The C-terminal domain of the arabinosyltransferase mycobacterium tuberculosis EmbC is a lectin-like carbohydrate binding module

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Alderwick, Luke J ^a   Lloyd, Georgina S ^a   Ghadbane, Hemza ^a   May, John W ^a   Bhatt, Apoorva ^a   Eggeling, Lothar ^b   Fütterer, Klaus ^a   Besra, Gurdyal S ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBOHYDRATE BINDING PROTEIN; EMBC PROTEIN; LIPOARABINOMANNAN; TRYPTOPHAN; UNCLASSIFIED DRUG; ARABINOGALACTAN; ARABINOSYLTRANSFERASE; GALACTAN; GLYCOSYLTRANSFERASE; LECTIN; LIPOPOLYSACCHARIDE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POINT MUTATION; PROTEIN STRUCTURE; CELL WALL; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

MYCOBACTERIUM TUBERCULOSIS;

CELL WALL; CRYSTALLOGRAPHY, X-RAY; GALACTANS; LECTINS; LIPOPOLYSACCHARIDES; MUTAGENESIS, SITE-DIRECTED; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PENTOSYLTRANSFERASES; PROTEIN CONFORMATION;

EID: 79952211396     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001299     Document Type: Article

References (47)

1. World Health Organisation (2009) Global Tuberculosis Control: a short update to the 2009 report (http://www.who.int/entity/tb/publications/2009/factsheet_tb_2009update_dec09.pdf).
2. Harries AD, Dye C, (2006) Tuberculosis. Ann Trop Med Parasitol 100: 415-431.
3. Jain A, Mondal R, (2008) Extensively drug-resistant tuberculosis: current challenges and threats. FEMS Immunol Med Microbiol 53: 145-150.
4. Crick DC, Mahapatra S, Brennan PJ, (2001) Biosynthesis of the arabinogalactan-peptidoglycan complex of Mycobacterium tuberculosis. Glycobiology 11: 107R-118R.
5. Briken V, Porcelli SA, Besra GS, Kremer L, (2004) Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 53: 391-403.
6. Belanger AE, Besra GS, Ford ME, Mikusova K, Belisle JT, et al. (1996) 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: 11919-11924.
7. Telenti A, Philipp WJ, Sreevatsan S, Bernasconi C, Stockbauer KE, et al. (1997) The emb operon, a gene cluster of Mycobacterium tuberculosis involved in resistance to ethambutol. Nat Med 3: 567-570.
8. Escuyer VE, Lety MA, Torrelles JB, Khoo KH, Tang JB, et al. (2001) 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: 48854-48862.
9. Zhang N, Torrelles JB, McNeil MR, Escuyer VE, Khoo KH, et al. (2003) 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: 69-76.
10. Berg S, Starbuck J, Torrelles JB, Vissa VD, Crick DC, et al. (2005) Roles of conserved proline and glycosyltransferase motifs of EmbC in biosynthesis of lipoarabinomannan. J Biol Chem 280: 5651-5663.
11. Shi L, Berg S, Lee A, Spencer JS, Zhang J, et al. (2006) The carboxy terminus of EmbC from Mycobacterium smegmatis mediates chain length extension of the Arabinan in lipoarabinomannan. J Biol Chem 281: 19512-19526.
12. Alderwick LJ, Seidel M, Sahm H, Besra GS, Eggeling L, (2006) Identification of a novel arabinofuranosyltransferase (AftA) involved in cell wall arabinan biosynthesis in Mycobacterium tuberculosis. J Biol Chem 281: 15653-15661.
13. Seidel M, Alderwick LJ, Birch HL, Sahm H, Eggeling L, et al. (2007) 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: 14729-14740.
14. Seidel M, Alderwick LJ, Sahm H, Besra GS, Eggeling L, (2007) Topology and mutational analysis of the single Emb arabinofuranosyltransferase of Corynebacterium glutamicum as a model of Emb proteins of Mycobacterium tuberculosis. Glycobiology 17: 210-219.
15. Liu J, Mushegian A, (2003) Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci 12: 1418-1431.
16. Lee RE, Mikusova K, Brennan PJ, Besra GS, (1995) Synthesis of the mycobacterial arabinose donor beta-D-arabinofuranosyl-1-monophosphoryldecaprenol, development of a basic arabinosyl-transferase assay, and identification of ethambutol as an arabinosyl transferase inhibitor. J Am Chem Soc 117: 11829-11832.
17. Wolucka BA, McNeil MR, de Hoffmann E, Chojnacki T, Brennan PJ, (1994) 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: 23328-23335.
18. Amin AG, Goude R, Shi L, Zhang J, Chatterjee D, et al. (2008) EmbA is an essential arabinosyltransferase in Mycobacterium tuberculosis. Microbiology 154: 240-248.
19. Goude R, Amin AG, Chatterjee D, Parish T, (2008) The critical role of embC in Mycobacterium tuberculosis. J Bacteriol 190: 4335-4341.
