A small multidrug resistance-like transporter involved in the arabinosylation of arabinogalactan and lipoarabinomannan in mycobacteria

Journal of Biological Chemistry

Volumn 287, Issue 47, 2012, Pages 39933-39941

  Larrouy Maumus, Gérald ^a,b   Škovierová, Henrieta ^c,d,e   Dhouib, Rabeb ^c   Angala, Shiva Kumar ^c   Zuberogoitia, Sophie ^a,b   Pham, Ha ^c   Villela, Anne Drumond ^c   Mikušová, Katarina ^d   Noguera, Audrey ^a,b   Gilleron, Martine ^a,b   Valentínová, Lucia ^d,f   Korduláková, Jana ^d   Brennan, Patrick J ^c   Puzo, Germain ^a,b   Nigou, Jérôme ^a,b   Jackson, Mary ^c  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c Department of Environmental and Radiological Health Sciences   (United States)

^d Faculty of Natural Sciences   (Slovakia)

^e University Hospital in Martin   (Slovakia)

^f INSTITUTE OF EXPERIMENTAL ENDOCRINOLOGY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINANS; ARABINOGALACTAN; CELL ENVELOPES; D-ARABINOSE; GALACTANS; GALACTOSYLTRANSFERASE; GLYCOCONJUGATES; GLYCOPOLYMERS; IN-VIVO; LIPOARABINOMANNANS; M. TUBERCULOSIS; MULTIDRUG RESISTANCE; MUTANT CELLS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; ORTHOLOGS; PERIPLASM; TRANSLOCASES; TWO-HYBRID SYSTEM; UNDECAPRENYL PHOSPHATE;

BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; ESCHERICHIA COLI; GENE EXPRESSION; HYBRID SYSTEMS; SUGARS; TUBES (COMPONENTS);

CELL MEMBRANES;

ACRIFLAVINE; AMPICILLIN; ARABINOGALACTAN; ARABINOSE; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CIPROFLOXACIN; DECAPRENYL MONOPHOSPHORYL BETA DEXTRO ARABINOSE; ETHAMBUTOL; GALACTAN; GALACTOSYLTRANSFERASE; ISONIAZID; LIPOARABINOMANNAN; RESERPINE; RIFAMPICIN; STREPTOMYCIN; UNCLASSIFIED DRUG;

ARABINOSYLATION; ARNE GENE; ARNF GENE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BIOSYNTHESIS; CONTROLLED STUDY; DPRE1 GENE; DPRE2 GENE; ESCHERICHIA COLI; GENE EXPRESSION; MINIMUM INHIBITORY CONCENTRATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; RV3789 GENE;

ARABINOSE; BACTERIAL PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GALACTANS; GENETIC COMPLEMENTATION TEST; GLYCOSYLATION; LIPOPOLYSACCHARIDES; MEMBRANE TRANSPORT PROTEINS; MUTATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; ESCHERICHIA COLI; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTA;

EID: 84869219067     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.400986     Document Type: Article

References (38)

