Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes
Hsp70 participates in a broad spectrum of protein folding processes extending from nascent chain folding to protein disaggregation. This versatility in function is achieved through a diverse family of J-protein cochaperones that select substrates for Hsp70. Substrate selection is further tuned by tr...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-05-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/24560 |
| _version_ | 1818019565375848448 |
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| author | Nadinath B Nillegoda Antonia Stank Duccio Malinverni Niels Alberts Anna Szlachcic Alessandro Barducci Paolo De Los Rios Rebecca C Wade Bernd Bukau |
| author_facet | Nadinath B Nillegoda Antonia Stank Duccio Malinverni Niels Alberts Anna Szlachcic Alessandro Barducci Paolo De Los Rios Rebecca C Wade Bernd Bukau |
| author_sort | Nadinath B Nillegoda |
| collection | DOAJ |
| description | Hsp70 participates in a broad spectrum of protein folding processes extending from nascent chain folding to protein disaggregation. This versatility in function is achieved through a diverse family of J-protein cochaperones that select substrates for Hsp70. Substrate selection is further tuned by transient complexation between different classes of J-proteins, which expands the range of protein aggregates targeted by metazoan Hsp70 for disaggregation. We assessed the prevalence and evolutionary conservation of J-protein complexation and cooperation in disaggregation. We find the emergence of a eukaryote-specific signature for interclass complexation of canonical J-proteins. Consistently, complexes exist in yeast and human cells, but not in bacteria, and correlate with cooperative action in disaggregation in vitro. Signature alterations exclude some J-proteins from networking, which ensures correct J-protein pairing, functional network integrity and J-protein specialization. This fundamental change in J-protein biology during the prokaryote-to-eukaryote transition allows for increased fine-tuning and broadening of Hsp70 function in eukaryotes. |
| first_indexed | 2024-04-14T07:54:00Z |
| format | Article |
| id | doaj.art-a20258da37e549069a38cb1d780a7bdf |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:54:00Z |
| publishDate | 2017-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-a20258da37e549069a38cb1d780a7bdf2022-12-22T02:05:07ZengeLife Sciences Publications LtdeLife2050-084X2017-05-01610.7554/eLife.24560Evolution of an intricate J-protein network driving protein disaggregation in eukaryotesNadinath B Nillegoda0https://orcid.org/0000-0002-9980-3991Antonia Stank1https://orcid.org/0000-0002-3424-4500Duccio Malinverni2https://orcid.org/0000-0002-3946-9709Niels Alberts3https://orcid.org/0000-0001-6963-5475Anna Szlachcic4https://orcid.org/0000-0002-4590-4375Alessandro Barducci5https://orcid.org/0000-0002-1911-8039Paolo De Los Rios6Rebecca C Wade7https://orcid.org/0000-0001-5951-8670Bernd Bukau8https://orcid.org/0000-0003-0521-7199Center for Molecular Biology (ZMBH), Heidelberg University, Heidelberg, Germany; DKFZ-ZMBH Alliance, German Cancer Research Center (DKFZ), Heidelberg, GermanyHeidelberg Institute for Theoretical Studies, Heidelberg, Germany; Heidelberg Graduate School of Mathematical and Computational Methods for the Sciences, University of Heidelberg, Heidelberg, GermanyLaboratory of Statistical Biophysics, School of Basic Sciences, Institute of Physics, École Polytechnique Fédérale de Lausanne, Lausanne, SwitzerlandCenter for Molecular Biology (ZMBH), Heidelberg University, Heidelberg, GermanyCenter for Molecular Biology (ZMBH), Heidelberg University, Heidelberg, GermanyInserm, U1054, Montpellier, France; CNRS, UMR 5048, Centre de Biochimie Structurale, Université de Montpellier, Montpellier, FranceLaboratory of Statistical Biophysics, School of Basic Sciences, Institute of Physics, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, SwitzerlandCenter for Molecular Biology (ZMBH), Heidelberg University, Heidelberg, Germany; Heidelberg Institute for Theoretical Studies, Heidelberg, Germany; Interdisciplinary Center for Scientific Computing, Heidelberg University, Heidelberg, GermanyCenter for Molecular Biology (ZMBH), Heidelberg University, Heidelberg, Germany; DKFZ-ZMBH Alliance, German Cancer Research Center (DKFZ), Heidelberg, GermanyHsp70 participates in a broad spectrum of protein folding processes extending from nascent chain folding to protein disaggregation. This versatility in function is achieved through a diverse family of J-protein cochaperones that select substrates for Hsp70. Substrate selection is further tuned by transient complexation between different classes of J-proteins, which expands the range of protein aggregates targeted by metazoan Hsp70 for disaggregation. We assessed the prevalence and evolutionary conservation of J-protein complexation and cooperation in disaggregation. We find the emergence of a eukaryote-specific signature for interclass complexation of canonical J-proteins. Consistently, complexes exist in yeast and human cells, but not in bacteria, and correlate with cooperative action in disaggregation in vitro. Signature alterations exclude some J-proteins from networking, which ensures correct J-protein pairing, functional network integrity and J-protein specialization. This fundamental change in J-protein biology during the prokaryote-to-eukaryote transition allows for increased fine-tuning and broadening of Hsp70 function in eukaryotes.https://elifesciences.org/articles/24560J-proteinchaperoneprotein disaggregation and refoldingevolutionHsp70Hsp40 |
| spellingShingle | Nadinath B Nillegoda Antonia Stank Duccio Malinverni Niels Alberts Anna Szlachcic Alessandro Barducci Paolo De Los Rios Rebecca C Wade Bernd Bukau Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes eLife J-protein chaperone protein disaggregation and refolding evolution Hsp70 Hsp40 |
| title | Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes |
| title_full | Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes |
| title_fullStr | Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes |
| title_full_unstemmed | Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes |
| title_short | Evolution of an intricate J-protein network driving protein disaggregation in eukaryotes |
| title_sort | evolution of an intricate j protein network driving protein disaggregation in eukaryotes |
| topic | J-protein chaperone protein disaggregation and refolding evolution Hsp70 Hsp40 |
| url | https://elifesciences.org/articles/24560 |
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