The ΔfbpA mutant derived from Mycobacterium tuberculosis H37Rv has an enhanced susceptibility to intracellular antimicrobial oxidative mechanisms, undergoes limited phagosome maturation and activates macrophages and dendritic cells

Cellular Microbiology

Volumn 10, Issue 6, 2008, Pages 1286-1303

  Katti, Muralidhar K ^a   Dai, Guixiang ^a   Armitige, Lisa Y ^a   Marrero, Carlos Rivera ^b   Daniel, Sundarsingh ^a   Singh, Christopher R ^a   Lindsey, Devin R ^a   Dhandayuthapani, Subramanian ^c   Hunter, Robert L ^a   Jagannath, Chinnaswamy ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; CD1D ANTIGEN; CD63 ANTIGEN; CORD FACTOR; GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; HEMATOPOIETIC CELL KINASE; INDUCIBLE NITRIC OXIDE SYNTHASE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYCOBACTERIUM ANTIGEN; OXIDIZING AGENT; OXIDOREDUCTASE; RAB PROTEIN; RAB11 PROTEIN; RAB7 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL ACTIVATION; CONTROLLED STUDY; DENDRITIC CELL; ENDOSOME; IMMUNOFLUORESCENCE; IMMUNOGENICITY; LYSOSOME; MACROPHAGE ACTIVATION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATION; PHAGOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; T LYMPHOCYTE; WESTERN BLOTTING;

ACYLTRANSFERASES; ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, CD1; CELLS, CULTURED; DENDRITIC CELLS; ENDOSOMES; GTP-BINDING PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERFERON TYPE II; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MACROPHAGES; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; NITRIC OXIDE SYNTHASE TYPE II; OXIDOREDUCTASES; PHAGOSOMES; POINT MUTATION; PROTO-ONCOGENE PROTEINS C-HCK; RAB5 GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES; TERMINAL REPEAT SEQUENCES; TUBERCULOSIS;

MUS; MYCOBACTERIUM TUBERCULOSIS;

EID: 43449095312     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01126.x     Document Type: Article

References (88)

1. Armitige, L.Y., Jagannath, C., Wanger, A.R., and Norris, S.J. (2000) Disruption of the genes encoding antigen 85A and antigen 85B of Mycobacterium tuberculosis H37Rv: Effect on growth in culture and in macrophages. Infect Immun 68: 767-778.
2. Armstrong, J.A., and Hart, P.D. (1971) Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 134: 713-740.
3. Astarie-Dequeker, C., N'Diaye, E.N., Le Cabec, V., Rittig, M.G., Prandi, J., and Maridonneau-Parini, I. (1999) The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages. Infect Immun 67: 469-477.
4. Astarie-Dequeker, C., Carreno, S., Cougoule, C., and Maridonneau-Parini, I. (2002) The protein tyrosine kinase Hck is located on lysosomal vesicles that are physically and functionally distinct from CD63-positive lysosomes in human macrophages. J Cell Sci 115: 81-89.
5. Babior, B.M. (1999) NADPH oxidase: An update. Blood 93: 1464-1476.
6. Banaiee, N., Kincaid, E.Z., Buchwald, U., Jacobs, W.R., Jr and Ernst, J.D. (2006) Potent inhibition of macrophage responses to IFN-gamma by live virulent Mycobacterium tuberculosis is independent of mature mycobacterial lipoproteins but dependent on TLR2. J Immunol 176: 3019-3027.
7. Bartz, H., Avalos, N.M., Baetz, A., Heeg, K., and Dalpke, A.H. (2006) Involvement of suppressors of cytokine signaling in toll-like receptor-mediated block of dendritic cell differentiation. Blood 108: 4102-4108.
8. Belisle, J.T., Vissa, V.D., Sievert, T., Takayama, K., Brennan, P.J., and Besra, G.S. (1997) Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276: 1420-1422.
9. Benghuzzi, H.A. (1995) The role of various biomedical polymers concentration on the adhesion rate and viability of monocyte and monocyte derived macrophages. Biomed Sci Instrum 31: 121-126.
10. Blander, J.M., and Medzhitov, R. (2004) Regulation of phagosome maturation by signals from toll-like receptors. Science 304: 1014-1018.
