In vitro infection of human cells with Mycobacterium tuberculosis

Tuberculosis

Volumn 93, Issue 2, 2013, Pages 123-129

  Rivero Lezcano, Octavio M ^a,b  

^a HOSPITAL DE LEÓN   (Spain)

^b Instituto de Estudios de Ciencias de La Salud de Castilla y Leon   (Spain)

Author keywords

Design of experiments; Infection protocols; Macrophage; Mycobacterium tuberculosis killing

Indexed keywords

BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; DISEASE MODEL; HUMAN; IN VITRO STUDY; INOCULATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUBERCULOSIS; BIOLOGICAL MODEL; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; PATHOGENICITY; PHAGOCYTE; VIRULENCE;

CYTOKINE;

CYTOKINES; HUMANS; IMMUNITY, INNATE; MODELS, BIOLOGICAL; MYCOBACTERIUM TUBERCULOSIS; PHAGOCYTES; TUBERCULOSIS; VIRULENCE;

EID: 84875214390     PISSN: 14729792     EISSN: 1873281X     Source Type: Journal    
DOI: 10.1016/j.tube.2012.09.002     Document Type: Review

References (92)

1. F.L. Soper Problems to be solved if the eradication of tuberculosis is to be realized Am J Public Health Nations Health 52 1962 734 748
2. J.F. Murray A century of tuberculosis Am J Respir Crit Care Med 169 2004 1181 1186
3. K. Lönnroth, K.G. Castro, J.M. Chakaya, L.S. Chauhan, K. Floyd, P. Glaziou, and M.C. Raviglione Tuberculosis control and elimination 2010-50: cure, care, and social development Lancet 375 2010 1814 1829
4. A. Sakula BCG: who were Calmette and Guérin? Thorax 38 1983 806 812
5. J. Morrison, M. Pai, and P.C. Hopewell Tuberculosis and latent tuberculosis infection in close contacts of people with pulmonary tuberculosis in low-income and middle-income countries: a systematic review and meta-analysis Lancet Infect Dis 8 2008 359 368
6. J.L. Casanova, and L. Abel Genetic dissection of immunity to mycobacteria: the human model Annu Rev Immunol 20 2002 581 620
7. J. Bustamante, A.A. Arias, G. Vogt, C. Picard, L.B. Galicia, C. Prando, A.V. Grant, C.C. Marchal, M. Hubeau, A. Chapgier, L. de Beaucoudrey, A. Puel, J. Feinberg, E. Valinetz, L. Jannière, C. Besse, A. Boland, J.M. Brisseau, S. Blanche, O. Lortholary, C. Fieschi, J.F. Emile, S. Boisson-Dupuis, S. Al-Muhsen, B. Woda, P.E. Newburger, A. Condino-Neto, M.C. Dinauer, L. Abel, and J.L. Casanova Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease Nat Immunol 12 2011 213 221
8. J.D. MacMicking, R.J. North, R. LaCourse, J.S. Mudgett, S.K. Shah, and C.F. Nathan Identification of nitric oxide synthase as a protective locus against tuberculosis Proc Natl Acad Sci USA 94 1997 5243 5248
9. E.D. Chan, J. Chan, and N.W. Schluger What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge Am J Respir Cell Mol Biol 25 2001 606 612
10. P.T. Liu, and R.L. Modlin Human macrophage host defense against Mycobacterium tuberculosis Curr Opin Immunol 20 2008 371 376
11. A.W. Segal How neutrophils kill microbes Annu Rev Immunol 23 2005 197 223
12. P.T. Liu, S. Stenger, H. Li, L. Wenzel, B.H. Tan, S.R. Krutzik, M.T. Ochoa, J. Schauber, K. Wu, C. Meinken, D.L. Kamen, M. Wagner, R. Bals, A. Steinmeyer, U. Zügel, R.L. Gallo, D. Eisenberg, M. Hewison, B.W. Hollis, J.S. Adams, B.R. Bloom, and R.L. Modlin Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response Science 311 2006 1770 1773
13. K. Rohde, R.M. Yates, G.E. Purdy, and D.G. Russell Mycobacterium tuberculosis and the environment within the phagosome Immunol Rev 219 2007 37 54
14. J. Lee, M. Hartman, and H. Kornfeld Macrophage apoptosis in tuberculosis Yonsei Med J 50 2009 1 11
15. V. Deretic Autophagy in immunity and cell-autonomous defense against intracellular microbes Immunol Rev 240 2011 92 104
