The Chaperones of the archaeon Thermoplasma acidophilum

Journal of Structural Biology

Volumn 135, Issue 2, 2001, Pages 126-138

  Ruepp, Andreas ^a,c   Rockel, Beate ^a,d   Gutsche, Irina ^a   Baumeister, Wolfgang ^a   Lupas, Andrei N ^b,e  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b GLAXOSMITHKLINE   (United States)

^c Epidauros Biotechnologie AG   (Germany)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Archaea; Chaperone; Thermoplasma; Thermosome; VAT

Indexed keywords

CHAPERONE; PROTEIN;

ARCHAEBACTERIUM; ARTICLE; EUKARYOTE; GENE SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; THERMOPLASMA ACIDOPHILUM; UNINDEXED SEQUENCE;

ARCHAEA; EUKARYOTA; THERMOPLASMA; THERMOPLASMA ACIDOPHILUM;

EID: 0035783399     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.2001.4402     Document Type: Article

References (102)

1. Akiyama, Y., Ehrmann, M., Kihara, A., and Ito, K. (1998) Polypeptide binding of Escherichia coli FtsH (HflB). Mol. Microbiol. 28, 803-812.
2. Archibald, J. M., Logsdon, J. M., and Doolittle, W. F. (1999) Recurrent paralogy in the evolution of archaeal chaperonins. Curr. Biol. 9, 1053-1056.
3. Babor, S. M., and Fass, D. (1999) Crystal structure of the Sec18p N-terminal domain. Proc. Natl. Acad. Sci. USA 96, 14759-14764.
4. Banuett, F., Hoyt, M. A., McFarlane, L., Echols, H., and Herskowitz, I. (1986) Hflb, a new Escherichia coli locus regulating lysogeny and the level of bacteriophage lambda-cII protein. J. Mol. Biol. 187, 213-224.
5. Benaroudj, N., and Goldberg, A. L. (2000) PAN, the proteasome-activating nucleotidase from archaebacteria, is a protein-unfolding molecular chaperone. Nat. Cell. Biol. 2, 833-839.
6. Beyer, A. (1997) Sequence analysis of the AAA protein family. Protein Sci. 6, 2043-2058.
7. Bosch, G., Baumeister, W., and Essen, L. O. (2000) Crystal structure of the beta-apical domain of the thermosome reveals structural plasticity in the protrusion region. J. Mol. Biol. 301, 19-25.
8. Bukau, B., and Horwich, A. L. (1998) The HSP70 and HSP60 chaperone machines. Cell 92, 351-366.
9. Bult, C. J., White, O., Olsen, G. J., Zhou, L. X., Fleischmann, R. D., Sutton, G. G., Blake, J. A., Fitzgerald, L. M., Clayton, R. A., Gocayne, J. D., Kerlavage, A. R., Dougherty, B. A., Tomb, J. F., Adams, M. D., Reich, C. I., Overbeek, R., Kirkness, E. F., Weinstock, K. G., Merrick, J. M., Glodek, A., Scott, J. L., Geoghagen, N. S. M., Weidman, J. F., Fuhrmann, J. L., Nguyen, D., Venter, J. C., et al. (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 1058-1073.
10. Castillo, R. M., Mizuguchi, K., Dhanaraj, V., Albert, A., Blundell, T. L., and Murzin, A. G. (1999) A six-stranded double-psi beta barrel is shared by several protein superfamilies. Structure 7, 227-236.
11. Chin, D. T., Goff, S. A., Webster, T., Smith, T., and Goldberg, A. L. (1988) Sequence of the lon gene in Escherichia coli: A heat-shock gene which encodes the ATP-dependent protease La. J. Biol. Chem. 263, 11 718-11 728.
12. Clarens, M., Macario, A. J. L., and Demacario, E. C. (1995) The archaeal dnaK-dnaJ gene-cluster: Organization and expression in the methanogen Methanosarcina mazei. J. Mol. Biol. 250, 191-201.
13. Coles, M., Diercks, T., Liermann, J., Gröger, A., Rockel, B., Baumeister, W., Koretke, K. K., Lupas, A., Peters, J., and Kessler, H. (1999) The solution structure of VAT-N reveals a "missing link" in the evolution of complex enzymes from a simple βαββ element. Curr. Biol. 9, 1158-1168.
