Biosynthesis and translocation of unsulfated acyltrehaloses in mycobacterium tuberculosis

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27952-27965

  Manuel Belardinelli, Juan ^a   Larrouy Maumus, Gérald ^b   Jones, Victoria ^a   De Carvalho, Luiz Pedro Sorio ^b   McNeil, Michael R ^a   Jackson, Mary ^a  

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

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; CYTOLOGY; ESTERS; MACHINERY; MEMBRANES; TOPOLOGY;

HOST IMMUNE RESPONSE; INTEGRAL MEMBRANE; INTRACELLULAR SURVIVAL; MYCOBACTERIUM TUBERCULOSIS; NUMBER OF SPECIES; PERIPLASMIC SPACE; SEQUENTIAL ORDERING; TRANSESTERIFICATION REACTION;

FATTY ACIDS;

2,3 DIACYLTREHALOSE; ACYLTRANSFERASE; CARRIER PROTEIN; PENTA ACYLTREHALOSE; PROTEIN CHP2; PROTEIN FADD21; PROTEIN MMPL10; PROTEIN PAPA3; PROTEIN PKS3; PROTEIN PKS4; TREHALOSE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; CARBOHYDRATE SYNTHESIS; CARBOHYDRATE TRANSPORT; CELL MEMBRANE; CELL SURFACE; CHP2 GENE; CONTROLLED STUDY; CYTOPLASM; GENE; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; MMPL10 GENE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; TRANSESTERIFICATION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; ESTERIFICATION; GENETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ACYLTRANSFERASES; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; ESTERIFICATION; MEMBRANE TRANSPORT PROTEINS; MYCOBACTERIUM TUBERCULOSIS; TREHALOSE;

EID: 84907484281     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.581199     Document Type: Article

References (55)

