4a0v › Citations

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 31 720-30 (2012)
Related entries: 4a0o, 4a0w, 4a13

Cited: 58 times
EuropePMC logo PMID: 22045336

Abstract

The eukaryotic group II chaperonin TRiC/CCT is a 16-subunit complex with eight distinct but similar subunits arranged in two stacked rings. Substrate folding inside the central chamber is triggered by ATP hydrolysis. We present five cryo-EM structures of TRiC in apo and nucleotide-induced states without imposing symmetry during the 3D reconstruction. These structures reveal the intra- and inter-ring subunit interaction pattern changes during the ATPase cycle. In the apo state, the subunit arrangement in each ring is highly asymmetric, whereas all nucleotide-containing states tend to be more symmetrical. We identify and structurally characterize an one-ring closed intermediate induced by ATP hydrolysis wherein the closed TRiC ring exhibits an observable chamber expansion. This likely represents the physiological substrate folding state. Our structural results suggest mechanisms for inter-ring-negative cooperativity, intra-ring-positive cooperativity, and protein-folding chamber closure of TRiC. Intriguingly, these mechanisms are different from other group I and II chaperonins despite their similar architecture.

Reviews - 4a0v mentioned but not cited (1)

  1. Intrinsic dynamics is evolutionarily optimized to enable allosteric behavior. Zhang Y, Doruker P, Kaynak B, Zhang S, Krieger J, Li H, Bahar I. Curr Opin Struct Biol 62 14-21 (2020)

Articles - 4a0v mentioned but not cited (4)

  1. 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)
  2. Variability of Protein Structure Models from Electron Microscopy. Monroe L, Terashi G, Kihara D. Structure 25 592-602.e2 (2017)
  3. VESPER: global and local cryo-EM map alignment using local density vectors. Han X, Terashi G, Christoffer C, Chen S, Kihara D. Nat Commun 12 2090 (2021)
  4. State-dependent sequential allostery exhibited by chaperonin TRiC/CCT revealed by network analysis of Cryo-EM maps. Zhang Y, Krieger J, Mikulska-Ruminska K, Kaynak B, Sorzano COS, Carazo JM, Xing J, Bahar I. Prog Biophys Mol Biol 160 104-120 (2021)


Reviews citing this publication (10)