14. Confalonieri, F., and Duguet, M. (1995) A 200-amino acid ATPase module in search of a basic function. BioEssays 17, 639-650.
15. Ditzel, L., Lowe, J., Stock, D., Stetter, K. O., Huber, H., Huber, R., and Steinbacher, S. (1998) Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93, 125-138.
16. Dolinski, K., Muir, S., Cardenas, M., and Heitman, J. (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94, 13 093-13 098.
17. Ellis, R. J., van der Vies, S. M., and Hemmingsen, S. M. (1989) The molecular chaperone concept. Biochem. Soc. Symp. 55, 145-153.
18. Fröhlich, K. U., Fries, H. W., Peters, J. M., and Mecke, D. (1995) The ATPase activity of purified CDC48p from Saccharomyces cerevisiae shows complex dependence on ATP-, ADP-, and NADH-concentrations and is completely inhibited by NEM. Biochim. Biophys. Acta 1253, 25-32.
19. Frydman, J., Nimmesgern, E., Erdjument-Bromage, H., Wall, J. S., Tempst, P., and Hartl, F. U. (1992) Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. EMBO J. 11, 4767-4778.
20. Furutani, M., Iida, T., Yoshida, T., and Maruyama, T. (1998) Group II chaperonin in a thermophilic methanogen, Methanococcus thermolithotrophicus - Chaperone activity and filament-forming ability. J. Biol. Chem. 273, 28 399-28 407.
21. Gao, Y., Thomas, J. O., Chow, R. L., Lee, G. H., and Cowan, N. J. (1992) A cytoplasmic chaperonin that catalyzes β-actin folding. Cell 69, 1043-1050.
22. Geissler, S., Siegers, K., and Schiebel, E. (1998) A novel protein complex promoting formation of functional α- and γ-tubulin. EMBO J. 17, 952-966.
23. Gething, M. J. (1999) Role and regulation of the ER chaperone BiP. Semin. Cell Dev. Biol. 10, 465-472.
24. Ghislain, M., Dohmen, R. J., Levy, F., and Varshavsky, A. (1996) Cdc48p interacts with Ufd3p, a WD repeat protein required for ubiquitin-mediated proteolysis in Saccharomyces cerevisiae. EMBO J. 15, 4884-4899.
25. Golbik, R., Lupas, A. N., Koretke, K. K., Baumeister, W., and Peters, J. (1999) The Janus face of the archaeal Cdc48/p97 homologue VAT: Protein folding versus unfolding. Biol. Chem. 380, 1049-1062.
26. Goldberg, A. L. (1992) The mechanism and functions of ATP-dependent proteases in bacterial and animal cells. Eur. J. Biochem. 203, 9-23.
27. Goldberg, A. L., Moerschell, R. P., Chung, C. H., and Maurizi, M. R. (1994) ATP-dependent protease La (lon) from Escherichia coli. Methods Enzymol. 244, 350-375.
28. Gottesman, S., Wickner, S., Jubete, Y., Singh, S. K., Kessel, M., and Maurizi, M. (1995) Selective, energy-dependent proteolysis in Escherichia coli. Cold Spring Harbor Symp. Quant. Biol. 60, 533-548.
29. Guagliardi, A., Cerchia, L., Bartolucci, S., and Rossi, M. (1994) The chaperonin from the archaeon Sulfolobus solfataricus promotes correct refolding and prevents thermal denaturation in vitro. Protein Sci. 3, 1436-1443.
30. Guagliardi, A., Cerchia, L., and Rossi, M. (1995) Prevention of in vitro protein thermal aggregation by the Sulfolobus solfataricus chaperonin. Evidence for nonequivalent binding surfaces on the chaperonin molecule. J. Biol. Chem. 270, 28 126-28 132.
31. Gutsche, I., Holzinger, J., Rößle, M., Heumann, H., Baumeister, W., and May, R. P. (2000a) Conformational rearrangements of an archaeal chaperonin upon ATPase cycling. Curr. Biol. 10, 405-409.
