Why are botulinum neurotoxin-producing bacteria so diverse and botulinum neurotoxins so toxic?

Toxins

Volumn 11, Issue 1, 2019, Pages

  Poulain, Bernard ^a   Popoff, Michel R ^b  

^a Institut des Neurosciences Cellulaires et Intégratives UPR3212   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

Botulinum neurotoxins; Botulism; Clostridium botulinum; Neuroexocytosis; SNARE proteins

Indexed keywords

BOTULINUM TOXIN; DIPHTHERIA TOXIN; HEMAGGLUTININ; RNA 16S; SYNAPTOBREVIN; SYNTAXIN; VACCINE; NEUROTOXIN;

BACTERIAL GENE; BACTERIAL SPORE; BLOOD BRAIN BARRIER; BOTULINUM NEUROTOXIN GENE; BOTULISM; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM SORDELLII; DYSAUTONOMIA; ENTEROCOCCUS FAECIUM; EXOCYTOSIS; GENETIC VARIABILITY; MICROBIAL DIVERSITY; MULTILOCUS SEQUENCE TYPING; NERVE ENDING; NEUROTOXICITY; NONHUMAN; PHENOTYPE; RESPIRATORY DISTRESS; REVIEW; TEMPERATURE; TOXICITY TESTING; ANIMAL; BACTERIUM; BIODIVERSITY; DRUG EFFECT; HUMAN; METABOLISM; SYNAPSE VESICLE;

ANIMALS; BACTERIA; BIODIVERSITY; BOTULINUM TOXINS; HUMANS; NEUROTOXINS; SYNAPTIC VESICLES;

EID: 85060010373     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins11010034     Document Type: Review

References (123)

1. Johnson, E.A. Clostridial toxins as therapeuic agents: Benefits and nature’s most toxic proteins. Annu. Rev. Microbiol. 1999, 53, 551-575.
2. Schantz, E.J.; Johnson, E.A. Properties and use of botulinum toxin and other microbial neurotoxins in medicine. Microbiol. Rev. 1992, 56, 80-99.
3. Peck, M.W. Clostridium botulinum and the safety of minimally heated, chilled foods: An emerging issue? J. Appl. Microbiol. 2006, 101, 556-570.
4. Barash, J.R.; Arnon, S.S. A Novel Strain of Clostridium botulinum That Produces Type B and Type H Botulinum Toxins. J. Infect. Dis. 2014, 209, 183-191.
5. Maslanka, S.E.; Luquez, C.; Dykes, J.K.; Tepp, W.H.; Pier, C.L.; Pellett, S.; Raphael, B.H.; Kalb, S.R.; Barr, J.R.; Rao, A.; et al. A Novel Botulinum Neurotoxin, Previously Reported as Serotype H, Has a Hybrid-Like Structure with Regions of Similarity to the Structures of Serotypes A and F and Is Neutralized with Serotype A Antitoxin. J. Infect. Dis. 2016, 213, 379-385.
6. Pellett, S.; Tepp,W.H.; Bradshaw, M.; Kalb, S.R.; Dykes, J.K.; Lin, G.; Nawrocki, E.M.; Pier, C.L.; Barr, J.R.; Maslanka, S.E.; et al. Purification and Characterization of Botulinum Neurotoxin FA from a Genetically Modified Clostridium botulinum Strain. mSphere 2016, 1.
7. Zhang, S.; Masuyer, G.; Zhang, J.; Shen, Y.; Lundin, D.; Henriksson, L.; Miyashita, S.I.; Martinez-Carranza, M.; Dong, M.; Stenmark, P. Identification and characterization of a novel botulinum neurotoxin. Nat. Commun.2017, 8, 14130.
8. Peck, M.W.; Smith, T.J.; Anniballi, F.; Austin, J.W.; Bano, L.; Bradshaw, M.; Cuervo, P.; Cheng, L.W.; Derman, Y.; Dorner, B.G.; et al. Historical Perspectives and Guidelines for Botulinum Neurotoxin Subtype Nomenclature. Toxins (Basel) 2017, 9, 38.
