Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Aug;85(16):6177–6181. doi: 10.1073/pnas.85.16.6177

Structure and action of buccalin: a modulatory neuropeptide localized to an identified small cardioactive peptide-containing cholinergic motor neuron of Aplysia californica.

E C Cropper 1, M W Miller 1, R Tenenbaum 1, M A Kolks 1, I Kupfermann 1, K R Weiss 1
PMCID: PMC281928  PMID: 3413086

Abstract

A model system that consists of a muscle utilized in biting, the accessory radula closer (ARC), and the two cholinergic motor neurons innervating this muscle, neurons B15 and B16, has been used to study the expression of food-induced arousal in the marine mollusk Aplysia. The ARC muscle receives modulatory input from an extrinsic source, the serotonergic metacerebral cells, which partially accounts for the progressive increase in the strength of biting seen in aroused animals. Another source of modulation may arise from the ARC motor neurons themselves, which synthesize neuropeptides that can potentiate ARC contractions. Neuron B15 synthesizes the two homologous peptides, small cardioactive peptides A and B, whereas neuron B16 synthesizes the structurally unrelated peptide myomodulin. Here we report the purification and sequencing of a neuropeptide termed buccalin and show that it is colocalized with the small cardioactive peptides to neuron B15. Buccalin is also bioactive at the ARC neuromuscular junction but, in contrast to the small cardioactive peptides, when exogenously applied, it decreases rather than increases the size of muscle contractions elicited by firing of the motor neurons. Also unlike the small cardioactive peptides, which exert postsynaptic actions, buccalin seems to act only presynaptically. It has no effect on muscle relaxation rate and decreases motor neuron-elicited excitatory junction potentials in the ARC without affecting contractions produced by direct application of acetylcholine to the muscle. Neuron B15, therefore, appears to contain three modulatory neurotransmitters, two of which may act postsynaptically on the muscle to potentiate the action of the primary neurotransmitter acetylcholine and one of which may act presynaptically on nerve terminals to inhibit acetylcholine release.

