The sensitivity of catecholamine release to botulinum toxin C1 and E suggests selective targeting of vesicles set into the readily releasable pool

Journal of Neurochemistry

Volumn 85, Issue 2, 2003, Pages 409-421

  Stigliani, Sara ^a   Raiteri, Luca ^a   Fassio, Anna ^a   Bonanno, Giambattista ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b Department of Experimental Medicine (DIMES)   (Italy)

Author keywords

Catecholamine release; Clostridial toxins; Exocytosis; Readily releasable pool; SNAP 25; Syntaxin

Indexed keywords

BOTULINUM TOXIN; BOTULINUM TOXIN C1; BOTULINUM TOXIN E; CALCIUM; CLOSTRIDIUM TOXIN; DOPAMINE; IONOMYCIN; NORADRENALIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHORBOL ESTER; POTASSIUM ION; SUCROSE; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID UPTAKE; ANIMAL TISSUE; ARTICLE; BRAIN PERFUSION; CATECHOLAMINE RELEASE; CONTROLLED STUDY; EXOCYTOSIS; HYDROLYSIS; MALE; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; SYNAPTOSOME;

ANIMALIA; CLOSTRIDIUM;

EID: 0037387648     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01689.x     Document Type: Article

References (57)

1. Ashton A. C. and Dolly J. O. (1991) Microtubule-dissociating drugs and A23187 reveal differences in the inhibition of synaptosomal transmitter release by botulinum neurotoxins types A and B. J. Neurochem. 56, 827-835.
2. Ashton A. C. and Dolly J. O. (1997) Microtubules and microfilaments participate in the inhibition of synaptosomal noradrenaline release by tetanus toxin. J. Neurochem. 68, 649-658.
3. i is not blocked by clostridial neurotoxins. J. Neurochem. 74, 1979-1988.
4. 2+-dependent activity is removed. J. Biol. Chem. 270, 31386-31390.
5. Attwell D., Barbour B. and Szatkowsky M. (1993) Nonvesicular release of neurotransmitter. Neuron 11, 401-407.
6. Berridge M. J. (1998) Neuronal calcium signalling. Neuron 21, 13-26.
7. Bigalke H., Heller I., Bizzini B. and Habermann R. (1981) Tetanus toxin and botulinum-A toxin inhibit release and uptake of various transmitters, as studied with particulate preparations from rat brain and spinal cord. Naunyn-Schmiedeberg's Arch. Pharmacol. 316, 244-251.
8. Blasi J., Binz T., Yamasaki S., Link E., Niemann H. and Jahn R. (1994) Inhibition of neurotransmitter release by clostridial neurotoxins correlates with specific proteolysis of synaptosomal proteins. J. Physiol. (Paris) 88, 235-241.
9. Bonanno G. and Raiteri M. (1987a) Carriers for GABA and noradrenaline uptake coexist on a same nerve terminal in rat hippocampus. Eur. J. Pharmacol. 136, 303-310.
10. Bonanno G. and Raiteri M. (1987b) Coexistence of carriers for dopamine and GABA uptake on a same nerve terminal in the rat brain. Br. J. Pharmacol. 91, 237-243.
11. Bonanno G. and Raiteri M. (1994) Release-regulating presynaptic heterocarriers. Prog. Neurobiol. 44, 451-462.
12. Bonanno G., Sala R., Cancedda L., Cavazzani P., Cossu M. and Raiteri M. (2000) Release of dopamine from human neocortex nerve terminals evoked by different stimuli involving extra- and intraterminal calcium. Br. J. Pharmacol. 129, 1780-1786.
13. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 72, 248-254.
14. Dobrunz L. E. and Stevens C. F. (1997) Heterogeneity of release probability, facilitation and depletion at central synapses. Neuron 18, 995-1008.
15. Egea G., Rabasseda X., Solsona C., Marsal J. and Bizzini B. (1990) Tetanus toxin blocks potassium-induced transmitter release and rearrangement of intramembrane particles at pure cholinergic synaptosomes. Toxicon 28, 311-318.
16. Fasshauer D., Otto H., Eliason W. K., Jahn R. and Brünger A. T. (1997) Structural changes are associated with soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor complex formation. J. Biol. Chem. 272, 28036-28041.
17. Fassio A., Bonanno G., Fontana G., Usai C., Marchi M. and Raiteri M. (1996) Role of external and internal calcium on heterocarrier-mediated transmitter release. J. Neurochem. 66, 1468-1474.
18. Fassio A., Sala R., Bonanno G., Marchi M. and Raiteri M. (1999) Evidence for calcium-dependent vesicular transmitter release insensitive to tetanus toxin and botulinum toxin type F. Neuroscience 90, 893-902.
19. 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 25, 2630-2636.
20. Garcia E. P., McPherson P. S., Chilcote T. J., Takei K. and De Camilli P. (1995) rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J. Cell Biol. 129, 105-120.
21. Goda Y. and Stevens C. F. (1998) Readily releasable pool size changes associated with long-term depression. Proc. Natl Acad. Sci. USA 95, 1283-1288.
22. 3H]GABA from rat brain homogenate. Experientia 44, 224-226.
23. Habermann E., Müller H. and Hudel M. (1988) Tetanus toxin and botulinum A and C neurotoxins inhibit noradrenaline release from cultured mouse brain. J. Neurochem. 51, 522-527.
24. Hayashi T., McMahon H., Yamasaki S., Binz T., Hata Y., Südhof T. C. and Niemann H. (1994) Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051-5061.
25. 2+. Biophys. J. 67, 2546-2557.
26. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