20. Ramaswamy SV, Amin AG, Goksel S, Stager CE, Dou SJ, et al. (2000) Molecular genetic analysis of nucleotide polymorphisms associated with ethambutol resistance in human isolates of Mycobacterium tuberculosis. Antimicrob Agents Chemother 44: 326-336.
21. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ, (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382: 769-781.
22. Harding MM, (2001) Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr 57: 401-411.
23. Holm L, Sander C, (1996) Mapping the protein universe. Science 273: 595-603.
24. Igura M, Maita N, Kamishikiryo J, Yamada M, Obita T, et al. (2008) Structure-guided identification of a new catalytic motif of oligosaccharyltransferase. EMBO J 27: 234-243.
25. Lee RE, Brennan PJ, Besra GS, (1997) Mycobacterial arabinan biosynthesis: the use of synthetic arabinoside acceptors in the development of an arabinosyl transfer assay. Glycobiology 7: 1121-1128.
26. Pires VM, Henshaw JL, Prates JA, Bolam DN, Ferreira LM, et al. (2004) The crystal structure of the family 6 carbohydrate binding module from Cellvibrio mixtus endoglucanase 5a in complex with oligosaccharides reveals two distinct binding sites with different ligand specificities. J Biol Chem 279: 21560-21568.
27. Bardarov S, Bardarov SJ Jr, Pavelka MSJ Jr, Sambandamurthy V, Larsen M, et al. (2002) Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148: 3007-3017.
28. Bhamidi S, Scherman MS, McNeil MR, (2009) Mycobacterial cell wall arabinogalactan: a detailed perspective on structure, biosynthesis, functions and drug tageting. In: Ullrich M, editors. Bacterial polysaccharides Norfolk, UK Caister Academic Press pp. 39-65.
29. Walser PJ, Haebel PW, Kunzler M, Sargent D, Kues U, et al. (2004) Structure and functional analysis of the fungal galectin CGL2. Structure 12: 689-702.
30. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J, (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229: 105-124.
31. Kabsch W, (1993) Automatic processing of rotation diffraction data from crystals of initially unknown cell constants and symmetry. J Appl Crystallogr 26: 795-800.
32. Sheldrick GM, (2008) A short history of SHELX. Acta Crystallogr A 64: 112-122.
33. de la Fortelle E, Bricogne G, (1997) Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multi-wavelength anomalous diffraction methods. Methods Enzymol 276: 472-494.
34. Abrahams JP, Leslie AG, (1996) Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr D Biol Crystallogr 52: 30-42.
35. Morris RJ, Perrakis A, Lamzin VS, (2002) ARP/wARP's model-building algorithms. I. The main chain. Acta Crystallogr D Biol Crystallogr 58: 968-975.
36. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
37. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
38. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
39. Winn MD, Isupov MN, Murshudov GN, (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57: 122-133.
40. Schuck P, (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78: 1606-1619.
41. Stover CK, de la Cruz VF, Fuerst TR, Burlein JE, Benson LA, et al. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
42. Nigou J, Gilleron M, Cahuzac B, Bounery JD, Herold M, et al. (1997) The phosphatidyl-myo-inositol anchor of the lipoarabinomannans from Mycobacterium bovis bacillus Calmette Guerin. Heterogeneity, structure, and role in the regulation of cytokine secretion. J Biol Chem 272: 23094-23103.
43. Gouet P, Courcelle E, Stuart DI, Metoz F, (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
44. Jamal-Talabani S, Boraston AB, Turkenburg JP, Tarbouriech N, Ducros VM, et al. (2004) Ab initio structure determination and functional characterization of CBM36; a new family of calcium-dependent carbohydrate binding modules. Structure 12: 1177-1187.
45. van Bueren AL, Morland C, Gilbert HJ, Boraston AB, (2005) Family 6 carbohydrate binding modules recognize the non-reducing end of beta-1,3-linked glucans by presenting a unique ligand binding surface. J Biol Chem 280: 530-537.
46. Henshaw J, Horne-Bitschy A, van Bueren AL, Money VA, Bolam DN, et al. (2006) Family 6 carbohydrate binding modules in beta-agarases display exquisite selectivity for the non-reducing termini of agarose chains. J Biol Chem 281: 17099-17107.
47. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-83.