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Research Article

Synaptic neuropeptide release induced by octopamine without Ca2+ entry into the nerve terminal

Dinara Shakiryanova, Geoffrey M. Zettel, Tingting Gu, Randall S. Hewes, and Edwin S. Levitan
PNAS March 15, 2011 108 (11) 4477-4481; https://doi.org/10.1073/pnas.1017837108
Dinara Shakiryanova
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Geoffrey M. Zettel
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Tingting Gu
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Randall S. Hewes
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Edwin S. Levitan
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  • For correspondence: elevitan@pitt.edu
  1. Edited by Eve Marder, Brandeis University, Waltham, MA, and approved February 4, 2011 (received for review December 1, 2010)

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Abstract

Synaptic release of neurotransmitters is evoked by activity-dependent Ca2+ entry into the nerve terminal. However, here it is shown that robust synaptic neuropeptide release from Drosophila motoneurons is evoked in the absence of extracellular Ca2+ by octopamine, the arthropod homolog to norepinephrine. Genetic and pharmacology experiments demonstrate that this surprising peptidergic transmission requires cAMP-dependent protein kinase, with only a minor contribution of exchange protein activated by cAMP (epac). Octopamine-evoked neuropeptide release also requires endoplasmic reticulum Ca2+ mobilization by the ryanodine receptor and the inositol trisphosphate receptor. Hence, rather than relying exclusively on activity-dependent Ca2+ entry into the nerve terminal, a behaviorally important neuromodulator uses synergistic cAMP-dependent protein kinase and endoplasmic reticulum Ca2+ signaling to induce synaptic neuropeptide release.

  • GCaMP
  • GFP
  • monoamine
  • neuromuscular junction
  • neurotransmission

Footnotes

  • 1To whom correspondence should be addressed. E-mail: elevitan{at}pitt.edu.
  • Author contributions: D.S. and E.S.L. designed research; D.S. and G.M.Z. performed research; T.G. and R.S.H. contributed new reagents/analytic tools; D.S., G.M.Z., and E.S.L. analyzed data; and E.S.L. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

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Synaptic neuropeptide release induced by octopamine without Ca2+ entry into the nerve terminal
Dinara Shakiryanova, Geoffrey M. Zettel, Tingting Gu, Randall S. Hewes, Edwin S. Levitan
Proceedings of the National Academy of Sciences Mar 2011, 108 (11) 4477-4481; DOI: 10.1073/pnas.1017837108

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Synaptic neuropeptide release induced by octopamine without Ca2+ entry into the nerve terminal
Dinara Shakiryanova, Geoffrey M. Zettel, Tingting Gu, Randall S. Hewes, Edwin S. Levitan
Proceedings of the National Academy of Sciences Mar 2011, 108 (11) 4477-4481; DOI: 10.1073/pnas.1017837108
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Proceedings of the National Academy of Sciences: 108 (11)
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