Cell entry strategy of clostridial neurotoxins

Journal of Neurochemistry

Volumn 109, Issue 6, 2009, Pages 1584-1595

  Binz, Thomas ^a   Rummel, Andreas ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Botulinum neurotoxin; Exocytosis; Ganglioside; Protein receptor; Synaptic vesicle; Tetanus neurotoxin

Indexed keywords

BOTULINUM TOXIN; CELL RECEPTOR; GANGLIOSIDE; SYNAPTOTAGMIN; SYNAPTOTAGMIN II; TETANUS TOXIN;

BOTULISM; CELL MEMBRANE; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM TETANI; HUMAN; MEMBRANE FUSION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; REVIEW; SYNAPSE VESICLE; TETANUS;

ANIMALS; BOTULINUM TOXINS; ENDOCYTOSIS; GANGLIOSIDES; HUMANS; MODELS, BIOLOGICAL; NEURONS; NEUROTRANSMITTER AGENTS; PROTEIN BINDING; SYNAPTIC VESICLES; TETANUS TOXIN;

ANIMALIA;

EID: 65949090949     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06093.x     Document Type: Review

References (107)

1. Angstrom J., Teneberg S. Karlsson K. A. (1994) Delineation and comparison of ganglioside-binding epitopes for the toxins of Vibrio cholerae, Escherichia coli, and Clostridium tetani: evidence for overlapping epitopes. Proc. Natl Acad. Sci. USA 91, 11859 11863. (Pubitemid 24368563)
2. Antonucci F., Rossi C., Gianfranceschi L., Rossetto O. Caleo M. (2008) Long-distance retrograde effects of botulinum neurotoxin A. J. Neurosci. 28, 3689 3696.
3. Arnon S. S., Schechter R., Maslanka S. E., Jewell N. P. Hatheway C. L. (2006) Human botulism immune globulin for the treatment of infant botulism. N. Engl. J. Med. 354, 462 471. (Pubitemid 43200297)
4. Bajjalieh S. M., Peterson K., Shinghal R. Scheller R. H. (1992) SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257, 1271 1273.
5. Bajjalieh S. M., Peterson K., Linial M. Scheller R. H. (1993) Brain contains two forms of synaptic vesicle protein 2. Proc. Natl Acad. Sci. USA 90, 2150 2154. (Pubitemid 23078583)
6. Baldwin M. R. Barbieri J. T. (2007) Association of botulinum neurotoxin serotypes a and B with synaptic vesicle protein complexes. Biochemistry 46, 3200 3210. (Pubitemid 46449141)
7. Bigalke H. Rummel A. (2005) Medical aspects of toxin weapons. Toxicology 214, 210 220. (Pubitemid 41406261)
8. Bigalke H., Muller H. Dreyer F. (1986) Botulinum A neurotoxin unlike tetanus toxin acts via a neuraminidase sensitive structure. Toxicon 24, 1065 1074. (Pubitemid 17215075)
9. Binz T., Blasi J., Yamasaki S., Baumeister A., Link E., Sudhof T. C., Jahn R. Niemann H. (1994) Proteolysis of SNAP-25 by types E and A botulinal neurotoxins. J. Biol. Chem. 269, 1617 1620. (Pubitemid 24035350)
10. Black J. D. Dolly J. O. (1986) Interaction of 125I-labeled botulinum neurotoxins with nerve terminals. II. Autoradiographic evidence for its uptake into motor nerves by acceptor-mediated endocytosis. J. Cell Biol. 103, 535 544. (Pubitemid 16055049)
11. Blasi J., Chapman E. R., Yamasaki S., Binz T., Niemann H. Jahn R. (1993a) Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin. EMBO J. 12, 4821 4828. (Pubitemid 23330288)
12. Blasi J., Chapman E. R., Link E., Binz T., Yamasaki S., De Camilli P., Sudhof T. C., Niemann H. Jahn R. (1993b) Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 365, 160 163. (Pubitemid 23282061)
13. Brunger A. T., Breidenbach M. A., Jin R., Fischer A., Santos J. S. Montal M. (2007) Botulinum neurotoxin heavy chain belt as an intramolecular chaperone for the light chain. PLoS Pathog. 3, 1191 1194. (Pubitemid 47510272)
14. Bullens R. W., O'Hanlon G. M., Wagner E., Molenaar P. C., Furukawa K., Furukawa K., Plomp J. J. Willison H. J. (2002) Complex gangliosides at the neuromuscular junction are membrane receptors for autoantibodies and botulinum neurotoxin but redundant for normal synaptic function. J. Neurosci. 22, 6876 6884. (Pubitemid 35379145)
