Buruli ulcer: Reductive evolution enhances pathogenicity of Mycobacterium ulcerans

Nature Reviews Microbiology

Volumn 7, Issue 1, 2009, Pages 50-60

  Demangel, Caroline ^a   Stinear, Timothy P ^b   Cole, Stewart T ^c  

^a INSTITUT PASTEUR   (France)

^b MONASH UNIVERSITY   (Australia)

^c EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BCG VACCINE; CYCLOSPORIN A; DNA VACCINE; MYCOLACTONE; NATURAL PRODUCT; RAPAMYCIN; RIFAMPICIN; STREPTOMYCIN; TACROLIMUS; UNCLASSIFIED DRUG;

APOPTOSIS; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BURULI ULCER; CELL CYCLE ARREST; CYTOKINE PRODUCTION; CYTOTOXICITY; DISEASE CARRIER; DRUG STRUCTURE; EVOLUTIONARY ADAPTATION; GENOMICS; HORIZONTAL GENE TRANSFER; HUMAN; IMMUNOGENICITY; IMMUNOPATHOLOGY; INFECTION CONTROL; INFECTION RATE; INFECTION RISK; INSECT BITE; MOLECULAR PHYLOGENY; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM ULCERANS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SKIN TRANSPLANTATION;

BURULI ULCER; EVOLUTION, MOLECULAR; HUMANS; MYCOBACTERIUM ULCERANS;

HEXAPODA; MYCOBACTERIUM MARINUM; MYCOBACTERIUM ULCERANS;

EID: 57649174709     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2077     Document Type: Review

References (104)

