The Mechanism and Function of Group II Chaperonins

Lopez, Tom; Dalton, Kevin; Frydman, Judith

doi:10.1016/j.jmb.2015.04.013

The Mechanism and Function of Group II Chaperonins

Journal Article · Thu Apr 30 00:00:00 EDT 2015 · Journal of Molecular Biology

DOI:https://doi.org/10.1016/j.jmb.2015.04.013· OSTI ID:1440550

Lopez, Tom ^[1]; Dalton, Kevin ^[2]; Frydman, Judith ^[3]

Stanford Univ., CA (United States). Department of Biology; Stanford University
Stanford Univ., CA (United States). Biophysics Program
Stanford Univ., CA (United States). Department of Biology and Department of Genetics

We report protein folding in the cell requires the assistance of enzymes collectively called chaperones. Among these, the chaperonins are 1-MDa ring-shaped oligomeric complexes that bind unfolded polypeptides and promote their folding within an isolated chamber in an ATP-dependent manner. Group II chaperonins, found in archaea and eukaryotes, contain a built-in lid that opens and closes over the central chamber. In eukaryotes, the chaperonin TRiC/CCT is hetero-oligomeric, consisting of two stacked rings of eight paralogous subunits each. TRiC facilitates folding of approximately 10% of the eukaryotic proteome, including many cytoskeletal components and cell cycle regulators. Folding of many cellular substrates of TRiC cannot be assisted by any other chaperone. A complete structural and mechanistic understanding of this highly conserved and essential chaperonin remains elusive. However, recent work is beginning to shed light on key aspects of chaperonin function and how their unique properties underlie their contribution to maintaining cellular proteostasis.

View Accepted Manuscript (DOE)

Research Organization:: Stanford Univ., CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0008504

OSTI ID:: 1440550

Alternate ID(s):: OSTI ID: 1246436

Journal Information:: Journal of Molecular Biology, Journal Name: Journal of Molecular Biology Journal Issue: 18 Vol. 427; ISSN 0022-2836

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (109)

Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. Frydman, J.; Nimmesgern, E.; Erdjument-Bromage, H. The EMBO Journal, Vol. 11, Issue 13 https://doi.org/10.1002/j.1460-2075.1992.tb05582.x	journal	December 1992
Three conformations of an archaeal chaperonin, TF55 from Sulfolobus shibatae Schoehn, Guy; Quaite-Randall, Elsie; Jiménez, José L. Journal of Molecular Biology, Vol. 296, Issue 3 https://doi.org/10.1006/jmbi.2000.3505	journal	February 2000
ATPase cycle of an archaeal chaperonin Gutsche, Irina; Mihalache, Oana; Baumeister, Wolfgang Journal of Molecular Biology, Vol. 300, Issue 1 https://doi.org/10.1006/jmbi.2000.3833	journal	June 2000
Crystal structure of the β-apical domain of the thermosome reveals structural plasticity in the protrusion region 1 1Edited by D. Rees Bosch, Gundula; Baumeister, Wolfgang; Essen, Lars-Oliver Journal of Molecular Biology, Vol. 301, Issue 1 https://doi.org/10.1006/jmbi.2000.3955	journal	August 2000
Analysis of the Interaction between the Eukaryotic Chaperonin CCT and Its Substrates Actin and Tubulin Llorca, Oscar; Martín-Benito, Jaime; Gómez-Puertas, Paulino Journal of Structural Biology, Vol. 135, Issue 2 https://doi.org/10.1006/jsbi.2001.4359	journal	August 2001
Flexible interwoven termini determine the thermal stability of thermosomes Zhang, Kai; Wang, Li; Liu, Yanxin Protein & Cell, Vol. 4, Issue 6 https://doi.org/10.1007/s13238-013-3026-9	journal	May 2013
The molecular chaperone TF55: Assesment of symmetry Marco, Sergio; Ureña, Dionisio; Carrascosa, José L. FEBS Letters, Vol. 341, Issue 2-3 https://doi.org/10.1016/0014-5793(94)80447-8	journal	March 1994
Mechanism of GroEL action: Productive release of polypeptide from a sequestered position under groes Weissman, Jonathan S.; Hohl, Corinne M.; Kovalenko, Oleg Cell, Vol. 83, Issue 4 https://doi.org/10.1016/0092-8674(95)90098-5	journal	November 1995
The eighth Cct gene, Cctq, encoding the theta subunit of the cytosolic chaperonin containing TCP-1 Kubota, Hiroshi; Hynes, Gillian; Willison, Keith Gene, Vol. 154, Issue 2 https://doi.org/10.1016/0378-1119(94)00880-2	journal	January 1995
Structure of the Molecular Chaperone Prefoldin Siegert, Ralf; Leroux, Michel R.; Scheufler, Clemens Cell, Vol. 103, Issue 4 https://doi.org/10.1016/S0092-8674(00)00165-3	journal	November 2000
Structure of the Substrate Binding Domain of the Thermosome, an Archaeal Group II Chaperonin Klumpp, Martin; Baumeister, Wolfgang; Essen, Lars-Oliver Cell, Vol. 91, Issue 2 https://doi.org/10.1016/S0092-8674(00)80408-0	journal	October 1997
Crystal Structure of the Thermosome, the Archaeal Chaperonin and Homolog of CCT Ditzel, Lars; Löwe, Jan; Stock, Daniela Cell, Vol. 93, Issue 1 https://doi.org/10.1016/S0092-8674(00)81152-6	journal	April 1998
Closing the Folding Chamber of the Eukaryotic Chaperonin Requires the Transition State of ATP Hydrolysis Meyer, Anne S.; Gillespie, Joel R.; Walther, Dirk Cell, Vol. 113, Issue 3 https://doi.org/10.1016/S0092-8674(03)00307-6	journal	May 2003
Thermodynamics of nucleotide binding to the chaperonin GroEL studied by isothermal titration calorimetry: evidence for noncooperative nucleotide binding Terada, Tomoki P.; Kuwajima, Kunihiro Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1431, Issue 2 https://doi.org/10.1016/S0167-4838(99)00049-7	journal	May 1999
EMBOSS: The European Molecular Biology Open Software Suite Rice, Peter; Longden, Ian; Bleasby, Alan Trends in Genetics, Vol. 16, Issue 6 https://doi.org/10.1016/S0168-9525(00)02024-2	journal	June 2000
Protein folding in vivo: the importance of molecular chaperones Feldman, Douglas E.; Frydman, Judith Current Opinion in Structural Biology, Vol. 10, Issue 1 https://doi.org/10.1016/S0959-440X(99)00044-5	journal	February 2000
Formation of the VHL–Elongin BC Tumor Suppressor Complex Is Mediated by the Chaperonin TRiC Feldman, Douglas E.; Thulasiraman, Vanitha; Ferreyra, Raul G. Molecular Cell, Vol. 4, Issue 6 https://doi.org/10.1016/S1097-2765(00)80233-6	journal	December 1999
Structural and Functional Analysis of the Middle Segment of Hsp90: Implications for ATP Hydrolysis and Client Protein and Cochaperone Interactions Meyer, Philippe; Prodromou, Chrisostomos; Hu, Bin Molecular Cell, Vol. 11, Issue 3 https://doi.org/10.1016/S1097-2765(03)00065-0	journal	March 2003
The CCT Chaperonin Promotes Activation of the Anaphase-Promoting Complex through the Generation of Functional Cdc20 Camasses, Alain; Bogdanova, Aliona; Shevchenko, Andrej Molecular Cell, Vol. 12, Issue 1 https://doi.org/10.1016/S1097-2765(03)00244-2	journal	July 2003
Tumorigenic Mutations in VHL Disrupt Folding In Vivo by Interfering with Chaperonin Binding Feldman, Douglas E.; Spiess, Christoph; Howard, Daniel E. Molecular Cell, Vol. 12, Issue 5 https://doi.org/10.1016/S1097-2765(03)00423-4	journal	November 2003
Chaperonins: The hunt for the Group II mechanism Bigotti, Maria Giulia; Clarke, Anthony R. Archives of Biochemistry and Biophysics, Vol. 474, Issue 2 https://doi.org/10.1016/j.abb.2008.03.015	journal	June 2008
Affinity purification reveals the association of WD40 protein constitutive photomorphogenic 1 with the hetero-oligomeric TCP-1 chaperonin complex in mammalian cells Yi, Chunling; Li, Shuting; Wang, Jian The International Journal of Biochemistry & Cell Biology, Vol. 38, Issue 7 https://doi.org/10.1016/j.biocel.2005.12.019	journal	January 2006
