The Secretion of Classical and Peptide Cotransmitters from a Single Presynaptic Neuron Involves a Synaptobrevin-like Molecule

Overview

Journal J Neurosci

Specialty Neurology

Date 1997 Apr 1

PMID 9065494

Citations 3

Authors

M D Whim

H Niemann

L K Kaczmarek

Affiliations

Soon will be listed here.

Abstract

It is not yet understood how the molecular mechanisms controlling the release of neuropeptides differ from those controlling the release of classical transmitters, mainly because there are few peptidergic synapses in which the environment at the presynaptic release sites can be manipulated. Using Aplysia californica neuron B2, which synthesizes both peptide and classical transmitters, we have established two synaptic types. When B2 is cocultured with a sensory neuron, a peptidergic synapse is formed. In contrast, when B2 is cocultured with neuron B6, a classical synapse is formed. In contrast to a common assumption, single action potentials can release both types of transmitters. The secretion of peptide and classical transmitters by B2 is inhibited by the presynaptic injection of tetanus toxin, but not by an inactive mutant. Thus a synaptobrevin-like molecule is involved in the secretion of these two types of transmitters.

Citing Articles

The uv1 Neuroendocrine Cells Provide Mechanosensory Feedback of Vulval Opening.

Yan L, Claman A, Bode A, Collins K J Neurosci. 2025; 45(6).

PMID: 39788737 PMC: 11800740. DOI: 10.1523/JNEUROSCI.0678-24.2024.

Corollary discharge promotes a sustained motor state in a neural circuit for navigation.

Ji N, Venkatachalam V, Rodgers H, Hung W, Kawano T, Clark C Elife. 2021; 10.

PMID: 33880993 PMC: 8139836. DOI: 10.7554/eLife.68848.

Presynaptic target of Ca2+ action on neuropeptide and acetylcholine release in Aplysia californica.

Ohnuma K, Whim M, Fetter R, Kaczmarek L, Zucker R J Physiol. 2001; 535(Pt 3):647-62.

PMID: 11559764 PMC: 2278817. DOI: 10.1111/j.1469-7793.2001.00647.x.

Heterologous expression of the Kv3.1 potassium channel eliminates spike broadening and the induction of a depolarizing afterpotential in the peptidergic bag cell neurons.

Whim M, Kaczmarek L J Neurosci. 1998; 18(22):9171-80.

PMID: 9801357 PMC: 6792887.

References

Mulle C, Benoit P, Pinset C, Roa M, Changeux J . Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc Natl Acad Sci U S A. 1988; 85(15):5728-32. PMC: 281834. DOI: 10.1073/pnas.85.15.5728. View

De Camilli P, Jahn R . Pathways to regulated exocytosis in neurons. Annu Rev Physiol. 1990; 52:625-45. DOI: 10.1146/annurev.ph.52.030190.003205. View

Niemann H, Blasi J, Jahn R . Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol. 1994; 4(5):179-85. DOI: 10.1016/0962-8924(94)90203-8. View

Hunt J, Bommert K, Charlton M, Kistner A, Habermann E, Augustine G . A post-docking role for synaptobrevin in synaptic vesicle fusion. Neuron. 1994; 12(6):1269-79. DOI: 10.1016/0896-6273(94)90443-x. View

Papini E, Rossetto O, Cutler D . Vesicle-associated membrane protein (VAMP)/synaptobrevin-2 is associated with dense core secretory granules in PC12 neuroendocrine cells. J Biol Chem. 1995; 270(3):1332-6. DOI: 10.1074/jbc.270.3.1332. View

Jan L, Jan Y . Peptidergic transmission in sympathetic ganglia of the frog. J Physiol. 1982; 327:219-46. PMC: 1225105. DOI: 10.1113/jphysiol.1982.sp014228. View

Haydon P, Drapeau P . From contact to connection: early events during synaptogenesis. Trends Neurosci. 1995; 18(4):196-201. DOI: 10.1016/0166-2236(95)93901-9. View

Lloyd P, Mahon A, Kupfermann I, Cohen J, Scheller R, Weiss K . Biochemical and immunocytological localization of molluscan small cardioactive peptides in the nervous system of Aplysia californica. J Neurosci. 1985; 5(7):1851-61. PMC: 6565124. View

Kupfermann I . Functional studies of cotransmission. Physiol Rev. 1991; 71(3):683-732. DOI: 10.1152/physrev.1991.71.3.683. View

10.

Reed W, Weiss K, Lloyd P, Kupfermann I, Chen M, Bailey C . Association of neuroactive peptides with the protein secretory pathway in identified neurons of Aplysia californica: immunolocalization of SCPA and SCPB to the contents of dense-core vesicles and the trans face of the Golgi apparatus. J Comp Neurol. 1988; 272(3):358-69. DOI: 10.1002/cne.902720306. View

11.

Baxter D, Byrne J . Serotonergic modulation of two potassium currents in the pleural sensory neurons of Aplysia. J Neurophysiol. 1989; 62(3):665-79. DOI: 10.1152/jn.1989.62.3.665. View

12.

Gardner D . Bilateral symmetry and interneuronal organization in the buccal ganglia of Aplysia. Science. 1971; 173(3996):550-3. DOI: 10.1126/science.173.3996.550. View

13.

Haydon P . The formation of chemical synapses between cell-cultured neuronal somata. J Neurosci. 1988; 8(3):1032-8. PMC: 6569237. View

14.

Peng Y, Horn J . Continuous repetitive stimuli are more effective than bursts for evoking LHRH release in bullfrog sympathetic ganglia. J Neurosci. 1991; 11(1):85-95. PMC: 6575190. View

15.

Cropper E, Price D, Tenenbaum R, Kupfermann I, Weiss K . Release of peptide cotransmitters from a cholinergic motor neuron under physiological conditions. Proc Natl Acad Sci U S A. 1990; 87(3):933-7. PMC: 53383. DOI: 10.1073/pnas.87.3.933. View

16.

Whim M, Lloyd P . Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia. Proc Natl Acad Sci U S A. 1989; 86(22):9034-8. PMC: 298427. DOI: 10.1073/pnas.86.22.9034. View

17.

Siegelbaum S, Camardo J, Kandel E . Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones. Nature. 1982; 299(5882):413-7. DOI: 10.1038/299413a0. View

18.

Yamasaki S, Hu Y, Binz T, Kalkuhl A, Kurazono H, Tamura T . Synaptobrevin/vesicle-associated membrane protein (VAMP) of Aplysia californica: structure and proteolysis by tetanus toxin and botulinal neurotoxins type D and F. Proc Natl Acad Sci U S A. 1994; 91(11):4688-92. PMC: 43853. DOI: 10.1073/pnas.91.11.4688. View

19.

Whim M, Lloyd P . Neuropeptide cotransmitters released from an identified cholinergic motor neuron modulate neuromuscular efficacy in Aplysia. J Neurosci. 1990; 10(10):3313-22. PMC: 6570179. View

20.

Whim M, Lloyd P . Differential regulation of the release of the same peptide transmitters from individual identified motor neurons in culture. J Neurosci. 1994; 14(7):4244-51. PMC: 6577053. View