Macrophages and tuberculosis

Current Opinion in Hematology

Volumn 5, Issue 1, 1998, Pages 72-78

  Fenton, Matthew J ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOST CELL; HUMAN; IMMUNE RESPONSE; MACROPHAGE; MONONUCLEAR PHAGOCYTE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUBERCULOSIS;

EID: 0031911839     PISSN: 10656251     EISSN: None     Source Type: Journal    
DOI: 10.1097/00062752-199801000-00012     Document Type: Review

References (68)

1. Schlesinger LS: Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis Is mediated by mannose receptors In addition to complement receptors, J Immunol 1993, 150:2920-2930.
2. Schlesinger LS, Kaufman TM, lyer S, Hull SR, Marchiando LK: Differences In mannose receptor-mediated uptake of lipoarabinomnnan from virulent and attenuated strains of Mycobacterium tuberculosis by human macrophages. J Immunol 1996, 157:4568-4575.
3. Da Silva RP, Hall BF, Joiner KA, Sacks DL: CR1, the C3b receptor, mediates binding of Infective Leischmanla major metacyclic promastlgotes to human macrophages. J Immunol 1989, 143:617-622.
4. Ishibashi Y, Arai T: Roles of the complement receptor type 1 (CR1) and type 3 (CR3) on phagocytosis and subsequent phagosome-lysosome fusion in Salmonella-Infected urine macrophages. FEMS Microbiol Immunol 1990, 2:89-96.
5. Drevets DA, Leenen PJ, Campbell PA: Complement receptor type 3 (CD11b/CD1B) involvement is essential for killing of Listeria monocytogenes by mouse macrophages. J Immunol 1993, 151:5431-5439.
6. Drevets DA, Sawyer RT, Potter TA, Campbell PA: Listeria monocytogenes infects human endothelial cells by two distinct mechanisms. Infect Immunol 1995, 63:4268-4276.
7. Ezekowitz RA, Sastry K, Bailly P, Warner A: Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeast in Cos-1 cells. J Exp Med 1990, 172:1785-1794.
8. Fallman D, Andersson R, Andersson T: Signalling properties of CR3 (CD11b/CD18) and CR1 (CD35) in relation to phagocytosis of complement-opsonized particles. J Immunol 1993, 151:330-338.
9. Ingalls RR, Golenbock DT: CD11c/CD18, a transmembrane signaling receptor for lipopolysaccharide. J Exp Med 1995, 181:1473-1479.
10. Zimmerli S, Edwards S, Ernst JD: Selective receptor blockade during phagocytosis does not alter the survlval and growth of Mycobacterium tuberculosis in human macrophages. Am J Respir Cell Mol Biol 1996, 15:760-770. These experiments tested the hypothesis that Mtb evades killing by entering naive macrophages through receptors that are unable to activate cellular microbicidal activities. Complement receptor types 1, 3, and 4 were blocked with monoclonal antibodies, and MMRs were blocked with a competitive ligand. Survival and replication of Mtb bacilli were evaluated after the bacteria were phagocytosed in the presence of blocking agents. The intracellular survival and replication of mycobacteria were equivalent, regardless of the receptor(s) used for binding and phagocytosis. Thus, the mechanisms whereby Mtb evades killing by human macrophages are independent of the receptor-mediated route of entry and operate at one or more steps common to all entry pathways. Class A scavenger receptors were also identified as novel and quantitatively important mediators of Mtb-macrophage interactions.
11. Schlesinger LS, Bellinger-Kawahara CG, Payne NR, Horwitz MA: Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 1990, 144:2771-2780.
12. Downing JF, Pasula R, Wright JR, Twigg HL, Martin WJ: Surfactant protein A promotes attachment of Mycobacterium tuberculosis to alveolar macrophages during infection with human immunodeficiency virus. Proc Natl Acad Sci U S A 1995,92:4848-4852.
13. Gaynor CD, McCormack FX, Voelker DR, McGowan SE, Schlesinger LS: Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J Immunol 1995, 155:5343-5351.
14. Xu S, Cooper A, Sturgill-Koszycki S, van Heyningen T, Chatterjee D, Orme I, Allen P, Russell DG: Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J Immunol 1993, 153:2568-2578.
15. Clemens DL, Horwitz MA: Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is Inhibited. J Exp Med 1995, 181:257-270.
