Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process

Journal of Cell Biology

Volumn 160, Issue 3, 2003, Pages 321-328

  Abrami, Laurence ^a   Liu, Shihui ^b   Cosson, Pierre ^a   Leppla, Stephen H ^b   Van der Goot, F Gisou ^a,c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c Dept of Genetics ^*  (Switzerland)

Author keywords

Anthrax toxin; Clustering; Microdomains; Protective antigen; Rafts

Indexed keywords

ANTHRAX TOXIN; CELL SURFACE RECEPTOR; CHOLESTEROL; CLATHRIN; DYNAMIN; GLYCOSPHINGOLIPID; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CYTOPLASM; ENDOCYTOSIS; ENZYME DEGRADATION; GENE CLUSTER; GENE TARGETING; INTERNALIZATION; LETHAL GENE; LIPID MEMBRANE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTHRAX; ANTIBODIES; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CAVEOLIN 1; CAVEOLINS; CHO CELLS; CLATHRIN; CRICETINAE; DYNAMINS; ENDOCYTOSIS; EUKARYOTIC CELLS; MACROMOLECULAR SUBSTANCES; MAP KINASE KINASE 1; MEMBRANE MICRODOMAINS; MICROSCOPY, ELECTRON; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, PEPTIDE; TRANSPORT VESICLES;

ANIMALIA; ANTHRAX; POSIBACTERIA;

EID: 0037415611     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200211018     Document Type: Article

References (45)