Systems Analyses Reveal Two Chaperone Networks with Distinct Functions in Eukaryotic Cells Albanèse, Véronique; Yam, Alice Yen-Wen; Baughman, Joshua Cell, Vol. 124, Issue 1 https://doi.org/10.1016/j.cell.2005.11.039	journal	January 2006
Dual Action of ATP Hydrolysis Couples Lid Closure to Substrate Release into the Group II Chaperonin Chamber Douglas, Nicholai R.; Reissmann, Stefanie; Zhang, Junjie Cell, Vol. 144, Issue 2 https://doi.org/10.1016/j.cell.2010.12.017	journal	January 2011
The Structural Basis of Substrate Recognition by the Eukaryotic Chaperonin TRiC/CCT Joachimiak, Lukasz A.; Walzthoeni, Thomas; Liu, Corey W. Cell, Vol. 159, Issue 5 https://doi.org/10.1016/j.cell.2014.10.042	journal	November 2014
Proteostatic Control of Telomerase Function through TRiC-Mediated Folding of TCAB1 Freund, Adam; Zhong, Franklin L.; Venteicher, Andrew S. Cell, Vol. 159, Issue 6 https://doi.org/10.1016/j.cell.2014.10.059	journal	December 2014
Function of phosducin-like proteins in G protein signaling and chaperone-assisted protein folding Willardson, Barry M.; Howlett, Alyson C. Cellular Signalling, Vol. 19, Issue 12 https://doi.org/10.1016/j.cellsig.2007.06.013	journal	December 2007
A Gradient of ATP Affinities Generates an Asymmetric Power Stroke Driving the Chaperonin TRIC/CCT Folding Cycle Reissmann, Stefanie; Joachimiak, Lukasz A.; Chen, Bryan Cell Reports, Vol. 2, Issue 4 https://doi.org/10.1016/j.celrep.2012.08.036	journal	October 2012
Genome-Scale RNAi Screen for Host Factors Required for HIV Replication Zhou, Honglin; Xu, Min; Huang, Qian Cell Host & Microbe, Vol. 4, Issue 5 https://doi.org/10.1016/j.chom.2008.10.004	journal	November 2008
The Asymmetric ATPase Cycle of the Thermosome: Elucidation of the Binding, Hydrolysis and Product-release Steps Bigotti, Maria Giulia; Bellamy, Stuart R. W.; Clarke, Anthony R. Journal of Molecular Biology, Vol. 362, Issue 4 https://doi.org/10.1016/j.jmb.2006.07.064	journal	September 2006
Yeast Phosducin-Like Protein 2 Acts as a Stimulatory Co-Factor for the Folding of Actin by the Chaperonin CCT via a Ternary Complex McCormack, Elizabeth A.; Altschuler, Gabriel M.; Dekker, Carien Journal of Molecular Biology, Vol. 391, Issue 1 https://doi.org/10.1016/j.jmb.2009.06.003	journal	August 2009
Chaperonin TRiC Promotes the Assembly of polyQ Expansion Proteins into Nontoxic Oligomers Behrends, Christian; Langer, Carola A.; Boteva, Raina Molecular Cell, Vol. 23, Issue 6 https://doi.org/10.1016/j.molcel.2006.08.017	journal	September 2006
Interaction of p53 with the CCT Complex Promotes Protein Folding and Wild-Type p53 Activity Trinidad, Antonio Garcia; Muller, Patricia A. J.; Cuellar, Jorge Molecular Cell, Vol. 50, Issue 6 https://doi.org/10.1016/j.molcel.2013.05.002	journal	June 2013
Reconstitution of the human chaperonin CCT by co-expression of the eight distinct subunits in mammalian cells Machida, Kodai; Masutani, Mamiko; Kobayashi, Tominari Protein Expression and Purification, Vol. 82, Issue 1 https://doi.org/10.1016/j.pep.2011.11.010	journal	March 2012
A cradle for new proteins: trigger factor at the ribosome Maier, Timm; Ferbitz, Lars; Deuerling, Elke Current Opinion in Structural Biology, Vol. 15, Issue 2 https://doi.org/10.1016/j.sbi.2005.03.005	journal	April 2005
The folding of single domain proteins—have we reached a consensus? Sosnick, Tobin R.; Barrick, Doug Current Opinion in Structural Biology, Vol. 21, Issue 1 https://doi.org/10.1016/j.sbi.2010.11.002	journal	February 2011
Crystal Structure of Group II Chaperonin in the Open State Huo, Yanwu; Hu, Zhongjun; Zhang, Kai Structure, Vol. 18, Issue 10 https://doi.org/10.1016/j.str.2010.07.009	journal	October 2010
Cryo-EM Structure of a Group II Chaperonin in the Prehydrolysis ATP-Bound State Leading to Lid Closure Zhang, Junjie; Ma, Boxue; DiMaio, Frank Structure, Vol. 19, Issue 5 https://doi.org/10.1016/j.str.2011.03.005	journal	May 2011
The Molecular Architecture of the Eukaryotic Chaperonin TRiC/CCT Leitner, Alexander; Joachimiak, Lukasz A.; Bracher, Andreas Structure, Vol. 20, Issue 5 https://doi.org/10.1016/j.str.2012.03.007	journal	May 2012
Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets Spiess, Christoph; Meyer, Anne S.; Reissmann, Stefanie Trends in Cell Biology, Vol. 14, Issue 11 https://doi.org/10.1016/j.tcb.2004.09.015	journal	November 2004
Chaperonins: two rings for folding Yébenes, Hugo; Mesa, Pablo; Muñoz, Inés G. Trends in Biochemical Sciences, Vol. 36, Issue 8 https://doi.org/10.1016/j.tibs.2011.05.003	journal	August 2011
Folding the proteome Braselmann, Esther; Chaney, Julie L.; Clark, Patricia L. Trends in Biochemical Sciences, Vol. 38, Issue 7 https://doi.org/10.1016/j.tibs.2013.05.001	journal	July 2013
Chaperonin TRiC/CCT participates in replication of hepatitis C virus genome via interaction with the viral NS5B protein Inoue, Yasushi; Aizaki, Hideki; Hara, Hiromichi Virology, Vol. 410, Issue 1 https://doi.org/10.1016/j.virol.2010.10.026	journal	February 2011
