Molecular basis for tetanus toxin coreceptor interactions

Biochemistry

Volumn 47, Issue 27, 2008, Pages 7179-7186

  Chen, Chen ^a   Baldwin, Michael R ^a   Barbieri, Joseph T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATES; MODAL ANALYSIS; NEUROLOGY; NEURONS; ORGANIC COMPOUNDS; SUGAR (SUCROSE); SUGARS;

AFFINITY BINDING; AMERICAN CHEMICAL SOCIETY (ACS); BINDING POCKETS; BINDING SPECIFICITIES; CARBOHYDRATE BINDING; CENTRAL NERVOUS SYSTEM (CNS); CO-RECEPTORS; FUNCTIONAL PROPERTIES; MEMBRANE PROTEINS; MOLECULAR BASES; NERVE CELLS; PERIPHERAL NERVES; SIALIC ACID (SIA); SOLID-PHASE; TETANUS TOXIN (TENT);

CARBOXYLIC ACIDS;

CARBOHYDRATE; GANGLIOSIDE; GANGLIOSIDE GD 1A; GANGLIOSIDE GD 1B; GANGLIOSIDE GM1; GANGLIOSIDE GT 1B; N ACETYLGALACTOSAMINE; SIALIC ACID; SYNAPTOBREVIN 2; TETANUS TOXIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; RECEPTOR BINDING; SPASTIC PARESIS; SYNAPSE;

ANIMALS; BINDING SITES; CARBOHYDRATE METABOLISM; CEREBRAL CORTEX; GANGLIOSIDES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTANT PROTEINS; N-ACETYLNEURAMINIC ACID; NEURONS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, CELL SURFACE; TETANUS TOXIN; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 46849085158     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800640y     Document Type: Article

References (41)