16. Clemens DL, Horwitz MA: The Mycobacterium tuberculosis phagosome Interacts with early endosomes and is accessible to exogenously-administered transferrin. J Exp Med 1996, 184:1349-1355.
17. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, et al.: Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPas. Science 1994, 263:678-681.
18. Pancholi P, Mirza A, Bhardwaj N, Steinman RM: Sequestration from Immune CD4+ T cells of mycobacteria growing in human macrophages. Science 1993, 260:984-986.
19. McDonough KA, Kress Y, Bloom BR: Pathogenesis of tuberculosis: Interaction of Mycobacterium tuberculosis with macrophages. Infect Immunol 1993, 61:2763-2773.
20. Moreira AL, Wang J, Tsenova-Berkova L, Hellmann W, Freedman VH, Kaplan G: Sequestration of Mycobacterium tuberculosis in tight vacuoles in vivo in lung macrophages of mice Infected by the respiratory route. Infect Immunol 1997, 65:305-308. Following aerosol infection of mice with Mtb, single mycobacteria or pairs of bacilli were observed within individual phagocytic vacuoles. The virulent organism was not observed free in the cytoplasm of the parasitized cells or in the extracellular space of the lung granulomata. This study indicates that in vivo, virulent mycobacteria survive and probably replicate within vacuoles in the infected phagocyte within the lung.
21. Chan J, Xing Y, Magliozzo RS, Bloom BR: Killing of virulent Mycobacterium tuberculosis by reactive nitrogen Intermediates produced by activated murlne macrophages. J Exp Med 1992, 175:1111-1122.
22. Nathan C, Xie Q-W: Nitrix oxide synthases: roles, tolls, and controls. Cell 1994, 78:915-918.
23. Chan J, Tanaka K, Carroll D, Flynn J, Bloom B: Effects of nitric oxide synthase Inhibitors on murine Infection with Mycobacterium tuberculosis. Infect Immunol 1995, 63:736-740.
24. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR: An essential role for Interferon gamma in resistance to Mycobacterium tuberculosis Infection. J Exp Med 1993, 178:2249-2254.
25. Jouanguy E, Altare F, Lamhamedi S, et al.: Interferon-gamma-recaptor deficiency in an Infant with fatal bacille Calmette-Guerin infection. M Engl J Med 1996, 335:1956-1961.
26. Newport MJ, Huxley CM, Huston S, Hawrylowicz CM, Oostra BA, Williamson R, Levin M: A mutation In the Interferon-gamma-receptor gene and susceptibility to mycobacterial infection. N Engl J Med 1996, 335:1941-1949.
27. Denis M: Human monocytes/macrophages: NO or no NO. J Leuk Biol 1994, 55:682-684.
28. Nicholson S, Bonecini-Almeida MDG, Lapa E Silva JR, et al.: inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med 1996, 183:2293-2302.
29. Zhao B, Collins MT, Czuprynski CJ: Effects of gamma Interferon and nitric oxide on the interaction of Mycobacterium avium subsp. paratuberculosis with bovine monocytes. Infect Immun 1997, 65:1761-1766. The effects of bovine IFN-γ and NO on the interaction of M. avium (subsp. paratuberculosis) with bovine monocytes were examined. Monocytes pretreated with IFN-γ exhibited slightly increased phagocytosis of the mycobacteria and modest inhibition of bacillary growth. The number of viable intracellular bacilli decreased earlier in IFN-γ-pretreated monocytes than in control cells. Inhibition of NO production did not alter the pattern of intracellular survival of mycobacteria in IFN-γ-treated monocytes. Although chemically generated NO killed the bacteria in a cell-free system in vitro, the amount of NO required was far greater than that released from infected monocytes. These data suggest that IFN-γ activates M. avium-infected bovine monocytes to release NO but only modestly increases bactericidal activity of monocytes against this organism. This may be caused, in part, by the fact that the amount of NO produced by IFN-γ-activated monocytes is insufficient to kill intracellular mycobacteria in vitro.
30. Molloy A, Laochumroonvorapong P, Kaplan G: Apoptosis, but not necrosis, of Infected monocytes is coupled with killing of intraceltular bacillus Calmette-Querin. J Exp Med 1994, 180:1499-1509.
31. 3 Induces monocyte apoptosis and reduces viability of Mycobacterium avium-M. intracellulare within cultured human monocytes. Infect Immun 1996, 64:452-459.
