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Cell Death and Differentiation Mar 2019Autophagy-dependent cell death can be defined as cell demise that has a strict requirement of autophagy. Although autophagy often accompanies cell death following many... (Review)
Review
Autophagy-dependent cell death can be defined as cell demise that has a strict requirement of autophagy. Although autophagy often accompanies cell death following many toxic insults, the requirement of autophagic machinery for cell death execution, as established through specific genetic or chemical inhibition of the process, is highly contextual. During animal development, perhaps the best validated model of autophagy-dependent cell death is the degradation of the larval midgut during larval-pupal metamorphosis, where a number of key autophagy genes are required for the removal of the tissues. Surprisingly though, even in the midgut, not all of the 'canonical' autophagic machinery appears to be required. In other organisms and cancer cells many variations of autophagy-dependent cell death are apparent, pointing to the lack of a unifying cell death pathway. It is thus possible that components of the autophagy machinery are selectively utilised or repurposed for this type of cell death. In this review, we discuss examples of cell death that utilise autophagy machinery (or part thereof), the current knowledge of the complexity of autophagy-dependent cellular demise and the potential mechanisms and regulatory pathways involved in such cell death.
Topics: Animals; Apoptosis; Autophagic Cell Death; Autophagy; Drosophila; Humans; Metamorphosis, Biological; Signal Transduction
PubMed: 30568239
DOI: 10.1038/s41418-018-0252-y -
ELife Jul 2023Analysis of specimens preserved in amber from the Cretaceous period suggests that nematodes changed their host preference towards insects with a complete metamorphosis...
Analysis of specimens preserved in amber from the Cretaceous period suggests that nematodes changed their host preference towards insects with a complete metamorphosis more recently.
Topics: Animals; Fossils; Insecta; Nematoda; Amber; Metamorphosis, Biological
PubMed: 37449733
DOI: 10.7554/eLife.90008 -
Philosophical Transactions of the Royal... Oct 2019Metamorphosis and, in particular, holometaboly, the development of organisms through a series of discrete stages (egg, larva, pupa, adult) that hardly resemble one... (Review)
Review
Metamorphosis and, in particular, holometaboly, the development of organisms through a series of discrete stages (egg, larva, pupa, adult) that hardly resemble one another but are finely adapted to specific roles in the life cycle of the organism, has fascinated and mystified humans throughout history. However, it can be difficult to visualize the dramatic changes that occur during holometaboly without destructive sampling, traditionally through histology. However, advances in imaging technologies developed mainly for medical sciences have been applied to studies of insect metamorphosis over the past couple of decades. These include micro-computed tomography, magnetic resonance imaging and optical coherence tomography. A major advantage of these techniques is that they are rapid and non-destructive, enabling virtual dissection of an organism in any plane by anyone who has access to the image files and the necessary software. They can also be applied in some cases to visualize metamorphosis in vivo, including the periods of most rapid and dramatic morphological change. This review focusses on visualizing the intra-puparial holometabolous metamorphosis of cyclorraphous flies (Diptera), including the primary model organism for all genetic investigations, Drosophila melanogaster, and the blow flies of medical, veterinary and forensic importance, but also discusses similar studies on other insect orders. This article is part of the theme issue 'The evolution of complete metamorphosis'.
Topics: Animals; Diagnostic Imaging; Diptera; Drosophila melanogaster; Insecta; Larva; Metamorphosis, Biological; Pupa
PubMed: 31438819
DOI: 10.1098/rstb.2019.0071 -
Developmental Dynamics : An Official... Jun 2021Amphibians display very diverse life cycles and development can be direct, where it occurs in ovo and a juvenile hatches directly, or biphasic, where an aquatic larva...
Amphibians display very diverse life cycles and development can be direct, where it occurs in ovo and a juvenile hatches directly, or biphasic, where an aquatic larva hatches and later undergoes metamorphosis followed by sexual maturation. In both cases, metamorphosis, corresponds to the post embryonic transition (PETr). A third strategy, only found in Urodeles, is more complex as larvae reach sexual maturity before metamorphosis, which can become accessory. The resulting paedomorphs retain their larval characters and keep their aquatic habitat. Does it mean that paedomorphs do not undergo PETr? Recent work using high throughput technologies coupled to system biology and developmental endocrinology revisited this question and provided novel datasets indicating that a paedomorph's "larval" tissue undergoes a proper developmental transition. Together with historical data, we propose that this transition is a marker of the PETr, which would be distinct from metamorphosis. This implies that (a) complex life cycles would result from the uncoupling of PETr and metamorphosis, and (b) biphasic life cycles would be a special cases where they occur simultaneously.
