5,076
Views
45
CrossRef citations to date
0
Altmetric
Review article

Trehalose and bacterial virulence

ORCID Icon & ORCID Icon
Pages 1192-1202 | Received 03 Apr 2020, Accepted 08 Aug 2020, Published online: 30 Aug 2020

References

  • Richards AB, Krakowka S, Dexter LB, et al. Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem Toxicol. 2002;40:871–898.
  • Furuki T, Oku K, Sakurai M. Thermodynamic, hydration and structural characteristics of alpha,alpha-trehalose. Front Biosci. 2009;14:3523–3535.
  • Elbein AD, Pan YT, Pastuszak I, et al. New insights on trehalose: a multifunctional molecule. Glycobiology. 2003;13:17R–27R.
  • Arguelles JC. Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol. 2000;174:217–224.
  • Wyatt GR, Kale GF. The chemistry of insect hemolymph. II. Trehalose and other carbohydrates. J Gen Physiol. 1957;40:833–847.
  • Muller J, Aeschbacher RA, Wingler A, et al. Trehalose and trehalase in Arabidopsis. Plant Physiol. 2001;125:1086–1093.
  • Iturriaga G, Suarez R, Nova-Franco B. Trehalose metabolism: from osmoprotection to signaling. Int J Mol Sci. 2009;10:3793–3810.
  • Tournu H, Fiori A, Van Dijck P. Relevance of trehalose in pathogenicity: some general rules, yet many exceptions. PLoS Pathog. 2013;9(8):e1003447.
  • Avonce N, Mendoza-Vargas A, Morett E, et al. Insights on the evolution of trehalose biosynthesis. BMC Evol Biol. 2006;6:109.
  • Strom AR, Kaasen I. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol Microbiol. 1993;8:205–210.
  • McIntyre HJ, Davies H, Hore TA, et al. Trehalose biosynthesis in Rhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. Appl Environ Microbiol. 2007;73:3984–3992.
  • Kandror O, DeLeon A, Goldberg AL. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA. 2002;99:9727–9732.
  • Harty CE, Martins D, Doing G, et al. Ethanol stimulates trehalose production through a SpoT-DksA-AlgU-dependent pathway in Pseudomonas aeruginosa. J Bacteriol. 2019;201:e00794–18.
  • Klein W, Horlacher R, Boos W. Molecular analysis of treB encoding the Escherichia coli enzyme II specific for trehalose. J Bacteriol. 1995;177:4043–4052.
  • Horlacher R, Boos W. Characterization of TreR, the major regulator of the Escherichia coli trehalose system. J Biol Chem. 1997;272:13026–13032.
  • Uhland K, Mondigler M, Spiess C, et al. Determinants of translocation and folding of TreF, a trehalase of Escherichia coli. J Biol Chem. 2000;275:23439–23445.
  • Horlacher R, Uhland K, Klein W, et al. Characterization of a cytoplasmic trehalase of Escherichia coli. J Bacteriol. 1996;178:6250–6257.
  • Sakaguchi M. Diverse and common features of trehalases and their contributions to microbial trehalose metabolism. Appl Microbiol Biotechnol. 2020;104:1837–1847.
  • Helfert C, Gotsche S, Dahl MK. Cleavage of trehalose-phosphate in Bacillus subtilis is catalysed by a phospho-alpha-(1-1)-glucosidase encoded by the treA gene. Mol Microbiol. 1995;16:111–120.
  • Schock F, Dahl MK. Expression of the tre operon of Bacillus subtilis 168 is regulated by the repressor TreR. J Bacteriol. 1996;178:4576–4581.
  • Baker JL, Lindsay EL, Faustoferri RC, et al. Characterization of the trehalose utilization operon in Streptococcus mutans reveals that the TreR transcriptional regulator is involved in stress response pathways and toxin production. J Bacteriol. 2018;200:e00057–18.
  • Matthijs S, Koedam N, Cornelis P, et al. The trehalose operon of Pseudomonas fluorescens ATCC 17400. Res Microbiol. 2000;151:845–851.
  • Rhoades ER, Streeter C, Turk J, et al. Characterization of sulfolipids of Mycobacterium tuberculosis H37Rv by multiple-stage linear ion-trap high-resolution mass spectrometry with electrospray ionization reveals that the family of sulfolipid II predominates. Biochemistry. 2011;50:9135–9147.
