Table of Contents
Advances in Biology
Volume 2016, Article ID 1840782, 6 pages
http://dx.doi.org/10.1155/2016/1840782
Research Article

Amino Acid Starvation Enhances Programmed Ribosomal Frameshift in Metavirus Ty3 of Saccharomyces cerevisiae

Department of Molecular Biology and Genetics, Faculty of Arts and Sciences, Uludag University, 16059 Bursa, Turkey

Received 16 April 2016; Accepted 14 June 2016

Academic Editor: Yoshito Abe

Copyright © 2016 Sezai Türkel. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. R. Cameron, E. Y. Loh, and R. W. Davis, “Evidence for transposition of dispersed repetitive DNA families in yeast,” Cell, vol. 16, no. 4, pp. 739–751, 1979. View at Publisher · View at Google Scholar · View at Scopus
  2. D. J. Clark, V. W. Bilanchone, L. J. Haywood, S. L. Dildine, and S. B. Sandmeyer, “A yeast sigma composite element, TY3, has properties of a retrotransposon,” The Journal of Biological Chemistry, vol. 263, no. 3, pp. 1413–1423, 1988. View at Google Scholar · View at Scopus
  3. P. Capy, “Classification and nomenclature of retrotransposable elements,” Cytogenetic and Genome Research, vol. 110, no. 1–4, pp. 457–461, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. D. Boeke, D. J. Garfinkel, C. A. Styles, and G. R. Fink, “Ty elements transpose through an RNA intermediate,” Cell, vol. 40, no. 3, pp. 491–500, 1985. View at Publisher · View at Google Scholar · View at Scopus
  5. P. J. Farabaugh, H. Zhao, and A. Vimaladithan, “A novel programed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast: frameshifting without tRNA slippage,” Cell, vol. 74, no. 1, pp. 93–103, 1993. View at Publisher · View at Google Scholar · View at Scopus
  6. P. J. Farabaugh, “Programmed translational frameshifting,” Microbiological Reviews, vol. 60, no. 1, pp. 103–134, 1996. View at Google Scholar · View at Scopus
  7. J.-F. Roth, “The yeast Ty virus-like particles,” Yeast, vol. 16, no. 9, pp. 785–795, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Türkel, Ö. Bayram, and E. Arik, “Glucose signaling pathway and growth conditions regulate gene expression in retrotransposon Ty2,” Zeitschrift fur Naturforschung—Section C, vol. 64, no. 7-8, pp. 526–532, 2009. View at Google Scholar · View at Scopus
  9. S. Türkel, G. Kaplan, and P. J. Farabaugh, “Glucose signalling pathway controls the programmed ribosomal frameshift efficiency in retroviral-like element Ty3 in Saccharomyces cerevisiae,” Yeast, vol. 28, no. 11, pp. 799–808, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. J. F. Atkins and G. R. Björk, “A gripping tale of ribosomal frameshifting: extragenic suppressors of frameshift mutations spotlight P-site realignment,” Microbiology and Molecular Biology Reviews, vol. 73, no. 1, pp. 178–210, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. A. G. Hinnebusch, “Mechanisms of gene regulation in the general control of amino acid biosynthesis in Saccharomyces cerevisiae,” Microbiological Reviews, vol. 52, no. 2, pp. 248–273, 1988. View at Google Scholar · View at Scopus
  12. R. C. Wek, M. Ramirez, B. M. Jackson, and A. G. Hinnebusch, “Identification of positive-acting domains in GCN2 protein kinase required for translational activation of GCN4 expression,” Molecular and Cellular Biology, vol. 10, no. 6, pp. 2820–2831, 1990. View at Publisher · View at Google Scholar · View at Scopus
  13. B. A. Castilho, R. Shanmugam, R. C. Silva, R. Ramesh, B. M. Himme, and E. Sattlegger, “Keeping the eIF2 alpha kinase Gcn2 in check,” Biochimica et Biophysica Acta (BBA)—Molecular Cell Research, vol. 1843, no. 9, pp. 1948–1968, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. C. R. Vazquez de Aldana, M. J. Marton, and A. G. Hinnebusch, “GCN20, a novel ATP binding cassette protein, and GCN1 reside in a complex that mediates activation of the elF-2α kinase GCN2 in amino acid-starved cells,” The EMBO Journal, vol. 14, no. 13, pp. 3184–3199, 1995. View at Google Scholar · View at Scopus
  15. M. J. Marton, C. R. Vazquez De Aldana, H. Qiu, K. Chakraburtty, and A. G. Hinnebusch, “Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2α kinase GCN2,” Molecular and Cellular Biology, vol. 17, no. 8, pp. 4474–4489, 1997. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Visweswaraiah, S. Lageix, B. A. Castilho et al., “Evidence that eukaryotic translation elongation factor 1A (eEF1A) binds the Gcn2 protein C terminus and inhibits Gcn2 activity,” The Journal of Biological Chemistry, vol. 286, no. 42, pp. 36568–36579, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Sattlegger and A. G. Hinnebusch, “Separate domains in GCN1 for binding protein kinase GCN2 and ribosomes are required for GCN2 activation in amino acid-starved cells,” The EMBO Journal, vol. 19, no. 23, pp. 6622–6633, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Visweswaraiah, S. J. Lee, A. G. Hinnebusch, and E. Sattlegger, “Overexpression of eukaryotic translation elongation factor 3 impairs Gcn2 protein activation,” The Journal of Biological Chemistry, vol. 287, pp. 37757–37768, 2012. View at Google Scholar
