Ty3 integrase mutants defective in reverse transcription or 3′-end processing of extrachromosomal Ty3 DNA

Journal of Virology

Volumn 70, Issue 7, 1996, Pages 4737-4747

  Kirchner, Jacqueline ^a   Sandmeyer, Suzanne B ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE; VIRUS RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA TRANSPOSITION; PRIORITY JOURNAL; PROTEIN FOLDING; RETROVIRUS; REVERSE TRANSCRIPTION; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; VIRUS MUTATION; VIRUS TRANSCRIPTION;

AMINO ACID SEQUENCE; ASPARTIC ACID; BASE SEQUENCE; DNA NUCLEOTIDYLTRANSFERASES; DNA, FUNGAL; GLUTAMIC ACID; INTEGRASES; MOLECULAR SEQUENCE DATA; MUTATION; RETROELEMENTS; RNA-DIRECTED DNA POLYMERASE; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION; TRANSCRIPTION, GENETIC;

EID: 0029938476     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.7.4737-4747.1996     Document Type: Article

References (80)

1. Arkhipova, I. R., A. M. Mazo, V. A. Cherkasova, T. V. Gorelova, N. G. Schuppe, and Y. V. Ilyin. 1986. The steps of reverse transcription of Drosophila mobile dispersed genetic elements and U3-R-U5 structure of their LTRs. Cell 44:555-563.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1996. Current protocols in molecular biology. Greene Publishing Associates/Wiley-Interscience, New York.
3. Berg, D. E., and M. M. Howe (ed.). 1989. Mobile DNA. American Society for Microbiology, Washington, D.C.
4. Bilanchone, V. B., and S. B. Sandmeyer. Unpublished data.
5. Bingham, P. M., and Z. Zachar. 1989. Retrotransposons and the FB transposon from Drosophila melanogaster, p. 485-502. In D. E. Berg and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
6. Boeke, J. D., D. Eichinger, D. Castrillon, and G. R. Fink. 1988. The Saccharomyces cerevisiae genome contains functional and nonfunctional copies of transposon Ty1. Mol. Cell. Biol. 8:1432-1442.
7. Braiterman, L. T., and J. D. Boeke. 1994. Ty1 in vitro integration: effects of mutations in cis and in trans. Mol. Cell. Biol. 14:5731-5740.
8. Brown, P. O., B. Bowerman, H. E. Varmus, and J. M. Bishop. 1989. Retroviral integration: structure of the initial covalent product and its precursor, and a role for the viral IN protein. Proc. Natl. Acad. Sci. USA 86:2525-2529.
9. Bushman, F. D., and R. Craigie. 1991. Activities of human immunodeficiency virus (HIV) integration protein in vitro: specific cleavage and integration of HIV DNA. Proc. Natl. Acad. Sci. USA 88:1339-1343.
10. Bushman, F. D., A. Engelman, I. Palmer, P. Wingfield, and R. Craigie. 1993. Domains of the integrase protein of human immunodeficiency virus type 1 responsible for polynucleotidyl transfer and zinc binding. Proc. Natl. Acad. Sci. USA 90:3428-3432.
11. Bushman, F. D., T. Fujiwara, and R. Craigie. 1990. Retroviral DNA integration directed by HIV integration protein in vitro. Science 249:1555-1558.
12. Bushman, F. D., and B. Wang. 1994. Rous sarcoma virus integrase protein: mapping functions for catalysis and substrate binding. J. Virol. 68:2215-2223.
13. Cannon, P. M., W. Wilson, E. Byles, S. M. Kingsntan, and A. J. Kingsman. 1994. Human immunodeficiency virus type 1 integrase: effect on viral replication of mutations at highly conserved residues. J. Virol. 68:4768-4775.
14. Chalker, D. L., and S. B. Sandmeyer. 1990. Transfer RNA genes are genomic targets for de novo transposition of the yeast retrotransposon Ty3. Genetics 126:837-850.
15. Chalker, D. L., and S. B. Sandmeyer. 1992. Ty3 integrates within the region of RNA polymerase III transcription initiation. Genes Dev. 6:117-128.
16. Chow, S. A., K. A. Vincent, V. Ellison, and P. O. Brown. 1992. Reversal of integration and DNA splicing mediated by integrase of human immunodeficiency virus. Science 255:723-726.
17. Clare, J. J., M. Belcourt, and P. J. Farabaugh. 1988. Efficient translational frameshifting occurs within a conserved sequence of the overlap between the two genes of a yeast Ty1 transposon. Proc. Natl. Acad. Sci. USA 85:6816-6820.