9. Gu, S.; Rumpel, S.; Zhou, J.; Strotmeier, J.; Bigalke, H.; Perry, K.; Shoemaker, C.B.; Rummel, A.; Jin, R. Botulinum neurotoxin is shielded by NTNHA in an interlocked complex. Science 2012, 335, 977-981.
10. Gu, S.; Jin, R. Assembly and function of the botulinum neurotoxin progenitor complex. Curr. Top. Microbiol. Immunol. 2013, 364, 21-44.
11. Peck, M.W.; Stringer, S.C.; Carter, A.T. Clostridium botulinum in the post-genomic era. Food Microbiol. 2011, 28, 183-191.
12. Popoff, M.R.; Mazuet, C.; Poulain, B. Botulism and Tetanus. In The Prokaryotes: Human Microbiology, 4th ed.; Springer: Berlin/Heidelberg, Germany, 2013; Volume 5, pp. 247-290.
13. Anniballi, F.; Fillo, S.; Giordani, F.; Auricchio, B.; Tehran, D.A.; di Stefano, E.; Mandarino, G.; De Medici, D.; Lista, F. Multiple-locus variable number of tandem repeat analysis as a tool for molecular epidemiology of botulism: The Italian experience. Infect. Genet. Evol. 2016, 46, 28-32.
14. Fillo, S.; Giordani, F.; Anniballi, F.; Gorge, O.; Ramisse, V.; Vergnaud, G.; Riehm, J.M.; Scholz, H.C.; Splettstoesser, W.D.; Kieboom, J.; et al. Clostridium botulinum Group I Strain Genotyping by 15-Locus Multilocus Variable-Number Tandem-Repeat Analysis. J. Clin. Microbiol. 2011, 49, 4252-4263.
15. Jacobson, M.J.; Lin, G.; Whittam, T.S.; Johnson, E.A. Phylogenetic analysis of Clostridium botulinum type A by multi-locus sequence typing. Microbiology 2008, 154, 2408-2415.
16. Macdonald, T.E.; Helma, C.H.; Ticknor, L.O.; Jackson, P.J.; Okinaka, R.T.; Smith, L.A.; Smith, T.J.; Hill, K.K. Differentiation of Clostridium botulinum serotype A strains by multiple-locus variable-number tandem-repeat analysis. Appl. Environ. Microbiol. 2008, 74, 875-882.
17. Umeda, K.; Wada, T.; Kohda, T.; Kozaki, S. Multi-locus variable number tandem repeat analysis for Clostridium botulinum type B isolates in Japan: Comparison with other isolates and genotyping methods. Infect. Genet. Evol. 2013, 16, 298-304.
18. Mazuet, C.; Legeay, C.; Sautereau, J.; Ma, L.; Bouchier, C.; Bouvet, P.; Popoff, M.R. Diversity of Group I and II Clostridium botulinum Strains from France Including Recently Identified Subtypes. Genome Biol. Evol. 2016, 8, 1643-1660.
19. Mansfield, M.J.; Adams, J.B.; Doxey, A.C. Botulinum neurotoxin homologs in non-Clostridium species. FEBS Lett. 2015, 589, 342-348.
20. Strahan, B.L.; Failor, K.C.; Batties, A.M.; Hayes, P.S.; Cicconi, K.M.; Mason, C.T.; Newman, J.D. Chryseobacterium piperi sp. nov., isolated from a freshwater creek. Int. J. Syst. Evol. Microbiol. 2011, 61, 2162-2166.
21. Wentz, T.G.; Muruvanda, T.; Lomonaco, S.; Thirunavukkarasu, N.; Hoffmann, M.; Allard, M.W.; Hodge, D.R.; Pillai, S.P.; Hammack, T.S.; Brown, E.W.; et al. Closed Genome Sequence of Chryseobacterium piperi Strain CTM(T)/ATCC BAA-1782, a Gram-Negative Bacterium with Clostridial Neurotoxin-Like Coding Sequences. Genome Announc. 2017, 5, e01296-17.
22. Brunt, J.; Carter, A.T.; Stringer, S.C.; Peck, M.W. Identification of a novel botulinum neurotoxin gene cluster in Enterococcus. FEBS Lett. 2018, 592, 310-317.
