Chaperonin-mediated folding of viral proteins

Advances in Experimental Medicine and Biology

Volumn 726, Issue , 2012, Pages 307-324

  Hildenbrand, Zacariah L ^a   Bernal, Ricardo A ^a  

^a UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN; CHAPERONIN CONTAINING TCP1; CHAPERONIN MM CPN; CHAPERONIN TRIC; HEAT SHOCK PROTEIN 60; THERMOSOME; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; ATP BINDING; BACTERIOPHAGE; BACTERIOPHAGE LAMBDA; BACTERIOPHAGE PHI EL; BACTERIOPHAGE RB49; BACTERIOPHAGE T4; BACTERIOPHAGE T5; BINDING KINETICS; NONHUMAN; POLEROVIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ENCAPSULATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN METABOLISM; PROTEIN SECRETION;

CHAPERONINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; VIRAL PROTEINS; VIRUSES;

EID: 84858171816     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-0980-9_13     Document Type: Article

References (117)

1. Anfi nsen CB (1973) Principles that govern the folding of protein chains. Science 181(96):223-230
2. Ang D, Richardson A, Mayer MP, Keppel F, Krisch H, Georgopoulos C (2001) Pseudo-T-even bacteriophage RB49 encodes CocO, a cochaperonin for GroEL, which can substitute for Escherichia coli's GroES and bacteriophage T4's Gp31. J Biol Chem 276(12):8720-8726
3. Baumketner A, Jewett A, Shea JE (2003) Effects of confi nement in chaperonin assisted protein folding: rate enhancement by decreasing the roughness of the folding energy landscape. J Mol Biol 332(3):701-713. doi: S002228360300929X [pii] (Pubitemid 37075991)
4. Bigotti MG, Clarke AR (2005) Cooperativity in the thermosome. J Mol Biol 348(1):13-26. doi: S0022-2836(05)00126-9 [pii] 10.1016/j.jmb.2005.01.066 (Pubitemid 40461837)
5. Bigotti MG, Clarke AR (2008) Chaperonins: the hunt for the group II mechanism. Arch Biochem Biophys 474(2):331- 339. doi: S0003-9861(08)00157-4 [pii] 10.1016/j.abb.2008.03.015
6. Booth CR, Meyer AS, Cong Y, Topf M, Sali A, Ludtke SJ, Chiu W, Frydman J (2008) Mechanism of lid closure in the eukaryotic chaperonin TRiC/CCT. Nat Struct Mol Biol 15(7):746-753 (Pubitemid 351931999)
7. Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 371(6498):578-586. doi: 10.1038/371578a0 (Pubitemid 24315736)
8. Brinker A, Pfeifer G, Kerner MJ, Naylor DJ, Hartl FU, Hayer-Hartl M (2001) Dual function of protein confi nement in chaperonin-assisted protein folding. Cell 107(2):223-233. doi: S0092-8674(01)00517-7 [pii] (Pubitemid 33035948)
9. Burkal'tseva MV, Krylov VN, Pleteneva EA, Shaburova OV, Krylov SV, Volkart G, Sykilinda NN, Kurochkina LP, Mesianzhinov VV (2002) Phenogenetic characterization of a group of giant Phi KZ-like bacteriophages of Pseudomonas aeruginosa . Genetika 38(11):1470-1479 (Pubitemid 44558344)
10. Burston SG, Ranson NA, Clarke AR (1995) The origins and consequences of asymmetry in the chaperonin reaction cycle. J Mol Biol 249(1):138-152. doi: S0022-2836(85)70285-9 [pii] 10.1006/jmbi.1995.0285
11. Carrascosa JL, Llorca O, Valpuesta JM (2001) Structural comparison of prokaryotic and eukaryotic chaperonins. Micron 32(1):43-50
12. Clark MA, Baumann L, Baumann P (1998) Sequence analysis of a 34.7-kb DNA segment from the genome of Buchnera aphidicola (endosymbiont of aphids) containing groEL, dnaA, the atp operon, gidA, and rho. Curr Microbiol 36(3):158-163 (Pubitemid 28100948)
13. Craig EA, Weissman JS, Horwich AL (1994) Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78(3):365-372. doi: 0092-8674(94)90416-2 [pii] (Pubitemid 24250802)
