The diversity of retrotransposons and the properties of their reverse transcriptases

Virus Research

Volumn 134, Issue 1-2, 2008, Pages 221-234

  Eickbush, Thomas H ^a   Jamburuthugoda, Varuni K ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Integration mechanism; Phylogenetic relationship; Retrotransposon; Reverse transcriptase

Indexed keywords

RNA DIRECTED DNA POLYMERASE;

ARTICLE; ENVELOPE GENE; ENZYME ACTIVITY; GENE SEQUENCE; GENE STRUCTURE; HUMAN; LONG TERMINAL REPEAT; PRIORITY JOURNAL; RETROPOSON; REVERSE TRANSCRIPTION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SILKWORM; TRYPANOSOMA;

ANIMALS; HUMANS; MODELS, MOLECULAR; PHYLOGENY; RETROELEMENTS; REVERSE TRANSCRIPTION; RNA-DIRECTED DNA POLYMERASE;

ANIMALIA; EUKARYOTA; PENELOPE; VERTEBRATA;

EID: 43049094016     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2007.12.010     Document Type: Article

References (124)

1. Anzai T., Takahashi H., and Fujiwara H. Sequence specific recognition and cleavage of telomeric repeats by the endonuclease of non-long terminal repeat retrotransposon TRAS1. Mol. Cell. Biol. 21 (2001) 100-108
2. Anzai T., Osanai M., Hamada M., and Fujiwara H. Functional roles of 3′-terminal structures of template RNA during in vivo retrotransposition on non-LTR retrotransposon, R1Bm. Nucleic Acids Res. 33 (2005) 1993-2002
3. Arkhipova I.R., Pyatkov K.I., Meselson M., and Evgen'ev M.B. Retroelements containing introns in diverse invertebrate taxa. Nat. Genet. 33 (2003) 123-124
4. Arnold J.J., and Cameron C.E. Poliovirus RNA-dependent RNA polymerase (3Dpol) is sufficient for template switching in vitro. J. Biol. Chem. 274 (1999) 2706-2716
5. Atwood-Moore A., Ejebe K., and Levin H.L. Specific recognition and cleavage of the plus-strand primer by reverse transcriptase. J. Virol. 79 (2005) 14863-14875
6. Atwood-Moore A., Yan K., Judson R.L., and Levin H.L. The self primer of the long terminal repeat retrotransposon Tf1 is not removed during reverse transcription. J. Virol. 80 (2006) 8267-8270
7. Bateman A., Birney E., Durbin R., Eddy S.R., Finn R.D., and Sonnhammer E.L. Pfam 3.1: 1313 multiple alignments match the majority of proteins. Nucleic Acids Res. 27 (1999) 260-262
8. Bibillo A., and Eickbush T.H. High processivity of the reverse transcriptase from a non-long terminal repeat retrotransposon. J. Biol. Chem. 277 (2002) 34836-34845
9. Bibillo A., and Eickbush T.H. The reverse transcriptase of the R2 non-LTR retrotransposon: continuous synthesis of cDNA on non-continuous RNA templates. J. Mol. Biol. 316 (2002) 459-473
10. Bibillo A., and Eickbush T.H. End-to-end template jumping by the reverse transcriptase encoded by the R2 retrotransposon. J. Biol. Chem. 279 (2004) 14945-14953
11. Bibillo A., Lener D., Klarmann G.J., and Le Grice S.F. Functional roles of carboxylate residues comprising the DNA polymerase active site triad of Ty3 reverse transcriptase. Nucleic Acids Res. 33 (2005) 171-181
12. Bibillo A., Lener D., Tewari A., and Le Grice S.F. Interaction of the Ty3 reverse transcriptase thumb subdomain with template-primer. J. Biol. Chem. 280 (2005) 30282-30290
13. Boeke J.D. Transposable elements in Saccharomyces cerevisiae. In: Berg D.E., and Howe M.M. (Eds). Mobile DNA (1989), American Society for Microbiology, Washington, DC 335-374
14. Boeke J.D., and Stoye J.P. Retrotransposons, endogenous retroviruses, and the evolution of retroelements. In: Coffin J.M., Hughes S.H., and Varmus H.E. (Eds). Retroviruses (1997), Cold Spring Harbor Laboratory Press, Plainview, NY 343-435
15. Boeke J.D., Garfinkel C.A., Styles A., and Fink G.R. Ty elements transpose through an RNA intermediate. Cell 40 (1985) 491-500
16. Boeke, J.D., Eickbush, T.H., Sandmeyer, S.B., Voytas, D.F., 2005. Pseudoviridae. In: Fauquet, C.M., Mayo, M.A., Maniloff, J., Desselberger, U., Ball, L.A. (Eds.), Virus Taxonomy, VIIIth Report of the ICTV. Elsevier/Academic Press, London, pp. 397-407.
