Recent advances in mycobacterial cell wall glycan biosynthesis

Current Opinion in Chemical Biology

Volumn 13, Issue 5-6, 2009, Pages 618-625

  Tam, Pui Hang ^a   Lowary, Todd L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOGALACTAN; ETHAMBUTOL; GALACTAN; GLUCAN; GLYCAN; GLYCOCONJUGATE; GLYCOSYLTRANSFERASE; LIPOARABINOMANNAN; MANNOSYLTRANSFERASE; PHENOLIC GLYCOLIPID;

BACTERIAL CELL WALL; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; CELL VIABILITY; GENETICS; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM TUBERCULOSIS; PATHOGENICITY; REVIEW; SEROTYPE;

CARBOHYDRATE SEQUENCE; CELL WALL; GLYCOCONJUGATES; GLYCOSYLTRANSFERASES; HUMANS; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM; POLYSACCHARIDES;

CORYNEBACTERINEAE; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM TUBERCULOSIS;

EID: 70549094241     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2009.09.012     Document Type: Review

References (54)

1. Ratledge C., and Stanford J. Introduction. In: Ratledge C., and Stanford J. (Eds). The Biology of Mycobacteria vol. 1 (1982), Academic Press 94-184
2. De Jong B.C., Israelski D.M., Corbett E.L., and Small P.M. Clinical management of tuberculosis in the context of HIV infection. Annu Rev Med 55 (2004) 283-301
3. Bass Jr. J.B., Farer L.S., Hopewell P.C., O'Brien R., Jacobs R.F., Ruben F., Snider Jr. D.E., and Thornton G. Treatment of tuberculosis and tuberculosis infection in adults and children. Am J Respir Crit Care Med 149 (1994) 1359-1374
4. Brennan P.J. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83 (2003) 91-97
5. Chiang C., and Yew W.W. Multidrug-resistant and extensively drug-resistant tuberculosis. Int J Tuberc Lung Dis 13 (2009) 304-311
6. Berg S., Kaur D., Jackson M., and Brennan P.J. The glycosyltransferases of Mycobacterium tuberculosis - roles in the synthesis of arabinogalactan, lipoarabinomannan, and other glycoconjugates. Glycobiology 17 (2007) 35R-56R. This article provides a comprehensive overview of glycosyltransferases involved in the biosynthesis of major cell wall components and other associated glycoconjugates of M. tuberculosis. In particular, it summarizes the structural and functional aspects of the characterized and putative GTs in Mycobacterium spp.
7. Lucas R., Balbuena P., Errey J., Squire M., Gurcha S., Mcneil M., Besra G., and Davis B. Glycomimetic inhibitors of mycobacterial glycosyltransferases: targeting the TB cell wall. ChemBioChem 9 (2008) 2197-2199
8. Janin Y.L. Antituberculosis drugs: ten years of research. Biorg Med Chem 15 (2007) 2479-2513
9. Briken V., Porcelli S.A., Besra G.S., and Kremer L. Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 53 (2004) 391-403
10. Besra G.S., Morehouse C.B., Rittner C.M., Waechter C.J., and Brennan P.J. Biosynthesis of mycobacterial lipoarabinomannan. J Biol Chem 272 (1997) 18460-18466
11. Korduláková J., Gilleron M., Mikušová K., Puzo G., Brennan P., Gicquel B., and Jackson M. Definition of the first mannosylation step in phosphatidylinositol mannoside synthesis. PimA is essential for growth of mycobacteria. J Biol Chem 277 (2002) 31335-31344
12. Guerin M.E., Korduláková J., Schaeffer F., Svetlikova Z., Buschiazzo A., Giganti D., Gicquel B., Mikušová K., Jackson M., and Alzari P.M. Molecular recognition and interfacial catalysis by the essential phosphatidylinositol mannosyltransferase PimA from mycobacteria. J Biol Chem 282 (2007) 20705-20714. The first X-ray crystal structure of a mycobacterial glycosyltransferase is reported.
13. Breton C., Šnajdrová L., Jeanneau C., Koča J., and Imberty A. Structures and mechanisms of glycosyltransferases. Glycobiology 16 (2006) 29R-37R
14. Guerin M.E., Schaeffer F., Chaffotte A., Gest P., Giganti D., Korduláková J., van der Woerd M., Jackson M., and Alzari P.M. Substrate-induced conformational changes in the essential peripheral membrane-associated mannosyltransferase PimA from mycobacteria. Implications for catalysis. J Biol Chem 284 (2009) 21613-21625
