Anthrax toxin protective antigen - Insights into molecular switching from prepore to pore

Protein Science

Volumn 21, Issue 1, 2012, Pages 1-12

  Bann, James G ^a  

^a WICHITA STATE UNIVERSITY   (United States)

Author keywords

Anthrax; Membrane protein; pH; Pore; Protective antigen; Review; Toxin

Indexed keywords

ANTHRAX TOXIN; BACTERIAL ANTIGEN; MONOMER; POLYPEPTIDE; PROTECTIVE ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN STRUCTURE; BACILLUS ANTHRACIS; BACTERIAL SPORE; CONFORMATIONAL TRANSITION; ENDOCYTOSIS; NONHUMAN; PH; PHI CLAMP; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW;

ANIMALS; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR;

EID: 84455204808     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.752     Document Type: Review

References (93)

1. Jernigan JA, Stephens DS, Ashford DA, Omenaca C, Topiel MS, Galbraith M, Tapper M, Fisk TL, Zaki S, Popovic T, Meyer RF, Quinn CP, Harper SA, Fridkin SK, Sejvar JJ, Shepard CW, McConnell M, Guarner J, Shieh WJ, Malecki JM, Gerberding JL, Hughes JM, Perkins BA (2001) Bioterrorism-related inhalational anthrax: the first 10 cases reported in the United States. Emerg Infect Dis 7:933-944.
2. Chitlaru T, Altboum Z, Reuveny S, Shafferman A (2011) Progress and novel strategies in vaccine development and treatment of anthrax. Immunol Rev 239:221-236.
3. Cote CK, Bozue J, Twenhafel N, Welkos SL (2009) Effects of altering the germination potential of Bacillus anthracis spores by exogenous means in a mouse model. J Med Microbiol 58:816-825.
4. Van Ness GB (1971) Ecology of anthrax. Science 172:1303-1307.
5. Durrheim DN, Freeman P, Roth I, Hornitzky M (2009) Epidemiologic questions from anthrax outbreak, Hunter Valley, Australia. Emerg Infect Dis 15:840-842.
6. Bell JH, Fee E, Brown TM (2002) Anthrax and the wool trade. 1902. Am J Public Health 92:754-757.
7. Stojkovic B, Torres EM, Prouty AM, Patel HK, Zhuang L, Koehler TM, Ballard JD, Blanke SR (2008) High-throughput, single-cell analysis of macrophage interactions with fluorescently labeled Bacillus anthracis spores. Appl Environ Microbiol 74:5201-5210.
8. Cleret A, Quesnel-Hellmann A, Vallon-Eberhard A, Verrier B, Jung S, Vidal D, Mathieu J, Tournier JN (2007) Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. J Immunol 178:7994-8001. (Pubitemid 46898070)
9. Guidi-Rontani C, Weber-Levy M, Labruyere E, Mock M (1999) Germination of Bacillus anthracis spores within alveolar macrophages. Mol Microbiol 31:9-17. (Pubitemid 29012143)
10. Friedlander AM, Welkos SL, Pitt ML, Ezzell JW, Worsham PL, Rose KJ, Ivins BE, Lowe JR, Howe GB, Mikesell P, Lawrence, WB (1993) Postexposure prophylaxis against experimental inhalation anthrax. J Infect Dis 167:1239-1243. (Pubitemid 23115626)
11. Jefferds MD, Laserson K, Fry AM, Roy S, Hayslett J, Grummer-Strawn L, Kettel-Khan L, Schuchat A (2002) Adherence to antimicrobial inhalational anthrax prophylaxis among postal workers, Washington, D.C., 2001. Emerg Infect Dis 8:1138-1144. (Pubitemid 35257007)
12. Green BD, Battisti L, Koehler TM, Thorne CB, Ivins BE (1985) Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun 49:291-297. (Pubitemid 15004855)
13. Beall FA, Taylor MJ, Thorne CB (1962) Rapid lethal effect in rats of a third component found upon fractionating the toxin of Bacillus anthracis. J Bacteriol 83:1274-1280.
14. Stanley JL, Smith H (1963) The three factors of anthrax toxin: their immunogenicity and lack of demonstrable enzymic activity. J Gen Microbiol 31:329-337.
15. Barth H, Aktories K, Popoff MR, Stiles BG (2004) Binary bacterial toxins: biochemistry, biology, and applications of common Clostridium and Bacillus proteins. Microbiol Mol Biol Rev 68:373-402. (Pubitemid 39238275)
