Gene duplication and the evolution of group II chaperonins: Implications for structure and function

Journal of Structural Biology

Volumn 135, Issue 2, 2001, Pages 157-169

  Archibald, John M ^a   Blouin, Christian ^a   Doolittle, W Ford ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Archaea; CCT; Chaperonins; Eukaryotes; Evolution; Gene duplication; TF55; Thermosome; TriC

Indexed keywords

AMINO ACID; CHAPERONIN; CHAPERONIN I; CHAPERONIN II; GENE PRODUCT; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARCHAEBACTERIUM; ARTICLE; BACTERIUM; CELL ORGANELLE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; EUKARYOTE; GENE DUPLICATION; GENETIC CODE; GENOME; MOLECULE; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; THERMOPLASMA ACIDOPHILUM;

ARCHAEA; EUKARYOTA; THERMOPLASMA ACIDOPHILUM;

EID: 0035783161     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.2001.4353     Document Type: Article

References (68)

1. Adachi, J. M., and Hasegawa, M. (1996) MOLPHY version 2.3: Programs for molecular phylogenetics based on maximum likelihood, Comput. Sci. Monogr. 28, 1-150.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs, Nucleic Acids Res. 25, 3389-3402.
3. Archibald, J. M., Cavalier-Smith, T., Maier, U., and Douglas, S. (2001) Molecular chaperones encoded by a reduced nucleus: The cryptomonad nucleomorph, J. Mol. Evol. 52, 490-501.
4. Archibald, J. M., Logsdon, J. M., and Doolittle, W. F. (1999) Recurrent paralogy in the evolution of archaeal chaperonins, Curr. Biol. 9, 1053-1056.
5. Archibald, J. M., Logsdon, J. M., Jr., and Doolittle, W. F. (2000) Origin and evolution of eukaryotic chaperonins: Phylogenetic evidence for ancient duplications in CCT genes, Mol. Biol. Evol. 17, 1456-1466.
6. 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.
7. Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D. C., Joachimiak, A., Horwich, A. L., and Sigler, P. B. (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 Å, Nature 371, 578-586.
8. Bukau, B., and Horwich, A. L. (1998) The Hsp70 and Hsp60 chaperone machines, Cell 92, 351-366.
9. Cavalier-Smith, T. (1987) Eukaryotes with no mitochondria, Nature 326, 332-333.
10. 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.
11. 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.
12. 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.
13. Felsenstein, J. (1995) PHYLIP (Phylogeny Inference Package). Distributed by the author, Department of Genetics, University of Washington, Seattle.
14. 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.
15. Gebauer, M., Melki, R., and Gehring, U. (1998) The chaperone cofactor Hop/p60 interacts with the cytosolic chaperonin-containing TCP-1 and affects its nucleotide exchange and protein folding activities, J. Biol. Chem. 273, 29475-29480.
16. 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.
17. Gilson, P. R., Maier, U. G., and McFadden, G. I. (1997) Size isn't everything: Lessons in genetic miniaturisation from nucleomorphs, Curr. Opin. Genet. Dev. 7, 800-806.
18. 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.
19. Hartl, F. U. (1996) Molecular chaperones in cellular protein folding, Nature 381, 571-579.
20. Hashimoto, T., Nakamura, Y., Nakamura, F., Shirakura, T., Adachi, J., Goto, N., Okamoto, K., and Hasegawa, M. (1994) Protein phylogeny gives a robust estimation for early divergences of eukaryotes: Phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia, Mol. Biol. Evol. 11, 65-71.
21. Horwich, A. L., and Saibil, H. R. (1998) The thermosome: Chaperonin with a built-in lid, Nat. Struct. Biol. 5, 333-336.
22. Houry, W. A., Frishman, D., Eckerskorn, C., Lottspeich, F., and Hartl, F. U. (1999) Identification of in vivo substrates of the chaperonin GroEL, Nature 402, 147-154.
23. Hynes, G., Kubota, H., and Willison, K. R. (1995) Antibody characterisation of two distinct conformations of the chaperonin-containing TCP-1 from mouse testis, FEBS Lett. 358, 129-132.
24. Kawarabayasi, Y., Hino, Y., Horikawa, H., Yamazaki, S., Haikawa, Y., Jinno, 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., Kikuchi, H., et al. (1999) Complete genome sequence of an aerobic hyperthermophilic crenarchaeon, Aeropyrum pernix K1, DNA Res. 6, 83-101, 145-152.
