Electric dipole reorientation in the interaction of botulinum neurotoxins with neuronal membranes

FEBS Letters

Volumn 583, Issue 14, 2009, Pages 2321-2325

  Fogolari, Federico ^a   Tosatto, Silvio C E ^b   Muraro, Lucia ^b   Montecucco, Cesare ^b  

^a UNIVERSITY OF UDINE   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Botulinum neurotoxin; Membrane electrostatics; Presynaptic membrane; Protein dipole

Indexed keywords

BOTULINUM TOXIN; MEMBRANE PROTEIN; NEUROTOXIN;

AMINO ACID SEQUENCE; ARTICLE; DIPOLE; LIGAND BINDING; MEMBRANE BINDING; NERVE CELL MEMBRANE POTENTIAL; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; RECEPTOR BINDING; TOXICOKINETICS;

ANIMALS; BOTULINUM TOXINS; MEMBRANES; MICE; MODELS, MOLECULAR; NEURONS; NEUROTOXINS; PRESYNAPTIC TERMINALS; PROTEIN CONFORMATION; STATIC ELECTRICITY; SURFACE PROPERTIES;

EID: 67650104280     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.06.046     Document Type: Article

References (56)

1. Johnson E.A., and Montecucco C. Chapter 11 botulism. Handbook Clin. Neurol. 91 (2008) 333-368
2. Humeau Y., Doussau F., Grant N.J., and Poulain B. How botulinum and tetanus neurotoxins block neurotransmitter release. Biochimie 82 (2000) 427-446
3. Davletov B., Bajohrs M., and Binz T. Beyond BOTOX: advantages and limitations of individual botulinum neurotoxins. Trends Neurosci. 28 (2005) 446-452
4. Rossetto O., and Montecucco C. Presynaptic neurotoxins with enzymatic activities. Handbook Exp. Pharmacol. 129 (2008) 170
5. Brunger, A.T. and Rummel, A. (in press) Receptor and substrate interactions of clostridial neurotoxins. Toxicon [Epub ahead of print].
6. Lacy D.B., and Stevens R.C. Sequence homology and structural analysis of the clostridial neurotoxins. J. Mol. Biol. 291 (1999) 1091-1104
7. Lacy D.B., Tepp W., Cohen A.C., DasGupta B.R., and Stevens R.C. Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat. Struct. Biol. 5 (1998) 898-902
8. Swaminathan S., and Eswaramoorthy S. Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B. Nat. Struct. Biol. 7 (2000) 693-699
9. Brunger A.T., Jin R., and Breidenbach M.A. Highly specific interactions between botulinum neurotoxins and synaptic vesicle proteins. Cell Mol. Life Sci. 65 (2008) 2296-2306
10. Kumaran D., Eswaramoorthy S., Furey W., Navaza J., Sax M., and Swaminathan S. Domain organization in Clostridium botulinum neurotoxin type E is unique: its implication in faster translocation. J. Mol. Biol. 386 (2009) 233-245
11. Montecucco C., Papini E., and Schiavo G. Bacterial protein toxins penetrate cells via a four-step mechanism. FEBS Lett. 346 (1994) 92-98
12. Nishiki T., Tokuyama Y., Kamata Y., Nemoto Y., Yoshida A., Sato K., Sekiguchi M., Takahashi M., and Kozaki S. The high-affinity binding of Clostridium botulinum type B neurotoxin to synaptotagmin II associated with gangliosides GT1b/GD1a. FEBS Lett. 378 (1996) 253-257
13. Rummel A., Mahrhold S., Bigalke H., and Binz T. The HCC-domain of botulinum neurotoxins A and B exhibits a singular ganglioside binding site displaying serotype specific carbohydrate interaction. Mol. Microbiol. 51 (2004) 631-643
14. Chai Q., Arndt J.W., Dong M., Tepp W.H., Johnson E.A., Chapman E.R., and Stevens R.C. Structural basis of cell surface receptor recognition by botulinum neurotoxin B. Nature 444 (2006) 1096-1100
15. Jin R., Rummel A., Binz T., and Brunger A.T. Botulinum neurotoxin B recognizes its protein receptor with high affinity and specificity. Nature 444 (2006) 1092-1095
