Posttranslational inhibition of Ty1 retrotransposition by nucleotide excision repair/transcription factor TFIIH subunits Ssl2p and Rad3p

Genetics

Volumn 148, Issue 4, 1998, Pages 1743-1761

  Lee, Bum Soo ^a   Lichtenstein, Conrad P ^a,c   Faiola, Brenda ^a,d   Rinckel, Lori A ^a,e   Wysock, William ^a,f   Curcio, M Joan ^b   Garfinkel, David J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; HELICASE; TRANSCRIPTION FACTOR;

ARTICLE; EXCISION REPAIR; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PROCESSING; RETROPOSON; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION;

ADENOSINE TRIPHOSPHATASES; ALCOHOL OXIDOREDUCTASES; ALLELES; AMINOHYDROLASES; CHROMOSOMES, FUNGAL; DNA HELICASES; DNA REPAIR; DNA TRANSPOSABLE ELEMENTS; DNA, COMPLEMENTARY; FUNGAL PROTEINS; GENE EXPRESSION REGULATION; MUTAGENESIS; PROTEIN BIOSYNTHESIS; PYROPHOSPHATASES; RECOMBINATION, GENETIC; RETROELEMENTS; SACCHAROMYCES CEREVISIAE PROTEINS; TATA-BINDING PROTEIN ASSOCIATED FACTORS; TRANSCRIPTION FACTOR TFIID; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS, TFII;

SACCHAROMYCES CEREVISIAE;

EID: 0031953262     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (90)

