Mycolactone-mediated inhibition of tumor necrosis factor production by macrophages infected with Mycobacterium ulcerans has implications for the control of infection

Infection and Immunity

Volumn 75, Issue 8, 2007, Pages 3979-3988

  Torrado, Egídio ^a   Adusumilli, Sarojini ^b   Fraga, Alexandra G ^a   Small, Pamela L C ^b   Castro, Antonio G ^a   Pedrosa, Jorge ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOTOXIN; MACROPHAGE INFLAMMATORY PROTEIN 2; MYCOLACTONE; PROTEIN P55; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BONE MARROW CELL; BURULI ULCER; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; GROWTH CURVE; IMMUNE RESPONSE; INFECTION CONTROL; INFLAMMATION; KNOCKOUT MOUSE; LIFE CYCLE; MACROPHAGE; MOUSE; MYCOBACTERIUM ULCERANS; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; STRAIN DIFFERENCE; WILD TYPE;

ANIMALS; BACTERIAL TOXINS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; FOOT; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOKINES; MYCOBACTERIUM INFECTIONS, ATYPICAL; MYCOBACTERIUM ULCERANS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; TUMOR NECROSIS FACTOR DECOY RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

EID: 34547624336     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00290-07     Document Type: Article

References (89)

1. Abalos, F. M., J. Aguiar, Sr., A. Guedenon, F. Portaels, and W. M. Meyers. 2000. Mycobacterium ulcerans infection (Buruli ulcer): a case report of the disseminated nonulcerative form. Ann. Diagn. Pathol. 4:386-390.
2. Adusumilli, S., A. Mve-Obiang, T. Sparer, W. Meyers, J. Hayman, and P. L. Small. 2005. 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.
3. Asiedu, K., and S. Etuaful. 1998. Socioeconomic implications of Buruli ulcer in Ghana: a three-year review. Am. J. Trop. Med. Hyg. 59:1015-1022.
4. Bean, A. G., D. R. Roach, H. Briscoe, M. P. France, H. Korner, J. D. Sedgwick, and W. J. Britton. 1999. Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J. Immunol. 162:3504-3511.
5. Bendtzen, K. 1988. Interleukin 1, interleukin 6 and tumor necrosis factor in infection, inflammation and immunity. Immunol. Lett. 19:183-191.
6. Busam, K. J., T. E. Kiehn, S. P. Salob, and P. L. Myskowski. 1999. Histologic reactions to cutaneous infections by Mycobacterium haemophilum. Am. J. Surg. Pathol. 23:1379-1385.
7. Chan, J., Y. Xing, R. S. Magliozzo, and B. R. Bloom. 1992. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175:1111-1122.
8. Chemlal, K., G. Huys, F. Laval, V. Vincent, C. Savage, C. Gutierrez, M. A. Laneelle, J. Swings, W. M. Meyers, M. Daffe, and F. Portaels. 2002. Characterization of an unusual Mycobacterium: a possible missing link between Mycobacterium marinum and Mycobacterium ulcerans. J. Clin. Microbiol. 40:2370-2380.
9. Clancey, J. K., O. G. Dodge, H. F. Lunn, and M. L. Oduori. 1961. Mycobacterial skin ulcers in Uganda. Lancet 278:951-954.
10. Clark, R. B., H. Spector, D. M. Friedman, K. J. Oldrati, C. L. Young, and S. C. Nelson. 1990. Osteomyelitis and synovitis produced by Mycobacterium marinum in a fisherman. J. Clin. Microbiol. 28:2570-2572.
11. Connor, D. H., and H. F. Lunn. 1965. Mycobacterium ulcerans infection (with comments on pathogenesis). Int. J. Lepr. 33:698-709.
12. Connor, D. H., and H. F. Lunn. 1966. Buruli ulceration. A clinicopathologic study of 38 Ugandans with Mycobacterium ulcerans ulceration. Arch. Pathol. 81:183-199.