14. Ditzel L, Lowe J, Stock D, Stetter KO, Huber H, Huber R, Steinbacher S (1998) Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93(1):125-138. doi: S0092-8674(00)81152-6 [pii] (Pubitemid 28173558)
15. Douglas NR, Reissmann S, Zhang J, Chen B, Jakana J, Kumar R, Chiu W, Frydman J (2011) Dual action of ATP hydrolysis couples lid closure to substrate release into the group II chaperonin chamber. Cell 144(2):240-252. doi: S0092-8674(10)01435-2 [pii] 10.1016/j.cell.2010.12.017
16. Ellis RJ (1994) Molecular chaperones. Opening and closing the Anfi nsen cage. Curr Biol 4(7):633-635
17. Ellis RJ, Hartl FU (1996) Protein folding in the cell: competing models of chaperonin function. FASEB J 10(1):20-26 (Pubitemid 26035502)
18. Eskandari F, Sylvester ES, Richardson J (1979) Evidence for lack of propagation of potato roll virus in its aphid vector, Myzus persicae . Phytopathology 69:45-47
19. Farr GW, Fenton WA, Horwich AL (2007) Perturbed ATPase activity and not "close confi nement" of substrate in the cis cavity affects rates of folding by tail-multiplied GroEL. Proc Natl Acad Sci USA 104(13):5342-5347. doi: 0700820104 [pii] 10.1073/pnas.0700820104 (Pubitemid 47175682)
20. Fayet O, Ziegelhoffer T, Georgopoulos C (1989) The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol 171(3):1379-1385 (Pubitemid 19080775)
21. Fenton WA, Horwich AL (1997) GroEL-mediated protein folding. Protein Sci 6(4):743-760. doi: 10.1002/pro.5560060401 (Pubitemid 27154801)
22. Fenton WA, Horwich AL (2003) Chaperonin-mediated protein folding: fate of substrate polypeptide. Q Rev Biophys 36(2):229-256 (Pubitemid 37493574)
23. Fenton WA, Kashi Y, Furtak K, Horwich AL (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371(6498):614-619 (Pubitemid 24315744)
24. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603-647
25. Gadad BS, Britton GB, Ks R (2011) Targeting oligomers in neurodegenerative disorders: lessons from alpha-synuclein, tau, and amyloid-beta peptide. J Alzheimers Dis. doi: RV33683375572T66 [pii] 10.3233/JAD-2011-110182
26. Georgopoulos CP, Hendrix RW, Casjens SR, Kaiser AD (1973) Host participation in bacteriophage lambda head assembly. J Mol Biol 76(1):45-60
27. Gray S, Gildow FE (2003) Luteovirus-aphid interactions. Annu Rev Phytopathol 41:539-566. doi: 10.1146/annurev. phyto.41.012203.105815 012203.105815 [pii] (Pubitemid 37399692)
28. Gutsche I, Essen LO, Baumeister W (1999) Group II chaperonins: new TRiC(k)s and turns of a protein folding machine. J Mol Biol 293(2):295-312 (Pubitemid 29516171)
29. Hansen JJ, Durr A, Cournu-Rebeix I, Georgopoulos C, Ang D, Nielsen MN, Davoine CS, Brice A, Fontaine B, Gregersen N, Bross P (2002) Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am J Hum Genet 70(5):1328-1332. doi: S0002-9297(07)62525-7 [pii] 10.1086/339935 (Pubitemid 34450582)
30. Harrison BD (1985) Usefulness and limitations of the species concept for plant viruses. Intervirology 24(2):71-78 (Pubitemid 15235282)
31. Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381(6583):571-579
32. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295(5561):1852-1858 (Pubitemid 34214115)
33. Hayer-Hartl MK, Weber F, Hartl FU (1996) Mechanism of chaperonin action: GroES binding and release can drive GroEL-mediated protein folding in the absence of ATP hydrolysis. EMBO J 15(22):6111-6121 (Pubitemid 26397883)
34. Hendrix RW, Casjens SR (1975) Assembly of bacteriophage lambda heads: protein processing and its genetic control in petit lambda assembly. J Mol Biol 91(2):187-199
