The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence

Infection and Immunity

Volumn 76, Issue 7, 2008, Pages 3027-3036

  Sinsimer, Daniel ^a,b   Huet, Gaelle ^c   Manca, Claudia ^a   Tsenova, Liana ^a   Koo, Mi Sun ^a   Kurepina, Natalia ^a   Kana, Bavesh ^d   Mathema, Barun ^a   Marras, Salvatore A E ^a   Kreiswirth, Barry N ^a   Guilhot, Christophe ^c   Kaplan, Gilla ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^b The State University of New Jersey   (United States)

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

^d UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; GLYCOLIPID; PHENOL; PHENOLGLYCOLIPID ANTIGEN; CYTOKINE; PHENOLIC GLYCOLIPID I, MYCOBACTERIUM LEPRAE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LIPOGENESIS; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RABBIT; TH1 CELL; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CLASSIFICATION; GENETICS; IMMUNOLOGY; LUNG TUBERCULOSIS; MICROBIOLOGY; MONOCYTE; MONONUCLEAR CELL; PATHOGENICITY; PATHOPHYSIOLOGY; SPECIES DIFFERENCE; VIRULENCE;

ANIMALS; ANTIGENS, BACTERIAL; CELLS, CULTURED; CYTOKINES; GLYCOLIPIDS; HUMANS; LEUKOCYTES, MONONUCLEAR; MICE; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; RABBITS; SPECIES SPECIFICITY; TUBERCULOSIS, PULMONARY; VIRULENCE;

EID: 46449110348     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01663-07     Document Type: Article

References (37)

