquet G, David JR, Hartl DL (1994) Horizontal transmission versus ancient origin: mariner in the witness box. Genetica 93:161–170

    Article  PubMed  CAS  Google Scholar 

  • Capy P, Langin T, Higuet D, Maurer P, Bazin C (1997) Do the integrases of LTR-retrotransposons and Class-II element transposases have a common ancestor? Genetica 100:63–72

    Article  PubMed  CAS  Google Scholar 

  • Chandler M, Clerget M, Galas DJ (1982) The transposition frequency of IS1-flanked transposon is a function of their size. J Mol Biol 154:229–243

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Engelman A (1998) The barrier-to-autointegration protein is a host factor for HIV type 1 integration. Proc Natl Acad Sci USA 95:15270–15274

    Article  PubMed  CAS  Google Scholar 

  • Claudianos C, Brownlie J, Russell R, Oakeshott J, Whyard S (2002) maT a clade of transposons intermediate between mariner and Tc1. Mol Biol Evol 19:2101–2109

    PubMed  CAS  Google Scholar 

  • Coates CJ, Jasinskiene N, Miyashiro L, James AA (1998) Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 95:3748–3751

    Article  PubMed  CAS  Google Scholar 

  • Colloms V, van Luenen HG, Plasterk RH (1994) DNA binding activities of the Caenorhabditis elegans Tc3 transposase. Nucleic Acids Res 22:5548–5554

    Article  PubMed  CAS  Google Scholar 

  • Converse AD, Belur LR, Gori JL, Liu G, Amaya F, Aguilar-Cordova E, Hackett PB, McIvor RS (2004) Counterselection and co-delivery of transposon and transposase functions for Sleeping Beauty-mediated transposition in cultured mammalian cells. Biosci Rep 24:577–794

    Article  PubMed  CAS  Google Scholar 

  • Coy MR, Tu Z (2005) Gambol and Tc1 are two distinct families of DD34E transposons: analysis of the Anopheles gambiae genome expands the diversity of the IS630-Tc1-mariner superfamily. Insect Mol Biol 14:537–546

    Article  PubMed  CAS  Google Scholar 

  • Cui Z, Geurts AM, Liu G, Kaufman CD, Hackett PB (2002) Structure–function analysis of the inverted terminal repeats of the Sleeping Beauty transposon. J Mol Biol 318:1221–1235

    Article  PubMed  CAS  Google Scholar 

  • Czerny T, Schaffner G, Busslinger M (1993) DNA sequence recognition by PAX proteins: bipartite structure of the paired domain and its binding site. Genes Dev 7:2048–2061

    Article  PubMed  CAS  Google Scholar 

  • Davies DR, Goryshin IY, Reznikoff WS, Rayment I (2000) Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 289:77–85

    Article  PubMed  CAS  Google Scholar 

  • Difilippantonio M, McMahan CJ, Eastman QM, Spanopoulou E, Schatz DG (1996) RAG1 mediates signal sequence recognition and recruitment of RAG2 in V(D)J recombination. Cell 87:253–262

    Article  PubMed  CAS  Google Scholar 

  • Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122:473–483

    Article  PubMed  CAS  Google Scholar 

  • Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common “D35E” motif. Proc Natl Acad Sci USA 91:942–946

    Article  PubMed  CAS  Google Scholar 

  • Feng JA, Johnson RC, Dickerson RE (1994) Hin recombinase bound to DNA: the origin of specificity in major and minor groove interactions. Science 263:348–355

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C, Osterlund MT, Peeler R, Wessler SR (2005) DNA-binding specificity of rice mariner-like transposases and interactions with Stowaway MITEs. Nucleic Acids Res 33:2153–2165

    Article  PubMed  CAS  Google Scholar 

  • Fischer SE., van Luenen HG, Plasterk RH (1999) Cis requirements for transposition of Tc1-like transposons in C. elegans. Mol Gen Genet 262:268–274

    PubMed  CAS  Google Scholar 

  • Fischer SE, Wienhld E, Plasterk RH (2003) Continuous exchange of sequence information between dispersed Tc1 transposons in the Caenorhabditis genome. Genetics 164:127–134

    PubMed  CAS  Google Scholar 

  • Franz G, Loukeris TG, Dialektaki G, Thompson CR, Savakis C (1994) Mobile Minos elements from Drosophila hydei encode a two-exon transposase with similarity to the paired DNA-binding domain. Proc Natl Acad Sci USA 91:4746–4750

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Saez I, Plasterk RH (2000) Purification of the Caenorhabditis elegans transposase TC1A refolded during gel filtration chromatography. Protein Expr Purif 19:355–361

