Atomic structure of anthrax protective antigen pore elucidates toxin translocation

Nature

Volumn 521, Issue 7553, 2015, Pages 545-549

  Jiang, Jiansen ^a   Pentelute, Bradley L ^b   Collier, R John ^c   Hong Zhou, Z ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; ANTHRAX VACCINE; PHENYLALANINE; BACTERIAL ANTIGEN; BACTERIAL TOXIN; ION CHANNEL;

ANTHRAX; ANTIGEN; CATALYSIS; MEMBRANE; PH; POROSITY; PROTEIN; TOXIN; TRANSLOCATION; VIRULENCE;

ANTHRAX; ANTIGEN STRUCTURE; ARTICLE; BACILLUS ANTHRACIS; BIOCHEMICAL ANALYSIS; CATALYSIS; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; EDEMA; ELECTRON; ELECTROPHYSIOLOGICAL PROCEDURES; LETHAL GENE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN LOCALIZATION; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; PROTEIN TRANSPORT; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

ANIMALIA; BACILLUS ANTHRACIS;

ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; BIOCATALYSIS; CRYOELECTRON MICROSCOPY; HYDROGEN-ION CONCENTRATION; ION CHANNELS; MODELS, MOLECULAR; PHENYLALANINE; PROTEIN CONFORMATION; PROTEIN TRANSPORT; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84930637225     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14247     Document Type: Article

References (49)

