The steroid hormone 20-hydroxyecdysone promotes switching from autophagy to apoptosis by increasing intracellular calcium levels

Li, Yongbo; Li, Xiangru; Yang, Ting; Wang, Jin-Xing; Zhao, Xiao‐Fan

doi:10.1016/j.ibmb.2016.10.004

Cited by 43 publications

(53 citation statements)

References 52 publications

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“…Autophagy was observed before apoptosis in the midgut of B. mori (44,45). In H. armigera, a high concentration of 20E promotes apoptosis, but a low concentration of 20E induces autophagy; autophagy is switched to apoptosis when a high concentration of 20E triggers Ca 2ϩ influx (34). We found that the decreased 20E titer after PDK1 knockdown could not trigger midgut remodeling and pupation.…”

Section: Pdk1 Is Necessary For 20e Synthesis To Regulate Insect Metammentioning

confidence: 73%

“…RFP-LC3 was overexpressed in HaEpi to indicate the autophagosomes to further confirm that overexpression of FoxO induces autophagy. RFP-LC3 is a fluorescent protein that can reveal autophagosomes (34,37,38). The number of autophagosomes increased after overexpression of FoxO-GFP-His; however, the addition of 20E for 72 h decreased the autophagosomes (Fig.…”

Section: Overexpression Of Foxo Induced Autophagy But Not Apoptosismentioning

confidence: 99%

“…PDK1 was knocked down in HaEpi to confirm that it caused autophagy, as observed in the midgut. The autophagy-related protein, microtubule-associated protein 1 light chain 3 (LC3, one isoform of ATG8) (33), was overexpressed as a fusion protein with the cell-penetrating TAT peptide and red fluorescent protein (RFP) (His-TAT-RFP-LC3-His) to detect autophagosomes in HaEpi (34). The TAT peptide helped the fusion protein His-TAT-RFP-LC3-His to enter the cells (35), RFP showed red fluorescence, and LC3 protein indicated the puncta of autophagosomes by its location in the autophagosome membrane (31).…”

Section: Complementation Of 20e Rescued the Effect Of Pdk1 Knockdownmentioning

confidence: 99%

“…Therefore, apoptosis is controlled by 20E in a FoxO-independent manner, which is inconsistent with the finding that FoxO induces apoptosis in humans (51, 52). This may be because 20E is necessary for inducing high cellular Ca 2ϩ levels for apoptosis (53) and the transformation of autophagy to apoptosis in insects (34).…”

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

confidence: 99%

“…FoxO-GFP-His, FoxO-His, GFP-His, or His tag proteins constructed in our laboratory (28) were overexpressed with 4 g of pIEx-4 plasmid (Novagen) and 10 l of QuickShuttle-enhanced transfection reagent (Biodragon Immunotechnologies Co., Ltd., Beijing, China) for 48 h in 1 ml of Grace's medium, according to the manufacturer's instructions and our previous study (34).…”

Section: Overexpression Of Proteins In the Haepi Cellsmentioning

confidence: 99%

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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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Section: Pdk1 Is Necessary For 20e Synthesis To Regulate Insect Metammentioning

confidence: 73%

Section: Overexpression Of Foxo Induced Autophagy But Not Apoptosismentioning

confidence: 99%

Section: Complementation Of 20e Rescued the Effect Of Pdk1 Knockdownmentioning

confidence: 99%

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

confidence: 99%

Section: Overexpression Of Proteins In the Haepi Cellsmentioning

confidence: 99%

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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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Cloning and functional analysis of autophagy‐related gene 7 in Bombyx mori, silkworm

Bian

Mao

et al. 2021

Arch Insect Biochem Physiol

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Silkworm (Bombyx mori) is an important economic insect and an attractive model system. A series of autophagyrelated genes (Atgs) are involved in the autophagic process, and these Atgs have been proved to play important roles in the development. Atg7 stands at the hub of two ubiquitinlike systems involving Atg8 and Atg12 in the autophagic vesicle. In the present study, we cloned and characterized a BmAtg7 gene in Bombyx mori. The open reading frame (ORF) of BmAtg7 was 1908 bp in length, and it encoded a polypeptide of 635 amino acids. BmAtg7 was highly expressed in the posterior silk gland, fatbody, and epidermis.The expression profile of BmAtg7 in the fatbody showed an increasing tendency from day 1 of the 5th instar to the prepupal stage. After chlorantraniliprole (CAP) exposure, the transcriptional level of BmAtg7 was continuously decreased. After depletion of BmAtg7 by RNAi, the expressions of BmAtg7, BmAtg8, and BmEcr were all downregulated, while the expression of BmJHBP2 was upregulated. However, depletion of BmAtg7 did not prevent the metamorphosis of silkworm from larvae to pupae, while the occurrence of such process was delayed. After the 20-hydroxyecdysone (20E) treatment, the expression characteristics of these four genes (BmAtg7, BmAtg8, BmEcr and BmJHBP2) were contrary to the results after depletion of BmAtg7. Our results suggested that although CAP exposure could significantly inhibit the expression of BmAtg7 continuously, the changes of BmAtg7 was not the key factor in CAP-induced metamorphosis defects.

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Methods for Monitoring Autophagy in Silkworm Organs

Montali

Casartelli

Bruno

et al. 2018

Autophagy in Differentiation and Tissue Maintenance

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In holometabolous insects, various larval organs are remodeled by autophagy during metamorphosis. Although moths and butterflies are among the first animal models in which this self-eating process was described, only in recent years autophagy has been analyzed in detail in these insects. In particular, the silkworm Bombyx mori, which represents a well-studied model among Lepidoptera, provides a wide repertoire of cellular and molecular tools useful for studying the occurrence of autophagy and for evaluating its role in postembryonic development. Here, we describe some morphological, biochemical, and molecular methods to monitor autophagy in silkworm organs.

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The steroid hormone 20-hydroxyecdysone promotes switching from autophagy to apoptosis by increasing intracellular calcium levels

Cited by 43 publications

References 52 publications

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

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

Cloning and functional analysis of autophagy‐related gene 7 in Bombyx mori, silkworm

Methods for Monitoring Autophagy in Silkworm Organs

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