Octanoylation of early intermediates of mycobacterial methylglucose lipopolysaccharides

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Maranha, Ana ^a   Moynihan, Patrick J ^b,g   Miranda, Vanessa ^c   Correia Lourenço, Eva ^c   Nunes Costa, Daniela ^a   Fraga, Joana S ^d,e   Jose Barbosa Pereira, Pedro ^d,e   MacEdo Ribeiro, Sandra ^d,e   Ventura, M Rita ^c   Clarke, Anthony J ^b   Empadinhas, Nuno ^a,f  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF GUELPH   (Canada)

^c UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

^e UNIVERSITY OF PORTO   (Portugal)

^f UNIVERSITY OF COIMBRA   (Portugal)

^g UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FATTY ACID; GLYCOSYLTRANSFERASE; LIPOPOLYSACCHARIDE; RECOMBINANT PROTEIN;

BIOSYNTHESIS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; GLYCOSYLATION; ISOLATION AND PURIFICATION; KINETICS; MASS SPECTROMETRY; METABOLISM; MYCOBACTERIUM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

BACTERIAL PROTEINS; FATTY ACIDS; GLYCOSYLATION; GLYCOSYLTRANSFERASES; KINETICS; LIPOPOLYSACCHARIDES; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; MYCOBACTERIUM; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84940705326     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13610     Document Type: Article

References (74)

