Clostridium perfringens epsilon toxin H149A mutant as a platform for receptor binding studies

Protein Science

Volumn 22, Issue 5, 2013, Pages 650-659

  Bokori Brown, Monika ^a   Kokkinidou, Maria C ^b   Savva, Christos G ^b   Da Costa, Sérgio P Fernandes ^a   Naylor, Claire E ^b   Cole, Ambrose R ^b   Moss, David S ^b   Basak, Ajit K ^b   Titball, Richard W ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Clostridium perfringens; Enterotoxemia; Epsilon toxin; Glycan binding; Pore forming toxin

Indexed keywords

ALANINE; BACTERIAL TOXIN; CELL SURFACE RECEPTOR; EPSILON TOXIN; GLYCAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CLOSTRIDIUM PERFRINGENS; CRYSTAL STRUCTURE; CYTOTOXICITY; ESCHERICHIA COLI; GENETIC MANIPULATION; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; RECEPTOR BINDING; STRUCTURE ANALYSIS;

ANIMALS; BACTERIAL TOXINS; BINDING SITES; CELL LINE; CELL SURVIVAL; CLOSTRIDIUM INFECTIONS; CLOSTRIDIUM PERFRINGENS; DOGS; HOST-PATHOGEN INTERACTIONS; MADIN DARBY CANINE KIDNEY CELLS; MODELS, MOLECULAR; POINT MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, CELL SURFACE;

CLOSTRIDIUM PERFRINGENS;

EID: 84878328587     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2250     Document Type: Article

References (42)