17. Boutabout M., Wilhelm M., and Wilhelm F.X. DNA synthesis fidelity by the reverse transcriptase of the yeast retrotransposon Ty1. Nucleic Acids Res. 29 (2001) 2217-2222
18. Bowen N.J., and McDonald J.F. Genomic analysis of Caenorhabditis elegans reveals ancient families of retroviral-like elements. Genome Res. 9 (1999) 924-935
19. Britt W.J., and Mach M. Human cytomegalovirus glycoproteins. Intervirology 39 (1996) 401-412
20. Burke W.D., Malik H.S., Lathe III W.C., and Eickbush T.H. Are retrotransposons long-term hitchhikers. Nature 392 (1998) 141-142
21. Cappello J., Handelsman K., and Lodish H. Sequence of Dictyostelium DIRS-1: an apparent retrotransposon with inverted terminal repeats and an internal circle junction sequence. Cell 43 (1985) 105-115
22. Capy P., Basin C., Higuet D., and Langin T. Dynamics and Evolution of Transposable Elements (1998), Springer-Verlag, New York
23. Chaboissier M.C., Finnegan D., and Bucheton A. Retrotransposition of the I factor, a non-long terminal repeat retrotransposon of Drosophila, generates tandem repeats at the 3′ end. Nucleic Acids Res. 28 (2000) 2467-2472
24. Chambeyron S., Bucheton A., and Busseau I. Tandem UAA repeats at the 3′-end of the transcript are essential for the precise initiation of reverse transcription of the I factor in Drosophila melanogaster. J. Biol. Chem. 277 (2002) 17877-17882
25. Charlesworth B., Sniegowski P., and Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371 (1994) 215-220
26. Christensen S., Pont-Kingdom G., and Carroll D. Target specificity of the endonuclease from Xenopus laevis non-long terminal repeat retrotransposons, Tx1L. Mol. Cell. Biol. 20 (2000) 1219-1226
27. Christensen S.M., Bibillo A., and Eickbush T.H. Role of the Bombyx mori R2 element N-terminal domain in the target-primed reverse transcription (TPRT) reaction. Nucleic Acids Res. 33 (2005) 6461-6468
28. Christensen S.M., Ye J., and Eickbush T.H. RNA from the 5' end of the R2 retrotransposon controls R2 protein binding to and cleavage of its DNA target site. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 17602-17607
29. Clare J., and Farabaugh P. Nucleotide sequence of a yeast Ty element: evidence for an unusal mechanism of gene expression. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 2829-2933
30. Cost G.J., and Boeke J.D. Targeting of human retrotransposons integration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure. Biochemistry 37 (1998) 18081-18093
31. Cost G.J., Feng Q., Jacquier A., and Boeke J.D. Human L1 element target-primed reverse transcription in vitro. EMBO J. 21 (2002) 5899-5910
32. Cristofari G., Gabus C., Ficheux D., Bona M., Le Grice S.F., and Darlix J.L. Characterization of active reverse transcriptase and nucleoprotein complexes of the yeast retrotransposon Ty3 in vitro. J. Biol. Chem. 274 (1999) 36643-36648
33. Dewannieux M., Esnault C., and Heidmann T. LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet. 35 (2003) 41-48
34. Doolittle R.F., Feng D.F., Johnson M.S., and McClure M.A. Origins and evolutionary relationships of retroviruses. Quart. Rev. Biol. 64 (1989) 1-30
35. Duncan L., Bouckaert K., Yeh F., and Kirk D.L. Kangaroo, a mobile element from Volvox carteri, is a member of a newly recognized third class of retrotransposons. Genetics 162 (2002) 1617-1630
36. Eickbush T.H. Origin and evolutionary relationships of retroelements. In: Morse S.S. (Ed). The Evolutionary Biology of Viruses (1994), Raven Press, New York 121-157
37. Eickbush T.H. Telomerase and retrotransposons: which came first?. Science 277 (1997) 911-912
38. Eickbush T.H. R2 and related site-specific non-LTR retrotransposons. In: Craig N., Craigie R., Gellert M., and Lambowitz A. (Eds). Mobile DNA II (2002), American Society of Microbiology Press, Washington, DC 813-835
