Thiamine leads to oxidative stress resistance via regulation of the glucose metabolism

Burcu Kartal; Bedia Palabiyik

doi:10.14715/cmb/2019.65.1.13

Issue

Vol. 65 No. 1: Issue 1

Issue Published : February 4, 2019

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Thiamine leads to oxidative stress resistance via regulation of the glucose metabolism

https://doi.org/10.14715/cmb/2019.65.1.13

Burcu Kartal

Department of Molecular Biology and Genetics, Institute of Graduate Studies in Sciences, Istanbul University, 34116, Istanbul, Turkey

Bedia Palabiyik

Department of Molecular Biology and Genetics, Faculty of Science, Istanbul University, 34134, Istanbul, Turkey

Corresponding Author(s) : Burcu Kartal

burcu.kartal@istanbul.edu.tr

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

Abstract

Thiamine diphosphate (ThDP) is an essential cofactor for important enzymes in carbohydrate, amino acid and lipid metabolisms. It is also known that thiamine plays an important role in stress response of some organisms. In this study, we focused on the effect of thiamine on stress responses triggered by various stress agents. For this purpose, firstly, viability of Schizosaccharomyces pombe cell cultures was examined under oxidative, osmotic and heat stresses. The highest tolerance observed in cell viability due to the presence of extracellular thiamine (1.5 µM) was found only against oxidative stress. Then, enzyme activity of catalase and superoxide dismutase (SOD) involved in antioxidant defense mechanism and the expression analysis of genes encoding enzymes related to glucose metabolism and stress response pathways were investigated under oxidative stress. In this condition, it was not observed any difference in SOD and catalase activities, and their gene expressions due to the presence of thiamine, whereas the upregulation of pyruvate dehydrogenase (pdb1), transketolase (SPBC2G5.05), fructose-1,6-bis-phosphatase (fbp1) and the downregulation of pyruvate decarboxylase (pdc201) were observed. In conclusion, these findings suggest that extracellular thiamine leading to oxidative stress resistance have an impact on the regulation of glucose metabolism by shifting the energy generation from fermentation to respiration.

Keywords

Schizosaccharomyces pombe Thiamine Stress response Glucose metabolism Oxidative stress.

Kartal, B., & Palabiyik, B. (2019). Thiamine leads to oxidative stress resistance via regulation of the glucose metabolism. Cellular and Molecular Biology, 65(1), 73–77. https://doi.org/10.14715/cmb/2019.65.1.13

