The protein-free ianus peptide array uncovers interaction sites between escherichia coli parvulin 10 and alkyl hydroperoxide reductase

Biochemistry

Volumn 49, Issue 39, 2010, Pages 8626-8635

  Malešević, Miroslav ^a   Poehlmann, Angela ^a   Hernandez Alvarez, Birte ^a   Diessner, André ^b   Träger, Mario ^a   Rahfeld, Jens Ulrich ^a   Jahreis, Günther ^a   Liebscher, Sandra ^b   Bordusa, Frank ^b   Fischer, Gunter ^a   Lücke, Christian ^a  

^a MAX PLANCK RESEARCH UNIT FOR ENZYMOLOGY OF PROTEIN FOLDING   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ALKYL HYDROPEROXIDE; BACTERIAL CELLS; BINDING PARTNERS; CATALYTIC ACTIVITY; CELLULAR PROTECTION; CHEMICAL CROSS-LINKING; CIS AND TRANS ISOMERS; DOCKING CALCULATIONS; E. COLI; ENZYMATIC ACTION; FLUORESCENCE RESONANCE ENERGY TRANSFER; INTERACTION SITE; ISOMERASES; MATRIX; NMR DATA; PEPTIDE ARRAYS; PROTEIN-FREE; STRUCTURAL ELEMENTS; WILD-TYPE STRAIN;

AFFINITY CHROMATOGRAPHY; ALKYLATION; CATALYST ACTIVITY; CROSSLINKING; ENERGY TRANSFER; ESCHERICHIA COLI; FLUORESCENCE; HYDROGEN PEROXIDE; ISOMERS;

PEPTIDES;

ALKYL HYDROPEROXIDE REDUCTASE SUBUNIT C; BACTERIAL PROTEIN; HYDROGEN PEROXIDE; ISOMERASE; PARVULIN 10; PEROXIREDOXIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; BINDING SITE; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION;

AMINO ACID SEQUENCE; BINDING SITES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATIVE STRESS; PEPTIDYLPROLYL ISOMERASE; PEROXIREDOXINS; PROTEIN ARRAY ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 77957283701     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101015p     Document Type: Article

References (60)

