Research Article
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Investigation of the Effects of Autophagy Signaling on the Transcription of Yeast Retrotransposon Ty2-917

Year 2021, Volume: 80 Issue: 2, 107 - 118, 17.12.2021
https://doi.org/10.26650/EurJBiol.2021.1011143

Abstract

Objective: Ty2-917 is a low copy retrotransposon found in the Saccharomyces cerevisiae genome. It has structural similarities to metazoan retroviruses in terms of genome organization and propagation mechanisms in the host cells. The objective of this study is to analyze the effects of autophagy signaling on the transcriptional regulation of Ty2 in yeast cells.

Materials and Methods: Ty2-LacZ gene fusions on the YEp vectors have been used as reporter genes to analyze the effects of amino acid starvation, nitrogen source, and autophagy signals on the transcription of Ty2. These reporter gene fusions have been transformed into the wild type and also isogenic mutant yeast strains that are defective for one of the regulatory factors involved in nutrient sensing and signaling. To activate autophagy signaling, yeast transformants were treated with caffeine or 3-amino 1-2-3 triazole. Transcription levels of Ty2-LacZ gene fusions in treated and untreated yeast cells were analyzed by β-galactosidase assays. Results:

Results of this study show that transcription of Ty2 decreases up to eightfold in response to amino acid starvation. Caffeine treatment of the yeast cells also represses Ty2 transcription, independent of the TOR1 pathway. In addition, our results suggest that Ty2 transcription is also regulated in a nitrogen source-dependent manner through the GATA factors.

Conclusions: Our results suggest that activation of autophagy signal results in significant level repression of Ty2 transcription. We have found that the GATA class of transcription factors is involved in the regulation of Ty2 transcription in response to autophagy signaling.

Thanks

Acknowledgment: Part of the data in this manuscript was taken from Ph.D. thesis research of S. Türkel completed at the University of Maryland Baltimore County, Department of Biological Sciences under the supervision of Prof.Dr. P. J. Farabaugh. I am thankful to him for his supervision for my thesis research.

