Domain flexibility modulates the heterogeneous assembly mechanism of anthrax toxin protective antigen

Journal of Molecular Biology

Volumn 415, Issue 1, 2012, Pages 159-174

  Feld, Geoffrey K ^a   Kintzer, Alexander F ^a   Tang, Iok I ^b   Thoren, Katie L ^a   Krantz, Bryan A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

anthrax toxin; anthrax toxin receptor; furin; macromolecular assembly

Indexed keywords

ANTHRAX TOXIN; ANTIGEN; FURIN; OLIGOMER; PROTECTIVE ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; CROSS LINKING; CRYSTAL STRUCTURE; ENZYME STRUCTURE; PRIORITY JOURNAL; STOICHIOMETRY; X RAY CRYSTALLOGRAPHY;

EID: 84855254449     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.10.035     Document Type: Article

References (78)

1. Young, J. A. & Collier, R. J. (2007). Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76, 243-265.
2. Thoren, K. L. & Krantz, B. A. (2011). The unfolding story of anthrax toxin translocation. Mol. Microbiol. 80, 588-595.
3. Smith, H. & Keppie, J. (1954). Observations on experimental anthrax: demonstration of a specific lethal factor produced in vivo by Bacillus anthracis. Nature, 173, 689.
4. Stanley, J. L. & Smith, H. (1961). Purification of factor I and recognition of a third factor of the anthrax toxin. J. Gen. Microbiol. 26, 49-66.
5. Beall, F. A., Taylor, M. J. & Thorne, C. B. (1962). Rapid lethal effects of a third factor of anthrax toxin. J. Bacteriol. 83, 1274-1280.
6. Duesbery, N. S. & Vande Woude, G. F. (1999). Anthrax lethal factor causes proteolytic inactivation of mitogen-activated protein kinase kinase. J. Appl. Microbiol. 87, 289-293.
7. Duesbery, N. S., Webb, C. P., Leppla, S. H., Gordon, V. M., Klimpel, K. R., Copeland, T. D. et al. (1998). Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science, 280, 734-737.
8. Pannifer, A. D., Wong, T. Y., Schwarzenbacher, R., Renatus, M., Petosa, C., Bienkowska, J. et al. (2001). Crystal structure of the anthrax lethal factor. Nature, 414, 229-233.
9. Pezard, C., Berche, P. & Mock, M. (1991). Contribution of individual toxin components to virulence of Bacillus anthracis. Infect. Immun. 59, 3472-3477.
10. 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.
11. Leppla, S. H. (1984). Bacillus anthracis calmodulin-dependent adenylate cyclase: chemical and enzymatic properties and interactions with eucaryotic cells. Adv. Cyclic Nucleotide Protein Phosphorylation Res. 17, 189-198.
12. Drum, C. L., Yan, S. Z., Bard, J., Shen, Y. Q., Lu, D., Soelaiman, S. et al. (2002). Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature, 415, 396-402.
13. Kintzer, A. F., Sterling, H. J., Tang, I. I., Abdul-Gader, A., Miles, A. J., Wallace, B. A. et al. (2010). Role of the protective antigen octamer in the molecular mechanism of anthrax lethal toxin stabilization in plasma. J. Mol. Biol. 399, 741-758.
14. Kintzer, A. F., Thoren, K. L., Sterling, H. J., Dong, K. C., Feld, G. K., Tang, I. I. et al. (2009). The protective antigen component of anthrax toxin forms functional octameric complexes. J. Mol. Biol. 392, 614-629.
15. Bradley, K. A., Mogridge, J., Mourez, M., Collier, R. J. & Young, J. A. (2001). Identification of the cellular receptor for anthrax toxin. Nature, 414, 225-229.
16. Scobie, H. M., Rainey, G. J. A., Bradley, K. A. &Young, J. A. (2003). Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc. Natl Acad. Sci. USA, 100, 5170-5174.
17. Santelli, E., Bankston, L. A., Leppla, S. H. &Liddington, R. C. (2004). Crystal structure of a complex between anthrax toxin and its host cell receptor. Nature, 430, 905-908.
