Severe adenine starvation activates Ty1 transcription and retrotransposition in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 25, Issue 17, 2005, Pages 7459-7472

  Todeschini, Anne Laure ^a   Morillon, Antonin ^a   Springer, Mathias ^a   Lesage, Pascale ^a,b  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ADENOSINE PHOSPHATE; COMPLEMENTARY DNA; MESSENGER RNA;

ADE GENE; ARTICLE; BAS1 GENE; BIOSYNTHESIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; FUNGAL GENE; GENE; GENE EXPRESSION; GENE INDUCTION; GENE SEQUENCE; HTA1 GENE; HTB1 GENE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; RETROPOSON; SACCHAROMYCES CEREVISIAE; SNF2 GENE; STARVATION; STRESS; TRANSCRIPTION INITIATION; TY1 GENE; YEAST;

ADENINE; ADENOSINE MONOPHOSPHATE; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; MUTATION; RETROELEMENTS; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 23844536533     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.17.7459-7472.2005     Document Type: Article

References (60)

1. Adams, A., D. E. Gottschling, C. A. Kaiser, and T. Stearns. 1997. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
2. Baur, M., R. K. Esch, and B. Errede. 1997. Cooperative binding interactions required for function of the Ty1 sterile responsive element. Mol. Cell. Biol. 17:4330-4337.
3. 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.
4. 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.
5. Bradshaw, V. A., and K. McEntee. 1989. DNA damage activates transcription and transposition of yeast Ty retrotransposons. Mol. Gen. Genet. 218: 465-474.
6. Bryk, M., M. Banerjee, M. Murphy, K. E. Knudsen, D. J. Garfinkel, and M. J. Curcio. 1997. Transcriptional silencing of Ty1 elements in the RDN1 locus of yeast. Genes Dev. 11:255-269.
7. Ciriacy, M., K. Freidel, and C. Lohning. 1991. Characterization of transacting mutations affecting Ty and Ty-mediated transcription in Saccharomyces cerevisiae. Curr. Genet. 20:441-448.
8. Conte, D. J., E. Barber, M. Banerjee, D. J. Garfinkel, and M. J. Curcio. 1998. Posttranslational regulation of Ty1 retrotransposition by mitogen-activated protein kinase Fus3. Mol. Cell. Biol. 18:2502-2513.
9. Conte, D. J., and J. M. Curcio. 2000. Fus3 controls Ty1 transpositional dormancy through the invasive growth MAPK pathway. Mol. Microbiol. 35:415-427.
10. Curcio, M. J., and D. J. Garfinkel. 1999. New lines of host defense: inhibition of Ty1 retrotransposition by Fus3p and NER/TFIIH. Trends Genet. 15:43-45.
11. 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.
12. Curcio, M. J., and D. J. Garfinkel. 1991. Single-step selection for Ty1 element retrotransposition. Proc. Natl. Acad. Sci. USA 88:936-940.
13. Daignan-Fornier, B., and G. R. Fink. 1992. Coregulation of purine and histidine biosynthesis by the transcriptional activators BAS1 and BAS2. Proc. Natl. Acad. Sci. USA 89:6746-6750.
14. Denis, V., H. Boucherie, C. Monribot, and B. Daignan-Fornier. 1998. Role of the myb-like protein bas1p in Saccharomyces cerevisiae: a proteome analysis. Mol. Microbiol. 30:557-566.
15. Dudley, A. M., L. J. Gansheroff, and F. Winston. 1999. Specific components of the SAGA complex are required for Gcn4- and Gcr1-mediated activation of the his4-912Δ promoter in Saccharomyces cerevisiae. Genetics 151:1365-1378.
16. Errede, B. 1993. MCM1 binds to a transcriptional control element in Ty1. Mol. Cell. Biol. 13:57-62.
17. Errede, B., M. Company, and C. A. D. Hutchison. 1987. Ty1 sequence with enhancer and mating-type-dependent regulatory activities. Mol. Cell. Biol. 7:258-265.
18. Fairhead, C., B. Llorente, F. Denis, M. Soler, and B. Dujon. 1996. New vectors for combinatorial deletions in yeast chromosomes and for gap-repair cloning using "split-marker" recombination. Yeast 12:1439-1457.