Conformational Rearrangements of Tail-less Complex Polypeptide 1 (TCP-1) Ring Complex (TRiC)-Bound Actin Villebeck, Laila; Persson, Malin; Luan, Shi-Lu Biochemistry, Vol. 46, Issue 17 https://doi.org/10.1021/bi062093o	journal	April 2007
Domain-Specific Chaperone-Induced Expansion Is Required for β-Actin Folding: A Comparison of β-Actin Conformations upon Interactions with GroEL and Tail-less Complex Polypeptide 1 Ring Complex (TRiC) Villebeck, Laila; Moparthi, Satish Babu; Lindgren, Mikael Biochemistry, Vol. 46, Issue 44 https://doi.org/10.1021/bi700658n	journal	October 2007
OpenMM 4: A Reusable, Extensible, Hardware Independent Library for High Performance Molecular Simulation Eastman, Peter; Friedrichs, Mark S.; Chodera, John D. Journal of Chemical Theory and Computation, Vol. 9, Issue 1 https://doi.org/10.1021/ct300857j	journal	November 2012
TCP1 complex is a molecular chaperone in tubulin biogenesis Yaffe, Michael B.; Farr, George W.; Miklos, David Nature, Vol. 358, Issue 6383 https://doi.org/10.1038/358245a0	journal	July 1992
Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones Frydman, Judith; Nimmesgern, Elmar; Ohtsuka, Kenzo Nature, Vol. 370, Issue 6485 https://doi.org/10.1038/370111a0	journal	July 1994
The crystal structure of the bacterial chaperonln GroEL at 2.8 Å Braig, Kerstin; Otwinowski, Zbyszek; Hegde, Rashmi Nature, Vol. 371, Issue 6498 https://doi.org/10.1038/371578a0	journal	October 1994
Specificity in chaperonin-mediated protein folding Tian, Guoling; Vainberg, Irina E.; Tap, William D. Nature, Vol. 375, Issue 6528 https://doi.org/10.1038/375250a0	journal	May 1995
The crystal structure of the asymmetric GroEL–GroES–(ADP)7 chaperonin complex Xu, Zhaohui; Horwich, Arthur L.; Sigler, Paul B. Nature, Vol. 388, Issue 6644 https://doi.org/10.1038/41944	journal	August 1997
Eukaryotic type II chaperonin CCT interacts with actin through specific subunits Llorca, Oscar; McCormack, Elizabeth A.; Hynes, Gillian Nature, Vol. 402, Issue 6762 https://doi.org/10.1038/45294	journal	December 1999
The crystal structure of yeast CCT reveals intrinsic asymmetry of eukaryotic cytosolic chaperonins Dekker, Carien; Roe, S. Mark; McCormack, Elizabeth A. The EMBO Journal, Vol. 30, Issue 15 https://doi.org/10.1038/emboj.2011.208	journal	June 2011
Symmetry-free cryo-EM structures of the chaperonin TRiC along its ATPase-driven conformational cycle: Symmetry-free Cryo-EM structures of the chaperonin TRiC Cong, Yao; Schröder, Gunnar F.; Meyer, Anne S. The EMBO Journal, Vol. 31, Issue 3 https://doi.org/10.1038/emboj.2011.366	journal	November 2011
Mechanism of nucleotide sensing in group II chaperonins: Nucleotide sensing in group II chaperonins Pereira, Jose H.; Ralston, Corie Y.; Douglas, Nicholai R. The EMBO Journal, Vol. 31, Issue 3 https://doi.org/10.1038/emboj.2011.468	journal	December 2011
Mechanism of folding chamber closure in a group II chaperonin Zhang, Junjie; Baker, Matthew L.; Schröder, Gunnar F. Nature, Vol. 463, Issue 7279 https://doi.org/10.1038/nature08701	journal	January 2010
Global landscape of HIV–human protein complexes Jäger, Stefanie; Cimermancic, Peter; Gulbahce, Natali Nature, Vol. 481, Issue 7381 https://doi.org/10.1038/nature10719	journal	December 2011
The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions Tam, Stephen; Geller, Ron; Spiess, Christoph Nature Cell Biology, Vol. 8, Issue 10 https://doi.org/10.1038/ncb1477	journal	September 2006
Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state Kitamura, Akira; Kubota, Hiroshi; Pack, Chan-Gi Nature Cell Biology, Vol. 8, Issue 10 https://doi.org/10.1038/ncb1478	journal	September 2006
Conformational variability in the refined structure of the chaperonin GroEL at 2.8 Å resolution Braig, Kerstin; Adams, Paul D.; Brünger, Axel T. Nature Structural & Molecular Biology, Vol. 2, Issue 12 https://doi.org/10.1038/nsb1295-1083	journal	December 1995
Mechanism of lid closure in the eukaryotic chaperonin TRiC/CCT Booth, Christopher R.; Meyer, Anne S.; Cong, Yao Nature Structural & Molecular Biology, Vol. 15, Issue 7 https://doi.org/10.1038/nsmb.1436	journal	June 2008
The structure of CCT–Hsc70NBD suggests a mechanism for Hsp70 delivery of substrates to the chaperonin Cuéllar, Jorge; Martín-Benito, Jaime; Scheres, Sjors H. W. Nature Structural & Molecular Biology, Vol. 15, Issue 8 https://doi.org/10.1038/nsmb.1464	journal	July 2008
Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies Yam, Alice Y.; Xia, Yu; Lin, Hen-Tzu Jill Nature Structural & Molecular Biology, Vol. 15, Issue 12 https://doi.org/10.1038/nsmb.1515	journal	November 2008
The chaperonin TRiC blocks a huntingtin sequence element that promotes the conformational switch to aggregation Tam, Stephen; Spiess, Christoph; Auyeung, William Nature Structural & Molecular Biology, Vol. 16, Issue 12 https://doi.org/10.1038/nsmb.1700	journal	November 2009
Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin Muñoz, Inés G.; Yébenes, Hugo; Zhou, Min Nature Structural & Molecular Biology, Vol. 18, Issue 1 https://doi.org/10.1038/nsmb.1971	journal	December 2010
Essential function of the built-in lid in the allosteric regulation of eukaryotic and archaeal chaperonins Reissmann, Stefanie; Parnot, Charles; Booth, Christopher R. Nature Structural & Molecular Biology, Vol. 14, Issue 5 https://doi.org/10.1038/nsmb1236	journal	April 2007