11. Brewer, T.F., and Colditz, G.A. (1995) Relationship between bacille Calmette-Guerin (BCG) strains and the efficacy of BCG vaccine in the prevention of tuberculosis. Clin Infect Dis 20: 126-135.
12. Chua, J., and Deretic, V. (2004) Mycobacterium tuberculosis reprograms waves of phosphatidylinositol 3-phosphate on phagosomal organelles. J Biol Chem 279: 36982-36992.
13. Chua, J., Vergne, I., Master, S., and Deretic, V. (2004) A tale of two lipids: Mycobacterium tuberculosis phagosome maturation arrest. Curr Opin Microbiol 7: 71-77.
14. Clemens, D.L. (1996) Characterization of the Mycobacterium tuberculosis phagosome. Trends Microbiol 4: 113-118.
15. Clemens, D.L., and Horwitz, M.A. (1995) Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181: 257-270.
16. Clemens, D.L., and Horwitz, M.A. (1996) The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 184: 1349-1355.
17. Connelly, M.A., Moulton, R.A., Smith, A.K., Lindsey, D.R., Sinha, M., Wetsel, R.A., and Jagannath, C. (2007) Mycobacteria-primed macrophages and dendritic cells induce an up-regulation of complement C5a anaphylatoxin receptor (CD88) in CD3+ murine T cells. J Leukoc Biol 81: 212-220.
18. Copenhaver, R.H., Sepulveda, E., Armitige, L.Y., Actor, J.K., Wanger, A., Norris, S.J., etal. (2004) A mutant of Mycobacterium tuberculosis H37Rv that lacks expression of antigen 85A is attenuated in mice but retains vaccinogenic potential. Infect Immun 72: 7084-7095.
19. Daniel, D.S., Dai, G., Singh, C.R., Lindsey, D.R., Smith, A.K., Dhandayuthapani, S., et al. (2006) The reduced bactericidal function of complement C5-deficient murine macrophages is associated with defects in the synthesis and delivery of reactive oxygen radicals to mycobacterial phagosomes. J Immunol 177: 4688-4698.
20. Deretic, V., and Fratti, R.A. (1999) Mycobacterium tuberculosis phagosome. Mol Microbiol 31: 1603-1609.
21. Deretic, V., Via, L.E., Fratti, R.A., and Deretic, D. (1997) Mycobacterial phagosome maturation, rab proteins, and intracellular trafficking. Electrophoresis 18: 2542-2547.
22. Deretic, V., Vergne, I., Chua, J., Master, S., Singh, S.B., Fazio, J.A., and Kyei, G. (2004) Endosomal membrane traffic: Convergence point targeted by Mycobacterium tuberculosis and HIV. Cell Microbiol 6: 999-1009.
23. Deretic, V., Singh, S., Master, S., Kyei, G., Davis, A., Naylor, J., etal. (2007) Phosphoinositides in phagolysosome and autophagosome biogenesis. Biochem Soc Symp 74: 141-148.
24. Dhandayuthapani, S., Via, L.E., Thomas, C.A., Horowitz, P.M., Deretic, D., and Deretic, V. (1995) Green fluorescent protein as a marker for gene expression and cell biology of mycobacterial interactions with macrophages. Mol Microbiol 17: 901-912.
25. Donald, P.R., Maher, D., and Qazi, S. (2007) A research agenda to promote the management of childhood tuberculosis within national tuberculosis programmes. Int J Tuberc Lung Dis 11: 370-380.
26. Edwards, K.M., Cynamon, M.H., Voladri, R.K., Hager, C.C., DeStefano, M.S., Tham, K.T., et al. (2001) Iron-cofactored superoxide dismutase inhibits host responses to Mycobacterium tuberculosis. Am J Respir Crit Care Med 164: 2213-2219.
27. Ernst, J.D. (1998) Macrophage receptors for Mycobacterium tuberculosis. Infect Immun 66: 1277-1281.
28. Fine, P.E. (1989) The BCG story: Lessons from the past and implications for the future. Rev Infect Dis 11 (Suppl. 2): S353-S359.
29. Fine, P.E. (2001) BCG: The challenge continues. Scand J Infect Dis 33: 243-245.
30. Fol, M., Chauhan, A., Nair, N.K., Maloney, E., Moomey, M., Jagannath, C., etal. (2006) Modulation of Mycobacterium tuberculosis proliferation by MtrA, an essential two-component response regulator. Mol Microbiol 60: 643-657.
