Timing of autophagy and apoptosis during posterior silk gland degeneration in Bombyx mori

Montali, Aurora; Romanelli, Davide; Cappellozza, Silvia; Grimaldi, Annalisa; Eguileor, Magda Anna De; Tettamanti, Gianluca

doi:10.1016/j.asd.2017.05.003

Cited by 23 publications

(25 citation statements)

References 44 publications

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“…The silk gland degradation is accomplished via PCD processes during the larval-pupal metamorphosis [ 9 , 24 ]. The ubiquitin-proteasome pathway (UPP) plays important role in the PCD of the silk gland [ 24 ].…”

Section: Resultsmentioning

confidence: 99%

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New insight into the mechanism underlying the silk gland biological process by knocking out fibroin heavy chain in the silkworm

et al. 2018

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BackgroundExploring whether and how mutation of silk protein contributes to subsequent re-allocation of nitrogen, and impacts on the timing of silk gland degradation, is important to understand silk gland biology. Rapid development and wide application of genome editing approach in the silkworm provide us an opportunity to address these issues.ResultsUsing CRISPR/Cas9 system, we successfully performed genome editing of Bmfib-H. The loss-of-function mutations caused naked pupa and thin cocoon mutant phenotypes. Compared with the wild type, the posterior silk gland of mutant showed obviously degraded into fragments in advance of programmed cell death of silk gland cells. Comparative transcriptomic analyses of silk gland at the fourth day of the fifth instar larval stage(L5D4)identified 1456 differential expressed genes (DEGs) between posterior silk gland (PSG) and mid silk gland (MSG) and 1388 DEGs between the mutant and the wild type. Hierarchical clustering of all the DEGs indicated a remarkable down-regulated and an up-regulated gene clade in the mutant silk glands, respectively. Down-regulated genes were overrepresented in the pathways involved in cancer, DNA replication and cell proliferation. Intriguingly, up-regulated DEGs are significantly enriched in the proteasome. By further comparison on the transcriptome of MSG and PSG between the wild type and the mutant, we consistently observed that up-regulated DEGs in the mutant PSG were enriched in protein degrading activity and proteasome. Meantime, we observed a series of up-regulated genes involved in autophagy. Since these protein degradation processes would be normally occur after the spinning time, the results suggesting that these progresses were activated remarkably ahead of schedule in the mutant.ConclusionsAccumulation of abnormal fib-H protein might arouse the activation of proteasomes as well as autophagy process, to promote the rapid degradation of such abnormal proteins and the silk gland cells. Our study therefore proposes a subsequent process of protein and partial cellular degradation caused by mutation of silk protein, which might be helpful for understanding its impact of the silk gland biological process, and further exploration the re-allocation of nitrogen in the silkworm.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4602-4) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

“…Once the cocoon is formed, the silk glands degenerate during the larva-pupa transition [ 7 ]. Apoptosis, autophagy and cathepsins play essential roles in this process and autophagy precedes apoptosis [ 8 , 9 ].…”

Section: Introductionmentioning

confidence: 99%

New insight into the mechanism underlying the silk gland biological process by knocking out fibroin heavy chain in the silkworm

et al. 2018

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“…The relationship between autophagy and apoptosis can be mutual antagonism, promotion, or replacement. Previous studies have shown that ecdysone‐induced autophagy precedes apoptosis in the midgut and silk gland, suggesting that the autophagy would lead to apoptosis when autophagy reaches a high level during silkworm metamorphosis (Franzetti et al, ; Montali et al, ). In the current study, we found that Baf‐A1 targeted to the lysosomes and decreased the expression of autophagy‐related genes BmATG5 , BmATG6, and BmATG8 (Figure ).…”

Section: Discussionmentioning

confidence: 99%

“…They experience four distinguished developmental stages. Autophagy and apoptosis happen in each developmental stage coordinated by juvenile hormone and ecdysone, such as the degradation of larval midgut and silk gland (Li et al, ; Montali et al, ). Therefore, the roles of V‐ATPase in tissue degradation and apoptosis in silkworm are of great interests and need more experiments to explore.…”

Section: Discussionmentioning

confidence: 99%

Inhibition of silkworm vacuolar‐type ATPase activity by its inhibitor Bafilomycin A1 induces caspase‐dependent apoptosis in an embryonic cell line of silkworm

