Phospholipase Cγ1 Connects the Cell Membrane Pathway to the Nuclear Receptor Pathway in Insect Steroid Hormone Signaling

Liu, Wen; Cai, Mei-Juan; Zheng, C.; Wang, Jin-Xing; Zhao, Xiao‐Fan

doi:10.1074/jbc.m113.547018

Cited by 51 publications

(68 citation statements)

References 52 publications

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“…Recent studies have shown that ultraspiracle (USP, a component of the functional ecdysteroid receptor complex) is phosphorylated by PKC in Drosophila (42). In H. armigera, it seems that the 20E-induced phosphorylation of USP relies on the function of PLC and Ca 2+ influx (43). Although different isoforms of PKC and PLC may be involved in 20E and JH signaling, it is possible that JH uses the membrane-initiated signaling to influence the cell responses to 20E.…”

Section: Discussionmentioning

confidence: 99%

Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein

Liu

Peng

Zhu

2015

Proc. Natl. Acad. Sci. U.S.A.

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Juvenile hormone (JH) is a key regulator of a wide diversity of developmental and physiological events in insects. Although the intracellular JH receptor methoprene-tolerant protein (MET) functions in the nucleus as a transcriptional activator for specific JHregulated genes, some JH responses are mediated by signaling pathways that are initiated by proteins associated with plasma membrane. It is unknown whether the JH-regulated gene expression depends on the membrane-mediated signal transduction. In Aedes aegypti mosquitoes, we found that JH activated the phospholipase C (PLC) pathway and quickly increased the levels of inositol 1,4,5-trisphosphate, diacylglycerol, and intracellular calcium, leading to activation and autophosphorylation of calcium/calmodulin-dependent protein kinase II (CaMKII). When abdomens from newly emerged mosquitoes were cultured in vitro, the JH-activated gene expression was repressed substantially if specific inhibitors of PLC or CaMKII were added to the medium together with JH. In newly emerged female mosquitoes, RNAi-mediated depletion of PLC or CaMKII considerably reduced the expression of JH-responsive genes, including the Krüppel homolog 1 gene (AaKr-h1) and the early trypsin gene (AaET). JH-induced loading of MET to the promoters of AaKr-h1 and AaET was weakened drastically when either PLC or CaMKII was inactivated in the cultured tissues. Therefore, the results suggest that the membraneinitiated signaling pathway modifies the DNA-binding activity of MET via phosphorylation and thus facilitates the genomic responses to JH. In summary, this study reveals an interplay of genomic and nongenomic signaling mechanisms of JH.insect hormone | development | phospholipase C | protein kinase | transcription J uvenile hormones (JH) are a group of acyclic sesquiterpenoids produced in insects by the corpora allata, a pair of endocrine glands connected to the brain (1). They are important regulators in a wide variety of developmental and physiological events in insects, including development, reproduction, caste determination, behavior, diapauses, polyphenisms, and longevity (2-4).Many effects of JH are mediated by the methoprene-tolerant (MET) protein, an intracellular JH receptor (5). MET contains a basic helix-loop-helix (bHLH) DNA-recognition motif near the N terminus, followed by two tandem Per-ARNT-Sim (PAS) domains, PAS-A and PAS-B (6). In vitro studies have demonstrated that JH-III binds MET with relatively high affinity and have identified a putative JH-binding pocket in the PAS-B domain of MET (7,8). In the presence of JH, MET forms a heterodimer with a p160 steroid receptor coactivator (SRC), which also contains the bHLH-PAS domain (7, 9). The orthologs of SRC are called "Taiman" (TAI) in Drosophila melanogaster and "Ftz-F1-interacting steroid receptor coactivator" (FISC) in the yellow fever mosquito Aedes aegypti (10, 11). For simplicity, we will use a single name, Taiman, to describe all its orthologs in insects. TAI acts as the DNA-binding partner of MET; the MET-TAI complex recogni...

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Section: Discussionmentioning

confidence: 99%

Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein

Liu

Peng

Zhu

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…20E mediates CDK10 phosphorylation to enhance formation of the EcRB1/USP1 transcription complex 36 . 20E via GPCR-, PLC-, Ca 21 -, and PKC-signaling mediates USP1 phosphorylation for gene transcription 12 . At the downstream of ligand activated-GPCR, PLC hydrolyzes phosphatidylinositol 4,5-bisphosphate to generate inositol 1,4,5-triphosphate (IP3) and diacylglycerol (DAG) 37 .…”

Section: Discussionmentioning

confidence: 99%

“…IP3 binds to its receptor in the endoplasmic reticulum membrane to drive the release of intracellular calcium ions, whereas DAG and Ca 21 bind to the protein kinase C (PKC) to activate PKC 38 . 20E via PKC regulates CDK10 11 and USP1 phosphorylation to form the EcR/USP transcription complex 12 . In the current study, the larvae died before pupation or delayed pupation after knockdown of ErGPCR-2, suggesting that ErGPCR-2 is involved in gene transcription and metamorphosis in the 20E pathway.…”

Section: Discussionmentioning

confidence: 99%

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G-protein-coupled receptor controls steroid hormone signaling in cell membrane

Wang¹

2016

2016 International Congress of Entomology

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“…The 20E-induced cell responses have been reported in our previous studies. 36 In summary CKS1 promotes midgut regenerative cell proliferation during the larval growth stage to increase midgut cell number, thereby increasing midgut size for nutrient absorption and larval growth. Insulin (via InR, PI3K, and AKT) promotes CKS1 expression Figure 9.…”

Section: Cks1 Expression Was Coordinately Regulated By Insulin and 20ementioning

confidence: 99%

Cyclin-dependent kinase regulatory subunit 1 promotes cell proliferation by insulin regulation

Liu¹,

Zhao²,

Wang

et al. 2015

Cell Cycle

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These authors contributed equally to this work.Keywords: body size, cell proliferation, CKS1, insulin, midgut Cyclin-dependent kinase regulatory subunit 1 (CKS1) helps regulate the cell cycle to increase cell number. However, the hormonal regulation on CKS1 expression is not well understood. We report that CKS1 is involved in the promotion of cell proliferation with insulin regulation in the lepidopteran insect Helicoverpa armigera. CKS1 is expressed in various tissues during the larval feeding stage. CKS1 knockdown results in larval death, body weight decrease, pupation time delay, and small-sized pupa formation. The underlying mechanism involves the blocking of cell proliferation and the repression of gene expression in the insulin pathway after CKS1 knockdown. CKS1 overexpression in the epidermal cell line results in cell proliferation. The N45 amino acid asparagine in the CKS domain is essential for the function of CKS in cell proliferation. CKS1 is upregulated by insulin via an insulin receptor, but is repressed by a high level of steroid hormone 20-hydroxyecdysone (20E). Results suggest that CKS1 promotes cell proliferation and body growth in coordination with the regulatory actions of insulin and steroid hormone 20E.

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Phospholipase Cγ1 Connects the Cell Membrane Pathway to the Nuclear Receptor Pathway in Insect Steroid Hormone Signaling

Cited by 51 publications

References 52 publications

Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein

Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein

G-protein-coupled receptor controls steroid hormone signaling in cell membrane

Cyclin-dependent kinase regulatory subunit 1 promotes cell proliferation by insulin regulation

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