32. Keane J, Balcewicz-Sablinska MK, Remold HG, Chupp GL, Meek BB, Fenton MJ, Kornfeld H: Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 1997, 65:298-304. The effect of Mtb infection on the viability of human alveolar macrophages was evaluated. Infection with Mtb H37Ra or H37Rv increased macrophage mortality at 6 days from the control level of 3.8% to 28.7% or 12.6%, respectively. The cytolytic mechanism was determined to be apoptosis by several distinct criteria . Extensive apoptosis within caseating granulomas from lung tissue samples from clinical tuberculosis cases was also observed. The induction of apoptosis in alveolar macrophages by Mtb may play a role in the macrophage-pathogen interaction of tuberculosis in vivo.
33. Paul S, Laochumroonvorapong P, Kaplan G: Comparable growth of vimlent and avirulent Mycobacterium tuberculosis in human macrophages in vitro. J Infect Dis 1996, 174:105-112.
34. Johansson A, Jesaitis AJ, Lundqvist H, Magnusson KE, Sjolin C, Karisson A, Dahlgren C: Different subceltular localization of cytochrome b and dormant NADPH-oxidase in neutrophils and macrophages: effect on the production of reactiva oxygen species during phagocytosis. Cell Immunol 1995, 161:61-71.
35. Kuo HP, Ho TC, Wang Ch, Yu CT, Lin HC: Increased production of hydrogen peroxide and expression of CD11b/CD18 on alveolar macrophages In patients with active pulmonary tuberculosis. Tuber Lung Dis 1996, 77:468-475.
36. Laochumroonvorapong P, Wang J, Liu CC, Ye W, Mofeira AL, Elkon KB, Freedman VH, Kaplan G: Perforin, a cytotoxlc molecule which mediates cell necrosis, Is not required for the early control of mycobacterial Infection in mice. Infect Immunol 1997, 65:127-132.
37. Reach IE, Kaufmann SH: Role of cytokines in tuberculosis. Immunobiology 1993, 189:316-339.
38. Sieling PA, Modlin RL: Cytokine patterns at the site of mycobacterial infection, Immunobiology 1994, 191:378-387.
39. Wallis RS, Ellner JJ: Cytokines and tuberculosis. J Leuk Biol 1994, 55:676-681.
40. Law K, Weiden M, Harkin T, Tchou-Wong K, Chi C, Rom WN: Increased release of Interleukin-1ß, Interieukin-6, and tumor necrosis factor-α by bronchoalveolar cells lavaged from Involved sites in pulmonary tuberculosis. Am J Respir Crit Care Med 1996, 153:799-804.
41. Hemandez-Pando R, Orozco H, Arriaga K, Sampieri A, Larriva-Sahd J, Madrid-Marina V: Analysis of the local kinetics and localization of interleukin-1α, tumor necrosis factor-α and transforming growth factor-α, during the course of experimental pulmonary tuberculosis. Immunology 1997, 90:607-617. A mouse model of tuberculosis induced by the intratracheal instillation of live Mtb was used to examine the histopathology and kinetics/cellular distribution of selected cytokines. During the initial acute phase of disease, which lasted from 1 to 28 days, high percentages of TNF-α-and IL-lα-containing macrophages were observed principally in the interstium-intralveolar inflammatory infiltrate and in granulomas. An initial peak of TNF-α and IL-1β expression correlated with a decrease in the bacillary count. A second peak was seen at days 14 and 21 to 28, when granulomas appeared. In contrast, few TGF-β-containing cells were observed in comparison with the advanced phase of the disease. A decrease in the TNF-α and IL-1α production in the chronic phase coincided with the highest level of TGF-β expression. The bacillary counts were highest in macrophages that displayed poor and scarce TNF-α and IL-1α immunostaining but still strong immunoreactivity to TGF-β. These data suggest an important role for TGF-β in the advanced phase of pulmonary tuberculosis.
42. Flynn JL, Goldstein MM, Triebold KJ, Sypek J, Wolf S, Bloom BR: IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis Infection. J Immunol 1995, 155:2515-2524.
43. Ladel CH, Szalay G, Riedel D, Kaufmann SH: Interleukin-12 secretion by Mycobacterium tuberculosis-infected macrophages. Infect Immunol 1997, 65:1936-1938.
