Pathogenetic mechanisms of the intracellular parasite Mycobacterium ulcerans leading to Buruli ulcer

The Lancet Infectious Diseases

Volumn 9, Issue 11, 2009, Pages 699-710

  Silva, Manuel T ^a   Portaels, Françoise ^b   Pedrosa, Jorge ^c  

^a UNIVERSITY OF PORTO   (Portugal)

^b INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^c UNIVERSITY OF MINHO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

EXOTOXIN; MYCOLACTONE; UNCLASSIFIED DRUG;

BACTERIAL GROWTH; BACTERIAL VIRULENCE; BURULI ULCER; CELLULAR IMMUNITY; CYTOTOXICITY; DELAYED HYPERSENSITIVITY; HOST PARASITE INTERACTION; HUMAN; INFLAMMATION; MYCOBACTERIUM ULCERANS; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

BACTERIAL TOXINS; BURULI ULCER; HUMANS; HYPERSENSITIVITY, DELAYED; IMMUNITY, CELLULAR; INFLAMMATION; MYCOBACTERIUM ULCERANS;

EID: 70349985959     PISSN: 14733099     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1473-3099(09)70234-8     Document Type: Review

References (139)

1. van der Werf T.S., Stienstra Y., Johnson R.C., et al. Mycobacterium ulcerans disease. Bull World Health Organ 83 (2005) 785-791
2. Walsh D.S., Portaels F., and Meyers W.M. Buruli ulcer (Mycobacterium ulcerans infection). Trans R Soc Trop Med Hyg 102 (2008) 969-978
3. Senior K. Buruli ulcer: dare we continue to ignore it?. Lancet Infect Dis 9 (2009) 273
4. Grietens K.P., Boock A.U., Peeters H., Hausmann-Muela S., Toomer E., and Ribera J.M. "It is me who endures but my family that suffers": social isolation as a consequence of the household cost burden of Buruli ulcer free of charge hospital treatment. PLoS Negl Trop Dis 2 (2008) e321
5. Stinear T.P., Jenkin G.A., Johnson P.D., and Davies J.K. Comparative genetic analysis of Mycobacterium ulcerans and Mycobacterium marinum reveals evidence of recent divergence. J Bacteriol 182 (2000) 6322-6330
6. Stinear T.P., Seemann T., Pidot S., et al. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res 17 (2007) 192-200
7. Yip M.J., Porter J.L., Fyfe J.A., et al. Evolution of Mycobacterium ulcerans and other mycolactone-producing mycobacteria from a common Mycobacterium marinum progenitor. J Bacteriol 189 (2007) 2021-2029
8. Stinear T.P., Mve-Obiang A., Small P.L., et al. Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans. Proc Natl Acad Sci USA 101 (2004) 1345-1349
9. Demangel C., Stinear T.P., and Cole S.T. Buruli ulcer: reductive evolution enhances pathogenicity of Mycobacterium ulcerans. Nat Rev Microbiol 7 (2009) 50-60
10. Stinear T.P., Hong H., Frigui W., et al. Common evolutionary origin for the unstable virulence plasmid pMUM found in geographically diverse strains of Mycobacterium ulcerans. J Bacteriol 187 (2005) 1668-1676
11. Kaser M., Rondini S., Naegeli M., et al. Evolution of two distinct phylogenetic lineages of the emerging human pathogen Mycobacterium ulcerans. BMC Evol Biol 7 (2007) 177
12. Cole S.T., Eiglmeier K., Parkhill J., et al. Massive gene decay in the leprosy bacillus. Nature 409 (2001) 1007-1011
13. Dega H., Robert J., Bonnafous P., Jarlier V., and Grosset J. Activities of several antimicrobials against Mycobacterium ulcerans infection in mice. Antimicrob Agents Chemother 44 (2000) 2367-2372
14. Eddyani M., and Portaels F. Survival of Mycobacterium ulcerans at 37 degrees C. Clin Microbiol Infect 13 (2007) 1033-1035
15. MacCallum P., Tolhurst J.C., Buckle G., and Sissons H.A. A new mycobacterial infection in man. J Pathol Bacteriol 60 (1948) 93-122