Full text

PDF
6177

Images in this article

6180Image
on p.6180

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams M. E., O'Shea M. Peptide cotransmitter at a neuromuscular junction. Science. 1983 Jul 15;221(4607):286–289. doi: 10.1126/science.6134339. [DOI] [PubMed] [Google Scholar]
  2. Bishop C. A., Wine J. J., Nagy F., O'Shea M. R. Physiological consequences of a peptide cotransmitter in a crayfish nerve-muscle preparation. J Neurosci. 1987 Jun;7(6):1769–1779. doi: 10.1523/JNEUROSCI.07-06-01769.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cohen J. L., Weiss K. R., Kupfermann I. Motor control of buccal muscles in Aplysia. J Neurophysiol. 1978 Jan;41(1):157–180. doi: 10.1152/jn.1978.41.1.157. [DOI] [PubMed] [Google Scholar]
  4. Cropper E. C., Lloyd P. E., Reed W., Tenenbaum R., Kupfermann I., Weiss K. R. Multiple neuropeptides in cholinergic motor neurons of Aplysia: evidence for modulation intrinsic to the motor circuit. Proc Natl Acad Sci U S A. 1987 May;84(10):3486–3490. doi: 10.1073/pnas.84.10.3486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cropper E. C., Tenenbaum R., Kolks M. A., Kupfermann I., Weiss K. R. Myomodulin: a bioactive neuropeptide present in an identified cholinergic buccal motor neuron of Aplysia. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5483–5486. doi: 10.1073/pnas.84.15.5483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kuhlman J. R., Li C., Calabrese R. L. FMRF-amide-like substances in the leech. II. Bioactivity on the heartbeat system. J Neurosci. 1985 Sep;5(9):2310–2317. doi: 10.1523/JNEUROSCI.05-09-02310.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kupfermann I. Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol. 1974 Jan;10(1):1–26. doi: 10.1016/s0091-6773(74)91644-7. [DOI] [PubMed] [Google Scholar]
  8. Kupfermann I., Weiss K. R. Activity of an identified serotonergic neuron in free moving Aplysia correlates with behavioral arousal. Brain Res. 1982 Jun 10;241(2):334–337. doi: 10.1016/0006-8993(82)91072-1. [DOI] [PubMed] [Google Scholar]
  9. Lange A. B., Orchard I., Adams M. E. Peptidergic innervation of insect reproductive tissue: the association of proctolin with oviduct visceral musculature. J Comp Neurol. 1986 Dec 15;254(3):279–286. doi: 10.1002/cne.902540302. [DOI] [PubMed] [Google Scholar]
  10. Lloyd P. E., Frankfurt M., Stevens P., Kupfermann I., Weiss K. R. Biochemical and immunocytological localization of the neuropeptides FMRFamide, SCPA, SCPB, to neurons involved in the regulation of feeding in Aplysia. J Neurosci. 1987 Apr;7(4):1123–1132. doi: 10.1523/JNEUROSCI.07-04-01123.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lloyd P. E., Kupfermann I., Weiss K. R. Evidence for parallel actions of a molluscan neuropeptide and serotonin in mediating arousal in Aplysia. Proc Natl Acad Sci U S A. 1984 May;81(9):2934–2937. doi: 10.1073/pnas.81.9.2934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lloyd P. E., Kupfermann I., Weiss K. R. Sequence of small cardioactive peptide A: a second member of a class of neuropeptides in Aplysia. Peptides. 1987 Jan-Feb;8(1):179–184. doi: 10.1016/0196-9781(87)90184-7. [DOI] [PubMed] [Google Scholar]
  13. Longley R. D., Longley A. J. Serotonin immunoreactivity of neurons in the gastropod Aplysia californica. J Neurobiol. 1986 Jul;17(4):339–358. doi: 10.1002/neu.480170408. [DOI] [PubMed] [Google Scholar]
  14. Maggi C. A., Santicioli P., Theodorsson-Norheim E., Meli A. Immunoblockade of response to capsaicin in the rat vas deferens: evidence for the involvement of endogenous calcitonin gene-related peptide. Neurosci Lett. 1987 Jul 9;78(1):63–68. doi: 10.1016/0304-3940(87)90562-3. [DOI] [PubMed] [Google Scholar]
  15. Mahon A. C., Lloyd P. E., Weiss K. R., Kupfermann I., Scheller R. H. The small cardioactive peptides A and B of Aplysia are derived from a common precursor molecule. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3925–3929. doi: 10.1073/pnas.82.11.3925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Meek J. L. Prediction of peptide retention times in high-pressure liquid chromatography on the basis of amino acid composition. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1632–1636. doi: 10.1073/pnas.77.3.1632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Morris H. R., Panico M., Karplus A., Lloyd P. E., Riniker B. Elucidation by FAB-MS of the structure of a new cardioactive peptide from Aplysia. Nature. 1982 Dec 16;300(5893):643–645. doi: 10.1038/300643a0. [DOI] [PubMed] [Google Scholar]
  18. Ono J. K., McCaman R. E. Identification of additional histaminergic neurons in Aplysia: improvement of single cell isolation techniques for in tandem physiological and chemical studies. Neuroscience. 1980;5(5):835–840. doi: 10.1016/0306-4522(80)90152-9. [DOI] [PubMed] [Google Scholar]
  19. Orchard I., Lange A. B. Neuromuscular transmission in an insect visceral muscle. J Neurobiol. 1986 Sep;17(5):359–372. doi: 10.1002/neu.480170502. [DOI] [PubMed] [Google Scholar]
  20. Rosen S. C., Kupfermann I., Goldstein R. S., Weiss K. R. Lesion of a serotonergic modulatory neuron in Aplysia produces a specific defect in feeding behavior. Brain Res. 1983 Jan 31;260(1):151–155. doi: 10.1016/0006-8993(83)90778-3. [DOI] [PubMed] [Google Scholar]
  21. Stjärne L., Lundberg J. M., Astrand P. Neuropeptide Y--a cotransmitter with noradrenaline and adenosine 5'-triphosphate in the sympathetic nerves of the mouse vas deferens? A biochemical, physiological and electropharmacological study. Neuroscience. 1986 May;18(1):151–166. doi: 10.1016/0306-4522(86)90184-3. [DOI] [PubMed] [Google Scholar]
  22. Weiss K. R., Cohen J. L., Kupfermann I. Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) in Aplysia. J Neurophysiol. 1978 Jan;41(1):181–203. doi: 10.1152/jn.1978.41.1.181. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES