Sequence of small cardioactive peptide A: A second member of a class of neuropeptides in Aplysia

Lloyd, Philip E.; Kupfermann, Irving; Weiss, Klaudiusz R.

doi:10.1016/0196-9781(87)90184-7

Cited by 75 publications

(41 citation statements)

References 14 publications

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“…The distinct staining patterns of SCP (A2) and buccalin (A1) indicate a lack of cross-reactivity between these two antibodies. Although the antibodies were raised against a single member of a peptide family, they probably recognize more than just that member because of the sequence similarities within peptide families (Morris et al, 1982;Mahon et al, 1985;Lloyd et al, 1987b;Miller et al, 1993). Thus, the antibodies will be referred to by the family they recognize, not the individual member they were raised against.…”

Section: The Arc Is Innervated By a Limited Number Of Neuronsmentioning

confidence: 99%

Costorage and Corelease of Modulatory Peptide Cotransmitters with Partially Antagonistic Actions on the Accessory Radula Closer Muscle ofAplysia californica

et al. 1996

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Many neurons that contain a classical neurotransmitter also contain modulatory peptides, but it has been difficult to establish unequivocally that these peptides are functional cotransmitters. Here, we provide evidence for functional cotransmission in a neuromuscular system of Aplysia. Using immunocytochemical techniques, we localize members of two peptide families, the small cardioactive peptides (SCPs) and the buccalins (BUCs), to a single subset of dense-core vesicles in the terminals of the cholinergic motorneuron B15. We describe a new preparation and method for the direct detection of released peptides and show that the SCPs and BUCs are released when neuron B15 is intracellularly stimulated. Consistent with their subcellular localization, the SCPs and BUCs are released in a stoichiometric ratio that is constant across conditions that change the absolute amount of peptides released. Peptide release is calcium-dependent but does not require muscle contractions. Thus, the release cannot be attributed to a displacement of peptides that may be present in the extracellular space. In previous studies, we characterized the physiological firing patterns of neuron B15. Here, we simulate these firing patterns and show that peptide release occurs. Additionally, we find that significant quantities of material are released under behaviorally relevant conditions. We find that concentrations of released peptides in the muscle are in the concentration range in which exogenously applied peptides exert characterized modulatory actions on muscle contractions. Together, our findings provide strong support for the hypothesis that peptides contained in neuron B15 are functional cotransmitters.Key words: neuropeptides; dense-core vesicles; peptide release; Aplysia; cotransmission; EM immunocytochemistry; motor neuron; modulation When several putative transmitters are found in a single neuron, it is easy to assume that they function as cotransmitters. This supposition, however, has been difficult to verify. A recent review of cotransmission (Kupfermann, 1991) concluded that there was no definitive evidence that cotransmission occurs under normal physiological conditions. In general, the greatest obstacle to establishing functional cotransmission has been the difficulty in demonstrating that putative cotransmitters are released when neurons fire in physiological patterns.To overcome difficulties in the study of cotransmission, simpler, more experimentally advantageous model systems were developed. One such system consists of the accessory radula closer (ARC) muscle and its cholinergic motorneurons, B15 and B16. B15 and B16 synthesize peptides that potentiate contraction size and relaxation rate. B15 synthesizes (Cropper et al., 1987a) the small cardioactive peptides (SCPs), and B16 synthesizes the myomodulins (MMs) (Cropper et al., 1987b(Cropper et al., , 1991Brezina et al., 1995). In addition, both motorneurons synthesize the buccalins (BUCs), which depress muscle contractions (Cropper et al., 1988(Cropper et al., , 1990aVilim et...

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Section: The Arc Is Innervated By a Limited Number Of Neuronsmentioning

confidence: 99%

Costorage and Corelease of Modulatory Peptide Cotransmitters with Partially Antagonistic Actions on the Accessory Radula Closer Muscle ofAplysia californica

et al. 1996

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“…Muneoka et al (1994) have proposed to group the peptides that have a PRXamide sequence at their carboxyl termini as PRXamide peptides. These are further divided into three sub-groups: (1) pheromone biosynthesis activating neuropeptide (PBAN) (Raina et al, 1989) and related peptides, (2) small cardioactive peptides (SCPs) (Morris et al, 1982;Lloyd et al, 1987) and (3) antho-RPamide (Carstensen et al, 1992) and related peptides. Members of the first sub-group have quite different functions, while peptides in the other two sub-groups all affect myoactivity.…”

