Research Article
BibTex RIS Cite

Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism

Year 2024, , 106 - 113, 28.06.2024
https://doi.org/10.46810/tdfd.1394491

Abstract

Protein kinase A signaling pathway is regulated by cAMP. PKA activity is inhibited by the cAMP phosphodiesterases. PDE1 and PDE2 genes encode two phosphodiesterases with low and high affinity for cAMP, respectively. NTH1 gene encodes the neutral trehalase enzyme, which is responsible for the stress-accumulated trehalose degradation. This study aimed to investigate the effect of PDE1 and PDE2 gene products on the expression of the NTH1 gene and reserve carbohydrate metabolism in response to a stressful environment and during a replenishment phase. The expression of the NTH1 gene was shown to be lower than that of the wild-type under normal conditions, heat stress, nitrogen starvation, and also during the replenishment period in pde1∆ and pde1∆ yeast cells. The accumulation of trehalose and glycogen was shown to be dramatically enhanced in pde1∆ yeast cells. However, deletion of the PDE2 gene did not lead to a significant change in trehalose and glycogen accumulation comparable to that found in the wild type. These results indicate that the PDE1 gene product is required for downregulation of reserve carbohydrate metabolism. Consequently, the Pde1 protein is considered to exert yet-unidentified regulatory control over the Pde2 protein.

Supporting Institution

The Scientific Research Coordination Unit of Çanakkale Onsekiz Mart University

Thanks

The work is an outcome of research project number FHD-2017-1325 financed by the Scientific Research Coordination Unit of Çanakkale Onsekiz Mart University, Türkiye. We thank to Professor Jean Marie François for gift of LacZ fusion systems.