    Article  PubMed  CAS  Google Scholar 

  • Gehring WJ, Qian YQ, Billeter M, Furukubo-Tokunaga K, Schier AF, Resendez-Perez D, Affolter M, Otting G, Wuthrich K (1994) Homeodomain-DNA recognition. Cell 78:211–223

    Article  PubMed  CAS  Google Scholar 

  • Guegen E, Rousseau P, Duval-Valentin G, Chandler M (2006) The transposome: control of transposition at level of catalysis. Trends Microbiol 13:543–549

    Article  CAS  Google Scholar 

  • Halaimia-Toumi N, Casse N, Demattei MV, Renault S, Pradier E, Bigot Y, Laulier M (2004) The GC-rich transposon Bytmar1 from the deep-sea hydrothermal crab, Bythograea thermydron, may encode three transposase isoforms from a single ORF. J Mol Evol 59:747–760

    Article  PubMed  CAS  Google Scholar 

  • Hickman AB, Perez ZN, Zhou L, Musingarimi P, Ghirlando R, Hinshaw JE, Craig NL, Dyda F (2005) Molecular architecture of a eukaryotic DNA transposase. Nat Struct Mol Biol 12:715–721

    Article  PubMed  CAS  Google Scholar 

  • Huffman JL, Brennan RG (2002) Prokaryotic transcription regulators: more than just the helix-turn-helix motif. Curr Opin Struct Biol 12:98–106

    Article  PubMed  CAS  Google Scholar 

  • Ivics Z, Izsvak Z, Minter A, Hackett PB (1996) Identification of functional domains and evolution of Tc1-like transposable elements. Proc Natl Acad Sci USA 93:5008–5013

    Article  PubMed  CAS  Google Scholar 

  • Ivics Z, Hackett PB, Plasterk RH, Izsvak Z (1997) Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:501–510

    Article  PubMed  CAS  Google Scholar 

  • Izsvák Z, Ivics Z, Plasterk RH (2000) Sleeping Beauty, a wide host-range transposon vector for genetic transformation in vertebrates. J Mol Biol 302:93–102

    Article  PubMed  CAS  Google Scholar 

  • Izsvák Z, Khare D, Behlke J, Heinemann U, Plasterk RH, Ivics Z (2002) Involvement of a bifunctional, paired-like DNA-binding domain and a transpositional enhancer in Sleeping Beauty transposition. J Biol Chem 277:34581–34588

    Article  PubMed  Google Scholar 

  • Izsvak Z, Stuwe EE, Fiedler D, Katzer A, Jeggo PA, Ivics Z (2004) Healing the wounds inflicted by Sleeping Beauty transposition by double-strand break repair in mammalian somatic cells. Mol Cell 13:279–290

    Article  PubMed  CAS  Google Scholar 

  • Jacobson JW, Medhora MM, Hartl DL (1986) Molecular structure of a somatically unstable transposable element in Drosophila. Proc Natl Acad Sci USA 83:8684–8688

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2004) Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biol 23:311–324

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PloS Biol 3:998–1011

    Article  CAS  Google Scholar 

  • Karsi A, Moav B, Hackett P, Liu Z (2001) Effect of size on transposition efficiency of the Sleeping Beauty transposon in mouse cells. Mar Biotechnol 3:241–245

    Article  PubMed  CAS  Google Scholar 

  • Lampe DJ, Churchill ME, Robertson HM (1996) A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J 15:5470–5479

    PubMed  CAS  Google Scholar 

  • Lampe DJ, Grant TE, Robertson HM (1998) Factors affecting transposition of the Himar1 mariner transposon in vitro. Genetics 149:179–187

    PubMed  CAS  Google Scholar 

  • Lampe DJ, Walden KK, Robertson HM (2001) Loss of transposase–DNA interaction may underlie the divergence of mariner family transposable elements and the ability of more than one mariner to occupy the same genome. Mol Biol Evol 18:954–961

    PubMed  CAS  Google Scholar 

  • Lipkow K, Buisine N, Lampe DJ, Chalmers R (2004) Early intermediates of mariner transposition: catalysis without synapsis of the transposon ends suggests a novel architecture of the synaptic complex. Mol Cell Biol 24:8301–8311

    Article  PubMed  CAS  Google Scholar 

  • Michel K, O’Brochta DA, Atkinson PW (2003) The C-terminus of the Hermes transposase contains a protein multimerization domain. Insect Biochem Mol Biol 33:359–390

    Google Scholar 

  • Mizuuchi M, Baker TA, Mizuuchi K (1992) Assembly of the active form of the transposase-Mu DNA complex: a critical control point in Mu transposition. Cell 70:303–311

