Original paper

Juvenile hormone interacts with insulin and potentiates the ERK signaling pathway for female reproduction in locusts

Li, Lunjie; Yang, Libin; Yu, Guangze; Guo, Mingfang; Liu, Lijun; Xu, Mengru; Fu, Xiaoyan; Zhang, Lin-Jie; Jing, Yu-Pu

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Entomologia Generalis Volume 45 Number 2 (2025), p. 547 - 556

published: May 22, 2025
published online: May 15, 2025
manuscript accepted: Mar 6, 2025
final revised version received: Feb 27, 2025
manuscript revision requested: Nov 19, 2024
manuscript received: Sep 29, 2024

DOI: 10.1127/entomologia/2025/3055

BibTeX file

ArtNo. ESP146004502022, Price: 29.00 €

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Abstract

Insulin-like peptides (ILPs) and juvenile hormone (JH) are pivotal endocrine regulators of insect reproduction, yet the mechanisms underlying their interaction in stimulating vitellogenesis and egg production remain largely unexplored. RNA-sequencing analysis of adult female locust fat bodies revealed that the mitogen-activated protein kinase (MAPK) signaling pathway showed significant activity, ranking at the top among the KEGG pathways. RNAi-mediated decomposition of extracellular signal-regulated kinase (ERK), a member of the MAPK family, inhibited vitellogenin (Vg) expression in the fat body and stopped ovarian development and oocyte maturation. Interestingly, ERK phosphorylation was significantly elevated during the vitellogenic phase. Both insulin and JH individually induced ERK phosphorylation; however, their combined application increased the effect. Pharmacological assays showed that insulin activated ERK by a signaling cascade involving the insulin receptor-related receptor (IRR), phosphoinositide 3-kinase (PI3K), rat sarcoma (Ras), fibrosarcoma (Raf) and MAPK kinase (MEK). JH promoted ERK phosphorylation via the G protein-coupled receptors (GPCRs) signaling pathway, involving phospholipase C (PLC), protein kinase C (PKC) and calcium/calmodulin-dependent protein kinase II (CaMKII). Notably, JH induced the formation of the Ras/Raf complex. Inhibitors of PKC and CaMKII attenuated JH-stimulated Ras/Raf interaction. Inhibition of ERK phosphorylation impacted multiple pathways and molecules involved in insect reproduction, encompassing Wingless/Integrated (Wnt), Transforming Growth Factor-β (TGF-β), Target of Rapamycin (TOR), Forkhead box protein O (FoxO), Krüppel homolog 1 (Kr-h1), Glucose-Regulated Protein 78 (Grp78), Cell Division Cycle 6 (Cdc6), and Vg. These findings advance our understanding of how ILPs and JH jointly regulate insect reproduction.

Keywords

insulin-like peptides • MAPK • vitellogenesis •
locusta migratoria
• phosphorylation