1. Young, J. A. & Collier, R. J. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76, 243-265 (2007).
2. Krantz, B. A. et al. A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309, 777-781 (2005).
3. Krantz, B. A., Finkelstein, A. &Collier, R. J. Protein translocation through the anthrax toxin transmembrane pore is driven by a proton gradient. J. Mol. Biol. 355, 968-979 (2006).
4. Basilio, D., Juris, S. J., Collier, R. J. & Finkelstein, A. Evidence for a proton-protein symport mechanism in the anthrax toxin channel. J. Gen. Physiol. 133, 307-314 (2009).
5. Janowiak, B. E., Fischer, A. & Collier, R. J. Effects of introducing a single charged residue into the phenylalanine clamp of multimeric anthrax protective antigen. J. Biol. Chem. 285, 8130-8137 (2010).
6. Basilio, D., Jennings-Antipov, L. D., Jakes, K. S. & Finkelstein, A. Trapping a translocating protein within the anthrax toxin channel: implications for the secondary structure of permeating proteins. J. Gen. Physiol. 137, 343-356 (2011).
7. Brown,M. J., Thoren, K. L. & Krantz, B. A. Charge requirements for proton gradientdriven translocation of anthrax toxin. J. Biol. Chem. 286, 23189-23199 (2011).
8. Wynia-Smith, S. L., Brown, M. J., Chirichella, G., Kemalyan, G. & Krantz, B. A. Electrostatic ratchet in the protective antigen channel promotes anthrax toxin translocation. J. Biol. Chem. 287, 43753-43764 (2012).
9. Feld, G. K., Brown, M. J. & Krantz, B. A. Ratcheting up protein translocation with anthrax toxin. Protein Sci. 21, 606-624 (2012).
10. Petosa, C., Collier, R. J., Klimpel, K. R., Leppla, S. H. & Liddington, R. C. Crystal structure of the anthrax toxin protective antigen. Nature 385, 833-838 (1997).
11. Santelli, E., Bankston, L. A., Leppla, S. H. & Liddington, R. C. Crystal structure of a complex between anthrax toxin and its host cell receptor. Nature 430, 905-908 (2004).
12. Lacy, D. B.,Wigelsworth,D. J.,Melnyk,R. A., Harrison, S. C. &Collier,R. J. 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 (2004).
13. Kintzer, A. F. et al. The protective antigen component of anthrax toxin forms functional octameric complexes. J. Mol. Biol. 392, 614-629 (2009).
14. Feld, G. K. et al. Structural basis for the unfolding of anthrax lethal factor by protective antigen oligomers. Nature Struct. Mol. Biol. 17, 1383-1390 (2010).
15. Vernier, G. et al. Solubilization and characterization of the anthrax toxin pore in detergent micelles. Protein Sci. 18, 1882-1895 (2009).
16. Sehnal, D. et al. MOLE 2. 0: advanced approach for analysis of biomacromolecular channels. J Cheminform. 5, 39 (2013).
17. Ziv, G., Haran, G. & Thirumalai, D. Ribosome exit tunnel can entropically stabilize alpha-helices. Proc. Natl Acad. Sci. USA 102, 18956-18961 (2005).
18. Voss, N. R., Gerstein, M., Steitz, T. A. & Moore, P. B. The geometry of the ribosomal polypeptide exit tunnel. J. Mol. Biol. 360, 893-906 (2006).
19. Killian, J. A. & von Heijne, G. How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 25, 429-434 (2000).
20. Wang, J., Vernier, G., Fischer, A. & Collier, R. J. Functions of phenylalanine residues within the beta-barrel stemof the anthrax toxin pore. PLoSONE 4, e6280 (2009).
21. Song, L. et al. Structure of staphylococcal a-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866 (1996).
22. De, S. &Olson,R. Crystal structure of the Vibrio cholerae cytolysin heptamer reveals common features among disparate pore-forming toxins. Proc. Natl Acad. Sci. USA 108, 7385-7390 (2011).
23. Sellman,B. R.,Nassi, S. &Collier,R. J. Pointmutations inanthrax protective antigen that block translocation. J. Biol. Chem. 276, 8371-8376 (2001).
24. Sellman, B. R., Mourez, M. & Collier, R. J. Dominant-negative mutants of a toxin subunit: an approach to therapy of anthrax. Science 292, 695-697 (2001).
25. Mourez, M. et al. Mapping dominant-negative mutations of anthrax protective antigen by scanning mutagenesis. Proc. Natl Acad. Sci. USA 100, 13803-13808 (2003).
26. Melnyk, R. A. & Collier, R. J. A loop network within the anthrax toxin pore positions the phenylalanine clamp in an active conformation. Proc. Natl Acad. Sci. USA 103, 9802-9807 (2006).
27. Ballester, P. & Biros, S. M. in The Importance of Pi-Interactions in Crystal Engineering 79-107 (John Wiley, 2012).
28. Goyal, P. et al. Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG. Nature 516, 250-253 (2014).
29. Finkelstein, A. Proton-coupled protein transport through the anthrax toxin channel. Phil. Trans. R. Soc. B 364, 209-215 (2009).
30. Kintzer, A. F. Tang, II, Schawel, A. K., Brown, M. J. & Krantz, B. A. Anthrax toxin protective antigen integrates poly-gamma-D-glutamate and pH signals to sense the optimal environment for channel formation. Proc. Natl Acad. Sci. USA 109, 18378-18383 (2012).
31. Wigelsworth, D. J. et al. Binding stoichiometry and kinetics of the interaction of a human anthrax toxin receptor, CMG2, with protective antigen. J. Biol. Chem. 279, 23349-23356 (2004).
32. Ortega, J., Singh, S. K., Ishikawa, T., Maurizi, M. R. & Steven, A. C. Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. Mol. Cell 6, 1515-1521 (2000).
33. Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41-60 (2005).
34. Suloway, C. et al. Fully automated, sequential tilt-series acquisition with Leginon. J. Struct. Biol. 167, 11-18 (2009).
35. Li, X. et al. Electron counting and beam-induced motion correction enable nearatomic-resolution single-particle cryo-EM. Nature Methods 10, 584-590 (2013).
36. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for highresolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
37. Mindell, J. A. &Grigorieff, N. Accurate determinationof local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
38. Heymann, J. B. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133, 156-169 (2001).
39. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
40. Scheres, S. H. A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 415, 406-418 (2012).
41. Scheres, S. H. Beam-induced motion correction for sub-megadalton cryo-EM particles. eLife 3, e03665 (2014).
42. Amunts, A. et al. Structure of the yeast mitochondrial large ribosomal subunit. Science 343, 1485-1489 (2014).
43. Swint-Kruse, L. & Brown, C. S. Resmap: automated representation of macromolecular interfaces as two-dimensional networks. Bioinformatics 21, 3327-3328 (2005).
44. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
45. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
46. Brunger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
47. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
48. Schrodinger, LLC. The PyMOL Molecular Graphics System, v. 1. 7. 2 (2014).
49. Krissinel, E. &Henrick, K. Inference ofmacromolecular assemblies fromcrystalline state. J. Mol. Biol. 372, 774-797 (2007).