18. Lacy,D. B.,Wigelsworth, D. J.,Melnyk, R. A.,Harrison, S. C. & Collier, R. J. (2004). Structure of heptameric protective antigen bound to an anthrax toxin receptor: a role for receptor in pH-dependent pore formation. Proc. Natl Acad. Sci. USA, 101, 13147-13151.
19. Wigelsworth, D. J., Krantz, B. A., Christensen, K. A., Lacy, D. B., Juris, S. J. & Collier, R. J. (2004). Binding stoichiometry and kinetics of the interaction of a human anthrax toxin receptor, CMG2, with protective antigen. J. Biol. Chem. 279, 23349-23356.
20. Lacy, D. B., Wigelsworth, D. J., Scobie, H. M., Young, J. A. & Collier, R. J. (2004). Crystal structure of the von Willebrand factor A domain of human capillary morphogenesis protein 2: an anthrax toxin receptor. Proc. Natl Acad. Sci. USA, 101, 6367-6372.
21. Scobie, H. M., Wigelsworth, D. J., Marlett, J. M., Thomas, D., Rainey, G. J., Lacy, D. B. et al. (2006). Anthrax toxin receptor 2-dependent lethal toxin killing in vivo. PLoS Pathog. 2, e111.
22. Milne, J. C., Furlong, D., Hanna, P. C., Wall, J. S. &Collier, R. J. (1994). Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J. Biol. Chem. 269, 20607-20612.
23. Petosa, C., Collier, R. J., Klimpel, K. R., Leppla, S. H. &Liddington, R. C. (1997). Crystal structure of the anthrax toxin protective antigen. Nature, 385, 833-838.
24. Feld, G. K., Thoren, K. L., Kintzer, A. F., Sterling, H. J., Tang, I. I., Greenberg, S. G. et al. (2010). Structural basis for the unfolding of anthrax lethal factor by protective antigen oligomers. Nat. Struct. Mol. Biol. 17, 1383-1390.
25. Abrami, L., Liu, S., Cosson, P., Leppla, S. H. & van der Goot, F. G. (2003). Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J. Cell Biol. 160, 321-328.
26. Friedlander, A. M. (1986). Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J. Biol. Chem. 261, 7123-7126.
27. Miller, C. J., Elliott, J. L. & Collier, R. J. (1999). Anthrax protective antigen: prepore-to-pore conversion. Biochemistry, 38, 10432-10441.
28. Katayama, H., Janowiak, B. E., Brzozowski, M., Juryck, J., Falke, S., Gogol, E. P. et al. (2008). GroEL as a molecular scaffold for structural analysis of the anthrax toxin pore. Nat. Struct. Mol. Biol. 15, 754-760.
29. Blaustein, R. O., Koehler, T. M., Collier, R. J. &Finkelstein, A. (1989). Anthrax toxin: channel-forming activity of protective antigen in planar phospholipid bilayers. Proc. Natl Acad. Sci. USA, 86, 2209-2213.
30. Mogridge, J., Mourez, M. & Collier, R. J. (2001). Involvement of domain 3 in oligomerization by the protective antigen moiety of anthrax toxin. J. Bacteriol. 183, 2111-2116.
31. Steiner, D. F. (1998). The proprotein convertases. Curr. Opin. Chem. Biol. 2, 31-39.
32. Nakayama, K. (1997). Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem. J. 327, 625-635.
33. Henrich, S., Cameron, A., Bourenkov, G. P., Kiefersauer, R., Huber, R., Lindberg, I. et al. (2003). The crystal structure of the proprotein processing proteinase furin explains its stringent specificity. Nat. Struct. Biol. 10, 520-526.
34. Thomas, G. (2002). Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3, 753-766.
35. Holyoak, T., Wilson, M. A., Fenn, T. D., Kettner, C. A., Petsko, G. A., Fuller, R. S. & Ringe, D. (2003). 2.4 Åresolution crystal structure of the prototypical hormone-processing protease Kex2 in complex with an Ala-Lys-Arg boronic acid inhibitor. Biochemistry, 42, 6709-6718.
36. 2+-dependent serine protease. Proc. Natl Acad. Sci. USA, 86, 1434-1438.
37. Fuller, R. S., Brake, A. J. & Thorner, J. (1989). Intracellular targeting and structural conservation of a prohormone-processing endoprotease. Science, 246, 482-486.