23. Zhang, S.; Lebreton, F.; Mansfield, M.J.; Miyashita, S.I.; Zhang, J.; Schwartzman, J.A.; Tao, L.; Masuyer, G.; Martinez-Carranza, M.; Stenmark, P.; et al. Identification of a Botulinum Neurotoxin-like Toxin in a Commensal Strain of Enterococcus faecium. Cell Host Microbe 2018, 23, 169-176.e6.
24. Hughes, J.M.; Blumenthal, J.R.; Merson, M.H.; Lombard, G.L.; Dowell, V.R., Jr.; Gangarosa, E.J. Clinical features of types A and B food-borne botulism. Ann. Intern. Med. 1981, 95, 442-445.
25. Sobel, J. Botulism. Clin. Infect. Dis. 2005, 41, 1167-1173.
26. Gupta, A.; Sumner, C.J.; Castor, M.; Maslanka, S.; Sobel, J. Adult botulism type F in the United States, 1981-2002. Neurology 2005, 65, 1694-1700.
27. Fenicia, L.; Anniballi, F.; Aureli, P. Intestinal toxemia botulism in Italy, 1984-2005. Eur. J. Clin. Microbiol. Infect. Dis. 2007, 26, 385-394.
28. Rosow, L.K.; Strober, J.B. Infant botulism: Review and clinical update. Pediatr. Neurol. 2015, 52, 487-492.
29. Lindstrôm, M.; Myllykoski, J.; Sivela, S.; Korkeala, H. Clostridium botulinum in cattle and dairy products. Crit. Rev. Food Sci. Nutr. 2010, 50, 281-304.
30. Uzal, F.; Songer, J.G.; Prescott, J.F.; Popoff, M.R. Clostridial Diseases of Animals;Wiley Balckwell: Ames, IA, USA, 2016; p. 332.
31. Espelund, M.; Klaveness, D. Botulism outbreaks in natural environments-An update. Front. Microbiol. 2014, 5, 287.
32. Benoit, R.M. Botulinum Neurotoxin Diversity from a Gene-Centered View. Toxins (Basel) 2018, 10, 310.
33. Carter, A.T.; Peck, M.W. Genomes, neurotoxins and biology of Clostridium botulinum Group I and Group II. Res. Microbiol. 2015, 166, 303-317.
34. Lund, B.M.; Peck, M.W. Clostridium botulinum. In Guide to Foodborne Pathogens; Labbé, R.G., Garcia, S., Eds.; John Willey: New York, NY, USA, 2001; pp. 69-85.
35. Fujinaga, Y.; Popoff, M.R. Translocation and dissemination of botulinum neurotoxin from the intestinal tract. Toxicon 2018, 147, 13-18.
36. Simpson, L. The life history of a botulinum toxin molecule. Toxicon 2013, 68, 40-59.
37. Connan, C.; Popoff, M.R. Uptake of Clostridial Neurotoxins into Cells and Dissemination. Curr. Top. Microbiol. Immunol. 2017, 406, 39-78.
38. Fujinaga, Y.; Sugawara, Y.; Matsumura, T. Uptake of botulinum neurotoxin in the intestine. Curr. Top. Microbiol. Immunol. 2013, 364, 45-59.
39. Poulain, B.; Molgo, J.; Popoff, M.R. Clostridial neurotoxins: From the cellular and molecular mode of action to their therapeutic use. In The Comprehensive Sourcebook of Bacterial Protein Toxins, 4th ed.; Alouf, J., Ladant, D., Popoff, M.R., Eds.; Elsevier: Amsterdam, The Netherlands, 2015; pp. 287-336.
40. Poulain, B.; Popoff, M.R.; Molgo, J. How do the botulinum neurotoxins block neurotransmitter release: From botulism to the molecular mechanism of action. Botulinum J. 2008, 1, 14-87.
41. Mazzocchio, R.; Caleo, M. More than at the neuromuscular synapse: Actions of botulinum neurotoxin A in the central nervous system. Neuroscientist 2015, 21, 44-61.
42. Rummel, A. Two Feet on the Membrane: Uptake of Clostridial Neurotoxins. Curr. Top. Microbiol. Immunol.2017, 406, 1-37.
43. Lam, K.H.; Yao, G.; Jin, R. Diverse binding modes, same goal: The receptor recognition mechanism of botulinum neurotoxin. Prog. Biophys. Mol. Biol. 2015, 117, 225-231.
