Diversity of chemical mechanisms in thioredoxin catalysis revealed by single-molecule force spectroscopy

Nature Structural and Molecular Biology

Volumn 16, Issue 8, 2009, Pages 890-896

  Perez Jimenez, Raul ^a   Li, Jingyuan ^a   Kosuri, Pallav ^a   Sanchez Romero, Inmaculada ^b   Wiita, Arun P ^a   Rodriguez Larrea, David ^b   Chueca, Ana ^c   Holmgren, Arne ^d   Miranda Vizuete, Antonio ^e   Becker, Katja ^f   Cho, Seung Hyun ^g   Beckwith, Jon ^g   Gelhaye, Eric ^h   Jacquot, Jean P ^h   Gaucher, Eric ⁱ   Sanchez Ruiz, Jose M ^b   Berne, Bruce J ^a   Fernandez, Julio M ^a  

^a Columbia University ^*  (United States)

^b UNIVERSITY OF GRANADA   (Spain)

^c CSIC   (Spain)

^d KAROLINSKA INSTITUTE   (Sweden)

^e Universidad Pablo de Olavide   (Spain)

^f JUSTUS LIEBIG UNIVERSITY   (Germany)

^g HARVARD MEDICAL SCHOOL   (United States)

^h UNIVERSITÉ DE LORRAINE   (France)

ⁱ GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

THIOREDOXIN; THIOREDOXIN 1; THIOREDOXIN 2;

ARTICLE; CATALYSIS; CATALYST; DISULFIDE BOND; ELECTRON TRANSPORT; HUMAN; MICHAELIS MENTEN KINETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REACTION ANALYSIS; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BINDING SITES; CATALYSIS; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; GENETIC VARIATION; HUMANS; ISOENZYMES; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; THIOREDOXINS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 68249144762     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1627     Document Type: Article

References (62)