References

  • Smets B, Ghillebert R, De Snijder P, Binda M, Swinnen E, De Virgilio C, et al. Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae. Curr Genet. 2010; 56(1):1-32.
  • Conrad M, Schothorst J, Kankipati HN, Van Zeebroeck G, Rubio-Texeira M, Thevelein JM. Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev. 2014; 38(2):254-299.
  • Huang G, Huang Q, Wei Y, Wang Y, Du H. Multiple roles and diverse regulation of the Ras/cAMP/protein kinase A pathway in Candida albicans. Mol Microbiol. 2019; 111(1):6-16.
  • Bouchez C, Devin A. Mitochondrial biogenesis and mitochondrial reactive oxygen species (ROS): A complex relationship regulated by the cAMP/PKA signaling pathway. cells. 2019; 8(4):287.
  • Creamer DR, Hubbard SJ, Ashe MP, Grant CM. Yeast protein kinase A isoforms: A means of encoding specificity in the response to diverse stress conditions? Biomolecules. 2022; 12(7):958.
  • Park JI, Grant CM, Dawes IW. The high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae is the major determinant of cAMP levels in stationary phase: involvement of different branches of the Ras-cyclic AMP pathway in stress responses. Biochem Biophys Res Commun. 2005; 327(1):311-319.
  • McCormick K, Baillie GS. Compartmentalisation of second messenger signalling pathways. Curr Opin Genet Dev. 2014; 27:20-25.
  • Eleutherio E, Panek A, De Mesquita JF, Trevisol E, Magalhães R. Revisiting yeast trehalose metabolism. Curr Genet. 2015; 61(3):263-274.
  • Tisi R, Belotti F, Martegani E. Yeast as a model for Ras signalling. In: Trabalzini L, Retta S. editors. Ras signaling methods and protocols. 1st ed. Humana Press, Totowa, NJ. 2014, p. 359-390.
  • François JM, Walther T, Parrou JL. Genetics and regulation of glycogen and trehalose metabolism in Saccharomyces cerevisiae. In: Liu Z. editor. Microbial stress tolerance for biofuels. 1st ed. Springer Berlin, Heidelberg. 2012, p.29-55.
  • Yap CF, Garcia-Albornoz M, Jarnuczak AF, Hubbard SJ, Schwartz JM. Model parameterization with quantitative proteomics: Case study with trehalose metabolism in Saccharomyces cerevisiae. Processes. 2021; 9(1):139.
  • Genc TT. The SAGA complex is essential for the regulation of genes involved in yeast trehalose metabolism. Trakya University Journal of Natural Sciences. 2022; 23(2):167-176.
  • Trimborn L, Hoecker U, Ponnu J. A Simple quantitative assay for measuring β-Galactosidase activity using X-Gal in yeast-based interaction analyses. Curr Protoc. 2022; 2(5):e421.
  • Chen Y, Futcher B. Assaying glycogen and trehalose in yeast. Bio-protocol. 2017; 7(13):e2371.
  • Gorner W, Durchschlag E, Martinez-Pastor MT, Estruch F, Ammerer G, et al. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12(4):586-597.
  • Lee P, Kim MS, Paik SM, Choi SH, Cho BR, Hahn JS. Rim15-dependent activation of Hsf1 and Msn2/4 transcription factors by direct phosphorylation in Saccharomyces cerevisiae. FEBS Lett. 2013; 587(22):3648-3655.
  • Sweeney K, McClean MN. Transcription factor localization dynamics and DNA binding drive distinct promoter interpretations. Cell Rep. 2023; 42(5):112426.
  • Plank M. Interaction of TOR and PKA signaling in S. cerevisiae. Biomolecules. 2022; 12(2):210.
  • Ferguson SB, Anderson ES, Harshaw RB, Thate T, Craig NL, Nelson HC. Protein kinase A regulates constitutive expression of small heat-shock genes in an Msn2/4p-independent and Hsf1p-dependent manner in Saccharomyces cerevisiae. Genetics. 2005; 169(3):1203-1214.
  • Alfatah M, Wong JH, Krishnan VG, Lee YC, Sin QF, Goh CJH, et al. TORC1 regulates the transcriptional response to glucose and developmental cycle via the Tap42-Sit4-Rrd1/2 pathway in Saccharomyces cerevisiae. BMC Biol. 2021; 19(1):95.
  • Chasman D, Ho YH, Berry DB, Nemec CM, MacGilvray ME, Hose J, et al. Pathway connectivity and signaling coordination in the yeast stress-activated signaling network. Mol Syst Biol. 2014; 10(11):759.
  • Ma P, Wera S, Van Dijck P, Thevelein JM. The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell. 1999; 10(1):91-104.
  • MacGilvray ME, Shishkova E, Chasman D, Place M, Gitter A, Coon JJ, et al. Network inference reveals novel connections in pathways regulating growth and defense in the yeast salt response. PLoS Comput Biol. 2018; 13(5):e1006088.
  • Kim JS, Lee KT, Bahn YS. Deciphering the regulatory mechanisms of the cAMP/protein kinase A pathway and their roles in the pathogenicity of Candida auris. Microbiol Spectr. 2023; e0215223.
  • Williamson T, Schwartz JM, Kell DB, Stateva L, Deterministic mathematical models of the cAMP pathway in Saccharomyces cerevisiae. BMC Syst Biol. 2009; 16(3):70.
  • Paalman JW, Verwaal R, Slofstra SH, Verkleij AJ, Boonstra J, Verrips CT. Trehalose and glycogen accumulation is related to the duration of the G1 phase of Saccharomyces cerevisiae. FEMS Yeast Res. 2003; 3:261-268.
  • Eardley J, Timson DJ. Yeast Cellular Stress: Impacts on Bioethanol Production. Fermentation. 2020; 6: 109.
  • Jung WH, Warn P, Ragni E, Popolo L, Nunn CD, Turner MP, Stateva L. Deletion of PDE2, the gene encoding the high-affinity cAMP phosphodiesterase, results in changes of the cell wall and membrane in Candida albicans. Yeast. 2005; 22(4):285-294.
  • Jacquel B, Matifas A, Charvin G. A trade-off between stress resistance and tolerance underlies the adaptive response to hydrogen peroxide. bioRxiv. 2021; ffhal-03451307f.
  • Zaccolo M, Zerio A, Lobo MJ. Subcellular organization of the cAMP signaling pathway. Pharmacol Rev. 2021; 73(1):278-309.

cAMP-bağımlı Fosfodiesteraz Aktivitesinin NTH1 Gen Ekspresyonu ve Depo Karbonhidrat Metabolizması Üzerine Etkisi

