Azadirachtin-induced apoptosis involves lysosomal membrane permeabilization and cathepsin L release in Spodoptera frugiperda Sf9 cells

Wang, Zheng; Cheng, Xiangdong; Meng, Qianqian; Wang, Peidan; Shu, Benshui; Hu, Qiongbo; Hu, Meiying; Zhong, Guohua

doi:10.1016/j.biocel.2015.03.018

Cited by 41 publications

(29 citation statements)

References 51 publications

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“…The effects of azadirachtin on adult mortality may be linked to the cytotoxicity and induction of apoptosis via the impairment of insulin‐signalling pathway known to interact with JH and ecdysteroid hormones inhibited by this insecticide. Azadirachtin‐induced apoptosis causes general disruption in the organs of D. melanogaster and in other species . In particular, detrimental effects on various tissues, such as muscles (suppressed peristalsis), fat body and gut epithelial cells, have been reported .…”

Section: Discussionmentioning

confidence: 99%

“…Azadirachtin-induced apoptosis causes general disruption in the organs of D. melanogaster 56 and in other species. 9,53,57 In particular, detrimental effects on various tissues, such as muscles (suppressed peristalsis), fat body and gut epithelial cells, have been reported. 9,58 A decrease of food intake and biochemical effects (decrease of -amylase, chitinase, proteases and lipases), published recently 59 in D. melanogaster, may also contribute to azadirachtin acute toxicity.…”

Section: Discussionmentioning

confidence: 99%

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Azadirachtin effects on mating success, gametic abnormalities and progeny survival in Drosophila melanogaster (Diptera)

Oulhaci

Denis

Kilani-Morakchi

et al. 2017

Pest Management Science

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BACKGROUND: Azadirachtin is a prominent natural pesticide and represents an alternative to conventional insecticides. It has been successfully used against insect pests. However, its effects on reproduction require further analysis. Here we investigated lethal and sublethal effects of azadirachtin, on treated adults in a model insect, Drosophila melanogaster (Meigen). Dose-mortality relationships as well as several parameters of reproduction (mating, spermatogenesis, oogenesis and fertility) were examined.RESULTS: Neem-Azal, a commercial formulation of azadirachtin, applied topically on newly emerged adults, increased mortality with a positive dose-dependent relationship. The LD 50 (0.63 g) was determined 24 h after treatment using a non-linear regression. Adults surviving this dose had a mating success that was divided by 3 and a progeny production reduced by half when males were treated, and even more when females were treated. When combining probability of survival, of mating and reduced progeny, it appeared that LD 50 induced a 98% reduction in reproductive rates. Reduced progeny was partially explained by the effect of adult treatment on gametes number and abnormalities. The number of cysts and the apical nuclei positions within the cysts decreased by 29.7% and 20%, respectively, in males. In females, the number of oocytes per ovary and the volume of basal oocytes also decreased by 16.1% and 32.4%, respectively. CONCLUSION: Azadirachtin causes significant toxic effects in both sexes and decreases the fecundity and fertility of D. melanogaster. Females are more sensitive to azadirachtin.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Azadirachtin effects on mating success, gametic abnormalities and progeny survival in Drosophila melanogaster (Diptera)

Oulhaci

Denis

Kilani-Morakchi

et al. 2017

Pest Management Science

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“…Previous studies have shown that AZA provoked potent growth-inhibitory effects in Drosophila larvae by dysregulating the insulin/insulin-like growth factor signaling pathway 28 and inducing programmed death, cytoskeletal damage and autophagic vacuoles on Trichoplusia ni BTI-Tn-5B1-4 cells by disrupting lysosomal function 29 . Recently, AZA-induced apoptosis has been shown to involve lysosomal membrane permeabilization and cathepsin L release in S. frugiperda Sf-9 cells 30 . However, given the lack of studies on the autophagy/apoptosis signaling pathway involved in AZA-induced proliferation arrest in cultured insect cells, the mechanism of AZA-induced autophagy remains largely unknown.…”

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confidence: 99%

Induction of Autophagy and Apoptosis via PI3K/AKT/TOR Pathways by Azadirachtin A in Spodoptera litura Cells