13. Coutanceau, E., L. Marsollier, R. Brosch, E. Perret, P. Goossens, M. Tanguy, S. T. Cole, P. L. Small, and C. Demangel. 2005. 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.
14. Dannenberg, A. M., Jr. 1994. Pathogenesis of pulmonary tuberculosis: an interplay of time-damaging and macrophage activating immune responses. Dual mechanisms that control bacilary multiplication, p. 459-483. In B. R. Bloom (ed.), Tuberculosis: protection, pathogenesis, and control. American Society for Microbiology, Washington, DC.
15. Debacker, M., J. Aguiar, C. Steunou, C. Zinsou, M. W. Meyers, A. Guedenom, J. T. Scott, M. Dramaix, and F. Portaels. 2004. Mycobacterium ulcerans disease (Buruli ulcer) in rural hospital, southern Benin, 1997-2001. Emerg. Infect. Dis. 10:1391-1398.
16. Debacker, M., J. Aguiar, C. Steunou, C. Zinsou, W. M. Meyers, J. T. Scott, M. Dramaix, and F. Portaels. 2004. Mycobacterium ulcerans disease: role of age and gender in incidence and morbidity. Trop. Med. Int. Health 9:1297-1304.
17. Denis, M. 1991. Involvement of cytokines in determining resistance and acquired immunity in murine tuberculosis. J. Leukoc. Biol. 50:495-501.
18. Dinarello, C. A. 1992. The role of interleukin-1 in host responses to infectious diseases. Infect. Agents Dis. 1:227-236.
19. Dobos, K. M., F. D. Quinn, D. A. Ashford, C. R. Horsburgh, and C. H. King. 1999. Emergence of a unique group of necrotizing mycobacterial diseases. Emerg. Infect. Dis. 5:367-378.
20. Dobos, K. M., E. A. Spotts, B. J. Marston, C. R. Horsburgh, Jr., and C. H. King. 2000. Serologic response to culture filtrate antigens of Mycobacterium ulcerans during Buruli ulcer disease. Emerg. Infect. Dis. 6:158-164.
21. Ehlers, S., J. Benini, S. Kutsch, R. Endres, E. T. Rietschel, and K. Pfeffer. 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.
22. Evans, M. R., H. S. Thangaraj, and M. H. Wansbrough-Jones. 2000. Buruli ulcer. Curr. Opin. Infect. Dis. 13:109-112.
23. Falcone, V., E. B. Bassey, A. Toniolo, P. G. Conaldi, and F. M. Collins. 1994. Differential release of tumor necrosis factor-alpha from murine peritoneal macrophages stimulated with virulent and avirulent species of mycobacteria. FEMS Immunol. Med. Microbiol. 8:225-232.
24. Flesch, I. E., and S. H. Kaufmann. 1990. Activation of tuberculostatic macrophage functions by gamma interferon, interleukin-4, and tumor necrosis factor. Infect. Immun. 58:2675-2677.
25. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93-129.
26. Flynn, J. L., M. M. Goldstein, J. Chan, K. J. Triebold, K. Pfeffer, C. J. Lowenstein, R. Schreiber, T. W. Mak, and B. R. Bloom. 1995. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2:561-572.
27. Fulton, S. A., S. M. Reba, T. D. Martin, and W. H. Boom. 2002. Neutrophil-mediated mycobacteriocidal immunity in the lung during Mycobacterium bovis BCG infection in C57BL/6 mice. Infect. Immun. 70:5322-5327.
28. Fumey, S. K., P. S. Skinner, A. D. Roberts, R. Appelberg, and I. M. Orme. 1992. Capacity of Mycobacterium avium isolates to grow well or poorly in murine macrophages resides in their ability to induce secretion of tumor necrosis factor. Infect. Immun. 60:4410-4413.
29. Gao, L. Y., S. Guo, B. McLaughlin, H. Morisaki, J. N. Engel, and E. J. Brown. 2004. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol. Microbiol. 53:1677-1693.
