Characterization of hexose transporter genes in the views of the chronological life span and glucose uptake in fission yeast
Fission yeast, Schizosaccharomyces pombe, possesses eight hexose transporters, Ght1~8. In order to clarify the role of each hexose transporter on glucose uptake, a glucose uptake assay system was established and the actual glucose uptake activity of each hexose transporter-deletion mutant was measur...
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| Published in | Journal of general and applied microbiology Vol. 68; no. 6; pp. 270 - 277 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Japan
Applied Microbiology, Molecular and Cellular Biosciences Research Foundation
01.01.2022
Japan Science and Technology Agency |
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| Online Access | Get full text |
| ISSN | 0022-1260 1349-8037 |
| DOI | 10.2323/jgam.2022.05.006 |
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| Abstract | Fission yeast, Schizosaccharomyces pombe, possesses eight hexose transporters, Ght1~8. In order to clarify the role of each hexose transporter on glucose uptake, a glucose uptake assay system was established and the actual glucose uptake activity of each hexose transporter-deletion mutant was measured. Under normal growth condition containing 2% glucose, ∆ght5 and ∆ght2 mutants showed large and small decrease in glucose uptake activity, respectively. On the other hand, the other deletion mutants did not show any decrease in glucose uptake activity indicating that, in the presence of Ght5 and Ght2, the other hexose transporters do not play a significant role in glucose uptake. To understand the relevance between glucose uptake and lifespan regulation, we measured the chronological lifespan of each hexose transporter deletion mutant, and found that only ∆ght5 mutant showed a significant lifespan extension. Based on these results we showed that Ght5 is mainly involved in the glucose uptake in Schizosaccharomyces pombe, and suggested that the ∆ght5 mutant has prolonged lifespan due to physiological changes similar to calorie restriction. |
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| AbstractList | Fission yeast, Schizosaccharomyces pombe, possesses eight hexose transporters, Ght1~8. In order to clarify the role of each hexose transporter on glucose uptake, a glucose uptake assay system was established and the actual glucose uptake activity of each hexose transporter-deletion mutant was measured. Under normal growth condition containing 2% glucose, ∆ght5 and ∆ght2 mutants showed large and small decrease in glucose uptake activity, respectively. On the other hand, the other deletion mutants did not show any decrease in glucose uptake activity indicating that, in the presence of Ght5 and Ght2, the other hexose transporters do not play a significant role in glucose uptake. To understand the relevance between glucose uptake and lifespan regulation, we measured the chronological lifespan of each hexose transporter deletion mutant, and found that only ∆ght5 mutant showed a significant lifespan extension. Based on these results we showed that Ght5 is mainly involved in the glucose uptake in Schizosaccharomyces pombe, and suggested that the ∆ght5 mutant has prolonged lifespan due to physiological changes similar to calorie restriction. |
| ArticleNumber | 2022.05.006 |
| Author | Maekawa, Yasukichi Hayashi, Kanako Shigeaki, Saitoh Matsui, Kotaro Ohtsuka, Hokuto Maruyama, Teppei Shimasaki, Takafumi Aiba, Hirofumi |
| Author_xml | – sequence: 1 fullname: Matsui, Kotaro organization: Laboratory of Molecular Microbiology, Department of Basic Medicinal Sciences, Graduate School of Pharmaceutical Sciences, Nagoya University – sequence: 1 fullname: Ohtsuka, Hokuto organization: Laboratory of Molecular Microbiology, Department of Basic Medicinal Sciences, Graduate School of Pharmaceutical Sciences, Nagoya University – sequence: 1 fullname: Shigeaki, Saitoh organization: Institute of Life Science, Kurume University – sequence: 1 fullname: Maruyama, Teppei organization: Laboratory of Molecular Microbiology, Department of Basic Medicinal Sciences, Graduate School of Pharmaceutical Sciences, Nagoya University – sequence: 1 fullname: Hayashi, Kanako organization: Laboratory of Molecular Microbiology, Department of Basic Medicinal Sciences, Graduate School of Pharmaceutical Sciences, Nagoya University – sequence: 1 fullname: Aiba, Hirofumi organization: Laboratory of Molecular Microbiology, Department of Basic Medicinal Sciences, Graduate School of Pharmaceutical Sciences, Nagoya University – sequence: 1 fullname: Maekawa, Yasukichi organization: Laboratory of Molecular Microbiology, Department of Basic Medicinal Sciences, Graduate School of Pharmaceutical Sciences, Nagoya University – sequence: 1 fullname: Shimasaki, Takafumi organization: Laboratory of Molecular Microbiology, Department of Basic Medicinal Sciences, Graduate School of Pharmaceutical Sciences, Nagoya University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35781263$$D View this record in MEDLINE/PubMed |
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| References | Vassiliadis, D., Wong, K. H., Andrianopoulos, A., and Monahan, B. J. (2019) A genome-wide analysis of carbon catabolite repression in Schizosaccharomyces pombe. BMC Genomics, 20, 251. Chen, B. R., and Runge, K. W. (2009) A new Schizosaccharomyces pombe chronological lifespan assay reveals that caloric restriction promotes efficient cell cycle exit and extends longevity. Exp. Gerontol., 44, 493-502. Oshiro, T., Aiba, H., and Mizuno, T. (2003) A defect in a fatty acyl-CoA synthetase gene, lcf1+, results in a decrease in viability after entry into the stationary phase in fission yeast. Mol. Genet. Genomics, 269, 437-442. Ozcan, S., and Johnston, M. (1999) Function and regulation of yeast hexose transporters. Microbiol. Mol. Biol. Rev., 63, 554–569. Matsuzawa, T., Hara, F., Tanaka, N., Tohda, H., and Takegawa, K. (2013) ght2⁺ is required for UDP-galactose synthesis from extracellular galactose by Schizosaccharomyces pombe. Appl. Microbiol. Biotech., 97, 4957–4964. Huerta-Cepas, J., Serra, F., and Bork, P. (2016) ETE 3: Reconstruction, analysis, and visualization of phylogenomic data. Mol. Biol. Evol., 33, 1635-1638. Johnston, M. (1999) Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet., 15, 29–33. Saitoh, S., Mori, A., Uehara, L., Masuda, F., Soejima, S. et al. (2015) Mechanisms of expression and translocation of major fission yeast glucose transporters regulated by CaMKK/phosphatases, nuclear shuttling, and TOR. Mol. Biol. Cell., 26, 373-386. Hentges, P., Driessche, B. V., Tafforeau, L., Vandenhaute, J., and Carr, A. M. (2005) Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast, 22, 1013-1019. Kurauchi, T., Hashizume, A., Imai, Y., Hayashi, K., Tsubouchi, S. et al. (2017) Identification of a novel protein kinase that affects the chronological lifespan in fission yeast. FEMS Microbiol. Lett., 364, fnw257. Ohtsuka, H., Ishida, M., Naito, C., Murakami, H., and Aiba, H. (2015). Sexual development of Schizosaccharomyces pombe is induced by zinc or iron limitation through Ecl1 family genes. Mol. Genet. Genomics, 290, 173–185. Ito, H., Oshiro, T., Fujita, Y., Kubota, S., Naito, C. et al. (2010) Pma1, a P-type proton ATPase, is a determinant of chronological life span in fission yeast. J. Biol. Chem., 285, 34616-34620. Naito, C., Ito, H., Oshiro, T., Ohtsuka, H., Murakami, H. et al. (2014) A new pma1 mutation identified in a chronologically long-lived fission yeast mutant. FEBS Open Bio., 4, 829-833. Hoffman, C. S. (2005) Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem. Soc. Trans., 33, 257–260. Krawchuk, M. D., DeVeaux, L. C., and