Features of the Chaperone Cellular Network Revealed through Systematic Interaction Mapping

doi:10.1016/j.celrep.2017.08.074

. 2017 Sep 12;20(11):2735-2748.

doi: 10.1016/j.celrep.2017.08.074.

Features of the Chaperone Cellular Network Revealed through Systematic Interaction Mapping

Kamran Rizzolo¹, Jennifer Huen¹, Ashwani Kumar², Sadhna Phanse³, James Vlasblom⁴, Yoshito Kakihara¹, Hussein A Zeineddine¹, Zoran Minic⁴, Jamie Snider⁵, Wen Wang⁶, Carles Pons⁷, Thiago V Seraphim⁸, Edgar Erik Boczek⁹, Simon Alberti⁹, Michael Costanzo⁵, Chad L Myers⁶, Igor Stagljar¹⁰, Charles Boone¹¹, Mohan Babu¹², Walid A Houry¹³

Affiliations

¹ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada.
² Department of Computer Science, University of Regina, Regina, SK S4S 0A2, Canada.
³ The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada; Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada.
⁴ Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada.
⁵ The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada.
⁶ Department of Computer Science & Engineering, University of Minnesota-Twin Cities, Minneapolis, MN 55455, USA; Program in Bioinformatics and Computational Biology, University of Minnesota-Twin Cities, Minneapolis, MN 55455, USA.
⁷ Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute for Science and Technology, Barcelona, Catalonia, Spain.
⁸ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada; Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada.
⁹ Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
¹⁰ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada; The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada; Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada.
¹¹ The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada; Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada.
¹² Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada. Electronic address: mohan.babu@uregina.ca.
¹³ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada; Department of Chemistry, University of Toronto, Toronto, ON M5S 3H6, Canada. Electronic address: walid.houry@utoronto.ca.

PMID: 28903051
DOI: 10.1016/j.celrep.2017.08.074

Free article

Features of the Chaperone Cellular Network Revealed through Systematic Interaction Mapping

Kamran Rizzolo et al. Cell Rep. 2017.

Free article

. 2017 Sep 12;20(11):2735-2748.

doi: 10.1016/j.celrep.2017.08.074.

Authors

Affiliations

¹ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada.
² Department of Computer Science, University of Regina, Regina, SK S4S 0A2, Canada.
³ The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada; Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada.
⁴ Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada.
⁵ The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada.
⁶ Department of Computer Science & Engineering, University of Minnesota-Twin Cities, Minneapolis, MN 55455, USA; Program in Bioinformatics and Computational Biology, University of Minnesota-Twin Cities, Minneapolis, MN 55455, USA.
⁷ Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute for Science and Technology, Barcelona, Catalonia, Spain.
⁸ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada; Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada.
⁹ Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
¹⁰ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada; The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada; Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada.
¹¹ The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada; Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada.
¹² Department of Biochemistry, University of Regina, Regina, SK S4S 0A2, Canada. Electronic address: mohan.babu@uregina.ca.
¹³ Department of Biochemistry, University of Toronto, Toronto, ON M5G 1M1, Canada; Department of Chemistry, University of Toronto, Toronto, ON M5S 3H6, Canada. Electronic address: walid.houry@utoronto.ca.

PMID: 28903051
DOI: 10.1016/j.celrep.2017.08.074

Abstract

A comprehensive view of molecular chaperone function in the cell was obtained through a systematic global integrative network approach based on physical (protein-protein) and genetic (gene-gene or epistatic) interaction mapping. This allowed us to decipher interactions involving all core chaperones (67) and cochaperones (15) of Saccharomyces cerevisiae. Our analysis revealed the presence of a large chaperone functional supercomplex, which we named the naturally joined (NAJ) chaperone complex, encompassing Hsp40, Hsp70, Hsp90, AAA+, CCT, and small Hsps. We further found that many chaperones interact with proteins that form foci or condensates under stress conditions. Using an in vitro reconstitution approach, we demonstrate condensate formation for the highly conserved AAA+ ATPases Rvb1 and Rvb2, which are part of the R2TP complex that interacts with Hsp90. This expanded view of the chaperone network in the cell clearly demonstrates the distinction between chaperones having broad versus narrow substrate specificities in protein homeostasis.

Keywords: Hsp90; NAJ chaperone complex; R2TP; Rvb1; Rvb2; chaperone network; genetic interaction profiles; genetic interactions; perinuclear condensate; physical interactions.

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Features of the Chaperone Cellular Network Revealed through Systematic Interaction Mapping

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Features of the Chaperone Cellular Network Revealed through Systematic Interaction Mapping

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