20-hydroxyecdysone activates Forkhead box O to promote proteolysis during <i>Helicoverpa armigera</i> molting

Cai, Mei-Juan; Zhao, Wenli; Jing, Yu-Pu; Song, Qian; Zhang, Xiaoqian; Wang, Jin-Xing; Zhao, Xiao‐Fan

doi:10.1242/dev.128694

Cited by 48 publications

(63 citation statements)

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“…Carboxypeptidases play important roles in many physiological processes, such as digestion, the maturation of neuroendocrine peptide precursors and potential influences upon peptide hormone activity (Gong et al ., ). In H. armigera , HaCPA participates in apolysis of the integument during larval moulting and metamorphosis mediated by 20E via EcRB1 and USP1 up‐regulation of FoxO expression (Sui et al ., ; Cai et al ., ). Our RNA‐seq and RT‐qPCR results showed that CPA and CPM were down‐regulated in the ds LmHR39 ‐injected insects compared with ds GFP ‐injected insects (Fig.…”

Section: Discussionmentioning

confidence: 97%

“…In Helicoverpa armigera , carboxypeptidase A (HaCPA) was characterized as being distributed in the moulting fluid in the moulting stage of fifth‐instar and the prepupal stage of sixth‐instar larvae and participated in the apolysis of the integument during larval moulting and metamorphosis (Sui et al ., ). Furthermore, the 20E signalling pathway regulates the expression of HaCPA for final proteolysis during insect moulting (Sui et al ., ; Cai et al ., ). Insect chitinases are responsible for the degradation of chitin and facilitate shedding of the old cuticle, playing important roles in insect moulting, extension of the wings, digestion and immunity (Hale et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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Nuclear receptor hormone receptor 39 is required for locust moulting by regulating the chitinase and carboxypeptidase genes

Zhao

Qin

Zhang

et al. 2019

Insect Molecular Biology

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The nuclear receptor‐mediated 20‐hydroxyecdysone (20E) signalling pathway plays crucial roles in insects by initiating and regulating moulting and metamorphosis. In the present study, we identified and characterized a cDNA encoding a putative nuclear receptor protein (Locusta migratoria hormone receptor 39, LmHR39) based on L. migratoria transcriptomics data. Reverse‐transcription quantitative PCR (RT‐qPCR) revealed that LmHR39 shows low‐level expression in the early days of fifth‐instar nymphs, and peak expression occurs on day 5, which is followed by a decrease before ecdysis. LmHR39 transcription could be induced by 20E in vivo and was significantly suppressed by knocking down the expression of the L. migratoria ecdysone receptor gene and early‐late gene LmHR3. After RNA interference of LmHR39 with double‐stranded RNA (dsRNA), 85% of the insects showed abnormal morphology, with curly wings after moulting and delayed eclosion time. Haematoxylin and eosin staining indicated that apolysis of the integument and wing pad cuticle in the dsLmHR39‐treated insects was delayed compared to that in the dsRNA for green fluorescent protein‐injected control. Furthermore, RNA‐sequencing and RT‐qPCR analysis showed the expression level of carboxypeptidase genes (Carboxypeptidase A (CPA) and Carboxypeptidase M (CPM)) and chitin degrading genes (LmChitinase5 (LmCHT5) and LmChitinase10 (LmCHT10)) dramatically declined in the dsLmHR39‐treated insects, implying that the LmHR39‐mediated 20E signalling pathway is involved in the regulation of carboxypeptidase genes (CPA and CPM) and chitinase genes (LmCHT5 and LmCHT10), and participated in apolysis of the integument and wing pads during locust moulting.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

Nuclear receptor hormone receptor 39 is required for locust moulting by regulating the chitinase and carboxypeptidase genes

Zhao

Qin

Zhang

et al. 2019

Insect Molecular Biology

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“…Apparently, BmSP95 expression appears to be upregulated in the integument during moulting and metamorphosis, and the pattern is consistent with the fluctuating 20E titre in B. mori (Kiguchi et al, 1985;Kawasaki et al, 1986;Kiuchi, 1992). Insect moulting is triggered by a higher titre of 20E, and the 20E-receptor complex directly or indirectly activates target genes to induce distinct metamorphic processes, such as cell death of obsolete larval tissue, proteolysis of the old cuticle, and pupal cuticle formation (Thummel, 2002;Li & White, 2003;Cai et al, 2016). After treatment with exogenous 20E, expression of the BmSP95 gene was upregulated.…”

Section: Discussionmentioning

confidence: 99%

A clip domain serine protease involved in moulting in the silkworm, Bombyx mori: cloning, characterization, expression patterns and functional analysis