1. Abrami, L., and F.G. van der Goot. 1999. Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J. Cell Biol. 147:175-184.
2. Abrami, L., M. Fivaz, and F.G. van Der Goot. 2000. Adventures of a pore-forming toxin at the target cell surface. Trends Microbiol. 8:168-172.
3. Beauregard, K.E., S. Wimer-Mackin, R.J. Collier, and W.I. Lencer. 1999. Anthrax toxin entry into polarized epithelial cells. Infect. Immun. 67:3026-3030.
4. Beauregard, K.E., R.J. Collier, and J.A. Swanson. 2000. Proteolytic activation of receptor-bound anthrax protective antigen on macrophages promotes its internalization. Cell Microbiol. 2:251-258.
5. Benmerah, A., M. Bayrou, N. Cerf-Bensussan, and A. Dautry-Varsat. 1999. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112:1303-1311.
6. Bickel, P.E., P.E. Scherer, J.E. Schnitzer, P. Oh, M.P. Lisanti, and H.F. Lodish. 1997. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272:13793-13802.
7. Bradley, K.A., J. Mogridge, M. Mourez, R.J. Collier, and J.A. Young. 2001. Identification of the cellular receptor for anthrax toxin. Nature. 414:225-229.
8. Brown, D.A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
9. Chapman, R.E., and S. Munro. 1994. Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO J. 13:2305-2312.
10. Chaudry, G.J., M. Moayeri, S. Liu, and S.H. Leppla. 2002. Quickening the pace of anthrax research: three advances point towards possible therapies. Trends Microbiol. 10:58-62.
11. Cheng, P.C., M.L. Dykstra, R.N. Mitchell, and S.K. Pierce. 1999. A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J. Exp. Med. 190:1549-1560.
12. Cunningham, K., D.B. Lacy, J. Mogridge, and R.J. Collier. 2002. Mapping the lethal factor and edema factor binding sites on oligomeric anthrax protective antigen. Proc. Natl. Acad. Sci. USA. 99:7049-7053.
13. Damke, H., T. Baba, D.E. Warnock, and S.L. Schmid. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:915-934.
14. Duesbery, N.S., C.P. Webb, S.H. Leppla, V.M. Gordon, K.R. Klimpel, T.D. Copeland, N.G. Ahn, M.K. Oskarsson, K. Fukasawa, K.D. Paull, and G.F. Vande Woude. 1998. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science. 280:734-737.
15. Fivaz, M., L. Abrami, and F.G. van der Goot. 1999. Landing on lipid rafts. Trends Cell Biol. 9:212-213.
16. Fivaz, M., F. Vilbois, S. Thurnheer, C. Pasquali, L. Abrami, P.E. Bickel, R.G. Parton, and and F.G. van der Goot. 2002. Different sorting and fate of endocytosed GPI-anchored proteins. EMBO J. 21:3989-4000.
17. Gordon, V.M., K.R. Klimpel, N. Arora, M.A. Henderson, and S.H. Leppla. 1995. Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect. Immun. 63:82-87.
18. Hanada, K., T. Hara, M. Nishijima, O. Kuge, R.C. Dickson, and M.M. Nagiec. 1997. A mammalian homolog of the yeast LCB1 encodes a component of serine palmitoyltransferase, the enzyme catalyzing the first step in sphingolipid synthesis. J. Biol. Chem. 272:32108-32114.
19. Hanada, K., T. Hara, M. Fukasawa, A. Yamaji, M. Umeda, and M. Nishijima. 1998. Mammalian cell mutants resistant to a sphingomyelin-directed cytolysin. Genetic and biochemical evidence for complex formation of the LCB1 protein with the LCB2 protein for serine palmitoyltransferase. J. Biol. Chem. 273:33787-33794.
20. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929-942.
21. Kiss, A.L., A. Turi, N. Mullner, and J. Timar. 2000. Caveolin isoforms in resident and elicited rat peritoneal macrophages. Eur. J. Cell Biol. 79:343-349.
22. Kurzchalia, T.V., and R.G. Parton. 1999. Membrane microdomains and caveolae. Curr. Opin. Cell Biol. 11:424-431.
23. Lafont, F., G. Tran Van Nhieu, K. Hanada, P.J. Sansonetti, and F.G. van der Goot. 2002. Initial steps of Shigella infection depend on the cholesterol/sphingolipid raft-mediated CD44-IpaB interaction. EMBO J. 21:4449-4457.
24. Leppla, S.H. 1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. USA. 79:3162-3166.
25. Leppla, S.H. 1988. Production and purification of anthrax toxin. Methods Enzymol. 165:103-116.
26. Leppla, S.H. 1991. The anthrax toxin complex. In Sourcebook of Bacterial Protein Toxins. J.E. Alouf and J.H. Freer, editors. Academic Press, New York. 277-302.
27. Liu, S., and S.H. Leppla. 2003. Cell surface tumor endothelium marker 8 cytoplasmic tail-independent anthrax toxin binding, proteolytic processing, oligomer formation and internalization. J. Biol. Chem. In press.
28. Liu, S., T.H. Bugge, and S.H. Leppla. 2001. Targeting of tumor cells by cell surface urokinase plasminogen activator-dependent anthrax toxin. J. Biol. Chem. 276:17976-17984.
29. Maxfield, F.R., and S. Mayor. 1997. Cell surface dynamics of GPI-anchored proteins. Adv. Exp. Med. Biol. 419:355-364.
30. McNiven, M.A., L. Kim, E.W. Krueger, J.D. Orth, H. Cao, and T.W. Wong. 2000. Regulated interactions between dynamin and the actin-binding prorein corractin modulate cell shape. J. Cell Biol. 151:187-198.
31. Milne, J.C., D. Furlong, P.C. Hanna, J.S. Wall, and R.J. Collier. 1994. Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J. Biol. Chem. 269:20607-20612.
32. Mogridge, J., M. Mourez, and R.J. Collier. 2001. Involvement of domain 3 in oligomerization by the protective antigen moiety of anthrax toxin. J. Bacteriol. 183:2111-2116.
33. Mourez, M., D.B. Lacy, K. Cunningham, R. Legmann, B.R. Sellman, J. Mogridge, and R.J. Collier. 2002. 2001: a year of major advances in anthrax toxin research. Trends Microbiol. 10:287-293.
34. Pelkmans, L., and A. Helenius. 2002. Endocytosis via caveolae. Traffic. 3:311-320.
35. Pelkmans, L., J. Kartenbeck, and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:473-483.
36. Petosa, C., R.J. Collier, K.R. Klimpel, S.H. Leppla, and R.C. Liddington. 1997. Crystal structure of the anthrax toxin protective antigen. Nature. 385:833-838.
37. Simons, K., and E. Ikonen. 1997. Functiomal rafts in cell membranes. Nature. 387:569-572.
38. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
39. Singh, Y., K.R. Klimpel, N. Arora, M. Sharma, and S.H. Leppla. 1994. The chymotrypsin-sensitive site, FFD315, in anthrax toxin protective antigen is required for translocation of lethal factor. J. Biol. Chem. 269:29039-29046.
40. St. Croix, B., C. Rago, V. Velculescu, G. Traverso, K.E. Romans, E. Montgomery, A. Lal, G.J. Riggins, C. Lengauer, B. Vogelstein, and K.W. Kinzler. 2000. Genes expressed in human tumor endothelium. Science. 289:1197-1202.
41. Stoddart, A., M.L. Dykstra, B.K. Brown, W. Song, S.K. Pierce, and F.M. Brodsky. 2002. Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity. 17:451-462.
42. Tang, G., and S.H. Leppla. 1999. Proteasome activity is required for anthrax lethal toxin to kill macrophages. Infect. Immun. 67:3055-3060.
43. Vitale, G., R. Pellizzari, C. Recchi, G. Napolitani, M. Mock, and C. Montecucco. 1998. Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem. Biophys. Res. Commun. 248:706-711.
44. Vitale, G., L. Bernardi, G. Napolirani, M. Mock, and C. Montecucco. 2000. Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem. J. 352:739-745.
45. Zurzolo, C., W. van't Hof, G. van Meer, and E. Rodriguez-Boulan. 1994. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J. 13:42-53.