The inter-ring arrangement of the cytosolic chaperonin CCT Martín-Benito, Jaime; Grantham, Julie; Boskovic, Jasminka EMBO reports, Vol. 8, Issue 3 https://doi.org/10.1038/sj.embor.7400894	journal	February 2007
Structure of the complex between the cytosolic chaperonin CCT and phosducin-like protein Martin-Benito, J.; Bertrand, S.; Hu, T. Proceedings of the National Academy of Sciences, Vol. 101, Issue 50 https://doi.org/10.1073/pnas.0405070101	journal	December 2004
Cytosolic chaperonin protects folding intermediates of Gbeta from aggregation by recognizing hydrophobic beta-strands Kubota, S.; Kubota, H.; Nagata, K. Proceedings of the National Academy of Sciences, Vol. 103, Issue 22 https://doi.org/10.1073/pnas.0600195103	journal	May 2006
4.0-A resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement Cong, Y.; Baker, M. L.; Jakana, J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 11 https://doi.org/10.1073/pnas.0913774107	journal	March 2010
Sensing cooperativity in ATP hydrolysis for single multisubunit enzymes in solution Jiang, Y.; Douglas, N. R.; Conley, N. R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 41 https://doi.org/10.1073/pnas.1112244108	journal	September 2011
Subunit order of eukaryotic TRiC/CCT chaperonin by cross-linking, mass spectrometry, and combinatorial homology modeling Kalisman, N.; Adams, C. M.; Levitt, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 8 https://doi.org/10.1073/pnas.1119472109	journal	February 2012
Regulatory interaction of phosducin-like protein with the cytosolic chaperonin complex McLaughlin, J. N.; Thulin, C. D.; Hart, S. J. Proceedings of the National Academy of Sciences, Vol. 99, Issue 12 https://doi.org/10.1073/pnas.112075699	journal	June 2002
Folding of large multidomain proteins by partial encapsulation in the chaperonin TRiC/CCT Russmann, F.; Stemp, M. J.; Monkemeyer, L. Proceedings of the National Academy of Sciences, Vol. 109, Issue 52 https://doi.org/10.1073/pnas.1218836109	journal	November 2012
Structures of the Gβ-CCT and PhLP1–Gβ-CCT complexes reveal a mechanism for G-protein β-subunit folding and Gβγ dimer assembly Plimpton, Rebecca L.; Cuéllar, Jorge; Lai, Chun Wan J. Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1419595112	journal	February 2015
Electrostatics of nanosystems: Application to microtubules and the ribosome Baker, N. A.; Sept, D.; Joseph, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041 https://doi.org/10.1073/pnas.181342398	journal	August 2001
The Kinetics of Formation of Native Ribonuclease During Oxidation of the Reduced Polypeptide Chain Anfinsen, C. B.; Haber, E.; Sela, M. Proceedings of the National Academy of Sciences, Vol. 47, Issue 9 https://doi.org/10.1073/pnas.47.9.1309	journal	September 1961
A yeast TCP-1-like protein is required for actin function in vivo. Vinh, D. B.; Drubin, D. G. Proceedings of the National Academy of Sciences, Vol. 91, Issue 19 https://doi.org/10.1073/pnas.91.19.9116	journal	September 1994
A structural model for GroEL-polypeptide recognition Buckle, A. M.; Zahn, R.; Fersht, A. R. Proceedings of the National Academy of Sciences, Vol. 94, Issue 8 https://doi.org/10.1073/pnas.94.8.3571	journal	April 1997
GroES in the asymmetric GroEL14-GroES7 complex exchanges via an associative mechanism Horowitz, P. M.; Lorimer, G. H.; Ybarra, J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 6 https://doi.org/10.1073/pnas.96.6.2682	journal	March 1999
Crystal Structures of a Group II Chaperonin Reveal the Open and Closed States Associated with the Protein Folding Cycle Pereira, Jose H.; Ralston, Corie Y.; Douglas, Nicholai R. Journal of Biological Chemistry, Vol. 285, Issue 36 https://doi.org/10.1074/jbc.M110.125344	journal	June 2010
Programmed Cell Death Protein 5 Interacts with the Cytosolic Chaperonin Containing Tailless Complex Polypeptide 1 (CCT) to Regulate β-Tubulin Folding Tracy, Christopher M.; Gray, Amy J.; Cuéllar, Jorge Journal of Biological Chemistry, Vol. 289, Issue 7 https://doi.org/10.1074/jbc.M113.542159	journal	February 2014
The Molecular Chaperone TRiC/CCT Binds to the Trp-Asp 40 (WD40) Repeat Protein WDR68 and Promotes Its Folding, Protein Kinase DYRK1A Binding, and Nuclear Accumulation Miyata, Yoshihiko; Shibata, Takeshi; Aoshima, Masato Journal of Biological Chemistry, Vol. 289, Issue 48 https://doi.org/10.1074/jbc.M114.586115	journal	November 2014
Characterization of Archaeal Group II Chaperonin-ADP-Metal Fluoride Complexes Iizuka, Ryo; Yoshida, Takao; Ishii, Noriyuki Journal of Biological Chemistry, Vol. 280, Issue 48 https://doi.org/10.1074/jbc.M506785200	journal	December 2005
PhLP3 Modulates CCT-mediated Actin and Tubulin Folding via Ternary Complexes with Substrates Stirling, Peter C.; Cuéllar, Jorge; Alfaro, Gabriel A. Journal of Biological Chemistry, Vol. 281, Issue 11 https://doi.org/10.1074/jbc.M513235200	journal	March 2006
Elucidation of Steps in the Capture of a Protein Substrate for Efficient Encapsulation by GroE Cliff, Matthew J.; Limpkin, Claire; Cameron, Angus Journal of Biological Chemistry, Vol. 281, Issue 30 https://doi.org/10.1074/jbc.M601605200	journal	July 2006