19. Garfinkel, D. J. 1992. Retroelements in microorganisms, p. 107-158. In J. A. Levy (ed.), The Retrovindae 1, vol. 1. Plenum Press, New York, N.Y.
20. Grant, P. A., L. Duggan, J. Cote, S. M. Roberts, J. E. Brownell, R. Candau, R. Ohba, T. Owen-Hughes, C. D. Allis, F. Winston, S. L. Berger, and J. L. Workman. 1997. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 11:1640-1650.
21. Gray, W. M., and J. S. Fassler. 1996. Isolation and analysis of the yeast tea1 gene, which encodes a zinc cluster Ty enhancer-binding protein. Mol. Cell. Biol. 16:347-358.
22. Gray, W. M., and J. S. Fassler. 1993. Role of Saccharomyces cerevisiae Rap1 protein in Ty1 and Ty1-mediated transcription. Gene Expr. 3:237-251.
23. Guetsova, M. L., K. Lecoq, and B. Daignan-Fornier. 1997. The isolation and characterization of Saccharomyces cerevisiae mutants that constitutively express purine biosynthetic genes. Genetics 147:383-397.
24. Happel, A. M., M. S. Swanson, and F. Winston. 1991. The SNF2, SNF5 and SNF6 genes are required for Ty transcription in Saccharomyces cerevisiae. Genetics 128:69-77.
25. Hinnebusch, A. G., and K. Natarajan. 2002. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell. 1:22-32.
26. Hirschhorn, J. N., S. A. Brown, C. D. Clark, and F. Winston. 1992. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 6:2288-2298.
27. Kasahara, Y., Y. Nakai, D. Miura, H. Kanatani, K. Yagi, K. Hirabayashi, Y. Takahashi, and Y. Izawa. 1993. Decrease in deoxyribonucleotide triphosphate pools and induction of alkaline-labile sites in mouse bone marrow cells by multiple treatments with methotrexate. Mutat. Res. 319:143-149.
28. Kent, N. A., N. Karabetsou, P. K. Politis, and J. Mellor. 2001. In vivo chromatin remodeling by yeast ISWI homologs Isw1p and Isw2p. Genes Dev. 15:619-626.
29. Laloux, I., E. Dubois, M. Dewerchin, and E. Jacobs. 1990. TEC1, a gene involved in the activation of Ty1 and Ty1-mediated gene expression in Saccharomyces cerevisiae: cloning and molecular analysis. Mol. Cell. Biol. 10:3541-3550.
30. Laurent, B. C., I. Treich, and M. Carlson. 1993. The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. Genes Dev. 7:583-591.
31. Lesage, P., and A.-L. Todeschini. Happy together: the life and times of Ty retrotransposons and their hosts. Cytogenet. Genome Res., in press.
32. Madhani, H. D., and G. R. Fink. 1997. Combinatorial control required for the specificity of yeast MAPK signaling. Science 275:1314-1317.
33. Madison, J. M., A. M. Dudley, and F. Winston. 1998. Identification and analysis of Mot3, a zinc finger protein that binds to the retrotransposon Ty long terminal repeat (8) in Saccharomyces cerevisiae. Mol. Cell. Biol. 18: 1879-1890.
34. Maxwell, P. H., C. Coombes, A. E. Kenny, J. F. Lawler, J. D. Boeke, and M. J. Curcio. 2004. Ty1 mobilizes subtelomeric Y′ elements in telomerase-negative Saccharomyces cerevisiae survivors. Mol. Cell. Biol. 24:9887-9898.
35. McClanahan, T., and K. Mc Entee. 1984. Specific transcripts are elevated in Saccharomyces cerevisiae in response to DNA damage. Mol. Cell. Biol. 4:2356-2363.
36. Morillon, A., L. Bénard, M. Springer, and P. Lesage. 2002. Differential effect of chromatin and Gcn4 on the 50-fold range of expression among individual Yeast Ty1 retrotransposons. Mol. Cell. Biol. 22:2078-2088.
37. Morillon, A., M. Springer, and P. Lesage. 2000. Activation of the Kss1 invasive-filamentous growth pathway induces Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:5766-5776.
38. Morillon, A., M. Springer, and P. Lesage. 2001. Strains isogenic to S288C used in the yeast genome sequencing programme carry a functional KSS1 gene. Curr. Genet. 39:291-296.