1. AGUILERA, A., 1994 Formamide sensitivity: a novel conditional phenotype in yeast. Genetics 136: 87-91.
2. ALANI, E., L. CAO and N. KLECKNER, 1987 A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116: 541-545.
3. ATKIN, A. L., N. ALTAMURA, P. LEEDS and M. R. CULBERTSON, 1995 The majority of yeast UPF1 colocalizes with polyribosomes in the cytoplasm. Mol. Biol. Cell 6: 611-625.
4. BAILIS, A. M., and S. MAINES, 1996 Nucleotide excision repair gene function in short-sequence recombination. J. Bacteriol. 178: 2136-2140.
5. BAILIS, A. M., S. MAINES and M. T. NEGRITTO, 1995 The essential helicase gene RAD3 suppresses short-sequence recombination in Sacchammyces cerevisiae. Mol. Cell. Biol. 15: 3998-4008.
6. BELCOURT, M. F., and P. J. FARABAUGH, 1990 Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell 62: 339-352.
7. BEST, S., P. LE TISSIER, G. TOWERS and J. P. STOYE, 1996 Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382: 826-829.
8. BOEKE, J. D., 1988 Retrotransposons, pp. 59-103 in RNA Genetics, Retroviruses, Viroids, and RNA Recombination, edited by E. DOMINGO, J. HOLLAND and P. AHLQUIST. CRC Press, Boca Raton, FL.
9. BOEKE, J. D., and S. B. SANDMEYER, 1991 Yeast transposable elements, pp. 193-261 in The Molecular and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis, and Energetics, edited by J. R. PRINGLE, E. W. JONES and J. R. BROACH. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
10. BOEKE, J. D., F. LACROUTE and G. R. FINK, 1984 A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoroorotic acid resistance. Mol. Gen. Genet. 197: 345-346.
11. BOEKE, J. D., D. J. GARFINKEL, C. A. STYLES and G. R. FINK, 1985 Ty elements transpose through an RNA intermediate. Cell 40: 491-500.
12. BOEKE, J. D., C. A. STYLES and G. R. FINK, 1986 Saccharomyces cerevisiae SPT3 gene is required for transposition and transpositional recombination of chromosomal Ty elements. Mol. Cell. Biol. 6: 3575-3581.
13. 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.
14. BRAUSHAW, V. A., and K. McENTEE, 1989 DNA damage activates transcription and transposition of yeast Tyretrotransposons. Mol. Gen. Genet. 218: 465-474.
15. BROACH, J. R., J. N. STRATHERN and J. B. HICKS, 1979 Transformation in yeast: development of a hybrid cloning vector and isolation of the CAN1 gene. Gene 8: 121-133.
16. CIGAN, A. M., E. K. PABICH and T. F. DONAHUE, 1988 Mutational analysis of the HIS4 translational initiator region in Saccharomyces cerevisiae, Mol. Cell. Biol. 8: 2964-2975.
17. CONTE, D., E. BARBER, M. BANERJEE, D. J. GARFINKEL and M. J. CURCIO, 1998 Posttranslational regulation of Ty1 retrotransposition by the MAP kinase, Fus 3. Mol. Cell. Biol. (in press).
18. CRAIGIE, R., 1992 Hotspots and warm spots: integration specificity of retroelements. Trends Genet. 8: 187-190.
19. CURCIO, M. J., and D. J. GARFINKEL, 1991 Single-step selection for Ty1 element retrotransposition. Proc. Natl. Acad. Sci. USA 88: 936-940.
20. CURCIO, M. J., and D. J. GARFINKEL, 1992 Posttranslational control of Ty1 retrotransposition occurs at the level of protein processing. Mol. Cell. Biol. 12: 2813-2825.
21. CURCIO, M. J., and D. J. GARFINKEL, 1994 Heterogenous functional Ty1 elements are abundant in the Saccharomyces cerevisiae genome. Genetics 136: 1245-1259.
22. CURCIO, M. J., and R. H. MORSE, 1996 Tying together integration and chromatin. Trends Genet. 12: 436-138.
23. CURCIO, M. J., A. M. HEDGE, J. D. BOEKE and D. J. GARFINKEL, 1990 Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Mol. Gen. Genet. 220: 213-221.
24. DEVINE, S. E., and J. D. BOEKE, 1996 Integration of the yeast retrotransposon Ty1 is targeted to regions upstream of genes transcribed by RNA polymerase III. Genes Dev. 10: 620-633.
25. DRAKE, J. W., 1970 The Molecular Basis of Mutation. Holden-Day, San Francisco.
26. 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.
27. EICHINGER, D. J., and J. D. BOEKE, 1990 A specific terminal structure is required for Ty1 transposition. Genes Dev. 4: 324-330.
28. ELDER, R. T., E. Y. LOH and R. W. DAVIS, 1983 RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc. Natl. Acad. Sci. USA 80: 2432-2436.
29. ERREDE, B., T. S. CARDILLO, F. SHERMAN, E. DUBOIS, J. DESCHAMPS et al., 1980 Mating signals control expression of mutations resulting from insertion of a transposable repetitive element adjacent to diverse yeast genes. Cell 22: 427-436.
30. FARABAUGH, P. J., 1995 Post-transcriptional regulation of transposition by Ty retrotransposons of Saccharomyces cerevisiae. J. Biol. Chem. 270: 10361-10364.
31. FARNET, C. M., and F. D. BUSHMAN, 1997 HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro. Cell 88: 483-492.
32. FEAVER, W. J., J. Q. SVEJSTRUP, L. BARDWELL, A. J. BARDWELL, S. BURATOWSKI et al., 1993 Dual roles of a multiprotein complex from S. cerevisiae in transcription and DNA repair. Cell 75: 1379-1387.