16. Rummel A., Eichner T., Weil T., Karnath T., Gutcaits A., Mahrhold S., Sandhoff K., Proia R.L., Acharya K.R., Bigalke H., and Binz T. Identification of the protein receptor binding site of botulinum neurotoxins B and G proves the double-receptor concept. Proc. Natl. Acad. Sci. USA 104 (2007) 359-364
17. Dong M., Yeh F., Tepp W.H., Dean C., Johnson E.A., Janz R., and Chapman E.R. SV2 is the protein receptor for botulinum neurotoxin A. Science 312 (2006) 592-596
18. Mahrhold S., Rummel A., Bigalke H., Davletov B., and Binz T. The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett. 580 (2006) 2011-2014
19. Dong M., Liu H., Tepp W.H., Johnson E.A., Janz R., and Chapman E.R. Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol. Biol. Cell 19 (2008) 5226-5237
20. Montecucco C. How do tetanus and botulinum toxins bind to neuronal membranes?. Trends Biochem. Sci. 11 8 (1986) 314-317
21. Takamori S., Holt M., Stenius K., Lemke E.A., Gronborg M., Riedel D., Urlaub H., Schenck S., Brugger B., Ringler P., Muller S.A., Rammner B., Grater F., Hub J.S., De Groot B.L., Mieskes G., Moriyama Y., Klingauf J., Grubmuller H., Heuser J., Wieland F., and Jahn R. Molecular anatomy of a trafficking organelle. Cell 127 (2006) 831-846
22. Koriazova L.K., and Montal M. Translocation of botulinum neurotoxin light chain protease through the heavy chain channel. Nat. Struct. Biol. 10 (2003) 13-18
23. Fischer A., and Montal M. Single molecule detection of intermediates during botulinum neurotoxin translocation across membranes. Proc. Natl. Acad. Sci. USA 104 (2007) 10447-10452
24. Maksymowych A.B., and Simpson L.L. Structural features of the botulinum neurotoxin molecule that govern binding and transcytosis across polarized human intestinal epithelial cells. J. Pharmacol. Exp. Ther. 310 (2004) 633-641
25. Ahsan C.R., Hajnoczky G., Maksymowych A.B., and Simpson L.L. Visualization of binding and transcytosis of botulinum toxin by human intestinal epithelial cells. J. Pharmacol. Exp. Ther. 315 (2005) 1028-1035
26. Engel A.G. Chapter 3 the neuromuscular junction. Handbook Clin. Neurol. 91 (2008) 103-148
27. Eleopra R., Tugnoli V., Caniatti L., and De Grandis D. Botulinum toxin treatment in the facial muscles of humans: evidence of an action in untreated near muscles by peripheral local diffusion. Neurology 46 (1996) 1158-1160
28. Rosales R.L., Bigalke H., and Dressler D. Pharmacology of botulinum toxin: differences between type A preparations. Eur. J. Neurol. 13 Suppl 1 (2006) 2-10
29. Carli, L., Montecucco, C. and Rossetto, O. (in press) Assay of diffusion of different botulinum neurotoxin type A formulations injected in the mouse leg. Muscle Nerve.
30. Tettamanti G., Bonali F., Marchesini S., and Zambotti V. A new procedure for the extraction, purification and fractionation of brain gangliosides. Biochim. Biophys. Acta 296 (1973) 160-170
31. Hansson H.A., Holmgren J., and Svennerholm L. Ultrastructural localization of cell membrane GM1 ganglioside by cholera toxin. Proc. Natl. Acad. Sci. USA 74 (1977) 3782-3786
32. Wiegandt H. In: Wiegandt H. (Ed). Glycolipids (1985), Elsevier Science Publishers
33. Ledeen W. Gangliosides of the neuron. Trends Neurosci. 8 (1985) 169-174
34. Prinetti A., Chigorno V., Tettamanti G., and Sonnino S. Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J. Biol. Chem. 275 (2000) 11658-11665
35. Vyas A.A., and Schnaar R.L. Brain gangliosides: functional ligands for myelin stability and the control of nerve regeneration. Biochimie 83 (2001) 677-682
36. Buchwald B., Zhang G., Vogt-Eisele A.K., Zhang W., Ahangari R., Griffin J.W., Hatt H., Toyka K.V., and Sheikh K.A. Anti-ganglioside antibodies alter presynaptic release and calcium influx. Neurobiol. Dis. 28 (2007) 113-121