38. Remacle, A. G., Shiryaev, S. A., Oh, E. S., Cieplak, P., Srinivasan, A., Wei, G. et al. (2008). Substrate cleavage analysis of furin and related proprotein convertases. A comparative study. J. Biol. Chem. 283, 20897-20906.
39. Molloy, S. S., Thomas, L., VanSlyke, J. K., Stenberg, P. E. & Thomas, G. (1994). Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J. 13, 18-33.
40. Gordon, V. M. & Leppla, S. H. (1994). Proteolytic activation of bacterial toxins: role of bacterial and host cell proteases. Infect. Immun. 62, 333-340.
41. Molloy, S. S., Bresnahan, P. A., Leppla, S. H., Klimpel, K. R. & Thomas, G. (1992). Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267, 16396-16402.
42. Garred, O., van Deurs, B. & Sandvig, K. (1995). Furin-induced cleavage and activation of Shiga toxin. J. Biol. Chem. 270, 10817-10821.
43. Tsuneoka, M., Nakayama, K., Hatsuzawa, K., Komada, M., Kitamura, N. & Mekada, E. (1993). Evidence for involvement of furin in cleavage and activation of diphtheria toxin. J. Biol. Chem. 268, 26461-26465.
44. Gordon, V. M., Benz, R., Fujii, K., Leppla, S. H. &Tweten, R. K. (1997). Clostridium septicum alpha-toxin is proteolytically activated by furin. Infect. Immun. 65, 4130-4134.
45. Abrami, L., Fivaz, M., Decroly, E., Seidah, N. G., Jean, F., Thomas, G. et al. (1998). The pore-forming toxin proaerolysin is activated by furin. J. Biol. Chem. 273, 32656-32661.
46. Stieneke-Grober, A., Vey, M., Angliker, H., Shaw, E., Thomas, G., Roberts, C. et al. (1992). Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 11, 2407-2414.
47. Hallenberger, S., Bosch, V., Angliker, H., Shaw, E., Klenk, H. D. & Garten, W. (1992). Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature, 360, 358-361.
48. Stadler, K., Allison, S. L., Schalich, J. & Heinz, F. X. (1997). Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71, 8475-8481.
49. Volchkov, V. E., Feldmann, H., Volchkova, V. A. &Klenk, H. D. (1998). Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc. Natl Acad. Sci. USA, 95, 5762-5767.
50. Remacle, A. G., Gawlik, K., Golubkov, V. S., Cadwell, G. W., Liddington, R. C., Cieplak, P. et al. (2010). Selective and potent furin inhibitors protect cells from anthrax without significant toxicity. Int. J. Biochem. Cell Biol. 42, 987-995.
51. Sarac, M. S., Peinado, J. R., Leppla, S. H. & Lindberg, I. (2004). Protection against anthrax toxemia by hexa-D-arginine in vitro and in vivo. Infect. Immun. 72, 602-605.
52. Komiyama, T., Swanson, J. A. & Fuller, R. S. (2005). Protection from anthrax toxin-mediated killing of macrophages by the combined effects of furin inhibitors and chloroquine. Antimicrob. Agents Chemother. 49, 3875-3882.
53. Oliva, R., Leone, M., Falcigno, L., D'Auria, G., Dettin, M., Scarinci, C. et al. (2002). Structural investigation of the HIV-1 envelope glycoprotein gp160 cleavage site. Chemistry, 8, 1467-1473.
54. Wimalasena, D. S., Janowiak, B. E., Lovell, S., Miyagi, M., Sun, J., Zhou, H. et al. (2010). Evidence that histidine protonation of receptor-bound anthrax protective antigen is a trigger for pore formation. Biochemistry, 49, 6973-6983.
55. Yin, L., Krantz, B., Russell, N. S., Deshpande, S. &Wilkinson, K. D. (2000). Nonhydrolyzable diubiquitin analogues are inhibitors of ubiquitin conjugation and deconjugation. Biochemistry, 39, 10001-10010.
56. Kintzer, A. F., Sterling, H. J., Tang, I. I., Williams, E. R. & Krantz, B. A. (2010). Anthrax toxin receptor drives protective antigen oligomerization and stabilizes the heptameric and octameric oligomer by a similar mechanism. PLoS One, 5, e13888.