25. Kawashima, T., Amano, N., Koike, H., Makino, S., Higuchi, S., Kawashima-Ohya, Y., Watanabe, K., Yamazaki, M., Kanehori, K., Kawamoto, T., Nunoshiba, T., Yamamoto, Y., Aramaki, H., Makino, K., and Suzuki, M. (2000) Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium, Proc. Natl. Acad. Sci. USA 97, 14257-14262.
26. Keeling, P. J., Deane, J. A., Hink-Schauer, C., Douglas, S. E., Maier, U. G., and McFadden, G. I. (1999) The secondary endosymbiont of the cryptomonad Guillardia theta contains alpha-, beta-, and gamma-tubulin genes, Mol. Biol. Evol. 16, 1308-1313.
27. Keeling, P. J., and Doolittle, W. F. (1996) Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family, Mol. Biol. Evol. 13, 1297-1305.
28. Kim, S., Willison, K. R., and Horwich, A. L. (1994) Cystosolic chaperonin subunits have a conserved ATPase domain but diverged polypeptide-binding domains, Trends. Biochem. Sci. 19, 543-548.
29. Klumpp, M., and Baumeister, W. (1998) The thermosome: Archetype of group II chaperonins, FEBS Lett. 430, 73-77.
30. 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.
31. 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.
32. Kubota, H., Hynes, G., and Willison, K. (1995a) The chaperonin containing t-complex polypeptide 1 (TCP-1). Multisubunit machinery assisting in protein folding and assembly in the eukaryotic cytosol, Eur. J. Biochem. 230, 3-16.
33. Kubota, H., Hynes, G., and Willison, K. (1995b) The eighth Cct gene, Cctq, encoding the theta subunit of the cytosolic chaperonin containing TCP-1, Gene 154, 231-236.
34. Kubota, H., Hynes, G. M., Kerr, S. M., and Willison, K. R. (1997) Tissue-specific subunit of the mouse cytosolic chaperonin-containing TCP-1, FEBS Lett. 402, 53-56.
35. Leipe, D. D., Gunderson, J. H., Nerad, T. A., and Sogin, M. L. (1993) Small subunit ribosomal RNA1 of Hexamita inflata and the quest for the first branch in the eukaryotic tree, Mol. Biochem. Parasitol. 59, 41-48.
36. Leroux, M. R., and Hartl, F. U. (2000) Protein folding: Versatility of the cytosolic chaperonin TRiC/CCT, Curr. Biol. 10, R260-R264.
37. 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.
38. Lin, P., Cardillo, T. S., Richard, L. M., Segel, G. B., and Sherman, F. (1997) Analysis of mutationally altered forms of the Cct6 subunit of the chaperonin from Saccharomyces cerevisiae, Genetics 147, 1609-1633.
39. Liou, A. K., and Willison, K. R. (1997) Elucidation of the subunit orientation in CCT (chaperonin containing TCP1) from the subunit composition of CCT micro-complexes, EMBO J. 16, 4311-4316.
40. Llorca, O., Martin-Benito, J., Ritco-Vonsovici, M., Grantham, J., Hynes, G. M., Willison, K. R., Carrascosa, J. L., and Valpuesta, J. M. (2000) Eukaryotic chaperonin CCT stabilizes actin and tubulin folding intermediates in open quasi-native conformations, EMBO J. 19, 5971-5979.
41. Llorca, O., McCormack, E. A., Hynes, G., Grantham, J., Cordell, J., Carrascosa, J. L., Willison, K. R., Fernandez, J. J., and Valpuesta, J. M. (1999) Eukaryotic type II chaperonin CCT interacts with actin through specific subunits, Nature 402, 693-696.
42. Melki, R., Batelier, G., Soulie, S., and Williams, R. C., Jr. (1997) Cytoplasmic chaperonin containing TCP-1: Structural and functional characterization, Biochemistry 36, 5817-5826.
43. Miklos, D., Caplan, S., Mertens, D., Hynes, G., Pitluk, Z., Kashi, Y., Harrison-Lavoie, K., Stevenson, S., Brown, C., Barrell, B., Horwich, A. L., and Willison, K. (1994) Primary structure and function of a second essential member of the heterooligomeric TCP1 chaperonin complex of yeast, TCP1β, Proc. Natl. Acad. Sci. USA 91, 2743-2747.
44. Ng, W. V., Kennedy, S. P., Mahairas, G. G., Berquist, B., Pan, M., Shukla, H. D., Lasky, S. R., Baliga, N. S., Thorsson, V., Sbrogna, J., Swartzell, S., Weir, D., Hall, J., Dahl, T. A., Welti, R., Goo, Y. A., Leithauser, B., Keller, K., Cruz, R., Danson, M. J., Hough, D. W., Maddocks, D. G., Jablonski, P. E., Krebs, M. P., Angevine, C. M., and Dale, H. (2000) Genome sequence of Halobacterium species NRC-1, Proc. Natl. Acad. Sci. USA 97, 12176-12181.