1. Schiavo, G., Matteoli, M., and Montecucco, C. (2000) Neurotoxins affecting neuroexocytosis. Physiol. Rev. 80, 717-766.
2. Montecucco, C., and Schiavo, G. (1994) Mechanism of action of tetanus and botulinum neurotoxins. Mol. Microbiol. 13, 1-8.
3. Poulain, B. (1994) [Molecular mechanism of action of tetanus toxin and botulinum neurotoxins]. Pathol. Biol. 42, 173-182.
4. Pellizzari, R., Rossetto, O., Schiavo, G., and Montecucco, C. (1999) Tetanus and botulinum neurotoxins: Mechanism of action and therapeutic uses. Philos. Trans. R. Soc. London, Ser. B 354, 259-268.
5. Lacy, D. B., and Stevens, R. C. (1999) Sequence homology and structural analysis of the clostridial neurotoxins. J. Mol. Biol. 291, 1091-1104.
6. Humeau, Y., Doussau, F., Grant, N. J., and Poulain, B. (2000) How botulinum and tetanus neurotoxins block neurotransmitter release. Biochimie 82, 427-446.
7. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B. R., and Montecucco, C. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835.
8. Blasi, J., Chapman, E. R., Link, E., Binz, T., Yamasaki, S., Camilli, P. D., Sudhof, T. C., Niemann, H., and Jahn, R. (1993) Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 365, 160-163.
9. Foran, P., Lawrence, G. W., Shone, C. C., Foster, K. A., and Dolly, J. O. (1996) Botulinum neurotoxin C1 cleaves both syntaxin and SNAP-25 in intact and permeabilized chromaffin cells: Correlation with its blockade of catecholamine release. Biochemistry 35, 2630-2636.
10. Williamson, L. C., Halpern, J. L., Montecucco, C., Brown, J. E., and Neale, E. A. (1996) Clostridial neurotoxins and substrate proteolysis in intact neurons: Botulinum neurotoxin C acts on synaptosomal-associated protein of 25 kDa. J. Biol. Chem. 271, 7694-7699.
11. Blasi, J., Chapman, E. R., Yamasaki, S., Binz, T., Niemann, H., and Jahn, R. (1993) Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin. EMBO J. 12, 4821-4828.
12. Shone, C. C., Hambleton, P., and Melling, J. (1987) A 50-kDa fragment from the NH2-terminus of the heavy subunit of Clostridium botulinum type A neurotoxin forms channels in lipid vesicles. Eur. J. Biochem. 167, 175-180.
13. Montecucco, C. (1986) How do tetanus and botulinum toxins bind to neuronal membranes? Trends Biochem. Sci. 11, 314-317.
14. Karlsson, K. A. (1998) On the character and functions of sphingolipids. Acta Biochim. Pol. 45, 429-438.
15. Mocchetti, I. (2005) Exogenous gangliosides, neuronal plasticity and repair, and the neurotrophins. Cell. Mol. Life Sci. 62, 2283-2294.
16. Singh, A. K., Harrison, S. H., and Schoeniger, J. S. (2000) Gangliosides as receptors for biological toxins: Development of sensitive fluoroimmunoassays using ganglioside-bearing liposomes. Anal. Chem. 72, 6019-6024.
17. Kitamura, M., Iwamori, M., and Nagai, Y. (1980) Interaction between Clostridium botulinum neurotoxin and gangliosides. Biochim. Biophys. Acta 628, 328-335.
18. Tsukamoto, K., Kohda, T., Mukamoto, M., Takeuchi, K., Ihara, H., Saito, M., and 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.
19. Rummel, A., Bade, S., Alves, J., Bigalke, H., and 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.
20. Pierce, E. J., Davison, M. D., Parton, R. G., Habig, W. H., and 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.
21. Herreros, J., Lalli, G., and Schiavo, G. (2000) C-Terminal half of tetanus toxin fragment C is sufficient for neuronal binding and interaction with a putative protein receptor. Biochem. J. 347 (Part 1), 199-204.
22. Sutton, J. M., Chow-Worn, O., Spaven, L., Silman, N. J., Hallis, B., and 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.
23. Fotinou, C., Emsley, P., Black, I., Ando, H., Ishida, H., Kiso, M., Sinha, K. A., Fairweather, N. F., and Isaacs, N. W. (2001) The crystal structure of tetanus toxin Hc fragment complexed with a synthetic GT1b analogue suggests cross-linking between ganglioside receptors and the toxin. J. Biol. Chem. 276, 32274-32281.
24. Jin, R., Rummel, A., Binz, T., and Brunger, A. T. (2006) Botulinum neurotoxin B recognizes its protein receptor with high affinity and specificity. Nature 444, 1092-1095.
25. Chai, Q., Arndt, J. W., Dong, M., Tepp, W. H., Johnson, E. A., Chapman, E. R., and Stevens, R. C. (2006) Structural basis of cell surface receptor recognition by botulinum neurotoxin B. Nature 444, 1096-1100.
26. Critchley, D. R., Habig, W. H., and Fishman, P. H. (1986) Reevaluation of the Role of Gangliosides as Receptors for Tetanus Toxin. J. Neurochem. 47, 213-222.
27. Angstrom, J., Teneberg, S., and 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. U.S.A. 91, 11859-11863.
28. Holmgren, J., Elwing, H., Fredman, P., and Svennerholm, L. (1980) Polystyrene-Adsorbed Gangliosides for Investigation of the Structure of the Tetanus-Toxin Receptor. Eur. J. Biochem. 106, 371-379.
29. Baldwin, M. R., and Barbieri, J. T. (2007) Association of botulinum neurotoxin serotypes A and B with synaptic vesicle protein complexes. Biochemistry 46, 3200-3210.
30. Rummel, A., Karnath, T., Henke, T., Bigalke, H., and Binz, T. (2004) Synaptotagmins I and II act as nerve cell receptors for botulinum neurotoxin G. J. Biol. Chem. 279, 30865-30870.
31. Montecucco, C., Schiavo, G., Brunner, J., Duflot, E., Boquet, P., and Roa, M. (1986) Tetanus toxin is labeled with photoactivatable phospholipids at low pH. Biochemistry 25, 919-924.
32. Swaminathan, S., and Eswaramoorthy, S. (2000) Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B. Nat. Struct. Biol. 7, 693-699.
33. Jayaraman, S., Eswaramoorthy, S., Kumaran, D., and Swaminathan, S. (2005) Common binding site for disialyllactose and tri-peptide in C-fragment of tetanus neurotoxin. Proteins 61, 288-295.
34. Herreros, J., Ng, T., and Schiavo, G. (2001) Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell 12, 2947-2960.
35. Kitamura, M., Takamiya, K., Aizawa, S., Furukawa, K., and Furukawa, K. (1999) Gangliosides are the binding substances in neural cells for tetanus and botulinum toxins in mice. Biochim. Biophys. Acta 1441, 1-3.
36. Kitamura, M., Igimi, S., Furukawa, K., and Furukawa, K. (2005) Different response of the knockout mice lacking b-series gangliosides against botulinum and tetanus toxins. Biochim. Biophys. Acta 1741, 1-3.
37. Shevchuk, N. A., Hathout, Y., Epifano, O., Su, Y., Liu, Y., Sutherland, M., and Ladisch, S. (2007) Alteration of ganglioside synthesis by GM3 synthase knockout in murine embryonic fibroblasts. Biochim. Biophys. Acta 1771, 1226-1234.
38. Gong, Y., Tagawa, Y., Lunn, M. P., Laroy, W., Heffer-Lauc, M., Li, C. Y., Griffin, J. W., Schnaar, R. L., and Sheikh, K. A. (2002) Localization of major gangliosides in the PNS: Implications for immune neuropathies. Brain 125, 2491-2506.
39. Rummel, A., Mahrhold, S., Bigalke, H., and Binz, T. (2004) 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.
40. Dong, M., Richards, D. A., Goodnough, M. C., Tepp, W. H., Johnson, E. A., and Chapman, E. R. (2003) Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells. J. Cell Biol. 162, 1293-1303.
41. Dong, M., Yeh, F., Tepp, W. H., Dean, C., Johnson, E. A., Janz, R., and Chapman, E. R. (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312, 592-596.