References

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  • 2. Boeke J, Garfinkel DJ, Styles CA, Fink G. Ty elements transpose through an RNA intermediate. Cell 1985; 40: 491-500. google scholar
  • 3. Curcio MJ, Lutz S, Lesage P. The Ty1 LTR-retrotransposon of bud-ding yeast, Saccharomyces cerevisiae. Microbiol Spectr 2015; 3: 1-35. google scholar
  • 4. Capy P. Classification and nomenclature of retrotransposable ele-ments. Cytogenet Genome Res 2005; 110: 457-61. google scholar
  • 5. Roeder GS, Farabaugh PJ, Chalef DT, Fink GR. The origin of gene instability in yeast. Science 1980; 209: 1375-80. google scholar
  • 6. Garfinkel DJ, Tucker JM, Saha A, Nishida Y, Pachulska-Wieczorek K, Btaszczyk L, et al. A self-encoded capsid derivative restricts Ty1 ret-rotransposition in Saccharomyces. Curr Genet 2016; 62: 321-9. google scholar
  • 7. Saha A, Mitchell JA, Nishida Y, Hildreth JE, Ariberre JA, Gilbert WV, et al. A trans-dominant form of Gag restricts Ty1 retrotransposition and mediates copy number control. J Virol 2015; 89: 3922-38. google scholar
  • 8. Curcio MJ, Hedge AM, Boeke JD, Garfinkel DJ. 1990. Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Mol Gen Genet 1990; 220: 213-21. google scholar
  • 9. Belcourt MF, Farabaugh PJ. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell 1990; 62: 339-52. google scholar
  • 10. Farabaugh PJ. Programmed translational frameshifting. Microbiol Rev 1996; 60: 103-134. google scholar
  • 11. Farabaugh PJ, XB. Liao, Belcourt M, Zhao H, Kapakos J, Clare J. En-hancer and silencer-like sites within the transcribed portion of a Ty2 transposable element of S. cerevisiae. Mol Cell Biol 1989; 9: 4824-34. google scholar
  • 12. Farabaugh PJ, Vimaladithan A, Türkel S, Johnson R, Zhao H. Three downstream sites repress transcription of a Ty2 retrotransposon in Saccharomyces cerevisiae. Mol Cell Biol 1993; 13: 2081-90. google scholar
  • 13. Türkel S, Farabaugh PJ. Interspersion of an unusual GCN4 activa-tion site with a complex transcriptional repression site in Ty ele-ments of Saccharomyces cerevisiae. Mol Cell Biol 1993; 13: 2091103. google scholar
  • 14. Laloux I, Dubois E ,Dewerchin M, Jacobs E. TEC1, a gene involved in the activation of Tyl and Tyl-mediated gene expression in Saccha-romyces cerevisiae: Cloning and molecular analysis. Mol Cell Biol 1990; 10: 3541-50. google scholar
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  • 26. Wen X, Klionsky DJ. An overview of macroautophagy in yeast. J Mol Biol 2016; 428: 1681-99. google scholar
  • 27. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 2000; 150: 1507-13. google scholar
  • 28. Yoshiaki Kamada Y, Yoshino K-İ, Kondo C, Kawamata T, Oshiro N, Yonezawa K, et al. Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Biol 2010; 30: 1049-58. google scholar
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  • 30. Cooper TG. Transmitting the signal of excess nitrogen in Saccha-romyces cerevisiae from the Tor proteins to the GATA factors: con-necting the dots. FEMS Microbiol Rev 2002; 26: 223-38. google scholar
  • 31. Ruta LL, Farcasanu IC. Saccharomyces cerevisiae and caffeine implications on the eukaryotic cell. Nutrients 2020; 12: 2440; doi:10.3390/nu12082440. google scholar
  • 32. Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cecconi F, et al. Molecular definitions of autophagy and related processes. EMBO J 2017; 13: 1811-36. google scholar
  • 33. Scott SV, Guan J, Hutchins MU, Kim J, Klionsky DJ. Cvt19 is a re-ceptor for the Cytoplasm-to-Vacuole targeting pathway. Mol Cell 2001; 7: 1131-41. google scholar
  • 34. Choi Y, Bowman JW, Jung JU. Autophagy during viral infection— a double-edged sword. Nat Rev Microbiol 2018; 16: 341-54. google scholar
  • 35. Campbell GR, Spector SA. Induction of autophagy to achieve a hu-man immunodeficiency virus type 1 cure. Cells 2021; 10: 1798. doi. org/10.3390/cells10071798. google scholar
  • 36. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998; 14: 115-32. google scholar