1. Alsop, D. The Bairnsdale ulcer. Aust. NZ J. Surg. 41, 317-319 (1972).
2. MacCallum, P., Tolhurst, J., Buckle, G. & Sissons, H. A new mycobacterial infection in man. J. Pathol. Bacteriol. 60, 93-122 (1948).
3. Johnson, P. D. et al. Buruli ulcer (M. ulcerans infection): new insights, new hope for disease control. PLoS Med. 2, e108 (2005).
4. Marsollier, L. et al. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLoS Pathog. 3, e62 (2007).
5. Guarner, J. et al. Histopathologic features of Mycobacterium ulcerans infection. Emerg. Infect. Dis. 9, 651-656 (2003).
6. Hayman, J. & McQueen, A. The pathology of Mycobacterium ulcerans infection. Pathology 17, 594-600 (1985).
7. Peduzzi, E. et al. Local activation of the innate immune system in Buruli ulcer lesions. J. Invest. Dermatol. 127, 638-645 (2007).
8. Hayman, J. Clinical features of Mycobacterium ulcerans infection. Australas. J. Dermatol. 26, 67-73 (1985).
9. Coutanceau, E. et al. Modulation of the host immune response by a transient intracellular stage of Mycobacterium ulcerans: The contribution of endogenous mycolactone toxin. Cell. Microbiol. 7, 1187-1196 (2005).
10. Torrado, E. et al. Evidence for an intramacrophage growth phase of Mycobacterium ulcerans. Infect. Immun. 75, 977-987 (2007).
11. Adusumilli, S. et al. Mycobacterium ulcerans toxic macrolide, mycolactone modulates the host immune response and cellular location of M. ulcerans in vitro and in vivo. Cell. Microbiol. 7, 1295-1304 (2005).
12. Connor, D. H. & Lunn, H. F. Mycobacterium ulcerans infection (with comments on pathogenesis). Int. J. Lepr. 33 (Suppl.), 698-709 (1965).
13. George, K. M. et al. Mycolactone: A polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283 854-857 (1999).
14. George, K. M., Pascopella, L., Welty, D. M. & Small, P. L. A Mycobacterium ulcerans toxin, mycolactone, causes apoptosis in guinea pig ulcers and tissue culture cells. Infect. Immun. 68, 877-883 (2000).
15. Hong, H., Demangel, C., Pidot, S. J., Leadlay, P. F. & Stinear, T. Mycolactones: Immunosuppressive and cytotoxic polyketides produced by aquatic mycobacteria. Nature Prod. Rep. 25, 447-454 (2008).
16. Goto, M. et al. Nerve damage in Mycobacterium ulcerans infected mice: Probable cause of painlessness in Buruli ulcer. Am. J. Pathol. 168, 805-811 (2006).
17. En, J. et al. Mycolactone is responsible for the painlessness of Mycobacterium ulcerans infection (Buruli ulcer) in a murine study. Infect. Immun. 76, 2002-2007 (2008).
18. Diaz, D. et al. Use of the immunodominant 18-kiloDalton small heat shock protein as a serological marker for exposure to Mycobacterium ulcerans. Clin. Vaccine Immunol. 13, 1314-1321 (2006).
19. Etuaful, S. et al. Efficacy of the combination rifampin- streptomycin in preventing growth of Mycobacterium ulcerans in early lesions of Buruli ulcer in humans. Antimicrob. Agents Chemother. 49, 3182-3186 (2005).
20. Smith, P. G., Revill, W. D., Lukwago, E. & Rykushin, Y. P. The protective effect of BCG against Mycobacterium ulcerans disease: A controlled trial in an endemic area of Uganda. Trans. R. Soc. Trop. Med. Hyg. 70, 449-457 (1977).
21. Huygen, K. Prospects for vaccine development against Buruli disease. Expert Rev. Vaccines 2, 561-569 (2003).
22. Coutanceau, E. et al. Immunogenicity of Mycobacterium ulcerans Hsp65 and protective efficacy of a Mycobacterium leprae Hsp65-based DNA vaccine against Buruli ulcer. Microbes Infect. 8, 2075-2081 (2006).
23. Tanghe, A., Content, J., Van Vooren, J. P., Portaels, F. & Huygen, K. Protective efficacy of a DNA vaccine encoding antigen 85A from Mycobacterium bovis BCG against Buruli ulcer. Infect. Immun. 69, 5403-5411 (2001).
24. Tanghe, A., Dangy, J. P., Pluschke, G. & Huygen, K. Improved protective efficacy of a species-specific DNA vaccine encoding mycolyl-transferase Ag85A from Mycobacterium ulcerans by homologous protein boosting. PLoS Negl. Trop. Dis. 2, e199 (2008).
25. Torrado, E. et al. Mycolactone-mediated inhibition of tumor necrosis factor production by macrophages infected with Mycobacterium ulcerans has implications for the control of infection. Infect. Immun. 75, 3979-3988 (2007).
26. Hayman, J. Postulated epidemiology of Mycobacterium ulcerans infection. Intern. J. Epidemiol. 20, 1093-1098 (1991).
27. Aiga, H. et al. Assessing water-related risk factors for Buruli ulcer: A case-control study in Ghana. Am. J. Trop. Med. Hyg. 71 387-392 (2004).
