Unexpected link between lipooligosaccharide biosynthesis and surface protein release in Mycobacterium marinum

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20417-20429

  Van Der Woude, Aniek D ^a,b   Sarkar, Debasmita ^c   Bhatt, Apoorva ^c   Sparrius, Marion ^a   Raadsen, Susanne A ^a   Boon, Louis ^d   Geurtsen, Jeroen ^a   Van Der Sar, Astrid M ^a   Luirink, Joen ^b   Houben, Edith N G ^a   Besra, Gurdyal S ^d   Bitter, Wilbert ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d BIOCEROS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ENVELOPES; CELL SURFACES; EXTRACELLULAR PROTEINS; FREE LIPIDS; GC-RICH SEQUENCES; GENE CLUSTERS; GLYCOLIPID COMPOSITION; INFECTION MODELS; LIPID ANALYSIS; LIPOOLIGOSACCHARIDES; MYCOBACTERIAL; MYCOBACTERIAL CELLS; MYCOLIC ACIDS; NOVEL COMPONENT; REGULATORY PROTEIN; SECRETION SYSTEMS; SURFACE PROTEINS; WILD-TYPE STRAIN; ZEBRAFISH EMBRYOS;

BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; GENES; PHYSIOLOGY;

PROTEINS;

BACTERIAL PROTEIN; GLYCOLIPID; LIPOOLIGOSACCHARIDE; LIPOOLIGOSACCHARIDE III; LIPOOLIGOSACCHARIDE IV; MEMBRANE PROTEIN; POLYMORPHIC GC RICH SEQUENCE PROTEIN; PROTEIN ESPE; PROTEIN WHIB4; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM EXAMINATION; CARBOHYDRATE SYNTHESIS; CELL SURFACE; CONTROLLED STUDY; EMBRYO; GENE CLUSTER; GENE FUNCTION; GENE INSERTION; GENETIC ASSOCIATION; LIPID ANALYSIS; LIPID COMPOSITION; LIPID STORAGE; MUTANT; MYCOBACTERIUM MARINUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; TRANSPOSON; WILD TYPE; ZEBRA FISH;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; DNA TRANSPOSABLE ELEMENTS; FISH DISEASES; LIPOPOLYSACCHARIDES; MUTATION; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS; MYCOBACTERIUM MARINUM; ZEBRAFISH;

DANIO RERIO; MYCOBACTERIUM MARINUM;

EID: 84862017657     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.336461     Document Type: Article

References (51)