33. FLAVELL, A. J., 1995 Retroelements, reverse transcriptase and evolution. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 110: 3-15.
34. GARFINKEL, D. J., 1992 Retroelements in microorganisms, pp. 107-158 in The Retroviridae, edited by J. A. LEVY. Plenum Press, New York.
35. GARFINKEL, D. J., J. D. BOKKE and G. R. FINK, 1985 Ty element transposition: reverse transcriptase and virus-like particles. Cell 42: 507-517.
36. GARFINKEL, D. J., A. M. HEDGE, S. D. YOUNGRKN and T. D. COPELAND, 1991 Proteolytic processing of pol-TYB proteins from the yeast retrotransposon Ty1. J. Virol. 65: 4573-4581.
37. GOFFEAU, A., B. G. BARRELL, H. BUSSEY, R. W. DAVLS, B. DUJON et al., 1996 Life with 6000 genes. Science 274: 563-567.
38. GULYAS, K. D., and T. F. DONAHUE, 1992 SSL2, a suppressor of a stem-loop mutation in the HIS4 leader encodes the yeast homolog of human ERCC-3. Cell 69: 1031-1042.
39. GUTHRIE, C., and G. R. FINK, 1991 Guide to Yeast Genetics and Molecular Biology, Methods in Enzymology, Vol. 194, Academic Press, Inc., San Diego.
40. GUZDER, S. N., H. QIU, C. H. SOMMERS, P. SUNG, L. PRAKASH et al., 1994a DNA repair gene RAD3 of S. cerevisiae is essential for transcription by RNA polymerase II. Nature 367: 91-94.
41. GUZDER, S. N., P. SUNG, V. BAILLY, L. PRAKASH and S. PRAKASH, 1994b RAD25 is a DNA helicase required for DNA repair and RNA polymerase II transcription. Nature 369: 578-581.
42. GUZDER, S. N., P. SUNG, L. PRAKASH and S. PRAKASH, 1996 Nucleotide excision repair in yeast is mediated by sequential assembly of repair factors and not be a pre-assembled repairosome. J. Biol. Chem. 271: 8903-8910.
43. HOFFMAN, C. S., and F. WINSTON, 1987 A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272.
44. JI, H., D. P. MOORE, M. A. BLOMBERG, L. T. BRAITERMAN, D. F. VOYTAS et al., 1993 Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell 73: 1007-1018.
45. KALPANA, G. V., S. MARMON, W. WANG, G. R. CRABTREE and S. P. GOFF, 1994 Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 266: 2002-2006.
46. LAWRENCE, C., 1994 The RAD6 DNA Repair Pathway in Saccharomyces cerevisiae: What does it do, and how does it do it? BioEssays 16: 253-258.
47. LEE, M. S., and R. CRAIGIK, 1994 Protection of retroviral DNA from autointegration: involvement of a cellular factor. Proc. Natl. Acad. Sci. USA 91: 9823-9827.
48. LEHMANN, A. R., 1995 Nucleotide excision repair and the link with transcription. Trends Biochem. Sci. 20: 402-405.
49. LIEBMAN, S. W., and G. NEWNAM, 1993 A ubiquitin-conjugating enzyme, RAD6, affects the distribution of Ty1 retrotransposon integration positions. Genetics 133: 499-508.
50. MANIVASAKAM, P., S. C. WEBKR, J. McELVER and R. H. SCHIESTL, 1995 Micro-homology mediated PCR targeting in Saccharomyces cerevisiae. Nucleic Acids Res. 23: 2799-2800.
51. McCLINTOCK, B., 1984 The significances of responses of the genome to challenge. Science 226: 792-801.
52. MILLER, M. D., C. M. FARNET and F. D. BUSHMAN, 1997 Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J. Virol. 71: 5382-5390.
53. MONTELONE, B. A., M. F. HOEKSTRA and R. E. MALONE, 1988 Spontaneous mitotic recombination in yeast: the hyper-recombinational rem1 mutations are alleles of the RAD3 gene. Genetics 119: 289-301.
54. MOUNKES, L. C., R. S. JONES, B. C. LIANO, W. GELBART and M. T. FULLER, 1992 A Drosophila model for xeroderma pigmentosum and Cockayne's syndrome: haywire encodes the fly homolog of ERCC3, a human excision repair gene. Cell 71: 925-937.
55. ORPHANIDES, G., T. LAGRANGE and D. REINBERG, 1996 The general transcription factors of RNA polymerase II. Genes Dev. 10: 2657-2683.
56. PARK, E., S. N. GUZDEK, M. H. KOKEN, I. JASPERS-DEKKER, G. WEEDA et al., 1992 RAD25 (SSL2), the yeast homolog of the human xeroderma pigmentosum group B DNA repair gene, is essential for viability. Proc. Natl. Acad. Sci. USA 89: 11416-11420.
57. PRYCIAK, P. M., and H. E. VARMUS, 1992 Fv-1 restriction and its effects on murine leukemia virus integration in vivo and in vitro. J. Virol. 66: 5959-5966.
58. QIU, H., E. PARK, L. PRAKASH and S. PRAKASH, 1993 The Saccharomfces cerevisiae DNA repair gene RAD25 is required for transcription by RNA polymerase II. Genes Dev. 7: 2161-2171.
59. RATTRAY, A. J., and L. S. SYMINGTON, 1994 Use of a chromosomal inverted repeat to demonstrate that the RAD51 and RAD52 genes of Saccharomyces cerevisiae have different roles in mitotic recombination. Genetics 138: 587-595.
60. RINCKEL., L. A., and D. J. GARFINKEL, 1996 Influences of histone stoichiometry on the target site preference of retrotransposons Ty1 and Ty2 in Saccharomyces cerevisiae. Genetics 142: 761-776.
61. ROBERTS, R. L., and G. R. FINK, 1994 Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev. 8: 2974-2985.
