Electrostatic ratchet in the protective antigen channel promotes anthrax toxin translocation

Journal of Biological Chemistry

Volumn 287, Issue 52, 2012, Pages 43753-43764

  Wynia Smith, Sarah L ^a   Brown, Michael J ^b   Chirichella, Gina ^b   Kemalyan, Gigi ^b   Krantz, Bryan A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC RESIDUES; ANTHRAX TOXINS; CHARGED RESIDUES; CHARGED SURFACES; CYTOSOLS; EDEMA FACTORS; ELECTRICAL POTENTIAL; HOST CELLS; LETHAL FACTOR; MOLECULAR MOTORS; NONEQUILIBRIUM FLUCTUATIONS; PROTECTIVE ANTIGENS; PROTEIN TRANSLOCATION; PROTON-MOTIVE FORCES; RATCHET MECHANISMS; SIMILAR SOLUTION; TRANSLOCASES; TRANSMEMBRANES; TRANSPORT SUBSTRATES;

ANTIGENS; CHARGED PARTICLES; DISEASES; ELECTROSTATICS; PROTEINS;

TOXIC MATERIALS;

ANTHRAX TOXIN; ANTIGEN; PROTECTIVE ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRIC FIELD; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; LETHAL GENE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; PROTEIN UNFOLDING; PROTON MOTIVE FORCE; RESIDUE ANALYSIS; SEQUENCE HOMOLOGY; STATIC ELECTRICITY; SURFACE CHARGE; THERMODYNAMICS;

ANTIGENS, BACTERIAL; BACTERIAL TOXINS; KINETICS; MEMBRANES, ARTIFICIAL; MODELS, CHEMICAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTON-MOTIVE FORCE; STATIC ELECTRICITY;

EID: 84871545524     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.419598     Document Type: Article

References (43)

