Functional properties of the protein disulfide oxidoreductase from the archaeon Pyrococcus furiosus: A member of a novel protein family related to protein disulfide-isomerase

European Journal of Biochemistry

Volumn 271, Issue 16, 2004, Pages 3437-3448

  Pedone, Emilia ^a   Ren, Bin ^b   Ladenstein, Rudolf ^b   Rossi, Mosè ^c,d   Bartolucci, Simonetta ^c  

^a CNR   (Italy)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

Archaea; Protein disulfide oxidoreductase; Protein disulfide isomerase; Pyrococcus furiosus; Redox sites

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CATION; ISOMERASE; MUTANT PROTEIN; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE);

ARCHAEBACTERIUM; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; MOLECULAR PHYLOGENY; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PH; PRIORITY JOURNAL; PROTEIN FAMILY; PYROCOCCUS FURIOSUS; REDUCTION; SEQUENCE HOMOLOGY; TEMPERATURE DEPENDENCE;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; CATTLE; CIRCULAR DICHROISM; CYSTEINE; INSULIN; MOLECULAR SEQUENCE DATA; MUTATION; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; PROTEIN DISULFIDE-ISOMERASE; PYROCOCCUS FURIOSUS; RIBONUCLEASES;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; PYROCOCCUS; PYROCOCCUS FURIOSUS;

EID: 4344586909     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-2956.2004.04282.x     Document Type: Article

References (55)