Tan

Wang

Liu

et al. 2018

Arch Insect Biochem Physiol

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Vacuolar‐type ATPase (V‐ATPase) is a type of hydrogen ion transporter located in the vesicular membrane‐like system, which mediates active transport and intracellular acidification in various compartments. In mammals, V‐ATPase has been reported to play a key role in cell proliferation and apoptosis. The studies of V‐ATPase in silkworm mainly focus on the acidification regulation of midgut and silk gland and immune resistance. However, there are few reports about the function of silkworm V‐ATPase on cell proliferation, autophagy, and apoptosis. Thus, the function of V‐ATPase in a cell line of Bombyx mori (BmE) was investigated by treating the cell line with bafilomycin A1, a specific inhibitor of V‐ATPase. Cell counting kit 8 (CCK8) and flow cytometry analysis showed that bafilomycin A1 treatment decreased the cell proliferation activity, affected the cell cycle progression and induced cell apoptosis. LysoTracker Red staining showed that the target of bafilomycin A1 is lysosome. The expression of all autophagy‐related genes ( BmATG5, BmATG6, and BmATG8) decreased, indicating that cell autophagy was inhibited. The analysis of the apoptosis pathway demonstrated that inhibiting the activity of V‐ATPase of BmE cells could promote mitochondria to release cytochrome C, inhibit the expression of BmIAP, and activate the caspase cascade to induce apoptosis. All these findings systematically illustrate the effects of V‐ATPase on the proliferation, autophagy, and apoptosis in BmE cells, and provide new ideas and a theoretical basis for further study on the function of V‐ATPase in BmE.

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“…Therefore, the roles of autophagy in development and the clearance of invading pathogens have been extensively investigated [32][33][34][35]. For instance, autophagy occurs during the remodeling and degeneration of various larval tissues [36,37], as well as during changes in larval instars and larva-pupa transition [36,38]. Our observations regarding TmAgt6 expression in different developmental stages and tissues also suggest its importance in the growth and development of T. molitor.…”

Section: Discussionmentioning

confidence: 78%

TmAtg6 Plays an Important Role in Anti-Microbial Defense Against Listeria monocytogenes in the Mealworm, Tenebrio molitor

Edosa

Keshavarz

et al. 2020

IJMS

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Autophagy-related gene-6 (Beclin-1 in mammals) plays a pivotal role in autophagy and is involved in autophagosome formation and autolysosome maturation. In this study, we identified and characterized the autophagy-related gene-6 from Tenebrio molitor (TmAtg6) and analyzed its functional role in the survival of the insect against infection. The expression of TmAtg6 was studied using qRT-PCR for the assessment of the transcript levels at various developmental stages in the different tissues. The results showed that TmAtg6 was highly expressed at the 6-day-old pupal stage. Tissue-specific expression studies revealed that TmAtg6 was highly expressed in the hemocytes of late larvae. The induction patterns of TmAtg6 in different tissues of T. molitor larvae were analyzed by injecting Escherichia coli, Staphylococcus aureus, Listeria monocytogenes, or Candida albicans. The intracellular Gram-positive bacteria, L. monocytogenes, solely induced the expression of TmAtg6 in hemocytes at 9 h-post-injection, whilst in the fat body and gut, bimodal expression times were observed. RNAi-mediated knockdown of the TmAtg6 transcripts, followed by a challenge with microbes, showed a significant reduction in larval survival rate against L. monocytogenes. Taken together, our results suggest that TmAtg6 plays an essential role in anti-microbial defense against intracellular bacteria.

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Timing of autophagy and apoptosis during posterior silk gland degeneration in Bombyx mori

Cited by 23 publications

References 44 publications

New insight into the mechanism underlying the silk gland biological process by knocking out fibroin heavy chain in the silkworm

New insight into the mechanism underlying the silk gland biological process by knocking out fibroin heavy chain in the silkworm

Inhibition of silkworm vacuolar‐type ATPase activity by its inhibitor Bafilomycin A1 induces caspase‐dependent apoptosis in an embryonic cell line of silkworm

TmAtg6 Plays an Important Role in Anti-Microbial Defense Against Listeria monocytogenes in the Mealworm, Tenebrio molitor

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