30. Garcia, I., Y. Miyazaki, G. Marchal, W. Lesslauer, and P. Vassalli. 1997. High sensitivity of transgenic mice expressing soluble TNFR1 fusion protein to mycobacterial infections: synergistic action of TNF and IFN-gamma in the differentiation of protective granulomas. Eur. J. Immunol. 27:3182-3190.
31. George, K. M., L. P. Barker, D. M. Welty, and P. L. Small. 1998. Partial purification and characterization of biological effects of a lipid toxin produced by Mycobacterium ulcerans. Infect. Immun. 66:587-593.
32. George, K. M., D. Chatterjee, G. Gunawardana, D. Welty, J. Hayman, R. Lee, and P. L. Small. 1999. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283:854-857.
33. George, K. M., L. Pascopella, D. M. Welty, and P. L. Small. 2000. A Mycobacterium ulcerans toxin, mycolactone, causes apoptosis in guinea pig ulcers and tissue culture cells. Infect. Immun. 68:877-883.
34. Giacomini, E., E. Iona, L. Ferroni, M. Miettinen, L. Fattorini, G. Orefici, I. Julkunen, and E. M. Coccia. 2001. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J. Immunol. 166:7033-7041.
35. Gooding, T. M., P. D. Johnson, D. E. Campbell, J. A. Hayman, E. L. Hartland, A. S. Kemp, and R. M. Robins-Browne. 2001. Immune response to infection with Mycobacterium ulcerans. Infect. Immun. 69:1704-1707.
36. Gooding, T. M., P. D. Johnson, M. Smith, A. S. Kemp, and R. M. Robins-Browne. 2002. Cytokine profiles of patients infected with Mycobacterium ulcerans and unaffected household contacts. Infect. Immun. 70:5562-5567.
37. Gooding, T. M., A. S. Kemp, R. M. Robins-Browne, M. Smith, and P. D. Johnson. 2003. Acquired T-helper 1 lymphocyte anergy following infection with Mycobacterium ulcerans. Clin. Infect. Dis. 36:1076-1077.
38. Guarner, J., J. Harden, E. A. Whitney, P. L. Raghunathan, Y. Stienstra, K. Asamoa, S. Etuaful, E. Klutse, E. Quarshie, T. S. van der Werf, W. T. van der Graaf, C. H. King, and D. A. Ashford. 2003. Histopathologic features of Mycobacterium ulcerans infection. Emerg. Infect. Dis. 9:651-656.
39. Havell, E. A. 1992. Role of TNF in resistance to bacteria. Immunol. Ser. 56:341-363.
40. Hayman, J. 1993. Out of Africa: observations on the histopathology of Mycobacterium ulcerans infection. J. Clin. Pathol. 46:5-9.
41. Hayman, J., and A. McQueen. 1985. The pathology of Mycobacterium ulcerans infection. Pathology 17:594-600.
42. Hofer, M., B. Hirschel, P. Kirschner, M. Beghetti, A. Kaelin, C. A. Siegrist, S. Suter, A. Teske, and E. C. Bottger. 1993. Brief report: disseminated osteomyelitis from Mycobacterium ulcerans after a snakebite. N. Engl. J. Med. 328:1007-1009.
43. Hong, H., P. J. Gates, J. Staunton, T. Stinear, S. T. Cole, P. F. Leadlay, and J. B. Spencer. 2003. Identification using LC-MSn of co-metabolites in the biosynthesis of the polyketide toxin mycolactone by a clinical isolate of Mycobacterium ulcerans. Chem. Commun. (Cambridge) 22:2822-2823.
44. Hong, H., J. B. Spencer, J. L. Porter, P. F. Leadlay, and T. Stinear. 2005. 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 6:1-5.
