Slam protein dictates subcellular localization and translation of its own mRNA
| Autor: | Jörg Großhans, Sreemukta Acharya, Shuling Yan, Stephanie Gröning |
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| Rok vydání: | 2017 |
| Předmět: |
Male
0301 basic medicine Embryology Embryo Nonmammalian Cell Membranes Gene Expression Biochemistry Animals Genetically Modified Computational biology Drosophila Proteins Biology (General) Feedback Physiological Messenger RNA General Neuroscience Intracellular Signaling Peptides and Proteins Gene Expression Regulation Developmental Translation (biology) Genomics Cell biology Nucleic acids Protein Transport Drosophila Female Cellular Structures and Organelles General Agricultural and Biological Sciences Genome complexity Subcellular Fractions Research Article QH301-705.5 Immunoprecipitation Nucleic acid synthesis Biology Green Fluorescent Protein General Biochemistry Genetics and Molecular Biology 03 medical and health sciences Extraction techniques Genetics Animals RNA Messenger Chemical synthesis RNA synthesis General Immunology and Microbiology Embryos Biology and Life Sciences Membrane Proteins Proteins RNA Colocalization Cell Biology Subcellular localization RNA extraction Research and analysis methods Biosynthetic techniques Luminescent Proteins Non-coding RNA sequences 030104 developmental biology Cytoplasm Protein Biosynthesis Protein Translation Cellularization Developmental Biology |
| Zdroj: | PLoS Biology PLoS Biology, Vol 15, Iss 12, p e2003315 (2017) |
| ISSN: | 1545-7885 |
| DOI: | 10.1371/journal.pbio.2003315 |
| Popis: | Many mRNAs specifically localize within the cytoplasm and are present in RNA-protein complexes. It is generally assumed that localization and complex formation of these RNAs are controlled by trans-acting proteins encoded by genes different than the RNAs themselves. Here, we analyze slow as molasses (slam) mRNA that prominently colocalizes with its encoded protein at the basal cortical compartment during cellularization. The functional implications of this striking colocalization have been unknown. Here, we show that slam mRNA translation is spatiotemporally controlled. We found that translation was largely restricted to the onset of cellularization when Slam protein levels at the basal domain sharply increase. slam mRNA was translated locally, at least partially, as not yet translated mRNA transiently accumulated at the basal region. Slam RNA accumulated at the basal domain only if Slam protein was present. Furthermore, a slam RNA with impaired localization but full coding capacity was only weakly translated. We detected a biochemical interaction of slam mRNA and protein as demonstrated by specific co-immunoprecipitation from embryonic lysate. The intimate relationship of slam mRNA and protein may constitute a positive feedback loop that facilitates and controls timely and rapid accumulation of Slam protein at the prospective basal region. Author summary While proteins and their encoding messenger RNAs share the same intracellular space during the translation process, thereafter they are usually spatially and biochemically separated. RNA localization follows a specific subcellular pattern—such as apical or basal—and is thought to have important physiological implications during development, which are generally independent from the protein function. Here, we investigate the potential mutual dependencies between slam mRNA and its encoded protein during cellularization in early Drosophila embryos. slam RNA and protein are known to colocalize and are essential for epithelial compartmentalization and timely invagination of the plasma membrane between adjacent nuclei. We now show that Slam protein is required for RNA localization at the basal domain and that this event is needed for efficient translation. In addition to the functional interactions, we find that slam RNA and protein are both present in a specific molecular complex. Our findings indicate that slam is locally translated and that the interaction between Slam protein and RNA constitutes a self-enhancing mechanism leading to the fast accumulation of Slam protein at the basal domain during the first minutes of cellularization. |
| Databáze: | OpenAIRE |
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