16. Fenner F. The pathogenic behavior of Mycobacterium ulcerans and Mycobacterium balnei in the mouse and the developing chick embryo. Am Rev Tuberc 73 (1956) 650-673
17. Feldman W.H., Karlson A.G., and Herrick J.F. Mycobacterium ulcerans; pathogenesis of infection in mice, including determinations of dermal temperatures. Am J Pathol 33 (1957) 1163-1179
18. Krieg R.E., Hockmeyer W.T., and Connor D.H. Toxin of Mycobacterium ulcerans: Production and effects in guinea pig skin. Arch Dermatol 110 (1974) 783-788
19. Read J.K., Heggie C.M., Meyers W.M., and Connor D.H. Cytotoxic activity of Mycobacterium ulcerans. Infect Immun 9 (1974) 1114-1122
20. Portaels F., Zinsou C., Aguiar J., et al. Les atteintes osseuses dans l'ulcère de Buruli: A propos de 73 cas. Bull Séanc Acad R Sci Outre-Mer 49 (2003) 161-190
21. Sizaire V., Nackers F., Comte E., and Portaels F. Mycobacterium ulcerans infection: control, diagnosis, and treatment. Lancet Infect Dis 6 (2006) 288-296
22. Pimsler M., Sponsler T.A., and Meyers W.M. Immunosuppressive properties of the soluble toxin from Mycobacterium ulcerans. J Infect Dis 157 (1988) 577-580
23. George K.M., Chatterjee D., Gunawardana G., et al. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283 (1999) 854-857
24. George K.M., Pascopella L., Welty D.M., and Small P.L. A Mycobacterium ulcerans toxin, mycolactone, causes apoptosis in guinea pig ulcers and tissue culture cells. Infect Immun 68 (2000) 877-883
25. Hong H., Demangel C., Pidot S.J., Leadlay P.F., and Stinear T. Mycolactones: immunosuppressive and cytotoxic polyketides produced by aquatic mycobacteria. Nat Prod Rep 25 (2008) 447-454
26. Mve-Obiang A., Lee R.E., Portaels F., and Small P.L. Heterogeneity of mycolactones produced by clinical isolates of Mycobacterium ulcerans: implications for virulence. Infect Immun 71 (2003) 774-783
27. Oswald E., Nougayrede J.P., Taieb F., and Sugai M. Bacterial toxins that modulate host cell-cycle progression. Curr Opin Microbiol 8 (2005) 83-91
28. Simmonds R.E., Lali F.V., Smallie T., Small P.L., and Foxwell B.M. Mycolactone inhibits monocyte cytokine production by a posttranscriptional mechanism. J Immunol 182 (2009) 2194-2202
29. Oliveira M.S., Fraga A.G., Torrado E., et al. Infection with Mycobacterium ulcerans induces persistent inflammatory responses in mice. Infect Immun 73 (2005) 6299-6310
30. Torrado E., Fraga A.G., Castro A.G., et al. Evidence for an intramacrophage growth phase of Mycobacterium ulcerans. Infect Immun 75 (2007) 977-987
31. Walsh D.S., Meyers W.M., Portaels F., et al. High rates of apoptosis in human Mycobacterium ulcerans culture-positive Buruli ulcer skin lesions. Am J Trop Med Hyg 73 (2005) 410-415
32. van der Werf T.S., Stinear T., Stienstra Y., van der Graaf W.T., and Small P.L. Mycolactones and Mycobacterium ulcerans disease. Lancet 362 (2003) 1062-1064
33. Hayman J., and McQueen A. The pathology of Mycobacterium ulcerans infection. Pathology 17 (1985) 594-600
34. Guarner J., Bartlett J., Whitney E.A., et al. Histopathologic features of Mycobacterium ulcerans infection. Emerg Infect Dis 9 (2003) 651-656
35. Dobos K.M., Quinn F.D., Ashford D.A., Horsburgh C.R., and King C.H. Emergence of a unique group of necrotizing mycobacterial diseases. Emerg Infect Dis 5 (1999) 367-378
36. Hayman J. Out of Africa: observations on the histopathology of Mycobacterium ulcerans infection. J Clin Pathol 46 (1993) 5-9
37. Meyers W.M. Mycobacterial infections of the skin. In: Doerr W., and Seifert G. (Eds). Tropical pathology (1995), Springer-Verlag, Berlin and Heidelberg 291-377