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References

Rindi G, Laforenza U. Thiamine intestinal transport and related issues: recent aspects. Proc Soc Exp Biol Med Sep 2000; 224(4): 246-255.
Gangolf M, Czerniecki J, Radermecker M et al. Thiamine status in humans and content of phosphorylated thiamine derivatives in biopsies and cultured cells. PLoS One Oct 25 2010; 5(10): e13616.
Friedrich W. Thiamin (Vitamin B1, aneurin). Hanbuch der Vitamine. Munich: Urban & Schwarzenberg; 1987: 240-258.
Flores CL, Rodriguez C, Petit T, Gancedo C. Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev Oct 2000; 24(4): 507-529.
Walker G. Yeast physiology and biotechnology. UK: John Wiley & Sons 1998.
Wood V, Harris MA, McDowall MD et al. PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res Jan 2012; 40(Database issue): D695-699.
Chen D, Toone WM, Mata J et al. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell Jan 2003; 14(1): 214-229.
Khlebodarova TM. [How cells protect themselves against stress?]. Genetika Apr 2002; 38(4): 437-452.
Jung IL, Kim IG. Thiamine protects against paraquat-induced damage: scavenging activity of reactive oxygen species. Environ Toxicol Pharmacol Dec 2003; 15(1): 19-26.
Rapala-Kozik M, Wolak N, Kujda M, Banas AK. The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response. BMC Plant Biol Jan 3 2012; 12: 2.
Tunc-Ozdemir M, Miller G, Song L et al. Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol Sep 2009; 151(1): 421-432.
Wolak N, Kowalska E, Kozik A, Rapala-Kozik M. Thiamine increases the resistance of baker's yeast Saccharomyces cerevisiae against oxidative, osmotic and thermal stress, through mechanisms partly independent of thiamine diphosphate-bound enzymes. FEMS Yeast Res Dec 2014; 14(8): 1249-1262.
Depeint F, Bruce WR, Shangari N, Mehta R, O'Brien PJ. Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem Biol Interact Oct 27 2006; 163(1-2): 94-112.
Palabiyik B, Ghods FJ, Ucar EO. A potential protective role for thiamine in glucose-driven oxidative stress. Genet Mol Res 2014; 13(3): 5582-5593.
Gutz H, Heslot H, Leupold U, Loprieno N. Schizosaccharomyces pombe. In: King RC, ed. Handbook of Genetics. New York: Plenum Press; 1974: 395–446.
Waterborg JH. The protein protocols handbook. New York: Humana Press; 2002.
Cho YWP, E. H. Lim, C. J. Catalase, glutathione S-transferase and thioltransferase respond differently to oxidative stress in Schizosaccharomyces pombe. J Biochem Mol Biol 2000; 33: 344-348.
Cakmak I, Marschner H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol Apr 1992; 98(4): 1222-1227.
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res May 1 2001; 29(9): e45.
Palabiyik B, Kig C, Pekmez M, Dalyan L, Arda N, Temizkan G. Investigation of the relationship between oxidative stress and glucose signaling in Schizosaccharomyces pombe. Biochem Genet Jun 2012; 50(5-6): 336-349.
Gioda CR, de Oliveira Barreto T, Primola-Gomes TN et al. Cardiac oxidative stress is involved in heart failure induced by thiamine deprivation in rats. Am J Physiol Heart Circ Physiol Jun 2010; 298(6): H2039-2045.
Nagae M, Parniske M, Kawaguchi M, Takeda N. The Thiamine Biosynthesis Gene THI1 Promotes Nodule Growth and Seed Maturation. Plant Physiol Nov 2016; 172(3): 2033-2043.
Li R, Xiong G, Yuan S, Wu Z, Miao Y, Weng P. Investigating the underlying mechanism of Saccharomyces cerevisiae in response to ethanol stress employing RNA-seq analysis. World J Microbiol Biotechnol Nov 3 2017; 33(11): 206.
Kartal B, Akcay A, Palabıyık B. Oxidative Stress Upregulates the Transcription of Genes Involved in Thiamine Metabolism. Turkish J Biol 2018; 42(5): 447-452.
Hoffman CS, Winston F. Isolation and characterization of mutants constitutive for expression of the fbp1 gene of Schizosaccharomyces pombe. Genetics Apr 1990; 124(4): 807-816.
Neely LA, Hoffman CS. Protein kinase A and mitogen-activated protein kinase pathways antagonistically regulate fission yeast fbp1 transcription by employing different modes of action at two upstream activation sites. Mol Cell Biol Sep 2000; 20(17): 6426-6434.
Petit T, Blazquez MA, Gancedo C. Schizosaccharomyces pombe possesses an unusual and a conventional hexokinase: Biochemical and molecular characterization of both hexokinases. Febs Lett Jan 8 1996; 378(2): 185-189.
Muller EH, Richards EJ, Norbeck J et al. Thiamine repression and pyruvate decarboxylase autoregulation independently control the expression of the Saccharomyces cerevisiae PDC5 gene. Febs Lett Apr 23 1999; 449(2-3): 245-250.
Carlson M. Glucose repression in yeast. Curr Opin Microbiol Apr 1999; 2(2): 202-207.
Bunik VI. 2-Oxo acid dehydrogenase complexes in redox regulation. Eur J Biochem Mar 2003; 270(6): 1036-1042.
Rapala-Kozik M, Kowalska E, Ostrowska K. Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. J Exp Bot 2008; 59(15): 4133-4143.

References

Rindi G, Laforenza U. Thiamine intestinal transport and related issues: recent aspects. Proc Soc Exp Biol Med Sep 2000; 224(4): 246-255.

Gangolf M, Czerniecki J, Radermecker M et al. Thiamine status in humans and content of phosphorylated thiamine derivatives in biopsies and cultured cells. PLoS One Oct 25 2010; 5(10): e13616.

Friedrich W. Thiamin (Vitamin B1, aneurin). Hanbuch der Vitamine. Munich: Urban & Schwarzenberg; 1987: 240-258.

Flores CL, Rodriguez C, Petit T, Gancedo C. Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev Oct 2000; 24(4): 507-529.

Walker G. Yeast physiology and biotechnology. UK: John Wiley & Sons 1998.

Wood V, Harris MA, McDowall MD et al. PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res Jan 2012; 40(Database issue): D695-699.

Chen D, Toone WM, Mata J et al. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell Jan 2003; 14(1): 214-229.

