The origami of thioredoxin-like folds

Protein Science

Volumn 15, Issue 10, 2006, Pages 2217-2227

  Pan, Jonathan L ^a   Bardwell, James C A ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b Department of Ecology and Evolutionary Biology   (United States)

Author keywords

Alkylhydroperoxidase; Dsb; Glutaredoxin; Glutathione S transferase; Protein engineering; Protein folds; Thioredoxin

Indexed keywords

ALKYL HYDROPEROXIDASE; DISULFIDE OXIDOREDUCTASE; GLUTAREDOXIN; GLUTATHIONE TRANSFERASE; OXIDOREDUCTASE; PEROXIDASE; THIOREDOXIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CHEMICAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW;

AMINO ACID MOTIFS; BINDING SITES; GENETIC VARIATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; STRUCTURAL HOMOLOGY, PROTEIN; THIOREDOXIN; THIOREDOXINS; VARIATION (GENETICS);

EID: 33749364627     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062268106     Document Type: Review

References (77)

1. Andersen, C.L., Matthey-Dupraz, A., Missiakas, D., and Raina, S. 1997. A new Escherichia coli gene, dsbG, encodes a periplasmic protein involved in disulphide bond formation, required for recycling DsbA/DsbB and DsbC redox proteins. Mol. Microbiol. 26: 121-132.
2. Aslund, F., Ehn, B., Miranda-Vizuete, A., Pueyo, C., and Holmgren, A. 1994. Two additional glutaredoxins exist in Escherichia coli: Glutaredoxin 3 is a hydrogen donor for ribonucleotide reductase in a thioredoxin/glutaredoxin 1 double mutant. Proc. Natl. Acad. Sci. 91: 9813-9817.
3. 15N NMR assignments, and structural analysis. J. Biol. Chem. 271: 6736-6745.
4. Aslund, F., Berndt, K.D., and Holmgren, A. 1997. Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J. Biol. Chem. 272: 30780-30786.
5. Bader, M., Muse, W., Ballou, D.P., Gassner, C., and Bardwell, J.C. 1999. Oxidative protein folding is driven by the electron transport system. Cell 98: 217-227.
6. Bader, M.W., Xie, T., Yu, C.A., and Bardwell, J.C. 2000. Disulfide bonds are generated by quinone reduction. J. Biol. Chem. 275: 26082-26088.
7. Bader, M.W., Hiniker, A., Regeimbal, J., Goldstone, D., Haebel, P.W., Riemer, J., Metcalf, P., and Bardwell, J.C. 2001. Turning a disulfide isomerase into an oxidase: DsbC mutants that imitate DsbA. EMBO J. 20: 1555-1562.
8. Bardwell, J.C., McGovern, K., and Beckwith, J. 1991. Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589.
9. Bieger, B. and Essen, L.O. 2001. Crystal structure of the catalytic core component of the alkylhydroperoxide reductase AhpF from Escherichia coli. J. Mol. Biol. 307: 1-8.
10. Bushweller, J.H., Billeter, M., Holmgren, A., and Wuthrich, K. 1994. The nuclear magnetic resonance solution structure of the mixed disulfide between Escherichia coli glutaredoxin(C14S) and glutathione. J. Mol. Biol. 235: 1585-1597.
11. Cha, M.K., Kim, H.K., and Kim, I.H. 1995. Thioredoxin-linked "thiol peroxidase" from periplasmic space of Escherichia coli. J. Biol. Chem. 270: 28635-28641.
12. Chivers, P.T., Prehoda, K.E., Volkman, B.F., Kim, B.M., Markley, J.L., and Raines, R.T. 1997. Microscopic pKa values of Escherichia coli thioredoxin. Biochemistry 36: 14985-14991.
13. Choi, J., Choi, S., Cha, M.K., Kim, I.H., and Shin, W. 2003. Crystal structure of Escherichia coli thiol peroxidase in the oxidized state: insights into intramolecular disulfide formation and substrate binding in atypical 2-Cys peroxiredoxins. J. Biol. Chem. 278: 49478-49486.
14. Coles, B. and Ketterer, B. 1990. The role of glutathione and glutathione transferases in chemical carcinogenesis. Crit. Rev. Biochem. Mol. Biol. 25: 47-70.
15. Collet, J.F., Riemer, J., Bader, M.W., and Bardwell, J.C. 2002. Reconstitution of a disulfide isomerization system. J. Biol. Chem. 277: 26886-26892.