1. World Health Organization (2011) 2011/2012 Tuberculosis Global Facts, WHO Press, Geneva, Switzerland
2. 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 (Pubitemid 351723507)
3. 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
4. Sani, M., Houben, E. N., Geurtsen, J., Pierson, J., de Punder, K., van Zon, M., Wever, B., Piersma, S. R., Jiménez, C. R., Daffé, M., Appelmelk, B. J., Bitter, W., van der Wel, N., and Peters, P. J. (2010) Direct visualization by cryo-EM of the mycobacterial capsular layer. A labile structure containing ESX-1-secreted proteins. PLoS Pathog. 6, e1000794
5. Brennan, P. J., and Nikaido, H. (1995) The envelope of mycobacteria. Annu. Rev. Biochem. 64, 29-63
6. Abdallah, A. M., Gey van Pittius, N. C., Champion, P. A., Cox, J., Luirink, J., Vandenbroucke-Grauls, C. M., Appelmelk, B. J., and Bitter, W. (2007) Type VII secretion. Mycobacteria show the way. Nat. Rev. Microbiol. 5, 883-891
7. Gey Van Pittius, N. C., Gamieldien, J., Hide, W., Brown, G. D., Siezen, R. J., and Beyers, A. D. (2001) The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol. 2, RESEARCH0044
8. Pallen, M. J. (2002) The ESAT-6/WXG100 superfamily and a new Gram-positive secretion system? Trends Microbiol. 10, 209-212
9. Abdallah, A. M., Verboom, T., Hannes, F., Safi, M., Strong, M., Eisenberg, D., Musters, R. J., Vandenbroucke-Grauls, C. M., Appelmelk, B. J., Luirink, J., and Bitter, W. (2006) A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol. Microbiol. 62, 667-679 (Pubitemid 44571593)
10. Abdallah, A. M., Verboom, T., Weerdenburg, E. M., Gey van Pittius, N. C., Mahasha, P. W., Jiménez, C., Parra, M., Cadieux, N., Brennan, M. J., Appelmelk, B. J., and Bitter, W. (2009) PPE and PE-PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol. Microbiol. 73, 329-340
11. Gey van Pittius, N. C., Sampson, S. L., Lee, H., Kim, Y., van Helden, P. D., and Warren, R. M. (2006) Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol. Biol. 6, 95
12. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., 3rd, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (Pubitemid 28319235)
13. Stinear, T. P., Seemann, T., Harrison, P. F., Jenkin, G. A., Davies, J. K., Johnson, P. D., Abdellah, Z., Arrowsmith, C., Chillingworth, T., Churcher, C., Clarke, K., Cronin, A., Davis, P., Goodhead, I., Holroyd, N., Jagels, K., Lord, A., Moule, S., Mungall, K., Norbertczak, H., Quail, M. A., Rabbinowitsch, E., Walker, D., White, B., Whitehead, S., Small, P. L., Brosch, R., Ramakrishnan, L., Fischbach, M. A., Parkhill, J., and Cole, S. T. (2008) Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res. 18, 729-741 (Pubitemid 351645063)
14. Poulet, S., and Cole, S. T. (1995) Characterization of the highly abundant polymorphic GC-rich-repetitive sequence (PGRS) present in Mycobacterium tuberculosis. Arch. Microbiol. 163, 87-95
15. Ren, H., Dover, L. G., Islam, S. T., Alexander, D. C., Chen, J. M., Besra, G. S., and Liu, J. (2007) Identification of the lipooligosaccharide biosynthetic gene cluster from Mycobacterium marinum. Mol. Microbiol. 63, 1345-1359
16. Burguière, A., Hitchen, P. G., Dover, L. G., Kremer, L., Ridell, M., Alexander, D. C., Liu, J., Morris, H. R., Minnikin, D. E., Dell, A., and Besra, G. S. (2005) LosA, a key glycosyltransferase involved in the biosynthesis of a novel family of glycosylated acyltrehalose lipooligosaccharides from Mycobacterium marinum. J. Biol. Chem. 280, 42124-42133 (Pubitemid 43023181)
17. Daffe, M., McNeil, M., and Brennan, P. J. (1991) Novel type-specific lipooligosaccharides from Mycobacterium tuberculosis. Biochemistry 30, 378-388