1. Thoren, K. L., and Krantz, B. A. (2011) The unfolding story of anthrax toxin translocation. Mol. Microbiol. 80, 588-595
2. Feld, G. K., Brown, M. J., and Krantz, B. A. (2012) Ratcheting up protein translocation with anthrax toxin. Protein Sci. 21, 606-624
3. Wickner, W., and Schekman, R. (2005) Protein translocation across biological membranes. Science 310, 1452-1456 (Pubitemid 41746334)
4. Feld, G. K., Thoren, K. L., Kintzer, A. F., Sterling, H. J., Tang, I. I, Greenberg, S. G., Williams, E. R., and Krantz, B. A. (2010) Structural basis for the unfolding of anthrax lethal factor by protective antigen oligomers. Nat. Struct. Mol. Biol. 17, 1383-1390
5. Kintzer, A. F., Thoren, K. L., Sterling, H. J., Dong, K. C., Feld, G. K., Tang, I. I., Zhang, T. T., Williams, E. R., Berger, J. M., and Krantz, B. A. (2009) The protective antigen component of anthrax toxin forms functional octameric complexes. J. Mol. Biol. 392, 614-629
6. Krantz, B. A., Finkelstein, A., and Collier, R. J. (2006) Protein translocation through the anthrax toxin transmembrane pore is driven by a proton gradient. J. Mol. Biol. 355, 968-979 (Pubitemid 43012140)
7. Krantz, B. A., Melnyk, R. A., Zhang, S., Juris, S. J., Lacy, D. B., Wu, Z., Finkelstein, A., and Collier, R. J. (2005) A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309, 777-781 (Pubitemid 41077325)
8. Thoren, K. L., Worden, E. J., Yassif, J. M., and Krantz, B. A. (2009) Lethal factor unfolding is the most force-dependent step of anthrax toxin translocation. Proc. Natl. Acad. Sci. U.S.A. 106, 21555-21560
9. Brown, M. J., Thoren, K. L., and Krantz, B. A. (2011) Charge requirements for proton gradient-driven translocation of anthrax toxin. J. Biol. Chem. 286, 23189-23199
10. Galán, J. E., and Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567-573 (Pubitemid 44864429)
11. Tsai, B., Ye, Y., and Rapoport, T. A. (2002) Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol. 3, 246-255 (Pubitemid 34619260)
12. Ruiz, N., Kahne, D., and Silhavy, T. J. (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4, 57-66 (Pubitemid 43135287)
13. Egea, P. F., Stroud, R. M., and Walter, P. (2005) Targeting proteins to membranes. Structure of the signal recognition particle. Curr. Opin. Struct. Biol. 15, 213-220
14. Collier, R. J. (2009) Membrane translocation by anthrax toxin. Mol. Aspects Med. 30, 413-422
15. Zhang, S., Udho, E., Wu, Z., Collier, R. J., and Finkelstein, A. (2004) Protein translocation through anthrax toxin channels formed in planar lipid bilayers. Biophys. J. 87, 3842-3849 (Pubitemid 39602890)
16. Pentelute, B. L., Sharma, O., and Collier, R. J. (2011) Chemical dissection of protein translocation through the anthrax toxin pore. Angew. Chem. Int. Ed. Engl. 50, 2294-2296
17. Pentelute, B. L., Barker, A. P., Janowiak, B. E., Kent, S. B., and Collier, R. J. (2010) A semisynthesis platform for investigating structure-function relationships in the N-terminal domain of the anthrax Lethal Factor. ACS Chem. Biol. 5, 359-364
18. Basilio, D., Juris, S. J., Collier, R. J., and Finkelstein, A. (2009) Evidence for a proton-protein symport mechanism in the anthrax toxin channel. J. Gen. Physiol. 133, 307-314
19. Katayama, H., Janowiak, B. E., Brzozowski, M., Juryck, J., Falke, S., Gogol, E. P., Collier, R. J., and Fisher, M. T. (2008) GroEL as a molecular scaffold for structural analysis of the anthrax toxin pore. Nat. Struct. Mol. Biol. 15, 754-760 (Pubitemid 351932002)
20. Lacy, D. B., Wigelsworth, D. J., Melnyk, R. A., Harrison, S. C., and Collier, R. J. (2004) Structure of heptameric protective antigen bound to an anthrax toxin receptor.Arole for receptor in pH-dependent pore formation. Proc. Natl. Acad. Sci. U.S.A. 101, 13147-13151 (Pubitemid 39209633)
21. Petosa, C., Collier, R. J., Klimpel, K. R., Leppla, S. H., and Liddington, R. C. (1997) Crystal structure of the anthrax toxin protective antigen. Nature 385, 833-838 (Pubitemid 27106075)
22. Kintzer, A. F., Sterling, H. J., Tang, I. I., Williams, E. R., and 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
23. Kintzer, A. F., Sterling, H. J., Tang, I. I., Abdul-Gader, A., Miles, A. J., Wallace, B. A., Williams, E. R., and Krantz, B. A. (2010) Role of the protective antigen octamer in the molecular mechanism of anthrax lethal toxin stabilization in plasma. J. Mol. Biol. 399, 741-758
24. Pannifer, A. D., Wong, T. Y., Schwarzenbacher, R., Renatus, M., Petosa, C., Bienkowska, J., Lacy, D. B., Collier, R. J., Park, S., Leppla, S. H., Hanna, P., and Liddington, R. C. (2001) Crystal structure of the anthrax lethal factor. Nature 414, 229-233 (Pubitemid 33051240)
25. Drum, C. L., Yan, S. Z., Bard, J., Shen, Y. Q., Lu, D., Soelaiman, S., Grabarek, Z., Bohm, A., and Tang, W. J. (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415, 396-402 (Pubitemid 34100945)
26. Shen, Y., Zhukovskaya, N. L., Guo, Q., Florián, J., and Tang, W. J. (2005) Calcium-independent calmodulin binding and two-metal-ion catalytic mechanism of anthrax edema factor. EMBO J. 24, 929-941 (Pubitemid 40470142)
27. Blaustein, R. O., Koehler, T. M., Collier, R. J., and Finkelstein, A. (1989) Anthrax toxin. Channel-forming activity of protective antigen in planar phospholipid bilayers. Proc. Natl. Acad. Sci. U.S.A. 86, 2209-2213 (Pubitemid 19102481)
28. Benson, E. L., Huynh, P. D., Finkelstein, A., and Collier, R. J. (1998) Identification of residues lining the anthrax protective antigen channel. Biochemistry 37, 3941-3948 (Pubitemid 28162951)
29. Nassi, S., Collier, R. J., and Finkelstein, A. (2002) PA63 channel of anthrax toxin: an extended β-barrel. Biochemistry 41, 1445-1450 (Pubitemid 34112732)
30. Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J. E. (1996) Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866 (Pubitemid 26424757)
31. Krantz, B. A., Trivedi, A. D., Cunningham, K., Christensen, K. A., and Collier, R. J. (2004) Acid-induced unfolding of the amino-terminal domains of the lethal and edema factors of anthrax toxin. J. Mol. Biol. 344, 739-756 (Pubitemid 39469217)
32. Vernier, G., Wang, J., Jennings, L. D., Sun, J., Fischer, A., Song, L., and Collier, R. J. (2009) Solubilization and characterization of the anthrax toxin pore in detergent micelles. Protein Sci. 18, 1882-1895
33. Mueller, P., Rudin, D. O., Tien, H. T., and Westcott, W. C. (1963) Methods for the formation of single bimolecular lipid membranes in aqueous solution. J. Phys. Chem. 67, 534-535
34. Robinson, R. A., and Stokes, R. H. (2002) Electrolyte Solutions, 2nd Ed., Dover, Mineola, NY
35. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera.Avisualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
36. Emsley, P., and Cowtan, K. (2004) COOT. Model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (Pubitemid 41742764)
37. Lacy, D. B., Mourez, M., Fouassier, A., and Collier, R. J. (2002) Mapping the anthrax protective antigen binding site on the lethal and edema factors. J. Biol. Chem. 277, 3006-3010 (Pubitemid 34953337)
38. Zhang, S., Finkelstein, A., and Collier, R. J. (2004) Evidence that translocation of anthrax toxin's lethal factor is initiated by entry of its N terminus into the protective antigen channel. Proc. Natl. Acad. Sci. U.S.A. 101, 16756-16761 (Pubitemid 39601311)
39. Woodhull, A. M. (1973) Ionic blockage of sodium channels in nerve. J. Gen. Physiol. 61, 687-708
40. Levinthal, C. (1968) Are there pathways for protein folding? J. Chim. Phys. 65, 44-45
41. Blanke, S. R., Milne, J. C., Benson, E. L., and Collier, R. J. (1996) Fused polycationic peptide mediates delivery of diphtheria toxin A chain to the cytosol in the presence of anthrax protective antigen. Proc. Natl. Acad. Sci. U.S.A. 93, 8437-8442 (Pubitemid 26269576)
42. Feld, G. K., Kintzer, A. F., Tang, I. I., Thoren, K. L., and Krantz, B. A. (2012) Domain flexibility modulates the heterogeneous assembly mechanism of anthrax toxin protective antigen. J. Mol. Biol. 415, 159-174
43. Katayama, H., Wang, J., Tama, F., Chollet, L., Gogol, E. P., Collier, R. J., and Fisher, M. T. (2010) Three-dimensional structure of the anthrax toxin pore inserted into lipid nanodiscs and lipid vesicles. Proc. Natl. Acad. Sci. U.S.A. 107, 3453-3457