16. M. Doherty, R.S. Wallis, and A. Zumla Biomarkers for tuberculosis disease status and diagnosis Curr Opin Pulm Med 15 2009 181 187
17. G.S. Douvas, D.L. Looker, A.E. Vatter, and A.J. Crowle Gamma interferon activates human macrophages to become tumoricidal and leishmanicidal but enhances replication of macrophage-associated mycobacteria Infect Immun 50 1985 1 8
18. U.D. Gupta, and V.M. Katoch Animal models of tuberculosis Tuberculosis (Edinb) 85 2005 277 293
19. G.A. Rook, J. Steele, M. Ainsworth, and B.R. Champion Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages Immunology 59 1986 333 338
20. J.L. Flynn, and J. Chan Immunology of tuberculosis Annu Rev Immunol 19 2001 93 129
21. D.E. Griffith, T. Aksamit, B.A. Brown-Elliott, A. Catanzaro, C. Daley, F. Gordin, S.M. Holland, R. Horsburgh, G. Huitt, M.F. Iademarco, M. Iseman, K. Olivier, S. Ruoss, C.F. Fordham von Reyn, R.J. Wallace Jr., and K. Winthrop An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases Am J Respir Crit Care Med 175 2007 367 416
22. M. Coscolla, and S. Gagneux Does M. tuberculosis genomic diversity explain disease diversity? Drug Discov Today Dis Mech 7 2010 e43 e59
23. R. Brosch, S.V. Gordon, M. Marmiesse, P. Brodin, C. Buchrieser, K. Eiglmeier, T. Garnier, C. Gutierrez, G. Hewinson, K. Kremer, L.M. Parsons, A.S. Pym, S. Samper, D. van Soolingen, and S.T. Cole A new evolutionary scenario for the Mycobacterium tuberculosis complex Proc Natl Acad Sci USA 99 2002 3684 3689
24. R. Hershberg, M. Lipatov, P.M. Small, H. Sheffer, S. Niemann, S. Homolka, J.C. Roach, K. Kremer, D.A. Petrov, M.W. Feldman, and S. Gagneux High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography PLoS Biol 6 2008 e311
25. I. Comas, and S. Gagneux A role for systems epidemiology in tuberculosis research Trends Microbiol 19 2011 492 500
26. K.A. McDonough, Y. Kress, and B.R. Bloom Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages Infect Immun 61 1993 2763 2773
27. R.F. Silver, Q. Li, and J.J. Ellner Expression of virulence of Mycobacterium tuberculosis within human monocytes: virulence correlates with intracellular growth and induction of tumor necrosis factor alpha but not with evasion of lymphocyte-dependent monocyte effector functions Infect Immun 66 1998 1190 1199
28. 2 killing in human monocytes in vitro Infect Immun 65 1997 4850 4857
29. M. Zhang, J. Gong, Y. Lin, and P.F. Barnes Growth of virulent and avirulent Mycobacterium tuberculosis strains in human macrophages Infect Immun 66 1998 794 799
30. K.C. Wong, W.M. Leong, H.K. Law, K.F. Ip, J.T. Lam, K.Y. Yuen, P.L. Ho, W.S. Tse, X.H. Weng, W.H. Zhang, S. Chen, and W.C. Yam Molecular characterization of clinical isolates of Mycobacterium tuberculosis and their association with phenotypic virulence in human macrophages Clin Vaccine Immunol 14 2007 1279 1284
31. C. Manca, L. Tsenova, C.E. Barry III, A. Bergtold, S. Freeman, P.A. Haslett, J.M. Musser, V.H. Freedman, and G. Kaplan 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 1999 6740 6746
32. Q. Li, C.C. Whalen, J.M. Albert, R. Larkin, L. Zukowski, M.D. Cave, and R.F. Silver Differences in rate and variability of intracellular growth of a panel of Mycobacterium tuberculosis clinical isolates within a human monocyte model Infect Immun 70 2002 6489 6493
33. T.R. Ioerger, Y. Feng, K. Ganesula, X. Chen, K.M. Dobos, S. Fortune, W.R. Jacobs Jr., V. Mizrahi, T. Parish, E. Rubin, C. Sassetti, and J.C. Sacchettini Variation among genome sequences of H37Rv strains of Mycobacterium tuberculosis from multiple laboratories J Bacteriol 192 2010 3645 3653
34. M. Zhang, J. Gong, Z. Yang, B. Samten, M.D. Cave, and P.F. Barnes Enhanced capacity of a widespread strain of Mycobacterium tuberculosis to grow in human macrophages J Infect Dis 179 1999 1213 1217
