The lipoprotein LpqW is essential for the mannosylation of periplasmic glycolipids in corynebacteria

Journal of Biological Chemistry

Volumn 287, Issue 51, 2012, Pages 42726-42738

  Rainczuk, Arek K ^a   Yamaryo Botte, Yoshiki ^b   Brammananth, Rajini ^a   Stinear, Timothy P ^c   Seemann, Torsten ^a   Coppel, Ross L ^a   McConville, Malcolm J ^b   Crellin, Paul K ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; BIOSYNTHETIC PATHWAY; CELL WALLS; CELL-FREE EXTRACTS; CORYNEBACTERIUM GLUTAMICUM; ESSENTIAL COMPONENT; GLYCO LIPIDS; HUMAN PATHOGENS; LIPOARABINOMANNANS; LIPOMANNAN; MEMBRANE ANCHORS; MYCOBACTERIUM TUBERCULOSIS; ORTHOLOGS; PHOSPHATIDYLINOSITOL; SLOW GROWTH; SYNTHASES;

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CYTOLOGY; GLUCOSE; GLYCEROL; LIPIDS;

CELL MEMBRANES;

BACTERIAL PROTEIN; GLYCOLIPID; LIPOARABINOMANNAN; LIPOMANNAN A; LIPOMANNAN B; LIPOPROTEIN; MANNOSYLTRANSFERASE; MANNOSYLTRANSFERASE MPTB; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL MANNOSIDE; POLYPRENOL PHOSPHOMANNOSE SYNTHASE; PROTEIN LPQW; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CELL COMPARTMENTALIZATION; CELL FREE SYSTEM; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; ENZYME ACTIVITY; GENETIC ASSOCIATION; LIPOGENESIS; MEMBRANE LEAFLET; NCGL1054 GENE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; SEQUENCE ANALYSIS;

BACTERIAL PROTEINS; BIOSYNTHETIC PATHWAYS; CELL WALL; CORYNEBACTERIUM GLUTAMICUM; GENE SILENCING; GENE TARGETING; GENETIC COMPLEMENTATION TEST; GLYCOLIPIDS; HUMANS; LIPOPOLYSACCHARIDES; LIPOPROTEINS; MANNOSE; MANNOSYLTRANSFERASES; MUTATION; PERIPLASM; SUPPRESSION, GENETIC;

CORYNEBACTERIACEAE; CORYNEBACTERINEAE; CORYNEBACTERIUM GLUTAMICUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 84871177385     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.373415     Document Type: Article

References (59)

