Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylation
Abstract Protein acetylation is a highly frequent protein modification. However, comparatively little is known about its enzymatic machinery. N‐α‐acetylation (NTA) and ε‐lysine acetylation (KA) are known to be catalyzed by distinct families of enzymes (NATs and KATs, respectively), although the poss...
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Springer Nature
2020-07-01
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| Series: | Molecular Systems Biology |
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| Online Access: | https://doi.org/10.15252/msb.20209464 |
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| author | Willy V Bienvenut Annika Brünje Jean‐Baptiste Boyer Jens S Mühlenbeck Gautier Bernal Ines Lassowskat Cyril Dian Eric Linster Trinh V Dinh Minna M Koskela Vincent Jung Julian Seidel Laura K Schyrba Aiste Ivanauskaite Jürgen Eirich Rüdiger Hell Dirk Schwarzer Paula Mulo Markus Wirtz Thierry Meinnel Carmela Giglione Iris Finkemeier |
| author_facet | Willy V Bienvenut Annika Brünje Jean‐Baptiste Boyer Jens S Mühlenbeck Gautier Bernal Ines Lassowskat Cyril Dian Eric Linster Trinh V Dinh Minna M Koskela Vincent Jung Julian Seidel Laura K Schyrba Aiste Ivanauskaite Jürgen Eirich Rüdiger Hell Dirk Schwarzer Paula Mulo Markus Wirtz Thierry Meinnel Carmela Giglione Iris Finkemeier |
| author_sort | Willy V Bienvenut |
| collection | DOAJ |
| description | Abstract Protein acetylation is a highly frequent protein modification. However, comparatively little is known about its enzymatic machinery. N‐α‐acetylation (NTA) and ε‐lysine acetylation (KA) are known to be catalyzed by distinct families of enzymes (NATs and KATs, respectively), although the possibility that the same GCN5‐related N‐acetyltransferase (GNAT) can perform both functions has been debated. Here, we discovered a new family of plastid‐localized GNATs, which possess a dual specificity. All characterized GNAT family members display a number of unique features. Quantitative mass spectrometry analyses revealed that these enzymes exhibit both distinct KA and relaxed NTA specificities. Furthermore, inactivation of GNAT2 leads to significant NTA or KA decreases of several plastid proteins, while proteins of other compartments were unaffected. The data indicate that these enzymes have specific protein targets and likely display partly redundant selectivity, increasing the robustness of the acetylation process in vivo. In summary, this study revealed a new layer of complexity in the machinery controlling this prevalent modification and suggests that other eukaryotic GNATs may also possess these previously underappreciated broader enzymatic activities. |
| format | Article |
| id | doaj-art-d26b41bab41445bf8117bc4fba9d0b24 |
| institution | Kabale University |
| issn | 1744-4292 |
| language | English |
| publishDate | 2020-07-01 |
| publisher | Springer Nature |
| record_format | Article |
| series | Molecular Systems Biology |
| spelling | doaj-art-d26b41bab41445bf8117bc4fba9d0b242024-11-17T12:55:08ZengSpringer NatureMolecular Systems Biology1744-42922020-07-0116712310.15252/msb.20209464Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylationWilly V Bienvenut0Annika Brünje1Jean‐Baptiste Boyer2Jens S Mühlenbeck3Gautier Bernal4Ines Lassowskat5Cyril Dian6Eric Linster7Trinh V Dinh8Minna M Koskela9Vincent Jung10Julian Seidel11Laura K Schyrba12Aiste Ivanauskaite13Jürgen Eirich14Rüdiger Hell15Dirk Schwarzer16Paula Mulo17Markus Wirtz18Thierry Meinnel19Carmela Giglione20Iris Finkemeier21CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris‐SaclayPlant Physiology, Institute of Plant Biology and Biotechnology, University of MuensterCEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris‐SaclayPlant Physiology, Institute of Plant Biology and Biotechnology, University of MuensterCEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris‐SaclayPlant Physiology, Institute of Plant Biology and Biotechnology, University of MuensterCEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris‐SaclayCentre for Organismal Studies Heidelberg, University of HeidelbergCentre for Organismal Studies Heidelberg, University of HeidelbergDepartment of Biochemistry, Molecular Plant Biology, University of TurkuCEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris‐SaclayInterfaculty Institute of Biochemistry, University of TübingenPlant Physiology, Institute of Plant Biology and Biotechnology, University of MuensterDepartment of Biochemistry, Molecular Plant Biology, University of TurkuPlant Physiology, Institute of Plant Biology and Biotechnology, University of MuensterCentre for Organismal Studies Heidelberg, University of HeidelbergInterfaculty Institute of Biochemistry, University of TübingenDepartment of Biochemistry, Molecular Plant Biology, University of TurkuCentre for Organismal Studies Heidelberg, University of HeidelbergCEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris‐SaclayCEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris‐SaclayPlant Physiology, Institute of Plant Biology and Biotechnology, University of MuensterAbstract Protein acetylation is a highly frequent protein modification. However, comparatively little is known about its enzymatic machinery. N‐α‐acetylation (NTA) and ε‐lysine acetylation (KA) are known to be catalyzed by distinct families of enzymes (NATs and KATs, respectively), although the possibility that the same GCN5‐related N‐acetyltransferase (GNAT) can perform both functions has been debated. Here, we discovered a new family of plastid‐localized GNATs, which possess a dual specificity. All characterized GNAT family members display a number of unique features. Quantitative mass spectrometry analyses revealed that these enzymes exhibit both distinct KA and relaxed NTA specificities. Furthermore, inactivation of GNAT2 leads to significant NTA or KA decreases of several plastid proteins, while proteins of other compartments were unaffected. The data indicate that these enzymes have specific protein targets and likely display partly redundant selectivity, increasing the robustness of the acetylation process in vivo. In summary, this study revealed a new layer of complexity in the machinery controlling this prevalent modification and suggests that other eukaryotic GNATs may also possess these previously underappreciated broader enzymatic activities.https://doi.org/10.15252/msb.20209464acetylomeacetyltransferaseco‐ and post‐translational modificationsplastidquantitative proteomics |
| spellingShingle | Willy V Bienvenut Annika Brünje Jean‐Baptiste Boyer Jens S Mühlenbeck Gautier Bernal Ines Lassowskat Cyril Dian Eric Linster Trinh V Dinh Minna M Koskela Vincent Jung Julian Seidel Laura K Schyrba Aiste Ivanauskaite Jürgen Eirich Rüdiger Hell Dirk Schwarzer Paula Mulo Markus Wirtz Thierry Meinnel Carmela Giglione Iris Finkemeier Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylation Molecular Systems Biology acetylome acetyltransferase co‐ and post‐translational modifications plastid quantitative proteomics |
| title | Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylation |
| title_full | Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylation |
| title_fullStr | Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylation |
| title_full_unstemmed | Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylation |
| title_short | Dual lysine and N‐terminal acetyltransferases reveal the complexity underpinning protein acetylation |
| title_sort | dual lysine and n terminal acetyltransferases reveal the complexity underpinning protein acetylation |
| topic | acetylome acetyltransferase co‐ and post‐translational modifications plastid quantitative proteomics |
| url | https://doi.org/10.15252/msb.20209464 |
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