35. D. Garcia de Viedma, G. Lorenzo, P.-J. Cardona, N.A. Rodriguez, S. Gordillo, M.J. Serrano, and E. Bouza Association between the infectivity of Mycobacterium tuberculosis strains and their efficiency for extrarespiratory infection J Infect Dis 192 2005 2059 2065
36. S.A. Theus, M.D. Cave, K. Eisenach, J. Walrath, H. Lee, W. Mackay, C. Whalen, and R.F. Silver Differences in the growth of paired Ugandan isolates of Mycobacterium tuberculosis within human mononuclear phagocytes correlate with epidemiological evidence of strain virulence Infect Immun 74 2006 6865 6876
37. E.G. Hoal-van Helden, D. Hon, L.-A. Lewis, N. Beyers, and P.D. van Helden Mycobacterial growth in human macrophages: variation according to donor, inoculum and bacterial strain Cell Biol Int 25 2001 71 81
38. G.B. Mackaness The growth of tubercle bacilli in monocytes from normal and vaccinated rabbits Am Rev Tuberc 69 1954 495 504
39. E. Suter The multiplication of tubercle bacilli within normal phagocytes in tissue culture J Exp Med 96 1952 137 150
40. R.J. Patterson, and G.P. Youmans Multiplication of Mycobacterium tuberculosis within normal and "immune" mouse macrophages cultivated with and without streptomycin Infect Immun 1 1970 30 40
41. D.J. Drutz, and M.J. Cline Incorporation of tritiated thymidine by leprosy bacilli in cultures of human lepromatous macrophages J Infect Dis 125 1972 416 419
42. A.J. Crowle, and M. May Preliminary demonstration of human tuberculoimmunity in vitro Infect Immun 31 1981 453 464
43. J. Steele, K.C. Flint, A.L. Pozniak, B. Hudspith, M.M. Johnson, and G.A. Rook Inhibition of virulent Mycobacterium tuberculosis by murine peritoneal macrophages and human alveolar lavage cells: the effects of lymphokines and recombinant gamma interferon Tubercle 67 1986 289 294
44. H.J. Henderson, A.M. Dannenberg Jr., and M.B. Lurie Phagocytosis of tubercle bacilli by rabbit pulmonary alveolar macrophages and its relation to native resistance to tuberculosis J Immunol 91 1963 553 556
45. P.K. Peterson, G. Gekker, S. Hu, W.S. Sheng, W.R. Anderson, R.J. Ulevitch, P.S. Tobias, K.V. Gustafson, T.W. Molitor, and C.C. Chao CD14 receptor-mediated uptake of nonopsonized Mycobacterium tuberculosis by human microglia Infect Immun 63 1995 1598 1602
46. A.E. Brown, T.J. Holzer, and B.R. Andersen Capacity of human neutrophils to kill Mycobacterium tuberculosis J Infect Dis 156 1987 985 989
47. R.S. Wallis, M. Palaci, S. Vinhas, A.G. Hise, F.C. Ribeiro, K. Landen, S.-H. Cheon, H.-Y. Song, M. Phillips, R. Dietze, and J.J. Ellner A whole blood bactericidal assay for tuberculosis J Infect Dis 183 2001 1300 1303
48. C.C. Shepard Growth characteristics of tubercle bacilli and certain other mycobacteria in HeLa cells J Exp Med 105 1957 39 48
49. R.W. Stokes, and D. Doxsee The receptor-mediated uptake, survival, replication, and drug sensitivity of Mycobacterium tuberculosis within the macrophage-like cell line THP-1: a comparison with human monocyte-derived macrophages Cell Immunol 197 1999 1 9
50. 3 induces nitric oxide synthase and suppresses growth of Mycobacterium tuberculosis in a human macrophage-like cell line Infect Immun 66 1998 5314 5321
51. J. Wei, J.L. Dahl, J.W. Moulder, E.A. Roberts, P. O'Gaora, D.B. Young, and R.L. Friedman Identification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages J Bacteriol 182 2000 377 384
52. L.E. Bermudez, and J. Goodman Mycobacterium tuberculosis invades and replicates within type II alveolar cells Infect Immun 64 1996 1400 1406
53. R.J. Dubos, and B.D. Davis Factors affecting the growth of tubercle bacilli in liquid media J Exp Med 83 1946 409 423
