Lipoamide dehydrogenase mediates retention of coronin-1 on BCG vacuoles, leading to arrest in phagosome maturation

Journal of Cell Science

Volumn 120, Issue 16, 2007, Pages 2796-2806

  Deghmane, Ala Eddine ^a   Soulhine, Hafid ^a   Bach, Horacio ^a   Sendide, Khalid ^b   Itoh, Saotomo ^c   Tam, Andrea ^a   Noubir, Sanaa ^a   Talal, Amina ^a   Lo, Raymond ^d   Toyoshima, Satoshi ^c   Av Gay, Yossef ^a   Hmama, Zakaria ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b AL AKHAWAYN UNIVERSITY   (Morocco)

^c HOSHI UNIVERSITY   (Japan)

^d SIMON FRASER UNIVERSITY   (Canada)

Author keywords

IFN ; LRG 47; Macrophage; Mycobacterium smegmatis; Mycobacterium tuberculosis; Phagosome biogenesis

Indexed keywords

CHOLESTEROL; COAT PROTEIN; CORONIN 1; CORONIN INTERACTING PROTEIN 50; DIHYDROLIPOAMIDE DEHYDROGENASE; DIHYDROLIPOAMIDE DEHYDROGENASE C; GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE LRG 47; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL VACUOLE; CONTROLLED STUDY; GROWTH INHIBITION; MACROPHAGE; MASS SPECTROMETRY; MOUSE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CHOLESTEROL; DIHYDROLIPOAMIDE DEHYDROGENASE; GTP-BINDING PROTEINS; INTERFERON-GAMMA; MACROPHAGES; MICE; MICROBIAL VIABILITY; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MYCOBACTERIUM BOVIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PHAGOSOMES; PROTEIN BINDING; PROTEIN TRANSPORT; VACUOLES;

MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 34548548443     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.006221     Document Type: Article

References (60)