  • 37. Scherens B, Feller A, Vierendeels F, Messenguy F, Dubois E. Identifi-cation of direct and indirect targets of the Gln3 and Gat1 activators by transcriptional profiling in response to nitrogen availability in the short and long term. FEMS Yeast Research 2006; 6: 777-91. google scholar
  • 38. Nagawa F, Fink GR. 1985. The relationship between the “TATA” se-quence and transcription initiation sites at the HIS4 gene of Sac-charomyces cerevisiae. Proc Natl Acad Sci (USA) 1985; 82: 8557-61. google scholar
  • 39. Arndt KT, Styles C, Fink GR. Multiple global regulators control HIS4 transcription in Yeast. Science 1987; 237: 874-80. google scholar
  • 40. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 1992; 110: 119-22. google scholar
  • 41. Gietz R., Schiestl R. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2007; 2: 31-4. google scholar
  • 42. Kuranda K, Leberre V, Sokol S, Palamarczyk G, Francois J. Investi-gating the caffeine effects in the yeast Saccharomyces cerevisiae brings new insights into the connection between TOR, PKC and Ras/cAMP signalling pathways. Molecular Microbiol 2006; 61: 1147-66. google scholar
  • 43. Guarente L, Patashe M. Fusion of Escherichia coli lacZ to the cy-tochrome c gene of Saccharomyces cerevisiae. Proc Natl Acad Sci (USA) 1981; 78: 2199-203. google scholar
  • 44. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measure-ment with the Folin phenol reagent. J Biol Chem 1951; 193: 265-75. google scholar
  • 45. Schmelzle T, Hall MN. TOR, a central controller of cell growth. Cell 2000; 103: 253-262. google scholar
  • 46. Coccetti P, Nicastro R, Tripodi F. Conventional and emerging roles of the energy sensor Snf1/AMPK in Saccharomyces cerevisiae. Mi-crob Cell 2018; 5: 482-94. google scholar
  • 47. Georis I, A. Feller A, Tate JJ, Cooper TG, Dubois E. Nitrogen catabo-lite repression-sensitive transcription as a readout of Tor pathway regulation: the genetic background, reporter gene and GATA fac-tor assayed determine the outcomes. Genetics 2009; 181: 861-74. google scholar
  • 48. Sasaki H, Kishimoto T, Mizuno T, Shinzato T, Uemura H. Expression of GCR1, the transcriptional activator of glycolytic enzyme genes in the yeast Saccharomyces cerevisiae, is positively autoregulated by Gcr1p. Yeast 2005; 22: 305-19. google scholar
  • 49. Barbara KE, Haley TM, Willis KA, Santangelo GM. The transcription factor Gcr1 stimulates cell growth by participating in nutrient-re-sponsive gene expression on a global level. Mol Genet Genomics 2007; 277: 171-88. google scholar
  • 50. Gonzalez A, Hall MN. Nutrient sensing and TOR signaling in yeast and mammals. EMBO J 2017; 36: 397-408. google scholar
  • 51. Türkel S, Bayram Ö, Arık E. Glucose signaling pathway and growth conditions regulate gene expression in retrotransposon Ty2. Z. Naturforsch 2009; 64 c: 526-32. google scholar
  • 52. Szijgyarto Z, Garedew A, Azevedo C, Saiardi A. Influence of inositol pyrophosphates on cellular energy dynamics. Science 2011; 334: 802-5. google scholar
  • 53. Morrissette VA, Rolfes RJ. The intersection between stress respons-es and inositol pyrophosphates in Saccharomyces cerevisiae. Curr Genet 2020; 66: 901-10. google scholar
  • 54. Nagata E, Saiardi A, Tsukamoto H, Satoh T, Itoh Y, Itoh J, et al. Ino-sitol hexakisphosphate kinases promote autophagy. Int J Biochem Cell Biol 2010; 42: 2065-71. google scholar
  • 55. Ronsmans A, Wery M, Szachnowski U, Gautier C, Descrimes M, Du-bois E, et al. Transcription-dependent spreading of the Dal80 yeast GATA factor across the body of highly expressed genes. PLoS Gen-et 2019; 15: e1007999. doi.org/10.1371/journal.pgen.1007999. google scholar
  • 56. Coffman JA, Rai R, Loprete DM, Cunningham T, Svetlov V, Cooper TG. Cross regulation of four GATA factors that control nitrogen catabolic gene expression in Saccharomyces cerevisiae. J Bacteriol 1997; 179: 3416-29. google scholar
  • 57. Lopez MC, Baker HV. Understanding the growth phenotype of the yeast gcr1 mutant in terms of global genomic expression patterns. J Bacteriol 2000; 182: 4970-8. google scholar
Year 2021, Volume: 80 Issue: 2, 107 - 118, 17.12.2021
https://doi.org/10.26650/EurJBiol.2021.1011143