1. Reyrat, J. M., and Kahn, D. (2001) Mycobacterium smegmatis: an absurd model for tuberculosis? Trends Microbiol. 9, 472-474
2. Barksdale, L. (1970) Corynebacterium diphtheriae and its relatives. Bacteriol. Rev. 34, 378-422
3. Barry, C. E., 3rd, and Mdluli, K. (1996) Drug sensitivity and environmental adaptation of mycobacterial cell wall components. Trends Microbiol. 4, 275-281
4. Haites, R. E., Morita, Y. S., McConville, M. J., and Billman-Jacobe, H. (2005) Function of phosphatidylinositol in mycobacteria. J. Biol. Chem. 280, 10981-10987 (Pubitemid 40418400)
5. Skovierová, H., Larrouy-Maumus, G., Zhang, J., Kaur, D., Barilone, N., Korduláková, J., Gilleron, M., Guadagnini, S., Belanová, M., Prevost, M. C., Gicquel, B., Puzo, G., Chatterjee, D., Brennan, P. J., Nigou, J., and Jackson, M. (2009) AftD, a novel essential arabinofuranosyltransferase from mycobacteria. Glycobiology 19, 1235-1247
6. Barry, C. E., 3rd, Lee, R. E., Mdluli, K., Sampson, A. E., Schroeder, B. G., Slayden, R. A., and Yuan, Y. (1998) Mycolic acids: structure, biosynthesis and physiological functions. Prog. Lipid Res. 37, 143-179 (Pubitemid 28391410)
7. Mishra, A. K., Driessen, N. N., Appelmelk, B. J., and Besra, G. S. (2011) Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction. FEMS Microbiol. Rev. 35, 1126-1157
8. Gande, R., Gibson, K. J., Brown, A. K., Krumbach, K., Dover, L. G., Sahm, H., Shioyama, S., Oikawa, T., Besra, G. S., and 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 (Pubitemid 39430897)
9. 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. (2005) Deletion of Cg-emb in corynebacterianeae leads to a novel truncated cell wall arabinogalactan, whereas inactivation of Cg-ubiA results in an arabi-nan- deficient mutant with a cell wall galactan core. J. Biol. Chem. 280, 32362-32371 (Pubitemid 41361846)
10. Alderwick, L. J., Seidel, M., Sahm, H., Besra, G. S., and Eggeling, L. (2006) Identification of a novel arabinofuranosyltransferase (AftA) involved in cell wall arabinan biosynthesis in Mycobacterium tuberculosis. J. Biol. Chem. 281, 15653-15661 (Pubitemid 43848451)
11. Lea-Smith, D. J., Pyke, J. S., Tull, D., McConville, M. J., Coppel, R. L., and Crellin, P. K. (2007) The reductase that catalyzes mycolic motif synthesis is required for efficient attachment of mycolic acids to arabinogalactan. J. Biol. Chem. 282, 11000-11008 (Pubitemid 47100777)
12. Mishra, A. K., Alderwick, L. J., Rittmann, D., Tatituri, R. V., Nigou, J., Gilleron, M., Eggeling, L., and Besra, G. S. (2007) Identification of an alpha(1-6) mannopyranosyltransferase (MptA), involved in Corynebacterium glutamicum lipomanann biosynthesis, and identification of its orthologue in Mycobacterium tuberculosis. Mol. Microbiol. 65, 1503-1517 (Pubitemid 47347833)
13. Seidel, M., Alderwick, L. J., Birch, H. L., Sahm, H., Eggeling, L., and Besra, G. S. (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 (Pubitemid 47093349)
14. Seidel, M., Alderwick, L. J., Sahm, H., Besra, G. S., and 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 (Pubitemid 46152537)
15. Birch, H. L., Alderwick, L. J., Bhatt, A., Rittmann, D., Krumbach, K., Singh, A., Bai, Y., Lowary, T. L., Eggeling, L., and Besra, G. S. (2008) Biosynthesis of mycobacterial arabinogalactan: identification of a novel α(1→3) arabinofuranosyltransferase. Mol. Microbiol. 69, 1191-1206
16. Lea-Smith, D. J., Martin, K. L., Pyke, J. S., Tull, D., McConville, M. J., Coppel, R. L., and Crellin, P. K. (2008) Analysis of a new mannosyltransferase required for the synthesis of phosphatidylinositol mannosides and lipoarbinomannan reveals two lipomannan pools in corynebacterineae. J. Biol. Chem. 283, 6773-6782
17. Mishra, A. K., Alderwick, L. J., Rittmann, D., Wang, C., Bhatt, A., Jacobs, W. R., Jr., Takayama, K., Eggeling, L., and Besra, G. S. (2008) Identification of a novel alpha(1-6) mannopyranosyltransferase MptB from Corynebacterium glutamicum by deletion of a conserved gene, NCgl1505, affords a lipomannan- and lipoarabinomannan-deficient mutant. Mol. Microbiol. 68, 1595-1613 (Pubitemid 351725269)
18. Mishra, A. K., Klein, C., Gurcha, S. S., Alderwick, L. J., Babu, P., Hitchen, P. G., Morris, H. R., Dell, A., Besra, G. S., and Eggeling, L. (2008) Structural characterization and functional properties of a novel lipomannan variant isolated from a Corynebacterium glutamicum pimB′ mutant. Antonie Van Leeuwenhoek 94, 277-287
19. Chatterjee, D., and Khoo, K. H. (1998) Mycobacterial lipoarabinomannan: an extraordinary lipoheteroglycan with profound physiological effects. Glycobiology 8, 113-120 (Pubitemid 28098211)