32. Gutsche, I., Mihalache, O., and Baumeister, W. (2000b) ATPase cycle of an archaeal chaperonin. J. Mol. Biol. 300, 187-196.
33. Gutsche, I., Holzinger, J., Rauh, N., Baumeister, W., and May, R. P. (2001) ATP-induced structural change of the thermosome is temperature-dependent. J. Struct. Biol. 135, 139-146, doi: 10.1006/jsbi.2001.4373.
34. Hansen, W. J., Cowan, N. J., and Welch, W. J. (1999) Prefoldinnascent chain complexes in the folding of cytoskeletal proteins. J. Cell Biol. 145, 265-277.
35. Hanson, P. I., Roth, R., Morisaki, H., Jahn, R., and Heuser, J. E. (1997) Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deepetch electron microscopy. Cell 90, 523-535.
36. Hartl, F. U. (1996) Molecular chaperones in cellular protein folding. Nature 381, 571-579.
37. Haslbeck, M., Walke, S., Stromer, T., Ehrnsperger, M., White, H. E., Chen, S. X., Saibil, H. R., and Buchner, J. (1999) Hsp26: A temperature-regulated chaperone. EMBO J. 18, 6744-6751.
38. Hendrix, R. W. (1979) Purification and properties of groE, a host protein involved in bacteriophage assembly. J. Mol. Biol. 129, 375-392.
39. Herman, C., Ogura, T., Tomoyasu, T., Hiraga, S., Akiyama, Y., Ito, K., Thomas, R., Dari, R., and Bouloc, P. (1993) Cell-growth and lambda-phage development controlled by the same essential Escherichia coli gene, Ftsh Hflb. Proc. Natl. Acad. Sci. USA 90, 10 861-10 865.
40. Hohn, T., Hohn, B., Engel, A., Wurtz, M., and Smith, P. R. (1979) Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. J. Mol. Biol. 129, 359-373.
41. Holmgren, A., Soderberg, B. O., Eklund, H., and Branden, C. I. (1975) 3-Dimensional structure of Escherichia coli thioredoxin-S2 to 2.8 Å resolution. Proc. Natl. Acad. Sci. USA 72, 2305-2309.
42. Horwich, A. L., and Saibil, H. R. (1998) The thermosome: Chaperonin with a built-in lid. Nat. Struct. Biol. 5, 333-336.
43. Ideno, A., Yoshida, T., Furutani, M., and Maruyama, T. (2000) The 28.3 kDa FK506 binding protein from a thermophilic archaeum, Methanobacterium thermoautotrophicum, protects the denaturation of proteins in vitro. Eur. J. Biochem. 267, 3139-3148.
44. Kaminska, M., Deniziak, M., Kerjan, P., Barciszewski, J., and Mirande, M. (2000) A recurrent general RNA binding domain appended to plant methionyl-tRNA synthetase acts as a cis-acting cofactor for aminoacylation. EMBO J. 19, 6908-6917.
45. Kawaguchi, S., Muller, J., Linde, D., Kuramitsu, S., Shibata, T., Inoue, Y., Vassylyev, D. G., and Yokoyama, S. (2001) The crystal structure of the ttCsaA protein: An export-related chaperone from Thermus thermophilus. EMBO J. 20, 562-569.
46. Kim, K. K., Kim, R., and Kim, S. H. (1998a) Crystal structure of a small heat-shock protein. Nature 394, 595-599.
47. Kim, R., Kim, K. K., Yokota, H., and Kim, S. H. (1998b) Small heat shock protein of Methanococcus jannaschii, a hyperthermophile. Proc. Natl. Acad. Sci. USA 95, 9129-9133.
48. Klumpp, M., Baumeister, W., and Essen, L. O. (1997) Structure of the substrate binding domain of the thermosome, an archaeal group II chaperonin. Cell 91, 263-270.
49. Koegl, M., Hoppe, T., Schlenker, S., Ulrich, H. D., Mayer, T. U., and Jentsch, S. (1999) A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 96, 635-644.
50. Kubota, H., Hynes, G., Carne, A., Ashworth, A., and Willison, K. (1994) Identification of six Tcp-1-related genes encoding divergent subunits of the TCP-1-containing chaperonin. Curr. Biol. 4, 89-99.
