Abstract
Establishing the function of trehalose in yeast cells has led us, over the years, through a long path—from simple energy storage carbohydrate, then a stabilizer and protector of membranes and proteins, through a safety valve against damage caused by oxygen radicals, up to regulator of the glycolytic path. In addition, trehalose biosynthesis has been proposed as a target for novel drugs against several pathogens. Since this pathway is entirely absent in mammalian cells and makes use of highly specific enzymes, trehalose metabolism might be an interesting target for the development of novel therapies. In this review, we want to address some recent points investigated about trehalose metabolism in Saccharomyces cerevisiae, focusing mainly on the mechanism by which this simple disaccharide protects against stress and on the enzymes involved in its synthesis and breakdown. We believe that these concepts are of great importance for medical and biotechnological applications.
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References
Alizadeh P, Klionsky DJ (1996) Purification and biochemical characterization of the ATH1 gene product, vacuolar acid trehalase, from Saccharomyces cerevisiae. FEBS Lett 391:273–278
Avonce N, Wuyts J, Verschooten K, Vandesteene L, Van Dijck P (2010) The Cytophaga hutchinsonii ChTPSP: first characterized bifunctional TPS-TPP protein as putative ancestor of all eukaryotic trehalose biosynthesis proteins. Mol Biol Evol 27:359–369. doi:10.1093/molbev/msp241
Basso LC, de Amorim HV, de Oliveira AJ, Lopes ML (2008) Yeast selection for fuel ethanol production in Brazil. FEMS Yeast Res 8:1155–1163. doi:10.1111/j.1567-1364.2008.00428.x
Becker A, Schloder P, Steele JE, Wegener G (1996) The regulation of trehalose metabolism in insects. Experientia 52:433–439
Behm CA (1997) The role of trehalose in the physiology of nematodes. Int J Parasitol 27:215–229
Bell W et al (1992) Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur J Biochem 209:951–959
Bell W et al (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J Biol Chem 273:33311–33319
Benaroudj N, Lee DH, Goldberg AL (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276:24261–24267. doi:10.1074/jbc.M101487200
Blazquez MA, Lagunas R, Gancedo C, Gancedo JM (1993) Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEBS Lett 329:51–54
Blazquez MA, Santos E, Flores CL, Martinez-Zapater JM, Salinas J, Gancedo C (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 13:685–689
Bonini BM et al (2000) Expression of escherichia coli otsA in a Saccharomyces cerevisiae tps1 mutant restores trehalose 6-phosphate levels and partly restores growth and fermentation with glucose and control of glucose influx into glycolysis. Biochem J 350:261–268
Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–228. doi:10.1016/j.cryobiol.2004.02.011
Cabib E, Leloir LF (1958) The biosynthesis of trehalose phosphate. J Biol Chem 231:259–275
Coutinho C, Bernardes E, Félix D, Panek AD (1988) Trehalose as cryoprotectant for preservation of yeast strains. J Biotechnol 7:23-32 doi:10.1016/0168-1656(88)90032-6
Crowe LM, Crowe JH (1986) Hydration-dependent phase transitions and permeability properties of biological membranes. In: Leopold AC (ed) Membranes, metabolism and dry organisms. Cornell University Press, NY, pp 210–230
Crowe CC, Koblasz KK (1971) Isolation of L-forms in recurrent urinary tract infections. Am J Med Technol 37:367–370
Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703. doi:10.1126/science.223.4637.701
Crowe JH, Tablin F, Wolkers WF, Gousset K, Tsvetkova NM, Ricker J (2003) Stabilization of membranes in human platelets freeze-dried with trehalose. Chem Phys Lipids 122:41–52
da Costa Morato Nery D, da Silva CG, Mariani D, Fernandes PN, Pereira MD, Panek AD, Eleutherio EC (2008) The role of trehalose and its transporter in protection against reactive oxygen species. Biochim Biophys Acta 1780:1408-1411 doi:10.1016/j.bbagen.2008.05.011
de Mesquita JF, Paschoalin VM, Panek AD (1997) Modulation of trehalase activity in Saccharomyces cerevisiae by an intrinsic protein. Biochim Biophys Acta 1334:233–239