20. Strohmeier, G. R., and Fenton, M. J. (1999) Roles of lipoarabinomannan in the pathogenesis of tuberculosis. Microbes Infect. 1, 709-717
21. Vercellone, A., Nigou, J., and Puzo, G. (1998) Relationships between the structure and the roles of lipoarabinomannans and related glycoconjugates in tuberculosis pathogenesis. Front. Biosci. 3, e149-163
22. Nigou, J., Gilleron, M., Rojas, M., García, L. F., Thurnher, M., and Puzo, G. (2002) Mycobacterial lipoarabinomannans: modulators of dendritic cell function and the apoptotic response. Microbes Infect. 4, 945-953 (Pubitemid 34775236)
23. Korduláková, J., Gilleron, M., Mikusova, K., Puzo, G., Brennan, P. J., Gicquel, B., and Jackson, M. (2002) Definition of the first mannosylation step in phosphatidylinositol mannoside synthesis. PimA is essential for growth of mycobacteria. J. Biol. Chem. 277, 31335-31344 (Pubitemid 34968932)
24. Guerin, M. E., Kaur, D., Somashekar, B. S., Gibbs, S., Gest, P., Chatterjee, D., Brennan, P. J., and Jackson, M. (2009) New insights into the early steps of phosphatidylinositol mannoside biosynthesis in mycobacteria: PimB′ is an essential enzyme of Mycobacterium smegmatis. J. Biol. Chem. 284, 25687-25696
25. Korduláková, J., Gilleron, M., Puzo, G., Brennan, P. J., Gicquel, B., Mikusová, K., and Jackson, M. (2003) Identification of the required acyltransferase step in the biosynthesis of the phosphatidylinositol mannosides of Mycobacterium species. J. Biol. Chem. 278, 36285-36295 (Pubitemid 37139953)
26. Besra, G. S., Morehouse, C. B., Rittner, C. M., Waechter, C. J., and Brennan, P. J. (1997) Biosynthesis of mycobacterial lipoarabinomannan. J. Biol. Chem. 272, 18460-18466 (Pubitemid 27306441)
27. Gibson, K. J., Eggeling, L., Maughan, W. N., Krumbach, K., Gurcha, S. S., Nigou, J., Puzo, G., Sahm, H., and Besra, G. S. (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 (Pubitemid 37280902)
28. 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. (2002) Ppm1, a novel polyprenol monophosphomannose synthase from Mycobacterium tuberculosis. Biochem. J. 365, 441-450 (Pubitemid 36135315)
29. Zhang, N., Torrelles, J. B., McNeil, M. R., Escuyer, V. E., Khoo, K. H., Brennan, P. J., and 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 (Pubitemid 37222787)
30. Morita, Y. S., Patterson, J. H., Billman-Jacobe, H., and McConville, M. J. (2004) Biosynthesis of mycobacterial phosphatidylinositol mannosides. Biochemical Journal 378, 589-597 (Pubitemid 38367248)
31. Morita, Y. S., Sena, C. B., Waller, R. F., Kurokawa, K., Sernee, M. F., Nakatani, F., Haites, R. E., Billman-Jacobe, H., McConville, M. J., Maeda, Y., and Kinoshita, T. (2006) PimE is a polyprenol-phosphate-mannose-dependent mannosyltransferase that transfers the fifth mannose of phosphatidylinositol mannoside in mycobacteria. J. Biol. Chem. 281, 25143-25155 (Pubitemid 44401901)
32. 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. (2006) Biosynthesis of mycobacterial lipoarabinomannan: role of a branching mannosyltransferase. Proc. Natl. Acad. Sci. U.S.A. 103, 13664-13669 (Pubitemid 44413964)
33. Kaur, D., McNeil, M. R., Khoo, K. H., Chatterjee, D., Crick, D. C., Jackson, M., and Brennan, P. J. (2007) New insights into the biosynthesis of mycobacterial lipomannan arising from deletion of a conserved gene. J. Biol. Chem. 282, 27133-27140 (Pubitemid 47501909)
34. Newton, G. L., Ko, M., Ta, P., Av-Gay, Y., and Fahey, R. C. (2006) Purification and characterization of Mycobacterium tuberculosis 1D-myo-inosityl-2-acetamido-2-deoxy-α-D-glucopyranoside deacetylase, MshB, a mycothiol biosynthetic enzyme. Protein Expr. Purif. 47, 542-550 (Pubitemid 43729027)
35. Sena, C. B., Fukuda, T., Miyanagi, K., Matsumoto, S., Kobayashi, K., Murakami, Y., Maeda, Y., Kinoshita, T., and Morita, Y. S. (2010) Controlled expression of branch-forming mannosyltransferase is critical for mycobacterial lipoarabinomannan biosynthesis. J. Biol. Chem. 285, 13326-13336
36. Kaur, D., Obregón-Henao, A., Pham, H., Chatterjee, D., Brennan, P. J., and Jackson, M. (2008) Lipoarabinomannan of Mycobacterium: mannose capping by a multifunctional terminal mannosyltransferase. Proc. Natl. Acad. Sci. U.S.A. 105, 17973-17977
37. Alderwick, L. J., Lloyd, G. S., Ghadbane, H., May, J. W., Bhatt, A., Eggeling, L., Fütterer, K., and Besra, G. S. (2011) The C-terminal domain of the arabinosyltransferase Mycobacterium tuberculosis EmbC is a lectin-like carbohydrate binding module. PLoS Pathog. 7, e1001299