1. Kraut, D.A., Carroll, K.S. & Herschlag, D. Challenges in enzyme mechanism and energetics. Annu. Rev. Biochem. 72, 517-571 (2003).
2. Henzler-Wildman, K.A. et al. Intrinsic motions along an enzymatic reaction trajectory. Nature 450, 838-844 (2007).
3. Dai, S. et al. Structural snapshots along the reaction pathway of ferredoxin-thioredoxin reductase. Nature 448, 92-96 (2007).
4. Mori, T., Vale, R.D. & Tomishige, M. How kinesin waits between steps. Nature 450, 750-754 (2007).
5. Asbury, C.L., Fehr, A.N. & Block, S.M. Kinesin moves by an asymmetric handover-hand mechanism. Science 302, 2130-2134 (2003).
6. Holmgren, A. Thioredoxin. Annu. Rev. Biochem. 54, 237-271 (1985).
7. Lillig, C.H. & Holmgren, A. Thioredoxin and related molecules-from biology to health and disease. Antioxid. Redox Signal. 9, 25-47 (2007).
8. Holmgren, A. Reduction of disulfides by thioredoxin. Exceptional reactivity of insulin and suggested functions of thioredoxin in mechanism of hormone action. J. Biol. Chem. 254, 9113-9119 (1979).
9. Holmgren, A. Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J. Biol. Chem. 254, 9627-9632 (1979).
10. Holmgren, A. Tryptophan fluorescence study of conformational transitions of the oxidized and reduced form of thioredoxin. J. Biol. Chem. 247, 1992-1998 (1972).
11. Wiita, A.P. et al. Probing the chemistry of thioredoxin catalysis with force. Nature 450, 124-127 (2007).
12. Koti Ainavarapu, S.R., Wiita, A.P., Dougan, L., Uggerud, E. & Fernandez, J.M. Single-molecule force spectroscopy measurements of bond elongation during a bimolecular reaction. J. Am. Chem. Soc. 130, 6479-6487 (2008).
13. Wiita, A.P., Ainavarapu, S.R., Huang, H.H. & Fernandez, J.M. Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques. Proc. Natl. Acad. Sci. USA 103, 7222-7227 (2006).
14. Damdimopoulos, A.E., Miranda-Vizuete, A., Pelto-Huikko, M., Gustafsson, J.A. & Spyrou, G. Human mitochondrial thioredoxin. Involvement in mitochondrial membrane potential and cell death. J. Biol. Chem. 277, 33249-33257 (2002).
15. Miranda-Vizuete, A., Damdimopoulos, A.E., Gustafsson, J. & Spyrou, G. Cloning, expression, and characterization of a novel Escherichia coli thioredoxin. J. Biol. Chem. 272, 30841-30847 (1997).
16. Spyrou, G., Enmark, E., Miranda-Vizuete, A. & Gustafsson, J. Cloning and expression of a novel mammalian thioredoxin. J. Biol. Chem. 272, 2936-2941 (1997).
17. Ye, J. et al. Crystal structure of an unusual thioredoxin protein with a zinc finger domain. J. Biol. Chem. 282, 34945-34951 (2007).
18. Boucher, I.W. et al. Structural and biochemical characterization of a mitochondrial peroxiredoxin from Plasmodium falciparum. Mol. Microbiol. 61, 948-959 (2006).
19. Powis, G. & Montfort, W.R. Properties and biological activities of thioredoxins. Annu. Rev. Biophys. Biomol. Struct. 30, 421-455 (2001).
20. Gelhaye, E., Rouhier, N., Navrot, N. & Jacquot, J.P. The plant thioredoxin system. Cell. Mol. Life Sci. 62, 24-35 (2005).
21. Meyer, Y. et al. Evolution of redoxin genes in the green lineage. Photosynth. Res. 89, 179-192 (2006).
22. Perez-Jimenez, R. et al. Force-clamp spectroscopy detects residue co-evolution in enzyme catalysis. J. Biol. Chem. 283, 27121-27129 (2008).
23. Carvalho, A.T. et al. Mechanism of thioredoxin-catalyzed disulfide reduction. Activation of the buried thiol and role of the variable active-site residues. J. Phys. Chem. B 112, 2511-2523 (2008).
24. Kappler, U. & Bailey, S. Molecular basis of intramolecular electron transfer in sulfite-oxidizing enzymes is revealed by high resolution structure of a heterodimeric complex of the catalytic molybdopterin subunit and a c-type cytochrome subunit. J. Biol. Chem. 280, 24999-25007 (2005).
25. -. J. Am. Chem. Soc. 122, 2329-2338 (2000).
26. Holm, R.H., Kennepohl, P. & Solomon, E.I. Structural and functional aspects of metal sites in biology. Chem. Rev. 96, 2239-2314 (1996).
27. McLendon, G., Komar-Panicucci, S. & Hatch, S. Applying Marcus's theory to electron transfer in vivo. Electron Transfer-from Isolated Molecules to Biomolecules. in Advances in Chemical Physics Vol 107 591-600 (John Wiley & Sons, New York, NY, 1999).
28. Erlandsson, M. & Hallbrink, M. Metallic zinc reduction of disulfide bonds between cysteine residues in peptides and proteins. Int. J. Pept. Res. Ther. 11, 261-265 (2005).
29. Aslund, F., Berndt, K.D. & Holmgren, A. 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 (1997).
30. Cheng, Z., Arscott, L.D., Ballou, D.P. & Williams, C.H. Jr. The relationship of the redox potentials of thioredoxin and thioredoxin reductase from Drosophila melanogaster to the enzymatic mechanism: reduced thioredoxin is the reductant of glutathione in Drosophila. Biochemistry 46, 7875-7885 (2007).
31. Yasui, S., Itoh, K., Tsujimoto, M. & Ohno, A. Irreversibility of single electron transfer occurring from trivalent phosphorus compounds to Iron(III) complexes in the presence of ethanol. Bull. Chem. Soc. Jpn. 75, 1311-1318 (2002).
