Functional characterization of the recombinant group II chaperonin α from Thermoplasma acidophilum

Journal of Biochemistry

Volumn 143, Issue 4, 2008, Pages 505-515

  Hirai, Hidenori ^a   Noi, Kentaro ^a   Hongo, Kunihiro ^a   Mizobata, Tomohiro ^a   Kawata, Yasushi ^a  

^a TOTTORI UNIVERSITY   (Japan)

Author keywords

Archaeal chaperonin; Chaperonin activity; Metal ion; Protein folding; Thermoplasma acidophilum

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN; CHAPERONIN ALPHA; COBALT; GREEN FLUORESCENT PROTEIN; LUCIFERASE; MAGNESIUM; MANGANESE; RECOMBINANT PROTEIN; THIOSULFATE SULFURTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; THERMOPLASMA ACIDOPHILUM; TRANSMISSION ELECTRON MICROSCOPY;

CHAPERONINS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR WEIGHT; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SPECTROMETRY, FLUORESCENCE; THERMOPLASMA;

ARCHAEA; THERMOPLASMA ACIDOPHILUM; THERMUS;

EID: 41349108000     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvm241     Document Type: Article

References (54)

1. Hartl, F.U. (1996) Molecular chaperones in cellular protein folding. Nature 381, 571-579
2. Hartl, F.U. and Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858
3. Bukau, B. and Horwich, A.L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366
4. Gutsche, I., Essen, L.O., and Baumeister, W. (1999) Group II chaperonins: new TRiC(k)s and turns of a protein folding machine. J. Mol. Biol. 293, 295-312
5. Gething, M.J. and Sambrook, J. (1992) Protein folding in the cell. Nature 355, 33-45
6. Mayhew, M., da Silva, A.C., Martin, J., Erdjument-Bromage, H., Tempst, P., and Hartl, F.U. (1996) Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 379, 420-426
7. Fenton, W.A. and Horwich, A.L. (1997) GroEL-mediated protein folding. Protein Sci. 6, 743-760
8. Chen, H.Y., Chu, Z.M., Ma, Y.H., Zhang, Y., and Yang, S.L. (2007) Expression and characterization of the chaperonin molecular machine from the hyperthermophilic archaeon Pyrococcus furiosus. J. Basic Microbiol. 47, 132-137
9. Okochi, M., Matsuzaki, H., Nomura, T., Ishii, N., and Yohda, M. (2005) Molecular characterization of the group II chaperonin from the hyperthermophilic archaeum Pyrococcus horikoshii OT3. Extremophiles 9, 127-134
10. Kowalski, J.M., Kelly, R.M., Konisky, J., Clark, D.S., and Wittrup, K.D. (1998) Purification and functional characterization of a chaperone from Methanococcus jannaschii. Syst. Appl. Microbiol. 21, 173-178
11. Andrä, S., Frey, G., Nitsch, M., Baumeister, W., and Stetter, K.O. (1996) Purification and structural characterization of the thermosome from the hyperthermophilic archaeum Methanopyrus kandleri. FEBS Lett. 379, 127-131
12. 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, 28399-28407
13. 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
14. Atomi, H., Fukui, T., Kanai, T., Morikawa, M., and Imanaka, T. (2004) Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1, 263-267
15. Izumi, M., Fujiwara, S., Takagi, M., Kanaya, S., and Imanaka, T. (1999) Isolation and characterization of a second subunit of molecular chaperonin from Pyrococcus kodakaraensis KOD1: analysis of an ATPase-deficient mutant enzyme. Appl. Environ. Microbiol. 65, 1801-1805
16. Minuth, T., Frey, G., Lindner, P., Rachel, R., Stetter, K.O., and Jaenicke, R. (1998) Recombinant homo- and hetero-oligomers of an ultrastable chaperonin from the archaeon Pyrodictium occultum show chaperone activity in vitro. Eur. J. Biochem. 258, 837-845