35. Hertveldt K, Lavigne R, Pleteneva E, Sernova N, Kurochkina L, Korchevskii R, Robben J, Mesyanzhinov V, Krylov VN, Volckaert G (2005) Genome comparison of Pseudomonas aeruginosa large phages. J Mol Biol 354(3): 536-545 (Pubitemid 41628273)
36. Hogenhout SA, van der Wilk F, Verbeek M, Goldbach RW, van den Heuvel JF (1998) Potato leafroll virus binds to the equatorial domain of the aphid endosymbiotic GroEL homolog. J Virol 72(1):358-365 (Pubitemid 28048847)
37. Horwich AL, Saibil HR (1998) The thermosome: chaperonin with a built-in lid. Nat Struct Biol 5(5):333-336 (Pubitemid 28211171)
38. Horwich AL, Fenton WA, Chapman E, Farr GW (2007) Two families of chaperonin: physiology and mechanism. Annu Rev Cell Dev Biol 23:115-145. doi: 10.1146/annurev.cellbio.23.090506.123555
39. Hunt JF, van der Vies SM, Henry L, Deisenhofer J (1997) Structural adaptations in the specialized bacteriophage T4 co-chaperonin Gp31 expand the size of the Anfi nsen cage. Cell 90(2):361-371 (Pubitemid 27329720)
40. Iizuka R, So S, Inobe T, Yoshida T, Zako T, Kuwajima K, Yohda M (2004) Role of the helical protrusion in the conformational change and molecular chaperone activity of the archaeal group II chaperonin. J Biol Chem 279(18):18834-18839. doi: 10.1074/jbc.M400839200 M400839200 [pii] (Pubitemid 38623310)
41. Ishii N, Taguchi H, Sumi M, Yoshida M (1992) Structure of holo-chaperonin studied with electron microscopy. Oligomeric cpn10 on top of two layers of cpn60 rings with two stripes each. FEBS Lett 299(2):169-174. doi: 0014- 5793(92)80240-H [pii]
42. Jewett AI, Baumketner A, Shea JE (2004) Accelerated folding in the weak hydrophobic environment of a chaperonin cavity: creation of an alternate fast folding pathway. Proc Natl Acad Sci USA 101(36):13192-13197. doi: 10.1073/pnas.0400720101 0400720101 [pii] (Pubitemid 39209641)
43. Kafri G, Willison KR, Horovitz A (2001) Nested allosteric interactions in the cytoplasmic chaperonin containing TCP-1. Protein Sci 10(2):445-449. doi: 10.1110/ps.44401 (Pubitemid 32225664)
44. Kakeda K, Ishikawa H (1991) Molecular chaperon produced by an intracellular symbiont. J Biochem 110(4):583-587
45. Kanno R, Koike-Takeshita A, Yokoyama K, Taguchi H, Mitsuoka K (2009) Cryo-EM structure of the native GroELGroES complex from Thermus thermophilus encapsulating substrate inside the cavity. Structure 17(2):287-293. doi: S0969-2126(09)00028-8 [pii] 10.1016/j.str.2008.12.012
46. Kanzaki T, Iizuka R, Takahashi K, Maki K, Masuda R, Sahlan M, Yebenes H, Valpuesta JM, Oka T, Furutani M, Ishii N, Kuwajima K, Yohda M (2008) Sequential action of ATP-dependent subunit conformational change and interaction between helical protrusions in the closure of the built-in lid of group II chaperonins. J Biol Chem 283(50):34773-34784. doi: M805303200 [pii] 10.1074/jbc.M805303200
47. Keppel F, Lipinska B, Ang D, Georgopoulos C (1990) Mutational analysis of the phage T4 morphogenetic 31 gene, whose product interacts with the Escherichia coli GroEL protein. Gene 86(1):19-25. doi: 0378-1119(90)90109-5 [pii] (Pubitemid 20082541)
48. Keppel F, Rychner M, Georgopoulos C (2002) Bacteriophage-encoded cochaperonins can substitute for Escherichia coli's essential GroES protein. EMBO Rep 3(9):893-898. doi: 10.1093/embo-reports/kvf176 kvf176 [pii] (Pubitemid 35154117)
49. Kim SK, Kim SR, Kim YH, Kwack P, Son D, Cheong GW (2002) Structural analysis of thermosome from hyperthermophilic archaeon Thermococcus. Mol Cells 14(1):85-92 (Pubitemid 41582984)