44. Taha RA, Kotsimbos TC, Song YL, Menzies D, Hamid Q: IFN-γ and IL-12 are Increased in active compared with inactive tuberculosis. Am J Respir Crit Care Med 1997, 155:1135-1139.
45. Hirsch CS, Hussain R, Toossi Z, Dawood G, Shahid F, Ellner JJ: Cross-modulation by transforming growth factor-β In human tuberculosis: suppression of antigen-driven blastogenesis and Interferon-γ production. Proc Natl Acad Sci U S A 1996, 93:3193-3198.
46. Murray PJ, Wang L, Onufryk C, Tepper RI, Young RA: T cell-derived IL-10 antagonizes macrophage function in mycobacterial Infection. J Immunol 1997, 158:315-321.
47. Shiratsuchi H, Hamilton B, Toossi Z, Ellner JJ: Evidence against a role for interleukin-10 in the regulation of growth of Mycobacterium avium in human monocytes. J Infect Dis 1996, 173:410-417.
48. Doherty TM, Sher A: Defects In cell-mediated Immunity after chronic, but not Innate, resistance of mice to Mycobacterium avium infection. J Immunol 1997, 158:4822-4831. The effects of targeted gene disruptions on T cell-dependent, macrophage-mediated responses against MAI were studied. Normal mice developed a chronic, asymptomatic infection, with rapid expression of IFN-γ, IL-12, and TNF-α. Bacterial loads in gene knockout, SCID, and wild-type mice were indistinguishable for the first 4 weeks of infection. However, by 8 weeks after infection, SCID mice, as well as animals with a targeted disruption of the IFN-γ gene, showed enhanced bacterial growth compared with wild-type mice. In contrast, knockout mice lacking the genes for both TNF-α receptors or inducible nitric oxide synthese developed comparable bacterial loads to wild-type animals and failed to display the splenomegaly and suppression of mitogen-induced lymphocyte proliferative responses evident in infected wild-type controls. Thus, MAI is clearly distinct from other intracellular pathogens whose initial replication in the host is tightly controlled by Th 1-dependent effector mechanisms. Instead, the major effect of host cell-mediated immunity is to limit bacterial growth during the chronic phase of infection.
49. Miller M, Krangel M: Biology and biochemistry of chemokines: a family of chemotactic and Inflammatory cytokines. Crit Rev Immunol 1992, 12:17-46.
50. Friedland JS, Remick DG, Shattock R, Griffin GE: Secretion of interteukin-8 following phagocytosis of Mycobacterium tuberculosis by human monocyte cell lines. Eur J Immunol 1992, 22:1373-1378.
51. Friedland JS, Shattock RJ, Griffin GE: Phagocytosis of Mycobacterium tuberculosis or particulate stimuli by human monocytic cells induce equivalent monocyte chemotactic protein-1 gene expression. Cytokine 1993, 5:150-156.
52. Rhoades ER, Cooper AM, Orme IM: Chemokine response in mice infected with Mycobacterium tuberculosis. Infect Immunol 1995, 63:3871-3877.
53. Zhang Y, Broser M, Cohen H, Bodkin M, Law K, Reigman J, Rom WN: Enhanced interleukin-8 release and gene expression in macrophages after exposure to Mycobacterium tuberculosis and its components. J Clin Invest 1995, 95:586-592.
54. Kurashima K, Mukaida N, Fujimura M, Yasui M, Nakazumi Y, Matsuda T, Matsushima K: Elevated cytokine levels In bronchoalveolar lavage fluid of tuberculosis patients. Am J Respir Crit Care Med 1997, 155:1474-1477.
55. Adams DH, Hathaway M, Shaw J, Burnett D, Elias E, Strain AJ: Transforming growth factor-β Induces human T lymphocyte migration In vitro. J Immunol 1991, 147:609-612.
56. Dahl KE, Shiratsuchi H, Hamilton BD, Ellner JJ, Toossi Z: Selective induction of transforming growth factor-β in human monocytes by lipoarabinomannan of Mycobacterium tuberculosis. Infect Immunol 1996, 64:399-405.
