Crystal structure of Cu/Zn superoxide dismutase from Taenia solium reveals metal-mediated self-assembly

FEBS Journal

Volumn 278, Issue 18, 2011, Pages 3308-3318

  Hernández Santoyo, Alejandra ^a   Landa, Abraham ^b   González Mondragón, Edith ^b   Pedraza Escalona, Martha ^a   Parra Unda, Ricardo ^b   Rodríguez Romero, Adela ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

crystal structure; metal mediated self assembly; superoxide dismutase; Taenia solium

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GLUTAMIC ACID; HISTIDINE; METAL ION; RECOMBINANT COPPER ZINC SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG DESIGN; ENZYME INHIBITION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; SPECIES DIFFERENCE; TAENIA SOLIUM;

ANIMALS; CATALYTIC DOMAIN; COPPER; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; HELMINTH PROTEINS; HOLOENZYMES; HOT TEMPERATURE; METALLOPROTEINS; MODELS, MOLECULAR; NEPHELOMETRY AND TURBIDIMETRY; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUPEROXIDE DISMUTASE; SURFACE PROPERTIES; TAENIA SOLIUM; ZINC;

CESTODA; SUS; TAENIA SOLIUM;

EID: 80052452799     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08247.x     Document Type: Article

References (51)

1. Fridovich I, (1998) Oxygen toxicity: a radical explanation. J Exp Biol 201, 1203-1209.
2. Fattman CL, Schaefer LM, &, Oury TD, (2003) Extracellular superoxide dismutase in biology and medicine. Free Radic Biol Med 35, 236-256.
3. Tainer JA, Getzoff ED, Beem KM, Richardson JS, &, Richardson DC, (1982) Determination and analysis of the 2 A-structure of copper, zinc superoxide dismutase. J Mol Biol 15, 181-217.
4. Henkle-Dührsen K, &, Kampkötter A, (2001) Antioxidant enzyme families in parasitic nematodes. Mol Biochem Parasitol 114, 129-142.
5. Antonyuk SV, Strange RW, Marklund SL, &, Hasnain SS, (2009) The structure of human extracellular copper-zinc superoxide dismutase at 1.7 Ã resolution: insights into heparin and collagen binding. J Mol Biol 388, 310-326.
6. Richardson JS, Thomas KA, Rubin BH, &, Richardson DC, (1975) Crystal structure of bovine Cu,Zn superoxide dismutase at 3Ã resolution: chain tracing and metal ligands. Proc Natl Acad Sci USA 72, 1349-1353.
7. Tainer JA, Getzoff ED, Richardson JS, &, Richardson DC, (1983) Structure and mechanism of copper, zinc superoxide dismutase. Nature 306, 284-287.
8. Shaw BF, &, Valentine JS, (2007) How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends Biochem Sci 32, 78-85.
9. Valdivia A, Pérez-Alvarez S, Aroca-Aguilar JD, Ikuta I, &, Jordán J, (2009) Superoxide dismutases: a physiopharmacological update. J Physiol Biochem 65, 195-208.
10. Vaca-Paniagua F, Torres-Rivera A, Parra-Unda R, &, Landa A, (2008) Taenia solium: antioxidant metabolism enzymes as targets for cestocidal drugs and vaccines. Curr Top Med Chem 8, 393-399.
11. Cardoso RM, Silva CH, Ulian de AraÃjo AP, Tanaka T, Tanaka M, &, Garratt RC, (2004) Structure of the cytosolic Cu,Zn superoxide dismutase from Schistosoma mansoni. Acta Crystallogr D Biol Crystallogr 60, 1569-1578.
12. Castellanos-González A, Jiménez L, &, Landa A, (2002) Cloning, production and characterisation of a recombinant Cu/Zn superoxide dismutase from Taenia solium. Int J Parasitol 32, 1175-1182.
13. Montresor A, &, Palmer K, (2006) Taeniasis/cysticercosis trend worldwide and rationale for control. Parasitol Int 55, Suppl-S301.
14. Marklund SL, (1982) Human copper-containing superoxide dismutase of high molecular weight. Proc Natl Acad Sci USA 79, 7634-7638.
15. Lin CW, Yang JH, &, Su LC, (1997) The extraction and properties of superoxide dismutase from porcine blood. Meat Sci 46, 303-312.
16. Benov L, Sage H, &, Fridovich I, (1997) The copper-and zinc-containing superoxide dismutase from Escherichia coli: molecular weight and stability. Arch Biochem Biophys 340, 305-310.
17. Lomakin A, Benedek GB, &, Teplow DB, (1999) Monitoring protein assembly using quasielastic light scattering spectroscopy. Methods Enzymol 309, 429-459.
18. Bush AI, Pettingell WH, Multhaup G, Paradis MD, Vonsattel JP, Gusella JF, Beyreuther K, Masters CL, &, Tanzi RE, (1994) Rapid induction of Alzheimer Ab amyloid formation by zinc. Science 265, 1464-1467.
19. Esler WP, Stimson ER, Jennings JM, Ghilardi JR, Mantyh PW, &, Maggio JE, (1996) Zinc-induced aggregation of human and rat b-amyloid peptides in vitro. J Neurochem 66, 723-732.