50. Klein G, Georgopoulos C (2001) Identification of important amino acid residues that modulate binding of Escherichia coli GroEL to its various cochaperones. Genetics 158(2):507-517 (Pubitemid 32552292)
51. Klumpp M, Baumeister W, Essen LO (1997) Structure of the substrate binding domain of the thermosome, an archaeal group II chaperonin. Cell 91(2):263-270. doi: S0092-8674(00)80408-0 [pii] (Pubitemid 27456393)
52. Knee KM, Goulet DR, Zhang J, Chen B, Chiu W, King JA (2011) The group II chaperonin Mm-Cpn binds and refolds human gammaD crystallin. Protein Sci 20(1):30-41. doi: 10.1002/pro.531
53. Koike-Takeshita A, Shimamura T, Yokoyama K, Yoshida M, Taguchi H (2006) Leu309 plays a critical role in the encapsulation of substrate protein into the internal cavity of GroEL. J Biol Chem 281(2):962-967. doi: M506298200 [pii] 10.1074/jbc.M506298200
54. Koll H, Guiard B, Rassow J, Ostermann J, Horwich AL, Neupert W, Hartl FU (1992) Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell 68(6): 1163-1175. doi: 0092-8674(92)90086-R [pii]
55. Koonin EV, van der Vies SM (1995) Conserved sequence motifs in bacterial and bacteriophage chaperonins. Trends Biochem Sci 20(1):14-15. doi: S0968000400889410 [pii]
56. Kubota S, Kubota H, Nagata K (2006) Cytosolic chaperonin protects folding intermediates of Gbeta from aggregation by recognizing hydrophobic beta-strands. Proc Natl Acad Sci USA 103(22):8360-8365. doi: 0600195103 [pii] 10.1073/pnas.0600195103 (Pubitemid 43838460)
57. Kusmierczyk AR, Martin J (2003a) Nested cooperativity and salt dependence of the ATPase activity of the archaeal chaperonin Mm-cpn. FEBS Lett 547(1-3):201-204. doi: S0014579303007221 [pii] (Pubitemid 36829406)
58. Kusmierczyk AR, Martin J (2003b) Nucleotide-dependent protein folding in the type II chaperonin from the mesophilic archaeon Methanococcus maripaludis . Biochem J 371(Pt 3):669-673 (Pubitemid 36578866)
59. Landry SJ, Zeilstra-Ryalls J, Fayet O, Georgopoulos C, Gierasch LM (1993) Characterization of a functionally important mobile domain of GroES. Nature 364(6434):255-258 (Pubitemid 23257087)
60. Langer T, Pfeifer G, Martin J, Baumeister W, Hartl FU (1992) Chaperonin-mediated protein folding - GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. EMBO J 11(13):4757-4765 (Pubitemid 23023418)
61. Lin Z, Rye HS (2006) GroEL-mediated protein folding: making the impossible, possible. Crit Rev Biochem Mol Biol 41(4):211-239. doi: M315627H22375T33 [pii] 10.1080/10409230600760382 (Pubitemid 44100582)
62. Lin Z, Madan D, Rye HS (2008) GroEL stimulates protein folding through forced unfolding. Nat Struct Mol Biol 15(3):303-311. doi: nsmb.1394 [pii] 10.1038/nsmb.1394 (Pubitemid 351654048)
63. Madan D, Lin Z, Rye HS (2008) Triggering protein folding within the GroEL-GroES complex. J Biol Chem 283(46):32003-32013. doi: M802898200 [pii] 10.1074/jbc.M802898200
64. Martin J, Langer T, Boteva R, Schramel A, Horwich AL, Hartl FU (1991) Chaperonin-mediated protein folding at the surface of groEL through a 'molten globule'-like intermediate. Nature 352(6330):36-42. doi: 10.1038/352036a0 (Pubitemid 21896688)
65. McCormack EA, Llorca O, Carrascosa JL, Valpuesta JM, Willison KR (2001) Point mutations in a hinge linking the small and large domains of beta-actin result in trapped folding intermediates bound to cytosolic chaperonin CCT. J Struct Biol 135(2):198-204. doi: 10.1006/jsbi.2001.4385 S1047-8477(01)94385-0 [pii]
66. Meyer AS, Gillespie JR, Walther D, Millet IS, Doniach S, Frydman J (2003) Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis. Cell 113(3):369-381 (Pubitemid 36556118)