16. Dailey, F.E. and Berg, H.C. 1993. Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc. Natl. Acad. Sci. 90: 1043-1047.
17. Darby, N.J., Penka, E., and Vincentelli, R. 1998a. The multi-domain structure of protein disulfide isomerase is essential for high catalytic efficiency. J. Mol. Biol. 276: 239-247.
18. Darby, N.J., Raina, S., and Creighton, T.E. 1998b. Contributions of substrate binding to the catalytic activity of DsbC. Biochemistry 37: 783-791.
19. 1H NMR spectroscopy. FEBS Lett. 228: 254-258.
20. _. 1989. Assignment of the proton NMR spectrum of reduced and oxidized thioredoxin: Sequence-specific assignments, secondary structure, and global fold. Biochemistry 28: 7074-7087.
21. 1H NMR. Biochemistry 30: 4262-4268.
22. Dyson, H.J., Jeng, M.F., Tennant, L.L., Slaby, I., Lindell, M., Cui, D.S., Kuprin, S., and Holmgren, A. 1997. Effects of buried charged groups on cysteine thiol ionization and reactivity in Escherichia coli thioredoxin: Structural and functional characterization of mutants of Asp 26 and Lys 57. Biochemistry 36: 2622-2636.
23. Eklund, H., Ingelman, M., Soderberg, B.O., Uhlin, T., Nordlund, P., Nikkola, M., Sonnerstam, U., Joelson, T., and Petratos, K. 1992. Structure of oxidized bacteriophage T4 glutaredoxin (thioredoxin). Refinement of native and mutant proteins. J. Mol. Biol. 228: 596-618.
24. Fernandes, A.P., Fladvad, M., Berndt, C., Andresen, C., Lillig, C.H., Neubauer, P., Sunnerhagen, M., Holmgren, A., and Vlamis-Gardikas, A. 2005. A novel monothiol glutaredoxin (Grx4) from Escherichia coli can serve as a substrate for thioredoxin reductase. J. Biol. Chem. 280: 24544-24552.
25. Fladvad, M., Bellanda, M., Fernandes, A.P., Mammi, S., Vlamis-Gardikas, A., Holmgren, A., and Sunnerhagen, M. 2005. Molecular mapping of functionalities in the solution structure of reduced Grx4, a monothiol glutaredoxin from Escherichia coli. J. Biol. Chem. 280: 24553-24561.
26. Foloppe, N. and Nilsson, L. 2004. The glutaredoxin -C-P-Y-C- motif: Influence of peripheral residues. Structure 12: 289-300.
27. Foloppe, N., Sagemark, J., Nordstrand, K., Berndt, K.D., and Nilsson, L. 2001. Structure, dynamics and electrostatics of the active site of glutaredoxin 3 from Escherichia coli: Comparison with functionally related proteins. J. Mol. Biol.. 310: 449-470.
28. Gerdes, S.Y., Scholle, M.D., Campbell, J.W., Balazsi, G., Ravasz, E., Daugherty, M.D., Somera, A.L., Kyrpides, N.C., Anderson, I., Gelfand, M.S., et al. 2003. Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J. Bacteriol. 185: 5673-5684.
29. Goulding, C.W., Sawaya, M.R., Parseghian, A., Lim, V., Eisenberg, D., and Missiakas, D. 2002. Thiol-disulfide exchange in an immunoglobulin-like fold: Structure of the N-terminal domain of DsbD. Biochemistry 41: 6920-6927.
30. Grauschopf, U., Winther, J.R., Korber, P., Zander, T., Dallinger, P., and Bardwell, J.C. 1995. Why is DsbA such an oxidizing disulfide catalyst? Cell 83: 947-955.
31. Guddat, L.W., Bardwell, J.C., and Martin, J.L. 1998. Crystal structures of reduced and oxidized DsbA: Investigation of domain motion and thiolate stabilization. Structure 6: 757-767.
32. Hiniker, A. and Bardwell, J.C. 2004. In vivo substrate specificity of periplasmic disulfide oxidoreductases. J. Biol. Chem. 279: 12967-12973.
33. Holmgren, A. 1976. Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc. Natl. Acad. Sci. 73: 2275-2279.
34. _. 1979a. Glutathione-dependent synthesis of deoxyribonucleotides. Characterization of the enzymatic mechanism of Escherichia coli glutaredoxin. J. Biol. Chem. 254: 3672-3678.