1. Frank, R. (2002) The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports - principles and applications J. Immunol. Methods 267, 13-26
2. Wenschuh, H., Volkmer-Engert, R., Schmidt, M., Schulz, M., Schneider-Mergener, J., and Reineke, U. (2000) Coherent membrane supports for parallel microsynthesis and screening of bioactive peptides Biopolymers 55, 188-206
3. Reimer, U., Reineke, U., and Schneider-Mergener, J. (2002) Peptide arrays: From macro to micro Curr. Opin. Biotechnol. 13, 315-320
4. Volkmer, R. (2009) Synthesis and application of peptide arrays: Quo vadis SPOT technology ChemBioChem 10, 1431-1442
5. Yu, C., Malesevic, M., Jahreis, G., Schutkowski, M., Fischer, G., and Schiene-Fischer, C. (2005) The architecture of protein-ligand binding sites revealed through template-assisted intramolecular peptide-peptide interactions Angew. Chem., Int. Ed. 44, 1408-1412
6. Fanghänel, J. and Fischer, G. (2004) Insights into the catalytic mechanism of peptidyl prolyl cis / trans isomerases Front. Biosci. 9, 3453-3478
7. Lu, K. P., Finn, G., Lee, T. H., and Nicholson, L. K. (2007) Prolyl cis-trans isomerization as a molecular timer Nat. Chem. Biol. 3, 619-629
8. Wedemeyer, W. J., Welker, E., and Scheraga, H. A. (2002) Proline cis-trans isomerization and protein folding Biochemistry 41, 14637-14644
9. Fischer, G. and Aumüller, T. (2003) Regulation of peptide bond cis / trans isomerization by enzyme catalysis and its implication in physiological processes Rev. Physiol. Biochem. Pharmacol. 148, 105-150
10. Luan, S., Albers, M. W., and Schreiber, S. L. (1994) Light-regulated, tissue-specific immunophilins in a higher plant Proc. Natl. Acad. Sci. U.S.A. 91, 984-988
11. Dolinski, K., Muir, S., Cardenas, M., and Heitman, J. (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U.S.A. 94, 13093-13098
12. Missiakas, D., Betton, J. M., and Raina, S. (1996) New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH Mol. Microbiol. 21, 871-884
13. Dartigalongue, C. and Raina, S. (1998) A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli EMBO J. 17, 3968-3980
14. Lee, J. P., Palfrey, H. C., Bindokas, V. P., Ghadge, G. D., Ma, L., Miller, R. J., and Roos, R. P. (1999) The role of immunophilins in mutant superoxide dismutase-1 linked familial amyotrophic lateral sclerosis Proc. Natl. Acad. Sci. U.S.A. 96, 3251-3256
15. Doyle, V., Virji, S., and Crompton, M. (1999) Evidence that cyclophilin-A protects cells against oxidative stress Biochem. J. 341, 127-132
16. Wen, Z. T., Suntharaligham, P., Cvitkovitch, D. G., and Burne, R. A. (2005) Trigger factor in Streptococcus mutans is involved in stress tolerance, competence development, and biofilm formation Infect. Immun. 73, 219-225
17. Rahfeld, J. U., Schierhorn, A., Mann, K., and Fischer, G. (1994) A novel peptidyl-prolyl cis / trans isomerase from Escherichia coli FEBS Lett. 343, 65-69
18. Rahfeld, J. U., Rücknagel, K. P., Schelbert, B., Ludwig, B., Hacker, J., Mann, K., and Fischer, G. (1994) Confirmation of the existence of a third family among peptidyl-prolyl cis / trans isomerases. Amino acid sequence and recombinant production of parvulins FEBS Lett. 352, 180-184
19. Hennig, L., Christner, C., Kipping, M., Schelbert, B., Rücknagel, K. P., Grabley, S., Küllertz, G., and Fischer, G. (1998) Selective inactivation of parvulin-like peptidyl-prolyl cis / trans isomerases by juglone Biochemistry 37, 5953-5960
20. Malesevic, M., Lücke, C., and Jahreis, G. (2005) Simple and efficient synthesis of new trifunctional templates. In Peptides 2004, Proceedings of the Third International and Twenty-Eighth European Peptide Symposium, pp 391 - 392, Kenes International, Ben-Gurion, Israel.
21. Frank, R. (1992) Spot-Synthesis: An Easy Technique for the Positionally Addressable, Parallel Chemical Synthesis on a Membrane Support Tetrahedron 48, 9217-9232
22. 15N chemical shift referencing in biomolecular NMR J. Biomol. NMR 6, 135-140
23. Kühlewein, A., Voll, G., Hernandez Alvarez, B., Kessler, H., Fischer, G., Rahfeld, J. U., and Gemmecker, G. (2004) Solution structure of Escherichia coli Par10: The prototypic member of the Parvulin family of peptidyl-prolyl cis / trans isomerases Protein Sci. 13, 2378-2387
24. Mulder, F. A. A., Schipper, D., Bott, R., and Boelens, R. (1999) Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins J. Mol. Biol. 292, 111-123
25. Dominguez, C., Boelens, R., and Bonvin, A. M. J. J. (2003) HADDOCK: A protein-protein docking approach based on biochemical or biophysical information J. Am. Chem. Soc. 125, 1731-1737
26. Hubbard, S. J. and Thornton, J. M. (1993) NACCESS Computer Program, Department of Biochemistry and Molecular Biology, University College London, London.
27. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
28. Cherepanov, P. P. and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant Gene 158, 9-14
29. Donnenberg, M. S. and Kaper, J. B. (1991) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector Infect. Immun. 59, 4310-4317
30. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in Gram-negative bacteria Nat. Biotechnol. 1, 784-791