28. Raghunathan, P. L. et al. Risk factors for Buruli ulcer disease (Mycobacterium ulcerans infection): Results from a case-control study in Ghana. Clin. Infect. Dis. 40, 1445-1453 (2005).
29. World Health Organization. Buruli ulcer: History and background. (WHO, Geneva, 1975).
30. Marsollier, L. et al. Aquatic plants stimulate the growth of and biofilm formation by Mycobacterium ulcerans in axenic culture and harbor these bacteria in the environment. Appl. Environ. Microbiol. 70, 1097-1103 (2004).
31. Marsollier, L. et al. Aquatic snails, passive hosts of Mycobacterium ulcerans. Appl. Environ. Microbiol. 70, 6296-6298 (2004).
32. Portaels, F., Elsen, P., Guimares-Peres, A., Fonteyne, P. A. & Meyers, W. M. Insects in the transmission of Mycobacterium ulcerans infection. Lancet 353, 986 (1999).
33. Yip, M. J. et al. Evolution of Mycobacterium ulcerans and other mycolactone-producing mycobacteria from a common Mycobacterium marinum progenitor. J. Bacteriol. 189, 2021-2029 (2007).
34. Marsollier, L. et al. Aquatic insects as a vector for Mycobacterium ulcerans. Appl. Environ. Microbiol. 68, 4623-4628 (2002).
35. Marsollier, L. et al. Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone. Cell. Microbiol. 7, 935-943 (2005).
36. Marsollier, L. et al. Early trafficking events of Mycobacterium ulcerans within Naucoris cimicoides. Cell. Microbiol. 9, 347-355 (2007).
37. Marsollier, L. et al. Protection against Mycobacterium ulcerans lesion development by exposure to aquatic insect saliva. PLoS Med. 4, e64 (2007).
38. Portaels, F. et al. First cultivation and characterization of Mycobacterium ulcerans from the environment. PLoS Negl. Trop. Dis. 2, e178 (2008).
39. Johnson, P. D. et al. Mycobacterium ulcerans in mosquitoes captured during outbreak of Buruli ulcer, southeastern Australia. Emerg. Infect. Dis. 13, 1653-1660 (2007).
40. Debacker, M. et al. Mycobacterium ulcerans disease (Buruli ulcer) in rural hospital, Southern Benin, 1997-2001. Emerg. Infect. Dis. 10, 1391-1398 (2004).
41. Debacker, M. et al. Mycobacterium ulcerans disease: Role of age and gender in incidence and morbidity. Trop. Med. Int. Health 9 1297-1304 (2004).
42. Quek, T. Y. et al. Risk factors for Mycobacterium ulcerans infection, southeastern Australia. Emerg. Infect. Dis. 13, 1661-1666 (2007).
43. Pouillot, R. et al. Risk factors for Buruli ulcer: A case control study in Cameroon. PLoS Negl. Trop. Dis. 1, e101 (2007).
44. Benbow, M. E. et al. Aquatic invertebrates as unlikely vectors of Buruli ulcer disease. Emerg. Infect. Dis. 14, 1247-1254 (2008).
45. Tobin, D. M. & Ramakrishnan, L. Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell. Microbiol. 10, 1027-1039 (2008).
46. Pozos, T. & Ramakrishnan, L. New models for the study of Mycobacterium-host interactions. Curr. Opin. Immunol. 16, 499-505 (2004).
47. Ross, B. C. et al. Development of a PCR assay for rapid diagnosis of Mycobacterium ulcerans infection. J. Clin. Microbiol. 35, 1696-1700 (1997).
48. Stinear, T. et al. Identification and characterization of IS2404 and IS2606: Two distinct repeated sequences for detection of Mycobacterium ulcerans by PCR. J. Clin. Microbiol. 37, 1018-1023 (1999).
49. Yip, M. J. et al. Evolution of Mycobacterium ulcerans and other mycolactone-producing mycobacteria from a common Mycobacterium marinum progenitor. J. Bacteriol. 189, 2021-2029 (2007).
50. Stinear, T. P., Jenkin, G. A., Johnson, P. D. R. & Davies, J. K. Comparative genetic analysis of Mycobacterium ulcerans and Mycobacterium marinum reveals evidence of recent divergence. J. Bacteriol. 182, 6322-6330 (2000).
51. Portaels, F. et al. Variability in 3′ end of 16S rRNA sequence of Mycobacterium ulcerans is related to geographic origin of isolates. J. Clin. Microbiol. 34, 962-965 (1996).
52. Rondini, S. et al. Ongoing genome reduction in Mycobacterium ulcerans. Emerg. Infect. Dis. 13, 1008-1015 (2007).
53. Kaser, M. et al. Evolution of two distinct phylogenetic lineages of the emerging human pathogen Mycobacterium ulcerans. BMC Evol. Biol. 7, 177 (2007).
54. Stinear, T. P. et al. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res. 17, 192-200 (2007).
55. Parkhill, J. et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523-527 (2001).