    Article  PubMed  CAS  Google Scholar 

  • Normand C, Duval-Valentin G, Haren L, Chandler M (2001) The terminal inverted repeats of IS911: requirements for synaptic complex assembly and activity. J Mol Biol 308:853–871

    Article  PubMed  CAS  Google Scholar 

  • Pavlopoulos A, Berghammer AJ, Averof M, Klingler M (2004) Efficient transformation of the beetle Tribolium castaneum using the minos transposable element: quantitative and qualitative analysis of genomic integration events. Genetics 167:737–746

    Article  PubMed  CAS  Google Scholar 

  • Perez ZN, Musingarimi P, Craig NL, Dyda F, Hickman AB (2005) Purification, crystallization and preliminary crystallographic analysis of the Hermes transposase. Acta Cryst F61:587–590

    CAS  Google Scholar 

  • Pietrokovski S, Henikoff S (1997) A helix-turn-helix DNA-binding motif predicted for transposases of DNA transposons. Mol Gen Genet 254:689–695

    Article  PubMed  CAS  Google Scholar 

  • Plasterk RH (1996) The Tc1/mariner transposon family. Curr Topics Microbiol Immunol 204:125–143

    CAS  Google Scholar 

  • Plasterk RH, Izsvak Z, Ivics Z (1999) Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet 15:326–332

    Article  PubMed  CAS  Google Scholar 

  • Pledger DW, Fu YQ, Coates CJ (2004) Analyses of cis-acting elements that affect the transposition of Mos1 mariner transposons in vivo. Mol Genet Genom 272:67–75

    CAS  Google Scholar 

  • Radice AD, Bugaj B, Fitch DH, Emmons SW (1994) Widespread occurrence of the Tc1 transposon family: Tc1-like transposons from teleost fish. Mol Gen Genet 244:606–612

    Article  PubMed  CAS  Google Scholar 

  • Renault S, Demattei MV, Lahouassa H, Bigot Y. Structure–function of large ITR of the mariner element Mcmar1-1. (Manuscript in preparation)

  • Richardson JM, Zhang L, Marcos S, Finnegan DJ, Harding MM, Taylor P, Walkinshaw MD (2004) Expression, purification and preliminary crystallographic studies of a single–point mutant of Mos1 mariner transposase. Acta Crystallogr D Biol Crystallogr D60:962–964

    Article  CAS  Google Scholar 

  • Richardson JM, Dawson A, O’Hagan N, Taylor P, Finnegan DJ, Walkinshaw MD (2006) Mechanism of Mos1 transposition: insights from structural analysis. EMBO J 25: 1324–1334

    Article  PubMed  CAS  Google Scholar 

  • Robertson HM (1993) The mariner transposable element is widespread in insects. Nature 362:241–245

    Article  PubMed  CAS  Google Scholar 

  • Robertson HM, Lampe DJ (1995) Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol Biol Evol 12:850–862

    PubMed  CAS  Google Scholar 

  • Sakai J, Chalmers RM, Kleckner N (1995) Identification and characterization of a pre-cleavage synaptic complex that is␣an early intermediate in Tn10 transposition. EMBO J 14:4374–4383

    PubMed  CAS  Google Scholar 

  • Score PR, Belur LR, Frandsen JL, Guerts JL, Yamaguchi T, Somia NV, Hackett PB, Largaespada DA, McIvor RS (2005) Sleeping Beauty-mediated transposition and long-term expression in vivo: use of the loxP/CRE recombinase system to distinguish transposition-specific expression. Mol Ther 13:617–624

    Google Scholar 

  • Shao H, Tu Z (2001) Expanding the diversity of the IS630–Tc1–mariner superfamily: discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons. Genetics 159:1103–1115

    PubMed  CAS  Google Scholar 

  • Silva JC, Bastida F, Bidwell SL, Johnson PJ, Carlton JM (2005) A potentially functional mariner transposable element in␣the protist Trichomonas vaginalis. Mol Biol Evol. 22:126–134

    Article  PubMed  CAS  Google Scholar 

  • Sinzelle L, Pollet N, Bigot Y, Mazabraud A (2005) Characterization of multiple lineages of Tc1-like elements within the genome of the amphibian Xenopus tropicalis. Gene 349:187–196

    Article  PubMed  CAS  Google Scholar 

  • Smit AFA, Riggs AD (1996) Tiggers and other DNA transposon fossils in the human genome. Proc Natl Acad Sci USA 93:1443–1448

    Article  PubMed  CAS  Google Scholar 

  • Spanopoulou E, Zaitseva F, Wang FH, Santagata S, Baltimore D, Panayotou G (1996) The homeodomain region of RAG1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell 87:263–276

