Distinct mechanisms produce functionally complementary actions of neuropeptides that are structurally related but derived from different precursors

Ferdinand S. Vilim, Kosei Sasaki, Jurgen Rybak, Vera Alexeeva, Elizabeth C. Cropper, Jian Jing, Irina V. Orekhova, Vladimir Brezina, David Price, Elena V. Romanova, Stanislav S. Rubakhin, Nathan Hatcher, Jonathan V. Sweedler, Klaudiusz R. Weiss

Research output: Contribution to journalArticle

Abstract

Many bioactive neuropeptides containing RFamide at their C terminus have been described in both invertebrates and vertebrates. To obtain insight into the functional logic of RFamide signaling, we investigate it here in the feeding system of Aplysia. We focus on the expression, localization, and actions of two families of RFamide peptides, the FRFamides and FMRFamide, in the central neuronal circuitry and the peripheral musculature that generate the feeding movements. We describe the cloning of the FRFamide precursor protein and show that the FRFamides and FMRFamide are derived from different precursors. We map the expression of the FRFamide and FMRFamide precursors in the feeding circuitry using in situ hybridization and immunostaining and confirm proteolytic processing of the FRFamide precursor by mass spectrometry. We show that the two precursors are expressed in different populations of sensory neurons in the feeding system. In a representative feeding muscle, we demonstrate the presence of both FRFamides and FMRFamide and their release, probably from the processes of the sensory neurons in the muscle. Both centrally and in the periphery, the FRFamides and FMRFamide act in distinct ways, apparently through distinct mechanisms, and nevertheless, from an overall functional perspective, their actions are complementary. Together, the FRFamides and FMRFamide convert feeding motor programs from ingestive to egestive and depress feeding muscle contractions. We conclude that these structurally related peptides, although derived from different precursors, expressed in different neurons, and acting through different mechanisms, remain related to each other in the functional roles that they play in the system.

Original languageEnglish (US)
Pages (from-to)131-147
Number of pages17
JournalJournal of Neuroscience
Volume30
Issue number1
DOIs
StatePublished - Jan 6 2010

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FMRFamide
Neuropeptides
Sensory Receptor Cells
Aplysia
Muscles
Protein Precursors
Invertebrates
Muscle Contraction
In Situ Hybridization
Vertebrates
Organism Cloning
Mass Spectrometry
Neurons
Peptides
Population

ASJC Scopus subject areas

  • Neuroscience(all)

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Distinct mechanisms produce functionally complementary actions of neuropeptides that are structurally related but derived from different precursors. / Vilim, Ferdinand S.; Sasaki, Kosei; Rybak, Jurgen; Alexeeva, Vera; Cropper, Elizabeth C.; Jing, Jian; Orekhova, Irina V.; Brezina, Vladimir; Price, David; Romanova, Elena V.; Rubakhin, Stanislav S.; Hatcher, Nathan; Sweedler, Jonathan V.; Weiss, Klaudiusz R.

In: Journal of Neuroscience, Vol. 30, No. 1, 06.01.2010, p. 131-147.

Research output: Contribution to journalArticle

Vilim, Ferdinand S. ; Sasaki, Kosei ; Rybak, Jurgen ; Alexeeva, Vera ; Cropper, Elizabeth C. ; Jing, Jian ; Orekhova, Irina V. ; Brezina, Vladimir ; Price, David ; Romanova, Elena V. ; Rubakhin, Stanislav S. ; Hatcher, Nathan ; Sweedler, Jonathan V. ; Weiss, Klaudiusz R. / Distinct mechanisms produce functionally complementary actions of neuropeptides that are structurally related but derived from different precursors. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 1. pp. 131-147.
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AU - Sasaki, Kosei

AU - Rybak, Jurgen

AU - Alexeeva, Vera

AU - Cropper, Elizabeth C.

AU - Jing, Jian

AU - Orekhova, Irina V.

AU - Brezina, Vladimir

AU - Price, David

AU - Romanova, Elena V.

AU - Rubakhin, Stanislav S.

AU - Hatcher, Nathan

AU - Sweedler, Jonathan V.

AU - Weiss, Klaudiusz R.

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N2 - Many bioactive neuropeptides containing RFamide at their C terminus have been described in both invertebrates and vertebrates. To obtain insight into the functional logic of RFamide signaling, we investigate it here in the feeding system of Aplysia. We focus on the expression, localization, and actions of two families of RFamide peptides, the FRFamides and FMRFamide, in the central neuronal circuitry and the peripheral musculature that generate the feeding movements. We describe the cloning of the FRFamide precursor protein and show that the FRFamides and FMRFamide are derived from different precursors. We map the expression of the FRFamide and FMRFamide precursors in the feeding circuitry using in situ hybridization and immunostaining and confirm proteolytic processing of the FRFamide precursor by mass spectrometry. We show that the two precursors are expressed in different populations of sensory neurons in the feeding system. In a representative feeding muscle, we demonstrate the presence of both FRFamides and FMRFamide and their release, probably from the processes of the sensory neurons in the muscle. Both centrally and in the periphery, the FRFamides and FMRFamide act in distinct ways, apparently through distinct mechanisms, and nevertheless, from an overall functional perspective, their actions are complementary. Together, the FRFamides and FMRFamide convert feeding motor programs from ingestive to egestive and depress feeding muscle contractions. We conclude that these structurally related peptides, although derived from different precursors, expressed in different neurons, and acting through different mechanisms, remain related to each other in the functional roles that they play in the system.

AB - Many bioactive neuropeptides containing RFamide at their C terminus have been described in both invertebrates and vertebrates. To obtain insight into the functional logic of RFamide signaling, we investigate it here in the feeding system of Aplysia. We focus on the expression, localization, and actions of two families of RFamide peptides, the FRFamides and FMRFamide, in the central neuronal circuitry and the peripheral musculature that generate the feeding movements. We describe the cloning of the FRFamide precursor protein and show that the FRFamides and FMRFamide are derived from different precursors. We map the expression of the FRFamide and FMRFamide precursors in the feeding circuitry using in situ hybridization and immunostaining and confirm proteolytic processing of the FRFamide precursor by mass spectrometry. We show that the two precursors are expressed in different populations of sensory neurons in the feeding system. In a representative feeding muscle, we demonstrate the presence of both FRFamides and FMRFamide and their release, probably from the processes of the sensory neurons in the muscle. Both centrally and in the periphery, the FRFamides and FMRFamide act in distinct ways, apparently through distinct mechanisms, and nevertheless, from an overall functional perspective, their actions are complementary. Together, the FRFamides and FMRFamide convert feeding motor programs from ingestive to egestive and depress feeding muscle contractions. We conclude that these structurally related peptides, although derived from different precursors, expressed in different neurons, and acting through different mechanisms, remain related to each other in the functional roles that they play in the system.

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