1. Daffé, M., and Draper, P. (1998) The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39, 131-203
2. Daffé, M., Crick, D. C, and Jackson M. (2014) Genetics of capsular polysaccharides and cell envelope (glyco)lipids. Microbiol. Spectrum 10.1128/ microbiolspec.MGM2-0021-2013
3. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M., and Engelhardt, H. (2008) Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U.S.A. 105, 3963-3967
4. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., and Daffé, M. (2008) Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190, 5672-5680
5. Bansal-Mutalik, R., and Nikaido, H. (2014) Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc. Natl. Acad. Sci. U.S.A. 111, 4958-4963
6. Husseini, H., and Eiberg, S. (1952) Cellular reactions to phthienoic acid and related branched-chain acids. Am. Rev. Tubero. 65, 655-672
7. Kato, M., and Goren, M. B. (1974) Synergistic action of cord factor and mycobacterial sulfatides on mitochondria. Infect. Immun. 10, 733-741
8. Goren, M. B., D'Arcy Hart, P., Young, M. R., and Armstrong, J. A. (1976) Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc. Natl. Acad. Soi. U.S.A. 73, 2510-2514
9. Pabst, M. J., Gross, J. M., Brozna, J. P., and Goren, M. B. (1988) Inhibition of macrophage priming by sulfatide from Mycobacterium tuberculosis. J. Immunol. 140, 634-640
10. Zhang, L., Goren, M. B., Holzer, T. J., and Andersen, B. R. (1988) Effect of Mycobacterium tuberculosis-derived sulfolipid I on human phagocytic cells. Infect. Immun. 56, 2876-2883
11. Goren, M. B. (1990) Mycobacterial fatty acid esters of sugars and sulfosugars. In Handbook of Lipid Research. Glycolipids, phosphoglycolipids and sulfoglycolipids, Vol. 6 (Kates, M., ed) pp. 363-461, Plenum Press, New York
12. Brozna, J. P., Horan, M., Rademacher, J. M., Pabst, K. M., and Pabst, M. J. (1991) Monocyte responses to sulfolipid from Mycobacterium tuberculosis: inhibition of priming for enhanced release of superoxide, associated with increased secretion of interleuldn-1 and tumor necrosis factor α and altered protein phosphorylation. Infect. Immun. 59, 2542-2548
13. Zhang, L., English, D., and Andersen, B. R. (1991) Activation of human neutrophils by Mycobacterium tuberculosis-derived sulfolipid I.J. Immunol. 146, 2730-2736
14. Saavedra, R., Segura, E., Leyva, R., Esparza, L. A., and López-Marin, L. M. (2001) Mycobacterial di-O-acyl-trehalose inhibits mitogen- and antigeninduced proliferation of murine T cells in vitro. Clin. Diagn. Lab. Immunol. 8, 1081-1088
15. Gilleron, M., Stenger, S., Mazorra, Z., Wittke, F., Mariotti, S., Böhmer, G., Prandi, J., Mori, L., Puzo, G., and De Libero, G. (2004) Diacylated sulfoglycolipids are novel mycobacterial antigens stimulating CD1-restricted T cells during infection with Mycobacterium tuberculosis. J. Exp. Med. 199, 649-659
16. Lee, K. S., Dubey, V. S., Kolattukudy, P. E., Song, C. H., Shin, A. R., Jung, S. B., Yang, C. S., Kim, S. Y., Jo, E. K., Park, J. K., and Kim, H. J. (2007) Diacyltrehalose of Mycobacterium tuberculosis inhibits lipopolysaccharideand mycobacteria-induced proinflammatory cytokine production in human monocytic cells. FEMS Microbiol. Lett. 267, 121-128
17. Brodin, P., Poquet, Y., Levillain, F., Peguillet, I., Larrouy-Maumus, G., Gilleron, M., Ewann, F., Christophe, T., Fenistein, D., Jang, J., Jang, M. S., Park, S. J., Rauzier, J., Carralot, J. P., Shrimpton, R., Genovesio, A., Gonzalo-Asensio, J. A., Puzo, G., Martin, C., Brosch, R., Stewart, G. R., Gicquel, B., and Neyrolles, O. (2010) High content phenotypic cell-based visual screen identifies Mycobacterium tuberculosis acyltrehalose-containing glycolipids involved in phagosome remodeling. PLoS Pathog. 6, e1001100
18. Gilmore, S. A., Schelle, M. W., Holsclaw, C. M., Leigh, C. D., Jain, M., Cox, J. S., Leary, J. A., and Bertozzi, C. R. (2012) Sulfolipid-1 biosynthesis restricts Mycobacterium tuberculosis growth in human macrophages. ACS Chem. Biol. 7, 863-870
19. Rousseau, C., Neyrolles, O., Bordat, Y., Giroux, S., Sirakova, T. D., Prevost, M.-C., Kolattukudy, P. E., Gicquel, B., and Jackson, M. (2003) Deficiency in mycolipenate- and mycosanoate-derived acyltrehaloses enhances early interactions of Mycobacterium tuberculosis with host cells. Cell Microbiol. 5, 405-415