Year 2024, , 106 - 113, 28.06.2024
https://doi.org/10.46810/tdfd.1394491

Abstract

Protein kinaz A sinyal yolağı cAMP tarafından düzenlenir. PKA aktivitesi, cAMP'yi hidrolize eden cAMP fosfodiesterazlar tarafından inhibe edilir. PDE1 ve PDE2 genleri cAMP için düşük ve yüksek afiniteye sahip iki fosfodiesterazı kodlar. NTH1 geni stres şartlarında biriktirilen trehalozun parçalanmasından sorumlu olan nötral trehalaz enzimini kodlar. Bu çalışmada, stres koşullarında ve stres sonrasında, PDE1 ve PDE2 genlerinin NTH1 gen ekspresyonu ve depo karbonhidrat metabolizması üzerine etkisinin belirlenmesi amaçladı. Normal koşullarda, ısı stresinde, azot açlığında ve stresten kurtulma sonrasında, pde1∆ ve pde1∆ maya hücrelerinde belirlenen NTH1 gen ekspresyonunun yaban tipten daha düşük olduğu görüldü. Trehaloz ve glikojen birikiminin pde1∆ maya hücrelerinde oldukça yüksek oranda arttığı gözlendi. Bununla birlikte, PDE2 yokluğunun trehaloz ve glikojen birikiminde önemli bir değişikliğe yol açmadığı gözlendi. Bu sonuçlar, depo karbonhidrat metabolizmasının aşağı regülasyonu için PDE1 gen ürününün gerekli olduğunu göstermektedir. Sonuç olarak, Pde1 proteininin, Pde2 proteini üzerinde henüz tanımlanamayan düzenleyici kontrol uyguladığı düşünülmektedir.

References

  • Smets B, Ghillebert R, De Snijder P, Binda M, Swinnen E, De Virgilio C, et al. Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae. Curr Genet. 2010; 56(1):1-32.
  • Conrad M, Schothorst J, Kankipati HN, Van Zeebroeck G, Rubio-Texeira M, Thevelein JM. Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev. 2014; 38(2):254-299.
  • Huang G, Huang Q, Wei Y, Wang Y, Du H. Multiple roles and diverse regulation of the Ras/cAMP/protein kinase A pathway in Candida albicans. Mol Microbiol. 2019; 111(1):6-16.
  • Bouchez C, Devin A. Mitochondrial biogenesis and mitochondrial reactive oxygen species (ROS): A complex relationship regulated by the cAMP/PKA signaling pathway. cells. 2019; 8(4):287.
  • Creamer DR, Hubbard SJ, Ashe MP, Grant CM. Yeast protein kinase A isoforms: A means of encoding specificity in the response to diverse stress conditions? Biomolecules. 2022; 12(7):958.
  • Park JI, Grant CM, Dawes IW. The high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae is the major determinant of cAMP levels in stationary phase: involvement of different branches of the Ras-cyclic AMP pathway in stress responses. Biochem Biophys Res Commun. 2005; 327(1):311-319.
  • McCormick K, Baillie GS. Compartmentalisation of second messenger signalling pathways. Curr Opin Genet Dev. 2014; 27:20-25.
  • Eleutherio E, Panek A, De Mesquita JF, Trevisol E, Magalhães R. Revisiting yeast trehalose metabolism. Curr Genet. 2015; 61(3):263-274.
  • Tisi R, Belotti F, Martegani E. Yeast as a model for Ras signalling. In: Trabalzini L, Retta S. editors. Ras signaling methods and protocols. 1st ed. Humana Press, Totowa, NJ. 2014, p. 359-390.
  • François JM, Walther T, Parrou JL. Genetics and regulation of glycogen and trehalose metabolism in Saccharomyces cerevisiae. In: Liu Z. editor. Microbial stress tolerance for biofuels. 1st ed. Springer Berlin, Heidelberg. 2012, p.29-55.
  • Yap CF, Garcia-Albornoz M, Jarnuczak AF, Hubbard SJ, Schwartz JM. Model parameterization with quantitative proteomics: Case study with trehalose metabolism in Saccharomyces cerevisiae. Processes. 2021; 9(1):139.
  • Genc TT. The SAGA complex is essential for the regulation of genes involved in yeast trehalose metabolism. Trakya University Journal of Natural Sciences. 2022; 23(2):167-176.
  • Trimborn L, Hoecker U, Ponnu J. A Simple quantitative assay for measuring β-Galactosidase activity using X-Gal in yeast-based interaction analyses. Curr Protoc. 2022; 2(5):e421.
  • Chen Y, Futcher B. Assaying glycogen and trehalose in yeast. Bio-protocol. 2017; 7(13):e2371.
  • Gorner W, Durchschlag E, Martinez-Pastor MT, Estruch F, Ammerer G, et al. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12(4):586-597.
  • Lee P, Kim MS, Paik SM, Choi SH, Cho BR, Hahn JS. Rim15-dependent activation of Hsf1 and Msn2/4 transcription factors by direct phosphorylation in Saccharomyces cerevisiae. FEBS Lett. 2013; 587(22):3648-3655.
  • Sweeney K, McClean MN. Transcription factor localization dynamics and DNA binding drive distinct promoter interpretations. Cell Rep. 2023; 42(5):112426.
  • Plank M. Interaction of TOR and PKA signaling in S. cerevisiae. Biomolecules. 2022; 12(2):210.
  • Ferguson SB, Anderson ES, Harshaw RB, Thate T, Craig NL, Nelson HC. Protein kinase A regulates constitutive expression of small heat-shock genes in an Msn2/4p-independent and Hsf1p-dependent manner in Saccharomyces cerevisiae. Genetics. 2005; 169(3):1203-1214.
  • Alfatah M, Wong JH, Krishnan VG, Lee YC, Sin QF, Goh CJH, et al. TORC1 regulates the transcriptional response to glucose and developmental cycle via the Tap42-Sit4-Rrd1/2 pathway in Saccharomyces cerevisiae. BMC Biol. 2021; 19(1):95.
  • Chasman D, Ho YH, Berry DB, Nemec CM, MacGilvray ME, Hose J, et al. Pathway connectivity and signaling coordination in the yeast stress-activated signaling network. Mol Syst Biol. 2014; 10(11):759.
  • Ma P, Wera S, Van Dijck P, Thevelein JM. The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell. 1999; 10(1):91-104.
  • MacGilvray ME, Shishkova E, Chasman D, Place M, Gitter A, Coon JJ, et al. Network inference reveals novel connections in pathways regulating growth and defense in the yeast salt response. PLoS Comput Biol. 2018; 13(5):e1006088.
  • Kim JS, Lee KT, Bahn YS. Deciphering the regulatory mechanisms of the cAMP/protein kinase A pathway and their roles in the pathogenicity of Candida auris. Microbiol Spectr. 2023; e0215223.
  • Williamson T, Schwartz JM, Kell DB, Stateva L, Deterministic mathematical models of the cAMP pathway in Saccharomyces cerevisiae. BMC Syst Biol. 2009; 16(3):70.
  • Paalman JW, Verwaal R, Slofstra SH, Verkleij AJ, Boonstra J, Verrips CT. Trehalose and glycogen accumulation is related to the duration of the G1 phase of Saccharomyces cerevisiae. FEMS Yeast Res. 2003; 3:261-268.
  • Eardley J, Timson DJ. Yeast Cellular Stress: Impacts on Bioethanol Production. Fermentation. 2020; 6: 109.
  • Jung WH, Warn P, Ragni E, Popolo L, Nunn CD, Turner MP, Stateva L. Deletion of PDE2, the gene encoding the high-affinity cAMP phosphodiesterase, results in changes of the cell wall and membrane in Candida albicans. Yeast. 2005; 22(4):285-294.
  • Jacquel B, Matifas A, Charvin G. A trade-off between stress resistance and tolerance underlies the adaptive response to hydrogen peroxide. bioRxiv. 2021; ffhal-03451307f.
  • Zaccolo M, Zerio A, Lobo MJ. Subcellular organization of the cAMP signaling pathway. Pharmacol Rev. 2021; 73(1):278-309.
There are 30 citations in total.

