The crystal structures of the eukaryotic chaperonin CCT reveal its functional partitioning

Structure

Volumn 21, Issue 4, 2013, Pages 540-549

  Kalisman, Nir ^a   Schröder, Gunnar F ^b,c   Levitt, Michael ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; CHAPERONIN CONTAINING TCP1; PROTEIN CCCT6; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME SUBSTRATE COMPLEX; EUKARYOTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION;

ACTINS; AMINO ACID SEQUENCE; BASE SEQUENCE; CHAPERONIN CONTAINING TCP-1; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY; SPECIES SPECIFICITY; TUBULIN;

EUKARYOTA;

EID: 84875883590     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.01.017     Document Type: Article

References (32)

1. M. Amit, S.J. Weisberg, M. Nadler-Holly, E.A. McCormack, E. Feldmesser, D. Kaganovich, K.R. Willison, and A. Horovitz Equivalent mutations in the eight subunits of the chaperonin CCT produce dramatically different cellular and gene expression phenotypes J. Mol. Biol. 401 2010 532 543
2. J.M. Archibald, C. Blouin, and W.F. Doolittle Gene duplication and the evolution of group II chaperonins: implications for structure and function J. Struct. Biol. 135 2001 157 169
3. A.T. Brunger Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2 2007 2728 2733
4. Y. Cong, M.L. Baker, J. Jakana, D. Woolford, E.J. Miller, S. Reissmann, R.N. Kumar, A.M. Redding-Johanson, T.S. Batth, and A. Mukhopadhyay 4.0-A resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement Proc. Natl. Acad. Sci. USA 107 2010 4967 4972
5. C. Dekker, S.M. Roe, E.A. McCormack, F. Beuron, L.H. Pearl, and K.R. Willison The crystal structure of yeast CCT reveals intrinsic asymmetry of eukaryotic cytosolic chaperonins EMBO J. 30 2011 3078 3090
6. L. Ditzel, J. Löwe, D. Stock, K.O. Stetter, H. Huber, R. Huber, and S. Steinbacher Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT Cell 93 1998 125 138
7. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
8. M. Gerstein, and C. Chothia Packing at the protein-water interface Proc. Natl. Acad. Sci. USA 93 1996 10167 10172
9. F. Herzog, A. Kahraman, D. Boehringer, R. Mak, A. Bracher, T. Walzthoeni, A. Leitner, M. Beck, F.U. Hartl, and N. Ban Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry Science 337 2012 1348 1352
10. Y. Jiang, N.R. Douglas, N.R. Conley, E.J. Miller, J. Frydman, and W.E. Moerner Sensing cooperativity in ATP hydrolysis for single multisubunit enzymes in solution Proc. Natl. Acad. Sci. USA 108 2011 16962 16967
11. N. Kalisman, and M. Levitt Insights into the intra-ring subunit order of tric/cct: a structural and evolutionary analysis Pac. Symp. Biocomput. 15 2010 252 259
12. N. Kalisman, C.M. Adams, and M. Levitt Subunit order of eukaryotic TRiC/CCT chaperonin by cross-linking, mass spectrometry, and combinatorial homology modeling Proc. Natl. Acad. Sci. USA 109 2012 2884 2889
13. G. Kapatai, A. Large, J.L. Benesch, C.V. Robinson, J.L. Carrascosa, J.M. Valpuesta, P. Gowrinathan, and P.A. Lund All three chaperonin genes in the archaeon Haloferax volcanii are individually dispensable Mol. Microbiol. 61 2006 1583 1597
14. G.G. Krivov, M.V. Shapovalov, and R.L. Dunbrack Jr. Improved prediction of protein side-chain conformations with SCWRL4 Proteins 77 2009 778 795
15. A. Leitner, L.A. Joachimiak, A. Bracher, L. Mönkemeyer, T. Walzthoeni, B. Chen, S. Pechmann, S. Holmes, Y. Cong, and B. Ma The molecular architecture of the eukaryotic chaperonin TRiC/CCT Structure 20 2012 814 825