45. 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.
46. 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.
47. Phipps, B. M., Typke, D., Hegerl, R., Volker, S., Hoffmann, A., Stetter, K. O., and Baumeister, W. (1993) Structure of a molecular chaperone from a thermophilic archaebacterium, Nature 361, 475-477.
48. Ranson, N. A., White, H. E., and Saibil, H. R. (1998) Chaperonins, Biochem. J. 333, 233-242.
49. Ritco-Vonsovici, M., and Willison, K. R. (2000) Defining the eukaryotic cytosolic chaperonin-binding sites in human tubulins, J. Mol. Biol. 304, 81-98.
50. Roger, A. J. (1999) Reconstructing early events in eukaryotic evolution, Am. Nat. 154 (Suppl.), S146-S163.
51. Rommelaere, H., Van Troys, M., Gao, Y., Melki, R., Cowan, N. J., Vandekerckhove, J., and Ampe, C. (1993) Eukaryotic cytosolic chaperonin contains t-complex polypeptide 1 and seven related subunits, Proc. Natl. Acad. Sci. USA 90, 11975-11979.
52. Siegers, K., Waldmann, T., Leroux, M. R., Grein, K., Shevchenko, A., Schiebel, E., and Hartl, F. U. (1999) Compartmentalization of protein folding in vivo: Sequestration of non-native polypeptide by the chaperonin-GimC system, EMBO J. 18, 75-84.
53. 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.
54. Sigler, P. B., Xu, Z., Rye, H. S., Burston, S. G., Fenton, W. A., and Horwich, A. L. (1998) Structure and function in GroEL-mediated protein folding, Annu. Rev. Biochem. 67, 581-608.
55. Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A., and Peattie, D. A. (1989) Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia, Science 243, 75-77.
56. Stiller, J. W., Duffield, E. C., and Hall, B. D. (1998) Amitochondriate amoebae and the evolution of DNA-dependent RNA polymerase II, Proc. Natl. Acad. Sci. USA 95, 11769-11774.
57. Stoldt, V., Rademacher, F., Kehren, V., Ernst, J. F., Pearce, D. A., and Sherman, F. (1996) The Cct eukaryotic chaperonin subunits of Saccharomyces cerevisiae and other yeasts, Yeast 12, 523-529.
58. 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.
59. Ursic, D., Sedbrook, J. C., Himmel, K. L., and Culbertson, M. R. (1994) The essential yeast Tcp1 protein affects actin and microtubules, Mol. Biol. Cell 5, 1065-1080.
60. 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.
61. Waldmann, T., Lupas, A., Kellermann, J., Peters, J., and Baumeister, W. (1995a) Primary structure of the thermosome from Thermoplasma acidophilum, Biol. Chem. Hoppe Seyler 376, 119-126.
62. Waldmann, T., Nimmesgern, E., Nitsch, M., Peters, J., Pfeifer, G., Muller, S., Kellermann, J., Engel, A., Hartl, F. U., and Baumeister, W. (1995b) The thermosome of Thermoplasma acidophilum and its relationship to the eukaryotic chaperonin TRiC, Eur. J. Biochem. 227, 848-856.
63. Willison, K. R. (1999) Composition and function of the eukaryotic cytosolic chaperonin-containing TCP-1, in Bukau, B. (Ed.), Molecular Chaperones and Folding Catalysts, pp. 555-571, Harwood, Amsterdam.
64. Willison, K. R., Dudley, K., and Potter, J. (1986) Molecular cloning and sequence analysis of a haploid expressed gene encoding t complex polypeptide 1, Cell 44, 727-738.
65. Willison, K. R., and Horwich, A. L. (1996) Structure and function of chaperonins in archaebacteria and eukaryotic cytosol, in Ellis, R. J. (Ed.), The Chaperonins, pp. 107-136, Academic Press, San Diego.
66. Willison, K. R., and Kubota, H. (1994) The structure, function, and genetics of the chaperonin containing TCP-1 (CCT) in eukaryotic cytosol, in Morimoto, R. I., Tissieres, A., and Georgopoulos, C. (Eds.), The Biology of Heat Shock Proteins and Molecular Chaperones, Vol. 26, pp. 299-312, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
67. Won, K. A., Schumacher, R. J., Farr, G. W., Horwich, A. L., and Reed, S. I. (1998) Maturation of human cyclin E requires the function of eukaryotic chaperonin CCT, Mol. Cell. Biol. 18, 7584-7589.
68. Zauner, S., Fraunholz, M., Wastl, J., Penny, S., Beaton, M., Cavalier-Smith, T., Maier, U. G., and Douglas, S. (2000) Chloroplast protein and centrosomal genes, a tRNA intron, and odd telomeres in an unusually compact eukaryotic genome, the cryptomonad nucleomorph, Proc. Natl. Acad. Sci. USA 97, 200-205.