Moonlighting by different stressors: Crystal structure of the chaperone species of a 2-Cys peroxiredoxin

Structure

Volumn 20, Issue 3, 2012, Pages 429-439

  Saccoccia, Fulvio ^a   Di Micco, Patrizio ^a   Boumis, Giovanna ^a   Brunori, Maurizio ^a,b   Koutris, Ilias ^a   Miele, Adriana E ^a   Morea, Veronica ^b   Sriratana, Palita ^c   Williams, David L ^c   Bellelli, Andrea ^a,b   Angelucci, Francesco ^a,d  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b CNR   (Italy)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CITRATE SYNTHASE; HYDROGEN PEROXIDE; PEROXIDASE; PEROXIREDOXIN 2;

ACIDITY; ALPHA HELIX; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; IN VIVO STUDY; MOLECULAR WEIGHT; NONHUMAN; OLIGOMERIZATION; OXIDATION; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SCHISTOSOMA MANSONI; STATIC ELECTRICITY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PEROXIDASE; PEROXIREDOXINS; PROTEIN CONFORMATION; SCHISTOSOMA MANSONI;

SCHISTOSOMA MANSONI;

EID: 84863230834     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.01.004     Document Type: Article

References (46)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221.
2. Aran, M., Ferrero, D.S., Pagano, E., and Wolosiuk, R.A. (2009). Typical 2-Cys peroxiredoxins-modulation by covalent transformations and noncovalent interactions. FEBS J. 276, 2478-2493.
3. Barranco-Medina, S., Kakorin, S., Lázaro, J.J., and Dietz, K.J. (2008). Thermodynamics of the dimer-decamer transition of reduced human and plant 2-cys peroxiredoxin. Biochemistry 47, 7196-7204. (Pubitemid 351956368)
4. 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.
5. Battye, T.G., Kontogiannis, L., Johnson, O., Powell, H.R., and Leslie, A.G. (2011). iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281.
6. Cass, C.L., Johnson, J.R., Califf, L.L., Xu, T., Hernandez, H.J., Stadecker, M.J., Yates, J.R., 3rd, and Williams, D.L. (2007). Proteomic analysis of Schistosoma mansoni egg secretions. Mol. Biochem. Parasitol. 155, 84-93. (Pubitemid 47238446)
7. Cremers, C.M., Reichmann, D., Hausmann, J., Ilbert, M., and Jakob, U. (2010). Unfolding of metastable linker region is at the core of Hsp33 activation as a redox-regulated chaperone. J. Biol. Chem. 285, 11243-11251.
8. Davis, I.W., Murray, L.W., Richardson, J.S., and Richardson, D.C. (2004). MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucl. Acids Res. 32, W615-W619. (Pubitemid 38997409)
9. Dekker, C., Willison, K.R., and Taylor, W.R. (2011). On the evolutionary origin of the chaperonins. Proteins 79, 1172-1192.
10. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010). Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501.
11. Evans, P.R. (2011). An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D Biol. Crystallogr. 67, 282-292.
12. Flohé, L., Budde, H., and Hofmann, B. (2003). Peroxiredoxins in antioxidant defense and redox regulation. Biofactors 19, 3-10. (Pubitemid 38073139)
13. Gourlay, L.J., Bhella, D., Kelly, S.M., Price, N.C., and Lindsay, J.G. (2003). 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, 32631-32637. (Pubitemid 37055701)
14. Green, W.F., and Colley, D.G. (1981). Modulation of Schistosoma mansoni egg-induced granuloma formation: I-J restriction of T cell-mediated suppression in a chronic parasitic infection. Proc. Natl. Acad. Sci. USA 78, 1152-1156. (Pubitemid 11102178)
15. Hall, A., Karplus, P.A., and Poole, L.B. (2009). Typical 2-Cys peroxiredoxins - structures, mechanisms and functions. FEBS J. 276, 2469-2477.
16. Harris, J.R., Schröder, E., Isupov, M.N., Scheffler, D., Kristensen, P., Littlechild, J.A., Vagin, A.A., and Meissner, U. (2001). Comparison of the decameric structure of peroxiredoxin-II by transmission electron microscopy and X-ray crystallography. Biochim. Biophys. Acta 1547, 221-234. (Pubitemid 32532140)
17. Hirotsu, S., Abe, Y., Okada, K., Nagahara, N., Hori, H., Nishino, T., and Hakoshima, T. (1999). Crystal structure of a multifunctional 2-Cys peroxiredoxin heme-binding protein 23 kDa/proliferation-associated gene product. Proc. Natl. Acad. Sci. USA 96, 12333-12338. (Pubitemid 29513502)
18. Hofmann, B., Hecht, H.J., and Flohé, L. (2002). Peroxiredoxins. Biol. Chem. 383, 347-364. (Pubitemid 34506276)
19. Jang, H.H., Lee, K.O., Chi, Y.H., Jung, B.G., Park, S.K., Park, J.H., Lee, J.R., Lee, S.S., Moon, J.C., Yun, J.W., et al. (2004). Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117, 625-635. (Pubitemid 38692528)
20. Jönsson, T.J., Johnson, L.C., and Lowther, W.T. (2008). Structure of the sulphiredoxin-peroxiredoxin complex reveals an essential repair embrace. Nature 451, 98-101.