1. Kaur, D., Guerin, M. E., Škovierová, H., Brennan, P. J., and Jackson, M. (2009) Biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv. Appl. Microbiol. 69, 23-78
2. Wolucka, B. A., McNeil, M. R., de Hoffmann, E., Chojnacki, T., and Brennan, P. J. (1994) Recognition of the lipid intermediate for arbinogalactan/arabinomannan biosynthesis and its relation to the mode of action of ethambutol on mycobacteria. J. Biol. Chem. 269, 23328-23335 (Pubitemid 24283325)
3. Berg, S., Kaur, D., Jackson, M., and Brennan, P. J. (2007) The glycosyltransferases of Mycobacterium tuberculosis. Roles in the synthesis of arabinogalactan, lipoarabinomannan, and other glycoconjugates. Glycobiology 17, 35R-56R (Pubitemid 47062700)
4. Daleke, D. L. (2007) Phospholipid flippases. J. Biol. Chem. 282, 821-825
5. Sanyal, S., Frank, C. G., and Menon, A. K. (2008) Distinct flippases translocate glycerophospholipids and oligosaccharide diphosphate dolichols across the endoplasmic reticulum. Biochemistry 47, 7937-7946
6. Feldman, M. F., Marolda, C. L., Monteiro, M. A., Perry, M. B., Parodi, A. J., and Valvano, M. A. (1999) The activity of a putative polyisoprenol-linked sugar translocase (Wzx) involved in Escherichia coli Oantigen assembly is independent of the chemical structure of the O repeat. J. Biol. Chem. 274, 35129-35138 (Pubitemid 129509568)
7. Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700 (Pubitemid 34800232)
8. Rick, P. D., Barr, K., Sankaran, K., Kajimura, J., Rush, J. S., and Waechter, C. J. (2003) Evidence that the wzxE gene of Escherichia coli K-12 encodes a protein involved in the transbilayer movement of a trisaccharide-lipid intermediate in the assembly of enterobacterial common antigen. J. Biol. Chem. 278, 16534-16542 (Pubitemid 36799514)
9. Whitfield, C. (2006) Biosynthesis and assembly of capsular polysaccharides in. Escherichia coli. Annu. Rev. Biochem. 75, 39-68
10. Alaimo, C., Catrein, I., Morf, L., Marolda, C. L., Callewaert, N., Valvano, M. A., Feldman, M. F., and Aebi, M. (2006) Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBOJ. 25, 967-976 (Pubitemid 43372111)
11. Raetz, C. R., Reynolds, C. M., Trent, M. S., and Bishop, R. E. (2007) Lipid A modification systems in Gram-negative bacteria. Annu. Rev. Biochem. 76, 295-329
12. Mohammadi, T., van Dam, V., Sijbrandi, R., Vernet, T., Zapun, A., Bouhss, A., Diepeveen-de Bruin, M., Nguyen-Distèche, M., de Kruijff, B., and Breukink, E. (2011) Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J. 30, 1425-1432
13. Henriques, A. O., Glaser, P., Piggot, P. J., and Moran, C. P., Jr. (1998) Control of cell shape and elongation by the rodA gene in. Bacillus subtilis. Mol. Microbiol. 28, 235-247 (Pubitemid 28182248)
14. Bay, D. C., Rommens, K. L., and Turner, R. J. (2008) Small multidrug resistance proteins. A multidrug transporter family that continues to grow. Biochim. Biophys. Acta 1778, 1814-1838
15. Yan, A., Guan, Z., and Raetz, C. R. (2007) An undecaprenyl phosphate-aminoarabinose flippase required for polymyxin resistance in Escherichia coli. J. Biol. Chem. 282, 36077-36089 (Pubitemid 350277131)
16. Guan, S., Bastin, D. A., and Verma, N. K. (1999) Functional analysis of the O antigen glucosylation gene cluster of Shigella flexneri bacteriophage SfX. Microbiology 145, 1263-1273 (Pubitemid 29231831)
17. Korres, H., Mavris, M., Morona, R., Manning, P. A., and Verma, N. K. (2005) Topological analysis of GtrA and GtrB proteins encoded by the serotype-converting cassette of. Shigella flexneri. Biochem. Biophys. Res. Commun. 328, 1252-1260 (Pubitemid 40246327)
18. Škovierová, H., Larrouy-Maumus, G., Pham, H., Belanová, M., Barilone, N., Dasgupta, A., Mikušová, K., Gicquel, B., Gilleron, M., Brennan, P. J., Puzo, G., Nigou, J., and Jackson, M. (2010) Biosynthetic origin of the galactosamine substituent of arabinogalactan in Mycobacterium tuberculosis. J. Biol. Chem. 285, 41348-41355
19. Korduláková, J., Gilleron, M., Mikušová, K., Puzo, G., Brennan, P. J., Gicquel, B., and Jackson, M. (2002) Definition of the first mannosylation step in phosphatidylinositol synthesis. PimA is essential for growth of mycobacteria. J. Biol. Chem. 277, 31335-31344 (Pubitemid 34968932)