Abstract

References

  • 1. Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF. Transposable Elements and Genome Organization: A Comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevi-siae genome sequence. Genome Res 1998; 8: 464-78. google scholar
  • 2. Boeke J, Garfinkel DJ, Styles CA, Fink G. Ty elements transpose through an RNA intermediate. Cell 1985; 40: 491-500. google scholar
  • 3. Curcio MJ, Lutz S, Lesage P. The Ty1 LTR-retrotransposon of bud-ding yeast, Saccharomyces cerevisiae. Microbiol Spectr 2015; 3: 1-35. google scholar
  • 4. Capy P. Classification and nomenclature of retrotransposable ele-ments. Cytogenet Genome Res 2005; 110: 457-61. google scholar
  • 5. Roeder GS, Farabaugh PJ, Chalef DT, Fink GR. The origin of gene instability in yeast. Science 1980; 209: 1375-80. google scholar
  • 6. Garfinkel DJ, Tucker JM, Saha A, Nishida Y, Pachulska-Wieczorek K, Btaszczyk L, et al. A self-encoded capsid derivative restricts Ty1 ret-rotransposition in Saccharomyces. Curr Genet 2016; 62: 321-9. google scholar
  • 7. Saha A, Mitchell JA, Nishida Y, Hildreth JE, Ariberre JA, Gilbert WV, et al. A trans-dominant form of Gag restricts Ty1 retrotransposition and mediates copy number control. J Virol 2015; 89: 3922-38. google scholar
  • 8. Curcio MJ, Hedge AM, Boeke JD, Garfinkel DJ. 1990. Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Mol Gen Genet 1990; 220: 213-21. google scholar
  • 9. Belcourt MF, Farabaugh PJ. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell 1990; 62: 339-52. google scholar
  • 10. Farabaugh PJ. Programmed translational frameshifting. Microbiol Rev 1996; 60: 103-134. google scholar
  • 11. Farabaugh PJ, XB. Liao, Belcourt M, Zhao H, Kapakos J, Clare J. En-hancer and silencer-like sites within the transcribed portion of a Ty2 transposable element of S. cerevisiae. Mol Cell Biol 1989; 9: 4824-34. google scholar
  • 12. Farabaugh PJ, Vimaladithan A, Türkel S, Johnson R, Zhao H. Three downstream sites repress transcription of a Ty2 retrotransposon in Saccharomyces cerevisiae. Mol Cell Biol 1993; 13: 2081-90. google scholar
  • 13. Türkel S, Farabaugh PJ. Interspersion of an unusual GCN4 activa-tion site with a complex transcriptional repression site in Ty ele-ments of Saccharomyces cerevisiae. Mol Cell Biol 1993; 13: 2091103. google scholar
  • 14. Laloux I, Dubois E ,Dewerchin M, Jacobs E. TEC1, a gene involved in the activation of Tyl and Tyl-mediated gene expression in Saccha-romyces cerevisiae: Cloning and molecular analysis. Mol Cell Biol 1990; 10: 3541-50. google scholar
  • 15. Löhning C, Ciriacy M. The TYE7 gene of Saccharomyces cerevisi-ae encodes a putative bHLH-LZ transcription factor required for Ty1-mediated gene expression. Yeast 1994; 10: 1329-39. google scholar
  • 16. Türkel S, Yenice B. Analysis of the effects of chromatin modifying complexes on the transcription of retrotransposon Ty2-917 in Sac-charomyces cerevisiae. Turk J Biol 2006; 30: 101-6. google scholar
  • 17. Türkel S, Liao XB, Farabaugh PJ. Gcr1-dependent transcriptional activation of yeast retrotransposon Ty2-917. Yeast 1997; 13: 91730. google scholar
  • 18. Cha S, Hong CP, Kang HA, Hahn J-S. Differential activation mecha-nisms of two isoforms of Gcr1 transcription factor generated from spliced and un-spliced transcripts in Saccharomyces cerevisiae. Nu-cleic Acids Res 2021; 49: 745-59. google scholar
  • 19. Hossain MA, Claggett JM, Edwards S, Shi A, Pennebaker S, Cheng M, et al. Post-transcriptional regulation of Gcr1 expression and ac-tivity are crucial for metabolic adjustment in response to glucose availability. Mol Cell 2016; 62: 346-58. google scholar