38. Meyers W., and Hayman J. Pathology. In: Asiedu K., Scherpbier R., and Raviglione M. (Eds). Buruli ulcer, Mycobacterium ulcerans infection (2000), World Health Organization, Geneva 35-36
39. Kathuria P., Agarwal K., and Koranne R.V. The role of fine-needle aspiration cytology and Ziehl Neelsen staining in the diagnosis of cutaneous tuberculosis. Diagn Cytopathol 34 (2006) 826-829
40. Dannenberg Jr. A.M. Pathogenesis of pulmonary tuberculosis: an interplay of time-damaging and macrophage activating immune responses-dual mechanisms that control bacillary multiplication. In: Bloom B.R. (Ed). Tuberculosis: protection, pathogenesis, and control (1994), American Society for Microbiology, Washington, DC 459-483
41. Wansbrough-Jones M., and Phillips R. Buruli ulcer: emerging from obscurity. Lancet 367 (2006) 1849-1858
42. Hong H., Coutanceau E., Leclerc M., Caleechurn L., Leadlay P.F., and Demangel C. Mycolactone diffuses from Mycobacterium ulcerans-infected tissues and targets mononuclear cells in peripheral blood and lymphoid organs. PLoS Negl Trop Dis 2 (2008) e325
43. Rastogi N., Blom-Potar M.C., and David H.L. Comparative intracellular growth of difficult-to-grow and other mycobacteria in a macrophage cell line. Acta Leprol 7 (1989) 156-159
44. Adusumilli S., Mve-Obiang A., Sparer T., Meyers W., Hayman J., and Small P.L. Mycobacterium ulcerans toxic macrolide, mycolactone modulates the host immune response and cellular location of M ulcerans in vitro and in vivo. Cell Microbiol 7 (2005) 1295-1304
45. Coutanceau E., Marsollier L., Brosch R., 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 (2005) 1187-1196
46. Gooding T.M., Johnson P.D., Campbell D.E., et al. Immune response to infection with Mycobacterium ulcerans. Infect Immun 69 (2001) 1704-1707
47. Rondini S., Horsfield C., Mensah-Quainoo E., Junghanss T., Lucas S., and Pluschke G. Contiguous spread of Mycobacterium ulcerans in Buruli ulcer lesions analysed by histopathology and real-time PCR quantification of mycobacterial DNA. J Pathol 208 (2006) 119-128
48. Schutte D., Um-Boock A., Mensah-Quainoo E., Itin P., Schmid P., and Pluschke G. Development of highly organized lymphoid structures in buruli ulcer lesions after treatment with rifampicin and streptomycin. PLoS Negl Trop Dis 1 (2007) e2
49. Casadevall A., and Pirofski L. Host-pathogen interactions: the attributes of virulence. J Infect Dis 184 (2001) 337-344
50. Tafelmeyer P., Laurent C., Lenormand P., et al. Comprehensive proteome analysis of Mycobacterium ulcerans and quantitative comparison of mycolactone biosynthesis. Proteomics 8 (2008) 3124-3138
51. Marsollier L., Brodin P., Jackson M., et al. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLoS Pathog 3 (2007) e62
52. Rousseau C., Winter N., Pivert E., et al. Production of phthiocerol dimycocerosates protects Mycobacterium tuberculosis from the cidal activity of reactive nitrogen intermediates produced by macrophages and modulates the early immune response to infection. Cell Microbiol 6 (2004) 277-287
53. Guenin-Mace L., Simeone R., and Demangel C. Lipids of pathogenic mycobacteria: contributions to virulence and host immune suppression. Transbound Emerg Dis 56 (2009) 255-268
54. Songer J.G. Bacterial phospholipases and their role in virulence. Trends Microbiol 5 (1997) 156-161
55. Gomez A., Mve-Obiang A., Vray B., et al. Biochemical and genetic evidence for phospholipase C activity in Mycobacterium ulcerans. Infect Immun 68 (2000) 2995-2997