39. Eickbush T.H., and Malik H.S. Evolution of retrotransposons. In: Craig N., Craigie R., Gellert M., and Lambowitz A. (Eds). Mobile DNA II (2002), American Society of Microbiology Press, Washington, DC 1111-1144
40. Eickbush, T.H., Boeke, J.D., Sandmeyer, S.B., Voytas, D.F., 2005. Metaviridae. In: Fauquet, C.M., Mayo, M.A., Maniloff, J., Desselberger, U., Ball, L.A. (Eds.), Virus Taxonomy, VIIIth Report of the ICTV. Elsevier/Academic Press, London, pp. 409-420.
41. Esnault C., Maestre J., and Heidmann T. Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 24 (2000) 363-367
42. Evgen'ev M.B., Zelentsova H., Shostak N., Kozitsina M., Barskyi V., Lankenau D.H., and Corces V.G. Penelope, a new family of transposable elements and its possible role in hybrid dysgenesis in Drosophila virilis. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 196-201
43. Felder H., Herzceq A., de Chastonay Y., Aeby P., Tobler H., and Muller F. TAS, a retrotransposon from the parasitic nematode Ascaris lumbricoides. Gene 149 (1994) 219-225
44. Feng Q., Schumann G., and Boeke J.D. Retrotransposon R1Bm endonuclease cleaves the target sequence. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 2083-2088
45. Gabriel A., and Boeke J.D. Reverse transcriptase encoded by a retrotransposon from the trypanosomatid Crithidia fasciculata. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 9794-9798
46. Gabriel A., Willems M., Mules E.H., and Boeke J.D. Replication infidelity during a single cycle of Ty1 retrotransposition. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 7767-7771
47. Gabus C., Ficheux D., Rau M., Keith G., Sandmeyer S., and Darlix J.L. The yeast Ty3 retrotransposon contains a 5′-3′ bipartite primer-binding site and encodes nucleocapsid protein NCp9 functionally homologous to HIV-1 NCp7. EMBO J. 17 (1998) 4873-4880
48. Garcia-Perez J.L., Gonzalez C.I., Thomas M.C., Olivaries M., and Lopez M.C. Characterization of reverse transcriptase activity of the L1Tc retroelement from Trypanosoma cruzi. Cell Mol. Life Sci. 60 (2003) 2692-2701
49. Gladyshev E.A., and Arkhipova I.R. Telomere-associated endonuclease-deficient Penelope-like retroelements in diverse eukaryotes. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 9352-9357
50. Goodwin T.J., and Poulter R.T. The DIRS1 group of retrotransposons. Mol. Biol. Evol. 18 (2001) 2067-2082
51. Goodwin T.J., and Poulter R.T. A group of deuterostome Ty3/gypsy-like retrotransposons with the Ty1/copia-like pol-domain order. Mol. Genet. Genomics 267 (2002) 481-491
52. Goodwin T.J., and Poulter R.T. A new group of tyrosine recombinase-encoding retrotransposons. Mol. Biol. Evol. 21 (2004) 746-759
53. Hansen L.J., and Sandmeyer S.B. Characterization of a transpositionally active Ty3 element and identification of the Ty3 integrase protein. J. Virol. 64 (1990) 2599-2607
54. Havecker E.R., Gao X., and Voytas D.F. The sireviruses, a plant-specific lineage of the Ty1/copia retrotransposons, interact with a family of proteins related to dynein light chain 8. Plant Physiol. 139 (2005) 857-868
55. 2 zinc finger motifs and is endowed with nucleic acid chaperone activity. Mol. Cell. Biol. 25 (2005) 9209-9220
56. Heredia F., Loreto E.L.S., and Valent V.L. Complex evolution of gypsy in Drosophilid species. Mol. Biol. Evol. 21 (2004) 1831-1842
57. Ivanov V.A., Melnikov A.A., Siunov A.V., Fodor I.I., and Ilyin Y.V. Authentic reverse transcriptase is coded by jockey, a mobile Drosophila element related to mammalian lines. EMBO J. 10 (1991) 2489-2495
58. Kajikawa M., and Okada N. LINEs mobilize SINEs in the eel through a shared 3′ sequence. Cell 111 (2002) 433-444
59. Kaushik N., Rege N., Yadav P.N., Sarafianos S.G., Modak M.J., and Pandey V.N. Biochemical analysis of catalytically crucial aspartate mutants of human immunodeficiency virus type 1 reverse transcriptase. Biochemistry 35 (1996) 11536-11546