56. Parkhill, J. et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nature Genet. 35, 32-40 (2003).
57. Abdallah, A. M. et al. Type VII secretion - mycobacteria show the way. Nature Rev. Microbiol. 5, 883-891 (2007).
58. Brodin, P., Rosenkrands, I., Andersen, P., Cole, S. T. & Brosch, R. ESAT-6 proteins: Protective antigens and virulence factors? Trends Microbiol. 12, 500-508 (2004).
59. Mishra, K. C. et al. Functional role of the PE domain and immunogenicity of the Mycobacterium tuberculosis triacylglycerol hydrolase LipY. Infect. Immun. 76, 127-140 (2008).
60. Fortune, S. M. et al. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc. Natl Acad. Sci. USA 102, 10676-10681 (2005).
61. Huber, C. A., Ruf, M. T., Pluschke, G. & Kaser, M. Independent loss of immunogenic proteins in Mycobacterium ulcerans suggests immune evasion. Clin. Vaccine Immunol. 15, 598-606 (2008).
62. Reed, M. B. et al. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431 84-87 (2004).
63. Daffe, M., Varnerot, A. & Levy-Frebault, V. V. The phenolic mycoside of Mycobacterium ulcerans: Structure and taxonomic implications. J. Gen. Microbiol. 138, 131-137 (1992).
64. Ramakrishnan, L., Tran, H. T., Federspiel, N. A. & Falkow, S. A crtB homolog essential for photochromogenicity in Mycobacterium marinum isolation, characterization, and gene disruption via homologous recombination. J. Bacteriol. 179, 5862-5868 (1997).
65. Stinear, T. P., Pryor, M. J., Porter, J. L. & Cole, S. T. Functional analysis and annotation of the virulence plasmid pMUM001 from Mycobacterium ulcerans. Microbiology 151, 683-692 (2005).
66. Stinear, T. P. et al. Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans. Proc. Natl Acad. Sci. USA 101, 1345-1349 (2004).
67. Hong, H., Stinear, T., Porter, J., Demangel, C. & Leadlay, P. F. A novel mycolactone toxin obtained by biosynthetic engineering. Chembiochem 8, 2043-2047 (2007).
68. Stinear, T. P. et al. Common evolutionary origin for the unstable virulence plasmid pMUM found in geographically diverse strains of Mycobacterium ulcerans. J. Bacteriol. 187, 1668-1676 (2005).
69. Mve-Obiang, A. et al. A newly discovered mycobacterial pathogen isolated from laboratory colonies of Xenopus species with lethal infections produces a novel form of mycolactone, the Mycobacterium ulcerans macrolide toxin. Infect. Immun. 73, 3307-3312 (2005).
70. Bali, S. & Weissman, K. J. Ketoreduction in mycolactone biosynthesis: insight into substrate specificity and stereocontrol from studies of discrete ketoreductase domains in vitro. Chembiochem 7, 1935-1942 (2006).
71. Meier, J. L., Barrows-Yano, T., Foley, T. L., Wike, C. L. & Burkart, M. D. The unusual macrocycle forming thioesterase of mycolactone. Mol. Biosyst. 4, 663-671 (2008).
72. Tafelmeyer, P. et al. Comprehensive proteome analysis of Mycobacterium ulcerans and quantitative comparison of mycolactone biosynthesis. Proteomics 8, 3124-3138 (2008).
73. Ranger, B. S. et al. Globally distributed mycobacterial fish pathogens produce a novel plasmid-encoded toxic macrolide, mycolactone F. Infect. Immun. 74, 6037-6045 (2006).
74. Mve-Obiang, A., Lee, R. E., Portaels, F. & Small, P. L. Heterogeneity of mycolactones produced by clinical isolates of Mycobacterium ulcerans implications for virulence. Infect. Immun. 71, 774-783 (2003).
75. Judd, T. C., Bischoff, A., Kishi, Y., Adusumilli, S. & Small, P. L. Structure determination of mycolactone C via total synthesis. Org. Lett. 6, 4901-4904 (2004).
76. Hong, H., Stinear, T., Skelton, P., Spencer, J. B. & Leadlay, P. F. Structure elucidation of a novel family of mycolactone toxins from the frog pathogen Mycobacterium sp. MU128FXT by mass spectrometry. Chem. Commun. (Camb.) 34, 4306-4308 (2005).
77. Hong, H., Spencer, J. B., Porter, J. L., Leadlay, P. F. & Stinear, T. A novel mycolactone from a clinical isolate of Mycobacterium ulcerans provides evidence for additional toxin heterogeneity as a result of specific changes in the modular polyketide synthase. Chembiochem 6, 643-648 (2005).
78. Rhodes, M. W. et al. Mycobacterium pseudoshottsii sp. nov., a slowly growing chromogenic species isolated from Chesapeake Bay striped bass (Morone saxatilis). Int. J. Syst. Evol. Microbiol. 55, 1139-1147 (2005).
79. Snyder, D. S. & Small, P. L. Uptake and cellular actions of mycolactone, a virulence determinant for Mycobacterium ulcerans. Microb. Pathog. 34, 91-101 (2003).
