Hydrogen peroxide-induced oxidative stress upregulates ght5 gene belonging to hexose transporters in Schizosaccharomyces pombe

Umit Yasar Kına; Bedia Palabiyik

doi:10.14715/cmb/2019.65.1.7

Issue

Vol. 65 No. 1: Issue 1

Issue Published : February 4, 2019

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Hydrogen peroxide-induced oxidative stress upregulates ght5 gene belonging to hexose transporters in Schizosaccharomyces pombe

https://doi.org/10.14715/cmb/2019.65.1.7

Umit Yasar Kına

Department of Molecular Biology and Genetics, Institute of Life Sciences and Biotechnology, Bezmialem Vakıf University, ć°stanbul, Turkey

Bedia Palabiyik

Department of Molecular Biology and Genetics, Faculty of Science, Istanbul University, Istanbul, Turkey

Corresponding Author(s) : Bedia Palabiyik

bediag@istanbul.edu.tr

Cellular and Molecular Biology, Vol. 65 No. 1: Issue 1
Article Published : January 31, 2019

Abstract

Hydrogen peroxide is an agent that triggers oxidative stress. Glucose, which is a source of carbon and energy has a regulatory role in many metabolic processes such as growth rate, fermentation capacity and stress response. Schizosaccharomyces pombe has eight hexose transporters with a different affinity for glucose and/or related monosaccharides. In S. pombe, Ght5 is a glucose transporter with high-affinity. We aimed to investigate the effects of H2O2-induced oxidative stress on hexose transporters using glucose repression-resistant mutant strains (ird5 and ird11) of S. pombe. We analyzed the percentage of glucose consumption in S. pombe wild-type and mutant cells under stressed and non-stressed conditions. Then we compared the expression levels of the genes encoding hexose transporters under the same conditions. We confirmed that the glucose consumption efficiencies of the mutants were slower than the wild-type as in earlier study under non-stressed condition. The percentage of glucose consumption reduced by approximately two-fold in ird11 and wild-type, but not change in ird5, under a stressed condition. There is no difference between cells shape and size of S. pombe strains under stressed and non-stressed conditions. Under stress-induced condition, the expression levels of ght3, ght4 genes in ird11 and wild-type, and ght4, ght6 genes in ird5 decreased, but that of ght5 gene remarkably increased in only wild-type. We suggested that oxidative stress caused by H2O2 leads to upregulation of the ght5 gene in S. pombe.

Keywords

Oxidative stress Hexose transporters ght5 Schizosaccharomyces pombe Glucose repression.

Kına, U. Y., & Palabiyik, B. (2019). Hydrogen peroxide-induced oxidative stress upregulates ght5 gene belonging to hexose transporters in Schizosaccharomyces pombe. Cellular and Molecular Biology, 65(1), 41–45. https://doi.org/10.14715/cmb/2019.65.1.7