54. G.P. Youmans Cultivation of mycobacteria, the morphology and metabolism of mycobacteria G.P. Youmans, Tuberculosis 1979 WB Saunders Company Philadelphia 25 35
55. O. Neyrolles, and C. Guilhot Recent advances in deciphering the contribution of Mycobacterium tuberculosis lipids to pathogenesis Tuberculosis (Edinb) 91 2011 187 195
56. A. Boyum Separation of leukocytes from blood and bone marrow. Introduction Scand J Clin Lab Invest Suppl 97 1968 7
57. A. Böyum Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g Scand J Clin Lab Invest Suppl 97 1968 77 89
58. A. Nakagawara, and C.F. Nathan A simple method for counting adherent cells: application to cultured human monocytes, macrophages and multinucleated giant cells J Immunol Methods 56 1983 261 268
59. R.F. Silver, Q. Li, W.H. Boom, and J.J. Ellner Lymphocyte-dependent inhibition of growth of virulent Mycobacterium tuberculosis H37Rv within human monocytes: requirement for CD4+ T cells in purified protein derivative-positive, but not in purified protein derivative-negative subjects J Immunol 160 1998 2408 2417
60. L. Danelishvili, J. McGarvey, Y.J. Li, and L.E. Bermudez Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells Cell Microbiol 5 2003 649 660
61. J. Lee, H.G. Remold, M.H. Ieong, and H. Kornfeld Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway J Immunol 176 2006 4267 4274
62. S. Lamhamedi-Cherradi, C. de Chastellier, and J.L. Casanova Growth of Mycobacterium bovis, Bacille Calmette-Guérin, within human monocytes-macrophages cultured in serum-free medium J Immunol Methods 225 1999 75 86
63. J.D. Ernst Macrophage receptors for Mycobacterium tuberculosis Infect Immun 66 1998 1277 1281
64. Biroum-Noerjasin Listericidal activity of non-stimulated and stimulated human macrophages in vitro Clin Exp Immunol 28 1977 138 145
65. N. Fazal, R. Bartlett, D.A. Lammas, and D.S. Kumararatne A comparison of the different methods available for determining BCG-macrophage interactions in vitro, including a new method of colony counting in broth FEMS Microbiol Immunol 5 1992 355 362
66. S.J. Skerrett, and T.R. Martin Alveolar macrophage activation in experimental legionellosis J Immunol 147 1991 337 345
67. 3H-thymidine into deoxyribonucleic acid by Mycobacterium leprae in cultivated blood monocytes Infect Immun 9 1974 187 191
68. M. Bonay, F. Bouchonnet, V. Pelicic, B. Lagier, M. Grandsaigne, D. Lecossier, A. Grodet, M. Vokurka, B. Gicquel, and A.J. Hance Effect of stimulation of human macrophages on intracellular survival of Mycobacterium bovis Bacillus Calmette-Guerin. Evaluation with a mycobacterial reporter strain Am J Respir Crit Care Med 159 1999 1629 1637
69. A.R. Martineau, K.A. Wilkinson, S.M. Newton, R.A. Floto, A.W. Norman, K. Skolimowska, R.N. Davidson, O.E. Sørensen, B. Kampmann, C.J. Griffiths, and R.J. Wilkinson IFN-γ- and TNF-independent vitamin D-inducible human suppression of mycobacteria: the role of cathelicidin LL-37 J Immunol 178 2007 7190 7198
70. 3 metabolites and tumour necrosis factor in the pathogenesis of tuberculosis Immunology 62 1987 229 234
71. S.K. Garg, E. Volpe, G. Palmieri, M. Mattei, D. Galati, A. Martino, M.S. Piccioni, E. Valente, E. Bonanno, P. De Vito, P.M. Baldini, L.G. Spagnoli, V. Colizzi, and M. Fraziano Sphingosine 1-phosphate induces antimicrobial activity both in vitro and in vivo J Infect Dis 189 2004 2129 2138
72. D.J. Kusner, and J. Adams ATP-induced killing of virulent Mycobacterium tuberculosis within human macrophages requires phospholipase D J Immunol 164 2000 379 388
73. T.H. Ottenhoff, F.A. Verreck, M.A. Hoeve, and E. van de Vosse Control of human host immunity to mycobacteria Tuberculosis (Edinb) 85 2005 53 64
