The mycobacterial acyltransferase PapA5 is required for biosynthesis of cell wall-associated phenolic glycolipids

Microbiology

Volumn 158, Issue 5, 2012, Pages 1379-1387

  Chavadi, Sivagami Sundaram ^a   Onwueme, Kenolisa C ^b,e   Edupuganti, Uthamaphani R ^a   Jerome, Jeff ^a   Chatterjee, Delphi ^c   Soll, Clifford E ^d   Quadri, Luis E N ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Veterinary Dentistry and Oral Surgery   (United States)

^d CITY UNIVERSITY OF NEW YORK   (United States)

^e North West Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; PHENOLIC GLYCOLIPID; POLYKETIDE;

ACYLATION; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BIOSYNTHESIS; CATALYSIS; DELETION MUTANT; ENZYME ACTIVITY; MUTATIONAL ANALYSIS; MYCOBACTERIUM MARINUM; NONHUMAN; PAPA5 BACTERIAL GENE; PRIORITY JOURNAL;

ACYLTRANSFERASES; BACTERIAL PROTEINS; CELL WALL; DNA MUTATIONAL ANALYSIS; DNA, BACTERIAL; GLYCOLIPIDS; LIPOYLATION; MUTATION; MYCOBACTERIUM MARINUM; SEQUENCE DELETION;

EID: 84860528767     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.057869-0     Document Type: Article

References (36)