57. Hirsch CS, Ellner JJ, Blinkhom R, Toossi Z: In vitro restoration of T cell responses in tuberculosis and augmentation of monocyte effector function against Mycobactarium tuberculosis by natural Inhibitors of transforming growth factor-β. Proc Natl Acad Sci U S A 1997, 94:3926-3931. The capacity of naturally occurring inhibitors of TGF-β, decorin, and latencyassociated peptide, to reverse depressed T cell functions and mycobacterial replication in peripheral blood mononuclear cells from patients with pulmonary tuberculosis was examined. T-cell blastogenesis in peripheral blood mononuclear cells of tuberculosis patients that were cocultured with decorin or latencyassociated peptide reached levels comparable with those observed in healthy tuberculin-responsive control subjects. Decorin and latency-associated peptide were as effective as neutralizing antibody to TGF-β in correcting depressed T-cell proliferation. Levels of IFN-γ in cultures of PPD-stimulated peripheral blood mononuclear cells from tuberculosis patients increased in the presence of maximal concentrations of either of the inhibitors of TGF-β. Coculture with optimal concentrations of decorin or latency-associated peptide also reduced mycobacterial growth in monocytes infected in vitro with Mtb, compared with untreated cells.
58. Toossi Z, Gogate P, Shiratsuchi H, Young T, Ellner JJ: Enhanced production of TGF-β by blood monocytes from patients with active tuberculosis and presence of TGF-β In tuberculous granulomatous lung lesions. J Immunol 1995, 154:465-473.
59. Berman JS, Blumenthal RL, Kornfeld H, Cook JA, Cruikshank WW, Vermeulen MW, Chatterjee D, Belisle JT, Fenton MJ: Chemotactic activity of mycobacterial lipoarabinomannans for human blood T lymphocytes in vitro. J Immunol 1996, 156:3828-3835.
60. Bemardo J, Billingslea AM, Blumenthal RL, Seetoo KF, Simons ER, Fenton MJ: Differential responses of human monocytes to mycobaterial lipoarabinomannans: a role for CD14 and the mannose receptor. Infect Immun 1998, 66:28-35.
61. Haregewoin A, Singh B, Gupta RS, Finberg FW: A mycobacterial heat-shock protein-responsive gamma delta T cell clone also responds to the homologous human heat-shock protein: a possible link between infection and autolmmunity. J Infect Dis 1991, 163:156-160.
62. D'Souza CD, Wooper AM, Frank AA, Mazzaccaro RJ, Bloom BR Orme IM: An anti-Inflammatory role for gamma delta T lymphocytes in acquired immunity to Mycobacterium tuberculosis. J Immunol 1997, 158:1217-1221. Modest low-dose inocula delivered by the aerosol route grew identically in wild-type controls and in mutant mice in which the δ gene of the γδ T-cell receptor has been disrupted by homologous recombination. The data presented indicate that γδ T cells do not directly contribute to protection against tuberculosis, or that they do so only when bacterial loads are very high. Instead, the data suggest that γδ T cells influence local cellular traffic, promoting the influx of lymphocytes and monocytes and limiting the access of inflammatory cells that do not contribute to protection but instead cause tissue damage.
63. + T cells. Nature 1994, 372:691-694.
64. Sieling PA, Chatterjee D, Porcelli SA, et al.: CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 1995, 269:227-230.
65. Beckman EM, Melian A, Behar SM, et al.: CD1c restricts responses of mycobacteria-specific T cells. Evidence for antigen presentation by a second member of the human CD1 family. J Immunol 1996, 157:2795-2803.
66. Prigozy TI, Sieling PA, Clemens D, Stewart PL, Behar SM, Porcelli SA, Brenner MB, Modlin RL, Kronenberg M: The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules. Immunity 1997, 6:187-197. The CD1b-mediated presentation pathway for the mycobacterial glycolipid lipoarabinomannan in monocyta-derived antigen-presenting cells was characterized. The MMRc was shown to be responsible for uptake of lipoarabinomannan. Intracellular MMRcs were most abundant in early endosomes, but they also were located in the compartment for MHC class II antigen loading. Internalized lipoarabinomannan was transported to late endosomes, lysosomes, and MHC class II proteins. MMRcs colocalized with CD1b molecules, suggesting that the mannose receptor could deliver lipoarabinomannan to late endosomes for loading onto CD1b. Lipoarabinomannan and CD1b colocalized in organelles that may be sites of glycolipid antigen loading.
67. Tascon RE, Colston MJ, Ragno S, Stavropoulos E, Gregory D, Lowrie DB: Vaccination against tuberculosis by DNA Injection. Nature Med 1996, 2:888-892.
68. + T cells in vitro. Immunology 1996, 87:339-342.