A eukaryotic cytosolic chaperonin is associated with a high molecular weight intermediate in the assembly of hepatitis B virus capsid, a multimeric particle. Lingappa, J. R.; Martin, R. L.; Wong, M. L. Journal of Cell Biology, Vol. 125, Issue 1 https://doi.org/10.1083/jcb.125.1.99	journal	April 1994
Compartmentation of protein folding invivo: sequestration of non-native polypeptide by the chaperonin-GimC system Siegers, K. The EMBO Journal, Vol. 18, Issue 1 https://doi.org/10.1093/emboj/18.1.75	journal	January 1999
In vivo newly translated polypeptides are sequestered in a protected folding environment Thulasiraman, V. The EMBO Journal, Vol. 18, Issue 1 https://doi.org/10.1093/emboj/18.1.85	journal	January 1999
MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin Leroux, M. R. The EMBO Journal, Vol. 18, Issue 23 https://doi.org/10.1093/emboj/18.23.6730	journal	December 1999
Effects of macromolecular crowding on protein folding and aggregation van den Berg, B. The EMBO Journal, Vol. 18, Issue 24 https://doi.org/10.1093/emboj/18.24.6927	journal	December 1999
Eukaryotic chaperonin CCT stabilizes actin and tubulin folding intermediates in open quasi-native conformations Llorca, O. The EMBO Journal, Vol. 19, Issue 22 https://doi.org/10.1093/emboj/19.22.5971	journal	November 2000
Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT Martin-Benito, J. The EMBO Journal, Vol. 21, Issue 23 https://doi.org/10.1093/emboj/cdf640	journal	December 2002
Hereditary sensory neuropathy is caused by a mutation in the delta subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct4 ) gene Lee, M. -J.; Stephenson, D. A.; Groves, M. J. Human Molecular Genetics, Vol. 12, Issue 15 https://doi.org/10.1093/hmg/ddg198	journal	July 2003
Differential substrate specificity of group I and group II chaperonins in the archaeon Methanosarcina mazei Hirtreiter, Angela M.; Calloni, Giulia; Forner, Francesca Molecular Microbiology, Vol. 74, Issue 5 https://doi.org/10.1111/j.1365-2958.2009.06924.x	journal	December 2009
Chaperonins from an Antarctic archaeon are predominantly monomeric: crystal structure of an open state monomer: Monomeric open state group II chaperonin structure Pilak, Oliver; Harrop, Stephen J.; Siddiqui, Khawar S. Environmental Microbiology, Vol. 13, Issue 8 https://doi.org/10.1111/j.1462-2920.2011.02477.x	journal	April 2011
Multiple chaperonins in bacteria – why so many? Lund, Peter A. FEMS Microbiology Reviews, Vol. 33, Issue 4 https://doi.org/10.1111/j.1574-6976.2009.00178.x	journal	July 2009
Molecular Chaperones in the Cytosol: from Nascent Chain to Folded Protein Hartl, F. U. Science, Vol. 295, Issue 5561 https://doi.org/10.1126/science.1068408	journal	March 2002
Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding Todd, M.; Viitanen, P.; Lorimer, G. Science, Vol. 265, Issue 5172 https://doi.org/10.1126/science.7913555	journal	July 1994
Cellular Chaperonin CCT Contributes to Rabies Virus Replication during Infection Zhang, J.; Wu, X.; Zan, J. Journal of Virology, Vol. 87, Issue 13 https://doi.org/10.1128/JVI.03186-12	journal	May 2013
Type D Retrovirus Gag Polyprotein Interacts with the Cytosolic Chaperonin TRiC Hong, Suntaek; Choi, Gyu; Park, Sunyoung Journal of Virology, Vol. 75, Issue 6 https://doi.org/10.1128/JVI.75.6.2526-2534.2001	journal	March 2001
Mutation in the epsilon subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct5) gene causes autosomal recessive mutilating sensory neuropathy with spastic paraplegia Bouhouche, A. Journal of Medical Genetics, Vol. 43, Issue 5 https://doi.org/10.1136/jmg.2005.039230	journal	September 2005
Molecular Chaperone Functions in Protein Folding and Proteostasis Kim, Yujin E.; Hipp, Mark S.; Bracher, Andreas Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-060208-092442	journal	June 2013
Folding of Newly Translated Proteins In Vivo: The Role of Molecular Chaperones Frydman, Judith Annual Review of Biochemistry, Vol. 70, Issue 1 https://doi.org/10.1146/annurev.biochem.70.1.603	journal	June 2001
The Search for Folding Intermediates and the Mechanism of Protein Folding Baldwin, Robert L. Annual Review of Biophysics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.biophys.37.032807.125948	journal	June 2008
Two Families of Chaperonin: Physiology and Mechanism Horwich, Arthur L.; Fenton, Wayne A.; Chapman, Eli Annual Review of Cell and Developmental Biology, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.cellbio.23.090506.123555	journal	November 2007
Modulation of STAT3 Folding and Function by TRiC/CCT Chaperonin Kasembeli, Moses; Lau, Wilson Chun Yu; Roh, Soung-Hun PLoS Biology, Vol. 12, Issue 4 https://doi.org/10.1371/journal.pbio.1001844	journal	April 2014
ATP Dependent Rotational Motion of Group II Chaperonin Observed by X-ray Single Molecule Tracking Sekiguchi, Hiroshi; Nakagawa, Ayumi; Moriya, Kazuki PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0064176	journal	May 2013
The TRiC/CCT Chaperone Is Implicated in Alzheimer's Disease Based on Patient GWAS and an RNAi Screen in Aβ-Expressing Caenorhabditis elegans Khabirova, Eleonora; Moloney, Aileen; Marciniak, Stefan J. PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0102985	journal	July 2014