16. Strange RE, Thorne CB (1958) Further purification studies on the protective antigen of Bacillus anthracis produced in vitro. J Bacteriol 76:192-202.
17. Ivins BE, Ezzell JW, Jr, Jemski J, Hedlund KW, Ristroph JD, Leppla SH (1986) Immunization studies with attenuated strains of Bacillus anthracis. Infect Immun 52:454-458. (Pubitemid 16117800)
18. Vick JA, Lincoln RE, Klein F, Mahlandt BG, Walker JS, Fish DC (1968) Neurological and physiological responses of the primate to anthrax toxin. J Infect Dis 118:85-96.
19. Fish DC, Mahlandt BG, Dobbs JP, Lincoln RE (1968) Purification and properties of in vitro-produced anthrax toxin components. J Bacteriol 95:907-918.
20. Leppla SH (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.
21. Hong J, Doebele RC, Lingen MW, Quilliam LA, Tang WJ, Rosner MR (2007) Anthrax edema toxin inhibits endothelial cell chemotaxis via Epac and Rap1. J Biol Chem 282:19781-19787. (Pubitemid 47100121)
22. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, Copeland TD, Ahn NG, Oskarsson MK, Fukasawa K, Paull KD, Vande Woude GF (1998) Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280:734-737. (Pubitemid 28243347)
23. Pellizzari R, Guidi-Rontani C, Vitale G, Mock M, Montecucco C (2000) Lethal factor of Bacillus anthracis cleaves the N-terminus of MAPKKs: analysis of the intracellular consequences in macrophages. Int J Med Microbiol 290:421-427.
24. Pellizzari R, Guidi-Rontani C, Vitale G, Mock M, Montecucco C (1999) Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/IFNgamma-induced release of NO and TNFalpha. FEBS Lett 462:199-204.
25. Lehmann M, Noack D, Wood M, Perego M, Knaus UG (2009) Lung epithelial injury by B. anthracis lethal toxin is caused by MKK-dependent loss of cytoskeletal integrity. PLoS One 4:e4755.
26. Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JA (2001) Identification of the cellular receptor for anthrax toxin. Nature 414:225-229. (Pubitemid 33051239)
27. St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B, Kinzler KW (2000) Genes expressed in human tumor endothelium. Science 289:1197-1202. (Pubitemid 30650733)
28. Scobie HM, Rainey GJ, Bradley KA, Young JA (2003) Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc Natl Acad Sci USA 100:5170-5174. (Pubitemid 36542677)
29. Martchenko M, Jeong SY, Cohen SN (2010) Heterodimeric integrin complexes containing beta1-integrin promote internalization and lethality of anthrax toxin. Proc Natl Acad Sci USA 107:15583-15588.
30. Bell SE, Mavila A, Salazar R, Bayless KJ, Kanagala S, Maxwell SA, Davis GE (2001) Differential gene expression during capillary morphogenesis in 3D collagen matrices: regulated expression of genes involved in basement membrane matrix assembly, cell cycle progression, cellular differentiation and G-protein signaling. J Cell Sci 114:2755-2773. (Pubitemid 32785455)
31. Nanda A, Carson-Walter EB, Seaman S, Barber TD, Stampfl J, Singh S, Vogelstein B, Kinzler KW, St Croix B (2004) TEM8 interacts with the cleaved C5 domain of collagen alpha 3(VI). Cancer Res 64:817-820. (Pubitemid 38176877)
32. Lee JO, Rieu P, Arnaout MA, Liddington R (1995) Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 80:631-638.
33. Santelli E, Bankston LA, Leppla SH, Liddington RC (2004) Crystal structure of a complex between anthrax toxin and its host cell receptor. Nature 430:905-908. (Pubitemid 39119219)
34. Lacy DB, Wigelsworth DJ, Melnyk RA, Harrison SC, Collier RJ (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. (Pubitemid 39209633)
35. Varughese M, Teixeira AV, Liu S, Leppla SH (1999) Identification of a receptor-binding region within domain 4 of the protective antigen component of anthrax toxin. Infect Immun 67:1860-1865. (Pubitemid 29144407)