60. Kaushik N., Chowdhury K., Pandey V.N., and Modak M.J. Valine of the YVDD motif of moloney murine leukemia virus reverse transcriptase: role in the fidelity of DNA synthesis. Biochemistry 39 (2000) 5155-5165
61. Kim A., Terzian C., Santamaria P., Pelisson A., Prudhomme N., and Bucheton A. Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 1285-1289
62. Kirchner J., and Sandmeyer S. Proteolytic processing of Ty3 proteins is required for transposition. J. Virol. 67 (1993) 19-28
63. Kirshenboim N., Hayouka Z., Friedler A., and Hizi A. Expression and characterization of a novel reverse transcriptase of the LTR retrotransposon Tf1. Virology 366 (2007) 263-276
64. Kohlstaedt L.A., Wang J., Friedman J.M., Rice P.A., and Steitz T.A. Crystal structure at 3.5 angstrom resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256 (1992) 1783-1790
65. Kojima K.K., Kuma K., Toh H., and Fujiwara H. Identification of rDNA-specific nonLTR retrotransposons in Cnidaria. Mol. Biol. Evol. 23 (2006) 1984-1993
66. Kulpa D.A., and Moran J.V. Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles. Nat. Struct. Mol. Biol. 13 (2006) 655-660
67. Kurzynska-Kokorniak A., Jamburuthugoda V.K., Bibillo A., and Eickbush T.H. DNA-directed DNA polymerase and strand displacement activity of the reverse transcriptase encoded by the R2 retrotransposon. J. Mol. Biol. 374 (2007) 322-333
68. Kuzio J., Pearson M.N., Harwood S.H., Funk C.J., Evans J.T., Slavicek J.M., and Rohrmann G.F. Sequence and analysis of the genome of a baculovirus pathogenic for Lymantria dispar. Virology 253 (1999) 17-34
69. Lai L., Liu H., Wu X., and Kappes J.C. Moloney murine leukemia virus integrase protein augments viral DNA synthesis in infected cells. J. Virol. 75 (2001) 11365-11372
70. Lander E.S., et al. Initial sequencing and analysis of the human genome. Nature 409 (2001) 860-921
71. Lapadat-Tapolsky M., Gabus C., Rau M., and Darlix J.L. Possible roles of HIV-1 nucleocapsid protein in the specificity of proviral DNA synthesis and in its variability. J. Mol. Biol. 268 (1997) 250-260
72. Laten H.M., Majumdar A., and Gaucher E.A. SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 6897-6902
73. Latham G.J., Forgacs E., Beard W.A., Prasad R., Bebenek K., Kunkel T.A., Wilson S.H., and Lloyd R.S. Vertical-scanning mutagenesis of a critical tryptophan in the "minor groove binding track" of HIV-1 reverse transcriptase. Major groove DNA adducts identify specific protein interactions in the minor groove. J. Biol. Chem. 275 (2000) 15025-15033
74. Levin H.L. A novel mechanism of self-primed reverse transcription defines a new family of retroelements. Mol. Cell. Biol. 15 (1995) 3310-3317
75. Levin H.L. An unusual mechanism of self-primed reverse transcription requires the RNase H domain of reverse transcriptase to cleave an RNA duplex. Mol. Cell. Biol. 16 (1996) 5645-5654
76. Levin H.L. It's prime time for reverse transcriptase. Cell 88 (1997) 5-8
77. Lin J.-H., and Levin H.L. A complex structure in the mRNA of Tf1 is recognized and cleaved to generate the primer of reverse transcription. Genes Dev. 11 (1997) 270-285
78. Lorenzi H.A., Robledo G., and Levin M.J. The VIPER elements of trypanosomes constitute a novel group of tyrosine recombinase-enconding retrotransposons. Mol. Biochem. Parasitol. 145 (2006) 184-194
79. Luan D.D., and Eickbush T.H. RNA template requirements for target DNA-primed reverse transcription by the R2 retrotransposable element. Mol. Cell. Biol. 15 (1995) 3882-3891
80. Luan D.D., and Eickbush T.H. Downstream 28S gene sequences on the RNA template affect the choice of primer and the accuracy of initiation by the R2 reverse transcriptase. Mol. Cell. Biol. 16 (1996) 4726-4734
81. Luan D.D., Korman M.H., Jakubczak J.L., and Eickbush T.H. Reverse transcription of R2Bm is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72 (1993) 595-605