51. Lee, G. J., Roseman, A. M., Saibil, H. R., and Vierling, E. (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J. 16, 659-671.
52. Leroux, M. R., Fandrich, M., Klunker, D., Siegers, K., Lupas, A. N., Brown, J. R., Schiebel, E., Dobson, C. M., and Hartl, F. U. (1999) MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. EMBO J. 18, 6730-6743.
53. Lewis, V. A., Hynes, G. M., Zheng, D., Saibil, H., and Willison, K. (1992) T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukaryotic cytosol. Nature 358, 249-252.
54. Lupas, A., Flanagan, J. M., Tamura, T., and Baumeister, W. (1997) Self-compartmentalizing proteases. Trends Biochem. Sci. 22, 399-404.
55. Macario, A. J., and Conway De Macario, E. (2001) The molecular chaperone system and other anti-stress mechanisms in archaea. Front. Biosci. 6, D262-E283.
56. Macario, A. J., Lange, M., Ahring, B. K., and De Macario, E. C. (1999) Stress genes and proteins in the archaea. Microbiol. Mol. Biol. Rev. 63, 923-967.
57. Maruyama, T., and Furutani, M. (2000) Archaeal peptidyl prolyl cis-trans isomerases (PPIases). Front. Biosci. 5, D821-D836.
58. May, A. P., Misura, K. M. S., Whiteheart, S. W., and Weis, W. I. (1999) Crystal structure of the amino-terminal domain of N-ethylmaleimide-sensitive fusion protein. Nat. Cell Biol. 1, 175-182.
59. Moore, J. M., Peattie, D. A., Fitzgibbon, M. J., and Thomson, J. A. (1991) Solution structure of the major binding-protein for the immunosuppressant FK506. Nature 351, 248-250.
60. Morales, A. J., Swairjo, M. A., and Schimmel, P. (1999) Structure-specific tRNA-binding protein from the extreme thermophile Aquifex aeolicus. EMBO J. 18, 3475-3483.
61. Muller, J., Walter, F., Vandijl, J. M., and Behnke, D. (1992) Suppression of the growth and export defects of an Escherichia coli secA(Ts) mutant by a gene cloned from Bacillus subtilis. Mol. Gen. Genet. 235, 89-96.
62. Muller, J. P., Ozegowski, J., Vettermann, S., Swaving, J., van Wely, K. H. M., and Driessen, A. J. M. (2000) Interaction of Bacillus subtilis CsaA with SecA and precursor proteins. Biochem. J. 348, 367-373.
63. Nagashima, K., Mitsuhashi, S., Kamino, K., and Maruyama, T. (1994) Cyclosporine A sensitive peptidyl-prolyl cis-trans isomerase in a halophilic archaeum, Halobacterium cutirubrum. Biochem. Biophys. Res. Commun. 198, 466-472.
64. Neuwald, A. F., Aravind, L., Spouge, J. L., and Koonin, E. V. (1999) AAA(+): A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43.
65. Nitsch, M., Klumpp, M., Lupas, A., and Baumeister, W. (1997) The thermosome: Alternating alpha and beta-subunits within the chaperonin of the archaeon Thermoplasma acidophilum. J. Mol. Biol. 267, 142-149.
66. Pamnani, V., Tamura, T., Lupas, A., Peters, J., Cejka, Z., Ashraf, W., and Baumeister, W. (1997) Cloning, sequencing and expression of VAT, a CDC48/p97 ATPase homologue from the archaeon Thermoplasma acidophilum. FEBS Lett. 404, 263-268.
67. Patel, S., and Latterich, M. (1998) The AAA team: Related ATPases with diverse functions. Trends Cell Biol. 8, 65-71.
68. Peters, J. M., Harris, J. R., Lustig, A., Muller, S., Engel, A., Volker, S., and Franke, W. W. (1992) Ubiquitous soluble Mg(2+)-ATPase complex. A structural study. J. Mol. Biol. 223, 557-571.
