F199E substitution reduced toxicity of Clostridium perfringens epsilon toxin by depriving the receptor binding capability

References

• Borrmann E, Gunther H, Kohler H. Effect of Clostridium perfringens epsilon toxin on MDCK cells. FEMS Immunol Med Microbiol 2001; 31:85-92; PMID:11549414
   PubMedGoogle Scholar
• Popoff MR. Epsilon toxin: a fascinating pore-forming toxin. FEBS J 2011; 278:4602-15; PMID:21535407; https://doi.org/10.1111/j.1742-4658.2011.08145.x
   PubMed Web of Science ®Google Scholar
• Stiles BG, Barth G, Barth H, Popoff MR. Clostridium perfringens epsilon toxin: a malevolent molecule for animals and man? Toxins 2013; 5:2138-60; PMID:24284826; https://doi.org/10.3390/toxins5112138
   PubMed Web of Science ®Google Scholar
• Minami J, Katayama S, Matsushita O, Matsushita C, Okabe A. Lambda-toxin of Clostridium perfringens activates the precursor of epsilon-toxin by releasing its N- and C-terminal peptides. Microbiol Immunol 1997; 41:527-35; PMID:9272698
   PubMed Web of Science ®Google Scholar
• Worthington RW, Mulders MS. Physical changes in the epsilon prototoxin molecule of Clostridium perfringens during enzymatic activation. Infect Immun 1977; 18:549-51; PMID:200566
   PubMed Web of Science ®Google Scholar
• Li Q, Xin W, Gao S, Kang L, Wang J. A low-toxic site-directed mutant of Clostridium perfringens epsilon-toxin as a potential candidate vaccine against enterotoxemia. Hum Vaccin Immunother 2013; 9:2386-92; PMID:23835363
   PubMed Web of Science ®Google Scholar
• Petit L, Gibert M, Gillet D, Laurent-Winter C, Boquet P, Popoff MR. Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex. J Bacteriol 1997; 179:6480-7; PMID:9335299
   PubMed Web of Science ®Google Scholar
• Centers for Disease Control and Prevention (CDC). Fatal foodborne Clostridium perfringens illness at a state psychiatric hospital–Louisiana, 2010. MMWR Morb Mortal Wkly Rep 2012; 61:605-8; PMID:22895383
   PubMedGoogle Scholar
• Bennett SD, Walsh KA, Gould LH. Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus–United States, 1998–2008. Clin Infect Dis 2013; 57:425-33; PMID:23592829; https://doi.org/10.1093/cid/cit244
   PubMed Web of Science ®Google Scholar
• Fernandez Miyakawa ME, Zabal O, Silberstein C. Clostridium perfringens epsilon toxin is cytotoxic for human renal tubular epithelial cells. Hum Exp Toxicol 2011; 30:275-82; PMID:20488848; https://doi.org/10.1177/0960327110371700
   PubMed Web of Science ®Google Scholar
• Bokori-Brown M, Savva CG, Fernandes da Costa SP, Naylor CE, Basak AK, Titball RW. Molecular basis of toxicity of Clostridium perfringens epsilon toxin. FEBS J 2011; 278:4589-601; PMID:21518257; https://doi.org/10.1111/j.1742-4658.2011.08140.x
   PubMed Web of Science ®Google Scholar
• Habeeb AF, Lee CL, Atassi MZ. Conformational studies on modified proteins and peptides. VII. Conformation of epsilon-prototoxin and epsilon-toxin from Clostridium perfringens. Conformational changes associated with toxicity. Biochim Biophys Acta 1973; 322:245-50; PMID:4358084
   PubMed Web of Science ®Google Scholar
• Bokori-Brown M, Kokkinidou MC, Savva CG, Fernandes da Costa S, Naylor CE, Cole AR, Naylor CE, Cole AR, Moss DS, et al. Clostridium perfringensepsilon toxin H149A mutant as a platform for receptor binding studies. Protein Sci 2013; 22:650-9; PMID:23504825; https://doi.org/10.1002/pro.2250
   PubMed Web of Science ®Google Scholar
• Ivie SE, McClain MS. Identification of amino acids important for binding of Clostridium perfringens epsilon toxin to host cells and to HAVCR1. Biochemistry (Mosc) 2012; 51:7588-95; PMID:22938730; https://doi.org/10.1021/bi300690a
   PubMed Web of Science ®Google Scholar
• Cole AR, Gibert M, Popoff M, Moss DS, Titball RW, Basak AK. Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin. Nat Struct Mol Biol 2004; 11:797-8; PMID:15258571; https://doi.org/10.1038/nsmb804
   PubMed Web of Science ®Google Scholar