82. Lyozin G.T., Makarova K.S., Velikodvorskaja V.V., Zelentsova H.S., Khechumian R.R., Kidwell M.G., Koonin E.V., and Evgen'ev M.B. The structure and evolution of Penelope in the virilis species group of Drosophila: an ancient lineage of retroelements. J. Mol. Evol. 52 (2001) 445-456
83. Malik H.S. Ribonuclease H evolution in retrotransposable elements. Cytogenet. Genome Res. 110 (2005) 392-401
84. Malik H.S., and Eickbush T.H. Phylogenetic analysis of Ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res. 11 (2001) 1187-1197
85. Malik H.S., Burke W.D., and Eickbush T.H. The age and evolution of non-LTR retrotransposable elements. Mol. Biol. Evol. 16 (1999) 793-805
86. Malik H.S., Henikoff S., and Eickbush T.H. Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res. 10 (2000) 1307-1318
87. Martin S.L., and Bushman F.D. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol. Cell. Biol. 21 (2001) 467-475
88. Martin F., Maranon C., Olivares M., Alonso C., and Lopez M.C. Characterization of a non-long terminal repeat retrotransposon cDNA (L1Tc) from Trypanosoma cruzi: homology of the first ORF with the APE family of DNA repair enzymes. J. Mol. Biol. 247 (1995) 49-59
89. Mathias S.L., Scott A.F., Kazazian H.H.J., Boeke J.D., and Gabriel A. Reverse transcriptase encoded by a human transposable element. Science 254 (1991) 1808-1810
90. Moran J.V., and Gilbert N. Mammalian LINE-1 retrotransposons and related elements. In: Craig N., Craigie R., Gellert M., and Lambowitz A. (Eds). Mobile DNA II (2002), American Society of Microbiology Press, Washington, DC 836-869
91. Moran J.V., Holmes S.E., Naas T.P., DeBerardinis R.J., Boeke J.D., and Kazazian H.H. High frequency retrotransposition in cultured mammalian cells. Cell 87 (1996) 917-927
92. Mount S.M., and Rubin G.M. Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol. Cell. Biol. 5 (1985) 1630-1638
93. Nakamura T.M., and Cech T.R. Reversing time: origin of telomerase. Cell 92 (1998) 587-590
94. Nymark-McMahon M.H., Beliakova-Bethell N.S., Darlix J.L., Le Grice S.F., and Sandmeyer S.B. Ty3 integrase is required for initiation of reverse transcription. J. Virol. 76 (2002) 2804-2816
95. Olivares M., Alonso C., and Lopez M.C. The open reading frame 1 of the L1Tc retrotransposon of Trypanosoma cruzi codes for a protein with apurinic-apyrimidinic nuclease activity. J. Biol. Chem. 272 (1997) 25224-25228
96. Olivares M., Thomas M.C., Alonso C., and Lopez M.C. The L1Tc, long interspersed nucleotide element from Trypanosoma cruzi, encodes a protein with 3′-phosphatase and 3′-phosphodiesterase enzymatic activities. J. Biol. Chem. 274 (1999) 23883-23886
97. Olivares M., Garcia-Perez J.L., Thomas M.C., Heras S.R., and Lopez M.C. The non-LTR (long terminal repeat) retrotransposon L1Tc from Trypanosoma cruzi codes for a protein with RNase H activity. J. Biol. Chem. 277 (2002) 28025-28030
98. Orlinsky K.J., and Sandmeyer S.B. The cys-his motif of Ty3 NC can be contributed by Gag3 or Gag3-Pol3 polyproteins. J. Virol. 68 (1994) 4152-4166
99. Ostertag E.M., and Kazazian Jr. H.H. Biology of mammalian L1 retrotransposons. Annu. Rev. Genet. 35 (2001) 501-538
100. Padow M., Lai L., Deivanayagam C., DeLucas L.J., Weiss R.B., Dunn D.M., Wu X., and Kappes J.C. Replication of chimeric human immunodeficiency virus type 1 (HIV-1) containing HIV-2 integrase (IN): naturally selected mutations in IN augment DNA synthesis. J. Virol. 77 (2003) 11050-11059
101. Pandey M., Patel S., and Gabriel A. Insights into the role of an active site aspartate in Ty1 reverse transcriptase polymerization. J. Biol. Chem. 279 (2004) 47840-47848
102. Peliska J.A., and Benkovic S.J. Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Science 258 (1992) 1112-1118
103. Piskareva O., and Schmatchenko V. DNA polymerization by the reverse transcriptase of the human L1 retrotransposon on its own template in vitro. FEBS Lett. 580 (2006) 661-668