17. Kawarabayasi, Y., Hino, Y., Horikawa, H., Yamazaki, S., Haikawa, Y., Jin-no, K., Takahashi, M., Sekine, M., Baba, S., Ankai, A., Kosugi, H., Hosoyama, A., Fukui, S., Nagai, Y., Nishijima, K., Nakazawa, H., Takamiya, M., Masuda, S., Funahashi, T., Tanaka, T., Kudoh, Y., Yamazaki, J., Kushida, N., Oguchi, A., Aoki, K., Kubota, K., Nakamura, Y., Nomura, N., Sako, Y., and Kikuchi, H. (1999) Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res. 6, 83-101, 145-152.
18. 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
19. Waldmann, T., Nimmesgern, E., Nitsch, M., Peters, J., Pfeifer, G., Müller, S., Kellermann, J., Engel, A., Hartl, F.U., and Baumeister, W. (1995) The thermosome of Thermoplasma acidophilum and its relationship to the eukaryotic chaperonin TRiC. Eur. J. Biochem. 227, 848-856
20. Archibald, J.M., Logsdon, J.M., and Doolittle, W.F. (1999) Recurrent paralogy in the evolution of archaeal chaperonins. Curr. Biol. 9, 1053-1056
21. Farr, G.W., Scharl, E.C., Schumacher, R.J., Sondek, S., and Horwich, A.L. (1997) Chaperonin-mediated folding in the eukaryotic cytosol proceeds through rounds of release of native and nonnative forms. Cell 89, 927-937
22. Feldman, D.E., Thulasiraman, V., Ferreyra, R.G., and Frydman, J. (1999) Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TRiC. Mol. Cell. 4, 1051-1061
23. Valpuesta, J.M., Martín-Benito, J., Gömez-Puertas, P., Carrascosa, J.L., and Willison, K.R. (2002) Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS Lett. 529, 11-16
24. Camasses, A., Bogdanova, A., Shevchenko, A., and Zachariae, W. (2003) The CCT chaperonin promotes activation of the anaphase-promoting complex through the generation of functional Cdc20. Mol. Cell. 12, 87-100
25. Spiess, C., Meyer, A.S., Reissmann, S., and Frydman, J. (2004) Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol. 14, 598-604
26. McClellan, A.J., Scott, M.D., and Frydman, J. (2005) Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121, 739-748
27. Tam, S., Geller, R., Spiess, C., and Frydman, J. (2006) The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions. Nat. Cell Biol. 8, 1155-1162
28. Kubota, S., Kubota, H., and Nagata, K. (2006) Cytosolic chaperonin protects folding intermediates of Gbeta from aggregation by recognizing hydrophobic beta-strands. Proc. Natl. Acad. Sci. USA 103, 8360-8365
29. Behrends, C., Langer, C.A., Boteva, R., Böttcher, U.M., Stemp, M.J., Schaffar, G., Rao, B.V., Giese, A., Kretzschmar, H., Siegers, K., and Hartl, F.U. (2006) Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers. Mol. Cell. 23, 887-897
30. Kitamura, A., Kubota, H., Pack, C.G., Matsumoto, G., Hirayama, S., Takahashi, Y., Kimura, H., Kinjo, M., Morimoto, R.I., and Nagata, K. (2006) Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state. Nat. Cell Biol. 8, 1163-1170
31. Spiess, C., Miller, E.J., McClellan, A.J., and Frydman, J. (2006) Identification of the TRiC/CCT substrate binding sites uncovers the function of subunit diversity in eukaryotic chaperonins. Mol. Cell. 24, 25-37
32. Ditzel, L., Löwe, 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
33. 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
34. Gutsche, I., Holzinger, J., Rössle, M., Heumann, H., Baumeister, W., and May, R.P. (2000) Conformational rearrangements of an archaeal chaperonin upon ATPase cycling. Curr. Biol. 10, 405-408