De Mesquita JF, Panek AD, de Araujo PS (2003a) In silico and in vivo analysis reveal a novel gene in Saccharomyces cerevisiae trehalose metabolism. BMC Genom 4:45. doi:10.1186/1471-2164-4-45
De Mesquita JF, Stambuck BU, Silva MA, Machado-Santelli GM, Araujo PS (2003b) Evidences for the down regulation of Saccharomyces cerevisiae trehalose transporter by endocytosis. Book of Abstracts of XXXII Annual Meeting of Brazilian Society for Biochemistry and Molecular Biology, pp. 25
De Smet KA, Weston A, Brown IN, Young DB, Robertson BD (2000) Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146(Pt 1):199–208
De Virgilio C, Burckert N, Boller T, Wiemken A (1991) A method to study the rapid phosphorylation-related modulation of neutral trehalase activity by temperature shifts in yeast. FEBS Lett 291:355–358
De Virgilio C, Burckert N, Bell W, Jeno P, Boller T, Wiemken A (1993) Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur J Biochem 212:315–323
Elbein AD (1968) Trehalose phosphate synthesis in Streptomyces hygroscopicus: purification of guanosine diphosphate d-glucose: d-glucose-6-phosphate 1-glucosyl-transferase. J Bacteriol 96:1623–1631
Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R
Eleutherio EC, Araujo PS, Panek AD (1993a) Protective role of trehalose during heat stress in Saccharomyces cerevisiae. Cryobiology 30:591–596. doi:10.1006/cryo.1993.1061
Eleutherio EC, Araujo PS, Panek AD (1993b) Role of the trehalose carrier in dehydration resistance of Saccharomyces cerevisiae. Biochim Biophys Acta 1156:263–266
Eleutherio EC, Maia FM, Pereira MD, Degre R, Cameron D, Panek AD (1997) Induction of desiccation tolerance by osmotic treatment in Saccharomyces uvarum var. carlsbergensis. Can J Microbiol 43:495–498
Esteves MI, Quintilio W, Sato RA, Raw I, De Araújo PS, Da Costa MHB (2000) Stabilisation of immunoconjugates by trehalose. Biotechnol Lett 22:417–420
Franca MB, Panek AD, Eleutherio EC (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A: Mol Integr Physiol 146:621–631. doi:10.1016/j.cbpa.2006.02.030
François J, Parrou JL (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 25:125–145. doi:10.1016/S0168-6445(00)00059-0
Francois J, Neves MJ, Hers HG (1991) The control of trehalose biosynthesis in Saccharomyces cerevisiae: evidence for a catabolite inactivation and repression of trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase. Yeast 7:575–587. doi:10.1002/yea.320070605
Fu H, Subramanian RR, Masters SC (2000) 14-3-3 proteins: structure, function, and regulation. Annu Rev Pharmacol Toxicol 40:617–647. doi:10.1146/annurev.pharmtox.40.1.617
Garre E, Perez-Torrado R, Gimeno-Alcaniz JV, Matallana E (2009) Acid trehalase is involved in intracellular trehalose mobilization during postdiauxic growth and severe saline stress in Saccharomyces cerevisiae. FEMS Yeast Res 9:52–62. doi:10.1111/j.1567-1364.2008.00453.x
Gasch AP et al (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257
Harland CW, Rabuka D, Bertozzi CR, Parthasarathy R (2008) The Mycobacterium tuberculosis virulence factor trehalose dimycolate imparts desiccation resistance to model mycobacterial membranes. Biophys J 94:4718–4724. doi:10.1529/biophysj.107.125542
He S, Bystricky K, Leon S, Francois JM, Parrou JL (2009) The Saccharomyces cerevisiae vacuolar acid trehalase is targeted at the cell surface for its physiological function. The FEBS journal 276:5432–5446. doi:10.1111/j.1742-4658.2009.07227.x
Herdeiro RS, Pereira MD, Panek AD, Eleutherio EC (2006) Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochim Biophys Acta 1760:340–346. doi:10.1016/j.bbagen.2006.01.010
Hino A, Mihara K, Nakashima K, Takano H (1990) Trehalose levels and survival ratio of freeze-tolerant versus freeze-sensitive yeasts. Appl Environ Microbiol 56:1386–1391
Hottiger T, Schmutz P, Wiemken A (1987) Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol 169:5518–5522
Huang J, Reggiori F, Klionsky DJ (2007) The transmembrane domain of acid trehalase mediates ubiquitin-independent multivesicular body pathway sorting. Mol Biol Cell 18:2511–2524. doi:10.1091/mbc.E06-11-0995
Magalhães R, De Mesquita JF, Eleutherio ECA (2014) Study of effects from deletion of agt1 and ath1 upon thermal stress in Saccharomyces cerevisiae. Paper presented at the ChemRio, Rio de Janeiro