  19. M. F. Belcourt and P. J. Farabaugh, “Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site,” Cell, vol. 62, no. 2, pp. 339–352, 1990. View at Publisher · View at Google Scholar · View at Scopus
  20. R. D. Gietz and R. H. Schiestl, “Transforming yeast with DNA,” Methods in Molecular and Cellular Biology, vol. 5, no. 5, pp. 255–269, 1994. View at Google Scholar · View at Scopus
  21. X.-B. Liao, J. J. Clare, and P. J. Farabaugh, “The upstream activation site of a Ty2 element of yeast is necessary but not sufficient to promote maximal transcription of the element,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 23, pp. 8520–8524, 1987. View at Publisher · View at Google Scholar · View at Scopus
  22. M. D. Rose, F. Winston, and P. Hieter, Methods in Yeast Genetics. A Laboratory Course Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA, 1990.
  23. C. M. Moehle and A. G. Hinnebusch, “Association of RAP1 binding sites with stringent control of ribosomal protein gene transcription in Saccharomyces cerevisiae,” Molecular and Cellular Biology, vol. 11, no. 5, pp. 2723–2735, 1991. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Klopotowski and A. Wiater, “Synergism of aminotriazole and phosphate on the inhibition of yeast imidazole glycerol phosphate dehydratase,” Archives of Biochemistry and Biophysics, vol. 112, no. 3, pp. 562–566, 1965. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Guarente, “Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast,” Methods in Enzymology, vol. 101, pp. 181–191, 1983. View at Publisher · View at Google Scholar · View at Scopus
  26. O. H. Lowry, N. J. Rosebrough, A. L. Farr, and R. J. Randall, “Protein measurement with the folin phenol reagent,” The Journal of Biological Chemistry, vol. 193, no. 1, pp. 265–275, 1951. View at Google Scholar · View at Scopus
  27. K. Arndt and G. R. Fink, “GCN4 protein, a positive transcription factor in yeast, binds general control promoters at all 5′ TGACTC 3′ sequences,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 22, pp. 8516–8520, 1986. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Vimaladithan and P. J. Farabaugh, “Special peptidyl-tRNA molecules can promote translational frameshifting without slippage,” Molecular and Cellular Biology, vol. 14, no. 12, pp. 8107–8116, 1994. View at Publisher · View at Google Scholar · View at Scopus
  29. E. Sattlegger and A. G. Hinnebusch, “Polyribosome binding by GCN1 is required for full activation of eukaryotic translation initiation factor 2α kinase GCN2 during amino acid starvation,” The Journal of Biological Chemistry, vol. 280, no. 16, pp. 16514–16521, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. A. G. Hinnebusch and K. Natarajan, “Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress,” Eukaryotic Cell, vol. 1, no. 1, pp. 22–32, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. R. J. Rolfes and A. G. Hinnebusch, “Translation of the yeast transcriptional activator GCN4 is stimulated by purine limitation: implications for activation of the protein kinase GCN2,” Molecular and Cellular Biology, vol. 13, no. 8, pp. 5099–5111, 1993. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. J. Joo, J.-H. Kim, U.-B. Kang, M.-H. Yu, and J. Kim, “Gcn4p-mediated transcriptional repression of ribosomal protein genes under amino-acid starvation,” The EMBO Journal, vol. 30, no. 5, pp. 859–872, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. I. K. Jordan and J. F. McDonald, “Tempo and mode of Ty element evolution in Saccharomyces cerevisiae,” Genetics, vol. 151, no. 4, pp. 1341–1351, 1999. View at Google Scholar · View at Scopus
  34. H. Xu and J. D. Boeke, “Host genes that influence transposition in yeast: the abundance of a rare tRNA regulates Ty1 transposition frequency,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 21, pp. 8360–8364, 1990. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Kirchner, S. B. Sandmeyer, and D. B. Forrest, “Transposition of a Ty3 GAG3-POL3 fusion mutant is limited by availability of capsid protein,” Journal of Virology, vol. 66, no. 10, pp. 6081–6092, 1992. View at Google Scholar · View at Scopus