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References

Hoffman CS, Winston F. Glucose repression of transcription of the Schizosaccharomyces pombe fbp1 gene occurs by a cAMP signaling pathway. Genes Dev. 1991; 5:561-571.
Byrne SM, Hoffman CS. Six git genes encode a glucose-induced adenylate cyclase activation pathway in the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1993; 105:1095-1100.
Hoffman CS, Welton R. Mutagenesis and gene cloning in Schizosaccharomyces pombe using nonhomologous plasmid integration and rescue. Biotechniques. 2000; 28:532-536.
Hoffman CS. Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Trans. 2005; 33:257-260.
Soto T, Fernandez J, Cansado J, Vicente-Soler J. Protein kinase Sck1 is involved in trehalase activation by glucose and nitrogen source in the fission yeast Schizosaccharomyces pombe. Microbiology. 1997; 143:2457-2463.
Johnston M. Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet. 1999; 15:29-33.
Montecinos VP, Aguayo C, Flores C, Wyatt AW. Regulation of adenosine transport by D-glucose in human fetal endothelial cells: involvement of nitric oxide, protein kinase C and mitogen-activated protein kinase. J Physiol. 2000; 529:777-790.
Flores CL, Rodriguez C, Petit T, Gancedo C. Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev. 2000; 24:507-529.
Ikner A, Shiozaki K. Yeast signaling pathways in the oxidative stress response. Mutat Res. 2005; 569:13-27.
Quinn J, Findlay VJ, Dawson K, Millar JB. Distinct regulatory proteins control the graded transcriptional response to increasing H2O2 levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell. 2002; 13:805-816.
He Y, Chen Y, Song W, Zhu L. A Pap1-Oxs1 signaling pathway for disulfide stress in Schizosaccharomyces pombe. Nucleic Acids Res. 2017; 45:106-114.
Marger MD, Saier MH, Jr. A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci. 1993; 18:13-20.
Boles E, Hollenberg CP. The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev. 1997; 21:85-111.
Uldry M, Thorens B. The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch. 2004; 447:480-489.
Manolescu AR, Witkowska K, Kinnaird A, Cessford T. Facilitated hexose transporters: new perspectives on form and function. Physiology (Bethesda). 2007; 22:234-240.
Ozcan S, Johnston M. Function and regulation of yeast hexose transporters. Microbiol Mol Biol Rev. 1999; 63:554-569.
Heiland S, Radovanovic N, Hofer M, Winderickx J. Multiple hexose transporters of Schizosaccharomyces pombe. J Bacteriol. 2000; 182:2153-2162.
Saitoh S, Mori A, Uehara L, Masuda F. Mechanisms of expression and translocation of major fission yeast glucose transporters regulated by CaMKK/phosphatases, nuclear shuttling, and TOR. Molecular Biology of the Cell. 2014; 26:373-386.
Mata J, Wilbrey A, Bahler J. Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol. 2007; 8:R217.
Palabiyik B, Kig C, Pekmez M, Dalyan L. Investigation of the Relationship Between Oxidative Stress and Glucose Signaling in Schizosaccharomyces pombe. Biochemical Genetics. 2012; 50:336-349.
Palabiyik B, Jafari Ghods F, Onay Ucar E. Effects of glucose sensing/signaling on oxidative stress response in glucose repression mutants of Schizosaccharomyces pombe. Genetics and Molecular Research. 2013; 12:5046-5056.
Kig C, Turkel S, Temizkan G. Isolation and characterization of glucose derepressed invertase mutants from Schizosaccharomyces pombe. Bioscience, Biotechnology, and Biochemistry. 2005; 69:2475-2478.
Xue-Franzen Y, Kjaerulff S, Holmberg C, Wright A. Genomewide identification of pheromone-targeted transcription in fission yeast. BMC Genomics. 2006; 7:303.
Pfaffl MW. A new mathematical model for. Nucleic Acids Res. 2001; 29:e45.
Carlson M. Glucose repression in yeast. Curr Opin Microbiol 1999; 2:202-207.
Madrid M, Soto T, Franco A, Paredes V. A cooperative role for Atf1 and Pap1 in the detoxification of the oxidative stress induced by glucose deprivation in Schizosaccharomyces pombe. J Biol Chem. 2004; 279:41594-41602.
Maslanka R, Kwolek-Mirek M, Zadrag-Tecza R. Consequences of calorie restriction and calorie excess for the physiological parameters of the yeast Saccharomyces cerevisiae cells. FEMS Yeast Res 2017; 17.
Roux AE, Leroux A, Alaamery MA, Hoffman CS. Pro-aging effects of glucose signaling through a G protein-coupled glucose receptor in fission yeast. PLoS Genet. 2009; 5:e1000408.
Maslanka R, Renata Z-T, Kornelia K, Magdalena KM. The Effect of Berry Juices on the Level of Oxidative Stress in Yeast Cells Exposed to Acrylamide. Journal of Food Biochemistry. 2016; 40:686-695.
Chen D, Toone WM, Mata J, Lyne R. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell. 2003; 14:214-229.
Chen D, Wilkinson CR, Watt S, Penkett CJ. Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol Biol Cell. 2008; 19:308-317.

References

Hoffman CS, Winston F. Glucose repression of transcription of the Schizosaccharomyces pombe fbp1 gene occurs by a cAMP signaling pathway. Genes Dev. 1991; 5:561-571.

Byrne SM, Hoffman CS. Six git genes encode a glucose-induced adenylate cyclase activation pathway in the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1993; 105:1095-1100.

Hoffman CS, Welton R. Mutagenesis and gene cloning in Schizosaccharomyces pombe using nonhomologous plasmid integration and rescue. Biotechniques. 2000; 28:532-536.

Hoffman CS. Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Trans. 2005; 33:257-260.

Soto T, Fernandez J, Cansado J, Vicente-Soler J. Protein kinase Sck1 is involved in trehalase activation by glucose and nitrogen source in the fission yeast Schizosaccharomyces pombe. Microbiology. 1997; 143:2457-2463.