Jules M, Beltran G, Francois J, Parrou JL (2008) New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals Ath1p-dependent trehalose mobilization. Appl Environ Microbiol 74:605–614. doi:10.1128/AEM.00557-07
Kaasen I, Falkenberg P, Styrvold OB, Strom AR (1992) Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by katF (AppR). J Bacteriol 174:889–898
Kaasen I, McDougall J, Strøm AR (1994) Analysis of the otsBA operon for osmoregulatory trehalose synthesis in Escherichia coli and homology of the OtsA and OtsB proteins to the yeast trehalose-6-phosphate synthase/phosphatase complex. Gene 145:9–15. doi:10.1016/0378-1119(94)90316-6
Kikawada T et al (2007) Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells. Proc Natl Acad Sci 104:11585–11590. doi:10.1073/pnas.0702538104
Kim J, Alizadeh P, Harding T, Hefner-Gravink A, Klionsky DJ (1996) Disruption of the yeast ATH1 gene confers better survival after dehydration, freezing, and ethanol shock: potential commercial applications. Appl Environ Microbiol 62:1563–1569
Kitahara AK, Suzuki Y, Zhan CW, Wada H, Nishimura Y (1998) Evaluation of new improved solution containing trehalose in free skin flap storage. Br J Plast Surg 51:118–121
Li C, Du Q, Deng W, Xie J (2012) The biology of Mycobacterium cord factor and roles in pathogen–host interaction. Crit Rev Eukaryot Gene Expr 22:289–297
Lillie SH, Pringle JR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143:1384–1394
Londesborough J, Vuorio OE (1993) Purification of trehalose synthase from baker’s yeast. Its temperature-dependent activation by fructose 6-phosphate and inhibition by phosphate. Eur J Biochem 216:841–848
Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J. n/a-n/a. doi:10.1111/tpj.12509
Macakova E et al (2013) Structural basis of the 14-3-3 protein-dependent activation of yeast neutral trehalase Nth1. Biochim Biophys Acta 1830:4491–4499. doi:10.1016/j.bbagen.2013.05.025
Maidan MM, De Rop L, Relloso M, Diez-Orejas R, Thevelein JM, Van Dijck P (2008) Combined inactivation of the Candida albicans GPR1 and TPS2 genes results in avirulence in a mouse model for systemic infection. Infect Immun 76:1686–1694. doi:10.1128/IAI.01497-07
Mansure JJ, Panek AD, Crowe LM, Crowe JH (1994) Trehalose inhibits ethanol effects on intact yeast cells and liposomes. Biochim Biophys Acta 1191:309–316
Maruta K, Hattori K, Nakada T, Kubota M, Sugimoto T, Kurimoto M (1996a) Cloning and sequencing of trehalose biosynthesis genes from Rhizobium sp. M-11. Biosci Biotechnol Biochem 60:717–720
Maruta K et al (1996b) Cloning and sequencing of a cluster of genes encoding novel enzymes of trehalose biosynthesis from thermophilic archaebacterium Sulfolobus acidocaldarius. Biochim Biophys Acta 1291:177–181
Matsuo T (2001) Trehalose protects corneal epithelial cells from death by drying. Br J Ophthalmol 85:610–612
McDougall J, Kaasen I, Strom AR (1993) A yeast gene for trehalose-6-phosphate synthase and its complementation of an Escherichia coli otsA mutant. FEMS Microbiol Lett 107:25–30
Murphy HN et al (2005) The OtsAB pathway is essential for trehalose biosynthesis in Mycobacterium tuberculosis. J Biol Chem 280:14524–14529. doi:10.1074/jbc.M414232200
Ngamskulrungroj P et al (2009) The trehalose synthesis pathway is an integral part of the virulence composite for Cryptococcus gattii. Infect Immun 77:4584–4596. doi:10.1128/IAI.00565-09
Nishimoto T, Nakano M, Ikegami S, Chaen H, Fukuda S, Sugimoto T, Kurimoto M (1995) Existence of a novel enzyme converting maltose into trehalose. Biosci Biotech Biochem 59:2189–2190
Nishimoto T et al (1996) Purification and properties of a novel enzyme, trehalose synthase, from Pimelobacter sp. R48. Biosci Biotechnol Biochem 60:640–644
Norcia MA (2000) Compositions and methods for wound management. Office Gazette US Pat Trademark Office 1232:424-448
Noubhani A, Bunoust O, Rigoulet M, Thevelein JM (2000) Reconstitution of ethanolic fermentation in permeabilized spheroplasts of wild-type and trehalose-6-phosphate synthase mutants of the yeast Saccharomyces cerevisiae. Eur J Biochem 267:4566–4576