20. Marolda, C. L., Feldman, M. F., and Valvano, M. A. (1999) Genetic organization of the O7-specific lipopolysaccharide biosynthetic cluster of Escherichia coli VW187 (O7:K1). Microbiology 145, 2485-2495 (Pubitemid 29454366)
21. Marolda, C. L., Vicarioli, J., and Valvano, M. A. (2004) Wzx proteins involved in biosynthesis of O antigen function in association with the first sugar of the O-specific lipopolysaccharide subunit. Microbiology 150, 4095-4105 (Pubitemid 40045338)
22. Grzegorzewicz, A. E., Pham, H., Gundi, V. A., Scherman, M. S., North, E. J., Hess, T., Jones, V., Gruppo, V., Born, S. E., Korduláková, J., Chavadi, S. S., Morisseau, C., Lenaerts, A. J., Lee, R. E., McNeil, M. R., and Jackson, M. (2012) Inhibition of mycolic acid transport across the Mycobacterium tuberculosis plasma membrane. Nat. Chem. Biol. 8, 334-341
23. De Rossi, E., Branzoni, M., Cantoni, R., Milano, A., Riccardi, G., and Ciferri, O. (1998) mmr, a Mycobacterium tuberculosis gene conferring resistance to small cationic dyes and inhibitors. J. Bacteriol. 180, 6068-6071 (Pubitemid 28514231)
24. 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)
25. Mikušová, K., Belánová, M., Korduláková, J., Honda, K., McNeil, M. R., Mahapatra, S., Crick, D. C., and Brennan, P. J. (2006) Identification of a novel galactosyl transferase involved in biosynthesis of the mycobacterial cell wall. J. Bacteriol. 188, 6592-6598 (Pubitemid 44412070)
26. Scherman, M. S., Kalbe-Bournonville, L., Bush, D., Xin, Y., Deng, L., and McNeil, M. (1996) Polyprenylphosphate-pentoses in mycobacteria are synthesized from 5-phosphoribose pyrophosphate. J. Biol. Chem. 271, 29652-29658 (Pubitemid 26389589)
27. Mikušová, K., Yagi, T., Stern, R., McNeil, M. R., Besra, G. S., Crick, D. C., and Brennan, P. J. (2000) Biosynthesis of the galactan component of the mycobacterial cell wall. J. Biol. Chem. 275, 33890-33897
28. Goude, R., Amin, A. G., Chatterjee, D., and Parish, T. (2008) The critical role of embC in Mycobacterium tuberculosis. J. Bacteriol. 190, 4335-4341 (Pubitemid 351812881)
29. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 5752-5756 (Pubitemid 28224168)
30. Baulard, A. R., Gurcha, S. S., Engohang-Ndong, J., Gouffi, K., Locht, C., and Besra, G. S. (2003) In vivo interaction between the polyprenol phosphate mannose synthase Ppm1 and the integral membrane protein Ppm2 from Mycobacterium smegmatis revealed by a bacterial two-hybrid system. J. Biol. Chem. 278, 2242-2248 (Pubitemid 36801292)
31. Clarke, B. R., Greenfield, L. K., Bouwman, C., and Whitfield, C. (2009) Coordination of polymerization, chain termination, and export in assembly of the Escherichia coli lipopolysaccharide O9a antigen in an ABC-transporter-dependent pathway. J. Biol. Chem. 284, 30662-30672
32. Schuldiner, S. (2009) EmrE, a model for studying evolution and mechanism of ion-coupled transporters. Biochim. Biophys. Acta 1794, 748-762
33. Liu, D., Cole, R. A., and Reeves, P. R. (1996) An O-antigen processing function for Wzx (RfbX). A promising candidate for O-unit flippase. J. Bacteriol. 178, 2102-2107 (Pubitemid 26111329)
34. Ninio, S., Rotem, D., and Schuldiner, S. (2001) Functional analysis of novel multidrug transporters from human pathogens. J. Biol. Chem. 276, 48250-48256
35. Wolucka, B. A. (2008) Biosynthesis of D-arabinose in mycobacteria. A novel bacterial pathway with implications for antimycobacterial therapy. FEBS J. 275, 2691-2711
36. Hug, I., Couturier, M. R., Rooker, M. M., Taylor, D. E., Stein, M., and Feldman, M. F. (2010) Helicobacter pylori lipopolysaccharide is synthesized via a novel pathway with an evolutionary connection to protein N-glycosylation. PLoS Pathog. 6, e1000819
37. Kremer, L., Dover, L. G., Morehouse, C., Hitchin, P., Everett, M., Morris, H. R., Dell, A., Brennan, P. J., McNeil, M. R., Flaherty, C., Duncan, K., and Besra, G. S. (2001) Galactan biosynthesis in Mycobacterium tuberculosis. Identification of a bifunctional UDP-galactofuranosyltransferase. J. Biol. Chem. 276, 26430-26440
38. Marolda, C. L., Tatar, L. D., Alaimo, C., Aebi, M., and Valvano, M. A. (2006) Interplay of the Wzx translocase and the corresponding polymerase and chain length regulator proteins in the translocation and periplasmic assembly of lipopolysaccharide O antigen. J. Bacteriol. 188, 5124-5135 . (Pubitemid 44051478)