Topics: Amphibians; Animals; Larva; Life Cycle Stages; Metamorphosis, Biological
PubMed: 33527613
DOI: 10.1002/dvdy.304 -
Philosophical Transactions of the Royal... Oct 2019The majority of described hexapod species are holometabolous insects, undergoing an extreme form of metamorphosis with an intercalated pupal stage between the larva and... (Review)
Review
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'.
Topics: Animals; Biological Evolution; Insecta; Metamorphosis, Biological
PubMed: 31438816
DOI: 10.1098/rstb.2019.0063 -
Cell Death and Differentiation Jan 2020The removal of superfluous and unwanted cells is a critical part of animal development. In insects the steroid hormone ecdysone, the focus of this review, is an... (Review)
Review
The removal of superfluous and unwanted cells is a critical part of animal development. In insects the steroid hormone ecdysone, the focus of this review, is an essential regulator of developmental transitions, including molting and metamorphosis. Like other steroid hormones, ecdysone works via nuclear hormone receptors to direct spatial and temporal regulation of gene transcription including genes required for cell death. During insect metamorphosis, pulses of ecdysone orchestrate the deletion of obsolete larval tissues, including the larval salivary glands and the midgut. In this review we discuss the molecular machinery and mechanisms of ecdysone-dependent cell and tissue removal, with a focus on studies in Drosophila and Lepidopteran insects.
Topics: Animals; Cell Death; Drosophila; Ecdysone; Lepidoptera; Metamorphosis, Biological; Molting
PubMed: 31745213
DOI: 10.1038/s41418-019-0456-9 -
Frontiers in Endocrinology 2020In all vertebrates, the thyroid axis is an endocrine feedback system that affects growth, differentiation, and reproduction, by sensing and translating central and... (Review)
Review
In all vertebrates, the thyroid axis is an endocrine feedback system that affects growth, differentiation, and reproduction, by sensing and translating central and peripheral signals to maintain homeostasis and a proper thyroidal set-point. Fish, the most diverse group of vertebrates, rely on this system for somatic growth, metamorphosis, reproductive events, and the ability to tolerate changing environments. The vast majority of the research on the thyroid axis pertains to mammals, in particular rodents, and although some progress has been made to understand the role of this endocrine axis in non-mammalian vertebrates, including amphibians and teleost fish, major gaps in our knowledge remain regarding other groups, such as elasmobranchs and cyclostomes. In this review, we discuss the roles of the thyroid axis in fish and its contributions to growth and development, metamorphosis, reproduction, osmoregulation, as well as feeding and nutrient metabolism. We also discuss how thyroid hormones have been/can be used in aquaculture, and potential threats to the thyroid system in this regard.
Topics: Animals; Fishes; Metamorphosis, Biological; Reproduction; Thyroid Gland; Thyroid Hormones
PubMed: 33240222
DOI: 10.3389/fendo.2020.596585 -
Cellular and Molecular Life Sciences :... May 2020Metamorphic transformation from larvae to adults along with the high fecundity is key to insect success. Insect metamorphosis and reproduction are governed by two... (Review)
Review
Metamorphic transformation from larvae to adults along with the high fecundity is key to insect success. Insect metamorphosis and reproduction are governed by two critical endocrines, juvenile hormone (JH), and 20-hydroxyecdysone (20E). Recent studies have established a crucial role of microRNA (miRNA) in insect metamorphosis and oogenesis. While miRNAs target genes involved in JH and 20E-signaling pathways, these two hormones reciprocally regulate miRNA expression, forming regulatory loops of miRNA with JH and 20E-signaling cascades. Insect metamorphosis and oogenesis rely on the coordination of hormones, cognate genes, and miRNAs for precise regulation. In addition, the alternative splicing of genes in JH and 20E-signaling pathways has distinct functions in insect metamorphosis and oogenesis. We, therefore, focus in this review on recent advances in post-transcriptional regulation, with the emphasis on the regulatory role of miRNA and alternative splicing, in insect metamorphosis and oogenesis. We will highlight important new findings of miRNA interactions with hormonal signaling and alternative splicing of JH receptor heterodimer gene Taiman.