1. Akahoshi, M., H. Nakashima, K. Miyake, Y. Inoue, S. Shimizu, Y. Tanaka, K. Okada, T. Otsuka, and M. Harada. 2003. Influence of interleukin-12 receptor B1 polymorphisms on tuberculosis. Hum. Genet. 112:237-243.
2. Bifani, P. J., B. Mathema, Z. Liu, S. L. Moghazeh, B. Shopsin, B. Tempalski, J. Driscol, R. Frothingham, J. M. Musser, P. Alcabes, and B. N. Kreiswirth. 1999. Identification of a W variant outbreak of Mycobacterium tuberculosis via population-based molecular epidemiology. JAMA 282:2321-2327.
3. Bloom, B. R., and C. J. L. Murray. 1992. Tuberculosis: commentary on a reemergent killer. Science 257:1055-1064.
4. Cho, S., J. Shin, M. Daffe, Y. Chong, S. Kim, and J. Kim. 1992. Production of monoclonal antibody to a phenolic glycolipid of Mycobacterium tuberculosis and its use in detection of the antigen in clinical isolates. J. Clin. Microbiol. 30:3065-3069.
5. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McLean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M. A. Quail, M.-A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J. E. Sulston, K. Taylor, S. Whitehead, and B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544. (Erratum, 396:190.)
6. Constant, P., E. Perez, W. Malaga, M. A. Laneelle, O. Saurel, M. Daffe, and C. Guilhot. 2002. Role of the pks15/1 gene in the biosynthesis of phenol-glycolipids in the Mycobacterium tuberculosis complex. Evidence that all strains synthesize glycosylated p-hydroxybenzoic methly esters and that strains devoid of phenolglycolipids harbor a frameshift mutation in the pks15/1 gene. J. Biol. Chem. 277:38148-38158.
7. Cooper, A. M., A. D. Roberts, E. R. Rhoades, J. E. Callahan, D. M. Getzy, and I. M. Orme. 1995. The role of interleukin 12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology 84:423-432.
8. Cox, J. S., B. Chen, M. McNeil, and W. R. Jacobs, Jr. 1999. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402:79-83.
9. Daffe, M., C. Lacave, M. Laneelle, and G. Laneelle. 1987. Structure of the major triglycosyl phenol-phthiocerol of Mycobacterium tuberculosis (strain Canetti). Eur. J. Biochem. 167:155-160.
10. Dawes, S. S., D. F. Warner, L. Tsenova, J. Timm, J. D. McKinney, G. Kaplan, H. Rubin, and V. Mizrahi. 2003. Ribonucleotide reduction in Mycobacterium tuberculosis: function and expression of genes encoding class Ib and class II ribonucleotide reductases. Infect. Immun. 71:6124-6131.
11. Dye, C., S. Scheele, P. Dolin, V. Pathania, and M. C. Raviglione. 1999. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 282:677-686.
12. Flynn, J., M. Goldstein, K. Triebold, J. Sypek, S. Wolf, and B. Bloom. 1995. IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis infection. J. Immunol. 155:2515-2524.
13. Freeman, R., M. Kato-Maeda, K. A. Hauge, K. L. Horan, E. Oren, M. Narita, C. K. Wallis, D. Cave, C. M. Nolan, P. M. Small, and G. A. Cangelosi. 2005. Use of rapid genomic deletion typing to monitor a tuberculosis outbreak within an urban homeless population. J. Clin. Microbiol. 43:5550-5554.
14. Gutacker, M. M., B. Mathema, H. Soini, E. Shashkina, B. N. Kreiswirth, E. A. Graviss, and J. M. Musser. 2006. Single-nucleotide polymorphism-based population genetic analysis of Mycobacterium tuberculosis strains from 4 geographic sites. J. Infect. Dis. 193:121-128.
15. Gutacker, M. M., J. C. Smoot, C. A. Migliaccio, S. M. Ricklefs, S. Hua, D. V. Cousins, E. A. Graviss, E. Shashkina, B. N. Kreiswirth, and J. M. Musser. 2002. Genome-wide analysis of synonymous single nucleotide polymorphisms in Mycobacterium tuberculosis complex organisms: resolution of genetic relationships among closely related microbial strains. Genetics 162:1533-1543.
16. Kurepina, N., E. Likhoshvay, E. Shashkina, B. Mathema, K. Kremer, D. van Soolingen, P. Bifani, and B. N. Kreiswirth. 2005. Targeted hybridization of IS6110 fingerprints identifies the W-Beijing Mycobacterium tuberculosis strains among clinical isolates. J. Clin. Microbiol. 43:2148-2154.
17. Lee, T., S. Cho, K. Yoon, J. Shin, and J. Kim. 1991. Comparison of DNA fragment patterns between the phenolic glycolipid-tb producers and non-producers of Mycobacterium tuberculosis. Yonsei Med. J. 32:243-249.
