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© The Rockefeller University Press, 0021-9525/1999/12/1249/ $5.00
The Journal of Cell Biology, Volume 147, Number 6, December 13, 1999 1249-1260

Original Article

Botulinum Neurotoxin A Blocks Synaptic Vesicle Exocytosis but Not Endocytosis at the Nerve Terminal

Elaine A. Nealea, Linda M. Bowersa, Min Jiaa, Karen E. Batemana, and Lura C. Williamsona
a Laboratory of Developmental Neurobiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892

Correspondence to: Elaine A. Neale, LDN, NICHD, NIH, Building 49, Room 5A38, Bethesda, MD 20892-4480. Tel:(301) 496-6419 Fax:(301) 496-9939 E-mail:eneale{at}codon.nih.gov.

The supply of synaptic vesicles in the nerve terminal is maintained by a temporally linked balance of exo- and endocytosis. Tetanus and botulinum neurotoxins block neurotransmitter release by the enzymatic cleavage of proteins identified as critical for synaptic vesicle exocytosis. We show here that botulinum neurotoxin A is unique in that the toxin-induced block in exocytosis does not arrest vesicle membrane endocytosis. In the murine spinal cord, cell cultures exposed to botulinum neurotoxin A, neither K+-evoked neurotransmitter release nor synaptic currents can be detected, twice the ordinary number of synaptic vesicles are docked at the synaptic active zone, and its protein substrate is cleaved, which is similar to observations with tetanus and other botulinal neurotoxins. In marked contrast, K+ depolarization, in the presence of Ca2+, triggers the endocytosis of the vesicle membrane in botulinum neurotoxin A–blocked cultures as evidenced by FM1-43 staining of synaptic terminals and uptake of HRP into synaptic vesicles. These experiments are the first demonstration that botulinum neurotoxin A uncouples vesicle exo- from endocytosis, and provide evidence that Ca2+ is required for synaptic vesicle membrane retrieval.

Key Words: botulinum toxin type A, presynaptic terminals, synaptic vesicles, endocytosis, exocytosis


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