15. Alderwick L.J., Radmacher E., Seidel M., Gande R., Hitchen P.G., Morris H.R., Dell A., Sahm H., Eggeling L., and Besra G.S. Deletion of Cg-emb in corynebacterianeae leads to a novel truncated cell wall arabinogalactan, whereas inactivation of Cg-ubiA results in an arabinan-deficient mutant with a cell wall galactan core. J Biol Chem 280 (2005) 32362-32371
16. Schaeffer M.L., Khoo K.H., Besra G.S., Chatterjee D., Brennan P.J., Belisle J.T., and Inamine J.M. The pimB gene of Mycobacterium tuberculosis encodes a mannosyltransferase involved in lipoarabinomannan biosynthesis. J Biol Chem 274 (1999) 31625-31631
17. Tatituri R.V.V., Illarionov P.A., Dover L.G., Nigou J., Gilleron M., Hitchen P., Krumbach K., Morris H.R., Spencer N., Dell A., et al. Inactivation of Corynebacterium glutamicum NCgI0452 and the role of MgtA in the biosynthesis of a novel mannosylated glycolipid involved in lipomannan biosynthesis. J Biol Chem 282 (2007) 4561-4572. The function of the Rv0557 gene product (previously known as PimB) was revised. This report demonstrated this enzyme (renamed MgtA) catalyzes the transfer of Manp residue to glucopyranosyluronic acid.
18. Lea-Smith D.J., Martin K.L., Pyke J.S., Tull D., McConville M.J., Coppel R.L., and Crellin P.K. Analysis of a new mannosyltransferase required for the synthesis of phosphatidylinositol mannosides and lipoarabinomannan reveals two lipomannan pools in Corynebacterineae. J Biol Chem 283 (2008) 6773-6782
19. Torrelles J.B., DesJardin L.E., MacNeil J., Kaufman T.M., Kutzbach B., Knaup R., McCarthy T.R., Gurcha S.S., Besra G.S., Clegg S., et al. Inactivation of Mycobacterium tuberculosis mannosyltransferase pimB reduces the cell wall lipoarabinomannan and lipomannan content and increases the rate of bacterial-induced human macrophage cell death. Glycobiology 19 (2009) 743-755
20. Gurcha S.S., Baulard A.R., Kremer L., Locht C., Moody D.B., Muhlecker W., Costello C.E., Crick D.C., Brennan P.J., and Besra G.S. Ppm1, a novel polyprenol monophosphomannose synthase from Mycobacterium tuberculosis. Biochem J 365 (2002) 441-450
21. Kaur D., McNeil M.R., Khoo K.H., Chatterjee D., Crick D.C., Jackson M., and Brennan P.J. New insights into the biosynthesis of mycobacterial lipomannan arising from deletion of a conserved gene. J Biol Chem 282 (2007) 27133-27140. The first PPM-dependent α-(1→6)-ManT (Rv2174) involved in the lipomannan synthesis was identified.
22. Mishra A.K., Alderwick L.J., Rittmann D., Tatituri R.V.V., Nigou J., Gilleron M., Eggeling L., and Besra G.S. Identification of an α-(1→6) mannopyranosyltransferase (MptA), involved in Corynebacterium glutamicum lipomanann biosynthesis, and identification of its orthologue in Mycobacterium tuberculosis. Mol Microbiol 65 (2007) 1503-1517
23. Mishra A., Alderwick L., Rittmann D., Wang C., Bhatt A., Jacobs Jr. W., Takayama K., Eggeling L., and Besra G. Identification of a novel α-(1→6) mannopyranosyltransferase MptB from Corynebacterium glutamicum by deletion of a conserved gene, NCgl1505, affords a lipomannan- and lipoarabinomannan-deficient mutant. Mol Microbiol 68 (2008) 1595-1613
24. Kaur D., Berg S., Dinadayala P., Gicquel B., Chatterjee D., McNeil M.R., Vissa V.D., Crick D.C., Jackson M., and Brennan P.J. Biosynthesis of mycobacterial lipoarabinomannan: role of a branching mannosyltransferase. Proc Natl Acad Sci U S A 103 (2006) 13664-13669
25. Tam P.H., Besra G.S., and Lowary T.L. Exploring the substrate specificity of a mycobacterial polyprenol monophosphomannose-dependent α-(1→6)-mannosyltransferase. ChemBioChem 9 (2008) 267-278
26. Dinadayala P., Kaur D., Berg S., Amin A.G., Vissa V.D., Chatterjee D., Brennan P.J., and Crick D.C. Genetic basis for the synthesis of the immunomodulatory mannose caps of lipoarabinomannan in Mycobacterium tuberculosis. J Biol Chem 281 (2006) 20027-20035