44. Yowler, B.C.; Kensinger, R.D.; Schengrund, C.L. Botulinum neurotoxin A activity is dependent upon the presence of specific gangliosides in neuroblastoma cells expressing synaptotagmin I. J. Biol. Chem. 2002, 277, 32815-32819.
45. Nishiki, T.; Tokuyama, Y.; Kamata, Y.; Nemoto, Y.; Yoshida, A.; Sekiguchi, M.; Takahashi, M.; Kozaki, S. Binding of botulinum type B neurotoxin to Chinese hamster ovary cells transfected with rat synaptotagmin II cDNA. Neurosci. Lett. 1996, 208, 105-108.
46. Fu, Z.; Chen, C.; Barbieri, J.T.; Kim, J.J.; Baldwin, M.R. Glycosylated SV2 and gangliosides as dual receptors for botulinum neurotoxin serotype F. Biochemistry 2009, 48, 5631-5641.
47. Iwamori, M.; Shimomura, J.; Tsuyuhara, S.; Nagai, Y. Gangliosides of various rat tissues: Distribution of ganglio-N-tetraose-containing gangliosides and tissue-characteristic composition of gangliosides. J. Biochem.1984, 95, 761-770.
48. Kolter, T. Ganglioside biochemistry. ISRN Biochem. 2012, 2012, 506160.
49. Yao, G.; Zhang, S.; Mahrhold, S.; Lam, K.H.; Stern, D.; Bagramyan, K.; Perry, K.; Kalkum, M.; Rummel, A.; Dong, M.; et al. N-linked glycosylation of SV2 is required for binding and uptake of botulinum neurotoxin A. Nat. Struct. Mol. Biol. 2016, 23, 656-662.
50. Dong, M.; Liu, H.; Tepp, W.H.; Johnson, E.A.; Janz, R.; Chapman, E.R. Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol. Biol. Cell 2008, 19, 5226-5237.
51. Bourdoulous, S.; Lemichez, E. Decoding glycan recognition by bacterial toxins. Nat. Microbiol. 2018, 3, 124-126.
52. Stern, D.; Weisemann, J.; Le Blanc, A.; von Berg, L.; Mahrhold, S.; Piesker, J.; Laue, M.; Luppa, P.B.; Dorner, M.B.; Dorner, B.G.; et al. A lipid-binding loop of botulinum neurotoxin serotypes B, DC and G is an essential feature to confer their exquisite potency. PLoS Pathog. 2018, 14, e1007048.
53. Desplantes, R.; Leveque, C.; Muller, B.; Lotierzo, M.; Ferracci, G.; Popoff, M.; Seagar, M.; Mamoun, R.; El Far, O. Affinity biosensors using recombinant native membrane proteins displayed on exosomes: Application to botulinum neurotoxin B receptor. Sci. Rep. 2017, 7, 1032.
54. Fischer, A.; Montal, M. Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes. J. Biol. Chem. 2007, 282, 29604-29611.
55. Koriazova, L.K.; Montal, M. Translocation of botulinum neurotoxin light chain protease through the heavy chain channel. Nat. Struct. Biol. 2003, 10, 13-18.
56. Montal, M. Botulinum Neurotoxin: A Marvel of Protein Design. Annu. Rev. Biochem. 2010, 79, 591-617.
57. Surana, S.; Tosolini, A.P.; Meyer, I.F.G.; Fellows, A.D.; Novoselov, S.S.; Schiavo, G. The travel diaries of tetanus and botulinum neurotoxins. Toxicon 2018, 147, 58-67.
58. Wang, J.; Meng, J.; Nugent, M.; Tang, M.; Dolly, J.O. Neuronal entry and high neurotoxicity of botulinum neurotoxin A require its N-terminal binding sub-domain. Sci. Rep. 2017, 7, 44474.
59. Nishiki, T.; Kamata, Y.; Nemoto, Y.; Omori, A.; Ito, T.; Takahashi, M.; Kozaki, S. Identification of protein receptor for Clostridium botulinum type B neurotoxin in rat brain synaptosomes. J. Biol. Chem. 1994, 269, 10498-10503.