Johnston M. Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet. 1999; 15:29-33.

Montecinos VP, Aguayo C, Flores C, Wyatt AW. Regulation of adenosine transport by D-glucose in human fetal endothelial cells: involvement of nitric oxide, protein kinase C and mitogen-activated protein kinase. J Physiol. 2000; 529:777-790.

Flores CL, Rodriguez C, Petit T, Gancedo C. Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev. 2000; 24:507-529.

Ikner A, Shiozaki K. Yeast signaling pathways in the oxidative stress response. Mutat Res. 2005; 569:13-27.

Quinn J, Findlay VJ, Dawson K, Millar JB. Distinct regulatory proteins control the graded transcriptional response to increasing H2O2 levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell. 2002; 13:805-816.

He Y, Chen Y, Song W, Zhu L. A Pap1-Oxs1 signaling pathway for disulfide stress in Schizosaccharomyces pombe. Nucleic Acids Res. 2017; 45:106-114.

Marger MD, Saier MH, Jr. A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci. 1993; 18:13-20.

Boles E, Hollenberg CP. The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev. 1997; 21:85-111.

Uldry M, Thorens B. The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch. 2004; 447:480-489.

Manolescu AR, Witkowska K, Kinnaird A, Cessford T. Facilitated hexose transporters: new perspectives on form and function. Physiology (Bethesda). 2007; 22:234-240.

Ozcan S, Johnston M. Function and regulation of yeast hexose transporters. Microbiol Mol Biol Rev. 1999; 63:554-569.

Heiland S, Radovanovic N, Hofer M, Winderickx J. Multiple hexose transporters of Schizosaccharomyces pombe. J Bacteriol. 2000; 182:2153-2162.

Saitoh S, Mori A, Uehara L, Masuda F. Mechanisms of expression and translocation of major fission yeast glucose transporters regulated by CaMKK/phosphatases, nuclear shuttling, and TOR. Molecular Biology of the Cell. 2014; 26:373-386.

Mata J, Wilbrey A, Bahler J. Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol. 2007; 8:R217.

Palabiyik B, Kig C, Pekmez M, Dalyan L. Investigation of the Relationship Between Oxidative Stress and Glucose Signaling in Schizosaccharomyces pombe. Biochemical Genetics. 2012; 50:336-349.

Palabiyik B, Jafari Ghods F, Onay Ucar E. Effects of glucose sensing/signaling on oxidative stress response in glucose repression mutants of Schizosaccharomyces pombe. Genetics and Molecular Research. 2013; 12:5046-5056.

Kig C, Turkel S, Temizkan G. Isolation and characterization of glucose derepressed invertase mutants from Schizosaccharomyces pombe. Bioscience, Biotechnology, and Biochemistry. 2005; 69:2475-2478.

Xue-Franzen Y, Kjaerulff S, Holmberg C, Wright A. Genomewide identification of pheromone-targeted transcription in fission yeast. BMC Genomics. 2006; 7:303.

Pfaffl MW. A new mathematical model for. Nucleic Acids Res. 2001; 29:e45.

Carlson M. Glucose repression in yeast. Curr Opin Microbiol 1999; 2:202-207.

Madrid M, Soto T, Franco A, Paredes V. A cooperative role for Atf1 and Pap1 in the detoxification of the oxidative stress induced by glucose deprivation in Schizosaccharomyces pombe. J Biol Chem. 2004; 279:41594-41602.

Maslanka R, Kwolek-Mirek M, Zadrag-Tecza R. Consequences of calorie restriction and calorie excess for the physiological parameters of the yeast Saccharomyces cerevisiae cells. FEMS Yeast Res 2017; 17.

Roux AE, Leroux A, Alaamery MA, Hoffman CS. Pro-aging effects of glucose signaling through a G protein-coupled glucose receptor in fission yeast. PLoS Genet. 2009; 5:e1000408.

Maslanka R, Renata Z-T, Kornelia K, Magdalena KM. The Effect of Berry Juices on the Level of Oxidative Stress in Yeast Cells Exposed to Acrylamide. Journal of Food Biochemistry. 2016; 40:686-695.

Chen D, Toone WM, Mata J, Lyne R. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell. 2003; 14:214-229.

Chen D, Wilkinson CR, Watt S, Penkett CJ. Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol Biol Cell. 2008; 19:308-317.