Flux through trehalose synthase flows from trehalose to the alpha anomer of maltose in mycobacteria

Chemistry and Biology

Volumn 20, Issue 4, 2013, Pages 487-493

  Miah, Farzana ^a   Koliwer Brandl, Hendrik ^b   Rejzek, Martin ^a   Field, Robert A ^a   Kalscheuer, Rainer ^b   Bornemann, Stephen ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MALTOSE; TREHALOSE; TREHALOSE SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; CARBOHYDRATE SYNTHESIS; FLUORINE NUCLEAR MAGNETIC RESONANCE; GENE DELETION; MYCOBACTERIUM; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE;

CELL WALL; GLUCOSYLTRANSFERASES; MAGNETIC RESONANCE SPECTROSCOPY; MALTOSE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORIC MONOESTER HYDROLASES; TREHALOSE;

CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 84876459348     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.02.014     Document Type: Article

References (41)

1. J.C. Argüelles Physiological roles of trehalose in bacteria and yeasts: a comparative analysis Arch. Microbiol. 174 2000 217 224
2. N. Avonce, A. Mendoza-Vargas, E. Morett, and G. Iturriaga Insights on the evolution of trehalose biosynthesis BMC Evol. Biol. 6 2006 109 10.1186/1471-2148-1186-1109
3. K.M. Backus, H.I. Boshoff, C.S. Barry, O. Boutureira, M.K. Patel, F. D'Hooge, S.S. Lee, L.E. Via, K. Tahlan, C.E. Barry 3rd, and B.G. Davis Uptake of unnatural trehalose analogs as a reporter for Mycobacterium tuberculosis Nat. Chem. Biol. 7 2011 228 235
4. J.M. Bailey, P.H. Fishman, and P.G. Pentchev Studies on mutarotases. I. Purification and properties of a mutarotase from higher plants J. Biol. Chem. 242 1967 4263 4269
5. B.L. Cantarel, P.M. Coutinho, C. Rancurel, T. Bernard, V. Lombard, and B. Henrissat The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Nucleic Acids Res. 37 Database issue 2009 D233 D238
6. J.D. Carroll, I. Pastuszak, V.K. Edavana, Y.T. Pan, and A.D. Elbein A novel trehalase from Mycobacterium smegmatis - purification, properties, requirements FEBS J. 274 2007 1701 1714
7. G. Chandra, K.F. Chater, and S. Bornemann Unexpected and widespread connections between bacterial glycogen and trehalose metabolism Microbiology 157 2011 1565 1572
8. K.A.L. De Smet, A. Weston, I.N. Brown, D.B. Young, and B.D. Robertson Three pathways for trehalose biosynthesis in mycobacteria Microbiology 146 2000 199 208
9. A. Drepper, R. Peitzmann, and H. Pape Maltokinase (ATP:maltose 1-phosphotransferase) from Actinoplanes sp.: demonstration of enzyme activity and characterization of the reaction product FEBS Lett. 388 1996 177 179
10. C. Dye Global epidemiology of tuberculosis Lancet 367 2006 938 940
11. A.D. Elbein, Y.T. Pan, I. Pastuszak, and D. Carroll New insights on trehalose: a multifunctional molecule Glycobiology 13 2003 17R 27R
12. A.D. Elbein, I. Pastuszak, A.J. Tackett, T. Wilson, and Y.T. Pan Last step in the conversion of trehalose to glycogen: a mycobacterial enzyme that transfers maltose from maltose 1-phosphate to glycogen J. Biol. Chem. 285 2010 9803 9812
13. S. Hoops, S. Sahle, R. Gauges, C. Lee, J. Pahle, N. Simus, M. Singhal, L. Xu, P. Mendes, and U. Kummer COPASI - a COmplex PAthway SImulator Bioinformatics 22 2006 3067 3074
14. R. Kalscheuer, and W.R. Jacobs Jr. The significance of GlgE as a new target for tuberculosis Drug News Perspect. 23 2010 619 624
15. R. Kalscheuer, B. Weinrick, U. Veeraraghavan, G.S. Besra, and W.R. Jacobs Jr. Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis Proc. Natl. Acad. Sci. USA 107 2010 21761 21766
16. R. Kalscheuer, K. Syson, U. Veeraraghavan, B. Weinrick, K.E. Biermann, Z. Liu, J.C. Sacchettini, G. Besra, S. Bornemann, and W.R. Jacobs Jr. Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an α-glucan pathway Nat. Chem. Biol. 6 2010 376 384
17. S. Koh, J. Kim, H.J. Shin, D. Lee, J. Bae, D. Kim, and D.S. Lee Mechanistic study of the intramolecular conversion of maltose to trehalose by Thermus caldophilus GK24 trehalose synthase Carbohydr. Res. 338 2003 1339 1343
18. F.L. Lin, H. van Halbeek, and C.R. Bertozzi Synthesis of mono- and dideoxygenated α,α-trehalose analogs Carbohydr. Res. 342 2007 2014 2030
19. V. Mendes, A. Maranha, P. Lamosa, M.S. da Costa, and N. Empadinhas Biochemical characterization of the maltokinase from Mycobacterium bovis BCG BMC Biochem. 11 2010 21 10.1186/1471-2091-1111-1121
20. H.N. Murphy, G.R. Stewart, V.V. Mischenko, A.S. Apt, R. Harris, M.S.B. McAlister, P.C. Driscoll, D.B. Young, and B.D. Robertson The OtsAB pathway is essential for trehalose biosynthesis in Mycobacterium tuberculosis J. Biol. Chem. 280 2005 14524 14529