60. Tao, L.; Peng, L.; Berntsson, R.P.; Liu, S.M.; Park, S.; Yu, F.; Boone, C.; Palan, S.; Beard, M.; Chabrier, P.E.; et al. Engineered botulinum neurotoxin B with improved efficacy for targeting human receptors. Nat. Commun.2017, 8, 53.
61. Iwamoto, R.; Higashiyama, S.; Mitamura, T.; Taniguchi, N.; Klagsbrun, M.; Mekada, E. Heparin-binding EGF-like growth factor, which acts as the diphtheria toxin receptor, forms a complex with membrane protein DRAP27/CD9, which up-regulates functional receptors and diphtheria toxin sensitivity. EMBO J. 1994, 13, 2322-2330.
62. Shishido, Y.; Sharma, K.D.; Higashiyama, S.; Klagsbrun, M.; Mekada, E. Heparin-like molecules on the cell surface potentiate binding of diphtheria toxin to the diphtheria toxin receptor/membrane-anchored heparin-binding epidermal growth factor-like growth factor. J. Biol. Chem. 1995, 270, 29578-29585.
63. Wigelsworth, D.J.; Krantz, B.A.; Christensen, K.A.; Lacy, D.B.; Juris, S.J.; Collier, R.J. Binding stoichiometry and kinetics of the interaction of a human anthrax toxin receptor, CMG2, with protective antigen. J. Biol. Chem.2004, 279, 23349-23356.
64. Scobie, H.M.; Thomas, D.; Marlett, J.M.; Destito, G.; Wigelsworth, D.J.; Collier, R.J.; Young, J.A.; Manchester, M. A soluble receptor decoy protects rats against anthrax lethal toxin challenge. J. Infect. Dis. 2005, 192, 1047-1051.
65. Nagahama, M.; Sakurai, J. High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain. Infect. Immun. 1992, 60, 1237-1240.
66. Varela Chavez, C.; Hoos, S.; Haustant, G.M.; Chenal, A.; England, P.; Blondel, A.; Pauillac, S.; Lacy, D.B.; Popoff, M.R. The catalytic domains of Clostridium sordellii lethal toxin and related large clostridial glucosylating toxins specifically recognize the negatively charged phospholipids phosphatidylserine and phosphatidic acid. Cell. Microbiol. 2015, 17, 1477-1493.
67. Schiavo, G.; Rossetto, O.; Santucci, A.; DasGupta, B.R.; Montecucco, C. Botulinum neurotoxins are zinc proteins. J. Biol. Chem. 1992, 267, 23479-23483.
68. Pirazzini, M.; Rossetto, O.; Eleopra, R.; Montecucco, C. Botulinum Neurotoxins: Biology, Pharmacology, and Toxicology. Pharmacol. Rev. 2017, 69, 200-235.
69. Rossetto, O.; Schiavo, G.; Montecucco, C.; Poulain, B.; Deloye, F.; Lozzi, L.; Shone, C.C. SNARE motif and neurotoxins. Nature 1994, 372, 415-416.
70. Brunger, A.T.; Rummel, A. Receptor and substrate interactions of clostridial neurotoxins. Toxicon 2009, 54, 550-560.
71. Tsai, Y.C.; Moller, B.E.; Adler, M.; Oyler, G.A. Molecular basis for persistence of botulinum neurotoxin: THE role of intracellular protein degradation pathways. In Molecular Aspects of Botulinum Neurotoxin; Foster, K.A., Ed.; Springer: New York, NY, USA, 2014; pp. 191-205.
72. Tsai, Y.C.; Kotiya, A.; Kiris, E.; Yang, M.; Bavari, S.; Tessarollo, L.; Oyler, G.A.; Weissman, A.M. Deubiquitinating enzyme VCIP135 dictates the duration of botulinum neurotoxin type A intoxication. Proc. Natl. Acad. Sci. USA 2017, 114, E5158-E5166.
73. Tsai, Y.C.; Maditz, R.; Kuo, C.L.; Fishman, P.S.; Shoemaker, C.B.; Oyler, G.A.; Weissman, A.M. Targeting botulinum neurotoxin persistence by the ubiquitin-proteasome system. Proc. Natl. Acad. Sci. USA 2010, 107, 16554-16559.
