Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogaster
Abstract The nascent polypeptide-associated complex (NAC) consisting of α- and β-subunits is an essential ribosome-associated protein conserved in eukaryotes. NAC is a ubiquitously expressed co-translational regulator of nascent protein folding and sorting providing for homeostasis of cellular prote...
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Nature Portfolio
2022-07-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-15233-3 |
| _version_ | 1811328732142501888 |
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| author | Galina L. Kogan Elena A. Mikhaleva Oxana M. Olenkina Sergei S. Ryazansky Oxana V. Galzitskaya Yuri A. Abramov Toomas A. Leinsoo Natalia V. Akulenko Sergey A. Lavrov Vladimir A. Gvozdev |
| author_facet | Galina L. Kogan Elena A. Mikhaleva Oxana M. Olenkina Sergei S. Ryazansky Oxana V. Galzitskaya Yuri A. Abramov Toomas A. Leinsoo Natalia V. Akulenko Sergey A. Lavrov Vladimir A. Gvozdev |
| author_sort | Galina L. Kogan |
| collection | DOAJ |
| description | Abstract The nascent polypeptide-associated complex (NAC) consisting of α- and β-subunits is an essential ribosome-associated protein conserved in eukaryotes. NAC is a ubiquitously expressed co-translational regulator of nascent protein folding and sorting providing for homeostasis of cellular proteins. Here we report on discovering the germline-specific NACαβ paralogs (gNACs), whose β-subunits, non-distinguishable by ordinary immunodetection, are encoded by five highly homologous gene copies, while the α-subunit is encoded by a single αNAC gene. The gNAC expression is detected in the primordial embryonic and adult gonads via immunostaining. The germline-specific α and β subunits differ from the ubiquitously expressed paralogs by the extended intrinsically disordered regions (IDRs) acquired at the N- and C-termini of the coding regions, predicted to be phosphorylated. The presence of distinct phosphorylated isoforms of gNAC-β subunits is confirmed by comparing of their profiles by 2D-isoeletrofocusing resolution before and after phosphatase treatment of testis ribosomes. We revealed that the predicted S/T sites of phosphorylation in the individual orthologous IDRs of gNAC-β sequences of Drosophila species are positionally conserved despite these disordered regions are drastically different. We propose the IDR-dependent molecular crowding and specific coordination of NAC and other proteostasis regulatory factors at the ribosomes of germinal cells. Our findings imply that there may be a functional crosstalk between the germinal and ubiquitous α- and β-subunits based on assessing their depletion effects on the fly viability and gonad development. |
| first_indexed | 2024-04-13T15:31:09Z |
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| id | doaj.art-9a958626297b4d54bb0e668dcd9a19a0 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-13T15:31:09Z |
| publishDate | 2022-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-9a958626297b4d54bb0e668dcd9a19a02022-12-22T02:41:23ZengNature PortfolioScientific Reports2045-23222022-07-0112111310.1038/s41598-022-15233-3Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogasterGalina L. Kogan0Elena A. Mikhaleva1Oxana M. Olenkina2Sergei S. Ryazansky3Oxana V. Galzitskaya4Yuri A. Abramov5Toomas A. Leinsoo6Natalia V. Akulenko7Sergey A. Lavrov8Vladimir A. Gvozdev9NRC “Kurchatov Institute”-Institute of Molecular GeneticsNRC “Kurchatov Institute”-Institute of Molecular GeneticsNRC “Kurchatov Institute”-Institute of Molecular GeneticsNRC “Kurchatov Institute”-Institute of Molecular GeneticsInstitute of Protein Research, Russian Academy of SciencesNRC “Kurchatov Institute”-Institute of Molecular GeneticsNRC “Kurchatov Institute”-Institute of Molecular GeneticsNRC “Kurchatov Institute”-Institute of Molecular GeneticsNRC “Kurchatov Institute”-Institute of Molecular GeneticsNRC “Kurchatov Institute”-Institute of Molecular GeneticsAbstract The nascent polypeptide-associated complex (NAC) consisting of α- and β-subunits is an essential ribosome-associated protein conserved in eukaryotes. NAC is a ubiquitously expressed co-translational regulator of nascent protein folding and sorting providing for homeostasis of cellular proteins. Here we report on discovering the germline-specific NACαβ paralogs (gNACs), whose β-subunits, non-distinguishable by ordinary immunodetection, are encoded by five highly homologous gene copies, while the α-subunit is encoded by a single αNAC gene. The gNAC expression is detected in the primordial embryonic and adult gonads via immunostaining. The germline-specific α and β subunits differ from the ubiquitously expressed paralogs by the extended intrinsically disordered regions (IDRs) acquired at the N- and C-termini of the coding regions, predicted to be phosphorylated. The presence of distinct phosphorylated isoforms of gNAC-β subunits is confirmed by comparing of their profiles by 2D-isoeletrofocusing resolution before and after phosphatase treatment of testis ribosomes. We revealed that the predicted S/T sites of phosphorylation in the individual orthologous IDRs of gNAC-β sequences of Drosophila species are positionally conserved despite these disordered regions are drastically different. We propose the IDR-dependent molecular crowding and specific coordination of NAC and other proteostasis regulatory factors at the ribosomes of germinal cells. Our findings imply that there may be a functional crosstalk between the germinal and ubiquitous α- and β-subunits based on assessing their depletion effects on the fly viability and gonad development.https://doi.org/10.1038/s41598-022-15233-3 |
| spellingShingle | Galina L. Kogan Elena A. Mikhaleva Oxana M. Olenkina Sergei S. Ryazansky Oxana V. Galzitskaya Yuri A. Abramov Toomas A. Leinsoo Natalia V. Akulenko Sergey A. Lavrov Vladimir A. Gvozdev Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogaster Scientific Reports |
| title | Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogaster |
| title_full | Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogaster |
| title_fullStr | Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogaster |
| title_full_unstemmed | Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogaster |
| title_short | Extended disordered regions of ribosome-associated NAC proteins paralogs belong only to the germline in Drosophila melanogaster |
| title_sort | extended disordered regions of ribosome associated nac proteins paralogs belong only to the germline in drosophila melanogaster |
| url | https://doi.org/10.1038/s41598-022-15233-3 |
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