Monitoring the kinetics of the pH-driven transition of the anthrax toxin prepore to the pore by biolayer interferometry and surface plasmon resonance

Biochemistry

Volumn 52, Issue 37, 2013, Pages 6335-6347

  Naik, Subhashchandra ^a   Brock, Susan ^a   Akkaladevi, Narahari ^a   Tally, Jon ^a   McGinn Straub, Wesley ^c   Zhang, Na ^d   Gao, Phillip ^d   Gogol, E P ^e   Pentelute, B L ^b   Collier, R John ^b   Fisher, Mark T ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Forté Bio A Division of Pall Life Sciences   (United States)

^d UNIVERSITY OF KANSAS   (United States)

^e UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXINS; COMPLEX FORMATIONS; EDEMA FACTORS; ENDOSOMAL MEMBRANE; KINETIC TRANSITION; PORE FORMATION; PROTECTIVE ANTIGENS; SOLUBLE RECEPTOR;

ACIDIFICATION; CYTOLOGY; ELECTRON MICROSCOPES; ELECTRON MICROSCOPY; INTERFEROMETRY; KINETICS; PLASMONS; SURFACE PLASMON RESONANCE; TOXIC MATERIALS;

DISEASES;

ANTHRAX PROTECTIVE ANTIGEN; ANTHRAX TOXIN; ANTIGEN; TRANSLOCON; UNCLASSIFIED DRUG;

ACIDIFICATION; ARTICLE; BIOSENSOR; CHANNEL GATING; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); ELECTRON MICROSCOPY; ENDOSOME; INTERFEROMETRY; MICELLE; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BINDING; SURFACE PLASMON RESONANCE;

ANTIGENS, BACTERIAL; BACTERIAL TOXINS; BIOSENSING TECHNIQUES; ENDOSOMES; HUMANS; HYDROGEN-ION CONCENTRATION; IMMOBILIZED PROTEINS; INTERFEROMETRY; INTRACELLULAR MEMBRANES; KINETICS; MICELLES; MICROSCOPY, ELECTRON; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PEPTIDE; SURFACE PLASMON RESONANCE;

EID: 84884267573     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400705n     Document Type: Article

References (33)