15. Chai Q., Arndt J. W., Dong M., Tepp W. H., Johnson E. A., Chapman E. R. Stevens R. C. (2006) Structural basis of cell surface receptor recognition by botulinum neurotoxin B. Nature 444, 1096 1100. (Pubitemid 46018532)
16. Chang W. P. Sudhof T. C. (2009) SV2 renders primed synaptic vesicles competent for Ca2+-induced exocytosis. J. Neurosci. 29, 883 897.
17. Chapman E. R. (2002) Synaptotagmin: a Ca(2+) sensor that triggers exocytosis? Nat. Rev. Mol. Cell Biol. 3, 498 508. (Pubitemid 34733431)
18. Chen C., Baldwin M. R. Barbieri J. T. (2008) Molecular basis for tetanus toxin coreceptor interactions. Biochemistry 47, 7179 7186.
19. Critchley D. R., Habig W. H. Fishman P. H. (1986) Reevaluation of the role of gangliosides as receptors for tetanus toxin. J. Neurochem. 47, 213 222. (Pubitemid 16069193)
20. Custer K. L., Austin N. S., Sullivan J. M. Bajjalieh S. M. (2006) Synaptic vesicle protein 2 enhances release probability at quiescent synapses. J. Neurosci. 26, 1303 1313. (Pubitemid 43237062)
21. Davletov B., Bajohrs M. Binz T. (2005) Beyond BOTOX: advantages and limitations of individual botulinum neurotoxins. Trends Neurosci. 28, 446 452. (Pubitemid 40982558)
22. Dolly J. O., Black J., Williams R. S. Melling J. (1984) Acceptors for botulinum neurotoxin reside on motor nerve terminals and mediate its internalization. Nature 307, 457 460. (Pubitemid 14132060)
23. Dong M., Richards D. A., Goodnough M. C., Tepp W. H., Johnson E. A. Chapman E. R. (2003) Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells. J. Cell Biol. 162, 1293 1303. (Pubitemid 37210885)
24. Dong M., Yeh F., Tepp W. H., Dean C., Johnson E. A., Janz R. Chapman E. R. (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312, 592 596.
25. Dong M., Tepp W. H., Liu H., Johnson E. A. Chapman E. R. (2007) Mechanism of botulinum neurotoxin B and G entry into hippocampal neurons. J. Cell Biol. 179, 1511 1522.
26. Dong M., Liu H., Tepp W. H., Johnson E. A., Janz R. Chapman E. R. (2008) Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol. Biol. Cell 19, 5226 5237.
27. C-fragment of tetanus toxin with carbohydrate subunit complexes provide insight into ganglioside binding. J. Biol. Chem. 275, 8889 8894. (Pubitemid 30180245)
28. Eswaramoorthy S., Kumaran D. Swaminathan S. (2001) Crystallographic evidence for doxorubicin binding to the receptor-binding site in Clostridium botulinum neurotoxin B. Acta Crystallogr. D Biol. Crystallogr. 57, 1743 1746. (Pubitemid 33037762)
29. Evinger C. Erichsen J. T. (1986) Transsynaptic retrograde transport of fragment C of tetanus toxin demonstrated by immunohistochemical localization. Brain Res. 380, 383 388. (Pubitemid 16015562)
30. Feany M. B., Lee S., Edwards R. H. Buckley K. M. (1992) The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70, 861 867.
31. Figueiredo D., Turcotte C., Frankel G., Li Y., Dolly O., Wilkin G., Marriott D., Fairweather N. Dougan G. (1995) Characterization of recombinant tetanus toxin derivatives suitable for vaccine development. Infect. Immun. 63, 3218 3221.
32. Fischer A. Montal M. (2007) Single molecule detection of intermediates during botulinum neurotoxin translocation across membranes. Proc. Natl Acad. Sci. USA 104, 10447 10452. (Pubitemid 47185685)
33. Fischer A., Mushrush D. J., Lacy D. B. Montal M. (2008) Botulinum neurotoxin devoid of receptor binding domain translocates active protease. PLoS Pathog. 4, e1000245.
34. Fishman P. S. Carrigan D. R. (1987) Retrograde transneuronal transfer of the C-fragment of tetanus toxin. Brain Res. 406, 275 279. (Pubitemid 17048411)