1. Koul, A., Arnoult, E., Lounis, N., Guillemont, J., Andries, K. The challenge of new drug discovery for tuberculosis. Nature 469, 483-490 (2011).
2. Pacheco, S. A., Powers, K. M., Engelmann, F., Messaoudi, I., Purdy, G. E. Autophagic Killing Effects against by Alveolar Macrophages from Young and Aged Rhesus Macaques. PloS one 8, e66985 (2013).
3. Daffé, M., Crick, D. C., Jackson, M. in Molecular Genetics of Mycobacteria, Second Edition (American Society of Microbiology, 2014).
4. Mendes, V., Maranha, A., Alarico, S., Empadinhas, N. Biosynthesis of mycobacterial methylglucose lipopolysaccharides. Nat Prod Rep 29, 834-844 (2012).
5. Xia, L., Zheng, R. B., Lowary, T. L. Revisiting the specificity of an alpha-(1-> 4)-mannosyltransferase involved in mycobacterial methylmannose polysaccharide biosynthesis. Chembiochem 13, 1139-1151 (2012).
6. Jackson, M., Brennan, P. J. Polymethylated polysaccharides from Mycobacterium species revisited. J Biol Chem 284, 1949-1953 (2009).
7. Bloch, K., Vance, D. Control mechanisms in the synthesis of saturated fatty acids. Annu Rev Biochem 46, 263-298 (1977).
8. Yabusaki, K. K., Ballou, C. E. Effect of polymethylpolysaccharides on the hydrolysis of palmitoyl coenzyme A by a thioesterase from Mycobacterium smegmatis. J Biol Chem 254, 12314-12317 (1979).
9. Yabusaki, K. K., Ballou, C. E. Interaction of mycobacterial polymethylpolysaccharides with paranaric acid and palmitoylcoenzyme A: structural specificity and monomeric dissociation constants. Proc Natl Acad Sci USA. 75, 691-695 (1978).
10. Banis, R. J., Peterson, D. O., Bloch, K. Mycobacterium smegmatis fatty acid synthetase. Polysaccharide stimulation of the ratelimiting step. J Biol Chem 252, 5740-5744 (1977).
11. Flick, P. K., Bloch, K. In Vitro Alterations of the Product Distribution of the Fatty Acid Synthetase from Mycobacterium phlei. Journal of Biological Chemistry 249, 1031-1036 (1974).
12. Bloch, K. in Advances in Enzymology and Related Areas of Molecular Biology 1-84 (John Wiley & Sons, Inc., 1977).
13. Stadthagen, G. et al. Genetic basis for the biosynthesis of methylglucose lipopolysaccharides in Mycobacterium tuberculosis. J Biol Chem 282, 27270-27276 (2007).
14. Smith, W. L., Ballou, C. E. The 6-O-methylglucose-containing lipopolysaccharides of Mycobacterium phlei. Locations of the neutral and acidic acyl groups. J Biol Chem 248, 7118-7125 (1973).
15. Dell, A., Ballou, C. E. Fast-atom-bombardment, negative-ion mass spectrometry of the mycobacterial O-methyl-d-glucose polysaccharide and lipopolysaccharides. Carbohydrate Research 120, 95-111 (1983).
16. Tuffal, G., Albigot, R., Riviere, M., Puzo, G. Newly found 2-N-acetyl-2,6-dideoxy-beta-glucopyranose containing methyl glucose polysaccharides in M.bovis BCG: revised structure of the mycobacterial methyl glucose lipopolysaccharides. Glycobiology 8, 675-684 (1998).
17. Hindsgaul, O., Ballou, C. E. Affinity purification of mycobacterial polymethyl polysaccharides and a study of polysaccharidelipid interactions by 1H NMR. Biochemistry 23, 577-584 (1984).
18. Grellert, E., Ballou, C. E. Biosynthesis of a Mycobacterial Lipopolysaccharide: EVIDENCE FOR AN ACYLPOLYSACCHARIDE METHYLTRANSFERASE. Journal of Biological Chemistry 247, 3236-3241 (1972).
19. Lee, Y. C., Ballou, C. E. 6-O-Methyl-D-Glucose from Mycobacteria. J Biol Chem 239, PC3602-3603 (1964).
20. Kamisango, K., Dell, A., Ballou, C. E. Biosynthesis of the mycobacterial O-methylglucose lipopolysaccharide. Characterization of putative intermediates in the initiation, elongation, and termination reactions. J Biol Chem 262, 4580-4586 (1987).
21. Empadinhas, N., Albuquerque, L., Mendes, V., Macedo-Ribeiro, S., da Costa, M. S. Identification of the mycobacterial glucosyl-3-phosphoglycerate synthase. FEMS Microbiol Lett 280, 195-202 (2008).
22. Kaur, D. et al. Initiation of methylglucose lipopolysaccharide biosynthesis in mycobacteria. PLoS One 4, e5447 (2009).
23. Mendes, V., Maranha, A., Alarico, S., da Costa, M. S., Empadinhas, N. Mycobacterium tuberculosis Rv2419c, the missing glucosyl-3-phosphoglycerate phosphatase for the second step in methylglucose lipopolysaccharide biosynthesis. Sci Rep 1, 177 (2011).
24. Alarico, S. et al. Mycobacterium hassiacum recovers from nitrogen starvation with up-regulation of a novel glucosylglycerate hydrolase and depletion of the accumulated glucosylglycerate. Sci Rep 4, 6766 (2014).