  • Kalscheuer R, Koliwer-Brandl H. Genetics of mycobacterial trehalose metabolism. Microbiol Spectr. 2014;2. DOI:https://doi.org/10.1128/microbiolspec.MGM2-0002-2013
  • Thanna S, Sucheck SJ. Targeting the trehalose utilization pathways of Mycobacterium tuberculosis. Medchemcomm. 2016;7:69–85.
  • Kalscheuer R, Syson K, Veeraraghavan U, et al. Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an alpha-glucan pathway. Nat Chem Biol. 2010;6:376–384.
  • Ghazaei C. Mycobacterium tuberculosis and lipids: insights into molecular mechanisms from persistence to virulence. J Res Med Sci. 2018;23:63.
  • Lederer E. Cord factor and related trehalose esters. Chem Phys Lipids. 1976;16:91–106.
  • Spargo BJ, Crowe LM, Ioneda T, et al. Cord factor (alpha,alpha-trehalose 6,6ʹ-dimycolate) inhibits fusion between phospholipid vesicles. Proc Natl Acad Sci USA. 1991;88:737–740.
  • Brennan PJ, Nikaido H. The envelope of mycobacteria. Annu Rev Biochem. 1995;64:29–63.
  • Reinink P, Buter J, Mishra VK, et al. Discovery of Salmonella trehalose phospholipids reveals functional convergence with mycobacteria. J Exp Med. 2019;216:757–771.
  • McBride MJ, Ensign JC. Effects of intracellular trehalose content on Streptomyces griseus spores. J Bacteriol. 1987;169:4995–5001.
  • Zeidler S, Hubloher J, Schabacker K, et al. Trehalose, a temperature- and salt-induced solute with implications in pathobiology of Acinetobacter baumannii. Environ Microbiol. 2017;19:5088–5099.
  • Hengge-Aronis R, Klein W, Lange R, et al. Trehalose synthesis genes are controlled by the putative sigma factor encoded by RpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol. 1991;173:7918–7924.
  • Howells AM, Bullifent HL, Dhaliwal K, et al. Role of trehalose biosynthesis in environmental survival and virulence of Salmonella enterica serovar Typhimurium. Res Microbiol. 2002;153:281–287.
  • Reina-Bueno M, Argandona M, Nieto JJ, et al. Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli. BMC Microbiol. 2012;12:207.
  • Ells TC, Truelstrup Hansen L. Increased Thermal and Osmotic Stress Resistance in Listeria monocytogenes 568 Grown in the Presence of Trehalose Due to Inactivation of the Phosphotrehalase-Encoding Gene treA. Appl Environ Microbiol. 2011;77(19):6841–6851.
  • Vanaporn M, Sarkar-Tyson M, Kovacs-Simon A, et al. Trehalase plays a role in macrophage colonization and virulence of Burkholderia pseudomallei in insect and mammalian hosts. Virulence. 2017;8:30–40.
  • Welsh DT, Herbert RA. Osmotically induced intracellular trehalose, but not glycine betaine accumulation promotes desiccation tolerance in Escherichia coli. FEMS Microbiol Lett. 1999;174:57–63.
  • Potts M. Desiccation tolerance of prokaryotes. Microbiol Rev. 1994;58:755–805.
  • Harland CW, Rabuka D, Bertozzi CR, et al. The Mycobacterium tuberculosis virulence factor trehalose dimycolate imparts desiccation resistance to model mycobacterial membranes. Biophys J. 2008;94:4718–4724.
  • Piazza A, Zimaro T, Garavaglia BS, et al. The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses. J Exp Bot. 2015;66:2795–2811.
  • Jain NK, Roy I. Effect of trehalose on protein structure. Protein Sci. 2009;18:24–36.
  • Moruno Algara M, Kuczynska-Wisnik D, Debski J, et al. Trehalose protects Escherichia coli against carbon stress manifested by protein acetylation and aggregation. Mol Microbiol. 2019;112:866–880.
  • Jensen JB, Ampomah OY, Darrah R, et al. Role of trehalose transport and utilization in Sinorhizobium meliloti–alfalfa interactions. Mol Plant Microbe Interact. 2005;18:694–702.
  • Sugawara M, Cytryn EJ, Sadowsky MJ. Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol. 2010;76:1071–1081.
  • MacIntyre AM, Barth JX, Scarlett CO, et al. Trehalose synthesis contributes to osmotic stress tolerance and virulence of the bacterial wilt pathogen Ralstonia solanacearum. Mol Plant Microbe Interact. 2019;33:462–473.