67. Miyazaki T, Yoshimi T, Furutsu Y, Hongo K, Mizobata T, Kanemori M, Kawata Y (2002) GroEL-substrate-GroES ternary complexes are an important transient intermediate of the chaperonin cycle. J Biol Chem 277(52):50621- 50628. doi: 10.1074/jbc.M209183200 M209183200 [pii] (Pubitemid 36042222)
68. Motojima F, Chaudhry C, Fenton WA, Farr GW, Horwich AL (2004) Substrate polypeptide presents a load on the apical domains of the chaperonin GroEL. Proc Natl Acad Sci USA 101(42):15005-15012 (Pubitemid 39391708)
69. Munoz IG, Yebenes H, Zhou M, Mesa P, Serna M, Park AY, Bragado-Nilsson E, Beloso A, de Carcer G, Malumbres M, Robinson CV, Valpuesta JM, Montoya G (2011) Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin. Nat Struct Mol Biol 18(1):14-19. doi: nsmb.1971 [pii] 10.1038/nsmb.1971
70. Murialdo H (1979) Early intermediates in bacteriophage lambda prohead assembly. Virology 96(2):341-367 (Pubitemid 9236676)
71. Nielsen KL, Cowan NJ (1998) A single ring is suffi cient for productive chaperonin-mediated folding in vivo. Mol Cell 2(1):93-99 (Pubitemid 128378970)
72. Nielsen KL, McLennan N, Masters M, Cowan NJ (1999) A single-ring mitochondrial chaperonin (Hsp60-Hsp10) can substitute for GroEL-GroES in vivo. J Bacteriol 181(18):5871-5875 (Pubitemid 29437165)
73. Nitsch M, Walz J, Typke D, Klumpp M, Essen LO, Baumeister W (1998) Group II chaperonin in an open conformation examined by electron tomography. Nat Struct Biol 5(10):855-857 (Pubitemid 28467404)
74. Ohtaka C, Nakamura H, Ishikawa H (1992) Structures of chaperonins from an intracellular symbiont and their functional expression in Escherichia coli groE mutants. J Bacteriol 174(6):1869-1874
75. Pace CN, Shirley BA, McNutt M, Gajiwala K (1996) Forces contributing to the conformational stability of proteins. FASEB J 10(1):75-83 (Pubitemid 26035509)
76. Pappenberger G, Wilsher JA, Roe SM, Counsell DJ, Willison KR, Pearl LH (2002) Crystal structure of the CCTgamma apical domain: implications for substrate binding to the eukaryotic cytosolic chaperonin. J Mol Biol 318(5): 1367-1379. doi: S0022-2836(02)00190-0 [pii] (Pubitemid 34754004)
77. Pereira JH, Ralston CY, Douglas NR, Meyer D, Knee KM, Goulet DR, King JA, Frydman J, Adams PD (2010) Crystal structures of a group II chaperonin reveal the open and closed states associated with the protein folding cycle. J Biol Chem 285(36):27958-27966. doi: M110.125344 [pii] 10.1074/jbc.M110.125344
78. Picketts DJ, Mayanil CS, Gupta RS (1989) Molecular cloning of a Chinese hamster mitochondrial protein related to the "chaperonin" family of bacterial and plant proteins. J Biol Chem 264(20):12001-12008 (Pubitemid 19185375)
79. Ranson NA, Farr GW, Roseman AM, Gowen B, Fenton WA, Horwich AL, Saibil HR (2001) ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107(7):869-879 (Pubitemid 34084978)
80. Reading DS, Hallberg RL, Myers AM (1989) Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor. Nature 337(6208):655-659. doi: 10.1038/337655a0
81. Reissmann S, Parnot C, Booth CR, Chiu W, Frydman J (2007) Essential function of the built-in lid in the allosteric regulation of eukaryotic and archaeal chaperonins. Nat Struct Mol Biol 14(5):432-440 (Pubitemid 46685886)
82. Richardson A, Georgopoulos C (1999) Genetic analysis of the bacteriophage T4-encoded cochaperonin Gp31. Genetics 152(4):1449-1457 (Pubitemid 29370328)