21. T. Nishimoto, M. Nakano, S. Ikegami, H. Chaen, S. Fukuda, T. Sugimoto, M. Kurimoto, and Y. Tsujisaka Existence of a novel enzyme converting maltose into trehalose Biosci. Biotechnol. Biochem. 59 1995 2189 2190
22. T. Nishimoto, M. Nakano, T. Nakada, H. Chaen, S. Fukuda, T. Sugimoto, M. Kurimoto, and Y. Tsujisaka Purification and properties of a novel enzyme, trehalose synthase, from Pimelobacter sp. R48 Biosci. Biotechnol. Biochem. 60 1996 640 644
23. Y.T. Pan, V. Koroth Edavana, W.J. Jourdian, R. Edmondson, J.D. Carroll, I. Pastuszak, and A.D. Elbein Trehalose synthase of Mycobacterium smegmatis: purification, cloning, expression, and properties of the enzyme Eur. J. Biochem. 271 2004 4259 4269
24. M.J. Paul, L.F. Primavesi, D. Jhurreea, and Y.H. Zhang Trehalose metabolism and signaling Annu. Rev. Plant Biol. 59 2008 417 441
25. J.D. Rose, J.A. Maddry, R.N. Comber, W.J. Suling, L.N. Wilson, and R.C. Reynolds Synthesis and biological evaluation of trehalose analogs as potential inhibitors of mycobacterial cell wall biosynthesis Carbohydr. Res. 337 2002 105 120
26. T. Sambou, P. Dinadayala, G. Stadthagen, N. Barilone, Y. Bordat, P. Constant, F. Levillain, O. Neyrolles, B. Gicquel, and A. Lemassu Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: biosynthesis and impact on the persistence in mice Mol. Microbiol. 70 2008 762 774
27. Y. Shirokane, and M. Suzuki A novel enzyme, maltose 1-epimerase from Lactobacillus brevis IFO 3345 FEBS Lett. 367 1995 177 179
28. M.R. Stam, E.G.J. Danchin, C. Rancurel, P.M. Coutinho, and B. Henrissat Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of α-amylase-related proteins Protein Eng. Des. Sel. 19 2006 555 562
29. C.L.M. Stults, A.P. Wade, and S.R. Crouch Immobilized enzyme kinetic study of D-glucose mutarotation by flow injection analysis Anal. Chem. 59 1987 2245 2247
30. B.M. Swarts, C.M. Holsclaw, J.C. Jewett, M. Alber, D.M. Fox, M.S. Siegrist, J.A. Leary, R. Kalscheuer, and C.R. Bertozzi Probing the mycobacterial trehalome with bioorthogonal chemistry J. Am. Chem. Soc. 134 2012 16123 16126 10.1021/ja3062419
31. K. Syson, C.E. Stevenson, M. Rejzek, S.A. Fairhurst, A. Nair, C.J. Bruton, R.A. Field, K.F. Chater, D.M. Lawson, and S. Bornemann Structure of Streptomyces maltosyltransferase GlgE, a homologue of a genetically validated anti-tuberculosis target J. Biol. Chem. 286 2011 38298 38310
32. K. Takayama, C. Wang, and G.S. Besra Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis Clin. Microbiol. Rev. 18 2005 81 101
33. K. Tantanarat, M. Rejzek, E. O'Neill, C. Ruzanski, L. Hill, S.A. Fairhurst, T. Limpaseni, and R.A. Field An expedient enzymatic route to isomeric 2-, 3- and 6-monodeoxy-monofluoro-maltose derivatives Carbohydr. Res. 358 2012 12 18
34. Y.B. Tewari, and R.N. Goldberg Thermodynamics of hydrolysis of disaccharides. Lactulose, alpha-D-melibiose, palatinose, D-trehalose, D-turanose and 3-o-beta-D-galactopyranosyl-D-arabinose Biophys. Chem. 40 1991 59 67
35. Y.B. Tewari, B.E. Lang, S.R. Decker, and R.N. Goldberg Thermodynamics of the hydrolysis reactions of 1,4-β-d-xylobiose, 1,4-β-d-xylotriose, d-cellobiose and d-maltose J. Chem. Thermodyn. 40 2008 1517 1526
36. M. Tzvetkov, C. Klopprogge, O. Zelder, and W. Liebl Genetic dissection of trehalose biosynthesis in Corynebacterium glutamicum: inactivation of trehalose production leads to impaired growth and an altered cell wall lipid composition Microbiology 149 2003 1659 1673
37. J. Wang, B. Elchert, Y. Hui, J.Y. Takemoto, M. Bensaci, J. Wennergren, H. Chang, R. Rai, and C.W.T. Chang Synthesis of trehalose-based compounds and their inhibitory activities against Mycobacterium smegmatis Bioorg. Med. Chem. 12 2004 6397 6413
38. S.G. Withers, K. Rupitz, and I.P. Street 2-Deoxy-2-fluoro-D-glycosyl fluorides. A new class of specific mechanism-based glycosidase inhibitors J. Biol. Chem. 263 1988 7929 7932
39. A. Wolf, R. Krämer, and S. Morbach Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress Mol. Microbiol. 49 2003 1119 1134
40. P.J. Woodruff, B.L. Carlson, B. Siridechadilok, M.R. Pratt, R.H. Senaratne, J.D. Mougous, L.W. Riley, S.J. Williams, and C.R. Bertozzi Trehalose is required for growth of Mycobacterium smegmatis J. Biol. Chem. 279 2004 28835 28843
41. R. Zhang, Y.T. Pan, S.M. He, M. Lam, G.D. Brayer, A.D. Elbein, and S.G. Withers Mechanistic analysis of trehalose synthase from Mycobacterium smegmatis J. Biol. Chem. 286 2011 35601 35609