35. Gutsche, I., Mihalache, O., Hegerl, R., Typke, D., and Baumeister, W. (2000) ATPase cycle controls the conformation of an archaeal chaperonin as visualized by cryo-electron microscopy. FEBS Lett. 477, 278-282
36. 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
37. Bigotti, M.G. and Clarke, A.R. (2005) Cooperativity in the thermosome. J. Mol. Biol. 348, 13-26
38. Bigotti, M.G., Bellamy, S.R., and Clarke, A.R. (2006) The asymmetric ATPase cycle of the thermosome: elucidation of the binding, hydrolysis and product-release steps. J. Mol. Biol. 362, 835-843
39. Waldmann, T., Nitsch, M., Klumpp, M., and Baumeister, W. (1995) Expression of an archaeal chaperonin in E. coli: formation of homo- (alpha, beta) and hetero-oligomeric (alpha+beta) thermosome complexes. FEBS Lett. 376, 67-73
40. Gutsche, I., Mihalache, O., and Baumeister, W. (2000) ATPase cycle of an archaeal chaperonin. J. Mol. Biol. 300, 187-196
41. Dawson, R.M.C., Elliot, D.C., Elliot, W.H., and Jones, K.M. (1986) Data for Biochemical Research, 3rd edn, Clarendon Press, Oxford
42. Lanzetta, P.A., Alvarez, L.J., Reinach, P.S., and Candia, O.A. (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100, 95-97
43. Diamant, S., Azem, A., Weiss, C., and Goloubinoff, P. (1995) Increased efficiency of GroE-assisted protein folding by manganese ions. J. Biol. Chem. 270, 28387-28391
44. Melkani, G.C., Zardeneta, G., and Mendoza, J.A. (2003) The ATPase activity of GroEL is supported at high temperatures by divalent cations that stabilize its structure. Biometals 16, 479-484
45. Hongo, K., Hirai, H., Uemura, C., Ono, S., Tsunemi, J., Higurashi, T., Mizobata, T., and Kawata, Y. (2006) A novel ATP/ADP hydrolysis activity of hyperthermostable group II chaperonin in the presence of cobalt or manganese ion. FEBS Lett. 580, 34-40
46. Son, H.J., Shin, E.J., Nam, S.W., Kim, D.E., and Jeon, S.J. (2007) Properties of the alpha subunit of a chaperonin from the hyperthermophilic Crenarchaeon Aeropyrum pernix K1. FEMS Microbiol. Lett. 266, 103-109
47. Kubo, T., Mizobata, T., and Kawata, Y. (1993) Refolding of yeast enolase in the presence of the chaperonin GroE. The nucleotide specificity of GroE and the role of GroES. J. Biol. Chem. 268, 19346-19351
48. Kawata, Y., Hongo, K., Mizobata, T., and Nagai, J. (1998) Chaperonin GroE-facilitated refolding of disulfide-bonded and reduced Taka-amylase A from Aspergillus oryzae. Protein Eng. 11, 1293-1298
49. +-dependent ATPase activity. Eur. J. Biochem. 255, 93-99
50. Kusmierczyk, A.R. and Martin, J. (2000) High salt-induced conversion of Escherichia coli GroEL into a fully functional thermophilic chaperonin. J. Biol. Chem. 275, 33504-33511
51. Kusmierczyk, A.R. and Martin, J. (2003) Nested cooperativity and salt dependence of the ATPase activity of the archaeal chaperonin Mm-cpn. FEBS Lett. 547, 201-204
52. Stryer, L. (1965) The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites. J. Mol. Biol. 13, 482-495
53. Yoshida, T., Kawaguchi, R., and Maruyama, T. (2002) Nucleotide specificity of an archaeal group II chaperonin from Thermococcus strain KS-1 with reference to the ATP-dependent protein folding cycle. FEBS Lett. 514, 269-274
54. Iizuka, R., Yoshida, T., Shomura, Y., Miki, K., Maruyama, T., Odaka, M., and Yohda, M. (2003) ATP binding is critical for the conformational change from an open to closed state in archaeal group II chaperonin. J. Biol. Chem. 278, 44959-44965