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Characterization of group II chaperonins from an acidothermophilic archaeon Picrophilus torridus Yamamoto, Yohei Y.; Tsuchida, Kanako; Noguchi, Keiichi FEBS Open Bio, Vol. 6, Issue 7 https://doi.org/10.1002/2211-5463.12090	journal	June 2016
In Vivo Function of the Chaperonin TRiC in α-Actin Folding during Sarcomere Assembly Berger, Joachim; Berger, Silke; Li, Mei Cell Reports, Vol. 22, Issue 2 https://doi.org/10.1016/j.celrep.2017.12.069	journal	January 2018
An information theoretic framework reveals a tunable allosteric network in group II chaperonins Lopez, Tom; Dalton, Kevin; Tomlinson, Anthony Nature Structural & Molecular Biology, Vol. 24, Issue 9 https://doi.org/10.1038/nsmb.3440	journal	July 2017
The ubiquitin ligase UBR5 suppresses proteostasis collapse in pluripotent stem cells from Huntington’s disease patients Koyuncu, Seda; Saez, Isabel; Lee, Hyun Ju Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05320-3	journal	July 2018
Structural and functional analysis of the role of the chaperonin CCT in mTOR complex assembly Cuéllar, Jorge; Ludlam, W. Grant; Tensmeyer, Nicole C. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10781-1	journal	June 2019
Chaperonin CCT checkpoint function in basal transcription factor TFIID assembly Antonova, Simona V.; Haffke, Matthias; Corradini, Eleonora Nature Structural & Molecular Biology, Vol. 25, Issue 12 https://doi.org/10.1038/s41594-018-0156-z	journal	December 2018
Large-scale aggregation analysis of eukaryotic proteins reveals an involvement of intrinsically disordered regions in protein folding Uemura, Eri; Niwa, Tatsuya; Minami, Shintaro Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-18977-5	journal	January 2018
Insights into the ubiquitin-proteasome system of human embryonic stem cells Saez, Isabel; Koyuncu, Seda; Gutierrez-Garcia, Ricardo Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-22384-9	journal	March 2018
Investigating Chaperonin-Containing TCP-1 subunit 2 as an essential component of the chaperonin complex for tumorigenesis Showalter, Anne E.; Martini, Ana C.; Nierenberg, Daniel Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57602-w	journal	January 2020
Differential conformational modulations of MreB folding upon interactions with GroEL/ES and TRiC chaperonin components Moparthi, Satish Babu; Carlsson, Uno; Vincentelli, Renaud Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28386	journal	June 2016
Functional characterization of chaperonin containing T-complex polypeptide-1 and its conserved and novel substrates in Arabidopsis Ahn, Hee-Kyung; Yoon, Joong-Tak; Choi, Ilyeong Journal of Experimental Botany, Vol. 70, Issue 10 https://doi.org/10.1093/jxb/erz099	journal	March 2019
Hetero-oligomeric CPN60 resembles highly symmetric group I chaperonin structure revealed by Cryo-EM Zhao, Qian; Zhang, Xiang; Sommer, Frederik bioRxiv https://doi.org/10.1101/432013	posted_content	October 2018
REP-X: An Evolution-guided Strategy for the Rational Design of Cysteine-less Protein Variants Dalton, Kevin; Lopez, Tom; Pande, Vijay Scientific Reports https://doi.org/10.1101/797969	journal	October 2019
Replacement of GroEL in Escherichia coli by the Group II Chaperonin from the Archaeon Methanococcus maripaludis Shah, Riddhi; Large, Andrew T.; Ursinus, Astrid Journal of Bacteriology, Vol. 198, Issue 19 https://doi.org/10.1128/jb.00317-16	journal	July 2016
Mutation in the Zebrafish cct2 Gene Leads to Abnormalities of Cell Cycle and Cell Death in the Retina: A Model of CCT2-Related Leber Congenital Amaurosis Minegishi, Yuriko; Nakaya, Naoki; Tomarev, Stanislav I. Investigative Opthalmology & Visual Science, Vol. 59, Issue 2 https://doi.org/10.1167/iovs.17-22919	journal	February 2018
Structural insight into the cooperation of chloroplast chaperonin subunits Zhang, Shijia; Zhou, Huan; Yu, Feng BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0251-8	journal	April 2016
Expression and diagnostic value of CCT3 and IQGAP3 in hepatocellular carcinoma Qian, E-Na; Han, Shuang-Yin; Ding, Song-Ze Cancer Cell International, Vol. 16, Issue 1 https://doi.org/10.1186/s12935-016-0332-3	journal	July 2016
Molecular chaperones: guardians of the proteome in normal and disease states Jeng, Wilson; Lee, Sukyeong; Sung, Nuri F1000Research, Vol. 4 https://doi.org/10.12688/f1000research.7214.1	journal	January 2015
Asymmetry in the function and dynamics of the cytosolic group II chaperonin CCT/TRiC Yamamoto, Yohei Y.; Uno, Yuko; Sha, Eiryo PLOS ONE, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pone.0176054	journal	May 2017
Cellular Proteomes Drive Tissue-Specific Regulation of the Heat Shock Response Ma, Jian; Grant, Christopher E.; Plagens, Rosemary N. G3: Genes\|Genomes\|Genetics, Vol. 7, Issue 3 https://doi.org/10.1534/g3.116.038232	journal	January 2017
Chaperonin containing TCP-1 subunit 3 is critical for gastric cancer growth Li, Li-Juan; Zhang, Lian-Sheng; Han, Zhi-Jian Oncotarget, Vol. 8, Issue 67 https://doi.org/10.18632/oncotarget.22838	journal	December 2017
Engineering and Evolution of Molecular Chaperones and Protein Disaggregases with Enhanced Activity Mack, Korrie L.; Shorter, James Frontiers in Molecular Biosciences, Vol. 3 https://doi.org/10.3389/fmolb.2016.00008	journal	March 2016
Chloroplast Chaperonin: An Intricate Protein Folding Machine for Photosynthesis Zhao, Qian; Liu, Cuimin Frontiers in Molecular Biosciences, Vol. 4 https://doi.org/10.3389/fmolb.2017.00098	journal	January 2018
Single-Ring Intermediates Are Essential for Some Chaperonins Bhatt, Jay M.; Enriquez, Adrian S.; Wang, Jinliang Frontiers in Molecular Biosciences, Vol. 5 https://doi.org/10.3389/fmolb.2018.00042	journal	April 2018
Protein Quality Control by Molecular Chaperones in Neurodegeneration Ciechanover, Aaron; Kwon, Yong Tae Frontiers in Neuroscience, Vol. 11 https://doi.org/10.3389/fnins.2017.00185	journal	April 2017
Contribution of the Type II Chaperonin, TRiC/CCT, to Oncogenesis Roh, Soung-Hun; Kasembeli, Moses; Bakthavatsalam, Deenadayalan International Journal of Molecular Sciences, Vol. 16, Issue 11 https://doi.org/10.3390/ijms161125975	journal	November 2015