104. Piskareva O., Denmukhametova S., and Schmatchenko V. Functional reverse transcriptase encoded by the human LINE-1 from baculovirus-infected insect cells. Protein Expr. Purif. 28 (2003) 125-130
105. Poch O., Sauvaget I., Delarue M., and Tordo N. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J. 8 (1989) 3867-3874
106. Powell M.D., Beard W.A., Bebenek K., Howard K.J., Le Grice S.F., Darden T.A., Kunkel T.A., Wilson S.H., and Levin J.G. Residues in the αH and αI helices of the HIV-1 reverse transcriptase thumb subdomain required for the specificity of RNase H-catalyzed removal of the polypurine tract primer. J. Biol. Chem. 274 (1999) 19885-19893
107. Pyatkov K.I., Arkhipova I.R., Malkova N.V., Finnegan D.J., and Evgen'ev M.B. Reverse transcriptase and endonuclease activities encoded by Penelope-like retroelements. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 14719-14724
108. Rothnie H.M., Chapdelaine Y., and Hohn T. Pararetroviruses and retroviruses: a comparative review of viral structure and gene expression strategies. Adv. Virus Res. 44 (1994) 1-67
109. Sandmeyer S.B., Hansen L.J., and Chalker D.L. Integration specificity of retrotransposons and Retroviruses. Annu. Rev. Genet. 24 (1990) 491-518
110. SanMiguel P., Gaut B.S., Tiknonov A., Nakajima Y., and Bennetzen J.L. The paleontology of intergene retrotransposons of maize. Nat. Genet. 20 (1998) 43-45
111. Song S.U., Gerasimova T., Kurkulos M., Boeke J.D., and Corces V.G. An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev. 8 (1994) 2046-2057
112. Steitz T.A., and Yin Y.W. Accuracy, lesion bypass, strand displacement and translocation by DNA polymerases. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 359 (2004) 17-23
113. Takahashi H., and Fujiwara H. Transplantation of target site specificity by swapping the endonuclease domains of two LINEs. EMBO J. 21 (2002) 408-417
114. Thomas J.A., and Gorelick R. Nucleocapsid protein function in early infection processes. Virus Res. 134 (2008) 39-63
115. Trentin B., Rebeyrotte N., and Mamoun R.Z. Human T-cell leukemia virus type 1 reverse transcriptase (RT) originates from the pro and pol open reading frames and requires the presence of RT-RNase H (RH) and RT-RH-integrase proteins for its activity. J. Virol. 72 (1998) 6504-6510
116. Uzun O., and Gabriel A. A Ty1 reverse transcriptase active-site aspartate mutation blocks transposition but not polymerization. J. Virol. 75 (2001) 6337-6347
117. Wei W., Gilbert N., Ooi S.-L., Lawler J.F., Ostertag E.M., Kazazian H.H., Boeke J.D., and Moran J.V. Human L1 retrotransposition: cis preference versus trans complementation. Mol. Cell. Biol. 21 (2001) 1429-1439
118. Weiner A.M., Deininger P.L., and Efstratiadis A. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu. Rev. Biochem. 55 (1986) 631-661
119. Wilhelm M., and Wilhelm F.X. Role of integrase in reverse transcription of the Saccharomyces cerevisiae retrotransposon Ty1. Eukaryot. Cell 4 (2005) 1057-1065
120. Wilhelm M., and Wilhelm F.X. Cooperation between reverse transcriptase and integrase during reverse transcription and formation of the preintegrative complex of Ty1. Eukaryot. Cell 5 (2006) 1760-1769
121. Wilhelm M., Boutabout M., and Wilhelm F.X. Expression of an active form of recombinant Ty1 reverse transcriptase in Escherichia coli: a fusion protein containing the C-terminal region of the Ty1 integrase linked to the reverse transcriptase-RNase H domain exhibits polymerase and RNase H activities. Biochem. J. 38 (2000) 337-342
122. Xiong Y., and Eickbush T.H. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol. Biol. Evol. 5 (1988) 675-690
123. Xiong Y., and Eickbush T.H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9 (1990) 3353-3362
124. Yang J., Malik H.S., and Eickbush T.H. Identification of the endonuclease domain encoded by R2 and other site-specific non-LTR retrotransposable elements. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7847-7852