18. Craigie, R., T. Fujiwara, and F. Bushman. 1990. The IN protein of Moloney murine leukemia virus processes the viral DNA ends and accomplishes their integration in vitro. Cell 62:829-837.
19. Donehower, L. A. 1988. Analysis of mutant Moloney murine leukemia viruses containing linker insertion mutations in the 3′ region of pol. J. Virol. 62:3958-3964.
20. Dotan, I., B. P. Scottoline, T. S. Heuer, and P. O. Brown. 1995. Characterization of recombinant murine leukemia virus integrase. J. Virol. 69:456-468.
21. Dyda, F., A. B. Hickman, T. M. Jenkins, A. Engelman, K. Craigie, and D. R. Davies. 1994. Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266:1981-1986.
22. Eichinger, D. J., and J. D. Boeke. 1988. The DNA intermediate in yeast Ty1 element transposition copurifies with virus-like particles: cell-free Ty1 transposition. Cell 54:955-966.
23. Eichinger, D. J., and J. D. Boeke. 1990. A specific terminal structure is required for Ty1 transposition. Genes Dev. 4:324-330.
24. Eijkelenboom, A. P. A. M., R. A. Puras Lutzke, R. Boelens, R. H. A. Plasterk, R. Kaptein, and K. Hard. 1995. The DNA-binding domain of HIV-1 integrase has an SH3-like fold. Nat. Struct. Biol. 2:807-810.
25. Ellison, V., and P. O. Brown. 1994. A stable complex between integrase and viral DNA ends mediates human immunodeficiency virus integration in vitro. Proc. Natl. Acad. Sci. USA 91:7316-7320.
26. Engelman, A., F. D. Bushman, and R. Craigie. 1993. Identification of discrete functional domains of HIV-1 integrase and their organization within an active multimeric complex. EMBO J. 12:3269-3275.
27. Engelman, A., and R. Craigie. 1992. Identification of conserved amino acid residues critical for human immunodeficiency virus type 1 integrase function in vitro. J. Virol. 66:6361-6369.
28. Engelman, A., G. Englund, J. M. Orenstein, M. A. Martin, and R. Craigie. 1995. Multiple effects of mutations in human immunodeficiency virus type 1 integrase on viral replication. J. Virol. 69:2729-2736.
29. Engelman, A., A. B. Hickman, and R. Craigie. 1994. The core and carboxyl-terminal domains of the integrase protein of human immunodeficiency virus type 1 each contribute to nonspecific DNA binding. J. Virol. 68:5911-5917.
30. Fujiwara, T., and K. Mizuuchi. 1988. Retroviral DNA integration: structure of an integration intermediate. Cell 54:497-504.
31. Gabriel, A., and J. D. Boeke. 1993. Retrotransposon reverse transcription, p. 275-328. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
32. Gibson, W., and I. Verma. 1974. Studies on the reverse transcriptase of RNA tumor viruses. Structural relatedness of two subunits of avian RNA tumor viruses. Proc. Natl. Acad. Sci. USA 71:4991-4994.
33. Hansen, L. J., D. L. Chalker, K. J. Orlinsky, and S. B. Sandmeyer. 1992. Ty3 GAG3 and POL3 genes encode the components of intracellular particles. J. Virol. 66:1414-1424.
34. Hansen, L. J., D. L. Chalker, and S. B. Sandmeyer. 1988. Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol. Cell. Biol. 8:5245-5256.
35. Hansen, L. J., and S. B. Sandmeyer. 1990. Characterization of a transpositionally active Ty3 element and identification of the Ty3 integrase protein. J. Virol. 64:2599-2607.
36. Hippenmeyer, P. J., and D. P. Grandgenett. 1984. Requirement of the avian retrovirus pp32 DNA binding protein domain for replication. Virology 137:358-370.
37. Johnson, M. S., M. A. McClure, D.-F. Feng, J. Gray, and R. F. Doolittle. 1986. Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homnologies with non-viral enzymes. Proc. Natl. Acad. Sci. USA 83:7648-7652.
38. Jonsson, C. B., and M. J. Roth. 1993. Role of the His-Cys finger of Moloney murine leukemia virus integrase protein in integration and disintegration. J. Virol. 67:5562-5571.
39. Kalpana, G. V., and S. P. Goff. 1993. Genetic analysis of homomeric interactions of human immunodeficiency virus type 1 integrase using the yeast two-hybrid system. Proc. Natl. Acad. Sci. USA 90:10593-10597.
