Neurosecretion of egg-laying hormone and other peptides from electrically active bag cell neurons of Aplysia

Stuart, Duncan K.; Chiu, Arlene Y.; Strumwasser, Felix

doi:10.1152/jn.1980.43.2.488

Cited by 89 publications

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“…The three peptides inhibit left upper quadrant neurons at relative potencies of 10:30:1 (seven-, eight-, and nine-residue peptides, respectively). Recent molecular genetic analysis shows that both a-BCP [1][2][3][4][5][6][7][8][9] and egg-laying hormone are encoded by the same bag cell-specific gene. The multiple neuronal effects of bag cells are therefore likely to be mediated by at least two transmitters that are cleaved from a common precursor molecule.…”

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“…They may also serve as autoexcitatory transmitters since the seven-residue peptide produces a slow depolarization of the bag cells similar to that which occurs during bag cell discharge. The amino acid sequence of the largest peptide, termed a-bag cell peptide [1][2][3][4][5][6][7][8][9], is H-Ala-Pro-Arg-Leu-Arg-Phe-Tyr-Ser-Leu-OH. The other two peptides are identical to a-BCP[I-9] except that they lack the COOH-terminal Ser-Leu or leucine residues.…”

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“…It has been determined that egg-laying hormone (ELH), a 4,400-dalton peptide that is synthesized and released by bag cells (5)(6)(7)(8), is probably the neurotransmitter mediating two types of excitatory neuronal responses, burst augmentation of cell R15 and prolonged excitation of left lower quadrant (LLQ) neurons (9)(10)(11). However, when perfused into the abdominal ganglion at physiological concentrations, purified ELH has little or no effect on left upper quadrant (LUQ) neurons, cells L2-L4, L6, which are normally inhibited by bag cell discharge (10,11).…”

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Primary structure and neuronal effects of α-bag cell peptide, a second candidate neurotransmitter encoded by a single gene in bag cell neurons of Aplysia

Rothman

Mayeri

et al. 1983

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

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A discharge of impulse activity in a group of neuroendocrine cells, the bag cells, produces several types of prolonged responses in various identified neurons of the abdominal ganglion of Aplysia. Two excitatory responses are almost certainly mediated by egg-laying hormone, but this peptide cannot account for other responses, such as inhibition of left upper quadrant neurons. We report here the isolation from bag cell clusters of three structurally similar peptides, seven, eight, and nine residues long, that are candidate transmitters for mediating bag cell-induced inhibition. They may also serve as autoexcitatory transmitters since the seven-residue peptide produces a slow depolarization of the bag cells similar to that which occurs during bag cell discharge. The amino acid sequence of the largest peptide, termed a-bag cell peptide [1][2][3][4][5][6][7][8][9], is H-Ala-Pro-Arg-Leu-Arg-Phe-Tyr-Ser-Leu-OH. The other two peptides are identical to a-BCP[I-9] except that they lack the COOH-terminal Ser-Leu or leucine residues. The three peptides inhibit left upper quadrant neurons at relative potencies of 10:30:1 (seven-, eight-, and nine-residue peptides, respectively). Recent molecular genetic analysis shows that both a-BCP [1][2][3][4][5][6][7][8][9] and egg-laying hormone are encoded by the same bag cell-specific gene. The multiple neuronal effects of bag cells are therefore likely to be mediated by at least two transmitters that are cleaved from a common precursor molecule.The marine mollusk Aplysia is a convenient experimental system for investigating at the cellular and molecular levels the roles of neuropeptides as neurotransmitters and in the regulation of behavior. Egg laying in Aplysia is accompanied by a stereotyped behavioral pattern that lasts for several hours. The behavior pattern is thought to be initiated and controlled by the bag cells, a group of neuroendocrine cells located in the abdominal ganglion. In intact animals, egg laying is invariably preceded by a repetitive impulse discharge of the bag cells (1). In the isolated abdominal ganglion, where the central actions of the bag cells have been most extensively studied, a bag cell discharge produces at least four types of long-lasting excitatory and inhibitory effects on various identified neurons (2-4).To identify the neurotransmitters mediating these effects, extracts of bag cells have been purified and assayed for activity on various neurons. It has been determined that egg-laying hormone (ELH), a 4,400-dalton peptide that is synthesized and released by bag cells (5-8), is probably the neurotransmitter mediating two types of excitatory neuronal responses, burst augmentation of cell R15 and prolonged excitation of left lower quadrant (LLQ) neurons (9-11). However, when perfused into the abdominal ganglion at physiological concentrations, purified ELH has little or no effect on left upper quadrant (LUQ) neurons, cells L2-L4, L6, which are normally inhibited by bag cell discharge (10, 11). This indicates that ELH does not directly or in...

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Primary structure and neuronal effects of α-bag cell peptide, a second candidate neurotransmitter encoded by a single gene in bag cell neurons of Aplysia

Rothman

Mayeri

et al. 1983

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

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“…The neuropeptidergic bag cells in the abdominal ganglion of Aplysia californica are able to initiate egg laying and its associated behavior by secreting egg-laying hormone (ELH) during a long-lasting afterdischarge (1)(2)(3). This afterdischarge may be triggered by electric stimulation of a presumed afferent pathway from the head ganglia (4,5).…”

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Purification and primary structure of two neuroactive peptides that cause bag cell afterdischarge and egg-laying in Aplysia