31. Fratti, R.A., Vergne, I., Chua, J., Skidmore, J., and Deretic, V. (2000) Regulators of membrane trafficking and Mycobacterium tuberculosis phagosome maturation block. Electrophoresis 21: 3378-3385.
32. Fratti, R.A., Chua, J., and Deretic, V. (2003) Induction of p38 mitogen-activated protein kinase reduces early endosome autoantigen 1 (EEA1) recruitment to phagosomal membranes. J Biol Chem 278: 46961-46967.
33. Gabay, J.E., Horwitz, M.A., and Cohn, Z.A. (1986) Phagosome-lysosome fusion. Biochem Soc Trans 14: 256-257.
34. Gagliardi, M.C., Teloni, R., Giannoni, F., Pardini, M., Sargentini, V., Brunori, L., et al. (2005) Mycobacterium bovis Bacillus Calmette-Guerin infects DC-SIGN-dendritic cell and causes the inhibition of IL-12 and the enhancement of IL-10 production. J Leukoc Biol 78: 106-113.
35. Gercken, J., Pryjma, J., Ernst, M., and Flad, H.D. (1994) Defective antigen presentation by Mycobacterium tuberculosis -infected monocytes. Infect Immun 62: 3472-3478.
36. Gioffre, A., Infante, E., Aguilar, D., Santangelo, M.P., Klepp, L., Amadio, A., et al. (2005) Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. Microbes Infect 7: 325-334.
37. Harding, C.V. (1991) Pathways of antigen processing. Curr Opin Immunol 3: 3-9.
38. Harries, A.D., and Dye, C. (2006) Tuberculosis. Ann Trop Med Parasitol 100: 415-431.
39. Harth, G., Horwitz, M.A., Tabatadze, D., and Zamecnik, P.C. (2002) Targeting the Mycobacterium tuberculosis 30/32-kDa mycolyl transferase complex as a therapeutic strategy against tuberculosis: Proof of principle by using antisense technology. Proc Natl Acad Sci USA 99: 15614-15619.
40. Imai, K., Kurita-Ochiai, T., and Ochiai, K. (2003) Mycobacterium bovis bacillus Calmette-Guerin infection promotes SOCS induction and inhibits IFN-gamma-stimulated JAK/STAT signaling in J774 macrophages. FEMS Immunol Med Microbiol 39: 173-180.
41. Jagannath, C., Actor, J.K., and Hunter, R.L. Jr (1998) Induction of nitric oxide in human monocytes and monocyte cell lines by Mycobacterium tuberculosis. Nitric Oxide 2: 174-186.
42. Kang, P.B., Azad, A.K., Torrelles, J.B., Kaufman, T.M., Beharka, A., Tibesar, E., et al. (2005) The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202: 987-999.
43. Kusner, D.J. (2005) Mechanisms of mycobacterial persistence in tuberculosis. Clin Immunol 114: 239-247.
44. Launois, P., DeLeys, R., Niang, M.N., Drowart, A., Andrien, M., Dierckx, P., et al. (1994) T-cell-epitope mapping of the major secreted mycobacterial antigen Ag85A in tuberculosis and leprosy. Infect Immun 62: 3679-3687.
45. Lee, N.K., Choi, Y.G., Baik, J.Y., Han, S.Y., Jeong, D.W., Bae, Y.S., et al. (2005) A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 106: 852-859.
46. Levine, T.P., and Chain, B.M. (1991) The cell biology of antigen processing. Crit Rev Biochem Mol Biol 26: 439-473.
47. Manca, C., Tsenova, L., Freeman, S., Barczak, A.K., Tovey, M., Murray, P.J., et al. (2005) Hypervirulent M.tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J Interferon Cytokine Res 25: 694-701.
48. McDonough, K.A., Kress, Y., and Bloom, B.R. (1993) Pathogenesis of tuberculosis: Interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 61: 2763-2773.
49. McKinney, J.D., Honer zu Bentrup, K., Munoz-Elias, E.J., Miczak, A., Chen, B., Chan, W.T., et al. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738.
50. Miller, B.H., Fratti, R.A., Poschet, J.F., Timmins, G.S., Master, S.S., Burgos, M., et al. (2004) Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect Immun 72: 2872-2878.