1. McFarlan, S.C., Terrell, C.A. & Hogenkamp, H.P. (1992) The purification, characterization, and primary structure of a small redox protein from Methanobacterium thermoautotrophicum, an archaebacterium. J. Biol. Chem. 267, 10561-10569.
2. Bhattacharyya, S., Habibi-Nazhad, B., Amegbey, G., Slupsky, C., Yee, A., Arrowsmith, C. & Wishart, D.S. (2002) Identification of a novel archaebacterial thioredoxin: determination of function through structure. Biochemistry 41, 4760-4770.
3. Bult, C.J., White, O., Olsen, G.J., Zhou, L., 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. & Venter, J.C. (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 1058-1073.
4. Lee, D.Y., Ahn, B. & Kim, K. (2000) A thioredoxin from the hyperthermophilic archaeon Methanococcus jannaschii has a glutaredoxin-like fold but thioredoxin-like activities. Biochemistry 39, 6652-6659.
5. Cave, J.W., Cho, H.S., Batchelder, A.M., Yokota, H., Kim, R. & Wemmer, D.E. (2001) Solution nuclear magnetic resonance structure of a protein disulfide oxidoreductase from Methanococcus jannaschii. Protein Sci. 10, 384-396.
6. Guagliardi, A., Nobile, V., Bartolucci, S. & Rossi, M. (1994) A thioredoxin from the extreme thermophilic archaeon Sulfolobus solfataricus. Int. J. Biochem. 26, 375-380.
7. Guagliardi, A., De Pascale, D., Cannio, R., Nobile, V., Bartolucci, S. & Rossi, M. (1995) The purification, cloning, and high level expression of a glutaredoxin-like protein from the hyperthermophilic archaeon Pyrococcus furiosus. J. Biol. Chem. 270, 5748-5755.
8. Bartolucci, S., De Pascale, D. & Rossi, M. (2001) Protein disulfide oxidoreductase from Pyrococcus furiosus: biochemical properties. Methods Enzymol. 334, 62-73.
9. Ren, B., Tibbelin, G., De Pascale, D., Rossi, M., Bartolucci, S. & Ladenstein, R. (1997) Crystallization and preliminary X-ray structure analysis of a hyperthermostable thioltransferase from the archaeon Pyrococcus furiosus. J. Struct. Biol. 119, 1-5.
10. Ren, B., Tibbelin, G., De Pascale, D., Rossi, M., Bartolucci, S. & Ladenstein, R. (1998) A protein disulfide oxidoreductase from the archaeon Pyrococcus furiosus contains two thioredoxin fold units. Nat. Struct. Biol. 5, 602-611.
11. Ren, B. & Ladenstein, R. (2001) Protein disulfide oxidoreductase from Pyrococcus furiosus: structural properties. Methods Enzymol. 334, 74-88.
12. Freedman, R.B. (1998) Novel disulfide oxidoreductase in search of a function. Nat. Struct. Biol. 5, 531-532.
13. Ruddock, L.W., Hirst, T.R. & Feedman, R.B. (1996) pH-dependence of the dithiol-oxidizing activity of DsbA (a periplasmic protein thiol: disulphide oxidoreductase) and protein disulphide-isomerase: studies with a novel simple peptide substrate. Biochem. J. 315, 1000-1005.
14. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
15. Barker, D.G. (1982) Cloning and amplified expression of the tyrosyl-tRNA synthetase genes of Bacillus stearothermophilus and Escherichia coli. Eur. J. Biochem. 125, 357-360.
16. Saiki, R.K. (1990) Amplification of genomic DNA. In PCR Protocols: A Guide to Methods and Applications (Innis, M.A., Gellfand, D.A., Sninski, J.J. & White, T.J., eds), pp. 13-20. Academic Press, New York.
17. Kunkel, T.A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA 82, 488-492.
18. Sanger, F., Nicklen, S. & Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA 76, 5653-5667.
19. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. & Klenk, D.C. (1995) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
20. Rabilloud, T., Vuillard, L., Gilly, C. & Lawrence, J.J. (1994) Silver-staining of proteins in polyacrylamide gels: a general overview. Cell. Mol. Biol. 40, 57-75.
21. Hollecker, M. & Creighton, T.E. (1980) Counting integral numbers of amino groups per polypeptide chain. FEBS Lett. 119, 187-190.
22. Davies, G.E. & Stark, G.R. (1970) Use of dimethyl sub-erimidate, a cross-linking reagent, in studying the subunit structure of oligomeric proteins. Proc. Natl Acad. Sci. USA 66, 651-656.
23. Holmgren, A. (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J. Biol. Chem. 254, 9627-9632.
24. Lambert, N. & Freedman, R.B. (1983) Kinetics and specificity of homogeneous protein disulphide-isomerase in protein disulphide isomerization and in thiol-protein-disulphide oxidoreduction. Biochem. J. 213, 235-243.
25. Kunitz, M. (1946) A spectrophotometric method for the measurement of ribonuclease activity. J. Biol. Chem. 164, 563-568.
26. Catz, S.D., Johnson, J.L. & Babior, B.M. (2001) Characterization of the nucleotide-binding capacity and the ATPase activity of the PIP3-binding protein JFC1. Proc. Natl Acad. Sci. USA 28, 11230-11235.
27. Guagliardi, A., Cerchia, L., Bartolucci, S. & Rossi, M. (1994) The chaperonin from the archaeon Sulfolobus solfataricus promotes correct refolding and prevents thermal denaturation in vitro. Protein Sci. 3, 1436-1443.
28. Lanzetta, P.A., Alvarez, L.J., Reinach, P.S. & Candia, O.A. (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem. 100, 95-97.
29. Guagliardi, A., Cerchia, L., Moracci, M. & Rossi, M. (2000) The chromosomal protein sso7d of the crenarchaeon Sulfolobus solfataricus rescues aggregated proteins in an ATP hydrolysis-dependent manner. J. Biol. Chem. 275, 31813-31818.