Nwaka S, Holzer H (1998) Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Prog Nucleic Acid Res Mol Biol 58:197–237
Nwaka S, Kopp M, Holzer H (1995a) Expression and function of the trehalase genes NTH1 and YBR0106 in Saccharomyces cerevisiae. J Biol Chem 270:10193–10198
Nwaka S, Mechler B, Destruelle M, Holzer H (1995b) Phenotypic features of trehalase mutants in Saccharomyces cerevisiae. FEBS Lett 360:286–290
Nwaka S, Mechler B, Holzer H (1996) Deletion of the ATH1 gene in Saccharomyces cerevisiae prevents growth on trehalose. FEBS Lett 386:235–238
Ohtake S, Wang YJ (2011) Trehalose: current use and future applications. J Pharm Sci 100:2020–2053. doi:10.1002/jps.22458
Ortiz CH, Maia JC, Tenan MN, Braz-Padrao GR, Mattoon JR, Panek AD (1983) Regulation of yeast trehalase by a monocyclic, cyclic AMP-dependent phosphorylation–dephosphorylation cascade system. J Bacteriol 153:644–651
Panek A (1963) Function of trehalose in Baker’s yeast (Saccharomyces cerevisiae). Arch Biochem Biophys 100:422–425. doi:10.1016/0003-9861(63)90107-3
Panek AC, de Araujo PS, Moura Neto V, Panek AD (1987) Regulation of the trehalose-6-phosphate synthase complex in Saccharomyces. I. Interconversion of forms by phosphorylation. Curr Genet 11:459–465
Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441. doi:10.1146/annurev.arplant.59.032607.092945
Pellny TK et al (2004) Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. Plant Biotechnol J 2:71–82. doi:10.1111/j.1467-7652.2004.00053.x
Pereira Ede J, Panek AD, Eleutherio EC (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperones 8:120–124
Petzold EW et al (2006) Characterization and regulation of the trehalose synthesis pathway and its importance in the pathogenicity of Cryptococcus neoformans. Infect Immun 74:5877–5887. doi:10.1128/IAI.00624-06
Plourde-Owobi L, Durner S, Parrou JL, Wieczorke R, Goma G, Francois J (1999) AGT1, encoding an alpha-glucoside transporter involved in uptake and intracellular accumulation of trehalose in Saccharomyces cerevisiae. J Bacteriol 181:3830–3832
Ratnakumar S et al (2011) Phenomic and transcriptomic analyses reveal that autophagy plays a major role in desiccation tolerance in Saccharomyces cerevisiae. Mol BioSyst 7:139–149. doi:10.1039/c0mb00114g
Reinders A, Burckert N, Hohmann S, Thevelein JM, Boller T, Wiemken A, De Virgilio C (1997) Structural analysis of the subunits of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae and their function during heat shock. Mol Microbiol 24:687–695
Ren Y, Dai X, Zhou J, Liu J, Pei H, Xiang H (2005) Gene expression and molecular characterization of a thermostable trehalose phosphorylase from Thermoanaerobacter tengcongensis. Sci China C Life Sci 48:221–227
Schepers W, Van Zeebroeck G, Pinkse M, Verhaert P, Thevelein JM (2012) In vivo phosphorylation of Ser21 and Ser83 during nutrient-induced activation of the yeast protein kinase A (PKA) target trehalase. J Biol Chem 287:44130–44142. doi:10.1074/jbc.M112.421503
Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6849–6854. doi:10.1073/pnas.1132018100
Schwarz A, Goedl C, Minani A, Nidetzky B (2007) Trehalose phosphorylase from Pleurotus ostreatus: characterization and stabilization by covalent modification, and application for the synthesis of alpha, alpha-trehalose. J Biotechnol 129:140–150. doi:10.1016/j.jbiotec.2006.11.022
Shi L et al (2013) Biochemical characterization and ligand-binding properties of trehalose-6-phosphate phosphatase from Mycobacterium tuberculosis. Acta Biochim Biophys Sin (Shanghai) 45:837–844. doi:10.1093/abbs/gmt084
Shima J et al (1999) Stress tolerance in doughs of Saccharomyces cerevisiae trehalase mutants derived from commercial Baker’s yeast. Appl Environ Microbiol 65:2841–2846
Singer MA, Lindquist S (1998a) Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1:639–648
Singer MA, Lindquist S (1998b) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16:460–468
Souza AC, De Mesquita JF, Panek AD, Silva JT, Paschoalin VM (2002) Evidence for a modulation of neutral trehalase activity by Ca2+ and cAMP signaling pathways in Saccharomyces cerevisiae. Braz J Med Biol Res 35:11–16