25. Ma, Q., Xu, Y. Global Genomic Arrangement of Bacterial Genes Is Closely Tied with the Total Transcriptional Efficiency. Genomics, Proteomics & Bioinformatics 11, 66-71 (2013).
26. Sassetti, C. M., Boyd, D. H., Rubin, E. J. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48, 77-84 (2003).
27. Griffin, J. E. et al. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS pathogens 7, e1002251 (2011).
28. Tiago, I. et al. Genome Sequence of Mycobacterium hassiacum DSM 44199, a Rare Source of Heat-Stable Mycobacterial Proteins. J Bacteriol 194, 7010-7011 (2012).
29. Chen, W., Biswas, T., Porter, V. R., Tsodikov, O. V., Garneau-Tsodikova, S. Unusual regioversatility of acetyltransferase Eis, a cause of drug resistance in XDR-TB. Proceedings of the National Academy of Sciences 108, 9804-9808 (2011).
30. Schulze-Gahmen, U., Pelaschier, J., Yokota, H., Kim, R., Kim, S.-H. Crystal structure of a hypothetical protein, TM841 of Thermotoga maritima, reveals its function as a fatty acid-binding protein. Proteins: Structure, Function, and Bioinformatics 50, 526-530 (2003).
31. Akoh, C. C., Lee, G. C., Liaw, Y. C., Huang, T. H., Shaw, J. F. GDSL family of serine esterases/lipases. Progress in lipid research 43, 534-552 (2004).
32. Pommier, M. T., Michel, G. Isolation and characterization of an O-methylglucose-containing lipopolysaccharide produced by Nocardia otitidis-caviarum. J Gen Microbiol 132, 2433-2441 (1986).
33. Harris, L. S., Gray, G. R. Acetylated methylmannose polysaccharide of Streptomyces. Journal of Biological Chemistry 252, 2470-2477 (1977).
34. Moynihan, P. J., Clarke, A. J. O-acetylation of peptidoglycan in gram-negative bacteria: identification and characterization of peptidoglycan O-acetyltransferase in Neisseria gonorrhoeae. J Biol Chem 285, 13264-13273 (2010).
35. Moynihan, P. J., Clarke, A. J. Mechanism of action of peptidoglycan O-acetyltransferase B involves a Ser-His-Asp catalytic triad. Biochemistry 53, 6243-6251 (2014).
36. Lourenço, E. C., Maycock, C. D., Rita Ventura, M. Synthesis of potassium (2R)-2-O-d-glucopyranosyl-(1 6)-dglucopyranosyl-2,3-dihydroxypropanoate a natural compatible solute. Carbohydrate Research 344, 2073-2078 (2009).
37. Lourenço, E. C., Ventura, M. R. Synthesis of Potassium (2R)-2-O-D-Mannopyranosyl-(1 2)-D-glucopyranosyl-2,3-dihydroxypropanoate: A Naturally Compatible Solute. European Journal of Organic Chemistry 2011, 6698-6703 (2011).
38. Fürstner, A., Albert, M., Mlynarski, J., Matheu, M., DeClercq, E. Structure Assignment, Total Synthesis, and Antiviral Evaluation of Cycloviracin B1. Journal of the American Chemical Society 125, 13132-13142 (2003).
39. Hoch, M., Heinz, E., Schmidt, R. R. Synthesis of 6-deoxy-6-sulfo-d-glucopyranosyl phosphate. Carbohydrate Research 191, 21-28 (1989).
40. Lourenço, E. C., Ventura, M. R. The effect of electron withdrawing protecting groups at positions 4 and 6 on 1,2-cis galactosylation. Tetrahedron 69, 7090-7097 (2013).
41. Crich, D., Cai, W. Chemistry of 4,6-O-Benzylidene-d-glycopyranosyl Triflates: Contrasting Behavior between the Gluco and Manno Series. The Journal of Organic Chemistry 64, 4926-4930 (1999).
42. Daragics, K., Fügedi, P. Regio-and chemoselective reductive cleavage of 4,6-O-benzylidene-type acetals of hexopyranosides using BH3•THF-TMSOTf. Tetrahedron Letters 50, 2914-2916 (2009).
43. Li, X., Huang, L., Hu, X., Huang, X. Thio-arylglycosides with various aglyconpara-substituents: a probe for studying chemical glycosylation reactions. Organic & Biomolecular Chemistry 7, 117-127 (2009).
44. Lourenço, E. C., Ventura, M. R. The synthesis of compatible solute analogues-solvent effects on selective glycosylation. Carbohydrate Research 346, 163-168 (2011).
45. Jorge, C. D., Lamosa, P., Santos, H.-d-Mannopyranosyl-(1 2)-d-glucopyranosyl-(1 2)-glycerate in the thermophilic bacterium Petrotoga miotherma structure, cellular content and function. FEBS Journal 274, 3120-3127 (2007).
46. Fernandes, C. et al. Two Alternative Pathways for the Synthesis of the Rare Compatible Solute Mannosylglucosylglycerate in Petrotoga mobilis. Journal of Bacteriology 192, 1624-1633 (2010).
47. Bashiri, G. et al. Tat-Dependent Translocation of an F 420-Binding Protein of Mycobacterium tuberculosis . PLoS ONE 7, e45003 (2012).
48. Mendes, V., Maranha, A., Lamosa, P., da Costa, M. S., Empadinhas, N. Biochemical characterization of the maltokinase from Mycobacterium bovis BCG. BMC Biochem 11, 21 (2010).
49. Spalding, M. D., Prigge, S. T. Lipoic Acid Metabolism in Microbial Pathogens. Microbiology and Molecular Biology Reviews 74, 200-228 (2010).
