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      Identification and In Vivo Characterisation of Cardioactive Peptides in Drosophila melanogaster

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          Abstract

          Neuropeptides and peptide hormones serve as critical regulators of numerous biological processes, including development, growth, reproduction, physiology, and behaviour. In mammals, peptidergic regulatory systems are complex and often involve multiple peptides that act at different levels and relay to different receptors. To improve the mechanistic understanding of such complex systems, invertebrate models in which evolutionarily conserved peptides and receptors regulate similar biological processes but in a less complex manner have emerged as highly valuable. Drosophila melanogaster represents a favoured model for the characterisation of novel peptidergic signalling events and for evaluating the relevance of those events in vivo. In the present study, we analysed a set of neuropeptides and peptide hormones for their ability to modulate cardiac function in semi-intact larval Drosophila melanogaster. We identified numerous peptides that significantly affected heart parameters such as heart rate, systolic and diastolic interval, rhythmicity, and contractility. Thus, peptidergic regulation of the Drosophila heart is not restricted to chronotropic adaptation but also includes inotropic modulation. By specifically interfering with the expression of corresponding peptides in transgenic animals, we assessed the in vivo relevance of the respective peptidergic regulation. Based on the functional conservation of certain peptides throughout the animal kingdom, the identified cardiomodulatory activities may be relevant not only to proper heart function in Drosophila, but also to corresponding processes in vertebrates, including humans.

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          A receptor that mediates the post-mating switch in Drosophila reproductive behaviour.

          Mating in many species induces a dramatic switch in female reproductive behaviour. In most insects, this switch is triggered by factors present in the male's seminal fluid. How these factors exert such profound effects in females is unknown. Here we identify a receptor for the Drosophila melanogaster sex peptide (SP, also known as Acp70A), the primary trigger of post-mating responses in this species. Females that lack the sex peptide receptor (SPR, also known as CG16752), either entirely or only in the nervous system, fail to respond to SP and continue to show virgin behaviours even after mating. SPR is expressed in the female's reproductive tract and central nervous system. The behavioural functions of SPR map to the subset of neurons that also express the fruitless gene, a key determinant of sex-specific reproductive behaviour. SPR is highly conserved across insects, opening up the prospect of new strategies to control the reproductive and host-seeking behaviours of agricultural pests and human disease vectors.
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              Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster.

              Mating elicits two major changes in the reproductive behavior of many insect females. The egg-laying rate increases and the readiness to accept males (receptivity) is reduced. These postmating responses last approximately 1 week in Drosophila melanogaster. Males that do not transfer sperm but transfer seminal fluid during mating induce a short-term response of 1 day. The long-term response of 1 week requires the presence of sperm (sperm effect). Hence, sperm is essential for the long-term persistence of the postmating responses. Three seminal fluid peptides elicit postmating responses: ovulin, sex-peptide (SP), and DUP99B. Using the technique of targeted mutagenesis by homologous recombination, we have produced males with mutant SP genes. Here, we report that males lacking functional SP elicit only a weak short-term response. However, these males do transfer sperm. Thus, (i) SP is the major agent eliciting the short-term and the long-term postmating responses and (ii) sperm is merely the carrier for SP. The second conclusion is supported by the finding that SP binds to sperm. The 36-aa-encoding SP gene is the first small Drosophila gene knocked out with the method of homologous recombination.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                20 December 2018
                January 2019
                : 20
                : 1
                : 2
                Affiliations
                Department of Zoology and Developmental Biology, University of Osnabrück, Barbarastraße 11, 49076 Osnabrück, Germany; Ronja.Schiemann@ 123456biologie.uni-osnabrueck.de (R.S.); kay.lammers@ 123456biologie.uni-osnabrueck.de (K.L.); Maren.Janz@ 123456biologie.uni-osnabrueck.de (M.J.); ja.lohmann@ 123456gmx.de (J.L.); achim.paululat@ 123456biologie.uni-osnabrueck.de (A.P.)
                Author notes
                Author information
                https://orcid.org/0000-0002-3304-4523
                Article
                ijms-20-00002
                10.3390/ijms20010002
                6337577
                30577424
                736396ca-1f13-454d-95e9-32e8ebd4c5b1
                © 2018 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 02 November 2018
                : 22 November 2018
                Categories
                Article

                Molecular biology
                endocrine signalling,dorsal vessel,heart function,heart physiology,neuropeptides,peptide hormones,peptide signalling

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