  • 20. Suzuki K, Morimoto M, Kondo C, Ohsumi Y. Selective autophagy regulates insertional mutagenesis by the Ty1 retrotransposon in Saccharomyces cerevisiae. Developmental Cell 2011; 21: 358-65. google scholar
  • 21. Çolakoğlu C, Türkel S. Apoptosis signaling pathway regulates the gene expression in the yeast retrotransposons Ty1 and Ty2. Eur J Biology 2020; 79: 36-42. google scholar
  • 22. Ohsumi Y. Historical landmarks of autophagy research. Cell Re-search 2014; 24: 9-23. google scholar
  • 23. Suzuki K, Ohsumi Y. Molecular machinery of autophagosome forma-tion in yeast, Saccharomyces cerevisiae. 2007; FEBS Lett 581: 2156-61. google scholar
  • 24. Yin Z, Pascual C, Klionsky DJ. Autophagy: machinery and regula-tion. Microb Cell 2016; 3: 588-96. google scholar
  • 25. Delorme-Axford E, Daniel J. Klionsky DJ. Transcriptional and post-transcriptional regulation of autophagy in the yeast Saccha-romyces cerevisiae. J Biol Chem 2018; 293: 5396-403. google scholar
  • 26. Wen X, Klionsky DJ. An overview of macroautophagy in yeast. J Mol Biol 2016; 428: 1681-99. google scholar
  • 27. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 2000; 150: 1507-13. google scholar
  • 28. Yoshiaki Kamada Y, Yoshino K-İ, Kondo C, Kawamata T, Oshiro N, Yonezawa K, et al. Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Biol 2010; 30: 1049-58. google scholar
  • 29. Hinnebusch, AG, Natarajan K. 2002. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryotic Cell 2002; 1: 22-32. google scholar
  • 30. Cooper TG. Transmitting the signal of excess nitrogen in Saccha-romyces cerevisiae from the Tor proteins to the GATA factors: con-necting the dots. FEMS Microbiol Rev 2002; 26: 223-38. google scholar
  • 31. Ruta LL, Farcasanu IC. Saccharomyces cerevisiae and caffeine implications on the eukaryotic cell. Nutrients 2020; 12: 2440; doi:10.3390/nu12082440. google scholar
  • 32. Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cecconi F, et al. Molecular definitions of autophagy and related processes. EMBO J 2017; 13: 1811-36. google scholar
  • 33. Scott SV, Guan J, Hutchins MU, Kim J, Klionsky DJ. Cvt19 is a re-ceptor for the Cytoplasm-to-Vacuole targeting pathway. Mol Cell 2001; 7: 1131-41. google scholar
  • 34. Choi Y, Bowman JW, Jung JU. Autophagy during viral infection— a double-edged sword. Nat Rev Microbiol 2018; 16: 341-54. google scholar
  • 35. Campbell GR, Spector SA. Induction of autophagy to achieve a hu-man immunodeficiency virus type 1 cure. Cells 2021; 10: 1798. doi. org/10.3390/cells10071798. google scholar
  • 36. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998; 14: 115-32. google scholar
  • 37. Scherens B, Feller A, Vierendeels F, Messenguy F, Dubois E. Identifi-cation of direct and indirect targets of the Gln3 and Gat1 activators by transcriptional profiling in response to nitrogen availability in the short and long term. FEMS Yeast Research 2006; 6: 777-91. google scholar
  • 38. Nagawa F, Fink GR. 1985. The relationship between the “TATA” se-quence and transcription initiation sites at the HIS4 gene of Sac-charomyces cerevisiae. Proc Natl Acad Sci (USA) 1985; 82: 8557-61. google scholar
  • 39. Arndt KT, Styles C, Fink GR. Multiple global regulators control HIS4 transcription in Yeast. Science 1987; 237: 874-80. google scholar
  • 40. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 1992; 110: 119-22. google scholar
  • 41. Gietz R., Schiestl R. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2007; 2: 31-4. google scholar
