Mycobacterium avium 104 deleted of the methyltransferase D gene by allelic replacement lacks serotype-specific glycopeptidolipids and shows attenuated virulence in mice

Molecular Microbiology

Volumn 56, Issue 5, 2005, Pages 1262-1273

  Krzywinska, Elzbieta ^a,c   Bhatnagar, Sanchita ^a   Sweet, Lindsay ^a   Chatterjee, Delphi ^b   Schorey, Jeffrey S ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

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

^c MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DI O METHYL RHAMNOSE; GLYCOLIPID; GLYCOPEPTIDOLIPID; METHYLTRANSFERASE; METHYLTRANSFERASE D; RANTES; RHAMNOSE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; BACTERIAL COUNT; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE DELETION; GENE SEQUENCE; IN VITRO STUDY; KNOCKOUT GENE; LIVER; LUNG; MACROPHAGE; MOUSE; MYCOBACTERIUM AVIUM; NONHUMAN; OPPORTUNISTIC INFECTION; PATHOGENESIS; PRIORITY JOURNAL; SEROTYPE; SYNTHESIS; UNITED STATES; WILD TYPE;

ANIMALS; ANTIGENS, BACTERIAL; CELLS, CULTURED; COLONY COUNT, MICROBIAL; DISEASE MODELS, ANIMAL; GENE DELETION; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; GLYCOLIPIDS; GLYCOPEPTIDES; LIVER; LUNG; MACROPHAGES; METHYLTRANSFERASES; MICE; MYCOBACTERIUM AVIUM COMPLEX; MYCOBACTERIUM AVIUM-INTRACELLULARE INFECTION; RANTES; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM; MYCOBACTERIUM AVIUM 104;

EID: 19944370501     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04608.x     Document Type: Article

References (42)