Section: Hym-355 Is a Neuropeptide Involved In Neuron Differentiationmentioning

confidence: 99%

A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra

Takahashi¹,

Koizumi²,

Ariura³

et al. 1999

Comparative Biochemistry and Physiology Part A: Molecular &

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During the course of a systematic screening of peptide signaling molecules in Hydra a novel peptide, Hym-355 (FPQSFLPRG-NH2), was identified. A cDNA encoding the peptide was isolated and characterized. Using both in situ hybridization and immunohistochemistry, Hym-355 was shown to be expressed in neurons and hence is a neuropeptide. The peptide was shown to specifically enhance neuron differentiation throughout the animal by inducing interstitial cells to enter the neuron pathway.Further, co-treatment with a PW peptide, which inhibits neuron differentiation, nullified the effects of both peptides, suggesting that they act in an antagonistic manner. This effect is discussed in terms of a feedback mechanism for maintaining the steady state neuron population in Hydra.

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“…The SCPs are represented by two peptides, SCPA and SCPB, which are 11 and 9 amino acids in length, respectively. These peptides have similar sequences, are derived from a common precursor polypeptide (9)(10)(11), and have been shown to satisfy many of the criteria required of neurotransmitters (12). They are present in, and synthesized by, individual neurons (6)(7)(8) and are contained in membrane-bound dense-core vesicles in central neurons and in varicosities in the central nervous system, muscle, and gut (13,14).…”

Section: Introductionmentioning

confidence: 99%

“…B15 has been shown to synthesize another neuropeptide termed buccalin (21). The other 15 motor neuron, B16, also synthesizes buccalin as well as a second modulatory peptide termed myomodulin (22 10,000…”

Section: Introductionmentioning

confidence: 99%

Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia.

Whim

Lloyd

1989

Proc. Natl. Acad. Sci. U.S.A.

143

110

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We have investigated the release of two peptide cotransmitters from the terminals of a cholinergic motor neuron in Aplysia. Identified motor neuron B15 synthesizes the two small cardioactive peptides (SCP) A and B in addition to acetylcholine. A symmetrical pair of B15 neurons innervate symmetrical buccal muscles, termed 15, which are involved in generating biting movements. The amplitude of I5 contractions is enhanced by the SCPs. Intracellular stimulation of one B15 produces depletion of the SCPs from the stimulated muscle as compared to the unstimulated control muscle. Significant depletion requires either high-frequency stimulation or prolonged bursts at lower frequencies. A second cholinergic motor neuron, B16, also innervates I5 but does not synthesize the SCPs. Stimulation of B16 produced no depletion of the SCPs. Exogenous SCPs potently increase cAMP levels in the muscle. If depletion is a reflection of release, it should be possible to demonstrate an effect ofB15 stimulation on muscle cAMP levels. Indeed, stimulation of B15 did elevate cAMP levels in I5. Stimulation of B16 had no effect on cAMP levels. Increases in cAMP were observed only when B15 was stimulated in a manner that would produce significantly facilitated acetylcholine release. This facilitation could be produced by increased stiniulation frequency, longer burst durations, or shorter interburst intervals. However, B15 is capable of producing cholinergically mediated contractions with stimulation parameters that would not cause release of the SCPs. Thus, B15 appears to function as a purely cholinergic motor neuron when firing slowly, and as a cholinergic/peptidergic neuron when firing rapidly.Over the last decade, it has become clear that many neurons contain multiple transmitters, often one or more peptide transmitters with a single conventional transmitter (1, 2). Knowledge of the regulation of release of coexisting transmitters is crucial to our understanding of the physiological roles of each transmitter and the interactions between them (3-5). The metabolism of conventional transmitters and peptide transmitters differs significantly. Conventional transmitters are synthesized enzymatically at synaptic terminals and, once released, usually have high-affinity uptake systems. Thus, there are cellular mechanisms for maintaining homeostatic levels of conventional transmitters. In contrast, peptide transmitters are cleaved from precursors in the neuronal cell body and transported to remote terminals and there is little evidence for efficient reuptake of most peptides. Consequently, during sustained activation, either the rates of peptide release must be very low compared to total content in the terminals or the peptide content must decline.One class of peptides that have been commonly found to coexist with other transmitters in Aplysia neurons are the small cardioactive peptides (SCPs) (6-8). The SCPs are represented by two peptides, SCPA and SCPB, which are 11 and 9 amino acids in length, respectively. These peptides have similar se...

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Sequence of small cardioactive peptide A: A second member of a class of neuropeptides in Aplysia

Cited by 75 publications

References 14 publications

Costorage and Corelease of Modulatory Peptide Cotransmitters with Partially Antagonistic Actions on the Accessory Radula Closer Muscle ofAplysia californica

Costorage and Corelease of Modulatory Peptide Cotransmitters with Partially Antagonistic Actions on the Accessory Radula Closer Muscle ofAplysia californica

A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra

Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia.

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