16. M. Levitt, M. Hirshberg, R. Sharon, and V. Daggett Potential energy function and parameters for simulations of the molecular dynamics of proteins and nucleic acids in solution Comput. Phys. Commun. 91 1995 215 231
17. P. Lin, T.S. Cardillo, L.M. Richard, G.B. Segel, and F. Sherman Analysis of mutationally altered forms of the Cct6 subunit of the chaperonin from Saccharomyces cerevisiae Genetics 147 1997 1609 1633
18. O. Llorca, J. Martín-Benito, P. Gómez-Puertas, M. Ritco-Vonsovici, K.R. Willison, J.L. Carrascosa, and J.M. Valpuesta Analysis of the interaction between the eukaryotic chaperonin CCT and its substrates actin and tubulin J. Struct. Biol. 135 2001 205 218
19. J. Martín-Benito, S. Bertrand, T. Hu, P.J. Ludtke, J.N. McLaughlin, B.M. Willardson, J.L. Carrascosa, and J.M. Valpuesta Structure of the complex between the cytosolic chaperonin CCT and phosducin-like protein Proc. Natl. Acad. Sci. USA 101 2004 17410 17415
20. J. Martín-Benito, J. Grantham, J. Boskovic, K.I. Brackley, J.L. Carrascosa, K.R. Willison, and J.M. Valpuesta The inter-ring arrangement of the cytosolic chaperonin CCT EMBO Rep. 8 2007 252 257
21. A.S. Meyer, J.R. Gillespie, D. Walther, I.S. Millet, S. Doniach, and J. Frydman Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis Cell 113 2003 369 381
22. I.G. Muñoz, H. Yébenes, M. Zhou, P. Mesa, M. Serna, A.Y. Park, E. Bragado-Nilsson, A. Beloso, G. de Cárcer, and M. Malumbres Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin Nat. Struct. Mol. Biol. 18 2011 14 19
23. M. Nadler-Holly, M. Breker, R. Gruber, A. Azia, M. Gymrek, M. Eisenstein, K.R. Willison, M. Schuldiner, and A. Horovitz Interactions of subunit CCT3 in the yeast chaperonin CCT/TRiC with Q/N-rich proteins revealed by high-throughput microscopy analysis Proc. Natl. Acad. Sci. USA 109 2012 18833 18838
24. G. Pappenberger, E.A. McCormack, and K.R. Willison Quantitative actin folding reactions using yeast CCT purified via an internal tag in the CCT3/gamma subunit J. Mol. Biol. 360 2006 484 496
25. S. Reissmann, L.A. Joachimiak, B. Chen, A.S. Meyer, A. Nguyen, and J. Frydman A gradient of ATP affinities generates an asymmetric power stroke driving the chaperonin TRIC/CCT folding cycle Cell Rep. 2 2012 866 877
26. D. Rivenzon-Segal, S.G. Wolf, L. Shimon, K.R. Willison, and A. Horovitz Sequential ATP-induced allosteric transitions of the cytoplasmic chaperonin containing TCP-1 revealed by EM analysis Nat. Struct. Mol. Biol. 12 2005 233 237
27. G.F. Schröder, M. Levitt, and A.T. Brunger Super-resolution biomolecular crystallography with low-resolution data Nature 464 2010 1218 1222
28. L. Shimon, G.M. Hynes, E.A. McCormack, K.R. Willison, and A. Horovitz ATP-induced allostery in the eukaryotic chaperonin CCT is abolished by the mutation G345D in CCT4 that renders yeast temperature-sensitive for growth J. Mol. Biol. 377 2008 469 477
29. Y. Shomura, T. Yoshida, R. Iizuka, T. Maruyama, M. Yohda, and K. Miki Crystal structures of the group II chaperonin from Thermococcus strain KS-1: steric hindrance by the substituted amino acid, and inter-subunit rearrangement between two crystal forms J. Mol. Biol. 335 2004 1265 1278
30. C. Spiess, E.J. Miller, A.J. McClellan, and J. Frydman Identification of the TRiC/CCT substrate binding sites uncovers the function of subunit diversity in eukaryotic chaperonins Mol. Cell 24 2006 25 37
31. A.A. Vaguine, J. Richelle, and S.J. Wodak SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model Acta Crystallogr. D Biol. Crystallogr. 55 1999 191 205
32. H. Yébenes, P. Mesa, I.G. Muñoz, G. Montoya, and J.M. Valpuesta Chaperonins: two rings for folding Trends Biochem. Sci. 36 2011 424 432