  1. 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)
  2. Chaperone machines for protein folding, unfolding and disaggregation. Saibil H. Nat. Rev. Mol. Cell Biol. 14 630-642 (2013)
  3. The Mechanism and Function of Group II Chaperonins. Lopez T, Dalton K, Frydman J. J. Mol. Biol. 427 2919-2930 (2015)
  4. ATP-driven molecular chaperone machines. Clare DK, Saibil HR. Biopolymers 99 846-859 (2013)
  5. Contribution of the Type II Chaperonin, TRiC/CCT, to Oncogenesis. Roh SH, Kasembeli M, Bakthavatsalam D, Chiu W, Tweardy DJ. Int J Mol Sci 16 26706-26720 (2015)
  6. Asymmetric perturbations of signalling oligomers. Maksay G, Tőke O. Prog. Biophys. Mol. Biol. 114 153-169 (2014)
  7. Heat shock proteins: Biological functions, pathological roles, and therapeutic opportunities. Hu C, Yang J, Qi Z, Wu H, Wang B, Zou F, Mei H, Liu J, Wang W, Liu Q. MedComm (2020) 3 e161 (2022)
  8. 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)
  9. Complex Destabilization in the Mitochondrial Chaperonin Hsp60 Leads to Disease. Rodriguez A, Von Salzen D, Holguin BA, Bernal RA. Front Mol Biosci 7 159 (2020)
  10. 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. Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Herzog F, Kahraman A, Boehringer D, Mak R, Bracher A, Walzthoeni T, Leitner A, Beck M, Hartl FU, Ban N, Malmström L, Aebersold R. Science 337 1348-1352 (2012)
  2. 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)
  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. Visualizing GroEL/ES in the act of encapsulating a folding protein. Chen DH, Madan D, Weaver J, Lin Z, Schröder GF, Chiu W, Rye HS. Cell 153 1354-1365 (2013)
  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. xTract: software for characterizing conformational changes of protein complexes by quantitative cross-linking mass spectrometry. Walzthoeni T, Joachimiak LA, Rosenberger G, Röst HL, Malmström L, Leitner A, Frydman J, Aebersold R. Nat. Methods 12 1185-1190 (2015)
  7. TRiC's tricks inhibit huntingtin aggregation. Shahmoradian SH, Galaz-Montoya JG, Schmid MF, Cong Y, Ma B, Spiess C, Frydman J, Ludtke SJ, Chiu W. Elife 2 e00710 (2013)
  8. 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)
  9. High resolution single particle refinement in EMAN2.1. Bell JM, Chen M, Baldwin PR, Ludtke SJ. Methods 100 25-34 (2016)
  10. Folding of large multidomain proteins by partial encapsulation in the chaperonin TRiC/CCT. Rüßmann F, Stemp MJ, Mönkemeyer L, Etchells SA, Bracher A, Hartl FU. Proc. Natl. Acad. Sci. U.S.A. 109 21208-21215 (2012)
  11. Single particle tomography in EMAN2. Galaz-Montoya JG, Flanagan J, Schmid MF, Ludtke SJ. J. Struct. Biol. 190 279-290 (2015)
  12. De novo modeling of the F(420)-reducing [NiFe]-hydrogenase from a methanogenic archaeon by cryo-electron microscopy. Mills DJ, Vitt S, Strauss M, Shima S, Vonck J. Elife 2 e00218 (2013)
  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. Structure and conformational variability of the mycobacterium tuberculosis fatty acid synthase multienzyme complex. Ciccarelli L, Connell SR, Enderle M, Mills DJ, Vonck J, Grininger M. Structure 21 1251-1257 (2013)
  15. 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)
  16. Chaperonin TRiC/CCT Modulates the Folding and Activity of Leukemogenic Fusion Oncoprotein AML1-ETO. Roh SH, Kasembeli M, Galaz-Montoya JG, Trnka M, Lau WC, Burlingame A, Chiu W, Tweardy DJ. J. Biol. Chem. 291 4732-4741 (2016)
  17. Chaperonin-containing TCP-1 complex directly binds to the cytoplasmic domain of the LOX-1 receptor. Bakthavatsalam D, Soung RH, Tweardy DJ, Chiu W, Dixon RA, Woodside DG. FEBS Lett. 588 2133-2140 (2014)
  18. Targeting chaperonin containing TCP1 (CCT) as a molecular therapeutic for small cell lung cancer. Carr AC, Khaled AS, Bassiouni R, Flores O, Nierenberg D, Bhatti H, Vishnubhotla P, Manuel JP, Santra S, Khaled AR. Oncotarget 8 110273-110288 (2017)
  19. Ring Separation Highlights the Protein-Folding Mechanism Used by the Phage EL-Encoded Chaperonin. Molugu SK, Hildenbrand ZL, Morgan DG, Sherman MB, He L, Georgopoulos C, Sernova NV, Kurochkina LP, Mesyanzhinov VV, Miroshnikov KA, Bernal RA. Structure 24 537-546 (2016)
  20. 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)
  21. 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)
