The long and the short of it – a perspective on peptidergic regulation of circuits and behaviour

Jékely, Gáspár; Melzer, Sarah; Beets, Isabel; Kadow, Ilona C. Grunwald; Koene, Joris M.; Haddad, Sara A.; Holden‐Dye, Lindy

doi:10.1242/jeb.166710

Cited by 84 publications

(86 citation statements)

References 188 publications

(199 reference statements)

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“…Neuropeptides can be released at synapses (either alone or together with small molecule transmitters [1]) and act on postsynaptic neurons. They can also be released extrasynaptically and act via volume transmission in the nervous system (2). Release at neurohemal release sites allows neuropeptides to act as hormones in long-range signaling.…”

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confidence: 99%

Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis

et al. 2018

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Neuropeptides commonly signal by metabotropic GPCRs. In some mollusks and cnidarians, RFamide neuropeptides mediate fast ionotropic signaling by peptide-gated ion channels that belong to the DEG/ENaC family. Here we describe a neuropeptide system with a dual mode of signaling by both a peptide-gated ion channel and a GPCR. We identified and characterized a peptide-gated channel in the marine annelid Platynereis dumerilii that is specifically activated by Wamide myoinhibitory peptides derived from the same proneuropeptide. The myoinhibitory peptide-gated ion channel (MGIC) belongs to the DEG/ENaC family and is paralogous to RFamide-gated ion channels. Platynereis myoinhibitory peptides also activate a previously described GPCR, MAG. We measured the potency of all Wamides on both MGIC and MAG and identified peptides that preferentially activate one or the other receptor. Analysis of a single-cell transcriptome resource indicates that MGIC and MAG signal in distinct target neurons. The identification of a Wamide-gated ion channel suggests that peptide-gated channels are more diverse and widespread in animals than previously appreciated. The possibility of neuropeptide signaling by both ionotropic and metabotropic receptors to different target cells in the same organism highlights an additional level of complexity in peptidergic signaling networks.-Schmidt, A., Bauknecht, P., Williams, E. A., Augustinowski, K., Gründer, S., Jékely, G. Dual signaling of Wamide myoinhibitory peptides through a peptide-gated channel and a GPCR in Platynereis.

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Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis

et al. 2018

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“…In T. adhaerens, several populations of topographically organized peptide-secreting cells can strongly modulate the animals' movements. Our results suggest that peptidergic signalling is an important mode of communication for placozoans, as is the case for cnidarians and bilaterians [11,[35][36][37][38][39].…”

Section: Neuropeptides Elicit Strong Stereotypical Behaviours In Tricmentioning

confidence: 57%

High cell diversity and complex peptidergic signalling underlie placozoan behaviour

Varoqueaux

Williams

Grandemange

et al. 2018

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Placozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioural control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive communication cells during the rise of animals is not yet understood [1][2][3][4][5]. The placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple bodyplan [6-9]: a flat upper epithelium and a cylindrical lower epithelium interspersed with a loose layer of fiber cells. Its genome encodes several proneuropeptide genes and genes involved in neurosecretion in animals with a nervous system [10-12]. Here we investigate neuropeptide signalling in Trichoplax adhaerens. We found specific expression of several neuropeptides in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected celltype diversity of Trichoplax adhaerens. Using live imaging, we uncovered that treatments with 11 different neuropeptides elicited striking and consistent effects on the animals' shape, patterns of movement and velocity that we categorized under three main types: (i) crinkling, (ii) turning, and (iii) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signalling in nerveless placozoans and suggest that peptidergic volume signalling may have predated synaptic signalling in the evolution of nervous systems.

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“…Amidated neuropeptides like MIH commonly signal through GPCRs, although other receptor types can also be used [23]. As the first step to select candidate MIH receptors, we compiled a comprehensive catalogue of Clytia GPCRs from a Clytia reference transcriptome covering all life-cycle stages.…”

Section: Selection Of Candidate Mih Gpcrsmentioning

confidence: 99%

A G-protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

Artigas

Lapébie

Leclère

et al. 2019

Preprint

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The reproductive hormones that trigger oocyte meiotic maturation and release from the ovary vary greatly between animal species. Identification of receptors for these Maturation Inducing Hormones (MIHs), and understanding how they initiate the largely conserved maturation process, remain important challenges. In hydrozoan cnidarians including the jellyfish Clytia hemisphaerica, MIH comprises neuropeptides released from somatic cells of the gonad. We identified the receptor (MIHR) for these MIH neuropeptides in Clytia using cell culture-based "deorphanization" of candidate oocyte-expressed GPCRs. MIHR mutant jellyfish generated using CRISPR-Cas9 had severe defects in gamete development or in spawning both in males and females. Female gonads, or oocytes isolated from MIHR mutants, failed to respond to synthetic MIH. Treatment with the cAMP analogue 5'Br-cAMP to mimic cAMP rise at maturation onset rescued meiotic maturation and spawning. Injection of inhibitory antibodies to Gα S into wild type oocytes phenocopied the MIHR mutants. These results provide the molecular links between MIH stimulation and meiosis initiation in hydrozoan oocytes. Molecular phylogeny grouped Clytia MIHR with a subset of bilaterian neuropeptide receptors including Neuropeptide Y, Gonadotropin Inhibitory Hormone, pyroglutamylated RFamide and Luqin, all upstream regulators of sexual reproduction. This identification and functional characterisation of a cnidarian peptide GPCR advances our understanding of oocyte maturation initiation and sheds light on the evolution of neuropeptidehormone systems. Non-standard Abbreviations: MIH -Maturation Inducing Hormone; GVBD -Germinal VesicleBreakdown.

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The long and the short of it – a perspective on peptidergic regulation of circuits and behaviour

Cited by 84 publications

References 188 publications

Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis

Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis

High cell diversity and complex peptidergic signalling underlie placozoan behaviour

A G-protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

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