Wahls, W. P. (1999) High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast, 15, 1419-1427. Pluskal, T., Hayashi, T., Saitoh, S., Fujisawa, A., and Yanagida, M. (2011) Specific biomarkers for stochastic division patterns and starvation-induced quiescence under limited glucose levels in fission yeast. FEBS J., 278, 1299-1315. Masuda, F., Ishii, M., Mori, A., Uehara, L., Yanagida, M. et al. (2016) Glucose restriction induces transient G2 cell cycle arrest extending cellular chronological lifespan. Sci. Rep., 6, 19629. Özkan, E., Kartal, B., Yılmazer, M., and Palabıyık, B. (2019) Iron regulates hexose transporters in Schizosaccharomyces pombe. J. Basic Microbiol., 59, 458-464. Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol., 59, 307-321. Welton, R. M., and Hoffman, C. S. (2000) Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. Genetics, 156, 513–521. Heiland, S., Radovanovic, N., Höfer, N., Winderickx, J., and Lichtenberg, H. (2000) Multiple hexose transporters of Schizosaccharomyces pombe. J. Bacteriol., 182, 2153-2162. Manolescu, A. R., Witkowska, K., Kinnaird, A., and Cessford, T. (2007) Facilitated hexose transporters: new perspectives on form and function. Physiology (Bethesda), 22, 234–240. Shimasaki, T., Ohtsuka, H., Naito, C., Azuma, K., Tenno, T. et al. (2017) Ecl1 is a zinc-binding protein involved in the zinc-limitation-dependent extension of chronological life span in fission yeast. Mol. Genet. Genomics, 292, 475–481. 11 22 12 23 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 10 21 |
| References_xml | – reference: Oshiro, T., Aiba, H., and Mizuno, T. (2003) A defect in a fatty acyl-CoA synthetase gene, lcf1+, results in a decrease in viability after entry into the stationary phase in fission yeast. Mol. Genet. Genomics, 269, 437-442. – reference: Vassiliadis, D., Wong, K. H., Andrianopoulos, A., and Monahan, B. J. (2019) A genome-wide analysis of carbon catabolite repression in Schizosaccharomyces pombe. BMC Genomics, 20, 251. – reference: Kurauchi, T., Hashizume, A., Imai, Y., Hayashi, K., Tsubouchi, S. et al. (2017) Identification of a novel protein kinase that affects the chronological lifespan in fission yeast. FEMS Microbiol. Lett., 364, fnw257. – reference: Heiland, S., Radovanovic, N., Höfer, N., Winderickx, J., and Lichtenberg, H. (2000) Multiple hexose transporters of Schizosaccharomyces pombe. J. Bacteriol., 182, 2153-2162. – reference: Hentges, P., Driessche, B. V., Tafforeau, L., Vandenhaute, J., and Carr, A. M. (2005) Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast, 22, 1013-1019. – reference: Shimasaki, T., Ohtsuka, H., Naito, C., Azuma, K., Tenno, T. et al. (2017) Ecl1 is a zinc-binding protein involved in the zinc-limitation-dependent extension of chronological life span in fission yeast. Mol. Genet. Genomics, 292, 475–481. – reference: Pluskal, T., Hayashi, T., Saitoh, S., Fujisawa, A., and Yanagida, M. (2011) Specific biomarkers for stochastic division patterns and starvation-induced quiescence under limited glucose levels in fission yeast. FEBS J., 278, 1299-1315. – reference: Ozcan, S., and Johnston, M. (1999) Function and regulation of yeast hexose transporters. Microbiol. Mol. Biol. Rev., 63, 554–569. – reference: Saitoh, S., Mori, A., Uehara, L., Masuda, F., Soejima, S. et al. (2015) Mechanisms of expression and translocation of major fission yeast glucose transporters regulated by CaMKK/phosphatases, nuclear shuttling, and TOR. Mol. Biol. Cell., 26, 373-386. – reference: Huerta-Cepas, J., Serra, F., and Bork, P. (2016) ETE 3: Reconstruction, analysis, and visualization of phylogenomic data. Mol. Biol. Evol., 33, 1635-1638. – reference: Ito, H., Oshiro, T., Fujita, Y., Kubota, S., Naito, C. et al. (2010) Pma1, a P-type proton ATPase, is a determinant of chronological life span in fission yeast. J. Biol. Chem., 285, 34616-34620. – reference: Naito, C., Ito, H., Oshiro, T., Ohtsuka, H., Murakami, H. et al. (2014) A new pma1 mutation identified in a chronologically long-lived fission yeast mutant. FEBS Open Bio., 4, 829-833. – reference: Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol., 59, 307-321. – reference: Ohtsuka, H., Ishida, M., Naito, C., Murakami, H., and Aiba, H. (2015). Sexual development of Schizosaccharomyces pombe is induced by zinc or iron limitation through Ecl1 family genes. Mol. Genet. Genomics, 290, 173–185. – reference: Welton, R. M., and Hoffman, C. S. (2000) Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. Genetics, 156, 513–521. – reference: Hoffman, C. S. (2005) Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem. Soc. Trans., 33, 257–260. – reference: Johnston, M. (1999) Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet., 15, 29–33. – reference: Krawchuk, M. D., DeVeaux, L. C., and Wahls, W. P. (1999) High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast, 15, 1419-1427. – reference: Chen, B. R., and Runge, K. W. (2009) A new Schizosaccharomyces pombe chronological lifespan assay reveals that caloric restriction promotes efficient cell cycle exit and extends longevity. Exp. Gerontol., 44, 493-502. – reference: Matsuzawa, T., Hara, F., Tanaka, N., Tohda, H., and Takegawa, K. (2013) ght2⁺ is required for UDP-galactose synthesis from extracellular galactose by Schizosaccharomyces pombe. Appl. Microbiol. Biotech., 97, 4957–4964. – reference: Manolescu, A. R., Witkowska, K., Kinnaird, A., and Cessford, T. (2007) Facilitated hexose transporters: new perspectives on form and function. Physiology (Bethesda), 22, 234–240. – reference: Masuda, F., Ishii, M., Mori, A., Uehara, L., Yanagida, M. et al. (2016) Glucose restriction induces transient G2 cell cycle arrest extending cellular chronological lifespan. Sci. Rep., 6, 19629. – reference: Özkan, E., Kartal, B., Yılmazer, M., and Palabıyık, B. (2019) Iron regulates hexose transporters in Schizosaccharomyces pombe. J. Basic Microbiol., 59, 458-464. – ident: 15 doi: 10.1007/s00438-014-0911-8 – ident: 20 doi: 10.1091/mbc.E14-11-1503 – ident: 6 doi: 10.1093/molbev/msw046 – ident: 8 doi: 10.1016/S0168-9525(98)01637-0 – ident: 12 doi: 10.1038/srep19629 – ident: 4 doi: 10.1002/yea.1291 – ident: 7 doi: 10.1074/jbc.M110.175562 – ident: 11 doi: 10.1152/physiol.00011.2007 – ident: 17 doi: 10.1128/MMBR.63.3.554-569.1999 – ident: 23 doi: 10.1093/genetics/156.2.513 – ident: 9 doi: 10.1002/(SICI)1097-0061(19990930)15:13<1419::AID-YEA466>3.0.CO;2-Q – ident: 3 doi: 10.1128/JB.182.8.2153-2162.2000 – ident: 16 doi: 10.1007/s00438-003-0841-3 – ident: 2 doi: 10.1093/sysbio/syq010 – ident: 5 doi: 10.1042/BST0330257 – ident: 19 doi: 10.1111/j.1742-4658.2011.08050.x – ident: 10 doi: 10.1093/femsle/fnw257 – ident: 13 doi: 10.1007/s00253-012-4637-4 – ident: 21 doi: 10.1007/s00438-016-1285-x – ident: 18 doi: 10.1002/jobm.201800618 – ident: 14 doi: 10.1016/j.fob.2014.09.006 – ident: 22 doi: 10.1186/s12864-019-5602-8 – ident: 1 doi: 10.1016/j.exger.2009.04.004 |
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| Snippet | Fission yeast, Schizosaccharomyces pombe, possesses eight hexose transporters, Ght1~8. In order to clarify the role of each hexose transporter on glucose... |
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| SubjectTerms | Deletion Deletion mutant Fission fission yeast Ght5 Glucose Glucose transporter Growth conditions Hexose Hexose transporter Life span lifespan Longevity Monosaccharide Transport Proteins - genetics Mutants Nutrient deficiency Schizosaccharomyces - genetics Schizosaccharomyces pombe Schizosaccharomyces pombe Proteins - genetics Schizosaccharomyces pombe Proteins - metabolism Yeast |
| Title | Characterization of hexose transporter genes in the views of the chronological life span and glucose uptake in fission yeast |
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