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Dual action of ATP hydrolysis couples lid closure to substrate release into the group II chaperonin chamber.

Douglas NR, Reissmann S, Zhang J, Chen B, Jakana J, Kumar R, Chiu W, Frydman J
Cell 144 240-52 (2011)
Related entries: 3izi, 3izj, 3izk, 3izl, 3izm, 3izn

Cited: 62 times
EuropePMC logo PMID: 21241893

Abstract

Group II chaperonins are ATP-dependent ring-shaped complexes that bind nonnative polypeptides and facilitate protein folding in archaea and eukaryotes. A built-in lid encapsulates substrate proteins within the central chaperonin chamber. Here, we describe the fate of the substrate during the nucleotide cycle of group II chaperonins. The chaperonin substrate-binding sites are exposed, and the lid is open in both the ATP-free and ATP-bound prehydrolysis states. ATP hydrolysis has a dual function in the folding cycle, triggering both lid closure and substrate release into the central chamber. Notably, substrate release can occur in the absence of a lid, and lid closure can occur without substrate release. However, productive folding requires both events, so that the polypeptide is released into the confined space of the closed chamber where it folds. Our results show that ATP hydrolysis coordinates the structural and functional determinants that trigger productive folding.

Reviews - 3izh mentioned but not cited (1)

  1. Chaperonins: Nanocarriers with Biotechnological Applications. Pipaón S, Gragera M, Bueno-Carrasco MT, García-Bernalt Diego J, Cantero M, Cuéllar J, Fernández-Fernández MR, Valpuesta JM. Nanomaterials (Basel) 11 503 (2021)

Articles - 3izh mentioned but not cited (2)

  1. Flexible Fitting of Atomic Models into Cryo-EM Density Maps Guided by Helix Correspondences. Dou H, Burrows DW, Baker ML, Ju T. Biophys. J. 112 2479-2493 (2017)
  2. Structural investigation of a chaperonin in action reveals how nucleotide binding regulates the functional cycle. Mas G, Guan JY, Crublet E, Debled EC, Moriscot C, Gans P, Schoehn G, Macek P, Schanda P, Boisbouvier J. Sci Adv 4 eaau4196 (2018)


Reviews citing this publication (16)

  1. Molecular chaperones in protein folding and proteostasis. Hartl FU, Bracher A, Hayer-Hartl M. Nature 475 324-332 (2011)
  2. Molecular chaperone functions in protein folding and proteostasis. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU. Annu. Rev. Biochem. 82 323-355 (2013)
  3. In vivo aspects of protein folding and quality control. Balchin D, Hayer-Hartl M, Hartl FU. Science 353 aac4354 (2016)
  4. The ribosome as a hub for protein quality control. Pechmann S, Willmund F, Frydman J. Mol. Cell 49 411-421 (2013)
  5. Chemical and biological approaches for adapting proteostasis to ameliorate protein misfolding and aggregation diseases: progress and prognosis. Lindquist SL, Kelly JW. Cold Spring Harb Perspect Biol 3 (2011)
  6. The Mechanism and Function of Group II Chaperonins. Lopez T, Dalton K, Frydman J. J. Mol. Biol. 427 2919-2930 (2015)
  7. Protein cages and synthetic polymers: a fruitful symbiosis for drug delivery applications, bionanotechnology and materials science. Rother M, Nussbaumer MG, Renggli K, Bruns N. Chem Soc Rev 45 6213-6249 (2016)
  8. Dynamics, flexibility, and allostery in molecular chaperonins. Skjærven L, Cuellar J, Martinez A, Valpuesta JM. FEBS Lett. 589 2522-2532 (2015)
  9. Chaperone-client interactions: Non-specificity engenders multifunctionality. Koldewey P, Horowitz S, Bardwell JCA. J. Biol. Chem. 292 12010-12017 (2017)
  10. Therapeutic Approaches for Inhibition of Protein Aggregation in Huntington's Disease. Kim S, Kim KT. Exp Neurobiol 23 36-44 (2014)
  11. Opportunities and challenges for molecular chaperone modulation to treat protein-conformational brain diseases. van der Putten H, Lotz GP. Neurotherapeutics 10 416-428 (2013)
  12. Evolution of the archaeal and mammalian information processing systems: towards an archaeal model for human disease. Lyu Z, Whitman WB. Cell. Mol. Life Sci. 74 183-212 (2017)
  13. Surface Engineering of Nanoparticles for Targeted Delivery to Hepatocellular Carcinoma. Lu J, Wang J, Ling D. Small 14 (2018)
  14. The TRiCky Business of Protein Folding in Health and Disease. Ghozlan H, Cox A, Nierenberg D, King S, Khaled AR. Front Cell Dev Biol 10 906530 (2022)
  15. Diversity in heat shock protein families: functional implications in virus infection with a comprehensive insight of their role in the HIV-1 life cycle. Iyer K, Chand K, Mitra A, Trivedi J, Mitra D. Cell Stress Chaperones 26 743-768 (2021)
  16. The ATP-powered gymnastics of TRiC/CCT: an asymmetric protein folding machine with a symmetric origin story. Gestaut D, Limatola A, Joachimiak L, Frydman J. Curr. Opin. Struct. Biol. 55 50-58 (2019)

