J-domain proteins: From molecular mechanisms to diseases

doi:10.1016/j.cstres.2023.12.002

. 2024 Feb;29(1):21-33.

doi: 10.1016/j.cstres.2023.12.002. Epub 2023 Dec 23.

J-domain proteins: From molecular mechanisms to diseases

Jaroslaw Marszalek¹, Paolo De Los Rios², Douglas Cyr³, Matthias P Mayer⁴, Vasista Adupa⁵, Claes Andréasson⁶, Gregory L Blatch⁷, Janice E A Braun⁸, Jeffrey L Brodsky⁹, Bernd Bukau⁴, J Paul Chapple¹⁰, Charlotte Conz¹¹, Sébastien Dementin¹², Pierre Genevaux¹³, Olivier Genest¹², Pierre Goloubinoff¹⁴, Jason Gestwicki¹⁵, Colin M Hammond¹⁶, Justin K Hines¹⁷, Koji Ishikawa⁴, Lukasz A Joachimiak¹⁸, Janine Kirstein¹⁹, Krzysztof Liberek¹, Dejana Mokranjac²⁰, Nadinath Nillegoda²¹, Carlos H I Ramos²², Mathieu Rebeaud²³, David Ron²⁴, Sabine Rospert¹¹, Chandan Sahi²⁵, Reut Shalgi²⁶, Bartlomiej Tomiczek¹, Ryo Ushioda²⁷, Elizaveta Ustyantseva²⁸, Yihong Ye²⁹, Maciej Zylicz³⁰, Harm H Kampinga³¹

Affiliations

¹ Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, Abrahama 58, Gdansk 80-307, Poland.
² Institute of Physics, School of Basic Sciences, École Polytechnique Fédérale de Lausanne - EPFL, Lausanne CH 1015, Switzerland; Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne - EPFL, Lausanne CH 1015, Switzerland.
³ Department of Cell Biology and Physiology, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
⁴ Center for Molecular Biology of Heidelberg University (ZMBH), Heidelberg 69120, Germany.
⁵ Zernike Institute for Advanced Materials, University of Groningen, Groningen, The Netherlands.
⁶ Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm S-10691, Sweden.
⁷ Biomedical Research and Drug Discovery Research Group, Faculty of Health Sciences, Higher Colleges of Technology, Sharjah, United Arab Emirates; The Vice Chancellery, The University of Notre Dame Australia, Fremantle, Western Australia, Australia; Biomedical Biotechnology Research Unit, Department of Biochemistry and Microbiology, Rhodes University, Grahamstown, South Africa.
⁸ Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada.
⁹ Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA.
¹⁰ William Harvey Research Institute, Barts and the London School of Medicine, Queen Mary University of London, London EC1M 6BQ, United Kingdom.
¹¹ Institute of Biochemistry and Molecular Biology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
¹² Aix Marseille Univ, CNRS, BIP UMR 7281, IMM, 31 Chemin Joseph Aiguier, Marseille 13402, France.
¹³ Laboratoire de Microbiologie et Génétique Moléculaires (LMGM), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS, Université Toulouse III - Paul Sabatier (UT3), Toulouse, France.
¹⁴ Department of Plant Molecular Biology, Faculty of Biology and Medicine, Lausanne University, Lausanne 1015, Switzerland.
¹⁵ Department of Pharmaceutical Chemistry and the Institute for Neurodegenerative Diseases, University of California San Francisco, San Francisco, CA 94308, USA.
¹⁶ Novo Nordisk Foundation Center for Protein Research (CPR), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark; Department of Molecular & Clinical Cancer Medicine, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, United Kingdom.
¹⁷ Department of Chemistry, Lafayette College, Easton, PA, USA.
¹⁸ Center for Alzheimer's and Neurodegenerative Diseases, UT Southwestern Medical Center, Dallas, TX, USA; Peter O'Donnell Jr Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA.
¹⁹ Leibniz Institute on Aging - Fritz Lipmann Institute and Institute of Biochemistry and Biophysics, Friedrich Schiller University Jena, Jena 07745, Germany.
²⁰ LMU Munich, Biocenter-Cell Biology, Großhadernerstr. 2, Planegg-Martinsried 82152, Germany.
²¹ Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia; Centre for Dementia and Brain Repair at the Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.
²² Institute of Chemistry, University of Campinas-UNICAMP, P.O. Box 6154, 13083-970 Campinas, SP, Brazil.
²³ Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne - EPFL, Lausanne CH 1015, Switzerland.
²⁴ University of Cambridge, Cambridge CB2 0XY, United Kingdom.
²⁵ Department of Biological Sciences, Indian Institute of Science Education and Research, Bhopal, Bhopal, Madhya Pradesh, India; IISER Bhopal, Room Number 117, AB3, Bhopal Bypass Road, Bhopal 462066, Madhya Pradesh, India.
²⁶ Department of Biochemistry, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, Israel.
²⁷ Department of Molecular Biosciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto 603-8555, Japan.
²⁸ Department of Biomedical Sciences, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
²⁹ National Institute of Diabetes, Digestive, and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
³⁰ Foundation for Polish Science, Warsaw 02-611, Poland.
³¹ Department of Biomedical Sciences, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands. Electronic address: h.h.kampinga@umcg.nl.