1. Alibaud, L., Rombouts, Y., Trivelli, X., Burguière, A., Cirillo, S. L., Cirillo, J. D., Dubremetz, J. F., Guérardel, Y., Lutfalla, G. & Kremer, L. (2011). A Mycobacterium marinum TesA mutant defective for major cell wall-associated lipids is highly attenuated in Dictyostelium discoideum and zebrafish embryos. Mol Microbiol 80, 919-934.
2. Astarie-Dequeker, C., Le Guyader, L., Malaga, W., Seaphanh, F. K., Chalut, C., Lopez, A. & Guilhot, C. (2009). Phthiocerol dimycocerosates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog 5, e1000289.
3. Brennan, P. J. & Nikaido, H. (1995). The envelope of mycobacteria. Annu Rev Biochem 64, 29-63.
4. Brennan, P. J., Chatterjee, D., Fujiwara, T. & Cho, S. N. (1994). Leprosy-specific neoglycoconjugates: synthesis and application to serodiagnosis of leprosy. Methods Enzymol 242, 27-37.
5. Brodin, P., Poquet, Y., Levillain, F., Peguillet, I., Larrouy-Maumus, G., Gilleron, M., Ewann, F., Christophe, T., Fenistein, D. & other authors (2010). High content phenotypic cell-based visual screen identifies Mycobacterium tuberculosis acyltrehalose-containing glycolipids involved in phagosome remodeling. PLoS Pathog 6, e1001100.
6. Buglino, J., Onwueme, K. C., Ferreras, J. A., Quadri, L. E. & Lima, C. D. (2004). Crystal structure of PapA5, a phthiocerol dimycocerosyl transferase from Mycobacterium tuberculosis. J Biol Chem 279, 30634-30642.
7. Camacho, L. R., Ensergueix, D., Perez, E., Gicquel, B. & Guilhot, C. (1999). Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34, 257-267.
8. Chavadi, S. S., Stirrett, K. L., Edupuganti, U. R., Vergnolle, O., Sadhanandan, G., Marchiano, E., Martin, C., Qiu, W. G., Soll, C. E. & Quadri, L. E. (2011a). Mutational and phylogenetic analyses of the mycobacterial mbt gene cluster. J Bacteriol 193, 5905-5913.
9. Chavadi, S. S., Edupuganti, U. R., Vergnolle, O., Fatima, I., Singh, S. M., Soll, C. E. & Quadri, L. E. (2011b). Inactivation of tesA reduces cell wall lipid production and increases drug susceptibility in mycobacteria. J Biol Chem 286, 24616-24625.
10. Collins, D. M., Skou, B., White, S., Bassett, S., Collins, L., For, R., Hurr, K., Hotter, G. & de Lisle, G. W. (2005). Generation of attenuated Mycobacterium bovis strains by signature-tagged mutagenesis for discovery of novel vaccine candidates. Infect Immun 73, 2379-2386.
11. Constant, P., Perez, E., Malaga, W., Lanéelle, M. A., Saurel, O., Daffé, M. & Guilhot, C. (2002). Role of the pks15/1 gene in the biosynthesis of phenolglycolipids in the Mycobacterium tuberculosis complex. Evidence that all strains synthesize glycosylated p-hydroxybenzoic methyl esters and that strains devoid of phenolglycolipids harbor a frameshift mutation in the pks15/1 gene. J Biol Chem 277, 38148-38158.
12. Cox, J. S., Chen, B., McNeil, M. & Jacobs, W. R., Jr (1999). Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402, 79-83.
13. Crick, D. C., Quadri, L. E. & Brennan, P. J. (2008). Biochemistry of the cell envelope of Mycobacterium tuberculosis. In Handbook of Tuberculosis: Molecular Biology and Biochemistry, pp. 1-19. Edited by S. H. E. Kaufmann & R. Rubin. Weinheim: Wiley-VCH.
14. Dhungel, S., Ranjit, C., Sapkota, B. R. & Macdonald, M. (2008). Role of PGL-I of M. leprae in TNF-alpha production by in vitro whole blood assay. Nepal Med Coll J 10, 1-3.
15. Ferreras, J. A., Ryu, J. S., Di Lello, F., Tan, D. S. & Quadri, L. E. (2005). Small-molecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis. Nat Chem Biol 1, 29-32.
16. Ferreras, J. A., Stirrett, K. L., Lu, X., Ryu, J. S., Soll, C. E., Tan, D. S. & Quadri, L. E. (2008). Mycobacterial phenolic glycolipid virulence factor biosynthesis: mechanism and small-molecule inhibition of polyketide chain initiation. Chem Biol 15, 51-61.
17. He, W., Soll, C. E., Chavadi, S. S., Zhang, G., Warren, J. D. & Quadri, L. E. (2009). Cooperation between a coenzyme A-independent stand-alone initiation module and an iterative type I polyketide synthase during synthesis of mycobacterial phenolic glycolipids. J Am Chem Soc 131, 16744-16750.
18. Horton, R. M., Hunt, H. D., Ho, S. N., Pullen, J. K. & Pease, L. R. (1989). Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77, 61-68.
19. Hunter, S. W. & Brennan, P. J. (1981). A novel phenolic glycolipid from Mycobacterium leprae possibly involved in immunogenicity and pathogenicity. J Bacteriol 147, 728-735.
20. Murry, J. P., Pandey, A. K., Sassetti, C. M. & Rubin, E. J. (2009). Phthiocerol dimycocerosate transport is required for resisting interferon-c-independent immunity. J Infect Dis 200, 774-782.
21. Ng, V., Zanazzi, G., Timpl, R., Talts, J. F., Salzer, J. L., Brennan, P. J. & Rambukkana, A. (2000). Role of the cell wall phenolic glycolipid-1 in the peripheral nerve predilection of Mycobacterium leprae. Cell 103, 511-524.
22. Onwueme, K. C., Ferreras, J. A., Buglino, J., Lima, C. D. & Quadri, L. E. (2004). Mycobacterial polyketide-associated proteins are acyltransferases: proof of principle with Mycobacterium tuberculosis PapA5. Proc Natl Acad Sci U S A 101, 4608-4613.
23. Onwueme, K. C., Vos, C. J., Zurita, J., Ferreras, J. A. & Quadri, L. E. (2005a). The dimycocerosate ester polyketide virulence factors of mycobacteria. Prog Lipid Res 44, 259-302.
24. Onwueme, K. C., Vos, C. J., Zurita, J., Soll, C. E. & Quadri, L. E. (2005b). Identification of phthiodiolone ketoreductase, an enzyme required for production of mycobacterial diacyl phthiocerol virulence factors. J Bacteriol 187, 4760-4766.
25. Parish, T. & Stoker, N. G. (1998). Mycobacteria Protocols. Totowa, NJ: Humana Press.
26. Parish, T. & Stoker, N. G. (2000). Use of a flexible cassette method to generate a double unmarked Mycobacterium tuberculosis tlyA plcABC mutant by gene replacement. Microbiology 146, 1969-1975.
27. Quadri, L. E. N. (2007). Strategic paradigm shifts in the antimicrobial drug discovery process of the 21st century. Infect Disord Drug Targets 7, 230-237.
28. Rambukkana, A., Zanazzi, G., Tapinos, N. & Salzer, J. L. (2002). Contact-dependent demyelination by Mycobacterium leprae in the absence of immune cells. Science 296, 927-931.
29. Reed, M. B., Domenech, P., Manca, C., Su, H., Barczak, A. K., Kreiswirth, B. N., Kaplan, G. & Barry, C. E., III (2004). A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431, 84-87.
30. Reed, M. B., Gagneux, S., Deriemer, K., Small, P. M. & Barry, C. E., III (2007). The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol 189, 2583-2589.
31. Robinson, N., Kolter, T., Wolke, M., Rybniker, J., Hartmann, P. & Plum, G. (2008). Mycobacterial phenolic glycolipid inhibits phagosome maturation and subverts the pro-inflammatory cytokine response. Traffic 9, 1936-1947.
32. Ruley, K. M., Ansede, J. H., Pritchett, C. L., Talaat, A. M., Reimschuessel, R. & Trucksis, M. (2004). Identification of Mycobacterium marinum virulence genes using signature-tagged mutagenesis and the goldfish model of mycobacterial pathogenesis. FEMS Microbiol Lett 232, 75-81.
33. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
34. Sinsimer, D., Huet, G., Manca, C., Tsenova, L., Koo, M. S., Kurepina, N., Kana, B., Mathema, B., Marras, S. A. & other authors (2008). The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 76, 3027-3036.
35. Stinear, T. P., Seemann, T., Harrison, P. F., Jenkin, G. A., Davies, J. K., Johnson, P. D., Abdellah, Z., Arrowsmith, C., Chillingworth, T. & other authors (2008). Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 18, 729-741.
36. Tsenova, L., Ellison, E., Harbacheuski, R., Moreira, A. L., Kurepina, N., Reed, M. B., Mathema, B., Barry, C. E., III & Kaplan, G. (2005). Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis 192, 98-106.