40. Katz, R. A., G. Merkel, J. Kulkoskv, J. Leis, and A. M. Skalka. 1990. The avian retroviral IN protein is both necessary and sufficient for integrative recombination in vitro. Cell 63:87-95.
41. Katzman, M., R. A. Katz, A. M. Skalka, and J. Leis. 1989. The avian retroviral integration protein cleaves the terminal sequences of linear viral DNA at the in vivo sites of integration. J. Virol. 63:5319-5327.
42. Katzman, M., J. P. G. Mack, A. M. Skalka, and J. Leis. 1991. A covalent complex between retroviral integrase and nicked substrate DNA. Proc. Natl. Acad. Sci. USA 88:4695-4699.
43. Keeney, J. B., K. B. Chapman, V. Lauermann, D. F. Voytas, S. V. Åstrom, U. von Pawel-Rammingen, A. Byström, and J. D. Boeke. 1995. Multiple molecular determinants for retrotransposition in a primer tRNA. Mol. Cell. Biol. 15:217-226.
44. Keeney, J. B., P. T. Kinsey, S. B. Sandmeyer, and J. D. Boeke. Unpublished data.
45. Khan, E., J. P. Mack, R. A. Katz, J. Kulkosky, and A. M. Skalka. 1991. Retroviral integrase domains: DNA binding and the recognition of LTR sequences. Nucleic Acids Res. 19:851-860.
46. Kirchner, J., C. M. Connolly, and S. B. Sandmeyer. 1995. Requirement of RNA polymerase III transcription factors for in vitro position-specific integration of a retroviruslike element. Science 267:1488-1491.
47. Kirchner, J., and B. S. Sandmeyer. 1993. Proteolytic processing of Ty3 proteins is required for transposition. J. Virol. 67:19-28.
48. knaus, R. J., P. J. Hippenmeyer, T. K. Misra, D. P. Grandgenett, U. R. Müller, and W. M. Fitch. 1984. Avian retrovirus pp32 DNA binding protein. Preferential binding to the promoter region of long terminal repeat DNA. Biochemistry 23:350-359.
49. Kohlstaedt, L. A., J. Wang, J. M. Friedman, P. A. Rice, and T. A. Steitz. 1992. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256:1783-1790.
50. Kulkosky, J., K. S. Jones, R. A. Katz, J. P. G. Mack, and A. M. Skalka. 1992. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol. Cell. Biol. 12:2331-2338.
51. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
52. Lauermann, V., and J. D. Boeke. 1994. The primer tRNA sequence is not inherited during Ty1 transposition. Proc. Natl. Acad. Sci. USA 91:9847-9851.
53. Leavitt, A. D., L. Shiue, and H. E. Varmus. 1993. Site-directed mutagenesis of HIV-1 integrase demonstrates differential effects on integrase functions in vitro. J. Biol. Chem. 268:2113-2119.
54. Leis, J. P. 1976. RNA-dependent DNA polymerase activity of RNA tumor virus. VI. Processive mode of action of avian myeloblastosis virus polymerase. J. Virol. 19:932-939.
55. Lightfoote, M. M., J. E. Coligan, T. M. Folks, A. S. Fauci, M. A. Martin, and S. Venkatesan. 1986. Structural characterization of reverse transcriptase and endonuclease polypeptides of the acquired immunodeficiency syndrome retrovirus. J. Virol. 60:771-775.
56. Lodi, P. J., J. A. Ernst, J. Kuszewski, A. B. Hickman, A. Engelman, R. Craigie, G. M. Clore, and A. M. Gronenborn. 1995. Solution structure of the DNA binding domain of HIV-1 integrase. Biochemistry 34:9826-9833.
57. Menees, T. M., and S. B. Sandmeyer. 1994. Transposition of the yeast retroviruslike element Ty3 is dependent on the cell cycle. Mol. Cell. Biol. 14:8229-8340.
58. Moore, S. P., and D. J. Garfinkel. 1994. Expression and partial purification of enzymatically active recombinant Ty1 integrase in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 91:1843-1847.
59. Müller, F., W. Laufer, U. Pott, and M. Ciriacy. 1991. Characterization of products of Ty1-mediated reverse transcription in Saccharomyces cerevisiae. Mol. Gen. Genet. 226:145-153.
60. Mumm, S. R., and D. P. Grandgenett. 1991. Defining nucleic acid-binding properties of avian retrovirus intcgrase by deletion analysis. J. Virol. 65:1160-1167.
61. Orlinsky, K. J., and S. B. Sandmeyer. 1994. The Cys-His motif of Ty3 NC can be contributed by Gag3 or Gag3-Pol3 polyproteins. J. Virol. 68:4152-4166.