1. Bokori-Brown M, Savva CG, Fernandes da Costa SP, Naylor CE, Basak AK, Titball RW (2011) Molecular basis of toxicity of Clostridium perfringens epsilon toxin. FEBS J 278:4589-4601.
2. Uzal FA, Songer JG (2008) Diagnosis of Clostridium perfringens intestinal infections in sheep and goats. J Vet Diagn Invest 20:253-265. (Pubitemid 352844373)
3. Songer JG (1996) Clostridial enteric diseases of domestic animals. Clin Microbiol Rev 9:216-234. (Pubitemid 26124457)
4. Popoff MR (2011) Epsilon toxin: a fascinating poreforming toxin. FEBS J 278:4602-4615.
5. Nagahama M, Sakurai J (1993) Effect of drugs acting on the central nervous system on the lethality in mice of Clostridium perfringens epsilon toxin. Toxicon 31: 427-435.
6. Miyamoto O, Minami J, Toyoshima T, Nakamura T, Masada T, Nagao S, Negi T, Itano T, Okabe A (1998) Neurotoxicity of Clostridium perfringens epsilon-toxin for the rat hippocampus via the glutamatergic system. Infect Immun 66:2501-2508. (Pubitemid 28261744)
7. Miyamoto O, Sumitani K, Nakamura T, Yamagami S, Miyata S, Itano T, Negi T, Okabe A (2000) Clostridium perfringens epsilon toxin causes excessive release of glutamate in the mouse hippocampus. FEMS Microbiol Lett 189:109-113. (Pubitemid 30456256)
8. Lonchamp E, Dupont JL, Wioland L, Courjaret R, Mbebi-Liegeois C, Jover E, Doussau F, Popoff MR, Bossu JL, de Barry J, Poulain B (2010) Clostridium perfringens epsilon toxin targets granule cells in the mouse cerebellum and stimulates glutamate release. PLoS One 5:e13046.
9. Finnie JW (2003) Pathogenesis of brain damage produced in sheep by Clostridium perfringens type D epsilon toxin: a review. Aust Vet J 81:219-221. (Pubitemid 43934479)
10. Popoff MR, Bouvet P (2009) Clostridial toxins. Future Microbiol 4:1021-1064.
11. McDonel JL, Toxins of Clostridium perfringens types A, B, C, D and E. In: Dorner F, Drews J, Eds. (1986) Pharmacology of bacterial toxins. Oxford: Pergamon Press, pp 477-517.
12. Bhown AS, Habeerb AF (1977) Structural studies on epsilon-prototoxin of Clostridium perfringens type D. Localization of the site of tryptic scission necessary for activation to epsilon-toxin. Biochem Biophys Res Commun 78:889-896. (Pubitemid 8209820)
13. Jin F, Matsushita O, Katayama S, Jin S, Matsushita C, Minami J, Okabe A (1996) Purification, characterization, and primary structure of Clostridium perfringens lambda-toxin, a thermolysin-like metalloprotease. Infect Immun 64:230-237. (Pubitemid 26009362)
14. Minami J, Katayama S, Matsushita O, Matsushita C, Okabe A (1997) Lambda-toxin of Clostridium perfringens activates the precursor of epsilon-toxin by releasing its N-and C-terminal peptides. Microbiol Immunol 41:527-535. (Pubitemid 27318089)
15. Cole AR, Gibert M, Popoff M, Moss DS, Titball RW, Basak AK (2004) Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin. Nat Struct Mol Biol 11:797-798. (Pubitemid 39014507)
16. Ivie SE, McClain MS (2012) Identification of amino acids important for binding of Clostridium perfringens epsilon toxin to host cells and to HAVCR1. Biochemistry 51:758827595.
17. Parker MW, Buckley JT, Postma JP, Tucker AD, Leonard K, Pattus F, Tsernoglou D (1994) Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature 367:292-295. (Pubitemid 24051148)
18. Miyata S, Minami J, Tamai E, Matsushita O, Shimamoto S, Okabe A (2002) Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of MDCK cells and rat synaptosomes. J Biol Chem 277:39463-39468. (Pubitemid 35190922)
19. Abrami L, van Der Goot FG (1999) Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J Cell Biol 147:175-184. (Pubitemid 30211805)
20. Abe Y, Shimada H, Kitada S (2008) Raft-targeting and oligomerization of Parasporin-2, a Bacillus thuringiensis crystal protein with anti-tumour activity. J Biochem 143:269-275. (Pubitemid 351238172)
21. Nagahama M, Ochi S, Sakurai J (1998) Assembly of Clostridium perfringens epsilon-toxin on MDCK cell membrane. J Nat Toxins 7:291-302. (Pubitemid 28456463)
22. Petit L, Gibert M, Gillet D, Laurent-Winter C, Boquet P, Popoff MR (1997) Clostridium perfringens epsilontoxin acts on MDCK cells by forming a large membrane complex. J Bacteriol 179:6480-6487. (Pubitemid 27443933)
23. Chassin C, Bens M, de Barry J, Courjaret R, Bossu JL, Cluzeaud F, Ben Mkaddem S, Gibert M, Poulain B, Popoff MR, Vandewalle A (2007) Pore-forming epsilon toxin causes membrane permeabilization and rapid ATP depletion-mediated cell death in renal collecting duct cells. Am J Physiol Renal Physiol 293:F927-F937. (Pubitemid 47403365)
24. Knight PA, Queminet J, Blanchard JH, Tilleray JH (1990) In vitro tests for the measurement of clostridial toxins, toxoids and antisera. II. Titration of Clostridium perfringens toxins and antitoxins in cell culture. Biologicals 18:263-270.
25. Payne DW, Williamson ED, Havard H, Modi N, Brown J (1994) Evaluation of a new cytotoxicity assay for Clostridium perfringens type D epsilon toxin. FEMS Microbiol Lett 116:161-167. (Pubitemid 124011993)
26. Ivie SE, Fennessey CM, Sheng J, Rubin DH, McClain MS (2011) Gene-trap mutagenesis identifies mammalian genes contributing to intoxication by Clostridium perfringens epsilon-toxin. PLoS One 6:e17787.
27. Recommendations of the CDC Strategic Planning Workgroup (2000) Biological and chemical terrorism: strategic plan for preparedness and response. MMWR Recomm Rep 49:1-14.
28. Oyston PCF, Payne DW, Havard HL, Williamson ED, Titball RW (1998) Production of a non-toxic sitedirected mutant of Clostridium perfringens epsilontoxin which induces protective immunity in mice. Microbiology 144:333-341. (Pubitemid 28067738)
29. Lavinder JJ, Hari SB, Sullivan BJ, Magliery TJ (2009) High-throughput thermal scanning: a general, rapid dye-binding thermal shift screen for protein engineering. J Am Chem Soc 131:3794-3795.
30. Diep DB, Nelson KL, Lawrence TS, Sellman BR, Tweten RK, Buckley JT (1999) Expression and properties of an aerolysin -Clostridium septicum alpha toxin hybrid protein. Mol Microbiol 31:785-794. (Pubitemid 29057282)
31. Pelish TM, McClain MS (2009) Dominant-negative inhibitors of the Clostridium perfringens epsilon-toxin. J Biol Chem 284:29446-29453.
32. McClain MS, Cover TL (2007) Functional analysis of neutralizing antibodies against Clostridium perfringens epsilon-toxin. Infect Immun 75:1785-1793. (Pubitemid 46559446)
33. De Colibus L, Sonnen AF, Morris KJ, Siebert CA, Abrusci P, Plitzko J, Hodnik V, Leippe M, Volpi E, Anderluh G, Gilbert RJ (2012) Structures of lysenin reveal a shared evolutionary origin for pore-forming proteins and its mode of sphingomyelin recognition. Structure 20:1498-1507.
34. Dorca-Arevalo J, Martin-Satue M, Blasi J (2012) Characterization of the high affinity binding of epsilon toxin from Clostridium perfringens to the renal system. Vet Microbiol 157:179-189.
35. Nagahama M, Sakurai J (1992) High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain. Infect Immun 60:1237-1240.
36. Pflugrath JW (1999) The finer things in X-ray diffraction data collection. Acta Crystallogr D Biol Crystallogr 55:1718-1725. (Pubitemid 29504426)
37. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 41:658-674. (Pubitemid 47080256)
38. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
39. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximumlikelihood method. Acta Cryst D53:240-255. (Pubitemid 27235885)
40. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Cryst D Biol Crystallogr 66:486-501.
41. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, 3rd, Snoeyink J, Richardson JS, Richardson DC (2007) Mol-Probity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
42. The PyMOL Molecular Graphics System, Version 1.3r1 (2010) Schrödinger LLC. http://www.pymol.org/citing.