Khlebodarova TM. [How cells protect themselves against stress?]. Genetika Apr 2002; 38(4): 437-452.

Jung IL, Kim IG. Thiamine protects against paraquat-induced damage: scavenging activity of reactive oxygen species. Environ Toxicol Pharmacol Dec 2003; 15(1): 19-26.

Rapala-Kozik M, Wolak N, Kujda M, Banas AK. The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response. BMC Plant Biol Jan 3 2012; 12: 2.

Tunc-Ozdemir M, Miller G, Song L et al. Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol Sep 2009; 151(1): 421-432.

Wolak N, Kowalska E, Kozik A, Rapala-Kozik M. Thiamine increases the resistance of baker's yeast Saccharomyces cerevisiae against oxidative, osmotic and thermal stress, through mechanisms partly independent of thiamine diphosphate-bound enzymes. FEMS Yeast Res Dec 2014; 14(8): 1249-1262.

Depeint F, Bruce WR, Shangari N, Mehta R, O'Brien PJ. Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem Biol Interact Oct 27 2006; 163(1-2): 94-112.

Palabiyik B, Ghods FJ, Ucar EO. A potential protective role for thiamine in glucose-driven oxidative stress. Genet Mol Res 2014; 13(3): 5582-5593.

Gutz H, Heslot H, Leupold U, Loprieno N. Schizosaccharomyces pombe. In: King RC, ed. Handbook of Genetics. New York: Plenum Press; 1974: 395–446.

Waterborg JH. The protein protocols handbook. New York: Humana Press; 2002.

Cho YWP, E. H. Lim, C. J. Catalase, glutathione S-transferase and thioltransferase respond differently to oxidative stress in Schizosaccharomyces pombe. J Biochem Mol Biol 2000; 33: 344-348.

Cakmak I, Marschner H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol Apr 1992; 98(4): 1222-1227.

Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res May 1 2001; 29(9): e45.

Palabiyik B, Kig C, Pekmez M, Dalyan L, Arda N, Temizkan G. Investigation of the relationship between oxidative stress and glucose signaling in Schizosaccharomyces pombe. Biochem Genet Jun 2012; 50(5-6): 336-349.

Gioda CR, de Oliveira Barreto T, Primola-Gomes TN et al. Cardiac oxidative stress is involved in heart failure induced by thiamine deprivation in rats. Am J Physiol Heart Circ Physiol Jun 2010; 298(6): H2039-2045.

Nagae M, Parniske M, Kawaguchi M, Takeda N. The Thiamine Biosynthesis Gene THI1 Promotes Nodule Growth and Seed Maturation. Plant Physiol Nov 2016; 172(3): 2033-2043.

Li R, Xiong G, Yuan S, Wu Z, Miao Y, Weng P. Investigating the underlying mechanism of Saccharomyces cerevisiae in response to ethanol stress employing RNA-seq analysis. World J Microbiol Biotechnol Nov 3 2017; 33(11): 206.

Kartal B, Akcay A, Palabıyık B. Oxidative Stress Upregulates the Transcription of Genes Involved in Thiamine Metabolism. Turkish J Biol 2018; 42(5): 447-452.

Hoffman CS, Winston F. Isolation and characterization of mutants constitutive for expression of the fbp1 gene of Schizosaccharomyces pombe. Genetics Apr 1990; 124(4): 807-816.

Neely LA, Hoffman CS. Protein kinase A and mitogen-activated protein kinase pathways antagonistically regulate fission yeast fbp1 transcription by employing different modes of action at two upstream activation sites. Mol Cell Biol Sep 2000; 20(17): 6426-6434.

Petit T, Blazquez MA, Gancedo C. Schizosaccharomyces pombe possesses an unusual and a conventional hexokinase: Biochemical and molecular characterization of both hexokinases. Febs Lett Jan 8 1996; 378(2): 185-189.

Muller EH, Richards EJ, Norbeck J et al. Thiamine repression and pyruvate decarboxylase autoregulation independently control the expression of the Saccharomyces cerevisiae PDC5 gene. Febs Lett Apr 23 1999; 449(2-3): 245-250.

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

Bunik VI. 2-Oxo acid dehydrogenase complexes in redox regulation. Eur J Biochem Mar 2003; 270(6): 1036-1042.

Rapala-Kozik M, Kowalska E, Ostrowska K. Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. J Exp Bot 2008; 59(15): 4133-4143.

Author biographies is not available.