PMID: 38320449
PMCID: PMC10939069
DOI: 10.1016/j.cstres.2023.12.002

J-domain proteins: From molecular mechanisms to diseases

Jaroslaw Marszalek et al. Cell Stress Chaperones. 2024 Feb.

. 2024 Feb;29(1):21-33.

doi: 10.1016/j.cstres.2023.12.002. Epub 2023 Dec 23.

Authors

Affiliations

¹ Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, Abrahama 58, Gdansk 80-307, Poland.
² Institute of Physics, School of Basic Sciences, École Polytechnique Fédérale de Lausanne - EPFL, Lausanne CH 1015, Switzerland; Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne - EPFL, Lausanne CH 1015, Switzerland.
³ Department of Cell Biology and Physiology, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
⁴ Center for Molecular Biology of Heidelberg University (ZMBH), Heidelberg 69120, Germany.
⁵ Zernike Institute for Advanced Materials, University of Groningen, Groningen, The Netherlands.
⁶ Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm S-10691, Sweden.
⁷ Biomedical Research and Drug Discovery Research Group, Faculty of Health Sciences, Higher Colleges of Technology, Sharjah, United Arab Emirates; The Vice Chancellery, The University of Notre Dame Australia, Fremantle, Western Australia, Australia; Biomedical Biotechnology Research Unit, Department of Biochemistry and Microbiology, Rhodes University, Grahamstown, South Africa.
⁸ Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada.
⁹ Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA.
¹⁰ William Harvey Research Institute, Barts and the London School of Medicine, Queen Mary University of London, London EC1M 6BQ, United Kingdom.
¹¹ Institute of Biochemistry and Molecular Biology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
¹² Aix Marseille Univ, CNRS, BIP UMR 7281, IMM, 31 Chemin Joseph Aiguier, Marseille 13402, France.
¹³ Laboratoire de Microbiologie et Génétique Moléculaires (LMGM), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS, Université Toulouse III - Paul Sabatier (UT3), Toulouse, France.
¹⁴ Department of Plant Molecular Biology, Faculty of Biology and Medicine, Lausanne University, Lausanne 1015, Switzerland.
¹⁵ Department of Pharmaceutical Chemistry and the Institute for Neurodegenerative Diseases, University of California San Francisco, San Francisco, CA 94308, USA.
¹⁶ Novo Nordisk Foundation Center for Protein Research (CPR), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark; Department of Molecular & Clinical Cancer Medicine, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, United Kingdom.
¹⁷ Department of Chemistry, Lafayette College, Easton, PA, USA.
¹⁸ Center for Alzheimer's and Neurodegenerative Diseases, UT Southwestern Medical Center, Dallas, TX, USA; Peter O'Donnell Jr Brain Institute, UT Southwestern Medical Center, Dallas, TX, USA.
¹⁹ Leibniz Institute on Aging - Fritz Lipmann Institute and Institute of Biochemistry and Biophysics, Friedrich Schiller University Jena, Jena 07745, Germany.
²⁰ LMU Munich, Biocenter-Cell Biology, Großhadernerstr. 2, Planegg-Martinsried 82152, Germany.
²¹ Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia; Centre for Dementia and Brain Repair at the Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.
²² Institute of Chemistry, University of Campinas-UNICAMP, P.O. Box 6154, 13083-970 Campinas, SP, Brazil.
²³ Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne - EPFL, Lausanne CH 1015, Switzerland.
²⁴ University of Cambridge, Cambridge CB2 0XY, United Kingdom.
²⁵ Department of Biological Sciences, Indian Institute of Science Education and Research, Bhopal, Bhopal, Madhya Pradesh, India; IISER Bhopal, Room Number 117, AB3, Bhopal Bypass Road, Bhopal 462066, Madhya Pradesh, India.
²⁶ Department of Biochemistry, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, Israel.
²⁷ Department of Molecular Biosciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto 603-8555, Japan.
²⁸ Department of Biomedical Sciences, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
²⁹ National Institute of Diabetes, Digestive, and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
³⁰ Foundation for Polish Science, Warsaw 02-611, Poland.
³¹ Department of Biomedical Sciences, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands. Electronic address: h.h.kampinga@umcg.nl.