35. C-fragment complexed with a synthetic GT1b analogue suggests cross-linking between ganglioside receptors and the toxin. J. Biol. Chem. 276, 32274 32281. (Pubitemid 37384892)
36. Geppert M., Archer III B. T. Sudhof T. C. (1991) Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J. Biol. Chem. 266, 13548 13552. (Pubitemid 21907384)
37. Gill D. M. (1982) Bacterial toxins: a table of lethal amounts. Microbiol. Rev. 46, 86 94.
38. Halpern J. L. Neale E. A. (1995) Neurospecific binding, internalization, and retrograde axonal transport. Curr. Top. Microbiol. Immunol. 195, 221 241.
39. Herreros J., Lalli G. Schiavo G. (2000a) C-terminal half of tetanus toxin fragment C is sufficient for neuronal binding and interaction with a putative protein receptor. Biochem. J. 347, 199 204. (Pubitemid 30199058)
40. Herreros J., Lalli G., Montecucco C. Schiavo G. (2000b) Tetanus toxin fragment C binds to a protein present in neuronal cell lines and motoneurons. J. Neurochem. 74, 1941 1950. (Pubitemid 30217649)
41. Herreros J., Ng T. Schiavo G. (2001) Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell 12, 2947 2960. (Pubitemid 33062953)
42. van Heyningen W. E. Miller P. A. (1961) The fixation of tetanus toxin by ganglioside. J. Gen. Microbiol. 24, 107 119.
43. Holmgren J., Elwing H., Fredman P. Svennerholm L. (1980) Polystyrene-adsorbed gangliosides for investigation of the structure of the tetanus-toxin receptor. Eur. J. Biochem. 106, 371 379. (Pubitemid 10025772)
44. Hughes R. Whaler B. C. (1962) Influence of nerve-ending activity and of drugs on the rate of paralysis of rat diaphragm preparations by Cl. botulinum type A toxin. J. Physiol. 160, 221 233.
45. Ihara H., Kohda T., Morimoto F., Tsukamoto K., Karasawa T., Nakamura S., Mukamoto M. Kozaki S. (2003) Sequence of the gene for Clostridium botulinum type B neurotoxin associated with infant botulism, expression of the C-terminal half of heavy chain and its binding activity. Biochim. Biophys. Acta 1625, 19 26. (Pubitemid 36084498)
46. Jahn R. Scheller R. H. (2006) SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631 643.
47. Janz R. Sudhof T. C. (1999) SV2C is a synaptic vesicle protein with an unusually restricted localization: anatomy of a synaptic vesicle protein family. Neuroscience 94, 1279 1290. (Pubitemid 29509692)
48. Jayaraman S., Eswaramoorthy S., Kumaran D. Swaminathan S. (2005) Common binding site for disialyllactose and tri-peptide in C-fragment of tetanus neurotoxin. Proteins 61, 288 295. (Pubitemid 41429136)
49. Jin R., Rummel A., Binz T. Brunger A. T. (2006) Botulinum neurotoxin B recognizes its protein receptor with high affinity and specificity. Nature 444, 1092 1095. (Pubitemid 46018531)
50. Keller J. E., Cai F. Neale E. A. (2004) Uptake of botulinum neurotoxin into cultured neurons. Biochemistry 43, 526 532. (Pubitemid 38082576)
51. Kitamura M., Takamiya K., Aizawa S. Furukawa K. (1999) Gangliosides are the binding substances in neural cells for tetanus and botulinum toxins in mice. Biochim. Biophys. Acta 1441, 1 3. (Pubitemid 29469431)
52. Kitamura M., Igimi S., Furukawa K. Furukawa K. (2005) Different response of the knockout mice lacking b-series gangliosides against botulinum and tetanus toxins. Biochim. Biophys. Acta 1741, 1 3. (Pubitemid 40824983)
53. Koriazova L. K. Montal M. (2003) Translocation of botulinum neurotoxin light chain protease through the heavy chain channel. Nat. Struct. Biol. 10, 13 18. (Pubitemid 36034171)
54. Kozaki S., Kamata Y., Watarai S., Nishiki T. Mochida S. (1998) Ganglioside GT1b as a complementary receptor component for Clostridium botulinum neurotoxins. Microb. Pathog. 25, 91 99. (Pubitemid 28398979)