Liu

Wang

Meng

et al. 2017

Insect Molecular Biology

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Clip domain serine proteases (CLIPs), characterized by one or more conserved clip domains, are essential components of extracellular signalling cascades in various biological processes, especially in innate immunity and the embryonic development of insects. Additionally, CLIPs may have additional non-immune functions in insect development. In the present study, the clip domain serine protease gene Bombyx mori serine protease 95 (BmSP95), which encodes a 527-residue protein, was cloned from the integument of B. mori. Bioinformatics analysis indicated that BmSP95 is a typical CLIP of the subfamily D and possesses a clip domain at the N terminus, a trypsin-like serine protease (tryp_spc) domain at the C terminus and a conserved proline-rich motif between these two domains. At the transcriptional level, BmSP95 is expressed in the integument during moulting and metamorphosis, and the expression pattern is consistent with the fluctuating 20-hydroxyecdysone (20E) titre in B. mori. At the translational level, BmSP95 protein is synthesized in the epidermal cells, secreted as a zymogen and activated in the moulting fluid. Immunofluorescence revealed that BmSP95 is distributed into the old endocuticle in the moulting stage. The expression of BmSP95 was upregulated by 20E. Moreover, expression of BmSP95 was downregulated by pathogen infection. RNA interference-mediated silencing of BmSP95 led to delayed moulting from pupa to moth. These results suggest that BmSP95 is involved in integument remodelling during moulting and metamorphosis.

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“…FoxO is phosphorylated by Akt and arrested in the cytoplasm to lose its transcriptional function under insulin regulation (13). The phosphorylation of Akt and FoxO in H. armigera is induced by insulin and repressed by 20E in HaEpi, and the nonphosphorylated FoxO is localized in the nucleus (28). However, little is known about the transcriptional regulation of FoxO, compared with its post-translational modifications (46).…”

Section: Insulin and 20e Cross-talk To Regulate Insect Pupationmentioning

confidence: 99%

“…Human insulin can induce Akt phosphorylation in Helicoverpa armigera, thereby inducing FoxO phosphorylation and cytoplasm localization. In contrast, 20E represses Akt phosphorylation, thereby repressing FoxO phosphorylation and inducing FoxO nuclear localization (28). Because PDK is a key protein kinase in the insulin pathway, we hypothesized that PDK is involved in the cross-talk between insulin and 20E.…”

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confidence: 99%

Insulin and 20-hydroxyecdysone oppose each other in the regulation of phosphoinositide-dependent kinase-1 expression during insect pupation

Pan

et al. 2018

Journal of Biological Chemistry

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Insulin promotes larval growth of insects by stimulating the synthesis of the steroid hormone 20-hydroxyecdysone (20E), which induces pupation and apoptosis. However, the mechanism underlying the coordinate regulation of insect pupation and apoptosis by these two functionally opposing hormones is still unclear. Here, using the lepidopteran insect and serious agricultural pest Helicoverpa armigera (cotton bollworm) as a model, we report that phosphoinositide-dependent kinase-1 (PDK1) and forkhead box O (FoxO) play key roles in these processes. We found that the transcript levels of the PDK1 gene are increased during the larval feeding stages. Moreover, PDK1 expression was increased by insulin, but repressed by 20E. dsRNA-mediated PDK1 knockdown in the H. armigera larvae delayed pupation and resulted in small pupae and also decreased Akt/protein kinase B expression and increased FoxO expression. Furthermore, the PDK1 knockdown blocked midgut remodeling and decreased 20E levels in the larvae. Of note, injecting larvae with 20E overcame the effect of the PDK1 knockdown and restored midgut remodeling. FoxO overexpression in an H. armigera epidermal cell line (HaEpi) did not induce apoptosis, but promoted autophagy and repressed cell proliferation. These results reveal cross-talk between insulin and 20E and that both hormones oppose each other's activities in the regulation of insect pupation and apoptosis by controlling PDK1 expression and, in turn, FoxO expression. We conclude that sufficiently high 20E levels are a key factor for inducing apoptosis during insect pupation.

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20-hydroxyecdysone activates Forkhead box O to promote proteolysis during Helicoverpa armigera molting

Cited by 48 publications

References 50 publications

Nuclear receptor hormone receptor 39 is required for locust moulting by regulating the chitinase and carboxypeptidase genes

Nuclear receptor hormone receptor 39 is required for locust moulting by regulating the chitinase and carboxypeptidase genes

A clip domain serine protease involved in moulting in the silkworm, Bombyx mori: cloning, characterization, expression patterns and functional analysis

Insulin and 20-hydroxyecdysone oppose each other in the regulation of phosphoinositide-dependent kinase-1 expression during insect pupation

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