Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria

Nature Cell Biology

Volumn 5, Issue 9, 2003, Pages 793-802

  Anes, Elsa ^a,b   Kühnel, Mark Philipp ^b   Bos, Evelyne ^b   Moniz Pereira, Jose ^a   Habermann, Anja ^b   Griffiths, Gareth ^b  

^a UNIVERSITY OF LISBON   (Portugal)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; LATEX; OMEGA 3 FATTY ACID;

ACIDIFICATION; ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; CELL MATURATION; CELL MEMBRANE; CONTROLLED STUDY; LYSOSOME; MACROPHAGE; MEMBRANE FUSION; MOUSE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY;

ACTINS; ANIMALS; CELL DIFFERENTIATION; CELL LINE; FEEDBACK, BIOCHEMICAL; HOST-PARASITE RELATIONS; INTRACELLULAR MEMBRANES; LIPID METABOLISM; LIPIDS; MACROPHAGES; MEMBRANE FUSION; MICE; MYCOBACTERIACEAE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; NITRIC OXIDE; PHAGOCYTOSIS; PHAGOSOMES; SIGNAL TRANSDUCTION;

ACTINOBACTERIA (CLASS); ANIMALIA; BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; UNCULTURED ACTINOMYCETE;

EID: 0042471938     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1036     Document Type: Article

References (41)

1. Barry, C. E. 3rd. Interpreting cell wall 'virulence factors' of Mycobacterium tuberculosis. Trends Microbiol. 9, 237-241 (2001).
2. Kaufmann, S. H. Is the development of a new tuberculosis vaccine possible? Nature Med. 6, 955-960 (2000).
3. Flynn, J. L. & Chan, J. Immunology of tuberculosis. Annu. Rev. Immunol. 19, 93-129 (2001).
4. Nathan, C. & Shiloh, M. U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97, 8841-8848 (2000).
5. Vieira, O. V., Botelho, R. J. & Grinstein, S. Phagosome maturation: aging gracefully. Biochem. J. 366, 689-704 (2002).
6. Clemens, D. L. Characterization of the Mycobacterium tuberculosis phagosome. Trends Microbiol. 4, 113-118 (1996).
7. Russell, D. G. Mycobacterium tuberculosis: here today, and here tomorrow. Nature Rev. Mol. Cell Biol. 2, 569-577 (2001).
8. Haas, A. Reprogramming the phagocytic pathway-intracellular pathogens and their vacuoles. Mol. Membrane Biol. 15, 103-121 (1998).
9. Tjelle, T. E., Lovdal, T. & Berg, T. Phagosome dynamics and function. Bioessays 22, 255-263 (2000).
10. Fischer, K. et al. Mycobacterial lysocardiolipin is exported from phagosomes upon cleavage of cardiolipin by a macrophage-derived lysosomal phospholipase A2. J. Immunol. 167, 2187-2192 (2001).
11. Pieters, J. Entry and survival of pathogenic mycobacteria in macrophages. Microbes Infect. 3, 249-255 (2001).
12. Blackwell, J. M. et al. SLC11A1 (formerly NRAMP1) and disease resistance. Cell Microbiol. 3, 773-784 (2001).
13. Via, L. E. et al. Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897-905 (1998).
14. Akaki, T., Tomioka, H., Shimizu, T., Dekio, S. & Sato, K. Comparative roles of free fatty acids with reactive nitrogen intermediates and reactive oxygen intermediates in expression of the anti-microbial activity of macrophages against Mycobacterium tuberculosis. Clin. Exp. Immunol. 121, 302-310 (2000).
15. Defacque, H. etal. Involvement of ezrin/moesin in denovoactin assembly on phagosomal membranes. EMBO J. 19, 199-212 (2000).
16. Desjardins, M. et al. Molecular characterization of phagosomes. J. Biol. Chem. 269, 32194-32200 (1994).
17. Desjardins, M., Huber, L. A., Parton, R. G. & Griffiths, G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 24, 677-688 (1994).
18. Garin, J. et al. The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152, 165-180 (2001).
19. Defacque, H. et al. Actin assembly induced by polylysine beads or purified phagosomes: quantitation by a new flow cytometry assay. Cytometry 41, 46-54 (2000).
20. Defacque, H. Phosphoinositides regulate membrane-dependent actin assembly by latex bead phagosomes. Mol. Biol. Cell 13, 1190-1202 (2002).
21. Emans, N., Nzala, N. N. & Desjardins, M. Protein phosphorylation during phagosome maturation. FEBS Lett. 398, 37-42. (1996).
22. Jahraus, A. et al. ATP-dependent membrane assembly of F-actin facilitates membrane fusion. Mol. Biol. Cell 12, 155-170 (2001).
23. Hotowka, D. & Baird, B. Antigen-mediated IGE receptor aggregation and signaling: a window on cell surface structure and dynamics. Annu. Rev. Biophys. Biomol. Struct. 25, 79-112 (1996).
24. Simons, K. & Toomre, D. Lipid rafts and signal transduction. Nature Rev. Mol. Cell Biol. 1, 31-39 (2000).
25. Caroni, P. New EMBO members' review: actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts. EMBO J. 20, 4332-4336 (2001).
26. Rozelle, A. L. et al. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10, 311-320 (2000).
27. Dermine, J. F. et al. Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J. Biol. Chem. 276, 18507-18512 (2001).
28. Bornfeldt, K. E. et al. Sphingosine-1-phosphate inhibits PDGF-induced chemotaxis of human arterial smooth muscle cells: spatial and temporal modulation of PDGF chemotactic signal transduction. J. Cell Biol. 130, 193-206 (1995).
29. Spiegel, S. & Milstien, S. Sphingosine-1-phosphate: signaling inside and out. FEBS Lett. 476, 55-57 (2000).
30. Hannun, Y. A., Luberto, C. & Argraves, K. M. Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry 40, 4893-4903 (2001).
31. Kuehnel, M. P. et al. Characterization of the intracellular survival of Mycobacterium avium ssp. paratuberculosis: phagosomal pH and fusogenicity in J774 macrophages compared with other mycobacteria. Cell Microbiol. 3, 551-566 (2001).
32. Guerin, I. & de Chastellier, C. Pathogenic mycobacteria disrupt the macrophage actin filament network. Infect. Immun. 68, 2655-2662 (2000).
33. Sturgill-Koszycki, S., Haddix, P. L. & Russell, D. G. The interaction between Mycobacterium and the macrophage analyzed by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis 18, 2558-2565 (1997).
34. +-ATPases. J. Biol. Chem. 272, 29810-29820 (1997).
35. Sturgill-Koszycki, S. et al. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681 (1994).
36. Goni, F. M. & Alonso, A. Structure and functional properties of diacylglycerols in membranes. Prog. Lipid Res. 38, 1-48 (1999).
37. Paul, K. P. et al. Influence of n-6 and n-3 polyunsaturated fatty acids on the resistance to experimental tuberculosis. Metabolism 46, 619-624 (1997).
38. Chang, H. R. et al. Fish oil decreases natural resistance of mice to infection with Salmonella typhimurium. Metabolism 41, 1-2 (1992).
39. Kaplan, G. J., Fraser, R. I. & Comstock, G. W. Tuberculosis in Alaska. Am. Rev. Respir. Disease 105, 920-926 (1970).
40. Bang, H. O. & Dyerberg, J. Lipid metabolism and ischemic heart disease in Greenland Eskimos. Adv. Nutr. Res. 3, 1-22 (1980).
41. Snapper, S. B., Melton, R. E., Mustafa, S., Kieser, T. & Jacobs, W. R. Jr. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4, 1911-1199 (1990).