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Curr Biol . 2020 Jun 8;

The Corazonin-PTTH Neuronal Axis Controls Systemic Body Growth by Regulating Basal Ecdysteroid Biosynthesis in Drosophila melanogaster

Liron Malki, Ofer Sarig, Nicole Cesarato, Janan Mohamad, Talia Canter, Sari Assaf, Mor Pavlovsky, Dan Vodo, Yossi Anis, Ofer Bihari, Kiril Malovitski, Andrea Gat, Holger Thiele, Bethany E Perez White, Liat Samuelov, Arti Nanda, Amy S Paller, Regina C Betz, Eli Sprecher, Xueyi Shen, David M Howard, Mark J Adams, W David Hill, Toni-Kim Clarke, Major Depressive Disorder Working Group of the Psychiatric Genomics Consortium, Ian J Deary, Heather C Whalley, Andrew M McIntosh, Samuel M Gonçalves, Cláudio Duarte-Oliveira, Cláudia F Campos, Vishukumar Aimanianda, Rob Ter Horst, Luis Leite, Toine Mercier, Paulo Pereira, Miguel Fernández-García, Daniela Antunes, Cláudia S Rodrigues, Catarina Barbosa-Matos, Joana Gaifem, Inês Mesquita, António Marques, Nuno S Osório, Egídio Torrado, Fernando Rodrigues, Sandra Costa, Leo Ab Joosten, Katrien Lagrou, Johan Maertens, João F Lacerda, António Campos Jr, Gordon D Brown, Axel A Brakhage, Coral Barbas, Ricardo Silvestre, Frank L van de Veerdonk, Georgios Chamilos, Mihai G Netea, Jean-Paul Latgé, Cristina Cunha, Agostinho Carvalho, Katarina Jurikova, Martin Gajarsky, Mona Hajikazemi, Jozef Nosek, Katarina Prochazkova, Katrin Paeschke, Lukas Trantirek, Lubomir Tomaska, Eisuke Imura, Yuko Shimada-Niwa, Takashi Nishimura, Sebastian Hückesfeld, Philipp Schlegel, Yuya Ohhara, Shu Kondo, Hiromu Tanimoto, Albert Cardona, Michael J Pankratz, Ryusuke Niwa

Steroid hormones play key roles in development, growth, and reproduction in various animal phyla [1]. The insect steroid hormone, ecdysteroid, coordinates growth and maturation, represented by molting and metamorphosis [2]. In Drosophila melanogaster, the prothoracicotropic hormone (PTTH)-producing neurons stimulate peak levels of ecdysteroid biosynthesis for maturation [3]. Additionally, recent studies on PTTH signaling indicated that basal levels of ecdysteroid negatively affect systemic growth prior to maturation [4-8]. However, it remains unclear how PTTH signaling is regulated for basal ecdysteroid biosynthesis. Here, we report that Corazonin (Crz)-producing neurons regulate basal ecdysteroid biosynthesis by affecting PTTH neurons. Crz belongs to gonadotropin-releasing hormone (GnRH) superfamily, implying an analogous role in growth and maturation [9]. Inhibition of Crz neuronal activity increased pupal size, whereas it hardly affected pupariation timing. This phenotype resulted from enhanced growth rate and a delay in ecdysteroid elevation during the mid-third instar larval (L3) stage. Interestingly, Crz receptor (CrzR) expression in PTTH neurons was higher during the mid- than the late-L3 stage. Silencing of CrzR in PTTH neurons increased pupal size, phenocopying the inhibition of Crz neuronal activity. When Crz neurons were optogenetically activated, a strong calcium response was observed in PTTH neurons during the mid-L3, but not the late-L3, stage. Furthermore, we found that octopamine neurons contact Crz neurons in the subesophageal zone (SEZ), transmitting signals for systemic growth. Together, our results suggest that the Crz-PTTH neuronal axis modulates ecdysteroid biosynthesis in response to octopamine, uncovering a regulatory neuroendocrine system in the developmental transition from growth to maturation.

PMID: 32386525