45. Hsu, T., S. M. Hingley-Wilson, B. Chen, M. Chen, A. Z. Dai, P. M. Morin, C. B. Marks, J. Padiyar, C. Goulding, M. Gingery, D. Eisenberg, R. G. Russell, S. C. Derrick, F. M. Collins, S. L. Morris, C. H. King, and W. R. Jacobs, Jr. 2003. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc. Natl. Acad. Sci. USA 100:12420-12425.
46. Judd, T. C., A. Bischoff, Y. Kishi, S. Adusumilli, and P. L. C. Small. 2004. Structure determination of mycolactone C via total synthesis. Org. Lett. 6:4901-4904.
47. Kaufmann, S. H. 1993. Immunity to intracellular bacteria. Annu. Rev. Immunol. 11:129-163.
48. Kindler, V., A. P. Sappino, G. E. Grau, P. F. Piguet, and P. Vassalli. 1989. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell 56:731-740.
49. Kiszewski, A. E., E. Becerril, L. D. Aguilar, I. T. Kader, W. Myers, F. Portaels, and P. R. Hernandez. 2006. The local immune response in ulcerative lesions of Buruli disease. Clin. Exp. Immunol. 143:445-451.
50. Krieg, R. E., W. T. Hockmeyer, and D. H. Connor. 1974. Toxin of Mycobacterium ulcerans. Production and effects in guinea pig skin. Arch. Dermatol. 110:783-788.
51. Lewis, K. N., R. Liao, K. M. Guinn, M. J. Hickey, S. Smith, M. A. Behr, and D. R. Sherman. 2003. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J. Infect. Dis. 187:117-123.
52. Liew, F. Y., Y. Li, and S. Millott. 1990. Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. J. Immunol. 145:4306-4310.
53. MacCallum, P., J. C. Tolhurst, G. Buckle, and H. A. Sissons. 1948. A new mycobacterial infection in man. J. Pathol. Bacteriol. 60:93-122.
54. Marston, B. J., M. O. Diallo, C. R. Horsburgh, Jr., I. Diomande, M. Z. Saki, J. M. Kanga, G. Patrice, H. B. Lipman, S. M. Ostroff, and R. C. Good. 1995. Emergence of Buruli ulcer disease in the Daloa region of Cote d'Ivoire. Am. J. Trop. Med. Hyg. 52:219-224.
55. Mor, N., I. Lutsky, and L. Levy. 1981. Response in the hindfoot pad and popliteal lymph node of C57BL mice to infection with Mycobacterium marinum. Isr. J. Med. Sci. 17:236-244.
56. Mve-Obiang, A., R. E. Lee, F. Portaels, and P. L. Small. 2003. Heterogeneity of mycolactones produced by clinical isolates of Mycobacterium ulcerans: implications for virulence. Infect. Immun. 71:774-783.
57. Mve-Obiang, A., R. E. Lee, E. S. Umstot, K. A. Trott, T. C. Grammer, J. M. Parker, B. S. Ranger, R. Grainger, E. A. Mahrous, and P. L. Small. 2005. 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.
58. Noeske, J., C. Kuaban, S. Rondini, P. Sorlin, L. Ciaffi, J. Mbuagbaw, F. Portaels, and G. Pluschke. 2004. Buruli ulcer disease in Cameroon rediscovered. Am. J. Trop. Med. Hyg. 70:520-526.
59. Oliveira, M. S., A. G. Fraga, E. Torrado, A. G. Castro, J. P. Pereira, A. L. Filho, F. Milanezi, F. C. Schmitt, W. M. Meyers, F. Portaels, M. T. Silva, and J. Pedrosa. 2005. Infection with Mycobacterium ulcerans induces persistent inflammatory responses in mice. Infect. Immun. 73:6299-6310.
60. Pahlevan, A. A., D. J. Wright, C. Andrews, K. M. George, P. L. Small, and B. M. Foxwell. 1999. The inhibitory action of Mycobacterium ulcerans soluble factor on monocyte/T cell cytokine production and NF-kappa B function. J. Immunol. 163:3928-3935.
61. + T cell-mediated suppression by dendritic cells. Science 299: 1033-1036.