1. Aderem, A. and Ulevitch, R. J. (2000). Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787.
2. Babior, B. M. (1995). The respiratory burst oxidase. Curr. Opin. Hematol. 2, 55-60.
3. Beatty, W. L. and Russell, D. G. (2000). Identification of mycobacterial surface proteins released into subcellular compartments of infected macrophages. Infect. Immun. 68, 6997-7002.
4. Bryk, R., Lima, C. D., Erdjument-Bromage, H., Tempst, P. and Nathan, C. (2002). Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295, 1073-1077.
5. Chan, J. and Flynn, J. (2004). The immunological aspects of latency in tuberculosis. Clin. Immunol. 110, 2-12.
6. Chan, J., Xing, Y., Magliozzo, R. S. and Bloom, B. R. (1992). Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175, 1111-1122.
7. Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S. C., Waterfleld, M. D., Backer, J. M. and Zerial, M. (1999). Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1, 249-252.
8. Clemens, D. and Horwitz, M. A. (1995). Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181, 257-270.
9. Cowley, S. C. and Av-Gay, Y. (2001). Monitoring promoter activity and protein localization in Mycobacterium spp. using green fluorescent protein. Gene 264, 225-231.
10. Dalton, D. K., Pitts-Meek, S., Keshav, S., Figari, I. S., Bradley, A. and Stewart, T. A. (1993). Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259, 1739-1742.
11. de Hostos, E. L. (1999). The coronin family of actin-associated proteins. Trends Cell Biol. 9, 345-350.
12. de Kok, A., Hengeveld, A. R, Martin, A. and Westphal, A. H. (1998). The pyruvate dehydrogenase multi-enzyme complex from Gram-negative bacteria. Biochim. Biophys. Acta 1385, 353-366.
13. Deretic, V., Singh, S., Master, S., Harris, J., Roberts, E., Kyei,G., Davis, A., de Haro, S., Naylor, J., Lee, H. H. and Vergne, I. (2006). Mycobacterium, tuberculosis inhibition of phagolysosorne biogenesis and autophagy as a host defence mechanism. Cell. Microbiol. 8, 719-727.
14. Desjardins, M., Huber, L. A., Parton, R. G. and Griffiths, G. (1994). Biogenesis of phagolysosomics; proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124, 677-688.
15. Desjardins, M., Houde, M. and Gagnon, E. (2005). Phagocytosis: the convoluted way from nutrition to adaptive immunity. Immunol. Rev. 207, 158-165.
16. Ehrt, S., Schnappinger, D., Bekiranov, S., Drenkow, J., Shi, S., Gingeras, T. R., Gaasterland, T., Schoolnik, G. and Nathan, C. (2001). Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J. Exp. Med. 194, 1123-1140.
17. Ferrari, G., Langen, H., Naito, M. and Pieters, J. (1999). A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97, 435-447.
18. Foger, N., Rangell, L., Danilenko, D. M. and Chan, A. C. (2006). Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science. 313, 839-842.
19. Fratti, R. A., Chua, J., Vergne, I. and Deretic, V. (2003). Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100, 5437-5442.
20. Gatrield, J. and Pieters, J. (2000). Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288, 1647-1650.
21. Gatfleld, J. and Pieters, J. (2003). Molecular mechanisms of host-pathogen interaction: entry and survival of mycobacteria in macrophages. Adv. Immunol. 81, 45-96.
22. Grogan, A., Reeves, E., Keep, N., Wientjes, F., Totty, N. F., Burlingame, A. L., Hsuan, J. J. and Segal, A. W. (1997). Cytosolic phox proteins interact with and regulate the assembly of coronin in neutrophils. J. Cell Sci. 110, 3071-3081.
23. Gruenberg, J. and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323.
24. Gutierrez, M. G., Master, S. S., Singh, S. B., Taylor, G. A., Colombo, M. I. and Deretie, V. (2004). Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766.
25. Harth, G. and Horwitz, M. A. (1997). Expression and efficient export of enzymatically active Mycobacterium tuberculosis glutamine synthetase in Mycobacterium smegmatis and evidence that the information for export is contained within the protein. J. Biol. Chem. 272, 22728-22735.
26. Harth, G. and Horwitz, M. A. (1999). Export of recombinant Mycobacterium tuberculosis superoxide dismutase is dependent upon both information in the protein and mycobacterial export machinery. A model for studying export of leaderless proteins by pathogenic mycobacteria. J. Biol. Chem. 274, 4281-4292.
27. Hestvik, A. L., Hmama, Z. and Av-Gay, Y. (2005). Mycobacterial manipulation of the host cell. FEMS Microbiol. Rev. 29, 1041-1050.
28. Hmama, Z., Gabathuler, R., Jefferies, W. A., de Jon, G. and Reiner, N. E. (1998). Attenuation of HLA-DR expression by monomiclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterdimers. J. Immunol. 161, 4882-4893.
29. Hmama, Z., Sendide, K., Talal, A., Garcia, R., Dobos, K. and Reiner, N. E. (2004). Quantitative analysis of phagolysosorne fusion in intact cells: inhibition by mycobacterial lipoarabinomannan and rescue by an 1alpha,25-dihydroxyvitamin D3-phosphoinositide 3-kinase pathway. J. Cell Sci. 117, 2131-2140.
30. Kaps, I., Ehrt, S., Seeber, S., Schnappinger, D., Martin, C., Riley, L. W. and Niederweis, M. (2001). Energy transfer between fluorescent proteins using a colocexpression system in Mycobacterium smegmatis. Gene 278, 115-124.
31. Katzmann, D. J., Odorizzi, G. and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905.
32. Koul, A., Choidas, A., Treder, M., Tyagi, A. K., Drlica, K., Singh, Y. and Ullrich, A. (2000). Cloning and characterization of secretory tyrosine phosphatases of Mycobacterium tuberculosis. J. Bacteriol. 182, 5425-5432.
33. Kusner, D. J. (2005). Mechanisms of mycobacterial persistence in tuberculosis. Clin. Immunol. 114, 239-247.
