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Differential Expression of Drosophila Transgelins Throughout Development.

ABSTRACT: Transgelins are a conserved family of actin-binding proteins involved in cytoskeletal remodeling, cell contractility, and cell shape. In both mammals and Drosophila, three genes encode transgelin proteins. Transgelins exhibit a broad and overlapping expression pattern, which has obscured the precise identification of their role in development. Here, we report the first systematic developmental analysis of all Drosophila transgelin proteins, namely, Mp20, CG5023, and Chd64 in the living organism. Drosophila transgelins display overall higher sequence identity with mammalian TAGLN-3 and TAGLN-2 than with TAGLN. Detailed examination in different developmental stages revealed that Mp20 and CG5023 are predominantly expressed in mesodermal tissues with the onset of myogenesis and accumulate in the cytoplasm of all somatic muscles and heart in the late embryo. Notably, at postembryonic developmental stages, Mp20 and CG5023 are detected in the gut's circumferential muscles with distinct subcellular localization: Z-lines for Mp20 and sarcomere and nucleus for CG5023. Only CG5023 is strongly detected in the adult fly in the abdominal, leg, and synchronous thoracic muscles. Chd64 protein is primarily expressed in endodermal and ectodermal tissues and has a dual subcellular localization in the cytoplasm and the nucleus. During the larval-pupae transition, Chd64 is expressed in the brain, eye, legs, halteres, and wings. In contrast, in the adult fly, Chd64 is expressed in epithelia, including the alimentary tract and genitalia. Based on the non-overlapping tissue expression, we predict that Mp20 and CG5023 mostly cooperate to modulate muscle function, whereas Chd64 has distinct roles in epithelial, neuronal, and endodermal tissues.

SUBMITTER: Vakaloglou KM

PROVIDER: S-EPMC8311604 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: This paper lies in the context of modeling the evolution of gene expression away from stationary states, for example in systems subject to external perturbations or during the development of an organism. We base our analysis on experimental data and proceed in a top-down approach, where we start from data on a system's transcriptome, and deduce rules and models from it without a priori knowledge. We focus here on a publicly available DNA microarray time series, representing the transcriptome of Drosophila across evolution from the embryonic to the adult stage. RESULTS: In the first step, genes were clustered on the basis of similarity of their expression profiles, measured by a translation-invariant and scale-invariant distance that proved appropriate for detecting transitions between development stages. Average profiles representing each cluster were computed and their time evolution was analyzed using coupled differential equations. A linear and several non-linear model structures involving a transcription and a degradation term were tested. The parameters were identified in three steps: determination of the strongest connections between genes, optimization of the parameters defining these connections, and elimination of the unnecessary parameters using various reduction schemes. Different solutions were compared on the basis of their abilities to reproduce the data, to keep realistic gene expression levels when extrapolated in time, to show the biologically expected robustness with respect to parameter variations, and to contain as few parameters as possible. CONCLUSIONS: We showed that the linear model did very well in reproducing the data with few parameters, but was not sufficiently robust and yielded unrealistic values upon extrapolation in time. In contrast, the non-linear models all reached the latter two objectives, but some were unable to reproduce the data. A family of non-linear models, constructed from the exponential of linear combinations of expression levels, reached all the objectives. It defined networks with a mean number of connections equal to two, when restricted to the embryonic time series, and equal to five for the full time series. These networks were compared with experimental data about gene-transcription factor and protein-protein interactions. The non-uniqueness of the solutions was discussed in the context of plasticity and cluster versus single-gene networks.

Project description:Alba-domain proteins are RNA-binding proteins found in archaea and eukaryotes and recently studied in protozoan parasites where they play a role in the regulation of virulence factors and stage-specific proteins. This work describes in silico structural characterization, cellular localization and biochemical analyses of Alba-domain proteins in Leishmania infantum. We show that in contrast to other protozoa, Leishmania have two Alba-domain proteins, LiAlba1 and LiAlba3, representative of the Rpp20- and the Rpp25-like eukaryotic subfamilies, respectively, which share several sequence and structural similarities but also important differences with orthologs in other protozoa, especially in sequences targeted for post-translational modifications. LiAlba1 and LiAlba3 proteins form a complex interacting with other RNA-binding proteins, ribosomal subunits, and translation factors as supported by co-immunoprecipitation and sucrose gradient sedimentation analysis. A higher co-sedimentation of Alba proteins with ribosomal subunits was seen upon conditions of decreased translation, suggesting a role of these proteins in translational repression. The Leishmania Alba-domain proteins display differential cellular localization throughout the parasite development. In the insect promastigote stage, Alba proteins co-localize predominantly to the cytoplasm but they translocate to the nucleolus and the flagellum upon amastigote differentiation in the mammalian host and are found back to the cytoplasm once amastigote differentiation is completed. Heat-shock, a major signal of amastigote differentiation, triggers Alba translocation to the nucleolus and the flagellum. Purification of the Leishmania flagellum confirmed LiAlba3 enrichment in this organelle during amastigote differentiation. Moreover, partial characterization of the Leishmania flagellum proteome of promastigotes and differentiating amastigotes revealed the presence of other RNA-binding proteins, as well as differences in the flagellum composition between these two parasite lifestages. Shuttling of Alba-domain proteins between the cytoplasm and the nucleolus or the flagellum throughout the parasite life cycle suggests that these RNA-binding proteins participate in several distinct regulatory pathways controlling developmental gene expression in Leishmania.

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Differential Expression of Drosophila Transgelins Throughout Development.

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