Switching between the alternative structures and functions of a 2-Cys peroxiredoxin, by site-directed mutagenesis

Journal of Molecular Biology

Volumn 425, Issue 22, 2013, Pages 4556-4568

  Angelucci, F ^a   Saccoccia, F ^b   Ardini, M ^a   Boumis, G ^b   Brunori, M ^b   Di Leandro, L ^a   Ippoliti, R ^a   Miele, A E ^b   Natoli, G ^b   Scotti, S ^a   Bellelli, A ^b  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

2 Cys peroxiredoxin; host parasite relationships; molecular chaperone; moonlighting behavior; protein nanotube

Indexed keywords

CHAPERONE; MUTANT PROTEIN; PEROXIREDOXIN;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ASSAY; GEL PERMEATION CHROMATOGRAPHY; PKA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROSCOPY;

SCHISTOSOMA MANSONI;

EID: 84886719210     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.09.002     Document Type: Article

References (49)

1. L. Soito, C. Williamson, S.T. Knutson, J.S. Fetrow, L.B. Poole, and K.J. Nelson PREX: PeroxiRedoxin classification indEX, a database of subfamily assignments across the diverse peroxiredoxin family Nucleic Acids Res 39 2011 D332 D337
2. H.H. Jang, K.O. Lee, Y.H. Chi, B.G. Jung, S.K. Park, and J.H. Park Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function Cell 117 2004 625 635
3. A. Cimini, R. Gentile, F. Angelucci, E. Benedetti, G. Pitari, and A. Giordano Neuroprotective effects of PrxI over-expression in an in vitro human Alzheimer's disease model J Cell Biochem 114 2013 708 715
4. 2-induced cell death J Biol Chem 280 2005 28775 28784
5. A. Hall, P.A. Karplus, and L.B. Poole Typical 2-Cys peroxiredoxins - structures, mechanisms and functions FEBS J 276 2009 2469 2477
6. A. Hall, K. Nelson, L.B. Poole, and P.A. Karplus Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins Antioxid Redox Signaling 15 2011 795 815
7. K.S. Yang, S.W. Kang, H.A. Woo, S.C. Hwang, H.Z. Chae, and K. Kim Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid J Biol Chem 277 2002 38029 38036
8. J.R. Harris, E. Schröder, M.N. Isupov, D. Scheffler, P. Kristensen, and J.A. Littlechild Comparison of the decameric structure of peroxiredoxin-II by transmission electron microscopy and X-ray crystallography Biochim Biophys Acta 1547 2001 221 234
9. U. Meissner, E. Schröder, D. Scheffler, A.G. Martin, and J.R. Harris Formation, TEM study and 3D reconstruction of the human erythrocyte peroxiredoxin-2 dodecahedral higher-order assembly Micron 38 2007 29 39
10. B. Biteau, J. La barre, and M.B. Toledano ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin Nature 425 2003 980 984
11. F. Angelucci, A. Basso, A. Bellelli, M. Brunori, L. Pica Mattoccia, and C. Valle The anti-schistosomal drug praziquantel is an adenosine antagonist Parasitology 134 2007 1215 1221
12. F. Angelucci, A.E. Miele, G. Boumis, M. Brunori, D. Dimastrogiovanni, and A. Bellelli Macromolecular bases of antischistosomal therapy Curr Top Med Chem 11 2011 2012 2028
13. A.A. Sayed, and D.L. Williams Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni J Biol Chem 279 2004 26159 26166
14. A.A. Sayed, S.K. Cook, and D.L. Williams Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets J Biol Chem 281 2006 17001 17010
15. F. Angelucci, D. Dimastrogiovanni, G. Boumis, M. Brunori, A.E. Miele, and F. Saccoccia Mapping the catalytic cycle of Schistosoma mansoni thioredoxin glutathione reductase by X-ray crystallography J Biol Chem 285 2010 32557 32567
16. F. Angelucci, A.A. Sayed, D.L. Williams, G. Boumis, M. Brunori, and D. Dimastrogiovanni Inhibition of Schistosoma mansoni thioredoxin-glutathione reductase by auranofin: structural and kinetic aspects J Biol Chem 284 2009 28977 28985
17. A.N. Kuntz, E. Davioud-Charvet, A.A. Sayed, L.L. Califf, J. Dessolin, and E.S. Arnér Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target PLoS Med 4 2007 e206
18. F. Saccoccia, F. Angelucci, G. Boumis, M. Brunori, A.E. Miele, and D.L. Williams On the mechanism and rate of gold incorporation into thiol-dependent flavoreductases J Inorg Biochem 108 2012 105 111
19. D. Cioli, C. Valle, F. Angelucci, and A.E. Miele Will new antischistosomal drugs finally emerge? Trends Parasitol 24 2008 379 382
20. D. Dimastrogiovanni, M. Anselmi, A.E. Miele, G. Boumis, L. Petersson, and F. Angelucci Combining crystallography and molecular dynamics: the case of Schistosoma mansoni phospholipid glutathione peroxidase Proteins 78 2010 259 270
21. G. Boumis, F. Angelucci, A. Bellelli, M. Brunori, D. Dimastrogiovanni, and A.E. Miele Structural and functional characterization of Schistosoma mansoni thioredoxin Protein Sci 20 2011 1069 1076