    Article  PubMed  CAS  Google Scholar 

  • Steiniger-White M, Reznikoff WS (2000) The C-terminal alpha helix of Tn5 transposase is required for synaptic complex formation. J Biol Chem 275:23127–23133

    Article  PubMed  CAS  Google Scholar 

  • Tanaka M, Yamamoto T, Sawai T (1983) Fine structure of transposition genes on Tn2603 and complementation of its TnpA and TnpR mutations by related transposons. Mol Gen Genet 191:442–450

    Article  PubMed  CAS  Google Scholar 

  • Tosi LR, Beverley SM (2000) Cis and trans factors affecting Mos1 mariner evolution and transposition in vitro, and its potential for functional genomics. Nucleic Acids Res 28:784–790

    Article  PubMed  CAS  Google Scholar 

  • Tu Z, Shao H (2002) Intra- and inter-specific diversity of Tc3-like transposons in nematodes and insects and implications for their evolution and transposition. Gene 282:133–142

    Article  PubMed  CAS  Google Scholar 

  • van Pouderoyen G, Ketting RF, Perrakis A, Plasterk RH, Sixma TK (1997) Crystal structure of the specific DNA-binding domain of Tc3 transposase of C. elegans in complex with transposon DNA. EMBO J 16:6044–6054

    Article  PubMed  Google Scholar 

  • Vos JC, Hackett PB, Plasterk RH, Izsvak Z (1993) Characterization of the Caenorhabditis elegans Tc1 transposase in vivo and in vitro. Genes Dev 7:1244–1253

    Article  PubMed  CAS  Google Scholar 

  • Vos JC, Plasterk RH (1994) Tc1 transposase of Caenorhabditis elegans is an endonuclease with a bipartite DNA binding domain. EMBO J 13:6125–6132

    PubMed  CAS  Google Scholar 

  • Vos JC, De Baere I, Plasterk RHA (1996) Transposase is the only nematode protein required for in vitro transposition of Tc1. Genes Dev 10:755–761

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Hartswood E, Finnegan DJ (1999) Pogo transposase contains a putative helix-turn-helix DNA binding domain that recognises a 12 bp sequence within the terminal inverted repeats. Nucleic Acids Res 27:455–461

    Article  PubMed  CAS  Google Scholar 

  • Watkins S, van Pouderoyen G, Sixma TK (2004) Structural analysis of the bipartite DNA-binding domain of Tc3 transposase bound to transposon DNA. Nucleic Acids Res 32:4306–4312

    Article  PubMed  CAS  Google Scholar 

  • Yant SR, Park J, Huang Y, Mikkelsen JG, Kay MA (2004) Mutational analysis of the N-terminal DNA-binding domain of Sleeping Beauty transposase: critical residues for DNA binding and hyperactivity in mammalian cells. Mol Cell Biol 24:9239–9247

    Article  PubMed  CAS  Google Scholar 

  • York D, Reznikoff WS (1996) Purification and biochemical analyses of a monomeric form of Tn5 transposase. Nucleic Acids Res 24:3790–3796

    Article  PubMed  CAS  Google Scholar 

  • Zayed H, Izsvak Z, Khare D, Heinemann U, Ivics Z (2003) The DNA-binding protein HMGB1 is a cellular cofactor of Sleeping Beauty transposition. Nucleic Acids Res 31:2313–2322

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Dawson A, Finnegan DJ (2001) DNA-binding activity and subunit interaction of the mariner transposase. Nucleic Acids Res 29:3566–3575

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was funded by grants from the C.N.R.S., the I.N.R.A., the GDR 2157, the IFR136, the Ministère de l’Education Nationale, de la Recherche et de la Technologie and the University of Tours. Benjamin Brillet holds a doctoral fellowship from the Association Française contre les Myopathies. The English text has been revised by Dr. M. Ghosh.

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  1. Laboratoire d’Etudes des Parasites Génétiques, Université François Rabelais, FRE CNRS 2969, UFR Sciences & Techniques, Parc Grandmont, 37200, Tours, France

    Brillet Benjamin, Bigot Yves & Augé-Gouillou Corinne

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  1. Brillet Benjamin
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  2. Bigot Yves
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  3. Augé-Gouillou Corinne
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Correspondence to Augé-Gouillou Corinne.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s10709-007-9161-6

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Benjamin, B., Yves, B. & Corinne, AG. Assembly of the Tc1 and mariner transposition initiation complexes depends on the origins of their transposase DNA binding domains. Genetica 130, 105–120 (2007). https://doi.org/10.1007/s10709-006-0025-2

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