Allatostatin A Signalling: Progress and New Challenges From a Paradigmatic Pleiotropic Invertebrate Neuropeptide Family

Overview

Journal Front Physiol

Date 2022 Jul 11

PMID 35812311

Authors

Christian Wegener

Jiangtian Chen

Affiliations

Soon will be listed here.

Abstract

Neuropeptides have gained broad attraction in insect neuroscience and physiology, as new genetic tools are increasingly uncovering their wide-ranging pleiotropic functions with high cellular resolution. Allatostatin A (AstA) peptides constitute one of the best studied insect neuropeptide families. In insects and other panarthropods, AstA peptides qualify as brain-gut peptides and have regained attention with the discovery of their role in regulating feeding, growth, activity/sleep and learning. AstA receptor homologs are found throughout the protostomia and group with vertebrate somatostatin/galanin/kisspeptin receptors. In this review, we summarise the current knowledge on the evolution and the pleiotropic and cell-specific non-allatostatic functions of AstA. We speculate about the core functions of AstA signalling, and derive open questions and challengesfor future research on AstA and invertebrate neuropeptides in general.

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References

Mirabeau O, Joly J . Molecular evolution of peptidergic signaling systems in bilaterians. Proc Natl Acad Sci U S A. 2013; 110(22):E2028-37. PMC: 3670399. DOI: 10.1073/pnas.1219956110. View

Santama N, BRIERLEY M, Burke J, Benjamin P . Neural network controlling feeding in Lymnaea stagnalis: immunocytochemical localization of myomodulin, small cardioactive peptide, buccalin, and FMRFamide-related peptides. J Comp Neurol. 1994; 342(3):352-65. DOI: 10.1002/cne.903420304. View

Lenz C, Williamson M, HANSEN G, Grimmelikhuijzen C . Identification of four Drosophila allatostatins as the cognate ligands for the Drosophila orphan receptor DAR-2. Biochem Biophys Res Commun. 2001; 286(5):1117-22. DOI: 10.1006/bbrc.2001.5475. View

Ni J, Gurav A, Liu W, Ogunmowo T, Hackbart H, Elsheikh A . Differential regulation of the sleep homeostat by circadian and arousal inputs. Elife. 2019; 8. PMC: 6363385. DOI: 10.7554/eLife.40487. View

Robertson L, Rodriguez E, Lange A . The neural and peptidergic control of gut contraction in Locusta migratoria: the effect of an FGLa/AST. J Exp Biol. 2012; 215(Pt 19):3394-402. DOI: 10.1242/jeb.073189. View

Murphy K, Deshpande S, Yurgel M, Quinn J, Weissbach J, Keene A . Postprandial sleep mechanics in . Elife. 2016; 5. PMC: 5119887. DOI: 10.7554/eLife.19334. View

Neupert S, Fusca D, Schachtner J, Kloppenburg P, Predel R . Toward a single-cell-based analysis of neuropeptide expression in Periplaneta americana antennal lobe neurons. J Comp Neurol. 2011; 520(4):694-716. DOI: 10.1002/cne.22745. View

Koyama T, Texada M, Halberg K, Rewitz K . Metabolism and growth adaptation to environmental conditions in Drosophila. Cell Mol Life Sci. 2020; 77(22):4523-4551. PMC: 7599194. DOI: 10.1007/s00018-020-03547-2. View

Allen A, Neville M, Birtles S, Croset V, Treiber C, Waddell S . A single-cell transcriptomic atlas of the adult ventral nerve cord. Elife. 2020; 9. PMC: 7173974. DOI: 10.7554/eLife.54074. View

10.

Donlea J, Pimentel D, Talbot C, Kempf A, Omoto J, Hartenstein V . Recurrent Circuitry for Balancing Sleep Need and Sleep. Neuron. 2018; 97(2):378-389.e4. PMC: 5779612. DOI: 10.1016/j.neuron.2017.12.016. View

11.

Deng B, Li Q, Liu X, Cao Y, Li B, Qian Y . Chemoconnectomics: Mapping Chemical Transmission in Drosophila. Neuron. 2019; 101(5):876-893.e4. DOI: 10.1016/j.neuron.2019.01.045. View

12.

Fuse M, Zhang J, Partridge E, Nachman R, Orchard I, Bendena W . Effects of an allatostatin and a myosuppressin on midgut carbohydrate enzyme activity in the cockroach Diploptera punctata. Peptides. 1999; 20(11):1285-93. DOI: 10.1016/s0196-9781(99)00133-3. View

13.

Onken H, Moffett S, Moffett D . The anterior stomach of larval mosquitoes (Aedes aegypti): effects of neuropeptides on transepithelial ion transport and muscular motility. J Exp Biol. 2004; 207(Pt 21):3731-9. DOI: 10.1242/jeb.01208. View

14.

MarderY E . Allatostatin decreases stomatogastric neuromuscular transmission in the crab Cancer borealis. J Exp Biol. 1998; 200(Pt 23):2937-46. DOI: 10.1242/jeb.200.23.2937. View

15.

Park J, Chen J, Jang S, Ahn T, Kang K, Choi M . A subset of enteroendocrine cells is activated by amino acids in the Drosophila midgut. FEBS Lett. 2016; 590(4):493-500. DOI: 10.1002/1873-3468.12073. View

16.

Vitzthum H, Homberg U, Agricola H . Distribution of Dip-allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. J Comp Neurol. 1996; 369(3):419-37. DOI: 10.1002/(SICI)1096-9861(19960603)369:3<419::AID-CNE7>3.0.CO;2-8. View

17.

Christie A, Roncalli V, Wu L, Ganote C, Doak T, Lenz P . Peptidergic signaling in Calanus finmarchicus (Crustacea, Copepoda): in silico identification of putative peptide hormones and their receptors using a de novo assembled transcriptome. Gen Comp Endocrinol. 2013; 187:117-35. DOI: 10.1016/j.ygcen.2013.03.018. View

18.

Stay B, Tobe S . The role of allatostatins in juvenile hormone synthesis in insects and crustaceans. Annu Rev Entomol. 2006; 52:277-99. DOI: 10.1146/annurev.ento.51.110104.151050. View

19.

Dircksen H, Skiebe P, Abel B, Agricola H, Buchner K, Muren J . Structure, distribution, and biological activity of novel members of the allatostatin family in the crayfish Orconectes limosus. Peptides. 1999; 20(6):695-712. DOI: 10.1016/s0196-9781(99)00052-2. View

20.

Sarkar N, Tobe S, Orchard I . The distribution and effects of Dippu-allatostatin-like peptides in the blood-feeding bug, Rhodnius prolixus. Peptides. 2004; 24(10):1553-62. DOI: 10.1016/j.peptides.2003.07.015. View