36. Scobie HM, Wigelsworth DJ, Marlett JM, Thomas D, Rainey GJ, Lacy DB, Manchester M, Collier RJ, Young JA (2006) Anthrax toxin receptor 2-dependent lethal toxin killing in vivo. PLoS Pathog 2:e111.
37. Williams AS, Lovell S, Anbanandam A, El-Chami R, Bann JG (2009) Domain 4 of the anthrax protective antigen maintains structure and binding to the host receptor CMG2 at low pH. Protein Sci 18:2277-2286.
38. Wigelsworth DJ, Krantz BA, Christensen KA, Lacy DB, Juris SJ, Collier RJ (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)
39. Klimpel KR, Molloy SS, Thomas G, Leppla SH (1992) Anthrax toxin protective antigen is activated by a cell surface protease with the sequence specificity and catalytic properties of furin. Proc Natl Acad Sci USA 89:10277-10281.
40. Mogridge J, Cunningham K, Collier RJ (2002) Stoichiometry of anthrax toxin complexes. Biochemistry 41:1079-1082. (Pubitemid 34065284)
41. Petosa C, Collier RJ, Klimpel KR, Leppla SH, Liddington RC (1997) Crystal structure of the anthrax toxin protective antigen. Nature 385:833-838. (Pubitemid 27106075)
42. Kintzer AF, Thoren KL, Sterling HJ, Dong KC, Feld GK, Tang, II, Zhang TT, Williams ER, Berger JM, Krantz BA (2009) The protective antigen component of anthrax toxin forms functional octameric complexes. J Mol Biol 392:614-629.
43. Mogridge J, Cunningham K, Lacy DB, Mourez M, Collier RJ (2002) The lethal and edema factors of anthrax toxin bind only to oligomeric forms of the protective antigen. Proc Natl Acad Sci USA 99:7045-7048. (Pubitemid 34527149)
44. Melnyk RA, Hewitt KM, Lacy DB, Lin HC, Gessner CR, Li S, Woods VL, Jr, Collier RJ (2006) Structural determinants for the binding of anthrax lethal factor to oligomeric protective antigen. J Biol Chem 281:1630-1635.
45. Ren G, Quispe J, Leppla SH, Mitra AK (2004) Large-scale structural changes accompany binding of lethal factor to anthrax protective antigen: a cryo-electron microscopic study. Structure 12:2059-2066. (Pubitemid 39469403)
46. Feld GK, Thoren KL, Kintzer AF, Sterling HJ, Tang, II, Greenberg SG, Williams ER, Krantz BA (2010) Structural basis for the unfolding of anthrax lethal factor by protective antigen oligomers. Nat Struct Mol Biol 17:1383-1390.
47. Ezzell JW, Jr, Abshire TG (1992) Serum protease cleavage of Bacillus anthracis protective antigen. J Gen Microbiol 138:543-549.
48. Panchal RG, Halverson KM, Ribot W, Lane D, Kenny T, Abshire TG, Ezzell JW, Hoover TA, Powell B, Little S, Kasianowicz JJ, Bavari S (2005) Purified Bacillus anthracis lethal toxin complex formed in vitro and during infection exhibits functional and biological activity. J Biol Chem 280:10834-10839. (Pubitemid 40395947)
49. Moayeri M, Wiggins JF, Leppla SH (2007) Anthrax protective antigen cleavage and clearance from the blood of mice and rats. Infect Immun 75:5175-5184. (Pubitemid 350033604)
50. Miller CJ, Elliott JL, Collier RJ (1999) Anthrax protective antigen: prepore-to-pore conversion. Biochemistry 38:10432-10441.
51. Milne JC, Furlong D, Hanna PC, Wall JS, Collier RJ (1994) Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J Biol Chem 269: 20607-20612. (Pubitemid 24260471)
52. Kintzer AF, Sterling HJ, Tang, II, Abdul-Gader A, Miles AJ, Wallace BA, Williams ER, Krantz BA (2010) Role of the protective antigen octamer in the molecular mechanism of anthrax lethal toxin stabilization in plasma. J Mol Biol 399:741-758.
53. Gawlik K, Remacle AG, Shiryaev SA, Golubkov VS, Ouyang M, Wang Y, Strongin AY (2010) A femtomol range FRET biosensor reports exceedingly low levels of cell surface furin: implications for the processing of anthrax protective antigen. PLoS One 5:e11305.
