1. Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in Platynereis
- Author
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Alessandra Polo, Andrea Bileck, Isabel Beets, Florian Raible, Charline Borghgraef, Caroline Broyart, Liliane Schoofs, Karim Vadiwala, Gabriele Andreatta, Christopher Gerner, and Vitaly V. Kozin
- Subjects
Receptors, Neuropeptide ,FOOD-INTAKE ,Proteomics ,Energy homeostasis ,Gonadotropin-Releasing Hormone ,0302 clinical medicine ,Homeostasis ,Sexual maturity ,PEPTIDE ,Sexual Maturation ,BRAIN ,Moon ,Receptor ,GLYCOGEN-SYNTHASE ,Phylogeny ,GONADOTROPIN-RELEASING-HORMONE ,0303 health sciences ,Multidisciplinary ,Brain ,Biological Sciences ,INSULIN ,Cell biology ,Multidisciplinary Sciences ,DNA-Binding Proteins ,PNAS Plus ,Hormone receptor ,Gene Knockdown Techniques ,Insect Hormones ,Science & Technology - Other Topics ,Insect Proteins ,KISSPEPTIN ,Signal Transduction ,Platynereis ,EXPRESSION ,Receptors, Peptide ,Biology ,lunar periodicity ,Preprohormone ,reproduction ,03 medical and health sciences ,Commentaries ,Animals ,corazonin ,030304 developmental biology ,Science & Technology ,Neuropeptides ,DIABETES-MELLITUS ,Polychaeta ,biology.organism_classification ,Invertebrates ,Corazonin ,GnRH ,regeneration ,Peptides ,ADIPOKINETIC HORMONE ,030217 neurology & neurosurgery ,Developmental Biology ,Transcription Factors - Abstract
Significance Gonadotropin Releasing Hormone (GnRH) acts as a key regulator of sexual maturation in vertebrates, and is required for the integration of environmental stimuli to orchestrate breeding cycles. Whether this integrative function is conserved across phyla remains unclear. We characterized GnRH-type signaling systems in the marine worm Platynereis dumerilii, in which both metabolic state and lunar cycle regulate reproduction. We find gnrh-like (gnrhl) genes upregulated in sexually mature animals, after feeding, and in specific lunar phases. Animals in which the corazonin1/gnrhl1 gene has been disabled exhibit delays in growth, regeneration, and maturation. Molecular analyses reveal glycoprotein turnover/energy homeostasis as targets of CRZ1/GnRHL1. These findings point at an ancestral role of GnRH superfamily signaling in coordinating energy demands dictated by environmental and developmental cues., The molecular mechanisms by which animals integrate external stimuli with internal energy balance to regulate major developmental and reproductive events still remain enigmatic. We investigated this aspect in the marine bristleworm, Platynereis dumerilii, a species where sexual maturation is tightly regulated by both metabolic state and lunar cycle. Our specific focus was on ligands and receptors of the gonadotropin-releasing hormone (GnRH) superfamily. Members of this superfamily are key in triggering sexual maturation in vertebrates but also regulate reproductive processes and energy homeostasis in invertebrates. Here we show that 3 of the 4 gnrh-like (gnrhl) preprohormone genes are expressed in specific and distinct neuronal clusters in the Platynereis brain. Moreover, ligand–receptor interaction analyses reveal a single Platynereis corazonin receptor (CrzR) to be activated by CRZ1/GnRHL1, CRZ2/GnRHL2, and GnRHL3 (previously classified as AKH1), whereas 2 AKH-type hormone receptors (GnRHR1/AKHR1 and GnRHR2/AKHR2) respond only to a single ligand (GnRH2/GnRHL4). Crz1/gnrhl1 exhibits a particularly strong up-regulation in sexually mature animals, after feeding, and in specific lunar phases. Homozygous crz1/gnrhl1 knockout animals exhibit a significant delay in maturation, reduced growth, and attenuated regeneration. Through a combination of proteomics and gene expression analysis, we identify enzymes involved in carbohydrate metabolism as transcriptional targets of CRZ1/GnRHL1 signaling. Our data suggest that Platynereis CRZ1/GnRHL1 coordinates glycoprotein turnover and energy homeostasis with growth and sexual maturation, integrating both metabolic and developmental demands with the worm’s monthly cycle.
- Published
- 2019