56. Portaels F., Silva M.T., and Meyers W.M. Buruli ulcer. Clin Dermatol 27 (2009) 291-305
57. Huygen K., Adjei O., Affolabi D., et al. Buruli ulcer disease: prospects for a vaccine. Med Microbiol Immunol 198 (2009) 69-77
58. Cosma C.L., Sherman D.R., and Ramakrishnan L. The secret lives of the pathogenic mycobacteria. Ann Rev Microbiol 57 (2003) 641-676
59. Johnson P.D., Stinear T., Small P.L., et al. Buruli ulcer (M ulcerans infection): new insights, new hope for disease control. PLoS Med 2 (2005) e108
60. Evans M.R., Thangaraj H.S., and Wansbrough-Jones M.H. Buruli ulcer. Curr Opin Infect Dis 13 (2000) 109-112
61. Pahlevan A.A., Wright D.J., Andrews C., George K.M., Small P.L., and Foxwell B.M. The inhibitory action of Mycobacterium ulcerans soluble factor on monocyte/T cell cytokine production and NF-κ B function. J Immunol 163 (1999) 3928-3935
62. Peduzzi E., Groeper C., Schutte D., et al. Local activation of the innate immune system in Buruli ulcer lesions. J Invest Dermatol 127 (2007) 638-645
63. Mor N., Lutsky I., and Levy L. Response in the hindfoot pad and popliteal lymph node of C57BL mice to infection with Mycobacterium marinum. Isr J Med Sci 17 (1981) 236-244
64. Silva M.T., Silva M.N., and Appelberg R. Neutrophil-macrophage cooperation in the host defence against mycobacterial infections. Microb Pathog 6 (1989) 369-380
65. Appelberg R., and Silva M.T. T cell-dependent chronic neutrophilia during mycobacterial infections. Clin Exp Immunol 78 (1989) 478-483
66. Abadie V., Badell E., Douillard P., et al. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 106 (2005) 1843-1850
67. D'Avila H., Roque N.R., Cardoso R.M., Castro-Faria-Neto H.C., Melo R.C., and Bozza P.T. Neutrophils recruited to the site of Mycobacterium bovis BCG infection undergo apoptosis and modulate lipid body biogenesis and prostaglandin E production by macrophages. Cell Microbiol 10 (2008) 2589-2604
68. Houngbedji M.G., Boissinot M., Bergeron G.M., and Frenette J. Subcutaneous injection of Mycobacterium ulcerans causes necrosis, chronic inflammatory response and fibrosis in skeletal muscle. Microbes Infect 10 (2008) 1236-1243
69. Schutte D., Umboock A., and Pluschke G. Phagocytosis of Mycobacterium ulcerans in the course of rifampicin and streptomycin chemotherapy in Buruli ulcer lesions. Br J Dermatol 160 (2009) 273-283
70. Phillips R., Horsfield C., Mangan J., et al. Cytokine mRNA expression in Mycobacterium ulcerans-infected human skin and correlation with local inflammatory response. Infect Immun 74 (2006) 2917-3014
71. Torrado E., Adusumilli S., Fraga A.G., Small P.L., Castro A.G., and Pedrosa J. Mycolactone-mediated inhibition of tumor necrosis factor production by macrophages infected with Mycobacterium ulcerans has implications for the control of infection. Infect Immun 75 (2007) 3979-3988
72. Scapini P., Lapinet-Vera J.A., Gasperini S., Calzetti F., Bazzoni F., and Cassatella M.A. The neutrophil as a cellular source of chemokines. Immunol Rev 177 (2000) 195-203
73. Tanimoto N., Terasawa M., Nakamura M., et al. Involvement of KC, MIP-2, and MCP-1 in leukocyte infiltration following injection of necrotic cells into the peritoneal cavity. Biochem Biophys Res Commun 361 (2007) 533-536
74. Gooding T.M., Johnson P.D., Smith M., Kemp A.S., and Robins-Browne R.M. Cytokine profiles of patients infected with Mycobacterium ulcerans and unaffected household contacts. Infect Immun 70 (2002) 5562-5567