80. Pahlevan, A. A. et al. The inhibitory action of Mycobacterium ulcerans soluble factor on monocyte/T cell cytokine production and NF-κB function. J. Immunol. 163, 3928-3935 (1999).
81. Coutanceau, E. et al. Selective suppression of dendritic cell functions by Mycobacterium ulcerans toxin mycolactone. J. Exp. Med. 204, 1395-1403 (2007).
82. Phillips, R. et al. Cytokine mRNA expression in Mycobacterium ulcerans-infected human skin and correlation with local inflammatory response. Infect. Immun. 74, 2917-2924 (2006).
83. Prevot, G. et al. Differential production of systemic and intralesional gamma interferon and interleukin-10 in nodular and ulcerative forms of Buruli disease. Infect. Immun. 72, 958-965 (2004).
84. Oliveira, M. S. et al. Infection with Mycobacterium ulcerans induces persistent inflammatory responses in mice. Infect. Immun. 73, 6299-6310 (2005).
85. Gooding, T. M. et al. Immune response to infection with Mycobacterium ulcerans. Infect. Immun. 69, 1704-1707 (2001).
86. Gooding, T. M., Johnson, P. D., Smith, M., Kemp, A. S. & Robins-Browne, R. M. Cytokine profiles of patients infected with Mycobacterium ulcerans and unaffected household contacts. Infect. Immun. 70, 5562-5567 (2002).
87. Gooding, T. M., Kemp, A. S., Robins-Browne, R. M., Smith, M. & Johnson, P. D. Acquired T-helper 1 lymphocyte anergy following infection with Mycobacterium ulcerans. Clin. Infect. Dis. 36, 1076-1077 (2003).
88. Westenbrink, B. D. et al. Cytokine responses to stimulation of whole blood from patients with Buruli ulcer disease in Ghana. Clin. Diagn. Lab. Immunol. 12, 125-129 (2005).
89. Phillips, R. et al. Cytokine response to antigen stimulation of whole blood from patients with Mycobacterium ulcerans disease compared to that from patients with tuberculosis. Clin. Vaccine Immunol. 13, 253-257 (2006).
90. Yeboah-Manu, D. et al. Systemic suppression of interferon-gamma responses in Buruli ulcer patients resolves after surgical excision of the lesions caused by the extracellular pathogen Mycobacterium ulcerans. J. Leukoc. Biol. 79, 1150-1156 (2006).
91. Kiszewski, A. E. et al. The local immune response in ulcerative lesions of Buruli disease. Clin. Exp. Immunol. 143, 445-451 (2006).
92. Bafende, A. E., Lukanu, N. P. & Numbi, A. N. Buruli ulcer in an AIDS patient. S. Afr. Med. J. 92, 437 (2002).
93. Johnson, R. C. et al. Disseminated Mycobacterium ulcerans disease in an HIV-positive patient: A case study. AIDS 16, 1704-1705 (2002).
94. Johnson, R. C. et al. Association of HIV infection and Mycobacterium ulcerans disease in Benin. AIDS 22, 901-903 (2008).
95. Hong, H. et al. Mycolactone diffuses from Mycobacterium ulcerans-infected tissues and targets mononuclear cells in peripheral blood and lymphoid organs. PLoS Negl. Trop. Dis. 2, e325 (2008).
96. Hong, H., Stinear, T., Porter, J., Demangel, C. & Leadlay, P. F. A novel mycolactone toxin obtained by biosynthetic engineering. Chembiochem 8, 2043-2047 (2007).
97. Stanford, J. L., Revill, W. D., Gunthorpe, W. J. & Grange, J. M. The production and preliminary investigation of Burulin, a new skin test reagent for Mycobacterium ulcerans infection. J. Hyg. (Lond. 74, 7-16 (1975).
98. Schutte, D. et al. Development of highly organized lymphoid structures in Buruli ulcer lesions after treatment with rifampicin and streptomycin. PLoS Negl. Trop. Dis. 1, e2 (2007).
99. Abe, M. & Thomson, A. W. Influence of immunosuppressive drugs on dendritic cells. Transpl. Immunol. 11, 357-365 (2003).
100. Staruch, M. J., Camacho, R. & Dumont, F. J. Distinctive calcineurin-dependent (FK506-sensitive) mechanisms regulate the production of the CC chemokines macrophage inflammatory protein (MIP)-1α, MIP-1β, and RANTES vs IL-2 and TNF-α by activated human T cells. Cell. Immunol. 190, 121-31 (1998).
101. Springer, B., Stockman, L., Teschner, K., Roberts, G. D. & Bottger, E. C. Two-laboratory collaborative study on identification of mycobacteria: molecular versus phenotypic methods. J. Clin. Microbiol. 34, 296-303 (1996).
102. Saitou, N. & Nei, M. The neighbour-joining method: A new method for constructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).
103. Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783-791 (1985).
104. Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599 (2007).