34. Lowe, D. C., Patki, V., Heller-Harrison, R., Lambright, D., Corvera, S., Patki, V., Lawe, D. C., Corvera, S., Virbasius, J. V. and Chawla, A. (2000). The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization A functional PtdIns(3)P-binding motif. J. Biol. Chem. 275, 3699-3705.
35. Lee, B. Y. and Horwitz, M. A. (1995). Identification of macrophage and stress-induced proteins of Mycobacterium tuberculosis. J. Clin. Invest. 96 245-249.
36. Li, H., Yao, Z., Degenbardt, B., Teper, G. and Papadopoulos, V. (2001). Cholesterol binding at the cholesterol recognition/interaction amino acid consensus (CRAC) of the peripheral-type benzodiazepine receptor and inhibition of steroidogenesis by an HIV TAT-CRAC peptide. Proc. Natl. Acad. Sci. USA 98, 1267-1272.
37. MacMicking, J. D., North, R. J., LaCourse, R., Mudgett, J. S., Shah, S. K. and Nathan, C. F. (1997). Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad Sci. USA 94, 5243-5248.
38. MacMicking, J. D., Taylor, G. A. and McKinney, J. D. (2003). Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 302, 654-659.
39. Malik, Z. A., Thompson, C. R., Hashimi, S., Porter, B., Iyer, S. S. and Kusner, D. J. (2003). Cutting edge: mycobacteriurn tuberculosis blocks Ca2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J. Immunol. 170, 2811-2815.
40. Maniak, M., Rauchenberger, R., Albrecht, R., Murphy, J. and Gerisch, G. (1995). Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell 83, 915-924.
41. Marcinkeviciene, J. and Blanchard, J. S. (1997). Catalytic properties of lipoamide dehydrogenase from Mycobacterium smegmatis. Arch. Biochem. Biophys. 340, 168-176.
42. Orlandi, P. A. and Fishman, P. H. (1998). Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141, 905-915.
43. Oku, T., Itoh, S., Okano, M., Suzuki, A., Suzuki, K., Nakajin, S., Tsuji, T., Nauseef, W. M. and Toyoshima, S. (2003). Two regions responsible for the actin binding of p57, a mammalian coronin family actin-binding protein. Biol. Pharm. Bull. 26, 409-416.
44. Rhee, K. Y., Erdjument-Bromage, H, Tempst, P. and Nathan, C. F. (2005). S-nitroso proteome of Mycobacterium tuberculosis: Enzymes of intermediary metabolism and antioxidant defense. Proc. Natl. Acad. Sci. USA 102, 467-472.
45. Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P. H. and Russell, D. G. (1998). Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160, 1290-1296.
46. Sendide, K., Deghmane, A. E., Reyrat, J. M., Talal, A. and Hmama, Z. (2004). Mycobacterium bovis BCG urease attenuates major histocompatibility complex class II trafficking to the macropbage cell surface. Infect. Immun. 72, 4200-4209.
47. Sendide, K., Deghmane, A. E., Pechkovsky, D., Av-Gay, Y, ThIal, A. and Hmama, Z. (2005a). Mycobacterium bovis BCG attenuates surface expression of mature class II molecules through IL-10-dependent inhibition of cathepsin S. J. Immunol. 175, 5324-5332.
48. Sendide, K., Reiner, N. E., Lee, J. S., Bourgoín, S., Talal, A. and Hmama, Z. (2005b). Cross-talk between CD14 and complement receptor 3 promotes phagocytosis of mycobacteria: regulation by phosphatidylinositol 3-kinase and cytohesin-1. J. Immunol. 174, 4210-4219.
49. Smith, A. W., Roche, H., Trombe, M. C., Briles, D. E. and Hakansson, A. (2002). Characterization of the dihydrolipoamide dehydrogenase from Streptococcus pneumoniae and its role in pneumococcal infection. Mol. Microbiol. 44, 431-448.
50. Sturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, F., Haddix, P. L., Collins, H. L., Fok, A. K., Allen, R. D., Gluck, S. L., Heuser, J. and Russell, D. G. (1994). Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681.
51. Suzuki, K., Nishihata, J., Arai, Y., Honma, N., Yamamoto, K., Irimura, T. and Toyoshima, S. (1995). Molecular cloning of a novel actin-binding protein, p57, with a WD repeat and a leucine zipper motif. FEBS Lett. 364, 283-288.
52. Thompson, C. R., Iyer, S. S., Melrose, N., Vanoosten, R., Johnson, K., Pitson, S. M., Obeid, L. M. and Kusner, D. J. (2005). Sphingosine kinase 1 (SK1) is recruited to nascent phagosornes in human macrophages: inhibition of SK1 translocation by mycobacterium tuberculosis. J. Immunol. 174, 3551-3561.
53. Via, L. E., Fratti, R. A., McFalone, M., Pagan-Ramos, E., Deretic, D. and Derefic, V. (1998). Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897-905.
54. Vergne, I., Chua, J. and Deretic, V. (2003). Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/caImodulin-PI3K hVPS34 cascade. J. Exp. Med. 198, 653-659.
55. Vergne, I., Chua, J., Lee, H, H., Lucas, M., Belisle, J. and Deretic, V. (2005). Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis. Proc. Natl. Acad Sci. USA 102, 4033-4038.
56. Vieira, O. V., Botelho, R. J. and Grinstein, S. (2002). Phagosome maturation: aging gracefully. Biochem. J. 366, 689-704,
57. Williams, C. H. (1992). Lipoamide dehydrogenase, glutathione reductase, thioredoxin reductase, and mercuric reductase. A family of flavoenzyme transhydrogenases. In Chemistry and Biochemistry of Flavoenzymes (ed. F. Müller), pp. 121-211. Boca Raton, FL: CRC.
58. Xu, S., Cooper, A., Sturgill-Koszycki, S., van Heyningen, T., Chatterjee, D., Orme, I., Allen, P. and Russell, D. G. (1994). Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 153, 2568-2578.
59. Yan, M., Collins, R. F., Grinstein, S. and Trimble, W. S. (2005). Coronin-1 function is required for phagosome formation. Mol. Biol. Cell 7, 3077-3087.
60. Zheng, P. Y. and Jones, N. L. (2003). Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein. Cell. Microbiol. 5, 25-40.