Articles citing this publication (43)

  1. The molecular architecture of the eukaryotic chaperonin TRiC/CCT. Leitner A, Joachimiak LA, Bracher A, Mönkemeyer L, Walzthoeni T, Chen B, Pechmann S, Holmes S, Cong Y, Ma B, Ludtke S, Chiu W, Hartl FU, Aebersold R, Frydman J. Structure 20 814-825 (2012)
  2. Interaction of p53 with the CCT complex promotes protein folding and wild-type p53 activity. Trinidad AG, Muller PA, Cuellar J, Klejnot M, Nobis M, Valpuesta JM, Vousden KH. Mol. Cell 50 805-817 (2013)
  3. The structural basis of substrate recognition by the eukaryotic chaperonin TRiC/CCT. Joachimiak LA, Walzthoeni T, Liu CW, Aebersold R, Frydman J. Cell 159 1042-1055 (2014)
  4. Symmetry-free cryo-EM structures of the chaperonin TRiC along its ATPase-driven conformational cycle. Cong Y, Schröder GF, Meyer AS, Jakana J, Ma B, Dougherty MT, Schmid MF, Reissmann S, Levitt M, Ludtke SL, Frydman J, Chiu W. EMBO J. 31 720-730 (2012)
  5. A gradient of ATP affinities generates an asymmetric power stroke driving the chaperonin TRIC/CCT folding cycle. Reissmann S, Joachimiak LA, Chen B, Meyer AS, Nguyen A, Frydman J. Cell Rep 2 866-877 (2012)
  6. Cryo-EM structure of a group II chaperonin in the prehydrolysis ATP-bound state leading to lid closure. Zhang J, Ma B, DiMaio F, Douglas NR, Joachimiak LA, Baker D, Frydman J, Levitt M, Chiu W. Structure 19 633-639 (2011)
  7. Human CCT4 and CCT5 chaperonin subunits expressed in Escherichia coli form biologically active homo-oligomers. Sergeeva OA, Chen B, Haase-Pettingell C, Ludtke SJ, Chiu W, King JA. J. Biol. Chem. 288 17734-17744 (2013)
  8. Mechanism of nucleotide sensing in group II chaperonins. Pereira JH, Ralston CY, Douglas NR, Kumar R, Lopez T, McAndrew RP, Knee KM, King JA, Frydman J, Adams PD. EMBO J. 31 731-740 (2012)
  9. Reprogramming an ATP-driven protein machine into a light-gated nanocage. Hoersch D, Roh SH, Chiu W, Kortemme T. Nat Nanotechnol 8 928-932 (2013)
  10. Structures of the Gβ-CCT and PhLP1-Gβ-CCT complexes reveal a mechanism for G-protein β-subunit folding and Gβγ dimer assembly. Plimpton RL, Cuéllar J, Lai CW, Aoba T, Makaju A, Franklin S, Mathis AD, Prince JT, Carrascosa JL, Valpuesta JM, Willardson BM. Proc. Natl. Acad. Sci. U.S.A. 112 2413-2418 (2015)
  11. Human TRiC complex purified from HeLa cells contains all eight CCT subunits and is active in vitro. Knee KM, Sergeeva OA, King JA. Cell Stress Chaperones 18 137-144 (2013)
  12. Programmed cell death protein 5 interacts with the cytosolic chaperonin containing tailless complex polypeptide 1 (CCT) to regulate β-tubulin folding. Tracy CM, Gray AJ, Cuéllar J, Shaw TS, Howlett AC, Taylor RM, Prince JT, Ahn NG, Valpuesta JM, Willardson BM. J. Biol. Chem. 289 4490-4502 (2014)
  13. Multiscale natural moves refine macromolecules using single-particle electron microscopy projection images. Zhang J, Minary P, Levitt M. Proc. Natl. Acad. Sci. U.S.A. 109 9845-9850 (2012)
  14. ATP dependent rotational motion of group II chaperonin observed by X-ray single molecule tracking. Sekiguchi H, Nakagawa A, Moriya K, Makabe K, Ichiyanagi K, Nozawa S, Sato T, Adachi S, Kuwajima K, Yohda M, Sasaki YC. PLoS ONE 8 e64176 (2013)