62. Pedrosa, J., B. M. Saunders, R. Appelberg, I. M. Orme, M. T. Silva, and A. M. Cooper. 2000. Neutrophils play a protective nonphagocytic role in systemic Mycobacterium tuberculosis infection of mice. Infect. Immun. 68: 577-583.
63. Peduzzi, E., C. Groeper, D. Schutte, P. Zajac, S. Rondini, E. Mensah-Quainoo, G. C. Spagnoli, G. Pluschke, and C. A. Daubenberger. 2006. Local activation of the innate immune system in Buruli ulcer lesions. J. Investig. Dermatol. 127:638-645.
64. Phillips, R., C. Horsfield, J. Mangan, K. Laing, S. Etuaful, P. Awuah, K. Nyarko, F. Osei-Sarpong, P. Butcher, S. Lucas, and M. Wansbrough-Jones. 2006. Cytokine mRNA expression in Mycobacterium ulcerans-infected human skin and correlation with local inflammatory response. Infect. Immun. 74:2917-2924.
65. Pimsler, M., T. A. Sponsler, and W. M. Meyers. 1988. Immunosuppressive properties of the soluble toxin from Mycobacterium ulcerans. J. Infect. Dis. 157:577-580.
66. Prevot, G., E. Bourreau, H. Pascalis, R. Pradinaud, A. Tanghe, K. Huygen, and P. Launois. 2004. Differential production of systemic and intralesional gamma interferon and interleukin-10 in nodular and ulcerative forms of Buruli disease. Infect. Immun. 72:958-965.
67. Read, J. K., C. M. Heggie, W. M. Meyers, and D. H. Connor. 1974. Cytotoxic activity of Mycobacterium ulcerans. Infect. Immun. 9:1114-1122.
68. Rhoades, E. R., A. M. Cooper, and I. M. Orme. 1995. Chemokine response in mice infected with Mycobacterium tuberculosis. Infect. Immun. 63:3871-3877.
69. Sarmento, A. M., and R. Appelberg. 1995. Relationship between virulence of Mycobacterium avium strains and induction of tumor necrosis factor alpha production in infected mice and in in vitro-cultured mouse macrophages. Infect. Immun. 63:3759-3764.
70. Saunders, B. M., and C. Cheers. 1995. Inflammatory response following intranasal infection with Mycobacterium avium complex: role of T-cell subsets and gamma interferon. Infect. Immun. 63:2282-2287.
71. Seiler, P., P. Aichele, B. Raupach, B. Odermatt, U. Steinhoff, and S. H. Kaufmann. 2000. Rapid neutrophil response controls fast-replicating intracellular bacteria but not slow-replicating Mycobacterium tuberculosis. J. Infect. Dis. 181:671-680.
72. Shepard, C. C., and D. H. McRae. 1968. A method for counting acid-fast bacteria. Int. J. Lepr. Other Mycobact. Dis. 36:78-82.
73. Shibuya, K., D. Robinson, F. Zonin, S. B. Hartley, S. E. Macatonia, C. Somoza, C. A. Hunter, K. M. Murphy, and A. O'Garra. 1998. IL-1 alpha and TNF-alpha are required for IL-12-induced development of Th1 cells producing high levels of IFN-gamma in BALB/c but not C57BL/6 mice. J. Immunol. 160:1708-1716.
74. Silva, M. T., M. N. Silva, and R. Appelberg. 1989. Neutrophil-macrophage cooperation in the host defence against mycobacterial infections. Microb. Pathog. 6:369-380.
75. Snyder, D. S., and P. L. Small. 2003. Uptake and cellular actions of mycolactone, a virulence determinant for Mycobacterium ulcerans. Microb. Pathog. 34:91-101.
76. Stanford, J. L., W. D. Revill, W. J. Gunthorpe, and J. M. Grange. 1975. The production and preliminary investigation of Burulin, a new skin test reagent for Mycobacterium ulcerans infection. J. Hyg. (London) 74:7-16.