35. _. 1979b. Glutathione-dependent synthesis of deoxyribonucleotides. Purification and characterization of glutaredoxin from Escherichia coli. J. Biol. Chem. 254: 3664-3671.
36. _. 1985. Thioredoxin. Annu. Rev. Biochem. 54: 237-271.
37. _. 1989. Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264: 13963-13966.
38. _. 1995. Thioredoxin structure and mechanism: Conformational changes on oxidation of the active-site sulfhydryls to a disulfide. Structure 3: 239-243.
39. _. 2000. Antioxidant function of thioredoxin and glutaredoxin systems. Antioxid. Redox Signal. 2: 811-820.
40. Holmgren, A. and Fagerstedt, M. 1982. The in vivo distribution of oxidized and reduced thioredoxin in Escherichia coli. J. Biol. Chem. 257: 6926-6930.
41. Holmgren, A., Soderberg, B.O., Eklund, H., and Branden, C.I. 1975. Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8 Å resolution. Proc. Natl. Acad. Sci. 72: 2305-2309.
42. Jeng, M.F., Campbell, A.P., Begley, T., Holmgren, A., Case, D.A., Wright, P.E., and Dyson, H.J. 1994. High-resolution solution structures of oxidized and reduced Escherichia coli thioredoxin. Structure 2: 853-868.
43. Kadokura, H., Katzen, F., and Beckwith, J. 2003. Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 72: 111-135.
44. Kallis, G.B. and Holmgren, A. 1980. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli. J. Biol. Chem. 255: 10261-10265.
45. Katti, S.K., LeMaster, D.M., and Eklund, H. 1990. Crystal structure of thioredoxin from Escherichia coli at 1.68 Å resolution. J. Mol. Biol. 212: 167-184.
46. 15N NMR resonance assignments of vaccinia glutaredoxin-1 in the fully reduced form. J. Biomol. NMR 12: 353-355.
47. Kobayashi, T., Kishigami, S., Sone, M., Inokuchi, H., Mogi, T., and Ito, K. 1997. Respiratory chain is required to maintain oxidized states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proc. Natl. Acad. Sci. 94: 11857-11862.
48. Lennon, B.W. and Williams Jr., C.H. 1996. Enzyme-monitored turnover of Escherichia coli thioredoxin reductase: Insights for catalysis. Biochemistry 35: 4704-4712.
49. Lillig, C.H., Prior, A., Schwenn, J.D., Aslund, F., Ritz, D., Vlamis-Gardikas, A., and Holmgren, A. 1999. New thioredoxins and glutaredoxins as electron donors of 3′-phosphoadenylylsulfate reductase. J. Biol. Chem. 274: 7695-7698.
50. Mannervik, B. and Danielson, U.H. 1988. Glutathione transferases - Structure and catalytic activity. CRC Crit. Rev. Biochem. 23: 283-337.
51. Martin, J.L., Bardwell, J.C., and Kuriyan, J. 1993. Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365: 464-468.
52. Masai, E., Ichimura, A., Sato, Y., Miyauchi, K., Katayama, Y., and Fukuda, M. 2003. Roles of the enantioselective glutathione S-transferases in cleavage of β-aryl ether. J. Bacteriol. 185: 1768-1775.
53. Masip, L., Pan, J.L., Haldar, S., Penner-Hahn, J.E., DeLisa, M.P., Georgiou, G., Bardwell, J.C., and Collet, J.F. 2004. An engineered pathway for the formation of protein disulfide bonds. Science 303: 1185-1189.
54. McCarthy, A.A., Haebel, P.W., Torronen, A., Rybin, V., Baker, E.N., and Metcalf, P. 2000. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat. Struct. Biol. 7: 196-199.
55. Missiakas, D., Georgopoulos, C., and Raina, S. 1993. Identification and characterization of the Escherichia coli gene dsbB, whose product is involved in the formation of disulfide bonds in vivo. Proc. Natl. Acad. Sci. 90: 7084-7088.
56. Nakamura, H. 2005. Thioredoxin and its related molecules: Update 2005. Antioxid. Redox Signal. 7: 823-828.
57. Nishida, M., Harada, S., Noguchi, S., Satow, Y., Inoue, H., and Takahashi, K. 1998. Three-dimensional structure of Escherichia coli glutathione S-transferase complexed with glutathione sulfonate: Catalytic roles of Cys10 and His106. J. Mol. Biol. 281: 135-147.