51. Mommaas, A.M., Mulder, A.A., Out, C.J., Girolomoni, G., Koerten, H.K., Vermeer, B.J., and Koning, F. (1995) Distribution of HLA class II molecules in epidermal Langerhans cells in situ. Eur J Immunol 25: 520-525.
52. Moulton, R., Connelly, M., Smith, K., Lindsey, D., Haviland, D., Wetsel, R., etal. (2007) Complement C5a is an innate determinant of dendritic cell induced Th1 immunity to Mycobacterium bovis BCG infection in mice. J Leucocyte Biology 82: 956-967.
53. Nathan, C.F. (1983) Mechanisms of macrophage antimicrobial activity. Trans R Soc Trop Med Hyg 77: 620-630.
54. Noss, E.H., Harding, C.V., and Boom, W.H. (2000) Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol 201: 63-74.
55. O'Keefe, G.M., Nguyen, V.T., Ping Tang, L.L., and Benveniste, E.N. (2001) IFN-gamma regulation of class II transactivator promoter IV in macrophages and microglia: Involvement of the suppressors of cytokine signaling-1 protein. J Immunol 166: 2260-2269.
56. Pancholi, P., Mirza, A., Bhardwaj, N., and Steinman, R.M. (1993) Sequestration from immune CD4+ T cells of mycobacteria growing in human macrophages. Science 260: 984-986.
57. Perskvist, N., Long, M., Stendahl, O., and Zheng, L. (2002a) Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol 168: 6358-6365.
58. Perskvist, N., Roberg, K., Kulyte, A., and Stendahl, O. (2002b) Rab5a GTPase regulates fusion between pathogen-containing phagosomes and cytoplasmic organelles in human neutrophils. J Cell Sci 115: 1321-1330.
59. Pieters, J. (2001) Entry and survival of pathogenic mycobacteria in macrophages. Microbes Infect 3: 249-255.
60. Puech, V., Guilhot, C., Perez, E., Tropis, M., Armitige, L.Y., Gicquel, B., and Daffe, M. (2002) Evidence for a partial redundancy of the fibronectin-binding proteins for the transfer of mycoloyl residues onto the cell wall arabinogalactan termini of Mycobacterium tuberculosis. Mol Microbiol 44: 1109-1122.
61. Ramachandra, L., Noss, E., Boom, W.H., and Harding, C.V. (2001) Processing of Mycobacterium tuberculosis antigen 85B involves intraphagosomal formation of peptide-major histocompatibility complex II complexes and is inhibited by live bacilli that decrease phagosome maturation. J Exp Med 194: 1421-1432.
62. Rink, J., Ghigo, E., Kalaidzidis, Y., and Zerial, M. (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122: 735-749.
63. Robinson, N., Wolke, M., Ernestus, K., and Plum, G. (2007) A mycobacterial gene involved in synthesis of an outer cell envelope lipid is a key factor in prevention of phagosome maturation. Infect Immun 75: 581-591.
64. Ronning, D.R., Vissa, V., Besra, G.S., Belisle, J.T., and Sacchettini, J.C. (2004) Mycobacterium tuberculosis antigen 85A and 85C structures confirm binding orientation and conserved substrate specificity. J Biol Chem 279: 36771-36777.
65. Russell, D.G. (1995) Mycobacterium and Leishmania: Stowaways in the endosomal network. Trends Cell Biol 5: 125-128.
66. Russell, D.G. (1998) What does 'inhibition of phagosome-lysosome fusion'really mean? Trends Microbiol 6: 212-214.
67. Russell, D.G. (2001) Mycobacterium tuberculosis: Here today, and here tomorrow. Nat Rev Mol Cell Biol 2: 569-577.
68. Russell, D.G. (2003) Phagosomes, fatty acids and tuberculosis. Nat Cell Biol 5: 776-778.
69. Sambandamurthy, V.K., Wang, X., Chen, B., Russell, R.G., Derrick, S., Collins, F.M., et al. (2002) A pantothenate auxotroph of Mycobacterium tuberculosis is highly attenuated and protects mice against tuberculosis. Nat Med 8: 1171-1174.
70. Sambandamurthy, V.K., Derrick, S.C., Hsu, T., Chen, B., Larsen, M.H., Jalapathy, K.V., et al. (2006) Mycobacterium tuberculosis DeltaRD1 DeltapanCD: A safe and limited replicating mutant strain that protects immunocompetent and immunocompromised mice against experimental tuberculosis. Vaccine 24: 6309-6320.
