Dataset Information

Recapitulation of the embryonic transcriptional program in holometabolous insect pupae.

ABSTRACT: Holometabolous insects are predominantly motionless during metamorphosis, when no active feeding is observed and the body is enclosed in a hardened cuticle. These physiological properties as well as undergoing processes resemble embryogenesis, since at the pupal stage organs and systems of the imago are formed. Therefore, recapitulation of the embryonic expression program during metamorphosis could be hypothesized. To assess this hypothesis at the transcriptome level, we have performed a comprehensive analysis of the developmental datasets available in the public domain. Indeed, for most datasets, the pupal gene expression resembles the embryonic rather than the larval pattern, interrupting gradual changes in the transcriptome. Moreover, changes in the transcriptome profile during the pupa-to-imago transition are positively correlated with those at the embryo-to-larvae transition, suggesting that similar expression programs are activated. Gene sets that change their expression level during the larval stage and revert it to the embryonic-like state during the metamorphosis are enriched with genes associated with metabolism and development.

SUBMITTER: Ozerova AM

PROVIDER: S-EPMC9584902 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Recapitulation of the embryonic transcriptional program in holometabolous insect pupae.

Ozerova Alexandra M AM Gelfand Mikhail S MS

Scientific reports 20221020 1

Holometabolous insects are predominantly motionless during metamorphosis, when no active feeding is observed and the body is enclosed in a hardened cuticle. These physiological properties as well as undergoing processes resemble embryogenesis, since at the pupal stage organs and systems of the imago are formed. Therefore, recapitulation of the embryonic expression program during metamorphosis could be hypothesized. To assess this hypothesis at the transcriptome level, we have performed a compreh ...[more]

PMID: 36266393

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Project description:BackgroundThe expression of carcino-embryonic antigen by colorectal cancer is an example of oncogenic activation of embryonic gene expression. Hypothesizing that oncogenesis-recapitulating-ontogenesis may represent a broad programmatic commitment, we compared gene expression patterns of human colorectal cancers (CRCs) and mouse colon tumor models to those of mouse colon development embryonic days 13.5-18.5.ResultsWe report here that 39 colon tumors from four independent mouse models and 100 human CRCs encompassing all clinical stages shared a striking recapitulation of embryonic colon gene expression. Compared to normal adult colon, all mouse and human tumors over-expressed a large cluster of genes highly enriched for functional association to the control of cell cycle progression, proliferation, and migration, including those encoding MYC, AKT2, PLK1 and SPARC. Mouse tumors positive for nuclear beta-catenin shifted the shared embryonic pattern to that of early development. Human and mouse tumors differed from normal embryonic colon by their loss of expression modules enriched for tumor suppressors (EDNRB, HSPE, KIT and LSP1). Human CRC adenocarcinomas lost an additional suppressor module (IGFBP4, MAP4K1, PDGFRA, STAB1 and WNT4). Many human tumor samples also gained expression of a coordinately regulated module associated with advanced malignancy (ABCC1, FOXO3A, LIF, PIK3R1, PRNP, TNC, TIMP3 and VEGF).ConclusionCross-species, developmental, and multi-model gene expression patterning comparisons provide an integrated and versatile framework for definition of transcriptional programs associated with oncogenesis. This approach also provides a general method for identifying pattern-specific biomarkers and therapeutic targets. This delineation and categorization of developmental and non-developmental activator and suppressor gene modules can thus facilitate the formulation of sophisticated hypotheses to evaluate potential synergistic effects of targeting within- and between-modules for next-generation combinatorial therapeutics and improved mouse models.

Project description:It is a long-standing challenge to understand how changes in food resources impact consumer life history traits and, in turn, impact how organisms interact with their environment. To characterize food quality effects on life history, most studies follow organisms throughout their life cycle and quantify major life events, such as age at maturity or fecundity. From these studies, we know that food quality generally impacts body size, juvenile development, and life span. Importantly, throughout juvenile development, many organisms develop through several stages of growth that can have different interactions with their environment. For example, some parasitoids typically attack larger instars, whereas larval insect predators typically attack smaller instars. Interestingly, most studies lump all juvenile stages together, which ignores these ecological changes over juvenile development.We combine a cross-sectional experimental approach with a stage-structured population model to estimate instar-specific vital rates in the bean weevil, Callosobruchus maculatus across a food quality gradient. We characterize food quality effects on the bean weevil's life history traits throughout its juvenile ontogeny to test how food quality impacts instar-specific vital rates.Vital rates differed across food quality treatments within each instar; however, their effect differed with instar. Weevils consuming low-quality food spent 38%, 37%, and 18% more time, and were 34%, 53%, and 63% smaller than weevils consuming high-quality food in the second, third, and fourth instars, respectively. Overall, our results show that consuming poor food quality means slower growth, but that food quality effects on vital rates, growth and development are not equal across instars. Differences in life history traits over juvenile ontogeny in response to food quality may impact how organisms interact with their environment, including how susceptible they are to predation, parasitism, and their competitive ability.

Dataset Information

Recapitulation of the embryonic transcriptional program in holometabolous insect pupae.

Publications

Recapitulation of the embryonic transcriptional program in holometabolous insect pupae.

Similar Datasets

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