1. Abrams, E.J. (2000) Opportunistic infections and other clinical manifestations of HIV disease in children. Pediatr Clin North Am 47: 79-108.
2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
3. Appelberg, R., and Orme, I.M. (1993) Effector mechanisms involved in cytokine-mediated bacteriostasis of Mycobacterium avium infections in murine macrophages. Immunology 80: 352-359.
4. Appelberg, R., Sarmento, A., and Castro, A.G. (1995) Tumour necrosis factor-alpha (TNF-alpha) in the host resistance to mycobacteria of distinct virulence. Clin Exp Immunol 101: 308-313.
5. Ausbel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K.e. (1999) Current Protocols in Molecular Biology. New York, NY: John Wiley & Sons.
6. Balasubramanian, V., Pavelka, M.S.J., Bardarov, S.S., Martin, J., Weisbrod, T.R., McAdam, R.A., et al. (1996) Allelic exchange in Mycobacterium tuberculosis with long linear recombination substrates. J Bacteriol 178: 273-279.
7. Barrow, W.W., and Brennan, P.J. (1982) Solation in high frequency of rough variants of Mycobacterium intracellulare lacking C-mycoside glycopeptidolipid antigens. J Bacteriol 150: 381-384.
8. Barrow, W.W., Davis, T.L., Wright, E.L., Labrousse, V., Bachelet, M., and Rastogi, N. (1995) Immunomodulatory spectrum of lipids associated with Mycobacterium avium serovar 8. Infect Immun 63: 126-133.
9. Belisle, J.T., and Brennan, P.J. (1994) Molecular basis of colony morphology in Mycobacterium avium. Res Microbiol 145: 237-242.
10. Belisle, J.T., Pascopella, L., Inamine, J.M., Brennan, P.J., and Jacobs, W.R.J. (1991) Isolation and expression of a gene cluster responsible for biosynthesis of the glycopeptidolipid antigens of Mycobacterium avium. J Bacteriol 173: 6991-6997.
11. Belisle, J.T., Klaczkiewicz, K., Brennan, P.J., Jacobs, W.R., Jr, and Inamine, J.M. (1993a) Rough morphological variants of Mycobacterium avium. Characterization of genomic deletions resulting in the loss of glycopeptidolipid expression. J Biol Chem 268: 10517-10523.
12. Belisle, J.T., McNeil, M.R., Chatterjee, D., Inamine, J.M., and Brennan, P.J. (1993b) Expression of the core lipopeptide of the glycopeptidolipid surface antigens in rough mutants of Mycobacterium avium. J Biol Chem 268: 10510-10516.
13. Billman-Jacobe, H., McConville, M.J., Haites, R.E., Kovacevic, S., and Coppel, R.L. (1999) Identification of a peptide synthetase involved in the biosynthesis of glycopeptidolipids of Mycobacterium smegmatis. Mol Microbiol 33: 1244-1253.
14. Chatterjee, D., and Khoo, K.H. (2001) The surface glycopeptidolipids of mycobacteria: structures and biological properties. Cell Mol Life Sci 58: 2018-2042.
15. Eckstein, T.M., Silbaq, F.S., Chatterjee, D., Kelly, N.J., Brennan, P.J., and Belisle, J.T. (1998) Identification and recombinant expression of a Mycobacterium avium rhamnosyltransferase gene (rtfA) involved in glycopeptidolipid biosynthesis. J Bacteriol 180: 5567-5573.
16. Eckstein, T.M., Inamine, J.M., Lambert, M.L., and Belisle, J.T. (2000) A genetic mechanism for deletion of the ser2 gene cluster and formation of rough morphological variants of Mycobacterium avium. J Bacteriol 182: 6177-6182.
17. Ehlers, S., Benini, J., Kutsch, S., Endres, R., Rietschel, E.T., and Pfeffer, K. (1999) Fatal granuloma necrosis without exacerbated mycobacterial growth in tumor necrosis factor receptor p55 gene-deficient mice intravenously infected with Mycobacterium avium. Infect Immun 67: 3571-3579.
18. Etienne, G., Villeneuve, C., Billman-Jacobe, H., Astarie-Dequeker, C., Dupont, M.A., and Daffe, M. (2002) The impact of the absence of glycopeptidolipids on the ultrastructure, cell surface and cell wall properties, and phagocytosis of Mycobacterium smegmatis. Microbiology 148: 3089-3100.
19. Govoni, G., and Gros, P. (1998) Macrophage NRAMP1 and its role in resistance to microbial infections. Inflamm Res 47: 277-284.
20. Horsburgh, C.R., Jr. (1999) The pathophysiology of disseminated Mycobacterium avium complex disease in AIDS. J Infect Dis 179 (Suppl. 3): S461-S465.
21. Hunter, S.W., Fujiwara, T., and Brennan, P.J. (1982) Structure and antigenicity of the major specific glycolipid antigen of Mycobacterium leprae. J Biol Chem 257: 15072-15078.