18. Manca, C., M. B. Reed, S. Freeman, B. Mathema, B. Kreiswirth, C. E. Barry III, and G. Kaplan. 2004. Differential monocyte activation underlies strain-specific Mycobacterium tuberculosis pathogenesis. Infect. Immun. 72:5511-5514.
19. Manca, C., L. Tsenova, C. E. Barry III, A. Bergtold, S. Freeman, P. A. J. Haslett, J. M. Musser, V. H. Freedman, and G. Kaplan. 1999. Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. J. Immunol. 162:6740-6746.
20. Manca, C., L. Tsenova, A. Bergtold, S. Freeman, M. Tovey, J. M. Musser, C. E. Barry III, V. H. Freedman, and G. Kaplan. 2001. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha/beta. Proc. Natl. Acad. Sci. USA 98:5752-5757.
21. Manca, C., L. Tsenova, S. Freeman, A. K. Barczak, M. Tovey, P. J. Murray, C. Barry, and G. Kaplan. 2005. Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J. Interferon Cytokine Res. 25:694-701.
22. Marmiesse, M., P. Brodin, C. Buchrieser, C. Gutierrez, N. Simoes, V. Vincent, P. Glaser, S. T. Cole, and R. Brosch. 2004. Macro-array and bioinformatic analyses reveal mycobacterial 'core' genes, variation in the ESAT-6 gene family and new phylogenetic markers for the Mycobacterium tuberculosis complex. Microbiology 150(Pt. 2):483-496.
23. Mendez-Samperio, P., H. E. Ayala-Verdin, and A. Trejo-Echeverria. 1999. Interleukin-12 regulates the production of bacille Calmette-Guerin-induced interferon-gamma from human cells in a CD40-dependent manner. Scand. J. Immunol. 50:61-67.
24. Molloy, A., P. Meyn, K. Smith, and G. Kaplan. 1993. Recognition and destruction of bacillus Calmette-Guerin-infected human monocytes. J. Exp. Med. 177:1691-1698.
25. Ordway, D., M. Henao-Tamayo, M. Harton, G. Palanisamy, J. Troudt, C. Shanley, R. J. Basaraba, and I. M. Orme. 2007. The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J. Immunol. 179:522-531.
26. Perez, E., P. Constant, F. Laval, A. Lemassu, M. A. Laneelle, M. Daffe, and C. Guilhot. 2004. Molecular dissection of the role of two methyltransferases in the biosynthesis of phenolglycolipids and phthiocerol dimycoserosate in the Mycobacterium tuberculosis complex. J. Biol. Chem. 279:42584-42592.
27. Perez, E., P. Constant, A. Lemassu, F. Laval, M. Daffe, and C. Guilhot. 2004. Characterization of three glycosyltransferases involved in the biosynthesis of the phenolic glycolipid antigens from the Mycobacterium tuberculosis complex. J. Biol. Chem. 279:42574-42583.
28. Raviglione, M. C., D. E. J. Snider, and A. Kochi. 1995. Global epidemiology of tuberculosis. Morbidity and mortality of a worldwide epidemic. JAMA 273:220-226.
29. Reed, M. B., P. Domenech, C. Manca, H. Su, A. K. Barczak, B. N. Kreiswirth, G. Kaplan, and C. E. Barry III. 2004. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431:84-87.
30. Reed, M. B., S. Gagneux, K. DeRiemer, P. M. Small, and C. E. Barry 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. Sreevatsan, S., X. Pan, K. E. Stockbauer, N. D. Connell, B. N. Kreiswirth, T. S. Whittam, and J. M. Musser. 1997. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc. Natl. Acad. Sci. 94:9869-9874.
32. Tsenova, L., E. Ellison, R. Harbacheuski, A. L. Moreira, N. Kurepina, M. B. Reed, B. Mathema, C. E. Barry III, and G. Kaplan. 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.
33. Tsenova, L., R. Harbacheuski, E. Ellison, C. Manca, and G. Kaplan. 2006. Aerosol exposure system for rabbits: application to M. tuberculosis infection. J. Am. Biol. Safety Assoc. 11:7-14.
34. Tsenova, L., A. Moreira, E. Party, V. H. Freedman, and G. Kaplan. 1997. Aerosol infection of mice with mycobacteria using a nose-only exposure device. J. Am. Biol. Safety Assoc. 2:20-31.
35. Tyagi, S., and F. R. Kramer. 1996. Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol. 14:303-308.
36. van Embden, J. D., M. D. Cave, J. T. Crawford, J. W. Dale, K. D. Eisenach, B. Gicquel, P. W. Hermans, C. Martin, R. McAdam, T. M. Shinnick, and P. M. Small. 1993. Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J. Clin. Microbiol. 31:406-409.
37. van Soolingen, D., T. Hoogenboezem, P. E. de Haas, P. W. Hermans, M. A. Koedam, K. S. Teppema, P. J. Brennan, G. S. Besra, F. Portaels, J. Top, L. M. Schouls, and J. D. van Embden. 1997. A novel pathogenic taxon of the Mycobacterium tuberculosis complex, Canetti: characterization of an exceptional isolate from Africa. Int. J. Syst. Bacteriol. 47:1236-1245.