Mycobacterium's arrest of phagosome maturation in macrophages requires Rab5 activity and accessibility to iron

Molecular Biology of the Cell

Volumn 14, Issue 8, 2003, Pages 3366-3377

  Kelley, Victoria A ^a   Schorey, Jeffrey S ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; IRON; RAB PROTEIN; RETROVIRUS VECTOR;

ANIMAL CELL; ARTICLE; BACTERICIDAL ACTIVITY; CELL MATURATION; CONTROLLED STUDY; CULTURE MEDIUM; ENDOSOME; GENETIC TRANSDUCTION; IMMUNOFLUORESCENCE MICROSCOPY; LYSOSOME; MOUSE; MYCOBACTERIUM; MYCOBACTERIUM AVIUM; NONHUMAN; OPSONIZATION; PHAGOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; CLONING, MOLECULAR; ENDOSOMES; IRON; MACROPHAGES; MICE; MICE, INBRED BALB C; MUTATION; MYCOBACTERIUM AVIUM; PHAGOSOMES; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; TRANSPORT VESICLES;

ACTINOBACTERIA (CLASS); ANIMALIA; CORYNEBACTERINEAE; MURINAE; MYCOBACTERIUM; MYCOBACTERIUM AVIUM; UNCULTURED ACTINOMYCETE; UNIDENTIFIED RETROVIRUS;

EID: 0041467786     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-12-0780     Document Type: Article

References (51)