54. Abrami L, Liu S, Cosson P, Leppla SH, van der Goot FG (2003) Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J Cell Biol 160:321-328. (Pubitemid 36182723)
55. Abrami L, Leppla SH, van der Goot FG (2006) Receptor palmitoylation and ubiquitination regulate anthrax toxin endocytosis. J Cell Biol 172:309-320.
56. Abrami L, Bischofberger M, Kunz B, Groux R, van der Goot FG (2010) Endocytosis of the anthrax toxin is mediated by clathrin, actin and unconventional adaptors. PLoS Pathog 6:e1000792.
57. Brown MS, Goldstein JL (1979) Receptor-mediated endocytosis: insights from the lipoprotein receptor system. Proc Natl Acad Sci USA 76:3330-3337. (Pubitemid 9233955)
58. Beauregard KE, Collier RJ, Swanson JA (2000) Proteolytic activation of receptor-bound anthrax protective antigen on macrophages promotes its internalization. Cell Microbiol 2:251-258. (Pubitemid 30616510)
59. Go MY, Chow EM, Mogridge J (2009) The cytoplasmic domain of anthrax toxin receptor 1 affects binding of the protective antigen. Infect Immun 77:52-59.
60. Zornetta I, Brandi L, Janowiak B, Dal Molin F, Tonello F, Collier RJ, Montecucco C (2010) Imaging the cell entry of the anthrax oedema and lethal toxins with fluorescent protein chimeras. Cell Microbiol 12:1435-1445.
61. Friedlander AM (1986) Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J Biol Chem 261:7123-7126.
62. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274:1859-1866. (Pubitemid 26424757)
63. Benson EL, Huynh PD, Finkelstein A, Collier RJ (1998) Identification of residues lining the anthrax protective antigen channel. Biochemistry 37:3941-3948. (Pubitemid 28162951)
64. Nassi S, Collier RJ, Finkelstein A (2002) PA63 channel of anthrax toxin: an extended beta-barrel. Biochemistry 41:1445-1450. (Pubitemid 34112732)
65. Nguyen TL (2004) Three-dimensional model of the pore form of anthrax protective antigen. Structure and biological implications. J Biomol Struct Dyn 22:253-265.
66. Katayama H, Janowiak BE, Brzozowski M, Juryck J, Falke S, Gogol EP, Collier RJ, Fisher MT (2008) GroEL as a molecular scaffold for structural analysis of the anthrax toxin pore. Nat Struct Mol Biol 15:754-760. (Pubitemid 351932002)
67. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612.
68. Katayama H, Wang J, Tama F, Chollet L, Gogol EP, Collier RJ, Fisher MT (2010) Three-dimensional structure of the anthrax toxin pore inserted into lipid nanodiscs and lipid vesicles. Proc Natl Acad Sci USA 107:3453-3457.
69. Krantz BA, Finkelstein A, Collier RJ (2006) Protein translocation through the anthrax toxin transmembrane pore is driven by a proton gradient. J Mol Biol 355:968-979. (Pubitemid 43012140)
70. Krantz BA, Melnyk RA, Zhang S, Juris SJ, Lacy DB, Wu Z, Finkelstein A, Collier RJ (2005) A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309:777-781. (Pubitemid 41077325)
71. Blaustein RO, Koehler TM, Collier RJ, Finkelstein A (1989) Anthrax toxin: channel-forming activity of protective antigen in planar phospholipid bilayers. Proc Natl Acad Sci USA 86:2209-2213. (Pubitemid 19102481)
72. Yeh HJC, Kirk KL, Cohen LA, Cohen JS (1975) 19F and 1H nuclear magnetic resonance studies of ring-fluorinated imidazoles and histidines. J Chem Soc Perkin Trans 2:928-934.
73. Wimalasena DS, Cramer JC, Janowiak BE, Juris SJ, Melnyk RA, Anderson DE, Kirk KL, Collier RJ, Bann JG (2007) Effect of 2-fluorohistidine labeling of the anthrax protective antigen on stability, pore formation, and translocation. Biochemistry 46:14928-14936. (Pubitemid 350308884)