55. Kumaran D., Eswaramoorthy S., Furey W., Navaza J., Sax M. Swaminathan S. (2009) Domain organization in Clostridium botulinum neurotoxin type E is unique: its implication in faster translocation. J. Mol. Biol. 386, 233 245.
56. Lacy D. B. Stevens R. C. (1999) Sequence homology and structural analysis of the clostridial neurotoxins. J. Mol. Biol. 291, 1091 1104. (Pubitemid 29423772)
57. Lalli G., Herreros J., Osborne S. L., Montecucco C., Rossetto O. Schiavo G. (1999) Functional characterisation of tetanus and botulinum neurotoxins binding domains. J. Cell Sci. 112, 2715 2724. (Pubitemid 29429794)
58. Lawrence G., Wang J., Chion C. K., Aoki K. R. Dolly J. O. (2007) Two protein trafficking processes at motor nerve endings unveiled by botulinum neurotoxin E. J. Pharmacol. Exp. Ther. 320, 410 418. (Pubitemid 46025755)
59. Lazarovici P. Yavin E. (1986) Affinity-purified tetanus neurotoxin interaction with synaptic membranes: properties of a protease-sensitive receptor component. Biochemistry 25, 7047 7054. (Pubitemid 17201611)
60. Lightstone F. C., Prieto M. C., Singh A. K., Piqueras M. C., Whittal R. M., Knapp M. S., Balhorn R. Roe D. C. (2000) Identification of novel small molecule ligands that bind to tetanus toxin. Chem. Res. Toxicol. 13, 356 362. (Pubitemid 30327155)
61. Louch H. A., Buczko E. S., Woody M. A., Venable R. M. Vann W. F. (2002) Identification of a binding site for ganglioside on the receptor binding domain of tetanus toxin. Biochemistry 41, 13644 13652. (Pubitemid 35332701)
62. Mahrhold S. (2008) Identifizierung neuronaler Proteinrezeptoren clostridieller Neurotoxine, pp. 106. Leibniz Universität Hannover, Hannover.
63. Mahrhold S., Rummel A., Bigalke H., Davletov B. Binz T. (2006) The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett. 580, 2011 2014.
64. Marxen P. Bigalke H. (1989) Tetanus toxin: inhibitory action in chromaffin cells is initiated by specified types of gangliosides and promoted in low ionic strength solution. Neurosci. Lett. 107, 261 266.
65. Marxen P., Fuhrmann U. Bigalke H. (1989) Gangliosides mediate inhibitory effects of tetanus and botulinum A neurotoxins on exocytosis in chromaffin cells. Toxicon 27, 849 859. (Pubitemid 19210674)
66. Marxen P., Erdmann G. Bigalke H. (1991) The translocation of botulinum A neurotoxin by chromaffin cells is promoted in low ionic strength solution and is insensitive to trypsin. Toxicon 29, 181 189.
67. Montecucco C. (1986) How do tetanus and Botulinum toxins bind to neuronal membranes? Trends Biochem. Sci. 11, 314 317.
68. Munro P., Kojima H., Dupont J. L., Bossu J. L., Poulain B. Boquet P. (2001) High sensitivity of mouse neuronal cells to tetanus toxin requires a GPI-anchored protein. Biochem. Biophys. Res. Commun. 289, 623 629. (Pubitemid 33141101)
69. Muraro L., Tosatto S., Motterlini L., Rossetto O. Montecucco C. (2009) The N-terminal half of the receptor domain of botulinum neurotoxin A binds to microdomains of the plasma membrane. Biochem. Biophys. Res. Commun. 380, 76 80.
70. Nishiki T., Kamata Y., Nemoto Y., Omori A., Ito T., Takahashi M. Kozaki S. (1994) Identification of protein receptor for Clostridium botulinum type B neurotoxin in rat brain synaptosomes. J. Biol. Chem. 269, 10498 10503. (Pubitemid 24198248)
71. Nishiki T., Tokuyama Y., Kamata Y., Nemoto Y., Yoshida A., Sato K., Sekiguchi M., Takahashi M. Kozaki S. (1996) The high-affinity binding of Clostridium botulinum type B neurotoxin to synaptotagmin II associated with gangliosides GT1b/GD1a. FEBS Lett. 378, 253 257. (Pubitemid 126334514)
72. Perin M. S., Fried V. A., Mignery G. A., Jahn R. Sudhof T. C. (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345, 260 263. (Pubitemid 20163058)