Details

Primary Language English
Subjects Signal Transduction, Biochemistry and Cell Biology (Other)
Journal Section Articles
Authors

Tulay Turgut Genc 0000-0001-5074-3572

Early Pub Date June 28, 2024
Publication Date June 28, 2024
Submission Date November 22, 2023
Acceptance Date June 10, 2024
Published in Issue Year 2024

Cite

APA Turgut Genc, T. (2024). Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism. Türk Doğa Ve Fen Dergisi, 13(2), 106-113. https://doi.org/10.46810/tdfd.1394491
AMA Turgut Genc T. Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism. TDFD. June 2024;13(2):106-113. doi:10.46810/tdfd.1394491
Chicago Turgut Genc, Tulay. “Effect of CAMP-Dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism”. Türk Doğa Ve Fen Dergisi 13, no. 2 (June 2024): 106-13. https://doi.org/10.46810/tdfd.1394491.
EndNote Turgut Genc T (June 1, 2024) Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism. Türk Doğa ve Fen Dergisi 13 2 106–113.
IEEE T. Turgut Genc, “Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism”, TDFD, vol. 13, no. 2, pp. 106–113, 2024, doi: 10.46810/tdfd.1394491.
ISNAD Turgut Genc, Tulay. “Effect of CAMP-Dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism”. Türk Doğa ve Fen Dergisi 13/2 (June 2024), 106-113. https://doi.org/10.46810/tdfd.1394491.
JAMA Turgut Genc T. Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism. TDFD. 2024;13:106–113.
MLA Turgut Genc, Tulay. “Effect of CAMP-Dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism”. Türk Doğa Ve Fen Dergisi, vol. 13, no. 2, 2024, pp. 106-13, doi:10.46810/tdfd.1394491.
Vancouver Turgut Genc T. Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism. TDFD. 2024;13(2):106-13.