74. Pellett, S.; Bradshaw, M.; Tepp,W.H.; Pier, C.L.; Whitemarsh, R.C.M.; Chen, C.; Barbieri, J.T.; Johnson, E.A. The Light Chain Defines the Duration of Action of Botulinum Toxin Serotype A Subtypes. MBio 2018, 9, e00089-18.
75. Megighian, A.; Zordan, M.; Pantano, S.; Scorzeto, M.; Rigoni, M.; Zanini, D.; Rossetto, O.; Montecucco, C. Evidence for a radial SNARE super-complex mediating neurotransmitter release at the Drosophila neuromuscular junction. J. Cell Sci. 2013, 126, 3134-3140.
76. Pantano, S.; Montecucco, C. The blockade of the neurotransmitter release apparatus by botulinum neurotoxins. Cell. Mol. Life Sci. 2014, 71, 793-811.
77. Binz, T.; Bade, S.; Rummel, A.; Kollewe, A.; Alves, J. Arg(326) and Tyr(365) of the botulinum neurotoxin type A light chain are involved in transition state stabilization. Biochemistry 2002, 41, 1717-1723.
78. Lebeda, F.J.; Cer, R.Z.; Mudunuri, U.; Stephens, R.; Singh, B.R.; Adler, M. The zinc-dependent protease activity of the botulinum neurotoxins. Toxins (Basel) 2010, 2, 978-997.
79. Wang, D.; Krilich, J.; Pellett, S.; Baudys, J.; Tepp,W.H.; Barr, J.R.; Johnson, E.A.; Kalb, S.R. Comparison of the catalytic properties of the botulinum neurotoxin subtypes A1 and A5. Biochim. Biophys. Acta 2013, 1834, 2722-2728.
80. Beaumont, A.; O’Donohue, M.J.; Paredes, N.; Rousselet, N.; Assicot, M.; Bohuon, C.; Fournie-Zaluski, M.C.; Roques, B.P. The role of histidine 231 in thermolysin-like enzymes. A site-directed mutagenesis study. J. Biol. Chem. 1995, 270, 16803-16808.
81. Humeau, Y.; Doussau, F.; Grant, N.J.; Poulain, B. How botulinum and tetanus neurotoxins block neurotransmitter release. Biochimie 2000, 82, 427-446.
82. Humeau, Y.; Doussau, F.; Popoff, M.R.; Benfenati, F.; Poulain, B. Fast changes in the functional status of release sites during short-term plasticity: Involvement of a frequency-dependent bypass of Rac at Aplysia synapses. J. Physiol. 2007, 583, 983-1004.
83. Burgen, A.S.; Dickens, F.; Zatman, L.J. The action of botulinum toxin on the neuro-muscular junction. J. Physiol. 1949, 109, 10-24.
84. Burakgazi, A.Z.; Hoke, A. Respiratory muscle weakness in peripheral neuropathies. J. Peripher. Nerv. Syst.2010, 15, 307-313.
85. Weisemann, J.; Krez, N.; Fiebig, U.; Worbs, S.; Skiba, M.; Endermann, T.; Dorner, M.B.; Bergstrom, T.; Munoz, A.; Zegers, I.; et al. Generation and Characterization of Six Recombinant Botulinum Neurotoxins as Reference Material to Serve in an International Proficiency Test. Toxins (Basel) 2015, 7, 5035-5054.
86. Worbs, S.; Fiebig, U.; Zeleny, R.; Schimmel, H.; Rummel, A.; Luginbuhl, W.; Dorner, B.G. Qualitative and Quantitative Detection of Botulinum Neurotoxins from Complex Matrices: Results of the First International Proficiency Test. Toxins (Basel) 2015, 7, 4935-4966.
87. Rasetti-Escargueil, C.; Jones, R.G.; Liu, Y.; Sesardic, D. Measurement of botulinum types A, B and E neurotoxicity using the phrenic nerve-hemidiaphragm: Improved precision with in-bred mice. Toxicon 2009, 53, 503-511.