50. Jogl, G., Hsiao, Y.-S., Tong, L. Structure and Function of Carnitine Acyltransferases. Annals of the New York Academy of Sciences 1033, 17-29 (2004).
51. Yang, J., Brown, M. S., Liang, G., Grishin, N. V., Goldstein, J. L. Identification of the Acyltransferase that Octanoylates Ghrelin, an Appetite-Stimulating Peptide Hormone. Cell 132, 387-396 (2008).
52. Saerens, S. M. G. et al. The Saccharomyces cerevisiae EHT1 and EEB1 Genes Encode Novel Enzymes with Medium-chain Fatty Acid Ethyl Ester Synthesis and Hydrolysis Capacity. Journal of Biological Chemistry 281, 4446-4456 (2006).
53. Saerens, S. M. G. et al. Parameters Affecting Ethyl Ester Production by Saccharomyces cerevisiae during Fermentation. Applied and Environmental Microbiology 74, 454-461 (2008).
54. Traut, T. in Allosteric Regulatory Enzymes 29-48 (Springer US, 2008).
55. Schröder, K.-H., Naumann, L., Kroppenstedt, R. M., Reischl, U. Mycobacterium hassiacum sp. nov., a New Rapidly Growing Thermophilic Mycobacterium. International Journal of Systematic and Evolutionary Microbiology 47, 86-91 (1997).
56. Tung, K. K., Ballou, C. E. Biosynthesis of a mycobacterial lipopolysaccharide. Properties of the polysaccharide: acyl coenzyme A acyltransferase reaction. J Biol Chem 248, 7126-7133 (1973).
57. Keller, J., Ballou, C. E. The 6-O-methylglucose-containing lipopolysaccharide of Mycobacterium phlei. Identification of the lipid components. J Biol Chem 243, 2905-2910 (1968).
58. Ohgusu, H., Takahashi, T., Kojima, M. in Methods in Enzymology, Vol. Volume 514. (eds. K., Masayasu & K., Kenji) 147-163 (Academic Press, 2012).
59. Gutierrez, J. A. et al. Ghrelin octanoylation mediated by an orphan lipid transferase. Proceedings of the National Academy of Sciences 105, 6320-6325 (2008).
60. Nishi, Y. et al. Changes in Subcellular Distribution of n-Octanoyl or n-Decanoyl Ghrelin in Ghrelin-Producing Cells. Front Endocrinol (Lausanne) 4, 84 (2013). doi: 10.3389/fendo.2013.00084.
61. Jogl, G., Hsiao, Y.-S., Tong, L. Crystal Structure of Mouse Carnitine Octanoyltransferase and Molecular Determinants of Substrate Selectivity. Journal of Biological Chemistry 280, 738-744 (2005).
62. Narumi, K., Keller, J. M., Ballou, C. E. Biosynthesis of a mycobacterial lipopolysaccharide. Incorporation of (14C)acyl groups by whole cells in vivo. Biochem J 132, 329-340 (1973).
63. Gray, G. R., Ballou, C. E. The 6-O-Methylglucose-containing Lipopolysaccharides of Mycobacterium phlei : LOCATIONS OF THE ACYL GROUPS. Journal of Biological Chemistry 247, 8129-8135 (1972).
64. Nobre, A., Alarico, S., Maranha, A., Mendes, V., Empadinhas, N. The molecular biology of mycobacterial trehalose in the quest for advanced tuberculosis therapies. Microbiology 160, 1547-1570 (2014).
65. Kalscheuer, R., Koliwer-Brandl, H. Genetics of Mycobacterial Trehalose Metabolism. Microbiol Spectr 2 (2014). doi: 10.1128/microbiolspec.MGM2-0002-2013.
66. Besra, G. S. et al. New pyruvylated, glycosylated acyltrehaloses from Mycobacterium smegmatis strains, and their implications for phage resistance in mycobacteria. Carbohydrate Research 251, 99-114 (1994).
67. McNeil, M. et al. Definition of the surface antigens of Mycobacterium malmoense and use in studying the etiology of a form of mycobacteriosis. Journal of Bacteriology 169, 3312-3320 (1987).
68. Lew, J. M., Kapopoulou, A., Jones, L. M., Cole, S. T. TubercuList-10 years after. Tuberculosis 91, 1-7 (2011).
69. Bond, C. S., Schuttelkopf, A. W. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallographica Section D 65, 510-512 (2009).
70. Sambrook, J., Russell, D. W. Molecular Cloning: A laboratory manual, Edn. 3rd. (Cold Spring Harbor Laboratory Press, New York, 2001).
71. Armarego, W. L. F., Chai, C. L. L. in Purification of Laboratory Chemicals (Fifth Edition). (ed. W. L. F. A. L. L., Chai) 1-52 (Butterworth-Heinemann, Burlington, 2003).
72. Jacin, H., Mishkin, A. R. Separation of carbonhydrates on borate-impregnated silica gel G plates. Journal of Chromatography A 18, 170-173 (1965).
73. Empadinhas, N. et al. Functional and structural characterization of a novel mannosyl-3-phosphoglycerate synthase from Rubrobacter xylanophilus reveals its dual substrate specificity. Mol Microbiol 79, 76-93 (2011).
74. Strohalm, M., Kavan, D., Novak, P., Volny, M., Havlicek, V. mMass 3: a cross-platform software environment for precise analysis of mass spectrometric data. Anal Chem 82, 4648-4651 (2010).