1. Atkinson, P.G., Blackwell, J.M., and Barton, C.H. (1997). Nramp1 locus encodes a 65 kDa interferon-gamma-inducible protein in murine macrophages. Biochem. J. 325, 779-786.
2. Baker, E., Baker, S.M., and Morgan, E.H. (1998). Characterisation of non-transferrin-bound iron (ferric citrate) uptake by rat hepatocytes in culture. Biochim. Biophys. Acta 1380, 21-30.
3. Barbieri, M.A., Li, G., Colombo, M.I., and Stahl, P.D. (1994). Rab5, an early acting endosomal GTPase, supports in vitro endosome fusion without GTP hydrolysis. J. Biol. Chem. 269, 18720-18722.
4. Bellamy, R. (1999). The natural resistance-associated macrophage protein and susceptibility to intracellular pathogens. Microbes Infect. 1, 23-27.
5. Bohlson, S.S., Strasser, J.A., Bower, J.J., and Schorey, J.S. (2001). Role of complement in Mycobacterium avium pathogenesis: in vivo and in vitro analyses of the host response to infection in the absence of complement component C3. Infect. Immun. 69, 7729-7735.
6. Boshans, R.L., Szanto, S., van Aelst, L., and D'Souza-Schorey, C. (2000). ADP-ribosylation factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA. Mol. Cell. Biol. 20, 3685-3694.
7. Chitambar, C.R., Matthaeus, W.G., Antholine, W.E., Graff, K., and O'Brien, W.J. (1988). Inhibition of leukemic HL60 cell growth by transferrin-gallium: effects on ribonucleotide reductase and demonstration of drug synergy with hydroxyurea. Blood 72, 1930-1936.
8. Chitambar, C.R., and Zivkovic, Z. (1987). Uptake of gallium-67 by human leukemic cells: demonstration of transferrin receptor-dependent and transferrin-independent mechanisms. Cancer Res. 47, 3929-3934.
9. Clemens, D.L. (1996). Characterization of the Mycobacterium tuberculosis phagosome. Trends Microbiol. 4, 113-118.
10. 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.
11. De Voss, J.J., Rutter, K., Schroeder, B.G., and Barry, C.E., 3rd. (1999). Iron acquisition and metabolism by mycobacteria. J. Bacteriol. 181, 4443-4451.
12. Deretic, V., and Fratti, R.A. (1999). Mycobacterium tuberculosis phagosome. Mol. Microbiol. 31, 1603-9.
13. Deretic, V., Via, L.E., Fratti, R.A., and Deretic, D. (1997). Mycobacterial phagosome maturation, rab proteins, and intracellular trafficking. Electrophoresis 18, 2542-2547.
14. Dhople, A.M., Ibanez, M.A., and Poirier, T.C. (1996). Role of iron in the pathogenesis of Mycobacterium avium infection in mice. Microbios 87, 77-87.
15. Duclos, S., Diez, R., Garin, J., Papadopoulou, B., Descoteaux, A., Stenmark, H., and Desjardins, M. (2000). Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J. Cell Sci. 113(Pt 19), 3531-3541.
16. Edwards, K.M., Cynamon, M.H., Voladri, R.K., Hager, C.C., DeStefano, M.S., Tham, K.T., Lakey, D.L., Bochan, M.R., and Kernodle, D.S. (2001). Iron-cofactored superoxide dismutase inhibits host responses to Mycobacterium tuberculosis. Am. J. Respir. Crit. Care Med. 164, 2213-9.
17. Feng, Y., Press, B., and Wandinger-Ness, A. (1995). Rab 7, an important regulator of late endocytic membrane traffic. J. Cell Biol. 131, 1435-1452.
18. Forbes, J.R., and Gros, P. (2001). Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol. 9, 397-403.
19. Fratti, R.A., Backer, J.M., Gruenberg, J., Corvera, S., and Deretic, V. (2001). Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154, 631-644.
20. Fratti, R.A., Chua, J., and Deretic, V. (2002). Cellubrevin alterations and Mycobacterium tuberculosis phagosome maturation arrest. J. Biol. Chem. 277, 17320-17326.
21. Govoni, G., Vidal, S., Cellier, M., Lepage, P., Malo, D., and Gros, P. (1995). Genomic structure, promoter sequence, and induction of expression of the mouse Nramp1 gene in macrophages. Genomics 27, 9-19.
22. Li, G. (1996). Rab5 GTPase and endocytosis. Biocell 20, 325-330.
23. Li, G., Barbieri, M.A., Colombo, M.I., and Stahl, P.D. (1994). Structural features of the GTP-binding defective Rab5 mutants required for their inhibitory activity on endocytosis. J. Biol. Chem. 269, 14631-14635.
24. Lounis, N., Truffot-Pernot, C., Grosset, J., Gordeuk, V.R., and Boelaert, J.R. (2001). Iron and Mycobacterium tuberculosis infection. J. Clin. Virol. 20, 123-126.
25. Martinez, O., and Goud, B. (1998). Rab proteins. Biochim. Biophys. Acta 1404, 101-112.
26. McCaffrey, M.W., Bielli, A., Cantalupo, G., Mora, S., Roberti, V., Santillo, M., Drummond, F., and Bucci, C. (2001). Rab4 affects both recycling and degradative endosomal trafficking. FEBS Lett. 495, 21-30.
27. Michiels, F., van der Kammen, R.A., Janssen, L., Nolan, G., and Collard, J.G. (2000). Expression of Rho GTPases using retroviral vectors. Methods Enzymol. 325, 295-302.
28. Mohrmann, K., and van der Sluijs, P. (1999). Regulation of membrane transport through the endocytic pathway by rabGTPases. Mol. Membr. Biol. 16, 81-87.
29. Murray, M.J., Murray, A.B., Murray, M.B., and Murray, C.J. (1978). The adverse effect of iron repletion on the course of certain infections. Br. Med. J. 2, 1113-1115.
30. Olakanmi, O., Schlesinger, L.S., Ahmed, A., and Britigan, B.E. (2002). Intraphagosomal Mycobacterium tuberculosis acquires iron from both extracellular transferrin and intracellular iron pools. J. Biol. Chem. 277, 49727-49734.
31. Olakanmi, O., Britigan, B.E., and Schlesinger, L.S. (2000). Gallium disrupts iron metabolism of mycobacteria residing within human macrophages. Infect. Immun. 68, 5619-5627.
32. Olakanmi, O., Stokes, J.B., and Britigan, B.E. (1994). Acquisition of iron bound to low molecular weight chelates by human monocyte-derived macrophages. J. Immunol. 153, 2691-2703.
33. Palacios, F., Price, L., Schweitzer, J., Collard, J.G., and D'Souza-Schorey, C. (2001). An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20, 4973-4986.
34. Racoosin, E.L., and Swanson, J.A. (1993). Macropinosome maturation and fusion with tubular lysosomes in macrophages. J. Cell Biol. 121, 1011-1020.
35. Raghu, B., Sarma, G.R., and Venkatesan, P. (1993). Effect of iron on the growth and siderophore production of mycobacteria. Biochem. Mol. Biol. Int. 31, 341-348.
36. Roach, S.K., and Schorey, J.S. (2002). Differential regulation of the mitogen-activated protein kinases by pathogenic and nonpathogenic mycobacteria. Infect. Immun. 70, 3040-3052.
37. Russell, D.G., Dant, J., and Sturgill-Koszycki, S. (1996). Mycobacterium avium- and Mycobacterium tuberculosis-containing vacuoles are dynamic, fusion-competent vesicles that are accessible to glycosphingolipids from the host cell plasmalemma. J. Immunol. 156, 4764-4773.
38. Russell, D.G., Sturgill-Koszycki, S., Vanheyningen, T., Collins, H., and Schaible, U.E. (1997). Why intracellular parasitism need not be a degrading experience for Mycobacterium. Philos. Trans. R Soc. Lond. B Biol. Sci. 352, 1303-1310.
39. Scaccabarozzi, A. et al. (2000). Relationship between TNF-alpha and iron metabolism in differentiating human monocytic THP-1 cells. Br. J. Haematol. 110, 978-984.
40. Schaible, U.E., Collins, H.L., Priem, F., and Kaufmann, S. (2002). Correction of the iron overload defect in β-2-microglobulin knock-out mice by lactoferrin abolishes their increased susceptibility to tuberculosis. J. Exp. Med. 196, 1507-1513.
41. Somsel Rodman, J., and Wandinger-Ness, A. (2000). Rab GTPases coordinate endocytosis. J. Cell Sci. 113(Pt 2), 183-192.
42. Stenmark, H., Parton, R.G., Steele-Mortimer, O., Lutcke, A., Gruenberg, J., and Zerial, M. (1994). Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296.
43. Sturgill-Koszycki, S. et al. (1994). Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681.
44. Thilo, L., Stroud, E., and Haylett, T. (1995). Maturation of early endosomes and vesicular traffic to lysosomes in relation to membrane recycling. J. Cell Sci. 108, 1791-1803.
45. 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.
46. Vidal, S., Gros, P., and Skamene, E. (1995). Natural resistance to infection with intracellular parasites: molecular genetics identifies Nramp1 as the Bcg/Ity/Lsh locus. J Leukoc. Biol. 58, 382-390.
47. Vitelli, R., Santillo, M., Lattero, D., Chiariello, M., Bifulco, M., Bruni, C.B., and Bucci, C. (1997). Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem. 272, 4391-4397.
48. Woodman, P.G. (2000a). Biogenesis of the sorting endosome: the role of Rab5. Traffic 1, 695-701.
49. Woodman, P.G. (2000b). Biogenesis of the sorting endosome: the role of Rab5. Traffic 1, 695-701.
50. 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.
51. Zerial, M. (1993). Regulation of endocytosis by the small GTP-ase rab5. Cytotechnology 11, S47-S49.