27. Belánová M., Dianišková P., Brennan P., Completo G., Rose N., Lowary T., and Mikušová K. Galactosyl transferases in mycobacterial cell wall synthesis. J Bacteriol 190 (2008) 1141-1145. This paper demonstrated that the two known galactofuranosyltransferases, GlfT1 and GlfT2, account for the full length of galactan biosynthesis.
28. Mikušová K., Belánová M., Korduláková J., Honda K., McNeil M.R., Mahapatra S., Crick D.C., and Brennan P.J. Identification of a novel galactosyl transferase involved in biosynthesis of the mycobacterial cell wall. J Bacteriol 188 (2006) 6592-6598
29. Kremer L., Dover L.G., Morehouse C., Hitchin P., Everett M., Morris H.R., Dell A., Brennan P.J., McNeil M.R., Flaherty C., et al. Galactan biosynthesis in Mycobacterium tuberculosis: identification of a bifunctional UDP-galactofuranosyltransferase. J Biol Chem 276 (2001) 26430-26440
30. Alderwick L.J., Dover L.G., Veerapen N., Gurcha S.S., Kremer L., Roper D.L., Pathak A.K., Reynolds R.C., and Besra G.S. Expression, purification and characterisation of soluble GlfT and the identification of a novel galactofuranosyltransferase Rv3782 involved in priming GlfT-mediated galactan polymerisation in Mycobacterium tuberculosis. Protein Expr Purif 58 (2008) 332-341
31. Rose N.L., Completo G.C., Lin S.J., McNeil M., Palcic M.M., and Lowary T.L. Expression, purification, and characterization of a galactofuranosyltransferase involved in Mycobacterium tuberculosis arabinogalactan biosynthesis. J Am Chem Soc 128 (2006) 6721-6729
32. Shi L.B., Berg S., Lee A., Spencer J.S., Zhang J., Vissa V., McNeil M.R., Khoo K.H., and Chatterjee D. The carboxy terminus of EmbC from Mycobacterium smegmatis mediates chain length extension of the arabinan in lipoarabinomannan. J Biol Chem 281 (2006) 19512-19526
33. Belanger A.E., Besra G.S., Ford M.E., Mikušová K., Belisle J.T., Brennan P.J., and Inamine J.M. The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol. Proc Natl Acad Sci U S A 93 (1996) 11919-11924
34. Wolucka B.A., McNeil M.R., Dehoffmann E., Chojnacki T., and Brennan P.J. Recognition of the lipid intermediate for arabinogalactan/arabinomannan biosynthesis and its relation to the mode of action of ethambutol on mycobacteria. J Biol Chem 269 (1994) 23328-23335
35. Zhang N., Torrelles J.B., McNeil M.R., Escuyer V.E., Khoo K.H., Brennan P.J., and Chatterjee D. The Emb proteins of mycobacteria direct arabinosylation of lipoarabinomannan and arabinogalactan via an N-terminal recognition region and a C-terminal synthetic region. Mol Microbiol 50 (2003) 69-76
36. Escuyer V.E., Lety M.A., Torrelles J.B., Khoo K.H., Tang J.B., Rithner C.D., Frehel C., McNeil M.R., Brennan P.J., and Chatterjee D. The role of the embA and embB gene products in the biosynthesis of the terminal hexaarabinofuranosyl motif of Mycobacterium smegmatis arabinogalactan. J Biol Chem 276 (2001) 48854-48862
37. Alderwick L.J., Seidel M., Sahm H., Besra G.S., and Eggeling L. Identification of a novel arabinofuranosyltransferase (AftA) involved in cell wall arabinan biosynthesis in Mycobacterium tuberculosis. J Biol Chem 281 (2006) 15653-15661
38. Seidel M., Alderwick L.J., Birch H.L., Sahm H., Eggeling L., and Besra G.S. Identification of a novel arabinofuranosyltransferase AftB involved in a terminal step of cell wall arabinan biosynthesis in corynebacterianeae, such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J Biol Chem 282 (2007) 14729-14740
39. Birch H., Alderwick L., Bhatt A., Rittmann D., Krumbach K., Singh A., Bai Y., Lowary T.L., Eggeling L., and Besra G. Biosynthesis of mycobacterial arabinogalactan: identification of a novel α-(1→3) arabinofuranosyltransferase. Mol Microbiol 69 (2008) 1191-1206
40. Shi L., Zhou R., Liu Z., Lowary T.L., Seeberger P.H., Stocker B.L., Crick D.C., Khoo K.H., and Chatterjee D. Transfer of the first arabinofuranose residue to galactan is essential for Mycobacterium smegmatis viability. J Bacteriol 190 (2008) 5248-5255
41. Zhang J., Khoo K.H., Wu S.W., and Chatterjee D. Characterization of a distinct arabinofuranosyltransferase in Mycobacterium smegmatis. J Am Chem Soc 129 (2007) 9650-9662
