Topology and mutational analysis of the single Emb arabinofuranosyltransferase of Corynebacterium glutamicum as a model of Emb proteins of Mycobacterium tuberculosis

Glycobiology

Volumn 17, Issue 2, 2007, Pages 210-219

  Seidel, Mathias ^a   Alderwick, Luke J ^b   Sahm, Hermann ^a   Besra, Gurdyal S ^b   Eggeling, Lothar ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOFURANOSYLTRANSFERASE; ARABINOGALACTAN; BACTERIAL PROTEIN; ETHAMBUTOL; GALACTAN; GLYCOSYLTRANSFERASE; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM MUTANT; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; LINKAGE ANALYSIS; MEMBRANE STRUCTURE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CELL MEMBRANE; CELL WALL; CORYNEBACTERIUM GLUTAMICUM; DNA MUTATIONAL ANALYSIS; ETHAMBUTOL; GALACTANS; LIPIDS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; PENTOSYLTRANSFERASES; PEPTIDOGLYCAN; PROTEIN STRUCTURE, TERTIARY;

CORYNEBACTERIUM GLUTAMICUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 33846522527     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwl066     Document Type: Article

References (47)

1. Alderwick LJ, Dover L, Seidel M, Gande R, Sahm H, Eggeling L, Besra GS. 2006. Arabinan deficient mutants of Corynebacterium glutamicum and the consequent flux in decaprenylmonophosphoryl-D-arabinose metabolism. Glycobiology. 16:1073-1081.
2. Alderwick LJ, Radmacher E, Seidel M, Gande R, Hitchen PG, Morris HR, Dell A, Sahm H, Eggeling L, Besra GS. 2005. 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. 280:32362-32371.
3. 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.
4. Alexeyev MF, Winkler HH. 1999. Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho-lac reporters. J Mol Biol. 285:1503-1513.
5. Becker A, Pühler A. 1998. Specific amino acid substitutions in the prolinerich motif of the Rhizobium meliloti ExoP protein result in enhanced production of low-molecular-weight succinoglycan at the expense of high-molecular-weight succinoglycan. J Bacteriol. 180:395-399.
6. Berg S, Starbuck J, Torrelles JB, Vissa V, Crick DC, Chatterjee D, Brennan PJ. 2005. Roles of conserved proline and glycosyltransferase motifs of EmbC in biosynthesis of lipoarabinomannan. J Biol Chem. 280: 5651-5663.
7. Besra GS, Khoo KH, McNeil MR, Dell A, Morris HR, Brennan PJ. 1995. A new interpretation of the structure of the mycolyl-arabinogalactan complex of Mycobacterium tuberculosis as revealed through characterization of oligoglycosylalditol fragments by fast-atom bombardment mass spectrometry and 1H nuclear magnetic resonance spectroscopy. Biochemistry. 34:4257-4266.
8. Bloom BR, Murray CJ. 1992. Tuberculosis: Commentary on a reemergent killer. Science. 257:1055-1064.
9. Brickman E, Beckwith J. 1975. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J Mol Biol. 96:307-316.
10. Calamia J, Manoil C. 1990. Lac permease of Escherichia coli: Topology and sequence elements promoting membrane insertion. Proc Natl Acad Sci USA. 87:4937-4941.
11. Chatterjee D, Hunter SW, McNeil M, Brennan PJ. 1992. Lipoarabinomannan. Multiglycosylated form of the mycobacterial mannosylphosphatidylinositols. J Biol Chem. 267:6228-33.
12. Cserzö M, Wallin E, Simon I, von Heijne G, Elofsson A. 1997. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: The dense alignment surface method. Protein Eng. 10:673-676.
13. Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ. 1998. JPred: A consensus secondary structure prediction server. Bioinformatics. 14: 892-893.
14. Daffe M, Brennan PJ, McNeil M. 1990. Predominant structural features of the cell wall arabinogalactan of Mycobacterium tuberculosis as revealed through characterization of oligoglycosyl alditol fragments by gas chromatography/mass spectrometry and by 1H and 13C NMR analyses. J Biol Chem. 265:6734-6743.
15. Daniels C, Morona R. 1999. Analysis of Shigella flexneri wzz (Rol) function by mutagenesis and cross-linking: Wzz is able to oligomerize. Mol Microbiol. 34:181-194.
16. Deisenhofer J, Michel H. 1989. Nobel lecture. The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J. 8: 2149-2170.
17. Eggeling L, Bott M. 2005. Handbook of Corynebacterium glutamicum. Boca Raton (FL): CRC Press, Taylor Francis Group.
18. Escuyer VE, Lety MA, Torrelles JB, Khoo KH, Tang J, Rithner CD, Frehel C, McNei MR, Brennan PJ, Chatterjee D. 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.
19. Gande R, Gibson KJ, Brown AK, Krumbach K, Dover LG, Sahm H, Shioyama S, Oikawa T, Besra GS, Eggeling L. 2004. Acyl-CoA carboxylases (accD2 and accD3), together with a unique polyketide synthase (Cg-pks), are key to mycolic acid biosynthesis in Corynebacterianeae such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J Biol Chem. 279:44847-44857.
20. Gibson KJ, Eggeling L, Maughan WN, Krumbach K, Gurcha SS, Nigou J, Puzo G, Sahm H, Besra GS. 2003. Disruption of Cg-Ppm1, a polyprenyl monophosphomannose synthase, and the generation of lipoglycan-less mutants in Corynebacterium glutamicum. J Biol Chem. 278: 40842-40850.
21. Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R. 1996. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol. 259:393-421.
22. Henikoff S. 1984. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 28:351-359.
23. Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A, Dusch N, Eggeling L, Eikmanns BJ, Gaigalat L, et al. 2003. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol. 104:5-25.
24. Kremer L, Dover LG, Morehouse C, Hitchin P, Everett M, Morris HR, Dell A, Brennan PJ, McNeil MR, Flaherty C, et al. 2001. Galactan biosynthesis in Mycobacterium tuberculosis. Identification of a bifunctional UDP-galactofuranosyltransferase. J Biol Chem. 276:26430-26440.
25. Landt O, Grunert HP, Hahn U. 1990. A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene. 96:125-128.
26. Liu J, Mushegian A. 2003. Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci. 12:1418-1431.
27. Maeda Y, Watanabe R, Harris CL, Hong Y, Ohishi K, Kinoshita K, Kinoshita T. 2001. PIG-M transfers the first mannose to glycosylphosphatidylinositol on the lumenal side of the ER. EMBO J. 20:250-261.
28. McNeil M, Daffe M, Brennan PJ. 1990. Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J Biol Chem. 265:18200-18206.
29. McNeil M, Daffe M, Brennan P. 1991. Location of the mycolyl ester substituents in the cell walls of mycobacteria. J Biol Chem. 266:13217-13223.
30. Mikusova K, Yagi T, Stern R, McNeil MR, Besra GS, Crick DC, Brennan PJ. 2000. Biosynthesis of the galactan component of the mycobacterial cell wall. J Biol Chem. 275:33890-33897.
31. Miller JH. 1992. A Short Course in Bacterial Genetics. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory.
32. Mills JA, Motichka K, Jucker M, Wu HP, Uhlik BC, Stern RJ, Scherman MS, Vissa VD, Pan F, Kundu M et al. 2004. Inactivation of the mycobacterial rhamnosyltransferase, which is needed for the formation of the arabinogalactan-peptidoglycan linker, leads to irreversible loss of viability. J Biol Chem. 279:43540-43546.
33. Morona R, van den Bosch L, Manning PA. 1995. Molecular, genetic, and topological characterization of O-antigen chain length regulation in Shigella flexneri. J Bacteriol. 177:1059-1068.
34. Nakamura Y, Nishio Y, Ikeo K, Gojobori T. 2003. The genome stability in Corynebacterium species due to lack of the recombinational repair system. Gene. 317:149-155.
35. Oriol R, Martinez-Duncker I, Chantret I, Mollicone R, Codogno P. 2002. Common origin and evolution of glycosyltransferases using Dol-P-monosaccharides as donor substrate. Mol Biol Evol. 19:1451-1463.
36. Pan F, Jackson M, Ma Y, McNeil M. 2001. Cell wall core galactofuran synthesis is essential for growth of mycobacteria. J Bacteriol. 183: 3991-3998.
37. Pohlschröder M, Hartmann E, Hand NJ, Dilks K, Haddad A. 2005. Diversity and evolution of protein translocation. Annu Rev Microbiol. 59:91-111.
38. Portevin D, De Sousa-D'Auria C, Houssin C, Grimaldi C, Chami M, Daffe M, Guilhot C. 2004. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci USA. 101:314-319.
39. Radmacher E, Stansen KC, Besra GS, Alderwick LJ, Maughan WN, Hollweg G, Sahm H, Wendisch VF, Eggeling L. 2005. Ethambutol, a cell wall inhibitor of Mycobacterium tuberculosis, elicits L-glutamate efflux of Corynebacterium glutamicum. Microbiology. 151:1359-1368.
40. Ramaswamy SV, Amin AG, Goksel S, Stager CE, Dou SJ, El Sahly H, Moghazeh SL, Kreiswirth BN, Musser JM. 2000. Molecular genetic analysis of nucleotide polymorphisms associated with ethambutol resistance in human isolates of Mycobacterium tuberculosis. Antimicrob Agents Chemother. 44:326-336.
41. Shi L, Berg S, Lee A, Spencer JS, Zhang J, Vissa V, McNeil MR, Khoo KH, Chatterjee D. 2006. The carboxy terminus of EmbC from Mycobacterium smegmatis mediates chain length extension of the arabinan in lipoarabinomannan. J Biol Chem. 281:19512-19526.
42. Subramanian AR, Weyer-Menkhoff J, Kaufmann M, Morgenstern B. 2005. DIALIGN-T: An improved algorithm for segment-based multiple sequence alignment BMC. Bioinformatics. 6:66.
43. Takayama K, Kilburn JO. 1989. Inhibition of synthesis of arabinogalactan by ethambutol in Mycobacterium smegmatis. Antimicrob Agents Chemother. 33:1493-1499.
44. Telenti A, Philipp WJ, Sreevatsan S, Bernasconi C, Stockbauer KE, Wieles B, Musser JM, Jacobs WR Jr. 1997. The emb operon, a gene cluster of Mycobacterium tuberculosis involved in resistance to ethambutol. Nat Med. 3:567-570.
45. Vilcheze C, Morbidoni HR, Weisbrod TR, Iwamoto H Kuo M, Sacchettini JC, Jacobs WR Jr. 2000. Inactivation of the inhA-encoded fatty acid synthase II (FASII) enoyl-acyl carrier protein reductase induces accumulation of the FASI end products and cell lysis of Mycobacterium smegmatis. J Bacteriol. 182:4059-4067.
46. Yernool D, Boudker O, Jin Y, Gouaux E. 2004. Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature. 431: 811-818.
47. Zhang N, Torrelles JB, McNeil MR, Escuyer VE, Khoo KH, Brennan PJ, Chatterjee D. 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.