22. Irani, V.R., Lee, S.H., Eckstein, T.M., Inamine, J.M., Belisle, J.T., and Maslow, J.N. (2004) Utilization of a ts-sacB selection system for the generation of a Mycobacterium avium serovar-8 specific glycopeptidolipid allelic exchange mutant. Ann Clin Microbiol Antimicrob 3: 18-22.
23. Jeevarajah, D., Patterson, J.H., Taig, E., Sargeant, T., McConville, M.J., and Billman-Jacobe, H. (2004) Methylation of GPLs in Mycobacterium smegmatis and Mycobacterium avium. J Bacteriol 186: 6792-6799.
24. Kaplan, J.E., Hanson, D., Dworkin, M.S., Frederick, T., Bertolli, J., Lindegren, M.L., et al. (2000) Epidemiology of human immunodeficiency virus-associated opportunistic infections in the United States in the era of highly active antiretroviral therapy. Clin Infect Dis 30 (Suppl. 1): S5-S14.
25. Khoo, K.H., Jarboe, E., Barker, A., Torrelles, J., Kuo, C.W., and Chatterjee, D. (1999) Altered expression profile of the surface glycopeptidolipids in drug-resistant clinical isolates of Mycobacterium avium complex. J Biol Chem 274: 9778-9785.
26. Krzywinska, E., and Schorey, J.S. (2003) Characterization of genetic differences between Mycobacterium avium subsp. avium strains of diverse virulence with a focus on the glycopeptidolipid biosynthesis cluster. Vet Microbiol 91: 249-264.
27. Luther, S.A., and Cyster, J.G. (2001) Chemokines as regulators of T cell differentiation. Nat Immunol 2: 102-107.
28. Maslow, J.N., Irani, V.R., Lee, S.H., Eckstein, T.M., Inamine, J.M., and Belisle, J.T. (2003) Biosynthetic specificity of the rhamnosyltransferase gene of Mycobacterium avium serovar 2 as determined by allelic exchange mutagenesis. Microbiology 149: 3193-3202.
29. Otero, J., Jacobs, W.R., Jr, and Glickman, M.S. (2003) Efficient allelic exchange and transposon mutagenesis in Mycobacterium avium by specialized transduction. Appl Environ Microbiol 69: 5039-5044.
30. Pedrosa, J., Florido, M., Kunze, Z.M., Castro, A.G., Portaels, F., McFadden, J., et al. (1994) Characterization of the virulence of Mycobacterium avium complex (MAC) isolates in mice. Clin Exp Immunol 98: 210-216.
31. Pelicic, V., Jackson, M., Reyrat, J.M., Jacobs, W.R., Jr, Gicquel, B., and Guilhot, C. (1997) Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 94: 10955-10960.
32. Race, E.M., Adelson-Mitty, J., Kriegel, G.R., Barlam, T.F., Reimann, K.A., Letvin, N.L., and Japour, A.J. (1998) Focal mycobacterial lymphadenitis following initiation of protease-inhibitor therapy in patients with advanced HIV-1 disease. Lancet 351: 252-255.
33. von Reyn, C.F., Maslow, J.N., Barber, T.W., Falkinham, J.O., III, and Arbeit, R.D. (1994) Persistent colonisation of potable water as a source of Mycobacterium avium infection in AIDS. Lancet 343: 1137-1141.
34. Roach, S.K., and Schorey, J.S. (2002) Differential regulation of the mitogen-activated protein kinases by pathogenic and nonpathogenic mycobacteria. Infect Immun 70: 3040-3052.
35. Rusin, P.A., Rose, J.B., Haas, C.N., and Gerba, C.P. (1997) Risk assessment of opportunistic bacterial pathogens in drinking water. Rev Environ Contam Toxicol 152: 57-83.
36. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Press.
37. Takayama, K., Garcia-Cardena, G., Sukhova, G.K., Comander, J., Gimbrone, M.A., Jr, and Libby, P. (2002) Prostaglandin E2 suppresses chemokine production in human macrophages through the EP4 receptor. J Biol Chem 277: 44147-44154.
38. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
39. Torrelles, J.B., Chatterjee, D., Lonca, J.G., Manterola, J.M., Ausina, V.R., and Brennan, P.J. (2000) Serovars of Mycobacterium avium complex isolated from AIDS and non-AIDS patients in Spain. J Appl Microbiol 88: 266-279.
40. Torrelles, J.B., Ellis, D., Osborne, T., Hoefer, A., Orme, I.M., Chatterjee, D., et al. (2002) Characterization of virulence, colony morphotype and the glycopeptidolipid of Mycobacterium avium strain 104. Tuberculosis 82: 293-300.
41. Yajko, D.M., Chin, D.P., Gonzalez, P.C., Nassos, P.S., Hopewell, P.C., Reingold, A.L., et al. (1995) Mycobacterium avium complex in water, food, and soil samples collected from the environment of HIV-infected individuals. J Acquir Immune Defic Syndr Hum Retrovirol 9: 176-182.
42. Yakrus, M.A., and Good, R.C. (1990) Geographic distribution, frequency, and specimen source of Mycobacterium avium complex serotypes isolated from patients with acquired immunodeficiency syndrome. J Clin Microbiol 28: 926-929.