Maintenance of Miranda Localization in Drosophila Neuroblasts Involves Interaction with the Cognate mRNA
How cells position their proteins is a key problem in cell biology. Targeting mRNAs to distinct regions of the cytoplasm contributes to protein localization by providing local control over translation. Here, we reveal that an interdependence of a protein and cognate mRNA maintains asymmetric protein...
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Published in | Current biology Vol. 27; no. 14; pp. 2101 - 2111.e5 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
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24.07.2017
Elsevier Cell Press |
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Abstract | How cells position their proteins is a key problem in cell biology. Targeting mRNAs to distinct regions of the cytoplasm contributes to protein localization by providing local control over translation. Here, we reveal that an interdependence of a protein and cognate mRNA maintains asymmetric protein distribution in mitotic Drosophila neural stem cells. We tagged endogenous mRNA or protein products of the gene miranda that is required for fate determination with GFP. We find that the mRNA localizes like the protein it encodes in a basal crescent in mitosis. We then used GFP-specific nanobodies fused to localization domains to alter the subcellular distribution of the GFP-tagged mRNA or protein. Altering the localization of the mRNA resulted in mislocalization of the protein and vice versa. Protein localization defects caused by mislocalization of the cognate mRNA were rescued by introducing untagged mRNA coding for mutant non-localizable protein. Therefore, by combining the MS2 system and subcellular nanobody expression, we uncovered that maintenance of Mira asymmetric localization requires interaction with the cognate mRNA.
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•Nanobody technology and the MS2 system can be used to alter mRNA localization•miranda mRNA localizes in two distinct pools in Drosophila neuroblasts in mitosis•Asymmetric Miranda localization requires an mRNA-dependent maintenance step
Ramat et al. combine the MS2 system and nanobody expression to alter the subcellular localization of mRNA. Shifting basally localized miranda mRNA in Drosophila neuroblasts to the apical pole resulted in Miranda protein localization defects. Miranda protein and cognate mRNA interaction positively feeds back on asymmetric Miranda localization. |
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AbstractList | How cells position their proteins is a key problem in cell biology. Targeting mRNAs to distinct regions of the cytoplasm contributes to protein localization by providing local control over translation. Here, we reveal that an interdependence of a protein and cognate mRNA maintains asymmetric protein distribution in mitotic Drosophila neural stem cells. We tagged endogenous mRNA or protein products of the gene miranda that is required for fate determination with GFP. We find that the mRNA localizes like the protein it encodes in a basal crescent in mitosis. We then used GFP-specific nanobodies fused to localization domains to alter the subcellular distribution of the GFP-tagged mRNA or protein. Altering the localization of the mRNA resulted in mislocalization of the protein and vice versa. Protein localization defects caused by mislocalization of the cognate mRNA were rescued by introducing untagged mRNA coding for mutant non-localizable protein. Therefore, by combining the MS2 system and subcellular nanobody expression, we uncovered that maintenance of Mira asymmetric localization requires interaction with the cognate mRNA.
[Display omitted]
•Nanobody technology and the MS2 system can be used to alter mRNA localization•miranda mRNA localizes in two distinct pools in Drosophila neuroblasts in mitosis•Asymmetric Miranda localization requires an mRNA-dependent maintenance step
Ramat et al. combine the MS2 system and nanobody expression to alter the subcellular localization of mRNA. Shifting basally localized miranda mRNA in Drosophila neuroblasts to the apical pole resulted in Miranda protein localization defects. Miranda protein and cognate mRNA interaction positively feeds back on asymmetric Miranda localization. How cells position their proteins is a key problem in cell biology. Targeting mRNAs to distinct regions of the cytoplasm contributes to protein localization by providing local control over translation. Here, we reveal that an interdependence of a protein and cognate mRNA maintains asymmetric protein distribution in mitotic Drosophila neural stem cells. We tagged endogenous mRNA or protein products of the gene miranda that is required for fate determination with GFP. We find that the mRNA localizes like the protein it encodes in a basal crescent in mitosis. We then used GFP-specific nanobodies fused to localization domains to alter the subcellular distribution of the GFP-tagged mRNA or protein. Altering the localization of the mRNA resulted in mislocalization of the protein and vice versa. Protein localization defects caused by mislocalization of the cognate mRNA were rescued by introducing untagged mRNA coding for mutant non-localizable protein. Therefore, by combining the MS2 system and subcellular nanobody expression, we uncovered that maintenance of Mira asymmetric localization requires interaction with the cognate mRNA. • Nanobody technology and the MS2 system can be used to alter mRNA localization • miranda mRNA localizes in two distinct pools in Drosophila neuroblasts in mitosis • Asymmetric Miranda localization requires an mRNA-dependent maintenance step Ramat et al. combine the MS2 system and nanobody expression to alter the subcellular localization of mRNA. Shifting basally localized miranda mRNA in Drosophila neuroblasts to the apical pole resulted in Miranda protein localization defects. Miranda protein and cognate mRNA interaction positively feeds back on asymmetric Miranda localization. How cells position their proteins is a key problem in cell biology. Targeting mRNAs to distinct regions of the cytoplasm contributes to protein localization by providing local control over translation. Here, we reveal that an interdependence of a protein and cognate mRNA maintains asymmetric protein distribution in mitotic Drosophila neural stem cells. We tagged endogenous mRNA or protein products of the gene miranda that is required for fate determination with GFP. We find that the mRNA localizes like the protein it encodes in a basal crescent in mitosis. We then used GFP-specific nanobodies fused to localization domains to alter the subcellular distribution of the GFP-tagged mRNA or protein. Altering the localization of the mRNA resulted in mislocalization of the protein and vice versa. Protein localization defects caused by mislocalization of the cognate mRNA were rescued by introducing untagged mRNA coding for mutant non-localizable protein. Therefore, by combining the MS2 system and subcellular nanobody expression, we uncovered that maintenance of Mira asymmetric localization requires interaction with the cognate mRNA. |
Author | Ramat, Anne Hannaford, Matthew Januschke, Jens |
AuthorAffiliation | 1 Cell and Developmental Biology, School of Life Sciences, University of Dundee, Dow Street, DD5 1EH Dundee, UK |
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CitedBy_id | crossref_primary_10_1021_acs_biochem_9b00813 crossref_primary_10_1083_jcb_202112097 crossref_primary_10_3389_fgene_2019_00135 crossref_primary_10_1016_j_ceb_2019_07_018 crossref_primary_10_1083_jcb_201807037 crossref_primary_10_7554_eLife_29939 crossref_primary_10_3390_ijms221910267 crossref_primary_10_1016_j_ceb_2019_06_001 crossref_primary_10_1242_dev_167650 crossref_primary_10_1242_dev_170589 crossref_primary_10_1007_s11427_020_1702_x crossref_primary_10_1016_j_jmb_2017_09_013 crossref_primary_10_1074_jbc_REV120_012960 crossref_primary_10_7554_eLife_97902 crossref_primary_10_3390_antib8010016 crossref_primary_10_15252_embj_2018100373 crossref_primary_10_1016_j_devcel_2023_04_006 crossref_primary_10_1016_j_bbagrm_2018_08_004 |
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Keywords | mRNA localization asymmetric cell division nanobody Drosophila neuroblasts polarity |
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Title | Maintenance of Miranda Localization in Drosophila Neuroblasts Involves Interaction with the Cognate mRNA |
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