  • Pavanelo DB, Houle S, Matter LB, et al. The periplasmic trehalase affects type 1 fimbria production and virulence of extraintestinal pathogenic Escherichia coli strain mt78. Infect Immun. 2018;86:e00241–18.
  • Chouikha I, Germon P, Bree A, et al. A selC-associated genomic island of the extraintestinal avian pathogenic Escherichia coli strain BEN2908 is involved in carbohydrate uptake and virulence. J Bacteriol. 2006;188:977–987.
  • Collins J, Robinson C, Danhof H, et al. Dietary trehalose enhances virulence of epidemic Clostridium difficile. Nature. 2018;553:291–294.
  • Collins J, Danhof H, Britton RA. The role of trehalose in the global spread of epidemic Clostridium difficile. Gut Microbes. 2019;10:204–209.
  • Zhang Y, Shaikh N, Ferey JL, et al. Lactotrehalose, an analog of trehalose, increases energy metabolism without promoting Clostridioides difficile infection in mice. Gastroenterology. 2020;158:1402–16.e2.
  • Decker K, Gerhardt F, Boos W. The role of the trehalose system in regulating the maltose regulon of Escherichia coli. Mol Microbiol. 1999;32:777–788.
  • Steen JA, Bohlke N, Vickers CE, et al. The trehalose phosphotransferase system (PTS) in E. coli W can transport low levels of sucrose that are sufficient to facilitate induction of the csc sucrose catabolism operon. PloS One. 2014;9:e88688.
  • Djonovic S, Urbach JM, Drenkard E, et al. Trehalose biosynthesis promotes Pseudomonas aeruginosa pathogenicity in plants. PLoS Pathog. 2013;9:e1003217.
  • Hunter RL, Olsen M, Jagannath C, et al. Trehalose 6,6ʹ-dimycolate and lipid in the pathogenesis of caseating granulomas of tuberculosis in mice. Am J Pathol. 2006;168:1249–1261.
  • Hunter RL, Hwang SA, Jagannath C, et al. Cord factor as an invisibility cloak? A hypothesis for asymptomatic TB persistence. Tuberculosis. 2016;101s:S2–s8.
  • Bowdish DM, Sakamoto K, Kim MJ, et al. MARCO, TLR2, and CD14 are required for macrophage cytokine responses to mycobacterial trehalose dimycolate and Mycobacterium tuberculosis. PLoS Pathog. 2009;5:e1000474.
  • Donnachie E, Fedotova EP, Hwang SA. Trehalose 6,6-dimycolate from Mycobacterium tuberculosisinduces hypercoagulation. Am J Pathol. 2016;186:1221–1233.
  • Ishikawa E, Ishikawa T, Morita YS, et al. Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med. 2009;206:2879–2888.
  • Zhao XQ, Zhu LL, Chang Q, et al. C-type lectin receptor dectin-3 mediates trehalose 6,6ʹ-dimycolate (TDM)-induced Mincle expression through CARD9/Bcl10/MALT1-dependent nuclear factor (NF)-kappaB activation. J Biol Chem. 2014;289:30052–30062.
  • Decout A, Silva-Gomes S, Drocourt D, et al. Rational design of adjuvants targeting the C-type lectin Mincle. Proc Natl Acad Sci USA. 2017;114:2675–2680.
  • Lima VM, Bonato VL, Lima KM, et al. Role of trehalose dimycolate in recruitment of cells and modulation of production of cytokines and NO in tuberculosis. Infect Immun. 2001;69:5305–5312.
  • Korte J, Alber M, Trujillo CM, et al. Trehalose-6-phosphate-mediated toxicity determines essentiality of otsb2 in Mycobacterium tuberculosisin vitro and in mice. PLoS Pathog. 2016;12:e1006043.
  • Murphy HN, Stewart GR, Mischenko VV, et al. The OtsAB pathway is essential for trehalose biosynthesis in Mycobacterium tuberculosis. J Biol Chem. 2005;280:14524–14529.
  • Blazquez MA, Lagunas R, Gancedo C, et al. Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEBS Lett. 1993;329:51–54.
  • Perfect JR, Tenor JL, Miao Y, et al. Trehalose pathway as an antifungal target. Virulence. 2017;8:143–149.
  • Arguelles J-C. Trehalose as antifungal target: the picture is still incomplete. Virulence. 2017;8(2):237–238.