62. ROLFE., M., A. SPANOS and G. BANKS, 1986 Induction of yeast Ty clement transcription by ultraviolet light. Nature 319: 339-340.
63. ROSE, M., M. J. CASADABAN and D. BOTSTEIN, 1981 Yeast genes fused to beta-galactosidase in Escherichia coli can be expressed normally in yeast. Proc. Natl. Acad. Sci. USA 78: 2460-2464.
64. ROSE, M. D., P. NOVICK, J. H. THOMAS, D. BOTSTEIN and G. R. FINK, 1987 A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60: 237-243.
65. ROSE, M. D., F. WINSION and P. HIETER, 1990 Hydroxylamine mutagcnesis of plasmid DNA, p. 198 in Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
66. SAMBROOK, J., E. FRITSCH and T. MANIATIS, 1989 Molecular Cloning, a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
67. SANDMEYER, S. B., L. J. HANSEN and D. L. CHALKER, 1990 Integration specificity of retrotransposons and retroviruses. Annu. Rev. Genet. 24: 491-518.
68. SHARON, G., T. J. BURKETT and D. J. GARFINKEL, 1994 Homologous recombination of Ty1 element cDNA when integration is blocked. Mol. Cell. Biol. 14: 6540-6551.
69. SHERMAN, F., G. R. FINK and J. B. HICKS, 1986 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
70. SIKORSKI, R. S., and P. HIETER, 1989 A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
71. SMITH, V., D. BOTSTEIN and P. O. BROWN, 1995 Genetic foot-printing: a genomic strategy for determining a gene's function given its sequence. Proc. Natl. Acad. Sci. USA 92: 6479-6483.
72. SONG, J. M., B. A. MONTELONE, W. SIEDE and E. C. FRIEDBERG, 1990 Effects of multiple yeast rad3 mutant alleles on UV sensitivity, mutability, and mitotic recombination. J. Bacteriol. 172: 6620-6630.
73. STRUHL, K., D. T. STINCHCOMB, S. SCHERER and R. W. DAVIS, 1979 High-frequency transformation of yeast: autonomous replication of hybrid DNA molecules. Proc. Natl. Acad. Sci. USA 76: 1035-1039.
74. SUBRAMANYA, H. S., L. E. BIRD, J. A. BRANNIGAN and D. B. WIGLEY, 1996 Crystal structure of a DExx box DNA helicase. Nature 384: 379-383.
75. SUNG, P., L. PRAKASH, S. WEBER and S. PRAKASH, 1987 The RAD3 gene of Saccharomyces cerevisiae encodes a DNA-dependent ATPase. Proc. Natl. Acad. Sci. USA 84: 6045-6049.
76. SUNG, P., S. N. GUZDER, L. PRAKASH and S. PRAKASH, 1996 Reconstitution of TFIIH and requirement of its DNA helicase subunits, Rad3 and Rad25, in the incision step of nucleotide excision repair. J. Biol. Chem. 271: 10821-10826.
77. SVEJSTRUP, J. Q., Z. WANG, W. J. FEAVER, X. Wu, D. A. BUSHNELL et al., 1995 Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nuclcotide excision repairosome. Cell 80: 21-28.
78. SVEJSTRUP, J. Q., P. VICHI and J. M. EGLY, 1996 The multiple roles of transcription/repair factor TFIIH. Trends Biochem. Sci. 21: 346-350.
79. SWEDKR, K. S., and P. C. HANAWALT, 1994 The COOH terminus of suppressor of stem loop Ss12/Rad25 in yeast is essential for overall genomic excision repair and transcription-coupled repair. J. Biol. Chem. 269: 1852-1857.
80. TFMIN, H. M., 1985 Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol. Biol. Evol. 2: 455-468.
81. VOYTAS, D. F., 1996 Retroelements in genome organization. Science 274: 737-738.
82. WALKER, J. E., M. SARASTE , M. J. RUNSWICK and N. J. GAY, 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. EMBOJ. 1: 945-951.
83. WANG, Z., J. Q. SVKJSTRUP, W. J. FEAVER, X. Wu, R. D. KORNBERG, et al., 1994 Transcription factor b (TFIIH) is required during nucleotide-excision repair in yeast. Nature 368: 74-76.
84. WANG, Z., S. BURATOWSKI, J. Q. SVKJSTRUP, W. J. FEAVER, X. Wu et al., 1995 The yeast TFB1 and SSL1 genes, which encode subunits of transcription factor IIH, are required for nucleotide excision repair and RNA polymerase II transcription. Mol. Cell. Biol. 15: 2288-2293.
85. WEEDA, G., R. C. VAN HAM, W. VERMEULEN, D. BOOTSMA, A. J. VAN DER EB et al., 1990 A presumed DNA helicase encoded by ERCC-3 is involved in the human repair disorders xeroderma pigmentosum and Cockayne's syndrome. Cell 62: 777-791.
86. WEEDA, G., M. ROSSIGNOL, R. A. FRASFR, G. S. WINKLER, W. VERMULEN et al., 1997 The XPB subunit of repair/transcription factor TFIIH directly interacts with SUG1, a subunit of the 26S proteasome and putative transcription factor. Nucleic Acids Res. 25: 2274-2283.
87. WESSLER, S. R., 1996 Turned on by stress. Plant retrotransposons. Curr. Biol. 6: 959-961.
88. WILKE, C. M., S. H. HEIDLER, N. BROWN and S. W. LIEBMAN, 1989 Analysis of yeast retrotransposon Ty insertions at the CAN1 locus. Genetics 123: 655-665.
89. WINSTON, F., K.J. DURBIN and G. R. Fink, 1984 The SPT3 gene is required for normal transcription of Ty elements in S. cerevisiae. Cell 39: 675-682.
90. YOUNGREN, S. D., J. D. BOEKE, N. J. SANDERS and D. J. GARFINKEL, 1988 Functional organization of the retrotransposon Ty from Saccharomyces cerevisiae: Ty protease is required for transposition. Mol. Cell. Biol. 8: 1421-1431.