73. Pierce E. J., Davison M. D., Parton R. G., Habig W. H. Critchley D. R. (1986) Characterization of tetanus toxin binding to rat brain membranes. Evidence for a high-affinity proteinase-sensitive receptor. Biochem. J. 236, 845 852. (Pubitemid 16067128)
74. Rummel A., Bade S., Alves J., Bigalke H. Binz T. (2003) Two carbohydrate binding sites in the H(CC)-domain of tetanus neurotoxin are required for toxicity. J. Mol. Biol. 326, 835 847. (Pubitemid 36279323)
75. Rummel A., Mahrhold S., Bigalke H. Binz T. (2004a) The HCC-domain of botulinum neurotoxins A and B exhibits a singular ganglioside binding site displaying serotype specific carbohydrate interaction. Mol. Microbiol. 51, 631 643. (Pubitemid 38233933)
76. Rummel A., Karnath T., Henke T., Bigalke H. Binz T. (2004b) Synaptotagmins I and II act as nerve cell receptors for botulinum neurotoxin G. J. Biol. Chem. 279, 30865 30870. (Pubitemid 38938022)
77. Rummel A., Eichner T., Weil T. et al. (2007) Identification of the protein receptor binding site of botulinum neurotoxins B and G proves the double-receptor concept. Proc. Natl Acad. Sci. USA 104, 359 364. (Pubitemid 46068036)
78. Schengrund C. L., DasGupta B. R. Ringler N. J. (1991) Binding of botulinum and tetanus neurotoxins to ganglioside GT1b and derivatives thereof. J. Neurochem. 57, 1024 1032.
79. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B. R. Montecucco C. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832 835.
80. Schiavo G., Shone C. C., Rossetto O., Alexander F. C. Montecucco C. (1993a) Botulinum neurotoxin serotype F is a zinc endopeptidase specific for VAMP/synaptobrevin. J. Biol. Chem. 268, 11516 11519. (Pubitemid 23168093)
81. Schiavo G., Rossetto O., Catsicas S., Polverino de Laureto P., DasGupta B. R., Benfenati F. Montecucco C. (1993b) Identification of the nerve terminal targets of botulinum neurotoxin serotypes A, D, and E. J. Biol. Chem. 268, 23784 23787. (Pubitemid 23335346)
82. Schiavo G., Shone C. C., Bennett M. K., Scheller R. H. Montecucco C. (1995) Botulinum neurotoxin type C cleaves a single Lys-Ala bond within the carboxyl-terminal region of syntaxins. J. Biol. Chem. 270, 10566 10570.
83. Schiavo G., Matteoli M. Montecucco C. (2000) Neurotoxins affecting neuroexocytosis. Physiol. Rev. 80, 717 766. (Pubitemid 30164948)
84. Schmitt A., Dreyer F. John C. (1981) At least three sequential steps are involved in the tetanus toxin-induced block of neuromuscular transmission. Naunyn Schmiedebergs Arch. Pharmacol. 317, 326 330. (Pubitemid 12247884)
85. Shapiro R. E., Specht C. D., Collins B. E., Woods A. S., Cotter R. J. Schnaar R. L. (1997) Identification of a ganglioside recognition domain of tetanus toxin using a novel ganglioside photoaffinity ligand. J. Biol. Chem. 272, 30380 30386. (Pubitemid 27512247)
86. Simpson L. L. (1980) Kinetic studies on the interaction between botulinum toxin type A and the cholinergic neuromuscular junction. J. Pharmacol. Exp. Ther. 212, 16 21. (Pubitemid 10131942)
87. Simpson L. L. (1984a) Botulinum toxin and tetanus toxin recognize similar membrane determinants. Brain Res. 305, 177 180. (Pubitemid 14117861)
88. Simpson L. L. (1984b) The binding fragment from tetanus toxin antagonizes the neuromuscular blocking actions of botulinum toxin. J. Pharmacol. Exp. Ther. 229, 182 187. (Pubitemid 14082929)
89. Simpson L. L. (1985) Pharmacological experiments on the binding and internalization of the 50,000 dalton carboxyterminus of tetanus toxin at the cholinergic neuromuscular junction. J. Pharmacol. Exp. Ther. 234, 100 105. (Pubitemid 15034897)