Shao

Lai

Zhang

et al. 2016

Sci Rep

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Azadirachtin is one of the most effective botanical insecticides and has been widely used in pest control. Toxicological reports show that azadirachtin can induce apoptosis in various insect cell lines. However, studies of azadirachtin-induced autophagy in cultured insect cells are lacking. This study reports that azadirachtin A significantly inhibits cell proliferation by inducing autophagic and apoptotic cell death in Spodoptera litura cultured cell line (SL-1 cell). Characteristic autophagolysosome and Atg8-PE (phosphatidylethanolamine) accumulation were observed by electron microscopy and western blotting, indicating that azadirachtin triggered autophagy in SL-1 cell. Furthermore, azadirachtin inhibited survival signaling by blocking the activation of PI3K, AKT and the down-stream target of rapamycin. Similar to the positive control of starvation, azadirachtin induced the activation of insulin receptor (InR) via a cellular feedback mechanism. In addition, the autophagy-related 5 (Atg5), a molecular switch of autophagy and apoptosis, was truncated (tAtg5) to trigger cytochrome c release into the cytoplasm under azadirachtin stress, which indicated that azadirachtin induced apoptosis through autophagy. Our findings suggest that azadirachtin primarily induced autophagy in SL-1 cell by dysregulating InR- and PI3K/AKT/TOR pathways, then stimulated apoptosis by activating tAtg5.

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“…Moreover, the identification of the cathepsin family and evidence from previous studied suggested that the lysosomal pathway plays a critical role in the apoptosis of Sf9 cells 29 . In addition, the existence of Traf family members (Traf 3, Traf 4 and Traf 6) and Fas-associated factor 1( Sf-FAF1 ) suggesting that the death receptor pathway could be functional in Sf9 cells.…”

Section: Discussionmentioning

confidence: 95%

“…For example, mitochondrial signalling is activated in apoptosis induced by azadirachtin in Sf9 cells with the evidence of physiological aspects and cytochrome c release 28 . The lysosomal signalling pathway plays a crucial role in apoptosis induced by azadirachtin, and cathepsin L exerts its function as a prop-apoptotic factor by engaging the release of cathepsin L into the cytosol and activating caspase-3 29 . The activation of Ca 2+ -CaM and EcR/Usp signalling pathways were confirmed in S2 cell apoptosis induced by azadirachtin 27 , and PI3K/AKT/TOR pathways were revealed to regulate the transformation of autophagy and apoptosis induced by azadirachtin in SL-1 cells 30 .…”

Section: Introductionmentioning

confidence: 99%

Transcriptome analysis of Spodoptera frugiperda Sf9 cells reveals putative apoptosis-related genes and a preliminary apoptosis mechanism induced by azadirachtin

Shu

Zhang

Veeran

et al. 2017

Sci Rep

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As an important botanical pesticide, azadirachtin demonstrates broad insecticidal activity against many agricultural pests. The results of a previous study indicated the toxicity and apoptosis induction of azadirachtin in Spodoptera frugiperda Sf9 cells. However, the lack of genomic data has hindered a deeper investigation of apoptosis in Sf9 cells at a molecular level. In the present study, the complete transcriptome data for Sf9 cell line was accomplished using Illumina sequencing technology, and 97 putative apoptosis-related genes were identified through BLAST and KEGG orthologue annotations. Fragments of potential candidate apoptosis-related genes were cloned, and the mRNA expression patterns of ten identified genes regulated by azadirachtin were examined using qRT-PCR. Furthermore, Western blot analysis showed that six putative apoptosis-related proteins were upregulated after being treated with azadirachtin while the protein Bcl-2 were downregulated. These data suggested that both intrinsic and extrinsic apoptotic signal pathways comprising the identified potential apoptosis-related genes were potentially active in S. frugiperda. In addition, the preliminary results revealed that caspase-dependent or caspase-independent apoptotic pathways could function in azadirachtin-induced apoptosis in Sf9 cells.

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Azadirachtin-induced apoptosis involves lysosomal membrane permeabilization and cathepsin L release in Spodoptera frugiperda Sf9 cells

Cited by 41 publications

References 51 publications

Azadirachtin effects on mating success, gametic abnormalities and progeny survival in Drosophila melanogaster (Diptera)

Azadirachtin effects on mating success, gametic abnormalities and progeny survival in Drosophila melanogaster (Diptera)

Induction of Autophagy and Apoptosis via PI3K/AKT/TOR Pathways by Azadirachtin A in Spodoptera litura Cells

Transcriptome analysis of Spodoptera frugiperda Sf9 cells reveals putative apoptosis-related genes and a preliminary apoptosis mechanism induced by azadirachtin

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