20. Rousseau, C., Turner, O. C., Rush, E., Bordat, Y., Sirakova, T. D., Kolattukudy, P. E., Ritter, S., Orme, I. M., Gicquel, B., and Jackson, M. (2003) Sulfolipid deficiency does not affect the virulence of Mycobacterium tuberculosis H37Rv in mice and guinea pigs. Infect. Immun. 71, 4684-4690
21. Converse, S. E., Mougous, J. D., Leavell, M. D., Leary, J. A., Bertozzi, C. R., and Cox, J. S. (2003) MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence. Proc. Natl. Acad. Sci. U.S.A. 100, 6121-6126
22. Domenech, P., Reed, M. B., and Barry, C. E., 3rd (2005) Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance. Infect. Immun. 73, 3492-3501
23. Domenech, P., Reed, M. B., Dowd, C. S., Manca, C., Kaplan, G., and Barry, C. E., 3rd (2004) The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis. J. Biol. Chem. 279, 21257-21265
24. Lamichhane, G., Tyagi, S., and Bishai, W. R. (2005) Designer arrays for defined mutant analysis to detect genes essential for survival of Mycobacterium tuberculosis in mouse lungs. Infect. Immun. 73, 2533-2540
25. Lynett, J., and Stokes, R. W. (2007) Selection of transposon mutants of Mycobacterium tuberculosis with increased macrophage infectivity identifies fadD23 to be involved in sulfolipid production and association with macrophages. Microbiology 153, 3133-3140
26. Kumar, P., Schelle, M. W., Jain, M., Lin, F. L., Petzold, C. J., Leavell, M. D., Leary, J. A., Cox, J. S., and Bertozzi, C. R. (2007) PapA1 and PapA2 are acyltransferases essential for the biosynthesis of the Mycobacterium tuberculosis virulence factor sulfolipid-1. Proc. Natl. Acad. Sci. U.S.A. 104, 11221-11226
27. Chesne-Seck, M.-L., Barilone, N., Boudou, F., Gonzalo Asensio, J., Kolattukudy, P. E., Martín, C., Cole, S. T., Gicquel, B., Gopaul, D. N., and Jackson, M. (2008) A point mutation in the two-component regulator PhoP-PhoR accounts for the absence of polyketide-derived acyltrehaloses but not that of phthiocerol dimycocerosates in Mycobacterium tuberculosis H37Ra. J. Bacteriol. 190, 1329-1334
28. Passemar, C., Arbués, A., Malaga, W., Mercier, I., Moreau, F., Lepourry, L., Neyrolles, O., Guilhot, C., and Astarie-Dequeker, C. (2014) Multiple deletions in the polyketide synthase gene repertoire of Mycobacterium tuberculosis reveal functional overlap of cell envelope lipids in host-pathogen interactions. Cell Microbiol. 16, 195-213
29. Singh, A., Crossman, D. K., Mai, D., Guidry, L., Voskuil, M. I., Renfrow, M. B., and Steyn, A. J. (2009) Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathogens 5, e1000545
30. Lee, W., VanderVen, B. C., Fahey, R. J., and Russell, D. G. (2013) Intracellular Mycobacterium tuberculosis exploits host-derived fatty acids to limit metabolic stress. J. Biol. Chem. 288, 6788-6800
31. Dubey, V. S., Sirakova, T. D., and Kolattukudy, P. E. (2002) Disruption of msl3 abolishes the synthesis of mycolipanoic and mycolipenic acids required for polyacyltrehalose synthesis in Mycobacterium tuberculosis H37Rv and causes cell aggregation. Mol. Microbiol. 45, 1451-1459
32. Hatzios, S. K., Schelle, M. W., Holsclaw, C. M., Behrens, C. R., Botyanszki, Z., Lin, F. L., Carlson, B. L., Kumar, P., Leary, J. A., and Bertozzi, C. R. (2009) PapA3 is an acyltransferase required for polyacyltrehalose biosynthesis in Mycobacterium tuberculosis. J. Biol. Chem. 284, 12745-12751
33. Seeliger, J. C., Holsclaw, C. M., Schelle, M. W., Botyanszki, Z., Gilmore, S. A., Tully, S. E., Niederweis, M., Cravatt, B. F., Leary, J. A., and Bertozzi, C. R. (2012) Elucidation and chemical modulation of sulfolipid-1 biosynthesis in Mycobacterium tuberculosis. J. Biol. Chem. 287, 7990-8000
34. Jackson, M., Camacho, L. R., Gicquel, B., and Guilhot, C. (2001) in Mycobacterium Tuberculosis Protocols, Vol. 54 (Parish, T., and Stocker, N. G., eds) pp. 59-75, Humana Press, Totowa, NJ
35. Grzegorzewicz, A. E., Pham, H., Gundi, V. A. K. B., Scherman, M. S., North, E. J., Hess, T., Jones, V., Gruppo, V., Born, S. E. M., 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
36. Mederlé, I., Bourguin, I, Ensergueix, D., Badeli, E., Moniz-Peireira, J., Gicquel, B., and Winter, N. (2002) Plasmidic versus insertional cloning of heterologous genes in Mycobacterium bovis BCG: impact on in vivo antigen persistence and immune responses. Infect. Immun. 70, 303-314