69. Phipps, B. M., Hoffmann, A., Stetter, K. O., and Baumeister, W. (1991) A novel ATPase complex selectively accumulated upon heat shock is a major cellular component of thermophilic archaebacteria. EMBO J. 10, 1711-1722.
70. Rep, M., van Dijl, J. M., Suda, K., Schatz, G., Grivell, L. A., and Suzuki, C. K. (1996) Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast. Science 274, 103-106.
71. Rockel, B., Walz, J., Hegerl, R., Peters, J., Typke, D., and Baumeister, W. (1999) Structure of VAT, a CDC48/p97 ATPase homologue from the archaeon Thermoplasma acidophilum as studied by electron tomography. FEBS Lett. 451, 27-32.
72. Rouiller, I., Butel, V. M., Latterich, M., Milligan, R. A., and Wilson-Kubalek, E. M. (2000) A major conformational change in p97 AAA ATPase upon ATP binding. Mol. Cell 6, 1485-1490.
73. Ruepp, A., Graml, W., Santos-Martinez, M. L., Koretke, K. K., Volker, C., Mewes, H. W., Frishman, D., Stocker, S., Lupas, A. N., and Baumeister, W. (2000) The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407, 508-513.
74. Schoehn, G., Hayes, M., Cliff, M., Clarke, A. R., and Saibil, H. R. (2000) Domain rotations between open, closed and bullet-shaped forms of the thermosome, an archaeal chaperonin. J. Mol. Biol. 301, 323-332.
75. Siegers, K., Waldmann, T., Leroux, M. R., Grein, K., Shevchenko, A., Schiebel, E., and Hartl, F. U. (1999) Compartmentation of protein folding in vivo: Sequestration of non-native polypeptide by the chaperonin-GimC system. EMBO J. 18, 75-84.
76. Siegert, R., Leroux, M. R., Scheufler, C., Hartl, F. U., and Moarefi, I. (2000) Structure of the molecular chaperone prefoldin: Unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell 103, 621-632.
77. Smith, D. R., Doucettestamm, L. A., Deloughery, C., Lee, H. M., Dubois, J., Aldredge, T., Bashirzadeh, R., Blakely, D., Cook, R., Gilbert, K., Harrison, D., Hoang, L., Keagle, P., Lumm, W., Pothier, B., Qiu, D. Y., Spadafora, R., Vicaire, R., Wang, Y., Wierzbowski, J., Gibson, R., Jiwani, N., Caruso, A., Bush, D., Safer, H., et al. (1997) Complete genome sequence of Methanobacterium thermoautotrophicum delta-H: Functional analysis and comparative genomics. J. Bacteriol. 179, 7135-7155.
78. Smykal, P., Hrdy, I., and Pechan, P. M. (2000) High-molecular-mass complexes formed in vivo contain smHSPs and HSP70 and display chaperone-like activity. Eur. J. Biochem. 267, 2195-2207.
79. Stahlberg, H., Kutejova, E., Suda, K., Wolpensinger, B., Lustig, A., Schatz, G., Engel, A., and Suzuki, C. K. (1999) Mitochondrial Lon of Saccharomyces cerevisiae is a ring-shaped protease with seven flexible subunits. Proc. Natl. Acad. Sci. USA 96, 6787-6790.
80. Steinbacher, S., and Ditzel, L. (2001) Review: Nucleotide binding to the thermoplasma thermosome: Implications for the functional cycle of group II chaperonins. J. Struct. Biol. 135, 147-156, doi:10.1006/jsbi2001.4382.
81. Swairjo, M. A., Morales, A. J., Wang, C. C., Ortiz, A. R., and Schimmel, P. (2000) Crystal structure of Trbp111: A structure-specific tRNA-binding protein. EMBO J. 19, 6287-6298.
82. Swamy, K. H., and Goldberg, A. L. (1981) E. coli contains eight soluble proteolytic activities, one being ATP dependent. Nature 292, 652-654.
83. Teter, S. A., Houry, W. A., Ang, D., Tradler, T., Rockabrand, D., Fischer, G., Blum, P., Georgopoulos, C., and Hartl, F. U. (1999) Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97, 755-765.