  • 42. Kuranda K, Leberre V, Sokol S, Palamarczyk G, Francois J. Investi-gating the caffeine effects in the yeast Saccharomyces cerevisiae brings new insights into the connection between TOR, PKC and Ras/cAMP signalling pathways. Molecular Microbiol 2006; 61: 1147-66. google scholar
  • 43. Guarente L, Patashe M. Fusion of Escherichia coli lacZ to the cy-tochrome c gene of Saccharomyces cerevisiae. Proc Natl Acad Sci (USA) 1981; 78: 2199-203. google scholar
  • 44. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measure-ment with the Folin phenol reagent. J Biol Chem 1951; 193: 265-75. google scholar
  • 45. Schmelzle T, Hall MN. TOR, a central controller of cell growth. Cell 2000; 103: 253-262. google scholar
  • 46. Coccetti P, Nicastro R, Tripodi F. Conventional and emerging roles of the energy sensor Snf1/AMPK in Saccharomyces cerevisiae. Mi-crob Cell 2018; 5: 482-94. google scholar
  • 47. Georis I, A. Feller A, Tate JJ, Cooper TG, Dubois E. Nitrogen catabo-lite repression-sensitive transcription as a readout of Tor pathway regulation: the genetic background, reporter gene and GATA fac-tor assayed determine the outcomes. Genetics 2009; 181: 861-74. google scholar
  • 48. Sasaki H, Kishimoto T, Mizuno T, Shinzato T, Uemura H. Expression of GCR1, the transcriptional activator of glycolytic enzyme genes in the yeast Saccharomyces cerevisiae, is positively autoregulated by Gcr1p. Yeast 2005; 22: 305-19. google scholar
  • 49. Barbara KE, Haley TM, Willis KA, Santangelo GM. The transcription factor Gcr1 stimulates cell growth by participating in nutrient-re-sponsive gene expression on a global level. Mol Genet Genomics 2007; 277: 171-88. google scholar
  • 50. Gonzalez A, Hall MN. Nutrient sensing and TOR signaling in yeast and mammals. EMBO J 2017; 36: 397-408. google scholar
  • 51. Türkel S, Bayram Ö, Arık E. Glucose signaling pathway and growth conditions regulate gene expression in retrotransposon Ty2. Z. Naturforsch 2009; 64 c: 526-32. google scholar
  • 52. Szijgyarto Z, Garedew A, Azevedo C, Saiardi A. Influence of inositol pyrophosphates on cellular energy dynamics. Science 2011; 334: 802-5. google scholar
  • 53. Morrissette VA, Rolfes RJ. The intersection between stress respons-es and inositol pyrophosphates in Saccharomyces cerevisiae. Curr Genet 2020; 66: 901-10. google scholar
  • 54. Nagata E, Saiardi A, Tsukamoto H, Satoh T, Itoh Y, Itoh J, et al. Ino-sitol hexakisphosphate kinases promote autophagy. Int J Biochem Cell Biol 2010; 42: 2065-71. google scholar
  • 55. Ronsmans A, Wery M, Szachnowski U, Gautier C, Descrimes M, Du-bois E, et al. Transcription-dependent spreading of the Dal80 yeast GATA factor across the body of highly expressed genes. PLoS Gen-et 2019; 15: e1007999. doi.org/10.1371/journal.pgen.1007999. google scholar
  • 56. Coffman JA, Rai R, Loprete DM, Cunningham T, Svetlov V, Cooper TG. Cross regulation of four GATA factors that control nitrogen catabolic gene expression in Saccharomyces cerevisiae. J Bacteriol 1997; 179: 3416-29. google scholar
  • 57. Lopez MC, Baker HV. Understanding the growth phenotype of the yeast gcr1 mutant in terms of global genomic expression patterns. J Bacteriol 2000; 182: 4970-8. google scholar
There are 57 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Sezai Türkel 0000-0001-7128-6948

Ceyda Çolakoğlu 0000-0002-7471-5071

Tuğçe Karaduman This is me 0000-0003-0479-0559

Publication Date December 17, 2021
Submission Date October 17, 2021
Published in Issue Year 2021 Volume: 80 Issue: 2

Cite

AMA Türkel S, Çolakoğlu C, Karaduman T. Investigation of the Effects of Autophagy Signaling on the Transcription of Yeast Retrotransposon Ty2-917. Eur J Biol. December 2021;80(2):107-118. doi:10.26650/EurJBiol.2021.1011143