75. Prevot G., Bourreau E., Pascalis H., et al. Differential production of systemic and intralesional gamma interferon and interleukin-10 in nodular and ulcerative forms of Buruli disease. Infect Immun 72 (2004) 958-965
76. Westenbrink B.D., Stienstra Y., Huitema M.G., et al. Cytokine responses to stimulation of whole blood from patients with Buruli ulcer disease in Ghana. Clin Diagn Lab Immunol 12 (2005) 125-129
77. Coutanceau E., Decalf J., Martino A., et al. Selective suppression of dendritic cell functions by Mycobacterium ulcerans toxin mycolactone. J Exp Med 204 (2007) 1395-1403
78. Hong H., Stinear T., Porter J., Demangel C., and Leadlay P.F. A novel mycolactone toxin obtained by biosynthetic engineering. Chembiochem 8 (2007) 2043-2047
79. Vilcek J., Klion A., Henriksen-DeStefano D., et al. Defective gamma-interferon production in peripheral blood leukocytes of patients with acute tuberculosis. J Clin Immunol 6 (1986) 146-151
80. Vanham G., Toossi Z., Hirsch C.S., et al. Examining a paradox in the pathogenesis of human pulmonary tuberculosis: immune activation and suppression/anergy. Tuberc Lung Dis 78 (1997) 145-158
81. Jo E.K., Park J.K., and Dockrell H.M. Dynamics of cytokine generation in patients with active pulmonary tuberculosis. Curr Opin Infect Dis 16 (2003) 205-210
82. Sarfo F.S., Phillips R.O., Ampadu E., et al. Dynamics of the cytokine response to Mycobacterium ulcerans during antibiotic treatment for human M ulcerans disease (Buruli ulcer). Clin Vaccine Immunol 16 (2009) 61-65
83. Kiszewski A.E., Becerril E., Aguilar L.D., et al. The local immune response in ulcerative lesions of Buruli disease. Clin Exp Immunol 143 (2006) 445-451
84. Schipper H.S., Rutgers B., Huitema M.G., et al. Systemic and local interferon-gamma production following Mycobacterium ulcerans infection. Clin Exp Immunol 150 (2007) 451-459
85. Stanford J.L., Revill W.D., Gunthorpe W.J., and Grange J.M. The production and preliminary investigation of Burulin, a new skin test reagent for Mycobacterium ulcerans infection. J Hyg 74 (1975) 7-16
86. Dobos K.M., Spotts E.A., Marston B.J., Horsburgh Jr. C.R., and King C.H. Serologic response to culture filtrate antigens of Mycobacterium ulcerans during Buruli ulcer disease. Emerg Infect Dis 6 (2000) 158-164
87. Dannenberg Jr. A.M. Delayed-type hypersensitivity and cell-mediated immunity in the pathogenesis of tuberculosis. Immunol Today 12 (1991) 228-233
88. Marston B.J., Diallo M.O., Horsburgh C.R., et al. Emergence of Buruli ulcer disease in the Daloa region of Cote d'Ivoire. Am J Trop Med Hyg 52 (1995) 219-224
89. Saunders B.M., and Cooper A.M. Restraining mycobacteria: role of granulomas in mycobacterial infections. Immunol Cell Biol 78 (2000) 334-341
90. Revill W.D., Morrow R.H., Pike M.C., and Ateng J. A controlled trial of the treatment of Mycobacterium ulcerans infection with clofazimine. Lancet 2 (1973) 873-877
91. Stienstra Y., van der Graaf W.T., te Meerman G.J., The T.H., de Leij L.F., and van der Werf T.S. Susceptibility to development of Mycobacterium ulcerans disease: review of possible risk factors. Trop Med Int Health 6 (2001) 554-562
92. Portaels F., Aguiar J., Debacker M., et al. Prophylactic effect of Mycobacterium bovis BCG vaccination against osteomyelitis in children with Mycobacterium ulcerans disease (Buruli ulcer). Clin Diagn Lab Immunol 9 (2002) 1389-1391
93. Portaels F., Aguiar J., Debacker M., et al. Mycobacterium bovis BCG vaccination as prophylaxis against Mycobacterium ulcerans osteomyelitis in Buruli ulcer disease. Infect Immun 72 (2004) 62-65