88. Gill, D.M. Bacterial toxins: A table of lethal amounts. Microbiol. Rev. 1982, 46, 86-94.
89. Popoff, M.R. Purification and characterization of Clostridium sordellii lethal toxin and cross-reactivity with Clostridium difficile cytotoxin. Infect. Immun. 1987, 55, 35-43.
90. Petit, L.; Maier, E.; Gibert, M.; Popoff, M.R.; Benz, R. Clostridium perfringens epsilon-toxin induces a rapid change in cell membrane permeability to ions and forms channels in artificial lipid bilayers. J. Biol. Chem.2001, 276, 15736-15740.
91. Popoff, M.R. Epsilon toxin: A fascinating pore-forming toxin. FEBS J. 2011, 278, 4602-4615.
92. Collier, R.J. Diphtheria toxin: Mode of action and structure. Bacteriol. Rev. 1975, 39, 54-85.
93. Wioland, L.; Dupont, J.L.; Bossu, J.L.; Popoff, M.R.; Poulain, B. Attack of the nervous system by Clostridium perfringens Epsilon toxin: From disease to mode of action on neural cells. Toxicon 2013, 75, 122-135.
94. Skarin, H.; Segerman, B. Horizontal gene transfer of toxin genes in Clostridium botulinum: Involvement of mobile elements and plasmids. Mob. Genet. Elem. 2011, 1, 213-215.
95. Marshall, K.M.; Bradshaw, M.; Johnson, E.A. Conjugative Botulinum Neurotoxin-Encoding Plasmids in Clostridium botulinum. PLoS ONE 2010, 5, e11087.
96. Nawrocki, E.M.; Bradshaw, M.; Johnson, E.A. Botulinum neurotoxin-encoding plasmids can be conjugatively transferred to diverse clostridial strains. Sci. Rep. 2018, 8, 3100.
97. Hill, K.K.; Smith, T.J.; Helma, C.H.; Ticknor, L.O.; Foley, B.T.; Svensson, R.T.; Brown, J.L.; Johnson, E.A.; Smith, L.A.; Okinaka, R.T.; et al. Genetic diversity among Botulinum Neurotoxin-producing clostridial strains. J. Bacteriol. 2007, 189, 818-832.
98. Hill, K.K.; Smith, T.J. Genetic diversity within Clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes. Curr. Top. Microbiol. Immunol. 2013, 364, 1-20.
99. Hill, K.K.; Xie, G.; Foley, B.T.; Smith, T.J. Genetic diversity within the botulinum neurotoxin-producing bacteria and their neurotoxins. Toxicon 2015, 107, 2-8.
100. DasGupta, B.R. Botulinum neurotoxins: Perspective on their existence and as polyproteins harboring viral proteases. J. Gen. Appl. Microbiol. 2006, 52, 1-8.
101. Sakaguchi, Y.; Hayashi, H.; Kurokawa, K.; Nakayama, K.; Oshima, K.; Fujinaga, Y.; Ohnishi, M.; Ohtsubo, E.; Hattori, M.; Oguma, K. The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. Proc. Natl. Acad. Sci. USA 2005, 102, 17472-17477.
102. Smith, L.D. The occurence of Clostridium botulinum and Clostridium tetani in the soil of the United States. Health Lab. Sci. 1978, 15, 74-80.
103. Dodds, K.L. Clostridium botulinum in the environment. In Clostridium botulinum: Ecology and Control in Foods; Hauschild, A.H.W., Dodds, K.L., Eds.; Marcel Dekker, Inc.: New York, NY, USA, 1993; pp. 21-51.
104. Hauschild, A.H.W. Clostridium botulinum. In Foodborne Bacterial Pathogens; Doyle, M.P., Ed.; Marcel Dekker, Inc.: New York, NY, USA, 1989; pp. 111-189.
105. Dahlenborg, M.; Borch, E.; Radstrom, P. Development of a combined selection and enrichment PCR procedure for Clostridium botulinum Types B, E, and F and its use to determine prevalence in fecal samples from slaughtered pigs. Appl. Environ. Microbiol. 2001, 67, 4781-4788.
106. Myllykoski, J.; Nevas, M.; Lindstrôm, M.; Korkeala, H. The detection and prevalence of Clostridium botulinum in pig intestinal samples. Int. J. Food Microbiol. 2006, 110, 172-177.