• Nestorovich EM, Karginov VA, Bezrukov SM. Polymer partitioning and ion selectivity suggest asymmetrical shape for the membrane pore formed by epsilon toxin. Biophys J 2010; 99:782-9; PMID:20682255; https://doi.org/10.1016/j.bpj.2010.05.014
   PubMed Web of Science ®Google Scholar
• Ivie SE, Fennessey CM, Sheng J, Rubin DH, McClain MS. Gene-trap mutagenesis identifies mammalian genes contributing to intoxication by Clostridium perfringens epsilon-toxin. PLoS One 2011; 6:e17787; PMID:21412435; https://doi.org/10.1371/journal.pone.0017787
   PubMed Web of Science ®Google Scholar
• Oyston PC, Payne DW, Havard HL, Williamson ED, Titball RW. Production of a non-toxic site-directed mutant of Clostridium perfringens epsilon-toxin which induces protective immunity in mice. Microbiology 1998; 144(Pt 2):333-41; PMID:9493371; https://doi.org/10.1099/00221287-144-2-333
   PubMed Web of Science ®Google Scholar
• Beal DR, Titball RW, Lindsay CD. The development of tolerance to Clostridium perfringens type D epsilon-toxin in MDCK and G-402 cells. Hum Exp Toxicol 2003; 22:593-605; PMID:14686482; https://doi.org/10.1191/0960327103ht397oa
   PubMed Web of Science ®Google Scholar
• Soler-Jover A, Blasi J, Gomez de Aranda I, Navarro P, Gibert M, Popoff MR, Martín-Satué M. Effect of epsilon toxin-GFP on MDCK cells and renal tubules in vivo. J Histochem Cytochem 2004; 52:931-42; PMID:15208360; https://doi.org/10.1369/jhc.4A6254.2004
   PubMed Web of Science ®Google Scholar
• Petit L, Maier E, Gibert M, Popoff MR, Benz R. Clostridium perfringens epsilon toxin induces a rapid change of cell membrane permeability to ions and forms channels in artificial lipid bilayers. J Biol Chem 2001; 276:15736-40; PMID:11278669; https://doi.org/10.1074/jbc.M010412200
   PubMed Web of Science ®Google Scholar
• Uzal FA, Wong JP, Kelly WR, Priest J. Antibody response in goats vaccinated with liposome-adjuvanted Clostridium perfringens type D epsilon toxoid. Vet Res Commun 1999; 23:143-50; PMID:10401718
   PubMed Web of Science ®Google Scholar
• Titball RW. Clostridium perfringens vaccines. Vaccine 2009; 27 Suppl 4:D44-7.
   PubMed Web of Science ®Google Scholar
• Miyata S, Minami J, Tamai E, Matsushita O, Shimamoto S, Okabe A. Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes. J Biol Chem 2002; 277:39463-8; PMID:12177068; https://doi.org/10.1074/jbc.M206731200
   PubMed Web of Science ®Google Scholar
• Nagahama M, Hara H, Fernandez-Miyakawa M, Itohayashi Y, Sakurai J. Oligomerization of Clostridium perfringens epsilon-toxin is dependent upon membrane fluidity in liposomes. Biochemistry (Mosc) 2006; 45:296-302; PMID:16388606; https://doi.org/10.1021/bi051805s
   PubMed Web of Science ®Google Scholar
• Li Q, Xin W, Gao S, Kang L, Wang J. A low-toxic site-directed mutant of Clostridium perfringens epsilon-toxin as a potential candidate vaccine against enterotoxemia. Human Vaccines & Immunotherapeutics 2013; 9:2386-92; PMID:23835363
   PubMed Web of Science ®Google Scholar
• Nagahama M, Sakurai J. High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain. Infect Immun 1992; 60:1237-40; PMID:1541539
   PubMed Web of Science ®Google Scholar
• Harkness JM, Li J, McClane BA. Identification of a lambda toxin-negative Clostridium perfringens strain that processes and activates epsilon prototoxin intracellularly. Anaerobe 2012; 18:546-52; PMID:22982043; https://doi.org/10.1016/j.anaerobe.2012.09.001
   PubMed Web of Science ®Google Scholar
• Rumah KR, Ma Y, Linden JR, Oo ML, Anrather J, Schaeren-Wiemers N, Alonso MA, Fischetti VA, McClain MS, Vartanian T. The Myelin and Lymphocyte Protein MAL Is Required for Binding and Activity of Clostridium perfringens epsilon-Toxin. PLoS Pathog 2015; 11:e1004896; PMID:25993478; https://doi.org/10.1371/journal.ppat.1004896
   PubMed Web of Science ®Google Scholar
• Yao W, Kang L, Gao S, Zhuang X, Zhang T, Yang H, Ji B, Xin W, Wang J. Amino acid residue Y196E substitution and C-terminal peptide synergistically alleviate the toxicity of Clostridium perfringens epsilon toxin. Toxicon 2015; 100:46-52; PMID:25912943; https://doi.org/10.1016/j.toxicon.2015.04.006