Topics: Animals; Drosophila melanogaster; Ecdysterone; Gene Expression Regulation, Developmental; Insecta; Juvenile Hormones; Larva; Metamorphosis, Biological; MicroRNAs; Oogenesis; Signal Transduction
PubMed: 31724082
DOI: 10.1007/s00018-019-03361-5 -
Current Biology : CB Dec 2019The evolution of insect metamorphosis is one of the most important sagas in animal history, transforming small, obscure soil arthropods into a dominant terrestrial group... (Review)
Review
The evolution of insect metamorphosis is one of the most important sagas in animal history, transforming small, obscure soil arthropods into a dominant terrestrial group that has profoundly shaped the evolution of terrestrial life. The evolution of flight initiated the trajectory towards metamorphosis, favoring enhanced differences between juvenile and adult stages. The initial step modified postembryonic development, resulting in the nymph-adult differences characteristic of hemimetabolous species. The second step was to complete metamorphosis, holometaboly, and occurred by profoundly altering embryogenesis to produce a larval stage, the nymph becoming the pupa to accommodate the deferred development needed to make the adult. These changing life history patterns were intimately linked to two hormonal systems, the ecdysteroids and the juvenile hormones (JH), which function in both embryonic and postembryonic domains and control the stage-specifying genes Krüppel homolog 1 (Kr-h1), broad and E93. The ecdysteroids induce and direct molting through the ecdysone receptor (EcR), a nuclear hormone receptor with numerous targets including a conserved transcription factor network, the 'Ashburner cascade', which translates features of the ecdysteroid peak into the different phases of the molt. With the evolution of metamorphosis, ecdysteroids acquired a metamorphic function that exploited the repressor capacity of the unliganded EcR, making it a hormone-controlled gateway for the tissue development preceding metamorphosis. JH directs ecdysteroid action, controlling Kr-h1 expression which in turn regulates the other stage-specifying genes. JH appears in basal insect groups as their embryos shift from growth and patterning to differentiation. As a major portion of embryogenesis was deferred to postembryonic life with the evolution of holometaboly, JH also acquired a potent role in regulating postembryonic growth and development. Details of its involvement in broad expression and E93 suppression have been modified as life cycles became more complex and likely underlie some of the changes seen in the shift from incomplete to complete metamorphosis.
Topics: Animals; Biological Evolution; Insecta; Life History Traits; Metamorphosis, Biological
PubMed: 31794762
DOI: 10.1016/j.cub.2019.10.009 -
Cell Death and Differentiation Mar 2020Macroautophagy (autophagy) delivers intracellular constituents to the lysosome to promote catabolism. During development in multiple organisms, autophagy mediates... (Review)
Review
Macroautophagy (autophagy) delivers intracellular constituents to the lysosome to promote catabolism. During development in multiple organisms, autophagy mediates various cellular processes, including survival during starvation, programmed cell death, phagocytosis, organelle elimination, and miRNA regulation. Our current understanding of autophagy has been enhanced by developmental biology research during the last quarter of a century. Through experiments that focus on animal development, fundamental mechanisms that control autophagy and that contribute to disease were elucidated. Studies in embryos revealed specific autophagy molecules that mediate the removal of paternally derived mitochondria, and identified autophagy components that clear protein aggregates during development. Importantly, defects in mtDNA inheritance, or removal of paternal mtDNA via mitochondrial autophagy, can contribute to mitochondrial-associated disease. In addition, impairment of the clearance of protein aggregates by autophagy underlies neurodegenerative diseases. Experiments in multiple organisms also reveal conserved mechanisms of tissue remodeling that rely on the cooperation between autophagy and apoptosis to clear cell corpses, and defects in autophagy and apoptotic cell clearance can contribute to inflammation and autoimmunity. Here we provide an overview of key developmental processes that are mediated by autophagy in multiple animals.
Topics: Animals; Apoptosis; Autophagy; Embryonic Development; Metamorphosis, Biological; MicroRNAs; Regeneration
PubMed: 31988494
DOI: 10.1038/s41418-020-0497-0