107. Wang, X.; Hoefel, D.; Saint, C.P.; Monis, P.T.; Jin, B. The isolation and microbial community analysis of hydrogen producing bacteria from activated sludge. J. Appl. Microbiol. 2007, 103, 1415-1423.
108. Mallet, C.; Basset, M.; Fonty, G.; Desvilettes, C.; Bourdier, G.; Debroas, D. Microbial population dynamics in the sediments of a eutrophic lake (Aydat, France) and characterization of some heterotrophic bacterial isolates. Microb. Ecol. 2004, 48, 66-77.
109. Weigand, M.R.; Pena-Gonzalez, A.; Shirey, T.B.; Broeker, R.G.; Ishaq, M.K.; Konstantinidis, K.T.; Raphael, B.H. Implications of Genome-Based Discrimination between Clostridium botulinum Group I and Clostridium sporogenes Strains for Bacterial Taxonomy. Appl. Environ. Microbiol. 2015, 81, 5420-5429.
110. Nakamura, S.; Okado, I.; Nakashio, S.; Nishida, S. Clostridium sporogenes isolates and their relationship to C. botulinum based on deoxyribonucleic acid reassociation. J. Gen. Microbiol. 1977, 100, 395-401.
111. Drouin, P.; Lafrenière, C. Clostridial spores in animal feeds and milk. In Milk Production; Chaiyabutr, N., Ed.; IntechOpen: Rijeka, Croatia, 2012.
112. Butler, R.R., 3rd; Schill, K.M.; Wang, Y.; Pombert, J.F. Genetic Characterization of the Exceptionally High Heat Resistance of the Non-toxic Surrogate Clostridium sporogenes PA 3679. Front. Microbiol. 2017, 8, 545.
113. Taylor, R.H.; Dunn, M.L.; Ogden, L.V.; Jefferies, L.K.; Eggett, D.L.; Steele, F.M. Conditions associated with Clostridium sporogenes growth as a surrogate for Clostridium botulinum in nonthermally processed canned butter. J. Dairy Sci. 2013, 96, 2754-2764.
114. Jahn, R.; Scheller, R.H. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 2006, 7, 631-643.
115. Hubalek, Z.; Halouzka, J. Persistence of Clostridium botulinum type C toxin in blow fly (Calliphoridae) larvae as a possible cause of avian botulism in spring. J. Wildl. Dis. 1991, 27, 81-85.
116. Anza, I.; Vidal, D.; Feliu, J.; Crespo, E.; Mateo, R. Differences in the Vulnerability of Waterbird Species to Botulism Outbreaks in MediterraneanWetlands: An Assessment of Ecological and Physiological Factors. Appl. Environ. Microbiol. 2016, 82, 3092-3099.
117. Poulain, B.; Tauc, L.; Maisey, E.A.; Wadsworth, J.D.; Mohan, P.M.; Dolly, J.O. Neurotransmitter release is blocked intracellularly by botulinum neurotoxin, and this requires uptake of both toxin polypeptides by a process mediated by the larger chain. Proc. Natl. Acad. Sci. USA 1988, 85, 4090-4094.
118. Janz, R.; Südhof, T.C. SV2C is a synaptic vesicle protein with an unusually restricted localization: Anatomy of a synaptic vesicle protein family. Neuroscience 1999, 94, 1279-1290.
119. Montecucco, C.; Rasotto, M.B. On botulinum neurotoxin variability. MBio 2015, 6.
120. Nevas, M.; Lindström, M.; Hielm, S.; Björkroth, K.J.; Peck, M.W.; Korkeala, H. Diversity of proteolytic Clostridium botulinum strains, determined by a pulse-field gel electrophoresis approach. Appl. Environ. Microbiol. 2005, 71, 1311-1317.
121. Peck, M.W. Biology and genomic analysis of Clostridium botulinum. Adv. Microb. Physiol. 2009, 55, 183-265, 320.
122. Erbguth, F.J. From poison to remedy: The chequered history of botulinum toxin. J. Neural Transm. 2008, 115, 559-565.
123. Erbguth, F.J.; Naumann, M. Historical aspects of botulinum toxin. Justinus Kerner (1786-1862) and the “sausage poison”. Neurology 1999, 53, 1850-1853.