30. Vuori, K., Myllyla, R., Pihlajaniemi, T. & Kivirikko, K.I. (1992) Expression and site-directed mutagenesis of human protein disulfide isomerase in Escherichia coli. This multifunctional polypeptide has two independently acting catalytic sites for the isomerase activity. J. Biol. Chem. 267, 7211-7217.
31. Saraste, M., Sibbald, P.R. & Wittinghofer, A. (1990) The P-loop: a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 15, 430-434.
32. Prodromou, C., Roe, S.M., O'Brien, R., Ladbury, J.E., Piper, P.W. & Pearl, L.H. (1997) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90, 65-75.
33. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A. & Forterre, P. (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature (London) 386, 414-417.
34. Jakob, U., Scheibel, T., Bose, S., Reinstein, J. & Buchner, J. (1996) Assessment of the ATP binding properties of Hsp90. J. Biol. Chem. 271, 10035-10041.
35. Quemeneur, E., Guthapfel, R. & Gueguen, P. (1994) A major phosphoprotein of the endoplasmic reticulum is protein disulfide isomerase. J. Biol. Chem. 269, 5485-5488.
36. Baross, J.A. & Holden, J.F. (1996) Overview of hyperthermophiles and their heat-shock proteins. Adv. Protein Chem. 48, 1-34.
37. Freedman, R.B., Klappa, P. & Ruddock, L.W. (2002) Protein disulfide isomerases exploit synergy between catalytic and specific binding domains. EMBO Report 3, 136-140.
38. 15N NMR spectroscopy. Biochemistry 35, 7684-7691.
39. Darby, N.J., Kemmink, J. & Creighton, T.E. (1996) Identifying and characterizing a structural domain of protein disulfide isomerase. Biochemistry 35, 10517-11052.
40. Quemeneur, E, Guthapfel, R. & Gueguen, P. (1994) A major phophoprotein of the endoplasmic reticulum is protein disulfide isomerase. J. Biol. Chem. 269, 5485-5488.
41. Guthapfel, R., Gueguen, P. & Quemeneur, E. (1996) ATP binding and hydrolysis by the multifunctional protein disulfide isomerase. J. Biol. Chem. 271, 2663-2666.
42. Zapun, A., Creighton, T.E., Rowling, P.J. & Freedman, R.B. (1992) Folding in vitro of bovine pancreatic trypsin inhibitor in the presence of proteins of the endoplasmic reticulum. Proteins 14, 10-15.
43. Robb, F.T., Maeder, D.L., Brown, J.R., DiRuggiero, J., Stump, M.D., Yeh, R.K., Weiss, R.B. & Dunn, D.M. (2001) Genomic sequence of hyperthermophile, Pyrococcus furiosus: implications for physiology and enzymology. Methods Enzymol. 330, 134-157.
44. She, Q., Singh, R.K., Confalonieri, F., Zivanovic, Y., Allard, G., Awayez, M.J., Chan-Weiher, C.C., Clausen, I.G., Curtis, B.A., De Moors, A., Erauso, G., Fletcher, C., Gordon, P.M., Heikamp-de Jong, I., Jeffries, A.C., Kozera, C.J., Medina, N., Peng, X., Thi-Ngoc, H.P., Redder, P., Schenk, M.E., Theriault, C., Tolstrup, N., Charlebois, R.L., Doolittle, W.F., Duguet, M., Gaasterland, T., Garrett, R.A., Ragan, M.A., Sensen, C.W. & Van der Oost, J. (2001) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc. Natl Acad. Sci. USA 98, 7835-7840.
45. Chinen, A., Uchiyama, I. & Kobayashi, I. (2000) Comparison between Pyrococcus horikoshii and Pyrococcus abyssi genome sequences reveals linkage of restriction-modification genes with large genome polymorphisms. Gene 259, 109-121.
46. Kawarabayasi, Y., Hino, Y., Horikawa, H., Jin-n., o, K., Takahashi, M., Sekine, M., Baba, S., Ankai, A., Kosugi, H., Hosoyama, A., Fukui, S., Nagai, Y., Nishijima, K., Otsuka, R., Nakazawa, H., Takamiya, M., Kalo, Y., Yoshizawa, T., Tanaka, T., Kudoh, Y., Yamazaki, J., Kushida, N., Oguchi, A., Aoki, K., Masuda, S., Yanagii, M., Nishimura, M., Yamagishi, A., Oshima, T. & Kikuchi, H. (2001) Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain7. DNA Res. 8, 123-140.
47. Ruepp, A., Graml, W., Santos-Martinez, M.L., Koretke, K.K., Volker, C., Mewes, H.W., Frishman, D., Stocker, S., Lupas, A.N. & Baumeister, W. (2000) The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature (London) 407, 508-513.
48. 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. & Suzuki, M. (2000) Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc. Natl Acad. Sci. USA 97, 14257-14262.
49. Kawarabayasi, Y., Hino, Y., Horikawa, H., Yamazaki, S., Haikawa, Y., Jin-n., o, 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. (1999) Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res. 6, 145-152.
50. Deckert, G., Warren, P.V., Gaasterland, T., Young, W.G., Lenox, L., Graham, D.E., Overbeek, R., Snead, M.A., Keller, M., Aujay, M., Huber, R., Feldman, R.A., Short, J.M., Olsen, G.J. & Swanson, R.V. (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature (London) 392, 353-358.
51. Bao, Q., Tian, Y., Li, W., Xu, Z., Xuan, Z., Hu, S., Dong, W., Yang, J., Chen, Y., Xue, Y., Xu, Y., Lai, X., Huang, L., Dong, X., Ma, Y., Ling, L., Tan, H., Chen, R. & Wang, J., Yu, J. & Yang, H. (2002) A complete sequence of the T. tengcongensis genome. Genome Res. 12, 689-700.
52. Nelson, K.E., Eisen, J.A. & Fraser, C.M. (2001) Genome of Thermotoga maritima MSB8. Methods Enzymol. 330, 169-180.
53. Makarova, K.S. & Koonin, E.V. (2003) Comparative genomics of archaea: how much have we learned in six years, and what's next? Genome Biol. 4, 115-145.
54. Kashima, Y. & Ishikawa, K. (2003) A hyperthermostable novel protein-disulfide oxidoreductase is reduced by thioredoxin reductase from hyperthermophilic archaeon Pyrococcus horikoshii. Arch. Biochem. Biophysics 418, 179-185.
55. Mallick, P., Boutz, D.R., Eisenberg, D. & Yeates, T.O. (2002) Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc. Natl Acad. Sci. USA 99, 9679-9684.