Cell death during complete metamorphosis

Tettamanti, Gianluca; Casartelli, Morena

doi:10.1098/rstb.2019.0065

Cited by 63 publications

(67 citation statements)

References 109 publications

(153 reference statements)

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“…Programmed cell death has two functions: to remodel the cellular content of tissues and organs and to make good use of the materials that were contained in them. Both autophagic and apoptotic cell death turn out to be important in holometabolous transformations, as is here reviewed by Tettamanti & Casartelli [15]. The extent and manner of cell death during metamorphosis differ considerably between different Endopterygota orders, and even different species.…”

Section: How Complete Metamorphosis Is Achievedmentioning

confidence: 84%

Complete metamorphosis of insects

Rolff

Johnston

Reynolds

2019

Phil. Trans. R. Soc. B

124

103

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The majority of described hexapod species are holometabolous insects, undergoing an extreme form of metamorphosis with an intercalated pupal stage between the larva and adult, in which organs and tissues are extensively remodelled and in some cases completely rebuilt. Here, we review how and why this developmental strategy has evolved. While there are many theories explaining the evolution of metamorphosis, many of which fit under the hypothesis of decoupling of life stages, there are few clear adaptive hypotheses on why complete metamorphosis evolved. We propose that the main adaptive benefit of complete metamorphosis is decoupling between growth and differentiation. This facilitates the exploitation of ephemeral resources and enhances the probability of the metamorphic transition escaping developmental size thresholds. The evolution of complete metamorphosis comes at the cost of exposure to predators, parasites and pathogens during pupal life and requires specific adaptations of the immune system at this time. Moreover, metamorphosis poses a challenge for the maintenance of symbionts and the gut microbiota, although it may also offer the benefit of allowing an extensive change in microbiota between the larval and adult stages. The regulation of metamorphosis by two main players, ecdysone and juvenile hormone, and the related signalling cascades are now relatively well understood. The mechanics of metamorphosis have recently been studied in detail because of the advent of micro-CT and research into the role of cell death in remodelling tissues and organs. We support the argument that the adult stage must necessarily have preceded the larval form of the insect. We do not resolve the still contentious question of whether the larva of insects in general originated through the modification of existing preadult forms or through heterochrony as a modified embryonic stage (pronymph), nor whether the holometabolous pupa arose as a modified hemimetabolous final stage larva. This article is part of the theme issue ‘The evolution of complete metamorphosis’.

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Section: How Complete Metamorphosis Is Achievedmentioning

confidence: 84%

Complete metamorphosis of insects

Rolff

Johnston

Reynolds

2019

Phil. Trans. R. Soc. B

124

103

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“…Starvation and 20E are the two major stimuli of autophagy in insects [5,7,35,43]. In B. mori and D. melanogaster, 20E-EcR/USP signaling predominantly upregulates autophagy through the induction of Atg gene expression in addition to antagonizing insulin/insulin-like growth factor (IGF) signaling (IIS) [5,33].…”

Section: E Functions Differently With Starvation In Regulating Bmtip60mentioning

confidence: 99%

Tip60 Phosphorylation at Ser 99 Is Essential for Autophagy Induction in Bombyx mori

Zhao

et al. 2020

IJMS

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Tip60, a key histone acetyltransferase of the MYST family and member of the nuclear multimeric protein complex (NuA4), regulates the activity and stability of proteins involved in the cell cycle, DNA damage responses, autophagy, etc. However, the function and regulatory mechanism of Tip60 homolog in Bombyx mori are not elucidated. In the present study, Bombyx Tip60 (BmTip60) was functionally identified. Developmental profiles showed that the protein levels and nuclear localization of BmTip60 peaked in fat body during the larval–pupal metamorphosis when autophagy was intensive; simultaneously, the BmTip60 protein migrated to form an upper band as detected by Western blot. Interestingly, the upper band of BmTip60 was reduced by λ-phosphatase treatment, indicating that it was a phosphorylated form of BmTip60. Results showed that BmTip60 was promoted by starvation but not 20-hydroxyecdysone treatment. Transcription factor AMP-activated protein kinase (AMPK) affected by starvation was pivotal for BmTip60 protein migration. In addition, one mammalian phosphorylation site was identified in BmTip60 at Ser99, the constitutive-activation mutation of Ser99 to Asp99 but not its inactive mutation to Ala99 significantly upregulated autophagy, showing the critical role of phosphorylation at Ser99 for BmTip60-mediated autophagy. In conclusion, the starvation-AMPK axis promotes BmTip60 in B. mori, which was requisite for autophagy induction. These results reveal a regulatory mechanism of histone acetyltransferase Tip60 homologs by phosphorylation in insects, and sheds light on further related studies of acetylation regulation.