Stambuk BU, de Araujo PS (2001) Kinetics of active alpha-glucoside transport in Saccharomyces cerevisiae. FEMS Yeast Res 1:73–78
Stambuk BU, Panek AD, Crowe JH, Crowe LM, de Araujo PS (1998) Expression of high-affinity trehalose-H + symport in Saccharomyces cerevisiae. Biochim Biophys Acta 1379:118–128
Stark C et al (2010) PhosphoGRID: a database of experimentally verified in vivo protein phosphorylation sites from the budding yeast Saccharomyces cerevisiae. Database (Oxford) bap026. doi:10.1093/database/bap026
Thevelein JM (1984) Regulation of trehalose mobilization in fungi. Microbiol Rev 48:42–59
Thevelein JM, de Winde JH (1999) Novel sensing mechanisms and targets for the cAMP-protein kinase a pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 33:904–918
Thevelein JM, Hohmann S (1995) Trehalose synthase: guard to the gate of glycolysis in yeast? Trends Biochem Sci 20:3–10
Trevisol ET, Panek AD, Mannarino SC, Eleutherio EC (2011) The effect of trehalose on the fermentation performance of aged cells of Saccharomyces cerevisiae. Appl Microbiol Biotechnol 90:697–704. doi:10.1007/s00253-010-3053-x
Trevisol ET, Panek AD, De Mesquita JF, Eleutherio EC (2014) Regulation of the yeast trehalose-synthase complex by cyclic AMP-dependent phosphorylation. Biochim Biophys Acta 1840:1646–1650. doi:10.1016/j.bbagen.2013.12.010
Van Dijck P, De Rop L, Szlufcik K, Van Ael E, Thevelein JM (2002) Disruption of the Candida albicans TPS2 gene encoding trehalose-6-phosphate phosphatase decreases infectivity without affecting hypha formation. Infect Immun 70:1772–1782
Vandercammen A, Francois J, Hers HG (1989) Characterization of trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase of Saccharomyces cerevisiae. Eur J Biochem 182:613–620
Veisova D et al (2012) Role of individual phosphorylation sites for the 14-3-3-protein-dependent activation of yeast neutral trehalase Nth1. Biochem J 443:663–670. doi:10.1042/BJ20111615
Vidgren V, Kankainen M, Londesborough J, Ruohonen L (2011) Identification of regulatory elements in the AGT1 promoter of ale and lager strains of brewer’s yeast. Yeast 28:579–594. doi:10.1002/yea.1888
Vuorio OE, Kalkkinen N, Londesborough J (1993) Cloning of two related genes encoding the 56- and 123-kDa subunits of trehalose synthase from the yeast Saccharomyces cerevisiae. Eur J Biochem 216:849–861
Wannet WJ, Op den Camp HJ, Wisselink HW, van der Drift C, Van Griensven LJ, Vogels GD (1998) Purification and characterization of trehalose phosphorylase from the commercial mushroom Agaricus bisporus. Biochim Biophys Acta 1425:177–188
Winderickx J, de Winde JH, Crauwels M, Hino A, Hohmann S, Van Dijck P, Thevelein JM (1996) Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control? Mol Gen Genet 252:470–482
Womersley C (1981) A micromethod for the extraction and quantitative analysis of “free” carbohydrates in nematode tissue. Anal Biochem 112:182–189
Zahringer H, Thevelein JM, Nwaka S (2000) Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: variations of PKA effect during stress and growth. Mol Microbiol 35:397–406
Zaragoza O, Blazquez MA, Gancedo C (1998) Disruption of the Candida albicans TPS1 gene encoding trehalose-6-phosphate synthase impairs formation of hyphae and decreases infectivity. J Bacteriol 180:3809–3815
Zaragoza O, de Virgilio C, Ponton J, Gancedo C (2002) Disruption in Candida albicans of the TPS2 gene encoding trehalose-6-phosphate phosphatase affects cell integrity and decreases infectivity. Microbiology 148:1281–1290
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This work was supported by grants from FAPERJ, CAPES and CNPq. This review article was supported in part by a grant from São Paulo Research Foundation (FAPESP) of Brazil # 2014/01229-4.
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Communicated by D.E.N. Rangel.
This article is part of the Special Issue “Fungal Stress Responses”.
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Eleutherio, E., Panek, A., De Mesquita, J.F. et al. Revisiting yeast trehalose metabolism. Curr Genet 61, 263–274 (2015). https://doi.org/10.1007/s00294-014-0450-1
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DOI: https://doi.org/10.1007/s00294-014-0450-1