37. Missler M., Fernandez-Chacon R., and Sudhof T.C. The making of neurexins. J. Neurochem. 71 (1998) 1339-1347
38. Missler M., and Sudhof T.C. Neurexophilins form a conserved family of neuropeptide-like glycoproteins. J. Neurosci. 18 (1998) 3630-3638
39. Berman H., Henrick K., Nakamura H., and Markley J.L. The worldwide Protein Data Bank (wwPDB): ensuring a single, uniform archive of PDB data. Nucl. Acids Res. 35 (2007) D301-D303
40. Bindewald E., Cestaro A., Hesser J., Heiler M., and Tosatto S.C. MANIFOLD: protein fold recognition based on secondary structure, sequence similarity and enzyme classification. Protein Eng. 16 (2003) 785-789
41. Sommer I., Toppo S., Sander O., Lengauer T., and Tosatto S.C. Improving the quality of protein structure models by selecting from alignment alternatives. BMC Bioinform. 7 (2006) 364
42. Tosatto S.C. The victor/FRST function for model quality estimation. J. Comput. Biol. 12 (2005) 1316-1327
43. Tosatto S.C., Bindewald E., Hesser J., and Manner R. A divide and conquer approach to fast loop modeling. Protein Eng. 15 (2002) 279-286
44. Canutescu A.A., Shelenkov A.A., and Dunbrack Jr. R.L. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 12 (2003) 2001-2014
45. Shindyalov I.N., and Bourne P.E. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11 (1998) 739-747
46. Lindahl E., Hess B., and Van Der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Mod. 7 (2001) 306-317
47. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., Field M.J., Fischer S., Gao J., Guo H., Ha S., Joseph-McCarthy D., Kuchnir L., Kuczera K., Lau F.T.K., Mattos C., Michnick S., Ngo T., Nguyen D.T., Prodhom B., Reiher W.E., Roux B., Schlenkrich M., Smith J.C., Stote R., Straub J., Watanabe M., Wiorkiewicz-Kuczera J., Yin D., and Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102 (1998) 3586-3616
48. Fischer A., Garcia-Rodriguez C., Geren I., Lou J., Marks J.D., Nakagawa T., and Montal M. Molecular architecture of botulinum neurotoxin E revealed by single particle electron microscopy. J. Biol. Chem. 283 (2008) 3997-4003
49. Fogolari F., Brigo A., and Molinari H. The Poisson-Boltzmann equation for biomolecular electrostatics: a tool for structural biology. J. Mol. Recognit. 15 (2002) 377-392
50. Madura J.D., Briggs J.M., Wade R.C., Davis M.E., Luty B.A., Ilin A., Antosiewicz J., Gilson M.K., Bagheri B., Scott L.R., and McCammon J.A. Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian Dynamics program. Comput. Phys. Commun. 91 (1995) 57-95
51. Sanner M.F., Spehner J.-C., and Olson A.J. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38 (1996) 305-320
52. Philippsen, A. (2003) DINO: Visualing Structural Biology. .
53. Schiavo G., Malizio C., Trimble W.S., Polverino de Laureto P., Milan G., Sugiyama H., Johnson E.A., and Montecucco C. Botulinum G neurotoxin cleaves VAMP/synaptobrevin at a single Ala-Ala peptide bond. J. Biol. Chem. 269 (1994) 20213-20216
54. Finn R.D., Tate J., Mistry J., Coggill P.C., Sammut S.J., Hotz H.R., Ceric G., Forslund K., Eddy S.R., Sonnhammer E.L., and Bateman A. The Pfam protein families database. Nucl. Acids Res. 36 (2008) D281-D288
55. Montecucco C., Rossetto O., and Schiavo G. Presynaptic receptor arrays for clostridial neurotoxins. Trends Microbiol. 12 (2004) 442-446
56. Muraro L., Tosatto S., Motterlini L., Rossetto O., and Montecucco C. The N-terminal half of the receptor domain of botulinum neurotoxin A binds to microdomains of the plasma membrane. Biochem. Biophys. Res. Commun. 380 (2009) 76-80