37. Gonzalo Asensio, J., Mai a, C., Ferrer, N. L., Barilone, N., Laval, F., Soto, C. Y., Winter, N., Daffé, M., Gicquel, B., Martín, C., and Jackson, M. (2006) The virulence-associated two-component PhoP-PhoR system controls the biosynthesis of polyketide-derived lipids in Mycobacterium tuberculosis. J. Biol. Chem. 281, 1313-1316
38. Layre, E., Paepe, D. C., Larrouy-Maumus, G., Vaubourgeix, J., Mundayoor, S., Lindner, B., Puzo, G., and Gilleron, M. (2011) Deciphering sulfoglycolipids of Mycobacterium tuberculosis. J. Lipid Res. 52, 1098-1110
39. Alexeyev, M. F., and Winkler, H. H. (1999) Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pholac reporters. J. Mol. Biol. 285, 1503-1513
40. Stover, C. K., de la Cruz, V. F., Fuerst, T. R., Burlein, J. E., Benson, L. A., Bennett, L. T., Bansal, G. P., Young, J. F., Lee, M. H., and Hatfull, G. F. (1991) New use of BCG for recombinant vaccines. Nature 351, 456-460
41. Hsieh, J. M., Besserer, G. M., Madej, M. G., Bui, H. Q., Kwon, S., and Abramson, J. (2010) Bridging the gap: a GFP-based strategy for overexpression and purification of membrane proteins with intra and extracellular C-termini. Protein Sci. 19, 868-880
42. Berg, S., Starbuck, J., Torrelles, J. B., Vissa, V. D., Crick, D. C., Chatterjee, D., and Brennan, P. J. (2005) Roles of the conserved proline and glycosyltransferase motifs of EmbC in biosynthesis of lipoarabinomannan. J. Biol. Chem. 280, 5651-5663
43. 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
44. Guerin, M. E., Schaeffer, F., Chaffotte, A., G est, P., Giganti, D., Korduláková, J., van der Woerd, M., Jackson, M., and Alzari, P. M. (2009) Substrateinduced conformational changes in the essential peripheral membraneassociated mannosyltransferase PimA from mycobacteria: implications for catalysis. J. Biol. Chem. 284, 21613-21625
45. Trivedi, O. A., Arora, P., Sridharan, V., Tickoo, R., Mohanty, D., and Gokhale, R. S. (2004) Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 428, 441-445
46. Jain, M., and Cox, J. S. (2005) Interaction between polyketide synthase and transporter suggests coupled synthesis and export of virulence lipid in M. tuberculosis. PLoS Pathog. 1, e2
47. Belisle, J. T., Vissa, V. D., Sievert, T., Takayama, K., Brennan, P. J., and Besra, G. S. (1997) Role of the major antigen of Mycobacterium tuberculosis in the cell wall biogenesis. Science 276, 1420 -1422
48. Murakami, S. (2008) Multi drug efflux transporter, AcrB: the pumping mechanism. Curr. Opin. Struct. Biol. 18, 459-465
49. Zgurskaya, H. I., and Nikaido, H. (1999) Bypassing the periplasm: reconstitution of the AcrAB multi drug efflux pump of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 7190-7195
50. Camacho, L. R., Constant, P., Raynaud, C., Laneelle, M. A., Triccas, J. A., Gicquel, B., Daffe, M., and Guilhot, C. (2001) Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis: evidence that this lipid is involved in the cell wall permeability barrier. J. Biol. Chem. 276, 19845-19854
51. Sulzenbacher, G., Canaan, S., Bordat, Y., Neyrolles, O., Stadthagen, G., Roig-Zamboni, V., Rauzier, J., Maurin, D., Laval, F., Daffé, M., Cambillau, C., Gicquel, B., Bourne, Y., and Jackson, M. (2006) LppX is a lipoprotein required for the translocation of phthiocerol dimycocerosates to the surface of Mycobacterium tuberculosis. EMBO J. 25, 1436-1444
52. Sondén, B., Kocíncová, D., Deshayes, C., Euphrasie, D., Rhayat, L., Laval, F., Frehel, C., Daffé, M., Etienne, G., and Reyrat, J.-M. (2005) Gap, a mycobacterial specific integral membrane protein, is required for glycolipid transport to the cell surface. Mol. Microbiol. 58, 426-440
53. Deshayes, C., Bach, H., Euphrasie, D., Attarian, R., Coureuil, M., Sougakoff, W., Laval, F., Av-Gay, Y., Daffé, M., Etienne, G., and Reyrat, J. M. (2010) MmpS4 promotes glycopeptidolipids biosynthesis and export in Mycobacterium smegmatis. Mol. Microbiol. 78, 989-1003
54. Wells, R. M., Jones, C. M., Xi, Z., Speer, A., Danilchanka, O., Doornbos, K. S., Sun, P., Wu, F., Tian, C., and Niederweis, M. (2013) Discovery of a siderophore export system essential for virulence of Mycobacterium tuberculosis. PLoS Pathog. 9, e1003120
55. Rezwan, M., Lanéelle, M. A., Sander, P., and Daffé, M. (2007) Breaking down the wall: fractionation of mycobacteria. J. Microbiol. Methods 68, 32-39