39. Oliphant, A. R., C. J. Brandl, and K. Struhl. 1989. Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Mol. Cell. Biol. 9:2944-2949.
40. Pinson, B., T. L. Kongsrud, E. Ording, L. Johansen, B. Daignan-Fornier, and O. S. Gabrielsen. 2000. Signaling through regulated transcription factor interaction: mapping of a regulatory interaction domain in the Myb-related Bas1p. Nucleic Acids Res. 28:4665-4673.
41. Pinson, B., I. Sagot, F. Borne, O. S. Gabrielsen, and B. Daignan-Fornier. 1998. Mutations in the yeast Myb-like protein Bas1p resulting in discrimination between promoters in vivo but not in vitro. Nucleic Acids Res. 26: 3977-3985.
42. Pollard, K. J., and C. L. Peterson. 1997. Role for ADA/GCN5 products in antagonizing chromatin-mediated transcriptional repression. Mol. Cell. Biol. 17:6212-6222.
43. Rebora, K., C. Desmoucelles, F. Borne, B. Pinson, and B. Daignan-Fornier. 2001. Yeast AMP pathway genes respond to adenine through regulated synthesis of a metabolic intermediate. Mol. Cell. Biol. 21:7901-7912.
44. Rolfe, M., A. Spanos, and G. Banks. 1986. Induction of yeast Ty element transcription by ultraviolet. Nature 319:339-340.
45. Rolfes, R. J., and A. G. Hinnebusch. 1993. Translation of the yeast transcriptional activator GCN4 is stimulated by purine limitation: implications for activation of the protein kinase GCN2. Mol. Cell. Biol. 13:5099-5111.
46. 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.
47. Sacerdot, C., G. Mercier, A. Todeschini, M. Dutreix, M. Springer, and P. Lesage. 2005. Impact of ionizing radiation on the life cycle of Saccharomyces cerevisiae Ty1 retrotransposon. Yeast 22:441-455.
48. Sandmeyer, S. B., M. Aye, and T. Menees. 2002. Ty3, a position specific, Gypsy-like element in Saccharomyces cerevisiae, p. 663-683. In N. L. Craig, R. Craig, M. Gellert, and A. M. Lambowitz (ed.), Mobile DNA II. ASM Press, Washington, D.C.
49. Scholes, D. T., M. Banerjee, B. Bowen, and M. J. Curcio. 2001. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159:1449-1465.
50. Scholes, D. T., A. E. Kenny, E. R. Gamache, Z. Mou, and M. J. Curcio. 2003. Activation of a LTR-retrotransposon by telomere erosion. Proc. Natl. Acad. Sci. USA 100:15736-15741.
51. Shen, X., H. Xiao, R. Ranallo, W. H. Wu, and C. Wu. 2003. Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science 299:112-114.
52. 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.
53. Staleva Staleva, L., and P. Venkov. 2001. Activation of Ty transposition by mutagens. Mutat. Res. 474:93-103.
54. Steger, D. J., E. S. Haswell, A. L. Miller, S. R. Wente, and E. K. O'Shea. 2003. Regulation of chromatin remodeling by inositol polyphosphates. Science 299:114-116.
55. Tice-Baldwin, K., G. R. Fink, and K. T. Arndt. 1989. BAS1 has a Myb motif and activates HIS4 transcription only in combination with BAS2. Science 246:931-935.
56. Turkel, S., X. B. Liao, and P. J. Farabaugh. 1997. Gcr1-dependent transcriptional activation of yeast retrotransposon Ty2-917. Yeast 13:917-930.
57. Voytas, D. F., and J. D. Boeke. 2002. Ty1 and Ty5 of Saccharomyces cerevisiae, p. 631-662. In N. L. Craig, R. Craig, M. Gellert, and A. M. Lambowitz (ed.), Mobile DNA II. ASM Press, Washington, D.C.
58. Winston, F., C. Dollard, E. A. Malone, J. Clare, J. G. Kapakos, P. Farabaugh, and P. L. Minehart. 1987. Three genes are required for transactivation of Ty transcription in yeast. Genetics 115:649-656.
59. 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.
60. Zhang, F., M. Kirouac, N. Zhu, A. G. Hinnebusch, and R. J. Rolfes. 1997. Evidence that complex formation by Bas1p and Bas2p (Pho2p) unmasks the activation function of Bas1p in an adenine-repressible step of ADE gene transcription. Mol. Cell. Biol. 17:3272-3283.