58. Poole, L.B. 1996. Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 2. Cystine disulfides involved in catalysis of peroxide reduction. Biochemistry 35: 65-75.
59. Poole, L.B., Godzik, A., Nayeem, A., and Schmitt, J.D. 2000. AhpF can be dissected into two functional units: Tandem repeats of two thioredoxin-like folds in the N-terminus mediate electron transfer from the thioredoxin reductase-like C-terminus to AhpC. Biochemistry 39: 6602-6615.
60. Reynolds, C.M. and Poole, L.B. 2000. Attachment of the N-terminal domain of Salmonella typhimurium AhpF to Escherichia coli thioredoxin reductase confers AhpC reductase activity but does not affect thioredoxin reductase activity. Biochemistry 39: 8859-8869.
61. Rietsch, A., Belin, D., Martin, N., and Beckwith, J. 1996. An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proc. Natl. Acad. Sci. 93: 13048-13053.
62. Rietsch, A., Bessette, P., Georgiou, G., and Beckwith, J. 1997. Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin. J. Bacteriol. 179: 6602-6608.
63. Ritz, D., Lim, J., Reynolds, C.M., Poole, L.B., and Beckwith, J. 2001. Conversion of a peroxiredoxin into a disulfide reductase by a triplet repeat expansion. Science 294: 158-160.
64. Rodriguez-Manzaneque, M.T., Ros, J., Cabiscol, E., Sorribas, A., and Herrero, E. 1999. Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 8180-8190.
65. Segatori, L., Murphy, L., Arredondo, S., Kadokura, H., Gilbert, H., Beckwith, J., and Georgiou, G. 2006. Conserved role of the linker α-helix of the bacterial disulfide isomerase DsbC in the avoidance of misoxidation by DsbB. J. Biol. Chem. 281: 4911-4919.
66. Shi, J., Vlamis-Gardikas, A., Aslund, F., Holmgren, A., and Rosen, B.P. 1999. Reactivity of glutaredoxins 1, 2, and 3 from Escherichia coli shows that glutaredoxin 2 is the primary hydrogen donor to ArsC-catalyzed arsenate reduction. J. Biol. Chem. 274: 36039-36042.
67. 2+. FEMS Microbiol. Lett. 174: 179-184.
68. Stewart, E.J., Aslund, F., and Beckwith, J. 1998. Disulfide bond formation in the Escherichia coli cytoplasm: An in vivo role reversal for the thioredoxins. EMBO J. 17: 5543-5550.
69. Tao, K. 1997. oxyR-dependent induction of Escherichia coli grx gene expression by peroxide stress. J. Bacteriol. 179: 5967-5970.
70. Vlamis-Gardikas, A., Aslund, F., Spyrou, G., Bergman, T., and Holmgren, A. 1997. Cloning, overexpression, and characterization of glutaredoxin 2, an atypical glutaredoxin from Escherichia coli. J. Biol. Chem. 272: 11236-11243.
71. Vuilleumier, S. 1997. Bacterial glutathione S-transferases: What are they good for? J. Bacteriol. 179: 1431-1441.
72. Walker, K.W. and Gilbert, H.F. 1997. Scanning and escape during protein-disulfide isomerase-assisted protein folding. J. Biol. Chem. 272: 8845-8848.
73. Wood, Z.A., Poole, L.B., and Karplus, P.A. 2001. Structure of intact AhpF reveals a mirrored thioredoxin-like active site and implies large domain rotations during catalysis. Biochemistry 40: 3900-3911.
74. Wood, Z.A., Schroder, E., Robin Harris, J., and Poole, L.B. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28: 32-40.
75. Xie, T., Yu, L., Bader, M.W., Bardwell, J.C., and Yu, C.A. 2002. Identification of the ubiquinone-binding domain in the disulfide catalyst disulfide bond protein B. J. Biol. Chem. 277: 1649-1652.
76. Zapun, A., Bardwell, J.C., and Creighton, T.E. 1993. The reactive and destabilizing disulfide bond of DsbA, a protein required for protein disulfide bond formation in vivo. Biochemistry 32: 5083-5092.
77. Zheng, M., Aslund, F., and Storz, G. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721.