  22. Structural and mechanistic characterization of an archaeal-like chaperonin from a thermophilic bacterium. An YJ, Rowland SE, Na JH, Spigolon D, Hong SK, Yoon YJ, Lee JH, Robb FT, Cha SS. Nat Commun 8 827 (2017)
  23. Arrangement of the Polymerase Complexes inside a Nine-Segmented dsRNA Virus. Kaelber JT, Jiang W, Weaver SC, Auguste AJ, Chiu W. Structure 28 604-612.e3 (2020)
  24. Assisted protein folding at low temperature: evolutionary adaptation of the Antarctic fish chaperonin CCT and its client proteins. Cuellar J, Yébenes H, Parker SK, Carranza G, Serna M, Valpuesta JM, Zabala JC, Detrich HW. Biol Open 3 261-270 (2014)
  25. Chaperonin TRiC/CCT Recognizes Fusion Oncoprotein AML1-ETO through Subunit-Specific Interactions. Roh SH, Kasembeli MM, Galaz-Montoya JG, Chiu W, Tweardy DJ. Biophys. J. 110 2377-2385 (2016)
  26. Development of a yeast internal-subunit eGFP labeling strategy and its application in subunit identification in eukaryotic group II chaperonin TRiC/CCT. Zang Y, Wang H, Cui Z, Jin M, Liu C, Han W, Wang Y, Cong Y. Sci Rep 8 2374 (2018)
  27. Hetero-oligomeric CPN60 resembles highly symmetric group-I chaperonin structure revealed by Cryo-EM. Zhao Q, Zhang X, Sommer F, Ta N, Wang N, Schroda M, Cong Y, Liu C. Plant J 98 798-812 (2019)
  28. 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)
  29. Approximating deformation fields for the analysis of continuous heterogeneity of biological macromolecules by 3D Zernike polynomials. Herreros D, Lederman RR, Krieger J, Jiménez-Moreno A, Martínez M, Myška D, Strelak D, Filipovic J, Bahar I, Carazo JM, Sanchez COS. IUCrJ 8 992-1005 (2021)
  30. Interaction with the CCT chaperonin complex limits APOBEC3A cytidine deaminase cytotoxicity. Green AM, DeWeerd RA, O'Leary DR, Hansen AR, Hayer KE, Kulej K, Dineen AS, Szeto JH, Garcia BA, Weitzman MD. EMBO Rep 22 e52145 (2021)
  31. Quantitative analysis of the impact of a human pathogenic mutation on the CCT5 chaperonin subunit using a proxy archaeal ortholog. Spigolon D, Gallagher DT, Velazquez-Campoy A, Bulone D, Narang J, San Biagio PL, Cappello F, Macario AJL, Conway de Macario E, Robb FT. Biochem Biophys Rep 12 66-71 (2017)
  32. An ensemble of cryo-EM structures of TRiC reveal its conformational landscape and subunit specificity. Jin M, Han W, Liu C, Zang Y, Li J, Wang F, Wang Y, Cong Y. Proc. Natl. Acad. Sci. U.S.A. 116 19513-19522 (2019)
  33. 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)
  34. Differential conformational modulations of MreB folding upon interactions with GroEL/ES and TRiC chaperonin components. Moparthi SB, Carlsson U, Vincentelli R, Jonsson BH, Hammarström P, Wenger J. Sci Rep 6 28386 (2016)
  35. Functional characterization of chaperonin containing T-complex polypeptide-1 and its conserved and novel substrates in Arabidopsis. Ahn HK, Yoon JT, Choi I, Kim S, Lee HS, Pai HS. J. Exp. Bot. 70 2741-2757 (2019)
  36. News Identification of an allosteric network that influences assembly and function of group II chaperonins. Jin M, Cong Y. Nat. Struct. Mol. Biol. 24 683-684 (2017)
  37. 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)
  38. Pathway and mechanism of tubulin folding mediated by TRiC/CCT along its ATPase cycle revealed using cryo-EM. Liu C, Jin M, Wang S, Han W, Zhao Q, Wang Y, Xu C, Diao L, Yin Y, Peng C, Peng C, Bao L, Wang Y, Cong Y. Commun Biol 6 531 (2023)
  39. Quantitative analysis of global protein stability rates in tissues. McClatchy DB, Martínez-Bartolomé S, Gao Y, Lavallée-Adam M, Yates JR. Sci Rep 10 15983 (2020)
  40. 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)
  41. Structural and functional analysis of the role of the chaperonin CCT in mTOR complex assembly. Cuéllar J, Ludlam WG, Tensmeyer NC, Aoba T, Dhavale M, Santiago C, Bueno-Carrasco MT, Mann MJ, Plimpton RL, Makaju A, Franklin S, Willardson BM, Valpuesta JM. Nat Commun 10 2865 (2019)
  42. Structural basis of plp2-mediated cytoskeletal protein folding by TRiC/CCT. Han W, Jin M, Liu C, Zhao Q, Wang S, Wang Y, Yin Y, Peng C, Wang Y, Cong Y. Sci Adv 9 eade1207 (2023)
  43. Structural visualization of the tubulin folding pathway directed by human chaperonin TRiC/CCT. Gestaut D, Zhao Y, Park J, Ma B, Leitner A, Collier M, Pintilie G, Roh SH, Chiu W, Frydman J. Cell 185 4770-4787.e20 (2022)


Quick links