83. Richardson A, van der Vies SM, Keppel F, Taher A, Landry SJ, Georgopoulos C (1999) Compensatory changes in GroEL/Gp31 affi nity as a mechanism for allele-specifi c genetic interaction. J Biol Chem 274(1):52-58 (Pubitemid 29035029)
84. Richardson A, Schwager F, Landry SJ, Georgopoulos C (2001) The importance of a mobile loop in regulating chaperonin/co-chaperonin interaction: humans versus Escherichia coli. J Biol Chem 276(7):4981-4987. doi: 10.1074/jbc. M008628200 M008628200 [pii]
85. Rivenzon-Segal D, Wolf SG, Shimon L, Willison KR, Horovitz A (2005) Sequential ATP-induced allosteric transitions of the cytoplasmic chaperonin containing TCP-1 revealed by EM analysis. Nat Struct Mol Biol 12(3): 233-237. doi: nsmb901 [pii] 10.1038/nsmb901 (Pubitemid 43079364)
86. Roseman AM, Chen S, White H, Braig K, Saibil HR (1996) The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87(2):241-251 (Pubitemid 26359002)
87. Roseman AM, Ranson NA, Gowen B, Fuller SD, Saibil HR (2001) Structures of unliganded and ATP-bound states of the Escherichia coli chaperonin GroEL by cryoelectron microscopy. J Struct Biol 135(2):115-125
88. Rospert S, Junne T, Glick BS, Schatz G (1993) Cloning and disruption of the gene encoding yeast mitochondrial chaperonin 10, the homolog of E. coli groES. FEBS Lett 335(3):358-360. doi: 0014-5793(93)80419-U [pii] (Pubitemid 23355962)
89. Rye HS, Burston SG, Fenton WA, Beechem JM, Xu Z, Sigler PB, Horwich AL (1997) Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388(6644):792-798. doi: 10.1038/42047 (Pubitemid 27375160)
90. Rye HS, Roseman AM, Chen S, Furtak K, Fenton WA, Saibil HR, Horwich AL (1999) GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell 97(3):325-338. doi: S0092-8674(00)80742-4[pii] (Pubitemid 29214589)
91. [pii] Saibil H, Dong Z, Wood S, auf der Mauer A (1991) Binding of chaperonins. Nature 353(6339):25-26. doi: 10.1038/353025b0
92. Saibil HR, Zheng D, Roseman AM, Hunter AS, Watson GM, Chen S, Auf Der Mauer A, O'Hara BP, Wood SP, Mann NH, Barnett LK, Ellis RJ (1993) ATP induces large quaternary rearrangements in a cage-like chaperonin structure. Curr Biol 3(5):265-273. doi: 0960-9822(93)90176-O [pii]
93. Schoehn G, Hayes M, Cliff M, Clarke AR, Saibil HR (2000a) Domain rotations between open, closed and bulletshaped forms of the thermosome, an archaeal chaperonin. J Mol Biol 301(2):323-332. doi: 10.1006/jmbi.2000. 3952S0022-2836(00)93952-4 [pii]
94. Schoehn G, Quaite-Randall E, Jimenez JL, Joachimiak A, Saibil HR (2000b) Three conformations of an archaeal chaperonin, TF55 from Sulfolobus shibatae . J Mol Biol 296(3):813-819. doi: 10.1006/jmbi.2000.3505S0022-2836(00)93505-8 [pii]
95. Sigler PB, Xu Z, Rye HS, Burston SG, Fenton WA, Horwich AL (1998) Structure and function in GroEL-mediated protein folding. Annu Rev Biochem 67, 581-608. doi: 10.1146/annurev.biochem.67.1.581 S0022-2836(00)93952-4 [pii] (Pubitemid 28411139)
96. Spiess C, Meyer AS, Reissmann S, Frydman J (2004) Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol 14(11):598-604 (Pubitemid 39440608)
97. Sternberg N (1973) Properties of a mutant of Escherichia coli defective in bacteriophage lambda head formation (groE). I. Initial characterization. J Mol Biol 76(1):1-23. doi: 0022-2836(73)90078-8 [pii]
98. Thulasiraman V, Yang CF, Frydman J (1999) In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J 18(1):85-95. doi: 10.1093/emboj/18.1.85 (Pubitemid 29005026)
99. Tilly K, Murialdo H, Georgopoulos C (1981) Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis. Proc Natl Acad Sci USA 78(3):1629-1633 (Pubitemid 11114244)