38. Tatituri, R. V., Illarionov, P. A., Dover, L. G., Nigou, J., Gilleron, M., Hitchen, P., Krumbach, K., Morris, H. R., Spencer, N., Dell, A., Eggeling, L., and Besra, G. S. (2007) Inactivation of Corynebacterium glutamicum NCgl0452 and the role of MgtA in the biosynthesis of a novel mannosylated glycolipid involved in lipomannan biosynthesis. J. Biol. Chem. 282, 4561-4572 (Pubitemid 47100964)
39. Mishra, A. K., Batt, S., Krumbach, K., Eggeling, L., and Besra, G. S. (2009) Characterization of the Corynebacterium glutamicum ΔpimB′ ΔmgtA double deletion mutant and the role of Mycobacterium tuberculosis orthologues Rv2188c and Rv0557 in glycolipid biosynthesis. J. Bacteriol. 191, 4465-4472
40. Sassetti, C. M., Boyd, D. H., and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84 (Pubitemid 36411469)
41. Kovacevic, S., Anderson, D., Morita, Y. S., Patterson, J., Haites, R., Mc-Millan, B. N., Coppel, R., McConville, M. J., and Billman-Jacobe, H. (2006) Identification of a novel protein with a role in lipoarabinomannan biosynthesis in mycobacteria. J. Biol. Chem. 281, 9011-9017 (Pubitemid 43864613)
42. Marland, Z., Beddoe, T., Zaker-Tabrizi, L., Lucet, I. S., Brammananth, R., Whisstock, J. C., Wilce, M. C., Coppel, R. L., Crellin, P. K., and Rossjohn, J. (2006) Hijacking of a substrate-binding protein scaffold for use in mycobacterial cell wall biosynthesis. J. Mol. Biol. 359, 983-997 (Pubitemid 43831927)
43. Crellin, P. K., Kovacevic, S., Martin, K. L., Brammananth, R., Morita, Y. S., Billman-Jacobe, H., McConville, M. J., and Coppel, R. L. (2008) Mutations in pimE restore lipoarabinomannan synthesis and growth in a Mycobacterium smegmatis lpqW mutant. J. Bacteriol. 190, 3690-3699
44. Thanky, N. R., Young, D. B., and Robertson, B. D. (2007) Unusual features of the cell cycle in mycobacteria: polar-restricted growth and the snapping-model of cell division. Tuberculosis 87, 231-236 (Pubitemid 46551845)
45. van der Rest, M. E., Lange, C., and Molenaar, D. (1999) A heat shock following electroporation induces highly efficient transformation of Corynebacterium glutamicum with xenogeneic plasmid DNA. Appl. Microbiol. Biotechnol. 52, 541-545 (Pubitemid 29513334)
46. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
47. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119 (Pubitemid 15122816)
48. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G., and Pühler, A. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69-73
49. McKean, S., Davies, J., and Moore, R. (2005) Identification of macrophage induced genes of Corynebacterium pseudotuberculosis by differential fluorescence induction. Microbes Infect. 7, 1352-1363 (Pubitemid 41572312)
50. McConville, M. J., Homans, S. W., Thomas-Oates, J. E., Dell, A., and Bacic, A. (1990) Structures of the glycoinositolphospholipids from Leishmania major. A family of novel galactofuranose-containing glycolipids. J. Biol. Chem. 265, 7385-7394
51. David, M., Dzamba, M., Lister, D., Ilie, L., and Brudno, M. (2011) SHRiMP2: sensitive yet practical SHort Read Mapping. Bioinformatics 27, 1011-1012
52. Morita, Y. S., Velasquez, R., Taig, E., Waller, R. F., Patterson, J. H., Tull, D., Williams, S. J., Billman-Jacobe, H., and McConville, M. J. (2005) Compartmentalization of lipid biosynthesis in mycobacteria. J. Biol. Chem. 280, 21645-21652 (Pubitemid 40805734)
53. Kalscheuer, R., Weinrick, B., Veeraraghavan, U., Besra, G. S., and Jacobs, W. R., Jr. (2010) Trehalose-recycling ABC transporter LpqY-SugA-SugBSugC is essential for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 107, 21761-21766
54. Ames, G. F. (1986) Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu. Rev. Biochem. 55, 397-425
55. Higgins, C. F. (1992) ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113
56. Typas, A., Banzhaf, M., Gross, C. A., and Vollmer, W. (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10, 123-136
57. Typas, A., Banzhaf, M., van den Berg van Saparoea, B., Verheul, J., Biboy, J., Nichols, R. J., Zietek, M., Beilharz, K., Kannenberg, K., von Rechenberg, M., Breukink, E., den Blaauwen, T., Gross, C. A., and Vollmer, W. (2010) Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143, 1097-1109
58. Paradis-Bleau, C., Markovski, M., Uehara, T., Lupoli, T. J., Walker, S., Kahne, D. E., and Bernhardt, T. G. (2010) Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143, 1110-1120
59. Bansal-Mutalik, R., and Nikaido, H. (2011) Quantitative lipid composition of cell envelopes of Corynebacterium glutamicum elucidated through reverse micelle extraction. Proc. Natl. Acad. Sci. U.S.A. 108, 15360-15365