  15. A modulator domain controlling thermal stability in the Group II chaperonins of Archaea. Luo H, Robb FT. Arch. Biochem. Biophys. 512 111-118 (2011)
  16. Staggered ATP binding mechanism of eukaryotic chaperonin TRiC (CCT) revealed through high-resolution cryo-EM. Zang Y, Jin M, Wang H, Cui Z, Kong L, Liu C, Cong Y. Nat. Struct. Mol. Biol. 23 1083-1091 (2016)
  17. The Role of Plastidic Trigger Factor Serving Protein Biogenesis in Green Algae and Land Plants. Rohr M, Ries F, Herkt C, Gotsmann VL, Westrich LD, Gries K, Trösch R, Christmann J, Chaux-Jukic F, Jung M, Zimmer D, Mühlhaus T, Sommer F, Schroda M, Keller S, Möhlmann T, Willmund F. Plant Physiol 179 1093-1110 (2019)
  18. A human CCT5 gene mutation causing distal neuropathy impairs hexadecamer assembly in an archaeal model. Min W, Angileri F, Luo H, Lauria A, Shanmugasundaram M, Almerico AM, Cappello F, de Macario EC, Lednev IK, Macario AJ, Robb FT. Sci Rep 4 6688 (2014)
  19. Molecular determinants of the ATP hydrolysis asymmetry of the CCT chaperonin complex. Chagoyen M, Carrascosa JL, Pazos F, Valpuesta JM. Proteins 82 703-707 (2014)
  20. Sequential allosteric mechanism of ATP hydrolysis by the CCT/TRiC chaperone is revealed through Arrhenius analysis. Gruber R, Levitt M, Horovitz A. Proc. Natl. Acad. Sci. U.S.A. 114 5189-5194 (2017)
  21. Structure of the human TRiC/CCT Subunit 5 associated with hereditary sensory neuropathy. Pereira JH, McAndrew RP, Sergeeva OA, Ralston CY, King JA, Adams PD. Sci Rep 7 3673 (2017)
  22. Flexible interwoven termini determine the thermal stability of thermosomes. Zhang K, Wang L, Liu Y, Chan KY, Pang X, Schulten K, Dong Z, Sun F. Protein Cell 4 432-444 (2013)
  23. Dissection of the ATP-dependent conformational change cycle of a group II chaperonin. Nakagawa A, Moriya K, Arita M, Yamamoto Y, Kitamura K, Ishiguro N, Kanzaki T, Oka T, Makabe K, Kuwajima K, Yohda M. J. Mol. Biol. 426 447-459 (2014)
  24. Asymmetry in the function and dynamics of the cytosolic group II chaperonin CCT/TRiC. Yamamoto YY, Uno Y, Sha E, Ikegami K, Ishii N, Dohmae N, Sekiguchi H, Sasaki YC, Yohda M. PLoS ONE 12 e0176054 (2017)
  25. Structural and Functional Insights into the Evolution and Stress Adaptation of Type II Chaperonins. Chaston JJ, Smits C, Aragão D, Wong AS, Ahsan B, Sandin S, Molugu SK, Molugu SK, Bernal RA, Stock D, Stewart AG. Structure 24 364-374 (2016)
  26. Structural and functional dissection of reovirus capsid folding and assembly by the prefoldin-TRiC/CCT chaperone network. Knowlton JJ, Gestaut D, Ma B, Taylor G, Seven AB, Leitner A, Wilson GJ, Shanker S, Yates NA, Prasad BVV, Aebersold R, Chiu W, Frydman J, Dermody TS. Proc Natl Acad Sci U S A 118 e2018127118 (2021)
  27. An information theoretic framework reveals a tunable allosteric network in group II chaperonins. Lopez T, Dalton K, Tomlinson A, Pande V, Frydman J. Nat. Struct. Mol. Biol. 24 726-733 (2017)