On the nature of the optimal form of the holdase‐type chaperone stress response Hall, Damien FEBS Letters, Vol. 594, Issue 1 https://doi.org/10.1002/1873-3468.13580	journal	August 2019
Chaperones in sporadic inclusion body myositis—Validation of proteomic data Güttsches, Anne‐Katrin; Jacobsen, Frank; Schreiner, Anja Muscle & Nerve, Vol. 61, Issue 1 https://doi.org/10.1002/mus.26742	journal	November 2019
Molecular Chaperones: Structure-Function Relationship and their Role in Protein Folding Chatterjee, Bhaskar K.; Puri, Sarita; Sharma, Ashima Regulation of Heat Shock Protein Responses https://doi.org/10.1007/978-3-319-74715-6_8	book	May 2018
Mechanisms of protein homeostasis (proteostasis) maintain stem cell identity in mammalian pluripotent stem cells Noormohammadi, Alireza; Calculli, Giuseppe; Gutierrez-Garcia, Ricardo Cellular and Molecular Life Sciences, Vol. 75, Issue 2 https://doi.org/10.1007/s00018-017-2602-1	journal	July 2017
REP-X: An Evolution-guided Strategy for the Rational Design of Cysteine-less Protein Variants Dalton, Kevin; Lopez, Tom; Pande, Vijay Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58794-x	journal	February 2020
Protein cages and synthetic polymers: a fruitful symbiosis for drug delivery applications, bionanotechnology and materials science Rother, Martin; Nussbaumer, Martin G.; Renggli, Kasper Chemical Society Reviews, Vol. 45, Issue 22 https://doi.org/10.1039/c6cs00177g	journal	January 2016
Heat shock response in archaea Lemmens, Liesbeth; Baes, Rani; Peeters, Eveline Emerging Topics in Life Sciences, Vol. 2, Issue 4 https://doi.org/10.1042/etls20180024	journal	November 2018
Identification of key sites controlling protein functional motions by using elastic network model combined with internal coordinates Zhang, Peng Fei; Su, Ji Guo The Journal of Chemical Physics, Vol. 151, Issue 4 https://doi.org/10.1063/1.5098542	journal	July 2019
The chaperonin TRiC/CCT is essential for the action of bacterial glycosylating protein toxins like Clostridium difficile toxins A and B Steinemann, Marcus; Schlosser, Andreas; Jank, Thomas Proceedings of the National Academy of Sciences, Vol. 115, Issue 38 https://doi.org/10.1073/pnas.1807658115	journal	September 2018
Chaperone-client interactions: Non-specificity engenders multifunctionality Koldewey, Philipp; Horowitz, Scott; Bardwell, James C. A. Journal of Biological Chemistry, Vol. 292, Issue 29 https://doi.org/10.1074/jbc.r117.796862	journal	June 2017
A cytosolic chaperone complex controls folding and degradation of type III CD38 Wu, Yang; Zhang, Jingzi; Fang, Lei Journal of Biological Chemistry, Vol. 294, Issue 11 https://doi.org/10.1074/jbc.ra118.005844	journal	January 2019
Vacuolar ATPase as a possible therapeutic target in human acute myeloid leukemia Aasebø, Elise; Bartaula-Brevik, Sushma; Hernandez-Valladares, Maria Expert Review of Hematology, Vol. 11, Issue 1 https://doi.org/10.1080/17474086.2018.1407239	journal	November 2017
Pathways of cellular proteostasis in aging and disease Klaips, Courtney L.; Jayaraj, Gopal Gunanathan; Hartl, F. Ulrich The Journal of Cell Biology, Vol. 217, Issue 1 https://doi.org/10.1083/jcb.201709072	journal	November 2017
A systematic atlas of chaperome deregulation topologies across the human cancer landscape Esfahani, Ali Hadizadeh; Sverchkova, Angelina; Saez-Rodriguez, Julio PLOS Computational Biology https://doi.org/10.1101/122044	journal	May 2017
Structural analysis of Sulfolobus solfataricus TF55β chaperonin in open and filamentous states Zeng, Yi Cheng; Sobti, Meghna; Stewart, Alastair G. bioRxiv https://doi.org/10.1101/2020.01.13.905216	posted_content	February 2021
E2F coregulates an essential HSF developmental program that is distinct from the heat-shock response Li, Jian; Chauve, Laetitia; Phelps, Grace Genes & Development, Vol. 30, Issue 18 https://doi.org/10.1101/gad.283317.116	journal	September 2016
The proteostasis network provides targets for neurodegeneration Newton, Timothy Mark; Duce, James Alex; Bayle, Elliott David British Journal of Pharmacology, Vol. 176, Issue 18 https://doi.org/10.1111/bph.14643	journal	May 2019
T-complex protein 1-ring complex enhances retrograde axonal transport by modulating tau phosphorylation Chen, Xu-Qiao; Fang, Fang; Florio, Jazmin B. Traffic, Vol. 19, Issue 11 https://doi.org/10.1111/tra.12610	journal	September 2018
The CCT chaperonin is a novel regulator of Ca ²⁺ signaling through modulation of Orai1 trafficking Hodeify, Rawad; Nandakumar, Manjula; Own, Maryam Science Advances, Vol. 4, Issue 9 https://doi.org/10.1126/sciadv.aau1935	journal	September 2018
Structural investigation of a chaperonin in action reveals how nucleotide binding regulates the functional cycle Mas, Guillaume; Guan, Jia-Ying; Crublet, Elodie Science Advances, Vol. 4, Issue 9 https://doi.org/10.1126/sciadv.aau4196	journal	September 2018
In vivo aspects of protein folding and quality control Balchin, David; Hayer-Hartl, Manajit; Hartl, F. Ulrich Science, Vol. 353, Issue 6294 https://doi.org/10.1126/science.aac4354	journal	June 2016
A systematic atlas of chaperome deregulation topologies across the human cancer landscape Hadizadeh Esfahani, Ali; Sverchkova, Angelina; Saez-Rodriguez, Julio PLOS Computational Biology, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pcbi.1005890	journal	January 2018
A systematic atlas of chaperome deregulation topologies across the human cancer landscape Hadizadeh Esfahani, Ali; Sverchkova, Angelina; Sáez Rodríguez, Julio RWTH Aachen University https://doi.org/10.18154/rwth-2018-222284	text	January 2018
Chaperoning the Mononegavirales: Current Knowledge and Future Directions Latorre, Victor; Mattenberger, Florian; Geller, Ron https://doi.org/10.20944/preprints201811.0475.v1	preprint	November 2018
Chaperoning the Mononegavirales: Current Knowledge and Future Directions Latorre, Victor; Mattenberger, Florian; Geller, Ron Viruses, Vol. 10, Issue 12 https://doi.org/10.3390/v10120699	journal	December 2018

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