18. Rombouts, Y., Alibaud, L., Carrère-Kremer, S., Maes, E., Tokarski, C., Elass, E., Kremer, L., and Guérardel, Y. (2011) Fatty acyl chains of Mycobacterium marinum lipooligosaccharides. Structure, localization, and acylation by PapA4 (MMAR-2343) protein. J. Biol. Chem. 286, 33678-33688
19. Rombouts, Y., Burguière, A., Maes, E., Coddeville, B., Elass, E., Guérardel, Y., and Kremer, L. (2009) Mycobacterium marinum lipooligosaccharides are unique caryophyllose-containing cell wall glycolipids that inhibit tumor necrosis factor-α secretion in macrophages. J. Biol. Chem. 284, 20975-20988
20. Sarkar, D., Sidhu, M., Singh, A., Chen, J., Lammas, D. A., van der Sar, A. M., Besra, G. S., and Bhatt, A. (2011) Identification of a glycosyltransferase from Mycobacterium marinum involved in addition of a caryophyllose moiety in lipooligosaccharides. J. Bacteriol. 193, 2336-2340
21. Talaat, A. M., Reimschuessel, R., Wasserman, S. S., and Trucksis, M. (1998) Goldfish, Carassius auratus, a novel animal model for the study of Mycobacterium marinum pathogenesis. Infect. Immun. 66, 2938-2942 (Pubitemid 28261806)
22. Puttinaowarat, S., Thompson, K. D., and Adams, A. (2000) Mycobacteriosis. Detection and identification of aquatic Mycobacterium species. Fish Vet. J. 5, 6-21
23. van der Sar, A. M., Abdallah, A. M., Sparrius, M., Reinders, E., Vandenbroucke-Grauls, C. M., and Bitter, W. (2004) Mycobacterium marinum strains can be divided into two distinct types based on genetic diversity and virulence. Infect. Immun. 72, 6306-6312 (Pubitemid 39425409)
24. 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)
25. Carlsson, F., Joshi, S. A., Rangell, L., and Brown, E. J. (2009) Polar localization of virulence-related Esx-1 secretion in mycobacteria. PLoS Pathog. 5, e1000285
26. + T cells. J. Exp. Med. 191, 551-560
27. Harboe, M., Malin, A. S., Dockrell, H. S., Wiker, H. G., Ulvund, G., Holm, A., Jørgensen, M. C., and Andersen, P. (1998) B-cell epitopes and quantification of the ESAT-6 protein of Mycobacterium tuberculosis. Infect. Immun. 66, 717-723 (Pubitemid 28074218)
28. Hayward, C. M., O'Gaora, P., Young, D. B., Griffin, G. E., Thole, J., Hirst, T. R., Castello-Branco, L. R., and Lewis, D. J. (1999) Construction and murine immunogenicity of recombinant Bacille Calmette Guérin vaccines expressing the B subunit of Escherichia coli heat labile enterotoxin. Vaccine 17, 1272-1281 (Pubitemid 29132962)
29. Meijer, A. H., van der Sar, A. M., Cunha, C., Lamers, G. E., Laplante, M. A., Kikuta, H., Bitter, W., Becker, T. S., and Spaink, H. P. (2008) Identification and real time imaging of a myc-expressing neutrophil population involved in inflammation and mycobacterial granuloma formation in zebrafish. Dev. Comp. Immunol. 32, 36-49 (Pubitemid 350160914)
30. van der Sar, A. M., Musters, R. J., van Eeden, F. J., Appelmelk, B. J., Vandenbroucke-Grauls, C. M., and Bitter, W. (2003) Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell. Microbiol. 5, 601-611 (Pubitemid 37080671)
31. Stoop, E. J., Schipper, T., Huber, S. K., Nezhinsky, A. E., Verbeek, F. J., Gurcha, S. S., Besra, G. S., Vandenbroucke-Grauls, C. M., Bitter, W., and van der Sar, A. M. (2011) Zebrafish embryo screen for mycobacterial genes involved in the initiation of granuloma formation reveals a newly identified ESX-1 component. Dis. Model. Mech. 4, 526-536
32. Rombouts, Y., Elass, E., Biot, C., Maes, E., Coddeville, B., Burguière, A., Tokarski, C., Buisine, E., Trivelli, X., Kremer, L., and Guérardel, Y. (2010) Structural analysis of an unusual bioactive N-acylated lipo-oligosaccharide LOS-IV in Mycobacterium marinum. J. Am. Chem. Soc. 132, 16073-16084