  28. Use of evolutionary information in the fitting of atomic level protein models in low resolution cryo-EM map of a protein assembly improves the accuracy of the fitting. Joseph AP, Swapna LS, Rakesh R, Srinivasan N. J. Struct. Biol. 195 294-305 (2016)
  29. Characterization of group II chaperonins from an acidothermophilic archaeon Picrophilus torridus. Yamamoto YY, Tsuchida K, Noguchi K, Ogawa N, Sekiguchi H, Sasaki YC, Yohda M. FEBS Open Bio 6 751-764 (2016)
  30. The dynamic conformational cycle of the group I chaperonin C-termini revealed via molecular dynamics simulation. Dalton KM, Frydman J, Pande VS. PLoS ONE 10 e0117724 (2015)
  31. Group II archaeal chaperonin recognition of partially folded human γD-crystallin mutants. Sergeeva OA, Yang J, King JA, Knee KM. Protein Sci. 23 693-702 (2014)
  32. Protein folding, misfolding and quality control: the role of molecular chaperones. Papsdorf K, Richter K. Essays Biochem. 56 53-68 (2014)
  33. Using the dendritic polymer PAMAM to form gold nanoparticles in the protein cage thermosome. Nussbaumer MG, Bisig C, Bruns N. Chem. Commun. (Camb.) 52 10537-10539 (2016)
  34. A structural vista of phosducin-like PhLP2A-chaperonin TRiC cooperation during the ATP-driven folding cycle. Park J, Kim H, Gestaut D, Lim S, Opoku-Nsiah KA, Leitner A, Frydman J, Roh SH. Nat Commun 15 1007 (2024)
  35. Co-expression of CCT subunits hints at TRiC assembly. Sergeeva OA, Haase-Pettingell C, King JA. Cell Stress Chaperones 24 1055-1065 (2019)
  36. CryoEM reveals the stochastic nature of individual ATP binding events in a group II chaperonin. Zhao Y, Schmid MF, Frydman J, Chiu W. Nat Commun 12 4754 (2021)
  37. Design of Light-Controlled Protein Conformations and Functions. Ritterson RS, Hoersch D, Barlow KA, Kortemme T. Methods Mol. Biol. 1414 197-211 (2016)
  38. Intraring allostery controls the function and assembly of a hetero-oligomeric class II chaperonin. Shoemark DK, Sessions RB, Brancaccio A, Bigotti MG. FASEB J. 32 2223-2234 (2018)
  39. Loss of exosomal miR-3188 in cancer-associated fibroblasts contributes to HNC progression. Wang X, Qin X, Yan M, Shi J, Xu Q, Li Z, Yang W, Zhang J, Chen W. J. Exp. Clin. Cancer Res. 38 151 (2019)
  40. Molecular Dynamics Mappings of the CCT/TRiC Complex-Mediated Protein Folding Cycle Using Diffracted X-ray Tracking. Araki K, Watanabe-Nakayama T, Sasaki D, Sasaki YC, Mio K. Int J Mol Sci 24 14850 (2023)
  41. REP-X: An Evolution-guided Strategy for the Rational Design of Cysteine-less Protein Variants. Dalton K, Lopez T, Pande V, Frydman J. Sci Rep 10 2193 (2020)
  42. Snapshots of actin and tubulin folding inside the TRiC chaperonin. Kelly JJ, Tranter D, Pardon E, Chi G, Kramer H, Happonen L, Knee KM, Janz JM, Steyaert J, Bulawa C, Paavilainen VO, Huiskonen JT, Yue WW. Nat Struct Mol Biol 29 420-429 (2022)
  43. Time-Resolved Measurement of the ATP-Dependent Motion of the Group II Chaperonin by Diffracted Electron Tracking. Ogawa N, Yamamoto YY, Abe K, Sekiguchi H, Sasaki YC, Ishikawa A, Frydman J, Yohda M. Int J Mol Sci 19 (2018)


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