94. Tanghe A., Content J., Van Vooren J.P., Portaels F., and Huygen K. Protective efficacy of a DNA vaccine encoding antigen 85A from Mycobacterium bovis BCG against Buruli ulcer. Infect Immun 69 (2001) 5403-5411
95. Coutanceau E., Legras P., Marsollier L., Reysset G., Cole S.T., and Demangel C. Immunogenicity of Mycobacterium ulcerans Hsp65 and protective efficacy of a Mycobacterium leprae Hsp65-based DNA vaccine against Buruli ulcer. Microbes Infect 8 (2006) 2075-2081
96. Tanghe A., Dangy J.P., Pluschke G., and 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 (2008) e199
97. Montessori V., Phillips P., Montaner J., et al. Species distribution in human immunodeficiency virus-related mycobacterial infections: implications for selection of initial treatment. Clin Infect Dis 22 (1996) 989-992
98. Johnson R.C., Ifebe D., Hans-Moevi A., et al. Disseminated Mycobacterium ulcerans disease in an HIV-positive patient: a case study. AIDS 16 (2002) 1704-1705
99. Johnson R.C., Nackers F., Glynn J.R., et al. Association of HIV infection and Mycobacterium ulcerans disease in Benin. AIDS 22 (2008) 901-903
100. Toll A., Gallardo F., Ferran M., et al. Aggressive multifocal Buruli ulcer with associated osteomyelitis in an HIV-positive patient. Clin Exp Dermatol 30 (2005) 649-651
101. Phillips R., Horsfield C., Kuijper S., 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 (2006) 253-257
102. Kaufmann S. Immunity to intracellular bacteria. In: Paul W.E. (Ed). Fundamental immunology (1999), Lippincott-Raven, New York, NY 1335-1371
103. Bogdan C. Mechanisms and consequences of persistence of intracellular pathogens: leishmaniasis as an example. Cell Microbiol 10 (2008) 1221-1234
104. Kaufmann S.H. Immunity to intracellular bacteria. Ann Rev Immunol 11 (1993) 129-163
105. Ramakrishnan L., and Falkow S. Mycobacterium marinum persists in cultured mammalian cells in a temperature-restricted fashion. Infect Immun 62 (1994) 3222-3229
106. Mehta P.K., King C.H., White E.H., Murtagh Jr. J.J., and Quinn F.D. Comparison of in vitro models for the study of Mycobacterium tuberculosis invasion and intracellular replication. Infect Immun 64 (1996) 2673-2679
107. Russell D.G. Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2 (2001) 569-577
108. Rengarajan J., Bloom B.R., and Rubin E.J. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci USA 102 (2005) 8327-8332
109. El-Etr S.H., Subbian S., Cirillo S.L., and Cirillo J.D. Identification of two Mycobacterium marinum loci that affect interactions with macrophages. Infect Immun 72 (2004) 6902-6913
110. Cooper A.M., and Flynn J.L. The protective immune response to Mycobacterium tuberculosis. Curr Opin Immunol 7 (1995) 512-516
111. Flynn J.L., and Chan J. Immunology of tuberculosis. Ann Rev Immunol 19 (2001) 93-129
112. Lewis K.N., Liao R., Guinn K.M., et al. Deletion of RD1 from Mycobacterium tuberculosis mimics Bacille Calmette-Guérin attenuation. J Infect Dis 187 (2003) 117-123
113. Gao L.Y., Guo S., McLaughlin B., Morisaki H., Engel J.N., and Brown E.J. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53 (2004) 1677-1693
114. Keane J., Remold H.G., and Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 164 (2000) 2016-2020
115. Schnappinger D., Ehrt S., Voskuil M.I., et al. Transcriptional Adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198 (2003) 693-704
116. Ramakrishnan L., Federspiel N.A., and Falkow S. Granuloma-specific expression of mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288 (2000) 1436-1439