71. Scherer, T.A., Lauredo, I.T., and Abraham, W.M. (1997) Scavenging of reactive oxygen species by a glycolipid fraction of Mycobacterium avium serovar 2. Free Radic Biol Med 22: 561-565.
72. Singh, C.R., Moulton, R.A., Armitige, L.Y., Bidani, A., Snuggs, M., Dhandayuthapani, S., et al. (2006) Processing and presentation of a mycobacterial antigen 85B epitope by murine macrophages is dependent on the phagosomal acquisition of vacuolar proton ATPase and in situ activation of cathepsin D. J Immunol 177: 3250-3259.
73. Skeiky, Y.A., and Sadoff, J.C. (2006) Advances in tuberculosis vaccine strategies. Nat Rev Microbiol 4: 469-476.
74. Spargo, B.J., Crowe, L.M., Ioneda, T., Beaman, B.L., and Crowe, J.H. (1991) Cord factor (alpha,alpha-trehalose 6,6′-dimycolate) inhibits fusion between phospholipid vesicles. Proc Natl Acad Sci USA 88: 737-740.
75. Stewart, G.R., Wilkinson, K.A., Newton, S.M., Sullivan, S.M., Neyrolles, O., Wain, J.R., et al. (2005) Effect of deletion or overexpression of the 19-kilodalton lipoprotein Rv3763 on the innate response to Mycobacterium tuberculosis. Infect Immun 73: 6831-6837.
76. Sturgill-Koszycki, S., Schaible, U.E., and Russell, D.G. (1996) Mycobacterium -containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 15: 6960-6968.
77. Suh, C.I., Stull, N.D., Li, X.J., Tian, W., Price, M.O., Grinstein, S., etal. (2006) The phosphoinositide-binding protein p40phox activates the NADPH oxidase during FcgammaIIA receptor-induced phagocytosis. J Exp Med 203: 1915-1925.
78. Teitelbaum, R., Cammer, M., Maitland, M.L., Freitag, N.E., Condeelis, J., and Bloom, B.R. (1999) Mycobacterial infection of macrophages results in membrane-permeable phagosomes. Proc Natl Acad Sci USA 96: 15190-15195.
79. Ullrich, H.J., Beatty, W.L., and Russell, D.G. (1999) Direct delivery of procathepsin D to phagosomes: Implications for phagosome biogenesis and parasitism by Mycobacterium. Eur J Cell Biol 78: 739-748.
80. Ullrich, H.J., Beatty, W.L., and Russell, D.G. (2000) Interaction of Mycobacterium avium -containing phagosomes with the antigen presentation pathway. J Immunol 165: 6073-6080.
81. Vazquez-Torres, A., and Fang, F.C. (2001) Salmonella evasion of the NADPH phagocyte oxidase. Microbes Infect 3: 1313-1320.
82. Vergne, I., Chua, J., Singh, S.B., and Deretic, V. (2004a) Cell biology of Mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 20: 367-394.
83. Vergne, I., Fratti, R.A., Hill, P.J., Chua, J., Belisle, J., and Deretic, V. (2004b) Mycobacterium tuberculosis phagosome maturation arrest: Mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell 15: 751-760.
84. Via, L.E., Deretic, D., Ulmer, R.J., Hibler, N.S., Huber, L.A., and Deretic, V. (1997) Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 272: 13326-13331.
85. Via, L.E., Fratti, R.A., McFalone, M., Pagan-Ramos, E., Deretic, D., and Deretic, V. (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111 (Pt 7): 897-905.
86. Vieira, O.V., Botelho, R.J., and Grinstein, S. (2002) Phagosome maturation: Aging gracefully. Biochem J 366: 689-704.
87. Vieira, O.V., Harrison, R.E., Scott, C.C., Stenmark, H., Alexander, D., Liu, J., et al. (2004) Acquisition of Hrs, an essential component of phagosomal maturation, is impaired by mycobacteria. Mol Cell Biol 24: 4593-4604.
88. Wang, Y., Zeigler, M.M., Lam, G.K., Hunter, M.G., Eubank, T.D., Khramtsov, V.V., etal. (2006) The Role of the NADPH oxidase complex, p38 MAPK and Akt in regulating human monocyte/macrophage survival. Am J Respir Cell Mol Biol 36: 68-77.