62. Pochart, P., B. Agooutin, S. Rousset, R. Chanet, V. Doroszkiewicz, and T. Heyman. 1993. Biochemical and electron microscope analyses of the DNA reverse transcripts present in the virus-like particles of the yeast transposon Ty1. Identification of a second origin of Ty1 DNA plus-strand synthesis. Nucleic Acids Res. 21:3513-3520.
63. Puras Lutzke, R. A., C. Vink, and R. H. A. Plasterk. 1994. Characterization of the minimal DNA-binding domain of the HIV integrase protein. Nucleic Acids Res. 22:4125-4131.
64. Lys primer-binding site of human immunodeficiency virus type 1 identify essential regions for reverse transcription. J. Virol. 65:4555-4564.
65. Rho, H. M., D. P. Grandgenett, and M. Green. 1975. Sequence relatedness between the subunits of avian myeloblastosis virus reverse transcriptase. J. Biol. Chem. 250:5278-5280.
66. Roth, M. J. 1991. Mutational analysis of the carboxyl terminus of the Moloney murine leukemia virus integration protein. J. Virol. 65:2141-2145.
67. Roth, M. J., P. L. Schwartzberg, and S. P. Goff. 1989. Structure of the termini of DNA intermediates in the integration of retroviral DNA: dependence on IN function and terminal DNA sequence. Cell 58:47-54.
68. Roth, M. J., P. Schwartzberg, N. Tanese, and S. P. Goff. 1990. Analysis of mutations in the integration function of Moloney murine leukemia virus: effects on DNA binding and cutting. J. Virol. 64:4709-4717.
69. Roth, M. J., N. Tanese, and S. P. Goff. 1988. Gene product of Moloney murine leukemia virus required for proviral integration is a DNA-binding protein. J. Mol. Biol. 203:131-139.
70. Schiff, R. D., and D. P. Grandgenett. 1978. Virus-coded origin of a 32,000-dalton protein from avian retrovirus cores: structural relatedness of p32 and the beta polypeptide of the avian retrovirus DNA polymerase. J. Virol. 28:279-291.
71. Sherman, P. A., and J. A. Fyfe. 1990. Human immunodeficiency virus integration protein expressed in Escherichia coli possesses selective DNA cleaving activity. Proc. Natl. Acad. Sci. USA 87:5119-5123.
72. Shin, C.-G., B. Taddeo, W. A. Haseltine, and C. M. Farnet. 1994. Genetic analysis of the human immunodeficiency virus type 1 integrase protein. J. Virol. 68:1633-1642.
73. Skalka, A. M., and S. P. Goff (ed.). 1993. Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
74. Telesnitsky, A., and S. P. Goff. 1993. Strong-stop strand transfer during reverse transcription, p. 49-83. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
75. van Gent, D. C., A. A. M. Oude Groeneger, and R. H. A. Plasterk. 1992. Mutational analysis of the integrase protein of human immunodeficiency virus type 2. Proc. Natl. Acad. Sci. USA 89:9598-9602.
76. Veronese, F. D., T. D. Copeland, A. L. DeVico, R. Rahman, S. Oroszlan, R. C. Gallo, and M. G. Sarngadharan. 1986. Characterization of highly immunogenic p66/p51 as the reverse transcriptase of HTLVIII/LAV. Science 231:1289-1291.
77. Vincent, K. A., V. Ellison, S. A. Chow, and P. O. Brown. 1993. Characterization of human immunodeficiency virus type 1 integrase expressed in Escherichia coli and analysis of variants with amino-terminal mutations. J. Virol. 67:425-437.
78. Vink, C., A. A. M. Oude Groeneger, and R. H. A. Plasterk. 1993. Identification of the catalytic and DNA-binding region of the human immunodeficiency virus type 1 integrase protein. Nucleic Acids Res. 21:1419-1425.
79. Vora, A. C., M. L. Fitzgerald, and D. P. Grandgenett. 1990. Removal of 3′-OH-terminal nucleotides from blunt-ended long terminal repeat termini by the avian retrovirus integration protein. J. Virol. 64:5656-5659.
80. Wiskerchen, M., and M. A. Muesing. 1995. Human immunodeficiency virus type 1 integrase: effects of mutations on viral ability to integrate, direct viral gene expression from unintegrated viral DNA templates, and sustain viral propagation in primary cells. J. Virol. 69:376-386.