22. C.L. Cass, J.R. Johnson, L.L. Califf, T. Xu, H.J. Hernandez, and M.J. Stadecker Proteomic analysis of Schistosoma mansoni egg secretions Mol Biochem Parasitol 155 2007 84 93
23. S. Donnelly, C.M. Stack, S.M. O'Neill, A.A. Sayed, D.L. Williams, and J.P. Dalton Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages FASEB J 22 2008 4022 4032
24. F. Saccoccia, P. Di Micco, G. Boumis, M. Brunori, I. Koutris, and A.E. Miele Moonlighting by different stressors: crystal structure of the chaperone species of a 2-Cys peroxiredoxin Structure 20 2012 429 439
25. M.C. Gretes, L.B. Poole, and P.A. Karplus Peroxiredoxins in parasites Antioxid Redox Signaling 17 2012 608
26. J.R. Harris Some negative contrast staining features of a protein from erythrocyte ghosts J Mol Biol 46 1969 329 335
27. L.R. Manning, W.T. Jenkins, J.R. Hess, K. Vandegriff, R.M. Winslow, and J.M. Manning Subunit dissociations in natural and recombinant hemoglobins Protein Sci 5 1996 775 781
28. C.C. Winterbourn, and M.B. Hampton Thiol chemistry and specificity in redox signaling Free Radical Biol Med 45 2008 549 561
29. J. Buchner, H. Grallert, and U. Jakob Analysis of chaperone function using citrate synthase as nonnative substrate protein Methods Enzymol 290 1998 323 338
30. D.H. Huberts, and I.J. van der Klei Moonlighting proteins: an intriguing mode of multitasking Biochim Biophys Acta 1803 2010 520 525
31. M. Montemartini, H.M. Kalisz, H.J. Hecht, P. Steinert, and L. Flohé Activation of active-site cysteine residues in the peroxiredoxin-type tryparedoxin peroxidase of Crithidia fasciculata Eur J Biochem 264 1999 516 524
32. Z. Cao, D. Bhella, and J.G. Lindsay Reconstitution of the mitochondrial PrxIII antioxidant defence pathway: general properties and factors affecting PrxIII activity and oligomeric state J Mol Biol 372 2007 1022 1033
33. E. Schröder, J.A. Littlechil, A.A. Lebedev, N. Errington, A.A. Vagin, and M.N. Isupov Crystal structure of decameric 2-Cys peroxiredoxin from human erythrocytes at 1.7 Å resolution Structure 8 2000 605 615
34. J.W. Park, G. Piszczek, S.G. Rhee, and P.B. Chock Glutathionylation of peroxiredoxin I induces decamer to dimers dissociation with concomitant loss of chaperone activity Biochemistry 50 2011 3204 3210
35. J. Liang, H. Edelsbrunner, and C. Woodward Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design Protein Sci 7 1998 1884 1897
36. G.W. Farr, K. Furtak, M.B. Rowland, N.A. Ranson, H.R. Saibil, and T. Kirchhausen Multivalent binding of nonnative substrate proteins by the chaperonin GroEL Cell 100 2000 561 573
37. C. Dekker, K.R. Willison, and W.R. Taylor On the evolutionary origin of the chaperonins Proteins 79 2011 1172 1192
38. L.J. Gourlay, D. Bhella, S.M. Kelly, N.C. Price, and J.G. Lindsay Structure-function analysis of recombinant substrate protein 22 kDa (SP-22). A mitochondrial 2-Cys peroxiredoxin organized as a decameric toroid J Biol Chem 278 2003 32631 32637
39. S. Poon, M.S. Rybchyn, S.B. Easterbrook-Smith, J.A. Carver, G.J. Pankhurst, and M.R. Wilson Mildly acidic pH activates the extracellular molecular chaperone clusterin J Biol Chem 277 2002 39532 39540
40. W. Kabsch XDS Acta Crystallogr Sect D Biol Crystallogr 66 2010 125 132
41. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, and N. Echols PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr Sect D Biol Crystallogr 66 2010 213 221
42. E. Stanley The identification of twins from intensity statistics J Appl Crystallogr 5 1972 191 194
43. D. Hamdane, C. Lechauve, M.C. Marden, and B. Golinelli-Pimpaneau Pseudo-merohedral twinning in monoclinic crystals of wild-type human brain neuroglobin Acta Crystallogr Sect D Biol Crystallogr 65 2009 388 389
44. P.A. Karplus, and K. Diederichs Linking crystallographic model and data quality Science 336 2012 1030 1033
45. N. Chandra, K.R. Acharya, and P.C.E. Moody Analysis and characterization of data from twinned crystals Acta Crystallogr Sect D Biol Crystallogr 55 1999 1750 1758
46. T.O. Yeates, and B.C. Fam Protein crystals and their evil twins Structure 7 1999 R25 R29G
47. G. Jogl, X. Tao, Y. Xu, and L. Tong COMO: a program for combined molecular replacement Acta Crystallogr Sect D Biol Crystallogr 57 2001 1127 1134
48. N. Murshudov, P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, and R.A. Nicholls REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr Sect D Biol Crystallogr 67 2011 355 367
49. P. Emsley, B. Lohkamp, W. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr Sect D Biol Crystallogr 66 2010 486 501