74. M. Denis Killing of Mycobacterium tuberculosis within human monocytes: activation by cytokines and calcitriol Clin Exp Immunol 84 1991 200 206
75. G.S. Jones, H.J. Amirault, and B.R. Andersen Killing of Mycobacterium tuberculosis by neutrophils: a nonoxidative process J Infect Dis 162 1990 700 704
76. J. Warwick-Davies, J. Dhillon, L. O'Brien, P.W. Andrew, and D.B. Lowrie Apparent killing of Mycobacterium tuberculosis by cytokine-activated human monocytes can be an artefact of a cytotoxic effect on the monocytes Clin Exp Immunol 96 1994 214 217
77. M. Denis Human neutrophils, activated with cytokines or not, do not kill virulent Mycobacterium tuberculosis J Infect Dis 163 1991 919 920
78. D. Reyes-Ruvalcaba, C. González-Cortés, and O.M. Rivero-Lezcano Human phagocytes lack the ability to kill Mycobacterium gordonae, a non-pathogenic mycobacteria Immunol Lett 116 2008 72 78
79. A.K. Robertson, and P.W. Andrew Interferon gamma fails to activate human monocyte-derived macrophages to kill or inhibit the replication of a non-pathogenic mycobacterial species Microb Pathog 11 1991 283 288
80. G. Vogt, and C. Nathan In vitro differentiation of human macrophages with enhanced antimycobacterial activity J Clin Invest 121 2011 3889 3901
81. R. Reljic, E. Stylianou, S. Balu, and J.K. Ma Cytokine interactions that determine the outcome of Mycobacterial infection of macrophages Cytokine 51 2010 42 46
82. L. Jordao, C.K. Bleck, L. Mayorga, G. Griffiths, and E. Anes On the killing of mycobacteria by macrophages Cell Microbiol 10 2008 529 548
83. S. Thoma-Uszynski, S. Stenger, O. Takeuchi, M.T. Ochoa, M. Engele, P.A. Sieling, P.F. Barnes, M. Röllinghoff, P.L. Bölcskei, M. Wagner, S. Akira, M.V. Norgard, J.T. Belisle, P.J. Godowski, B.R. Bloom, and R.L. Modlin Induction of direct antimicrobial activity through mammalian toll-like receptors Science 291 2001 1544 1547
84. + transport enhance intracellular killing of M. tuberculosis by non-killing macrophages In Vivo 22 2008 69 75
85. K.O. Kisich, M. Higgins, G. Diamond, and L. Heifets Tumor necrosis factor alpha stimulates killing of Mycobacterium tuberculosis by human neutrophils Infect Immun 70 2002 4591 4599
86. + T cell and natural killer cell-dependent killing of Mycobacterium tuberculosis by human monocytes Am J Respir Crit Care Med 158 1998 395 403
87. M.G. Bonecini-Almeida, S. Chitale, I. Boutsikakis, J. Geng, H. Doo, S. He, and J.L. Ho Induction of in vitro human macrophage anti-Mycobacterium tuberculosis activity: requirement for IFN-γ and primed lymphocytes J Immunol 160 1998 4490 4499
88. K.A. Birkness, M. Deslauriers, J.H. Bartlett, E.H. White, C.H. King, and F.D. Quinn An in vitro tissue culture bilayer model to examine early events in Mycobacterium tuberculosis infection Infect Immun 67 1999 653 658
89. L.E. Bermudez, F.J. Sangari, P. Kolonoski, M. Petrofsky, and J. Goodman The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model of the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells Infect Immun 70 2002 140 146
90. R.S. Wallis, S. Vinhas, and E. Janulionis Strain specificity of antimycobacterial immunity in whole blood culture after cure of tuberculosis Tuberculosis (Edinb) 89 2009 221 224
91. D.C. Montgomery Design and analysis of experiments 5th ed. 2001 John Wiley & Sons New York
92. J.M. Guerra-Laso, S. González-Garcia, C. González- Cortés, C. Diez-Tascón, R. López-Medrano, and O.M. Rivero-Lezcano Macrophages from elders are more permissive to intracellular multiplication of Mycobacterium tuberculosis Age (Dordr) 2012 10.1007/s11357-012-9451-5 [Epub ahead of print]