Heller

Kaczmarek

Hunkapiller

et al. 1980

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

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Two neuroactive peptides, A and B, have been isolated from the atrial gland in the reproductive tract of Aplysia. Each of the two peptides is able to induce egg-laying behavior in reci ient animals. In vitro recordings rom the abdominal ganglion show that both peptides also trigger longlasting discharges in the bag cell neurons at concentrations around 0.1 #M. The peptides were purified by a combination of ammonium sulfate precipitation, agarose gel filtration, and cation exchange chromatography. Each peptide has 34 amino acid residues. Microsequencing together wi carboxypeptidase Y degradation and analysis of tryptic peptides revealed the following sequence for peptide A: H-Ala-Val-Lys-Leu-Ser-SerAsp-Gly-Asn-Tyr-Pro-Phe-Asp-Leu-Ser-Lys-Glu-Asp-Gly-AlaGln-Pro-Tyr-Phe-Met-Thr-Pro-Arg-Leu-Arg-Phe-Tyr-Pro-Ile.Peptide B differs from A in only four positions. The first nine residues of B are: Ala-Val-Lys-Ser-Ser-Ser-Tyr-Glu-Lys-, whereas residues 10-34 of B are identical to those of A. The calculated M, of A is 3924 and that of B is 4032. The pI of peptide A as determined by isoelectric focusing in polyacrylamide gels is 7.9-8.1 and that of peptide B is 9.0-9.2. It is estimated that each atrial gland contains at least 150 jug of peptide A and 50 ,ug of B. Neither peptide resembles the egg-laying hormone isolated from bag cell neurons. It is postu ated that the atrial gland peptides are released during copulation, and then by interacting with neuronal receptors in the head ganglia and pleuroabdominal connectives they cause the bag cells to afterdischarge, thereby releasing egg-laying hormone.The neuropeptidergic bag cells in the abdominal ganglion of Aplysia californica are able to initiate egg laying and its associated behavior by secreting egg-laying hormone (ELH) during a long-lasting afterdischarge (1-3). This afterdischarge may be triggered by electric stimulation of a presumed afferent pathway from the head ganglia (4, 5). Neither the location in the head ganglia nor the transmitter of these input neurons to the bag cells are presently known.When a homogenate of bag cells containing ELH is injected into the hemocoel of a sexually mature animal, a pattern of egg-laying behavior is triggered that results in egg laying within an hour after injection (6, 7). ELH has been purified and found to be a polypeptide of 36 amino acids with a Mr of 4385 and a pI of 9.0-9.2 (8). Copulation may be a natural stimulus for egg laying and it has recently been shown that the atrial glabd in the reproductive tract of Aplysia contains a factor that is able to induce egg-laying behavior, in a similar way to ELH, when injected into recipient Aplysia (9, 10). Moreover, it was shown that the atrial gland factor resembles ELH in apparent molecular weight and pI, although in contrast to bag cell homogenates some bioactive material was at pH 7.4 on isoelectric focusing gels in addition to the pI 9.3 material (9, 10). This paper describes the purification and primary structure of two atrial gland peptides, each of which is able to in...

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“…We chose to follow the appearance of AP and ELH as indicators of the final stages of precursor processing because they are known to be transported by a colchicine-sensitive process and secreted in response to depolarization (Arch, 1972a;Arch et al, 1976bKupfermann, 1972Loh et al, 1975;Stuart et al, 1980). Moreover, because of their relatively high leucine content (Chiu et al, 1979;Scheller et al, 1983) and dissimilar isoelectric points (Arch et al, 1976a), radiolabeling and isoelectric focusing give clear indications of their presence in samples of interest (e.g., Fig.…”

Section: Our Initial Experimentsmentioning

confidence: 99%

Neuropeptide routing in the bag cells: kinetic differences in the appearance of newly labeled peptides in transport and secretion

Arch¹,

Linstedt²,

Whitney³

et al. 1986

J. Neurosci.

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The bag cell neurons of Aplysia synthesize and secrete several peptides. Some of these, in addition to the egg-laying hormone (ELH), are strongly implicated in the various alterations of central neuronal activity that accompany an electrical discharge of the bag cells. Thus, the secreted peptides appear to play a variety of roles in the animal's physiology. We have been interested in the intracellular mechanisms that precede peptide secretion from the bag cells because of the evidence that most, if not all, of these peptides are derived from a common precursor. Our objective has been to determine if presumed products of this precursor are processed coordinately following their synthesis. We have concentrated on two peptides (ELH and the acidic peptide, AP) because they are most easily identified in our analytical systems. On pulse-chase radiolabeling of the cells in vitro, we found that labeled AP appears before labeled ELH in axonal transport. This observation is not easily accounted for by the assumption, taken from studies of other peptide-secreting cells, that a precursor to both peptides is loaded into secretory granules before further processing ensues. Since the initial disproportion in the representation of the peptides in transport is no longer detectable at long chase times (18 and 24 hr), we examined the possibilities that ELH production is delayed relative to that of AP or that AP is degraded more rapidly than ELH. No evidence was found for either process. The disproportion between the newly labeled peptides in transport was evident on analysis of the medium bathing bag cells depolarized after 24 hr of chase.(ABSTRACT TRUNCATED AT 250 WORDS)

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Neurosecretion of egg-laying hormone and other peptides from electrically active bag cell neurons of Aplysia

Cited by 89 publications

References 0 publications

Primary structure and neuronal effects of α-bag cell peptide, a second candidate neurotransmitter encoded by a single gene in bag cell neurons of Aplysia

Primary structure and neuronal effects of α-bag cell peptide, a second candidate neurotransmitter encoded by a single gene in bag cell neurons of Aplysia

Purification and primary structure of two neuroactive peptides that cause bag cell afterdischarge and egg-laying in Aplysia

Neuropeptide routing in the bag cells: kinetic differences in the appearance of newly labeled peptides in transport and secretion

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