21. Jönsson, T.J., Johnson, L.C., and Lowther, W.T. (2009). Protein engineering of the quaternary sulfiredoxin.peroxiredoxin enzyme.substrate complex reveals the molecular basis for cysteine sulfinic acid phosphorylation. J. Biol. Chem. 284, 33305-33310.
22. Kabsch, W., and Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.
23. Kumsta, C., and Jakob, U. (2009). Redox-regulated chaperones. Biochemistry 48, 4666-4676.
24. Lim, J.C., Choi, H.I., Park, Y.S., Nam, H.W., Woo, H.A., Kwon, K.S., Kim, Y.S., Rhee, S.G., Kim, K., and Chae, H.Z. (2008). Irreversible oxidation of the active-site cysteine of peroxiredoxin to cysteine sulfonic acid for enhanced molecular chaperone activity. J. Biol. Chem. 283, 28873-28880.
25. Lowther, W.T., and Haynes, A.C. (2011). Reduction of cysteine sulfinic acid in eukaryotic, typical 2-Cys peroxiredoxins by sulfiredoxin. Antioxid. Redox Signal. 15, 99-109.
26. Moon, J.C., Hah, Y.S., Kim, W.Y., Jung, B.G., Jang, H.H., Lee, J.R., Kim, S.Y., Lee, Y.M., Jeon, M.G., Kim, C.W., et al. (2005). Oxidative stress-dependent structural and functional switching of a human 2-Cys peroxiredoxin isotype II that enhances HeLa cell resistance to H2O2-induced cell death. J. Biol. Chem. 280, 28775-28784. (Pubitemid 41105779)
27. Murshudov, G.N., Skubák, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F., and Vagin, A.A. (2011). REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367.
28. Nelson, K.J., Knutson, S.T., Soito, L., Klomsiri, C., Poole, L.B., and Fetrow, J.S. (2011). Analysis of the peroxiredoxin family: using active-site structure and sequence information for global classification and residue analysis. Proteins 79, 947-964.
29. Neumann, C.A., Cao, J., and Manevich, Y. (2009). Peroxiredoxin 1 and its role in cell signaling. Cell Cycle 8, 4072-4078.
30. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
31. Phalen, T.J., Weirather, K., Deming, P.B., Anathy, V., Howe, A.K., van der Vliet, A., Jönsson, T.J., Poole, L.B., and Heintz, N.H. (2006). Oxidation state governs structural transitions in peroxiredoxin II that correlate with cell cycle arrest and recovery. J. Cell Biol. 175, 779-789. (Pubitemid 44878510)
32. Poon, S., Rybchyn, M.S., Easterbrook-Smith, S.B., Carver, J.A., Pankhurst, G.J., and Wilson, M.R. (2002). Mildly acidic pH activates the extracellular molecular chaperone clusterin. J. Biol. Chem. 277, 39532-39540. (Pubitemid 35190931)
33. Potterton, L., McNicholas, S., Krissinel, E., Gruber, J., Cowtan, K., Emsley, P., Murshudov, G.N., Cohen, S., Perrakis, A., and Noble, M. (2004). Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 60, 2288-2294. (Pubitemid 41742782)
34. Sali, D., Bycroft, M., and Fersht, A.R. (1988). Stabilization of protein structure by interaction of alpha-helix dipole with a charged side chain. Nature 335, 740-743.
35. Sayed, A.A., and Williams, D.L. (2004). Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. J. Biol. Chem. 279, 26159-26166. (Pubitemid 38798761)
36. Sayed, A.A., Cook, S.K., and Williams, D.L. (2006). Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets. J. Biol. Chem. 281, 17001-17010.
37. Soito, L., Williamson, C., Knutson, S.T., Fetrow, J.S., Poole, L.B., and Nelson, K.J. (2011). PREX: PeroxiRedoxin classification indEX, a database of subfamily assignments across the diverse peroxiredoxin family. Nucleic Acids Res. 39 (Database issue), D332-D337.
38. Stadecker, M.J. (1992). The role of T-cell anergy in the immunomodulation of schistosomiasis. Parasitol. Today 8, 199-204.
39. Vagin, A., and Teplyakov, A. (2010). Molecular Replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25.
40. Williams, D.L., Asahi, H., Botkin, D.J., and Stadecker, M.J. (2001). Schistosome infection stimulates host CD4(+) T helper cell and B-cell responses against a novel egg antigen, thioredoxin peroxidase. Infect. Immun. 69, 1134-1141. (Pubitemid 32109582)
41. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G., McCoy, A., et al. (2011). Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242.
42. Winter, J., Linke, K., Jatzek, A., and Jakob, U. (2005). Severe oxidative stress causes inactivation of DnaK and activation of the redox-regulated chaperone Hsp33. Mol. Cell 17, 381-392. (Pubitemid 40193309)
43. Winterbourn, C.C., and Hampton, M.B. (2008). Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45, 549-561.
44. 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. (Pubitemid 34429383)
45. Wood, Z.A., Schröder, E., Robin Harris, J., and Poole, L.B. (2003). Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32-40. (Pubitemid 36051004)
46. Yeates, T.O. (1997). Detecting and overcoming crystal twinning. Methods Enzymol. 276, 344-358.