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“…As an important type of programmed cell death, apoptosis has emerged as a critical event that manifests in a large amount of tissue degradation and removes redundant cells in the metamorphosis process during egg-larva-pupa-adult stages transition in lepidopteran insects [26,27]. In Drosophila, the transcriptional expression of RHG family genes was considered to be the premonition of the occurrence of apoptosis [12].…”

Section: Discussionmentioning

confidence: 99%

“…During larva-pupa transition, many organs of insects need to be degenerated and remade, including midgut, fat body, head glands, etc. [26]. The differences in expression levels of Sf-IBM1 among different tissues could forebode the different apoptotic states associated with these tissues.…”

Section: Discussionmentioning

confidence: 99%

Pro-Apoptotic Function Analysis of the Reaper Homologue IBM1 in Spodoptera frugiperda

Shu

Zhang

Veeran

et al. 2020

IJMS

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As an important type of programmed cell death, apoptosis plays a critical role in lepidopteran insects in response to various internal and external stresses. It is controlled by a network of genes such as those encoding the inhibitor of apoptosis proteins. However, there are few studies on apoptosis-related genes in Spodoptera frugiperda. In this study, an orthologue to the Drosophila reaper gene, named Sf-IBM1, was identified from S. frugiperda, and a full-length sequence was obtained by reverse transcription polymerase chain reaction (RT-PCR) and rapid amplification of cDNA ends PCR (RACE-PCR). The expression pattern of Sf-IBM1 was determined in different developmental stages and various tissues. Apoptotic stimuli including azadirachtin, camptothecin, and ultraviolet radiation (UV) induced the expression of Sf-IBM1 at both transcript and protein levels. Overexpression of Sf-IBM1 induced apoptosis in Sf9 cells, and the Sf-IBM1 protein was localized in mitochondria. The apoptosis induced by Sf-IBM1 could be blocked by the caspase universal inhibitor carbobenzoxy-valyl-alanyl-aspartyl-[O-methyl]-fluoromethylketone (Z-VAD-FMK) and Sf-IAP1. Our results provide valuable information that should contribute to a better understanding of the molecular events that lead to apoptosis in lepidopterans.Apoptosis is inhibited by the inhibitor of apoptosis proteins (IAPs), which are endogenous caspase inhibitors and were originally identified in the genomes of lepidopteran baculoviruses [8]. Numerous IAPs have been identified from various insects and have been demonstrated to be the negative regulators of apoptosis [9]. For example, the Drosophila IAP1 (DIAP1) can enhance ubiquitylation and inhibit the activity of Dronc both in vitro and in vivo [10]. Co-expression of Bm-IAP1 in Bombyx mori suppresses apoptosis induced by overexpression of Bm-Dronc in BM-N cells [9]. IAPs contain two functional domains, the baculoviral IAP repeat (BIR) domain and the Really Interesting New Gene (RING) domain. The IBR domain may be involved in direct inhibition of apoptosis, whereas the RING domain may take part in protein-protein interactions. IAPs can bind to both initiator and effector caspases directly and degrade activated caspases through the E3 ubiquitin ligase activity, resulting in inhibition of apoptosis [11].The anti-apoptotic function of IAPs can be neutralized by IAP antagonists. IAP antagonists are the proteins containing the evolutionarily conserved IAP binding motif (IBM), which consists of several amino acids at the N-terminal [12]. In Drosophila, five RHG (Rpr, Hid, Grim) family proteins including Reaper, Hid, Grim, Sickle, and Jafrac2 have been identified, each with an IBM motif in the N-terminus and identified as the IAP antagonists [13]. Similarly, two IAP antagonists, Smac/Diablo and HtrA2/Omi have also been identified in mammals [14]. IAP antagonists compete with caspases by binding to the BIR domains of IAPs with different affinities via IBM directly [15]. Besides, the IAP antagonists can also function as positive regulato...

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Cell death during complete metamorphosis

Cited by 63 publications

References 109 publications

Complete metamorphosis of insects

Complete metamorphosis of insects

Tip60 Phosphorylation at Ser 99 Is Essential for Autophagy Induction in Bombyx mori

Pro-Apoptotic Function Analysis of the Reaper Homologue IBM1 in Spodoptera frugiperda

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