84. Tomoyasu, T., Gamer, J., Bukau, B., Kanemori, M., Mori, H., Rutman, A., Oppenheim, A., Yura, T., Yamanaka, K., Niki, H., et al. (1995) Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J. 14, 2551-2560.
85. Tomoyasu, T., Yuki, T., Morimura, S., Mori, H., Yamanaka, K., Niki, H., Hiraga, S., and Ogura, T. (1993) The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J. Bacteriol. 175, 1344-1351.
86. Trent, J. D., Nimmesgern, E., Wall, J. S., Hartl, F. U., and Horwich, A. L. (1991) A molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide-1. Nature 354, 490-493.
87. Vainberg, I. E., Lewis, S. A., Rommelaere, H., Ampe, C., Vandekerckhove, J., Klein, H. L., and Cowan, N. J. (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93, 863-873.
88. Vale, R. D. (2000) AAA proteins. Lords of the ring. J. Cell Biol. 150, F13-F20.
89. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L., and Clardy, J. (1991) Atomic-structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science 252, 839-842.
90. Veinger, L., Diamant, S., Buchner, J., and Goloubinoff, P. (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273, 11 032-11 037.
91. Weaver, A. J., Sullivan, W. P., Felts, S. J., Owen, B. A. L., and Toft, D. O. (2000) Crystal structure and activity of human p23, a heat shock protein 90 co-chaperone. J. Biol. Chem. 275, 23045-23052.
92. Weber-Ban, E. U., Reid, B. G., Miranker, A. D., and Horwich, A. L. (1999) Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 401, 90-93.
93. Wickner, S., Maurizi, M. R., and Gottesman, S. (1999) Posttranslational quality control: Folding, refolding, and degrading proteins. Science 286, 1888-1893.
94. Wilson, H. L., Ou, M. S., Aldrich, H. C., and Maupin-Furlow, J. (2000) Biochemical and physical properties of the Methanococcus jannaschii 20S proteasome and PAN, a homolog of the ATPase (Rpt) subunits of the eucaryal 26S proteasome. J. Bacteriol. 182, 1680-1692.
95. 7 chaperonin complex. Nature 388, 741-750.
96. Yifrach, O., and Horovitz, A. (1995) Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34, 5303-5308.
97. Yoshida, T., Yohda, M., Iida, T., Maruyama, T., Taguchi, H., Yazaki, K., Ohta, T., Odaka, M., Endo, I., and Kagawa, Y. (1997) Structural and functional characterization of homo-oligomeric complexes of alpha and beta chaperonin subunits from the hyperthermophilic archaeum Thermococcus strain KS-1. J. Mol. Biol. 273, 635-645.
98. Yoshida T., Ideno, A., Hiyamuta, S., Yohda, M., and Maruyama, T. (2001) Natural chaperonin of the hyperthermophilic archaeum, Thermococcus strain KS-1: A hetero-oligomeric chaperonin with variable subunit composition. Mol. Microbiol. 39, 1406-1413.
99. Yu, R. C., Jahn, R., and Brunger, A. T. (1999) NSF N-terminal domain crystal structure: Models of NSF function. Mol. Cell 4, 97-107.
100. Zhang, X. D., Shaw, A., Bates, P. A., Newman, R. H., Gowen, B., Orlova, E., Gorman, M. A., Kondo, H., Dokurno, P., Lally, J., Leonard, G., Meyer, H., van Heel, M., and Freemont, P. S. (2000) Structure of the AAA ATPase p97. Mol. Cell 6, 1473-1484.
101. Zwickl, P., and Baumeister, W. (1999) AAA-ATPases at the crossroads of protein life and death. Nat. Cell. Biol. 1, E97-E98.
102. Zwickl, P., Ng, D., Woo, K. M., Klenk, H. P., and Goldberg, A. L. (1999) An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26 S proteasome, activates protein breakdown by 20 S proteasomes. J. Biol. Chem. 274, 26008-26014.