1. 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
2. Wesche, J., Elliott, J. L., Falnes, P. O., Olsnes, S., and Collier, R. J. (1998) Characterization of membrane translocation by anthrax protective antigen Biochemistry 37, 15737-15746 (Pubitemid 28524745)
3. Zako, T., Harada, K., Mannen, T., Yamaguchi, S., Kitayama, A., Ueda, H., and Nagamune, T. (2001) Monitoring of the refolding process for immobilized firefly luciferase with a biosensor based on surface plasmon resonance J. Biochem. 129, 1-4 (Pubitemid 32150475)
4. Chen, L. Y. (2009) Monitoring conformational changes of immobilized RNase A and lysozyme in reductive unfolding by surface plasmon resonance Anal. Chim. Acta 631, 96-101
5. Paynter, S. and Russell, D. A. (2002) Surface plasmon resonance measurement of pH-induced responses of immobilized biomolecules: Conformational change or electrostatic interaction effects? Anal. Biochem. 309, 85-95 (Pubitemid 35305794)
6. 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)
7. Miller, C. J., Elliott, J. L., and Collier, R. J. (1999) Anthrax protective antigen: Prepore-to-pore conversion Biochemistry 38, 10432-10441
8. Akkaladevi, N., Hinton-Chollet, L., Katayama, H., Mitchell, J., Szerszen, L., Mukherjee, S., Gogol, E. P., Pentelute, B. L., Collier, R. J., and Fisher, M. T. (2013) Assembly of anthrax toxin pore: Lethal-factor complexes into lipid nanodiscs Protein Sci. 22, 492-501
9. Gogol, E. P., Akkaladevi, N., Szerszen, L., Mukherjee, S., Chollet-Hinton, L., Katayama, H., Pentelute, B. L., Collier, R. J., and Fisher, M. T. (2013) Three dimensional structure of the anthrax toxin translocon-lethal factor complex by cryo-electron microscopy Protein Sci. 22, 586-594
10. 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
11. Bayburt, T. H. and Sligar, S. G. (2010) Membrane protein assembly into Nanodiscs FEBS Lett. 584, 1721-1727
12. Pimental, R. A., Christensen, K. A., Krantz, B. A., and Collier, R. J. (2004) Anthrax toxin complexes: Heptameric protective antigen can bind lethal factor and edema factor simultaneously Biochem. Biophys. Res. Commun. 322, 258-262 (Pubitemid 39093863)
13. Mogridge, J., Cunningham, K., and Collier, R. J. (2002) Stoichiometry of anthrax toxin complexes Biochemistry 41, 1079-1082 (Pubitemid 34065284)
14. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128, 82-97 (Pubitemid 30013436)
15. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., and Leith, A. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116, 190-199 (Pubitemid 26093143)
16. 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
17. 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: A visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-1612
18. Milne, J. C. and Collier, R. J. (1993) pH-dependent permeabilization of the plasma membrane of mammalian cells by anthrax protective antigen Mol. Microbiol. 10, 647-653 (Pubitemid 23334445)
19. Milne, J. C., Furlong, D., Hanna, P. C., Wall, J. S., and Collier, R. J. (1994) Anthrax protective antigen forms oligomers during intoxication of mammalian cells J. Biol. Chem. 269, 20607-20612 (Pubitemid 24260471)
20. 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)
21. Wolfe, J. T., Krantz, B. A., Rainey, G. J., Young, J. A., and Collier, R. J. (2005) Whole-cell voltage clamp measurements of anthrax toxin pore current J. Biol. Chem. 280, 39417-39422 (Pubitemid 41713899)
22. Rainey, G. J., Wigelsworth, D. J., Ryan, P. L., Scobie, H. M., Collier, R. J., and Young, J. A. (2005) Receptor-specific requirements for anthrax toxin delivery into cells Proc. Natl. Acad. Sci. U.S.A. 102, 13278-13283 (Pubitemid 41325014)
23. 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: A role for receptor in pH-dependent pore formation Proc. Natl. Acad. Sci. U.S.A. 101, 13147-13151 (Pubitemid 39209633)
24. Santelli, E., Bankston, L. A., Leppla, S. H., and Liddington, R. C. (2004) Crystal structure of a complex between anthrax toxin and its host cell receptor Nature 430, 905-908 (Pubitemid 39119219)
25. Scobie, H. M., Marlett, J. M., Rainey, G. J., Lacy, D. B., Collier, R. J., and Young, J. A. (2007) Anthrax toxin receptor 2 determinants that dictate the pH threshold of toxin pore formation PLoS One 2, e329
26. Wigelsworth, D. J., Krantz, B. A., Christensen, K. A., Lacy, D. B., Juris, S. J., and 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 (Pubitemid 38685644)
27. 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
28. Pilpa, R. M., Bayrhuber, M., Marlett, J. M., Riek, R., and Young, J. A. (2011) A receptor-based switch that regulates anthrax toxin pore formation PLoS Pathog. 7, e1002354
29. Sun, J., Vernier, G., Wigelsworth, D. J., and Collier, R. J. (2007) Insertion of Anthrax Protective Antigen into Liposomal Membranes: Effects of a Receptor J. Biol. Chem. 282, 1059-1065 (Pubitemid 47076531)
30. Zhu, P. J., Hobson, J. P., Southall, N., Qiu, C., Thomas, C. J., Lu, J., Inglese, J., Zheng, W., Leppla, S. H., Bugge, T. H., Austin, C. P., and Liu, S. (2009) Quantitative high-throughput screening identifies inhibitors of anthrax-induced cell death Bioorg. Med. Chem. 17, 5139-5145
31. Cryan, L. M., Habeshian, K. A., Caldwell, T. P., Morris, M. T., Ackroyd, P. C., Christensen, K. A., and Rogers, M. S. (2013) Identification of Small Molecules That Inhibit the Interaction of TEM8 with Anthrax Protective Antigen Using a FRET Assay J. Biomol. Screening 18, 714-725
32. Wein, A. N., Williams, B. N., Liu, S., Ermolinsky, B., Provenzano, D., Abagyan, R., Orry, A., Leppla, S. H., and Peredelchuk, M. (2012) Small molecule inhibitors of Bacillus anthracis protective antigen proteolytic activation and oligomerization J. Med. Chem. 55, 7998-8006
33. 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