27. Levi G. and Raiteri M. (1993) Carrier-mediated release of neurotransmitters. Trends Neurosci. 16, 415-419.
28. Liu G. and Tsien R. W. (1995) Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375, 404-408.
29. Lonart G. and Südhof T. C. (2000) Assembly of SNARE core complexes prior to neurotransmitter release set the size of the readily releasable pool of synaptic vesicles. J. Biol. Chem. 275, 27703-27707.
30. McMahon H. T., Foran P., Dolly J. O., Verhage M., Wiegant V. M. and Nicholls D. G. (1992) Tetanus toxin and botulinum toxins type A and B inhibit glutamate, γ-aminobutyric acid, aspartate, and metenkephalin release from synaptosomes. J. Biol. Chem. 267, 21338-21343.
31. Montecucco C. and Schiavo G. (1994) Mechanism of action of tetanus and botulinum neurotoxins. Mol. Microbiol. 13, 1-8.
32. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399.
33. Nichols R. A., Haycock J. W., Wang J. K. and Greengard P. (1987) Phorbol ester enhancement of neurotransmitter release from rat brain synaptosomes. J. Neurochem. 48, 615-621.
34. Otto H., Hanson P. I. and Jahn R. (1997) Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles. Proc. Natl Acad. Sci. USA 94, 6197-6201.
35. 3H]GABA release from developing cell cultures of the rat cerebellum. J. Neurochem. 40, 887-890.
36. Pellegrini L. L., O'Connor V. and Betz H. (1994) Fusion complex formation protects synaptobrevin against proteolysis by tetanus toxin light chain. FEBS Lett. 353, 319-323.
37. Raiteri L. and Raiteri M. (2000) Synaptosomes still viable after 25 years of superfusion. Neurochem. Res. 25, 1265-1274.
38. Raiteri M., Marchi M. and Maura G. (1984) Release of catecholamines, serotonin and acetylcholine from isolated brain tissue, in Handbook of Neurochemistry (Lajtha A., ed.), pp. 431-462. Plenum, New York.
39. Raiteri M., Sala R., Fassio A., Rossetto O. and Bonanno G. (2000) Entrapping of impermeant probes of different size into nonpermeabilized synaptosomes as a method to study presynaptic mechanisms. J. Neurochem. 74, 423-431.
40. Rizzuto R., Pinton P., Brini M., Chiesa A., Filippin L. and Pozzan T. (1999) Mitochondria as biosensor of calcium microdomains. Cell Calcium 26, 193-199.
41. Rosenmund C. and Stevens C. F. (1996) Definition of the readily releasable pool of vesicles and hippocampal synapses. Neuron 16, 1197-1207.
42. Sanchez-Prieto J., Sihra T. S., Evans D., Ashton A., Dolly J. O. and Nicholls D. G. (1987) Botulinum toxin A blocks glutamate exocytosis from guinea-pig cerebral cortical synaptosomes. Eur. J. Biochem. 165, 675-681.
43. 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.
44. Schiavo G., Shone C. C., Rossetto O., Alexander F. C. G. and Montecucco C. (1993) Botulinum neurotoxin serotype F is a zinc endopeptidase specific for VAMP/synaptobrevin. J. Biol. Chem. 268, 11516-11519.
45. Schiavo G., Shone C. C., Bennett M. K., Scheller R. H. and 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.
46. Schweizer F. E., Betz H. and Augustine G. J. (1995) From vesicle docking to endocytosis: intermediate reactions of exocytosis. Neuron 14, 689-696.
47. 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.
48. Simpson L. L. (1986) Molecular pharmacology of botulinum toxin and tetanus toxin. Annu. Rev. Pharmacol. Toxicol. 26, 427-453.
49. Smith J. E., Lane J. D., Shea P. A., McBride W. J. and Aprison M. H. (1975) A method for concurrent measurement of picomole quantities of acetylcholine, choline, dopamine, norepinephrine, serotonin, 5-hydroxytryptophan, 5-hydroxyindoleacetic acid, tryptophan, tyrosine, glycine, aspartate, glutamate, alanine and gamma-aminobutyric acid in single tissue samples from different areas of the rat central nervous system. Anal. Biochem. 64, 149-169.
50. Stecher B., Hens J. J. H., Weller U., Gratzl M., Gispen W.-H. and De Graan P. N. E. (1992) Noradrenaline release from permeabilized synaptosomes is inhibited by the light chain of tetanus toxin. FEBS Lett. 312, 192-194.
51. Stevens C. F. and Sullivan J. M. (1998) Regulation of the readily releasable pool by protein kinase C. Neuron 21, 885-893.
52. Stevens C. F. and Tsujimoto T. (1995) Estimates of the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc. Natl Acad. Sci. USA 92, 846-849.
53. Südhof T. C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
54. Van Vliet B. J., Sebben M., Dumuis A., Gabrion J., Bockaert J. and Pin J.-P. (1989) Endogenous amino acid release from cultured cerebellar neuronal cells: effect of tetanus toxin on glutamate release. J. Neurochem. 52, 1229-1239.
55. Verhage M., McMahon H. T., Ghijsen W. E. J. M., Boomsma F., Scholten G., Wiegant V. M. and Nicholls D. G. (1991) Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 6, 517-524.
56. Walch-Solimena C., Blasi J., Edelmann L., Chapman E. R., von Mollard G. F. and Jahn R. (1995) The t-SNARE syntaxin-1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 128, 637-645.
57. Wu L. G. and Burst J. G. (1999) The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23, 821-832.