31. Ubben, D. and Schmitt, R. (1986) Tn1721 derivatives for transposon mutagenesis, restriction mapping and nucleotide sequence analysis Gene 41, 145-152
32. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
33. Christman, M. F., Morgan, R. W., Jacobson, F. S., and Ames, B. N. (1985) Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium Cell 41, 753-762
34. Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., and Schmid, F. X. (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins Nature 337, 476-478
35. Poole, L. B. (2005) Bacterial defenses against oxidants: Mechanistic features of cysteine-based peroxidases and their flavoprotein reductases Arch. Biochem. Biophys. 433, 240-254
36. Chae, H. Z., Uhm, T. B., and Rhee, S. G. (1994) Dimerization of thiol-specific antioxidant and the essential role of cysteine 47 Proc. Natl. Acad. Sci. U.S.A. 91, 7022-7026
37. Spector, A. (1995) Oxidative stress-induced cataract: Mechanism of action FASEB J. 9, 1173-1182
38. Jacobson, F. S., Morgan, R. W., Christman, M. F., and Ames, B. N. (1989) An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. Purification and properties J. Biol. Chem. 264, 1488-1496
39. 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
40. Wood, Z. A., Poole, L. B., Hantgan, R. R., and Karplus, P. A. (2002) Dimers to doughnuts: Redox-sensitive oligomerization of 2-cysteine peroxiredoxins Biochemistry 41, 5493-5504
41. Barranco-Medina, S., Lázaro, J. J., and Dietz, K. J. (2009) The oligomeric conformation of peroxiredoxins links redox state to function FEBS Lett. 583, 1809-1816
42. Hall, A., Karplus, P. A., and Poole, L. B. (2009) Typical 2-Cys peroxiredoxins: Structures, mechanisms and functions FEBS J. 276, 2469-2477
43. Wu, P. and Brand, L. (1994) Resonance energy transfer: Methods and applications Anal. Biochem. 218, 1-13
44. Sapsford, K. E., Berti, L., and Medintz, I. L. (2006) Materials for fluorescence resonance energy transfer analysis: Beyond traditional donor-acceptor combinations Angew. Chem., Int. Ed. 45, 4562-4588
45. García-Echeverría, C. and Rich, D. H. (1992) New intramolecularly quenched fluorogenic peptide substrates for the study of the kinetic specificity of papain FEBS Lett. 297, 100-102
46. Janowski, B., Wöllner, S., Schutkowski, M., and Fischer, G. (1997) A protease-free assay for peptidyl prolyl cis / trans isomerases using standard peptide substrates Anal. Biochem. 252, 299-307
47. Zoldák, G., Aumüller, T., Lücke, C., Hritz, J., Oostenbrink, C., Fischer, G., and Schmid, F. X. (2009) A library of fluorescent peptides for exploring the substrate specificities of prolyl isomerases Biochemistry 48, 10423-10436
48. Chauhan, R. and Mande, S. C. (2002) Site-directed mutagenesis reveals a novel catalytic mechanism of Mycobacterium tuberculosis alkylhydroperoxidase C Biochem. J. 367, 255-261
49. Schiene-Fischer, C., Habazettl, J., Schmid, F. X., and Fischer, G. (2002) The hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isomerase Nat. Struct. Biol. 9, 419-424
50. Ranganathan, R., Lu, K. P., Hunter, T., and Noel, J. P. (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent Cell 89, 875-886
51. Heikkinen, O., Seppala, R., Tossavainen, H., Heikkinen, S., Koskela, H., Permi, P., and Kilpeläinen, I. (2009) Solution structure of the parvulin-type PPIase domain of Staphylococcus aureus PrsA: Implications for the catalytic mechanism of parvulins BMC Struct. Biol. 9, 17
52. Bailey, M. L., Shilton, B. H., Brandl, C. J., and Litchfield, D. W. (2008) The dual histidine motif in the active site of Pin1 has a structural rather than catalytic role Biochemistry 47, 11481-11489
53. Daniels, D. L., Plunkett, G., Burland, V., and Blattner, F. R. (1992) Analysis of the Escherichia coli genome: DNA sequence of the region from 84.5 to 86.5 minutes Science 257, 771-778
54. Wood, Z. A., Poole, L. B., and Karplus, A. (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling Science 300, 650-653
55. Woo, H. A., Chae, H. Z., Hwang, S. C., Yang, K. S., Kang, S. W., Kim, K., and Rhee, S. G. (2003) Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation Science 300, 653-656
56. Malešević, M., Jahreis, G., Wawra, S., Fischer, G., and Lücke, C. (2008) Conformational consequences of regio- and stereoselective disulfide bridge oxidation in a cyclic peptide ChemBioChem 9, 46-49
57. Poole, L. B. and Ellis, H. R. (1996) Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins Biochemistry 35, 56-64
58. Storz, G., Jacobson, F. S., Tartaglia, L. A., Morgan, R. W., Silveira, L. A., and Ames, B. N. (1989) An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: Genetic characterization and cloning of ahp J. Bacteriol. 171, 2049-2055
59. Trandinh, C. C., Pao, G. M., and Saier, M. H., Jr. (1992) Structural and evolutionary relationships among the immunophilins: Two ubiquitous families of peptidyl-prolyl cis-trans isomerases FASEB J. 6, 3410-3420
60. Hacker, J. and Fischer, G. (1993) Immunophilins: Structure-function relationship and possible role in microbial pathogenicity Mol. Microbiol. 10, 445-456