33. Hwang, B. Y., Lee, H. J., Yang, Y. H., Joo, H. S., and Kim, B. G. (2004) Characterization and investigation of substrate specificity of the sugar aminotransferase WecE from E. coli K12. Chem. Biol. 11, 915-925
34. Etienne, G., Malaga, W., Laval, F., Lemassu, A., Guilhot, C., and Daffé, M. (2009) Identification of the polyketide synthase involved in the biosynthesis of the surface-exposed lipooligosaccharides in mycobacteria. J. Bacteriol. 191, 2613-2621
35. Belisle, J. T., and Brennan, P. J. (1989) Chemical basis of rough and smooth variation in mycobacteria. J. Bacteriol. 171, 3465-3470 (Pubitemid 19145703)
36. Allen, M. M. (1984) Cyanobacterial cell inclusions. Annu. Rev. Microbiol. 38, 1-25
37. Füser, G., and Steinbüchel, A. (2007) Analysis of genome sequences for genes of cyanophycin metabolism: identifying putative cyanophycin metabolizing prokaryotes. Macromol. Biosci. 7, 278-296
38. 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 Pathog. 5, e1000545
39. Matsunaga, I., Bhatt, A., Young, D. C., Cheng, T. Y., Eyles, S. J., Besra, G. S., Briken, V., Porcelli, S. A., Costello, C. E., Jacobs, W. R., Jr., and Moody, D. B. (2004) Mycobacterium tuberculosis pks12 produces a novel polyketide presented by CD1c to T cells. J. Exp. Med. 200, 1559-1569 (Pubitemid 40094180)
40. Parish, T., and Stoker, N. G. (1998) Mycobacteria. Bugs and bugbears. Methods Mol. Biol. 101, 1-13
41. Hunter, S. W., Murphy, R. C., Clay, K., Goren, M. B., and Brennan, P. J. (1983) Trehalose-containing lipooligosaccharides. A new class of species-specific antigens from Mycobacterium. J. Biol. Chem. 258, 10481-10487 (Pubitemid 14242834)
42. Davis, J. M., Clay, H., Lewis, J. L., Ghori, N., Herbomel, P., and Ramakrishnan, L. (2002) Real time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17, 693-702 (Pubitemid 35477789)
43. Lesley, R., and Ramakrishnan, L. (2008) Insights into early mycobacterial pathogenesis from the zebrafish. Curr. Opin. Microbiol. 11, 277-283
44. Gilleron, M., Vercauteren, J., and Puzo, G. (1993) Lipooligosaccharidic antigen containing a novel C4-branched 3,6-dideoxy-α-hexopyranose typifies Mycobacterium gastri. J. Biol. Chem. 268, 3168-3179 (Pubitemid 23070941)
45. Lemassu, A., Lévy-Frébault, V. V., Lanéelle, M. A., and Daffé, M. (1992) Lack of correlation between colony morphology and lipooligosaccharide content in the Mycobacterium tuberculosis complex. J. Gen. Microbiol. 138, 1535-1541
46. Rachman, H., Strong, M., Schaible, U., Schuchhardt, J., Hagens, K., Mollenkopf, H., Eisenberg, D., and Kaufmann, S. H. (2006) Mycobacterium tuberculosis gene expression profiling within the context of protein networks. Microbes Infect. 8, 747-757
47. Geiman, D. E., Raghunand, T. R., Agarwal, N., and Bishai, W. R. (2006) Differential gene expression in response to exposure to antimycobacterial agents and other stress conditions among seven Mycobacterium tuberculosis whiB-like genes. Antimicrob. Agents Chemother. 50, 2836-2841 (Pubitemid 44198709)
48. Betts, J. C., Lukey, P. T., Robb, L. C., McAdam, R. A., and Duncan, K. (2002) Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43, 717-731 (Pubitemid 34597265)
49. Alam, M. S., Garg, S. K., and Agrawal, P. (2007) Molecular function of WhiB4/Rv3681c of Mycobacterium tuberculosis H37Rv. A [4Fe-4S] cluster co-ordinating protein disulphide reductase. Mol. Microbiol. 63, 1414-1431
50. Collins, F. M., and Cunningham, D. S. (1981) Systemic Mycobacterium kansasii infection and regulation of the alloantigenic response. Infect. Immun. 32, 614-624 (Pubitemid 11101692)
51. 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