PMID: 38320449
PMCID: PMC10939069
DOI: 10.1016/j.cstres.2023.12.002

Abstract

J-domain proteins (JDPs) are the largest family of chaperones in most organisms, but much of how they function within the network of other chaperones and protein quality control machineries is still an enigma. Here, we report on the latest findings related to JDP functions presented at a dedicated JDP workshop in Gdansk, Poland. The report does not include all (details) of what was shared and discussed at the meeting, because some of these original data have not yet been accepted for publication elsewhere or represented still preliminary observations at the time.

Keywords: Evolution; Hsp70 cycle; JDP.

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Conflict of interest statement

Declaration of interests The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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References

1. Zylicz M., Yamamoto T., McKittrick N., Sell S., Georgopoulos C. Purification and properties of the dnaJ replication protein of Escherichia coli. J Biol Chem. 1985;260:7591–7598. https://www.jbc.org/article/S0021-9258(17)39649-7/pdf - PubMed
1. Liberek K., Georgopoulos C., Zylicz M. Role of the Escherichia coli DnaK and DnaJ heat shock proteins in the initiation of bacteriophage lambda DNA replication. Proc Natl Acad Sci USA. 1988;85:6632–6636. doi: 10.1073/pnas.85.18.6632. - DOI - PMC - PubMed
1. Skowyra D., Georgopoulos C., Zylicz M. The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell. 1990;62(1990):939–944. doi: 10.1016/0092-8674(90)90268-j. - DOI - PubMed
1. Liberek K., Marszalek J., Ang D., Georgopoulos C., Zylicz M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA. 1991;88:2874–2878. doi: 10.1073/pnas.88.7.2874. - DOI - PMC - PubMed
1. Malinverni D., Zamuner S., Rebeaud M.E., Barducci A., Nillegoda N.B., De Los Rios P. Data-driven large-scale genomic analysis reveals an intricate phylogenetic and functional landscape in J-domain proteins. Proc Natl Acad Sci USA. 2023;120 doi: 10.1073/pnas.2218217120. - DOI - PMC - PubMed

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[1] Zylicz M., Yamamoto T., McKittrick N., Sell S., Georgopoulos C. Purification and properties of the dnaJ replication protein of Escherichia coli. J Biol Chem. 1985;260:7591–7598. https://www.jbc.org/article/S0021-9258(17)39649-7/pdf - PubMed

[2] Zylicz M., Yamamoto T., McKittrick N., Sell S., Georgopoulos C. Purification and properties of the dnaJ replication protein of Escherichia coli. J Biol Chem. 1985;260:7591–7598. https://www.jbc.org/article/S0021-9258(17)39649-7/pdf - PubMed

[3] Liberek K., Georgopoulos C., Zylicz M. Role of the Escherichia coli DnaK and DnaJ heat shock proteins in the initiation of bacteriophage lambda DNA replication. Proc Natl Acad Sci USA. 1988;85:6632–6636. doi: 10.1073/pnas.85.18.6632. - DOI - PMC - PubMed

[4] Liberek K., Georgopoulos C., Zylicz M. Role of the Escherichia coli DnaK and DnaJ heat shock proteins in the initiation of bacteriophage lambda DNA replication. Proc Natl Acad Sci USA. 1988;85:6632–6636. doi: 10.1073/pnas.85.18.6632. - DOI - PMC - PubMed

[5] Skowyra D., Georgopoulos C., Zylicz M. The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell. 1990;62(1990):939–944. doi: 10.1016/0092-8674(90)90268-j. - DOI - PubMed

[6] Skowyra D., Georgopoulos C., Zylicz M. The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell. 1990;62(1990):939–944. doi: 10.1016/0092-8674(90)90268-j. - DOI - PubMed

[7] Liberek K., Marszalek J., Ang D., Georgopoulos C., Zylicz M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA. 1991;88:2874–2878. doi: 10.1073/pnas.88.7.2874. - DOI - PMC - PubMed

[8] Liberek K., Marszalek J., Ang D., Georgopoulos C., Zylicz M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA. 1991;88:2874–2878. doi: 10.1073/pnas.88.7.2874. - DOI - PMC - PubMed

[9] Malinverni D., Zamuner S., Rebeaud M.E., Barducci A., Nillegoda N.B., De Los Rios P. Data-driven large-scale genomic analysis reveals an intricate phylogenetic and functional landscape in J-domain proteins. Proc Natl Acad Sci USA. 2023;120 doi: 10.1073/pnas.2218217120. - DOI - PMC - PubMed

[10] Malinverni D., Zamuner S., Rebeaud M.E., Barducci A., Nillegoda N.B., De Los Rios P. Data-driven large-scale genomic analysis reveals an intricate phylogenetic and functional landscape in J-domain proteins. Proc Natl Acad Sci USA. 2023;120 doi: 10.1073/pnas.2218217120. - DOI - PMC - PubMed

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J-domain proteins: From molecular mechanisms to diseases

Affiliations

J-domain proteins: From molecular mechanisms to diseases

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