74. Mourez M, Yan M, Lacy DB, Dillon L, Bentsen L, Marpoe A, Maurin C, Hotze E, Wigelsworth D, Pimental RA, Ballard JD, Collier RJ, Tweten RK (2003) Mapping dominant-negative mutations of anthrax protective antigen by scanning mutagenesis. Proc Natl Acad Sci USA 100:13803-13808. (Pubitemid 37499147)
75. Sellman BR, Mourez M, Collier RJ (2001) Dominant-negative mutants of a toxin subunit: an approach to therapy of anthrax. Science 292:695-697. (Pubitemid 32385534)
76. Sellman BR, Nassi S, Collier RJ (2001) Point mutations in anthrax protective antigen that block translocation. J Biol Chem 2768371-8376.
77. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Cryst 66:486-501.
78. Janowiak BE, Finkelstein A, Collier RJ (2009) An approach to characterizing single-subunit mutations in multimeric prepores and pores of anthrax protective antigen. Protein Sci 18:348-358.
79. Sun J, Lang AE, Aktories K, Collier RJ (2008) Phenylalanine- 427 of anthrax protective antigen functions in both pore formation and protein translocation. Proc Natl Acad Sci USA 105:4346-4351. (Pubitemid 351754383)
80. Melnyk RA, Collier RJ (2006) A loop network within the anthrax toxin pore positions the phenylalanine clamp in an active conformation. Proc Natl Acad Sci USA 103:9802-9807. (Pubitemid 43993578)
81. Schleberger C, Hochmann H, Barth H, Aktories K, Schulz GE (2006) Structure and action of the binary C2 toxin from Clostridium botulinum. J Mol Biol 364:705-715. (Pubitemid 44755316)
82. Scobie HM, Marlett JM, Rainey GJ, Lacy DB, Collier RJ, Young JA (2007) Anthrax toxin receptor 2 determinants that dictate the pH threshold of toxin pore formation. PLoS One 2:e329.
83. Wimalasena DS, Janowiak BE, Lovell S, Miyagi M, Sun J, Zhou H, Hajduch J, Pooput C, Kirk KL, Battaile KP, Bann JG (2010) Evidence that histidine protonation of receptor-bound anthrax protective antigen is a trigger for pore formation. Biochemistry 49:6973-6983.
84. Rainey GJ, Wigelsworth DJ, Ryan PL, Scobie HM, Collier RJ, Young JA (2005) Receptor-specific requirements for anthrax toxin delivery into cells. Proc Natl Acad Sci USA 102:13278-13283. (Pubitemid 41325014)
85. Rajapaksha M, Eichler JF, Hajduch J, Anderson DE, Kirk KL, Bann JG (2009) Monitoring anthrax toxin receptor dissociation from the protective antigen by NMR. Protein Sci 18:17-23.
86. Williams DH, O'Brien DP, Sandercock AM, Stephens E (2004) Order changes within receptor systems upon ligand binding: receptor tightening/oligomerisation and the interpretation of binding parameters. J Mol Biol 340:373-383. (Pubitemid 38759916)
87. Pentelute BL, Sharma O, Collier RJ (2011) Chemical dissection of protein translocation through the anthrax toxin pore. Angew Chem Int Ed Engl 50:2294-2296.
88. Gajewski C, Dagcan A, Roux B, Deutsch C (2011) Biogenesis of the pore architecture of a voltage-gated potassium channel. Proc Natl Acad Sci USA 108:3240-3245.
89. Krantz BA, Trivedi AD, Cunningham K, Christensen KA, Collier RJ (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)
90. Backer MV, Patel V, Jehning BT, Claffey KP, Karginov VA, Backer JM (2007) Inhibition of anthrax protective antigen outside and inside the cell. Antimicrob Agents Chemother 51:245-251. (Pubitemid 46047713)
91. Salles, II, Voth DE, Ward SC, Averette KM, Tweten RK, Bradley KA, Ballard JD (2006) Cytotoxic activity of Bacillus anthracis protective antigen observed in a macrophage cell line overexpressing ANTXR1. Cell Microbiol 8:1272-1281.
92. Wesche J, Elliott JL, Falnes PO, Olsnes S, Collier RJ (1998) Characterization of membrane translocation by anthrax protective antigen. Biochemistry 37:15737-15746. (Pubitemid 28524745)
93. Thoren KL, Krantz BA (2011) The unfolding story of anthrax toxin translocation. Mol Microbiol 80:588-595.