57. Christensen, K. A., Krantz, B. A., Melnyk, R. A. &Collier, R. J. (2005). Interaction of the 20 kDa and 63 kDa fragments of anthrax protective antigen: kinetics and thermodynamics. Biochemistry, 44, 1047-1053.
58. Ramachandran, G. N. & Sasisekharan, V. (1968). Conformation of polypeptides and proteins. Adv. Protein Chem. 23, 283-438.
59. Murray, E. J., Leaman, D. P., Pawa, N., Perkins, H., Pickford, C., Perros, M. et al. (2010). A low-molecular-weight entry inhibitor of both CCR5- and CXCR4-tropic strains of human immunodeficiency virus type 1 targets a novel site on gp41. J. Virol. 84, 7288-7299.
60. Lacy, D. B., Mourez, M., Fouassier, A. & Collier, R. J. (2002). Mapping the anthrax protective antigen binding site on the lethal and edema factors. J. Biol. Chem. 277, 3006-3010.
61. Jancarik, J. & Kim, S. H. (1991). Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallogr. 24, 409-411.
62. McPherson, A., Jr. (1976). The growth and preliminary investigation of protein and nucleic acid crystals for X-ray diffraction analysis. Methods Biochem. Anal. 23, 249-345.
63. MacDowell, A. A., Celestre, R. S., Howells, M., McKinney, W., Krupnick, J., Cambie, D. et al. (2004). Suite of three protein crystallography beamlines with single superconducting bend magnet as the source. J. Synchrotron Radiat. 11, 447-455.
64. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. In Methods in EnzymologyMacromolecular Crystallography, Part A (Carter, C. W. & Sweet, R. M., eds), Macromolecular Crystallography, Part A, vol. 276, pp. 307-326 Academic Press, Inc., New York, NY.
65. Storoni, L. C., McCoy, A. J. & Read, R. J. (2004). Likelihood-enhanced fast rotation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 432-438.
66. Emsley, P. & Cowtan, K. (2004). COOT: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132.
67. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N. et al. (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221.
68. Lang, P. T., Ng, H. L., Fraser, J. S., Corn, J. E., Echols, N., Sales, M. et al. (2010). Automated electron-density sampling reveals widespread conformational polymorphism in proteins. Protein Sci. 19, 1420-1431.
69. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X. et al. (2007). MolProbity: allatom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383.
70. Laskowski, R. A., MacArthur, M. W., Moss, D. S. &Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
71. Collaborative Computational Project (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763.
72. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. & Ferrin, T. E. (2004). UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
73. Christensen, K. A., Krantz, B. A. & Collier, R. J. (2006). Assembly and disassembly kinetics of anthrax toxin complexes. Biochemistry, 45, 2380-2386.
74. Ludtke, S. J., Baldwin, P. R. & Chiu, W. (1999). EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97.
75. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M. & Leith, A. (1996). SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199.
76. Stark, H., Mueller, F., Orlova, E. V., Schatz, M., Dube, P., Erdemir, T. et al. (1995). The 70S Escherichia coli ribosome at 23 Å resolution: fitting the ribosomal RNA. Structure, 3, 815-821.
77. van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R. &Schatz, M. (1996). A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24.
78. White, H. E., Saibil, H. R., Ignatiou, A. & Orlova, E. V. (2004). Recognition and separation of single particles with size variation by statistical analysis of their images. J. Mol. Biol. 336, 453-460.