42. Schorey J., and Sweet L. The mycobacterial glycopeptidolipids: structure, function, and their role in pathogenesis. Glycobiology 18 (2008) 832-841. This article provides an overview of current understanding of the mycobacterial glycopeptidolipid biosynthesis. Discussion focuses on the structural and functional aspects of GPLs and their roles in mycobacterial virulence.
43. Miyamoto Y., Mukai T., Maeda Y., Kai M., Naka T., Yano I., and Makino M. The Mycobacterium avium complex gtfTB gene encodes a glucosyltransferase required for the biosynthesis of serovar 8-specific glycopeptidolipid. J Bacteriol 190 (2008) 7918-7924
44. Chatterjee D., and Khoo K.H. The surface glycopeptidolipids of mycobacteria: structures and biological of properties. Cell Mol Life Sci 58 (2001) 2018-2042. This review summarizes the structure and function of glycopeptidolipids.
45. Fujiwara N., Nakata N., Naka T., Yano I., Doe M., Chatterjee D., McNeil M., Brennan P.J., Kobayashi K., Makino M., et al. Structural analysis and biosynthesis gene cluster of an antigenic glycopeptidolipid from Mycobacterium intracellulare. J Bacteriol 190 (2008) 3613-3621. The chemical structure of 16 serotype-specific GPLs was determined and revealed an unusual N-acyl-dideoxy-hexose at the nonreducing end of the carbohydrate moiety.
46. Constant P., Pérez E., Malaga W., Lanéelle M.A., Saurel O., Daffé M., and Guilhot C. Role of the pks15/1 gene in the biosynthesis of phenolglycolipids in the Mycobacterium tuberculosis complex. J Biol Chem 277 (2002) 38148-38158
47. Pérez E., Constant P., Lemassu A., Laval F., Daffé M., and Guilhot C. Characterization of three glycosyltransferases involved in the biosynthesis of the phenolic glycolipid antigens from the Mycobacterium tuberculosis complex. J Biol Chem 279 (2004) 42574-42583
48. Malaga W., Constant P., Euphrasie D., Cataldi A., Daffé M., Reyrat J.M., and Guilhot C. Deciphering the genetic bases of the structural diversity of phenolic glycolipids in strains of the Mycobacterium tuberculosis complex. J Biol Chem 283 (2008) 15177-15184. This report showed that a frameshift mutation within Rv2958c, encoding a glycosyltransferase required for the transfer of the second rhamnosyl residue of PGL-tb, leads to the formation of monoglycosylated PGLs. This genetic defect accounts for one of the factors resulting in the structural diversity of PGLs among Mycobacterium species.
49. Dinadayala P., Lemassu A., Granovski P., Cérantola S., Winter N., and Daffé M. Revisiting the structure of the anti-neoplastic glucans of Mycobacterium bovis Bacille Calmette-Guerin. Structural analysis of the extracellular and boiling water extract-derived glucans of the vaccine substrains. J Biol Chem 279 (2004) 12369-12378
50. Sambou T., Dinadayala P., Stadthagen G., Barilone N., Bordat Y., Constant P., Levillain F., Neyrolles O., Gicquel B., Lemassu A., et al. Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: biosynthesis and impact on the persistence in mice. Mol Microbiol 70 (2008) 762-774
51. Garg S.K., Alam M.S., Kishan K.V.R., and Agrawal P. Expression and characterization of α-(1→4)-glucan branching enzyme Rv1326c of Mycobacterium tuberculosis H37Rv. Protein Expr Purif 51 (2007) 198-208
52. Stadthagen G., Sambou T., Guerin M., Barilone N., Boudou F., Korduláková J., Charles P., Alzari P.M., Lemassu A., Daffé M., et al. Genetic basis for the biosynthesis of methylglucose lipopolysaccharides in Mycobacterium tuberculosis. J Biol Chem 282 (2007) 27270-27276
53. Jackson M., and Brennan P. Polymethylated polysaccharides from Mycobacterium species revisited. J Biol Chem 284 (2008) 1949-1953
54. Fulton Z., Mcalister A., Wilce M.C.J., Brammananth R., Zaker-Tabrizi L., Perugini M.A., Bottomley S.P., Coppel R., Crellin P., Rossjohn J., et al. Crystal structure of a UDP-glucose-specific glycosyltransferase from a Mycobacterium species. J Biol Chem 283 (2008) 27881-27890