   PubMed Web of Science ®Google Scholar
• Chassin C, Bens M, de Barry J, Courjaret R, Bossu JL, Cluzeaud F, Ben Mkaddem S, Gibert M, Poulain B, Popoff MR, et al. Pore-forming epsilon toxin causes membrane permeabilization and rapid ATP depletion-mediated cell death in renal collecting duct cells. Am J Physiol Renal Physiol 2007; 293:F927-37; PMID:17567938; https://doi.org/10.1152/ajprenal.00199.2007
   PubMed Web of Science ®Google Scholar
• Wioland L, Dupont JL, Doussau F, Gaillard S, Heid F, Isope P, Pauillac S, Popoff MR, Bossu JL, Poulain B. Epsilon toxin from Clostridium perfringens acts on oligodendrocytes without forming pores, and causes demyelination. Cell Microbiol 2015; 17:369-88; PMID:25287162; https://doi.org/10.1111/cmi.12373
   PubMed Web of Science ®Google Scholar
• Linden JR, Ma Y, Zhao B, Harris JM, Rumah KR, Schaeren-Wiemers N, Vartanian T. Clostridium perfringens Epsilon Toxin causes selective death of mature Oligodendrocytes and central nervous system demyelination. Mbio 2015; 6:e02513; PMID:26081637; https://doi.org/10.1128/mBio.02513-14
   PubMed Web of Science ®Google Scholar
• Petit L, Gibert M, Gourch A, Bens M, Vandewalle A, Popoff MR. Clostridium perfringens epsilon toxin rapidly decreases membrane barrier permeability of polarized MDCK cells. Cell Microbiol 2003; 5:155-64; PMID:12614459
   PubMed Web of Science ®Google Scholar
• Palmer M, Valeva A, Kehoe M, Bhakdi S. Kinetics of streptolysin O self-assembly. Eur J Biochem 1995; 231:388-95; PMID:7635150
   PubMedGoogle Scholar
• Walker B, Braha O, Cheley S, Bayley H. An intermediate in the assembly of a pore-forming protein trapped with a genetically-engineered switch. Chem Biol 1995; 2:99-105; PMID:9383410
   PubMedGoogle Scholar
• Valeva A, Walev I, Kemmer H, Weis S, Siegel I, Boukhallouk F, Wassenaar TM, Chavakis T, Bhakdi S. Binding of Escherichia coli hemolysin and activation of the target cells is not receptor-dependent. J Biol Chem 2005; 280:36657-63; PMID:16131494; https://doi.org/10.1074/jbc.M507690200
   PubMed Web of Science ®Google Scholar
• Skals M, Jorgensen NR, Leipziger J, Praetorius HA. Alpha-hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proc Natl Acad Sci U S A 2009; 106:4030-5; PMID:16131494; https://doi.org/10.1074/jbc.M507690200
   PubMed Web of Science ®Google Scholar
• Manni MM, Sot J, Goni FM. Interaction of Clostridium perfringens epsilon-toxin with biological and model membranes: A putative protein receptor in cells. Biochim Biophys Acta 2015; 1848:797-804; PMID:25485476; https://doi.org/10.1016/j.bbamem.2014.11.028
   PubMed Web of Science ®Google Scholar
• Lonchamp E, Dupont JL, Wioland L, Courjaret R, Mbebi-Liegeois C, Jover E, Doussau F, Popoff MR, Bossu JL, de Barry J, et al. Clostridium perfringens epsilon toxin targets granule cells in the mouse cerebellum and stimulates glutamate release. PLoS One 2010; 5:e13046; PMID:20941361; https://doi.org/10.1371/journal.pone.0013046
   PubMed Web of Science ®Google Scholar
• Finnie JW. Neurological disorders produced by Clostridium perfringens type D epsilon toxin. Anaerobe 2004; 10:145-50; PMID:16701511; https://doi.org/10.1016/j.anaerobe.2003.08.003
   PubMed Web of Science ®Google Scholar
• Zhao Y, Kang L, Gao S, Zhou Y, Su L, Xin W, Su Y, Wang J. Expression and purification of functional Clostridium perfringens alpha and epsilon toxins in Escherichia coli. Protein Expr Purif 2011; 77:207-13; PMID:21300155; https://doi.org/10.1016/j.pep.2011.02.001
   PubMed Web of Science ®Google Scholar
• Miyata S, Matsushita O, Minami J, Katayama S, Shimamoto S, Okabe A. Cleavage of a C-terminal peptide is essential for heptamerization of Clostridium perfringens epsilon-toxin in the synaptosomal membrane. J Biol Chem 2001; 276:13778-83; PMID:11278924; https://doi.org/10.1074/jbc.M011527200
   PubMed Web of Science ®Google Scholar