77. Stanley, S. A., S. Raghavan, W. W. Hwang, and J. S. Cox. 2003. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc. Natl. Acad. Sci. USA 100:13001-13006.
78. Stienstra, Y., W. T. van der Graaf, G. J. te Meerman, T. H. The, L. F. de Leij, and T. S. van der Werf. 2001. Susceptibility to development of Mycobacterium ulcerans disease: review of possible risk factors. Trop. Med. Int. Health 6:554-562.
79. Stinear, T. P., H. Hong, W. Frigui, M. J. Pryor, R. Brosch, T. Gamier, P. F. Leadlay, and S. T. Cole. 2005. Common evolutionary origin for the unstable virulence plasmid pMUM found in geographically diverse strains of Mycobacterium ulcerans. J. Bacteriol. 187:1668-1676.
80. Stinear, T. P., A. Mve-Obiang, P. L. Small, W. Frigui, M. J. Pryor, R. Brosch, G. A Jenkin, P. D. Johnson, J. K. Davies, R. E. Lee, S. Adusumilli, T. Garnier, S. F. Haydock, P. F. Leadlay, and S. T. Cole. 2004. Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans. Proc. Natl. Acad. Sci. USA 101:1345-1349.
81. Strohmeier, G. R., and M. J. Fenton. 1999. Roles of lipoarabinomannan in the pathogenesis of tuberculosis. Microbes Infect. 1:709-717.
82. Tanghe, A., J. Content, J. P. Van Vooren, F. Portaels, and K. Huygen. 2001. Protective efficacy of a DNA vaccine encoding antigen 85A from Mycobacterium bovis BCG against Buruli ulcer. Infect. Immun. 69:5403-5411.
83. Tonjum, T., D. B. Welty, E. Jantzen, and P. L. Small. 1998. Differentiation of Mycobacterium ulcerans, M. marinum, and M. haemophilum: mapping of their relationships to M. tuberculosis by fatty acid profile analysis, DNA-DNA hybridization, and 16S rRNA gene sequence analysis. J. Clin. Microbiol. 36:918-925.
84. Torrado, E., A. G. Fraga, A. G. Castro, P. Stragier, M. W. Meyers, F. Portaels, M. T. Silva, and J. Pedrosa. 2007. Evidence for an intramacrophage growth phase of Mycobacterium ulcerans. Infect. Immun. 75:977-987.
85. Travis, W. D., L. B. Travis, G. D. Roberts, D. W. Su, and L. W. Weiland. 1985. The histopathologic spectrum in Mycobacterium marinum infection. Arch. Pathol. Lab. Med. 109:1109-1113.
86. van der Werf, T. S., W. T. van der Graaf, J. W. Tappero, and K. Asiedu. 1999. Mycobacterium ulcerans infection. Lancet 354:1013-1018.
87. Westenbrink, B. D., Y. Stienstra, M. G. Huitema, W. A. Thompson, E. O. Klutse, E. O. Ampadu, H. M. Boezen, P. C. Limburg, and T. S. van der Werf. 2005. Cytokine responses to stimulation of whole blood from patients with Buruli ulcer disease in Ghana. Clin. Diagn. Lab. Immunol. 12:125-129.
88. Widmer, U., K. R. Manogue, A. Cerami, and B. Sherry. 1993. Genomic cloning and promoter analysis of macrophage inflammatory protein (MIP)-2, MIP-1 alpha, and MIP-1 beta, members of the chemokine superfamily of proinflammatory cytokines. J. Immunol. 150:4996-5012.
89. Yip, M. J., J. L. Porter, J. A. Fyfe, C. J. Lavender, F. Portaels, M. Rhodes, H. Kator, A. Colorni, G. A. Jenkin, and T. Stinear. 2007. Evolution of Mycobacterium ulcerans and other mycolactone-producing mycobacteria from a common Mycobacterium marinum progenitor. J. Bacteriol. 189:2021-2029.