100. Todd MJ, Viitanen PV, Lorimer GH (1994) Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265(5172):659-666 (Pubitemid 24268276)
101. Todd MJ, Walke S, Lorimer G, Truscott K, Scopes RK (1995) The single-ring Thermoanaerobacter brockii chaperonin 60 (Tbr-EL7) dimerizes to Tbr-EL14.Tbr-ES7 under protein folding conditions. Biochemistry 34(45): 14932-14941
102. Valpuesta JM, Martin-Benito J, Gomez-Puertas P, Carrascosa JL, Willison KR (2002) Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS Lett 529(1):11-16. doi: S0014579302031800 [pii] (Pubitemid 35283904)
103. van den Heuvel JF, Verbeek M, van der Wilk F (1994) Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J Gen Virol 75(Pt 10):2559-2565 (Pubitemid 24303171)
104. van der Vies SM, Gatenby AA, Georgopoulos C (1994) Bacteriophage T4 encodes a co-chaperonin that can substitute for Escherichia coli GroES in protein folding. Nature 368(6472):654-656 (Pubitemid 24153392)
105. Viitanen PV, Gatenby AA, Lorimer GH (1992) Purifi ed chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins. Protein Sci 1(3):363-369. doi: 10.1002/pro.5560010308 (Pubitemid 23007303)
106. Viitanen PV, Lorimer G, Bergmeier W, Weiss C, Kessel M, Goloubinoff P (1998) Purifi cation of mammalian mitochondrial chaperonin 60 through in vitro reconstitution of active oligomers. Methods Enzymol 290:203-217 (Pubitemid 28157752)
107. Waldmann T, Nimmesgern E, Nitsch M, Peters J, Pfeifer G, Muller S, Kellermann J, Engel A, Hartl FU, Baumeister W (1995) The thermosome of Thermoplasma acidophilum and its relationship to the eukaryotic chaperonin TRiC. Eur J Biochem 227(3):848-856
108. Weissman JS, Kashi Y, Fenton WA, Horwich AL (1994) Groel-mediated protein-folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78(4):693-702 (Pubitemid 24268591)
109. Weissman JS, Hohl CM, Kovalenko O, Kashi Y, Chen S, Braig K, Saibil HR, Fenton WA, Horwich AL (1995) Mechanism of GroEL action: productive release of polypeptide from a sequestered position under GroES. Cell 83(4):577-587. doi: 0092-8674(95)90098-5 [pii]
110. Weissman JS, Rye HS, Fenton WA, Beechem JM, Horwich AL (1996) Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 84(3):481-490. doi: S0092-8674(00)81293-3 [pii] (Pubitemid 26058572)
111. Xu Z, Sigler PB (1998) GroEL/GroES: structure and function of a two-stroke folding machine. J Struct Biol 124 (2-3): 129-141. doi: S1047-8477(98)94060-6 [pii] 10.1006/jsbi.1998.4060 (Pubitemid 29143055)
112. Xu Z, Horwich AL, Sigler PB (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388(6644):741-750 (Pubitemid 27375147)
113. Yam AY, Xia Y, Lin HT, Burlingame A, Gerstein M, Frydman J (2008) Defi ning the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat Struct Mol Biol 15(12):1255-1262
114. Yifrach O, Horovitz A (1995) Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34(16):5303-5308
115. Zeilstra-Ryalls J, Fayet O, Baird L, Georgopoulos C (1993) Sequence analysis and phenotypic characterization of groEL mutations that block lambda and T4 bacteriophage growth. J Bacteriol 175(4):1134-1143 (Pubitemid 23060152)
116. Zhang J, Baker ML, Schroder GF, Douglas NR, Reissmann S, Jakana J, Dougherty M, Fu CJ, Levitt M, Ludtke SJ, Frydman J, Chiu W (2010) Mechanism of folding chamber closure in a group II chaperonin. Nature 463(7279):379-383
117. Zweig M, Cummings DJ (1973) Cleavage of head and tail proteins during bacteriophage T5 assembly: selective host involvement in the cleavage of a tail protein. J Mol Biol 80(3):505-518