117. Rohde K., Yates R.M., Purdy G.E., and Russell D.G. Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219 (2007) 37-54
118. Yamagami A., and Chang Y.T. Growth of Mycobacterium lepraemurium in cultures of macrophages obtained from various sources. Infect Immun 17 (1977) 531-534
119. Leiriao P., Rodrigues C.D., Albuquerque S.S., and Mota M.M. Survival of protozoan intracellular parasites in host cells. EMBO reports 5 (2004) 1142-1147
120. Hsu T., Hingley-Wilson S.M., Chen B., et al. The primary mechanism of attenuation of bacillus Calmette-Guérin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci USA 100 (2003) 12420-12425
121. Chopra P., Singh A., Koul A., et al. Cytotoxic activity of nucleoside diphosphate kinase secreted from Mycobacterium tuberculosis. Eur J Biochem 270 (2003) 625-634
122. Fischer L.J., Quinn F.D., White E.H., and King C.H. Intracellular growth and cytotoxicity of Mycobacterium haemophilum in a human epithelial cell line (Hec-1-B). Infect Immun 64 (1996) 269-276
123. Richter-Dahlfors A., Buchan A.M., and Finlay B.B. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186 (1997) 569-580
124. Navarre W.W., and Zychlinsky A. Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell Microbiol 2 (2000) 265-273
125. Hybiske K., and Stephens R.S. Exit strategies of intracellular pathogens. Nature Rev 6 (2008) 99-110
126. McDonough K.A., and Kress Y. Cytotoxicity for lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis. Infect Immun 63 (1995) 4802-4811
127. Alli O.A., Gao L.Y., Pedersen L.L., et al. Temporal pore formation-mediated egress from macrophages and alveolar epithelial cells by Legionella pneumophila. Infect Immun 68 (2000) 6431-6440
128. Al-Khodor S., Price C.T., Habyarimana F., Kalia A., and Kwaik Y.A. A Dot/Icm-translocated ankyrin protein of Legionella pneumophila is required for intracellular proliferation within human macrophages and protozoa. Mol Microbiol 70 (2008) 908-923
129. Banaiee N., Jacobs Jr. W.R., and Ernst J.D. Regulation of Mycobacterium tuberculosis whiB3 in the mouse lung and macrophages. Infect Immun 74 (2006) 6449-6457
130. van Furth R. Current view of the mononuclear phagocyte system. Haematol Blood Transfus 27 (1981) 3-10
131. Serbina N.V., Jia T., Hohl T.M., and Pamer E.G. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26 (2008) 421-452
132. Nahm M.H., Apicella M.A., and Briles D.E. Immunity to extracellular bacteria. In: Paul W.E. (Ed). Fundamental Immunology (1999), Lippincott-Raven, Philadelphia, PA 1373-1386
133. Casadevall A. Evolution of intracellular pathogens. Ann Rev Microbiol 62 (2008) 19-33
134. Casadevall A., and Pirofski L.A. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun 67 (1999) 3703-3713
135. Grosset J. Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrob Agents Chemother 47 (2003) 833-836
136. Casadevall A., and Pirofski L.A. A reappraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens. Adv Immunol 91 (2006) 1-44
137. Glatman-Freedman A. The role of antibody-mediated immunity in defense against Mycobacterium tuberculosis: advances toward a novel vaccine strategy. Tuberculosis (Edinb) 86 (2006) 191-197
138. Okenu D.M., Ofielu L.O., Easley K.A., et al. Immunoglobulin M antibody responses to Mycobacterium ulcerans allow discrimination between cases of active Buruli ulcer disease and matched family controls in areas where the disease is endemic. Clin Diagn Lab Immunol 11 (2004) 387-391
139. Diaz D., Dobeli H., Yeboah-Manu 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 (2006) 1314-1321