  • Thammahong A, Puttikamonkul S, Perfect JR, et al. Central role of the trehalose biosynthesis pathway in the pathogenesis of human fungal infections: opportunities and challenges for therapeutic development. Microbiol Mol Biol Rev. 2017;81:e00053–16.
  • Guirao-Abad JP, Sanchez-Fresneda R, Valentin E, et al. Analysis of validamycin as a potential antifungal compound against Candida albicans. Int Microbiol. 2013;16:217–225.
  • Karlinsey JE, Stepien TA, Mayho M, et al. Genome-wide analysis of Salmonella enterica serovar Typhi in humanized mice reveals key virulence features. Cell Host Microbe. 2019;26:426–34.e6.
  • Moule MG, Spink N, Willcocks S, et al. Characterization of new virulence factors involved in the intracellular growth and survival of Burkholderia pseudomallei. Infect Immun. 2015;84:701–710.
  • Moule MG, Hemsley CM, Seet Q, et al. Genome-wide saturation mutagenesis of Burkholderia pseudomallei K96243 predicts essential genes and novel targets for antimicrobial development. mBio. 2014;5:e00926–13.
  • Cross M, Rajan S, Chekaiban J, et al. Enzyme characteristics of pathogen-specific trehalose-6-phosphate phosphatases. Sci Rep. 2017;7:2015.
  • Cross M, Biberacher S, Park SY, et al. Trehalose 6-phosphate phosphatases of Pseudomonas aeruginosa. Faseb J. 2018;32:5470–5482.
  • Pan YT, Elbein AD. Inhibition of the trehalose-P synthase of mycobacteria by various antibiotics. Arch Biochem Biophys. 1996;335:258–266.
  • Kapil S, Petit C, Drago VN, et al. Synthesis and in Vitro Characterization of trehalose-based Inhibitors of mycobacterial trehalose 6-phosphate phosphatases. Chembiochem. 2019;20:260–269.
  • Danielson ND, Collins J, Stothard AI, et al. Degradation-resistant trehalose analogues block utilization of trehalose by hypervirulent Clostridioides difficile. Chem Commun. 2019;55:5009–5012.
  • Veleti SK, Lindenberger JJ, Ronning DR, et al. Synthesis of a C-phosphonate mimic of maltose-1-phosphate and inhibition studies on Mycobacterium tuberculosis GlgE. Bioorg Med Chem. 2014;22:1404–1411.
  • Dupont C, Chen Y, Xu Z, et al. A piperidinol-containing molecule is active against Mycobacterium tuberculosis by inhibiting the mycolic acid flippase activity of MmpL3. J Biol Chem. 2019;294:17512–17523.
  • Wilson R, Kumar P, Parashar V, et al. Antituberculosis thiophenes define a requirement for Pks13 in mycolic acid biosynthesis. Nat Chem Biol. 2013;9:499–506.
  • Feinberg H, Rambaruth ND, Jegouzo SA, et al. Binding sites for acylated trehalose analogs of glycolipid ligands on an extended carbohydrate recognition domain of the macrophage receptor Mincle. J Biol Chem. 2016;291:21222–21233.
  • Izutsu KI. Applications of freezing and freeze-drying in pharmaceutical formulations. Adv Exp Med Biol. 2018;1081:371–383.
  • Oslan SNH, Halim M, Ramle NA, et al. Improved stability of live attenuated vaccine gdhA derivative Pasteurella multocida B:2 by freeze drying method for use as animal vaccine. Cryobiology. 2017;79:1–8.
  • Lal M, Priddy S, Bourgeois L, et al. Development of a fast-dissolving tablet formulation of a live attenuated enterotoxigenic E. coli vaccine candidate. Vaccine. 2013;31(42):4759–4764.
  • Ohtake S, Martin RA, Saxena A, et al. Formulation and stabilization of Francisella tularensis live vaccine strain. J Pharm Sci. 2011;100(8):3076–3087.
  • Ohtake S, Martin R, Saxena A, et al. Room temperature stabilization of oral, live attenuated Salmonella enterica serovar Typhi-vectored vaccines. Vaccine. 2011;29:2761–2771.
  • Edwards AD, Slater NK. Formulation of a live bacterial vaccine for stable room temperature storage results in loss of acid, bile and bile salt resistance. Vaccine. 2008;26:5675–5678.
  • Bullifent HL, Dhaliwal K, Howells AM, et al. Stabilisation of Salmonella vaccine vectors by the induction of trehalose biosynthesis. Vaccine. 2000;19:1239–1245.