90. Simpson L. L. Rapport M. M. (1971) The binding of botulinum toxin to membrane lipids: sphingolipids, steroids and fatty acids. J. Neurochem. 18, 1751 1759.
91. Sinha K., Box M., Lalli G., Schiavo G., Schneider H., Groves M., Siligardi G. Fairweather N. (2000) Analysis of mutants of tetanus toxin Hc fragment: ganglioside binding, cell binding and retrograde axonal transport properties. Mol. Microbiol. 37, 1041 1051. (Pubitemid 30180245)
92. Stenmark P., Dupuy J., Imamura A., Kiso M. Stevens R. C. (2008) Crystal structure of botulinum neurotoxin type A in complex with the cell surface co-receptor GT1b-insight into the toxin-neuron interaction. PLoS Pathog. 4, e1000129.
93. Sudhof T. C. (2002) Synaptotagmins: why so many? J. Biol. Chem. 277, 7629 7632.
94. Sutton R. B., Fasshauer D., Jahn R. Brunger A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347 353. (Pubitemid 28450677)
95. Sutton J. M., Chow-Worn O., Spaven L., Silman N. J., Hallis B. Shone C. C. (2001) Tyrosine-1290 of tetanus neurotoxin plays a key role in its binding to gangliosides and functional binding to neurones. FEBS Lett. 493, 45 49. (Pubitemid 32241174)
96. Swaminathan S. Eswaramoorthy S. (2000) Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B. Nat. Struct. Biol. 7, 693 699. (Pubitemid 30636683)
97. Takamizawa K., Iwamori M., Kozaki S., Sakaguchi G., Tanaka R., Takayama H. Nagai Y. (1986) TLC immunostaining characterization of Clostridium botulinum type A neurotoxin binding to gangliosides and free fatty acids. FEBS Lett. 201, 229 232. (Pubitemid 16060736)
98. Tsukamoto K., Kohda T., Mukamoto M., Takeuchi K., Ihara H., Saito M. Kozaki S. (2005) Binding of Clostridium botulinum type C and D neurotoxins to ganglioside and phospholipid. Novel insights into the receptor for clostridial neurotoxins. J. Biol. Chem. 280, 35164 35171. (Pubitemid 41532703)
99. Tsukamoto K., Kozai Y., Ihara H., Kohda T., Mukamoto M., Tsuji T. Kozaki S. (2008) Identification of the receptor-binding sites in the carboxyl-terminal half of the heavy chain of botulinum neurotoxin types C and D. Microb. Pathog. 44, 484 493.
100. Vaidyanathan V. V., Yoshino K., Jahnz M., Dorries C., Bade S., Nauenburg S., Niemann H. Binz T. (1999) Proteolysis of SNAP-25 isoforms by botulinum neurotoxin types A, C, and E: domains and amino acid residues controlling the formation of enzyme-substrate complexes and cleavage. J. Neurochem. 72, 327 337. (Pubitemid 29013908)
101. Verderio C., Coco S., Rossetto O., Montecucco C. Matteoli M. (1999) Internalization and proteolytic action of botulinum toxins in CNS neurons and astrocytes. J. Neurochem. 73, 372 379. (Pubitemid 29289146)
102. Williamson L. C., Bateman K. E., Clifford J. C. Neale E. A. (1999) Neuronal sensitivity to tetanus toxin requires gangliosides. J. Biol. Chem. 274, 25173 25180. (Pubitemid 129529415)
103. Xu T. Bajjalieh S. M. (2001) SV2 modulates the size of the readily releasable pool of secretory vesicles. Nat. Cell Biol. 3, 691 698. (Pubitemid 32734246)
104. Yamasaki S., Binz T., Hayashi T., Szabo E., Yamasaki N., Eklund M., Jahn R. Niemann H. (1994) Botulinum neurotoxin type G proteolyses the Ala81-Ala82 bond of rat synaptobrevin 2. Biochem. Biophys. Res. Commun. 200, 829 835.
105. Yowler B. C. Schengrund C. L. (2004a) Botulinum neurotoxin A changes conformation upon binding to ganglioside GT1b. Biochemistry 43, 9725 9731. (Pubitemid 38993822)
106. Yowler B. C. Schengrund C. L. (2004b) Glycosphingolipids-sweets for botulinum neurotoxin. Glycoconj. J. 21, 287 293.
107. Yowler B. C., Kensinger R. D. Schengrund C. L. (2002) Botulinum neurotoxin A activity is dependent upon the presence of specific gangliosides in neuroblastoma cells expressing synaptotagmin I. J. Biol. Chem. 277, 32815 32819.