32. Hazzard, J.T., Marchesini, A., Curir, P. & Tollin, G. Direct measurement by laser flash photolysis of intramolecular electron transfer in the three-electron reduced form of ascorbate oxidase from zucchini. Biochim. Biophys. Acta 1208, 166-170 (1994).
33. Farver, O. & Pecht, I. Low activation barriers characterize intramolecular electron transfer in ascorbate oxidase. Proc. Natl. Acad. Sci. USA 89, 8283-8287 (1992).
34. Maeda, K., Hagglund, P., Finnie, C., Svensson, B. & Henriksen, A. Structural basis for target protein recognition by the protein disulfide reductase thioredoxin. Structure 14, 1701-1710 (2006).
35. Li, Y. et al. Conformational fluctuations coupled to the thiol-disulfide transfer between thioredoxin and arsenate reductase in Bacillus subtilis. J. Biol. Chem. 282, 11078-11083 (2007).
36. Lennon, B.W., Williams Jr., C.H., & Ludwig, M.L. Twists in catalysis: alternating conformations of Escherichia coli thioredoxin reductase. Science 289, 1190-1194 (2000).
37. Falkowski, P.G. Evolution. Tracing oxygen's imprint on earth's metabolic evolution. Science 311, 1724-1725 (2006).
38. Raymond, J. & Segre, D. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311, 1764-1767 (2006).
39. Kirschvink, J.L. & Kopp, R.E. Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II. Phil. Trans. R. Soc. Lond. B 363, 2755-2765 (2008).
40. Lemaire, S.D. et al. New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 101, 7475-7480 (2004).
41. Sharma, A. et al. Microbial activity at gigapascal pressures. Science 295, 1514-1516 (2002).
42. La Duc, M.T. et al. Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl. Environ. Microbiol. 73, 2600-2611 (2007).
43. Koch, A.L. Shrinkage of growing Escherichia coli cells by osmotic challenge. J. Bacteriol. 159, 919-924 (1984).
44. Malone, A.S., Chung, Y.K. & Yousef, A.E. Genes of Escherichia coli O157:H7 that are involved in high-pressure resistance. Appl. Environ. Microbiol. 72, 2661-2671 (2006).
45. Gaucher, E.A., Govindarajan, S. & Ganesh, O.K. Palaeotemperature trend for Precambrian life inferred from resurrected proteins. Nature 451, 704-707 (2008).
46. Jones, P.R., Manabe, T., Awazuhara, M. & Saito, K. A new member of plant CS-lyases. A cystine lyase from Arabidopsis thaliana. J. Biol. Chem. 278, 10291-10296 (2003).
47. Beynon, R.J., Bond, J.S. & NetLibrary Inc. Proteolytic enzymes: a practical approach. in Practical Approach Series 2nd edn, xviii, 340 (Oxford University Press, Oxford; New York, 2001).
48. Forman-Kay, J.D., Clore, G.M., Wingfield, P.T. & Gronenborn, A.M. High-resolution three-dimensional structure of reduced recombinant human thioredoxin in solution. Biochemistry 30, 2685-2698 (1991).
49. Qin, J., Clore, G.M., Kennedy, W.M., Huth, J.R. & Gronenborn, A.M. Solution structure of human thioredoxin in a mixed disulfide intermediate complex with its target peptide from the transcription factor NF kappa B. Structure 3, 289-297 (1995).
50. Peterson, F.C. et al. Solution structure of thioredoxin h1 from Arabidopsis thaliana. Protein Sci. 14, 2195-2200 (2005).
51. Capitani, G. et al. Crystal structures of two functionally different thioredoxins in spinach chloroplasts. J. Mol. Biol. 302, 135-154 (2000).
52. Smeets, A. et al. Crystal structures of oxidized and reduced forms of human mitochondrial thioredoxin 2. Protein Sci. 14, 2610-2621 (2005).
53. Katti, S.K., LeMaster, D.M. & Eklund, H. Crystal structure of thioredoxin from Escherichia coli at 1.68 resolution. J. Mol. Biol. 212, 167-184 (1990).
54. Lancelin, J.M., Guilhaudis, L., Krimm, I., Blackledge, M.J., Marion, D. & Jacquot, J.P. NMR structures of thioredoxin m from the green alga Chlamydomonas reinhardtii. Proteins 41, 334-349 (2000).
55. Qin, J., Clore, G.M., Kennedy, W.P., Kuszewski, J. & Gronenborn, A.M. The solution structure of human thioredoxin complexed with its target from Ref-1 reveals peptide chain reversal. Structure 4, 613-620 (1996).
56. Kanzok, S.M., Schirmer, R.H., Turbachova, I., Iozef, R. & Becker, K. The thioredoxin system of the malaria parasite Plasmodium falciparum. Glutathione reduction revisited. J. Biol. Chem. 275, 40180-40186 (2000).
57. Kanzok, S.M. et al. Substitution of the thioredoxin system for glutathione reductase in Drosophila melanogaster. Science 291, 643-646 (2001).
58. Behm, M. & Jacquot, J.P. Isolation and characterization of thioredoxin h from poplar xylem. Plant Physiol. Biochem. 38, 363-369 (2000).
59. Gelhaye, E. et al. Identification and characterization of a third thioredoxin h in poplar. Plant Physiol. Biochem. 41, 629-635 (2003).
60. López Jaramillo, J. et al. High-yield expression of pea thioredoxin m and assessment of its efficiency in chloroplast fructose-1,6-bisphosphatase activation. Plant Physiol. 114, 1169-1175 (1997).
61. Perez-Jimenez, R., Godoy-Ruiz, R., Ibarra-Molero, B. & Sanchez-Ruiz, J.M. The efficiency of different salts to screen charge interactions in proteins: a Hofmeister effect? Biophys. J. 86, 2414-2429 (2004).
62. Fernandez, J.M. & Li, H.B. Force-clamp spectroscopy monitors the folding trajectory of a single protein. Science 303, 1674-1678 (2004).