20. Stellato F, Menestrina G, Dalla-Serra M, Potrich C, Tomazzolli R, Meyer-Klaucke W, &, Morante S, (2006) Metal binding in amyloid β-peptides shows intra- and inter-peptide coordination modes. Eur Biophys J 35, 340-351.
21. Seetharaman SV, Prudencio M, Karch C, Holloway SP, Borchelt DR, &, Hart PJ, (2009) Immature copper-zinc superoxide dismutase and familial amyotrophic lateral sclerosis. Exp Biol Med 234, 1140-1154.
22. Matthews BW, (1968) Solvent content of protein crystals. J Mol Biol 33, 491-497.
23. Getzoff ED, Tainer JA, Weiner PK, Kollman PA, Richardson JS, &, Richardson DC, (1983) Electrostatic recognition between superoxide and copper, zinc superoxide dismutase. Nature 306, 284-287.
24. Banci L, Bertini I, Hallewell RA, Luchinat C, &, Viezzoli MS, (1989) Water in the active cavity of copper/zinc superoxide dismutase. A water 1H-nuclear-magnetic-relaxation-dispersion study. Eur J Biochem 184, 125-129.
25. Ascone I, Castañer R, Tarricone C, Bolognesi M, Stroppolo ME, &, Desideri A, (1997) Evidence of His61 imidazolate bridge rupture in reduced crystalline Cu,Zn superoxide dismutase. Biochem Biophys Res Commun 241, 119-121.
26. Hough MA, &, Hasnain SS, (2003) Structure of fully reduced bovine copper zinc superoxide dismutase at 1.15 Ã. Structure 11, 937-946.
27. Palmiter RD, &, Findley SD, (1995) Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J 14, 639-649.
28. Strange RW, Yong CW, Smith W, &, Hasnain SS, (2007) Molecular dynamics using atomic-resolution structure reveal structural fluctuations that may lead to polymerization of human Cu-Zn superoxide dismutase. Proc Natl Acad Sci 104, 10040-10044.
29. Hough MA, Grossman JG, Antonyuk SV, Strange RW, Doucette PA, Rodriguez JA, Whitson LJ, Hart PJ, Hayward LJ, Valentine JS, et al. (2004) Dimer destabilization in superoxide dismutase may result in disease-causing properties: structures of motor neuron disease mutants. Proc Natl Acad Sci 101, 5976-5981.
30. Cudkowicz ME, McKenna-Yasek D, Sapp PE, Chin W, Geller B, Hayden DL, Shoenfeld DA, Hosler BA, Horvitz H, &, Brown RH, (1997) Epidemiology of mutations in superoxide dismutase in amyotrophic lateral sclerosis. Ann Neurol 41, 210-221.
31. Baden EM, Owen BA, Peterson FC, Volkman BF, Ramirez-Alvarado M, &, Thompson JR, (2008) Altered dimer interface decreases stability in an amyloidogenic protein. J Biol Chem 283, 15853-15860.
32. Hernández-Santoyo A, del Pozo-Yauner L, Fuentes-Silva D, Ortiz E, Rudiño-Piñera E, Horjales E, Becerril B, &, Rodríguez- Romero A, (2010) A single mutation at the sheet switch region results in conformational changes favoring Î6-light-chain fibrillogenesis. J Mol Biol 396, 280-292.
33. Richardson JS, &, Richardson DC, (2002) Natural beta-sheet proteins use negative design to avoid edge-to-edge aggregation. Proc Natl Acad Sci 99, 2754-2759.
34. Jabeen T, Sharma S, Singh N, Bhushan A, &, Singh TP, (2005) Structure of the zinc-saturated C-terminal lobe of bovine lactoferrin at 2.0 Ã resolution. Acta Crystallogr D Biol Crystallogr 61, 1107-1115.
35. Salgado EN, Lewis RA, Faraone-Mennella J, &, Tezcan FA, (2008) Metal-mediated self-assembly of protein superstructures: influence of secondary interactions on protein oligomerization and aggregation. J Am Chem Soc 130, 6082-6084.
36. Banci L, Bertini I, Durazo A, Girotto S, Gralla EB, Martinelli M, Valentine JS, Vieru M, &, Whitelegge JP, (2007) Metal-free superoxide dismutase forms soluble oligomers under physiological conditions: a possible general mechanism for familial ALS. Proc Natl Acad Sci 104, 11263-11267.
37. Huang X, Atwood CS, Moir RD, Hartshorn MA, Tanzi RE, &, Bush AI, (2004) Trace metal contamination initiates the apparent auto-aggregation, amyloidosis, and oligomerization of Alzheimer's Abeta peptides. J Biol Inorg Chem 9, 954-960.
38. Cherny RA, Legg JT, McLean CA, Fairlie DP, Huang X, Atwood CS, Beyreuther K, Tanzi RE, Masters CL, &, Bush AI, (1999) Aqueous dissolution of Alzheimer's disease Abeta amyloid deposits by biometal depletion. J Biol Chem 274, 23223-23228.
39. Dong J, Atwood CS, Anderson VE, Siedlak SL, Smith MA, Perry G, &, Carey PR, (2003) Metal binding and oxidation of amyloid-beta within isolated senile plaque cores: Raman microscopic evidence. Biochemistry 42, 2768-2773.
40. Szczerbowska-Boruchowska M, Lankosz M, Ostachowicz J, Adamek D, Krygowska-Wajs A, Tomik B, Szczudlik A, Simionovici A, &, Bohic S, (2004) Topographic and quantitative microanalysis of human central nervous system tissue using synchrotron radiation. X-ray Spectrom 33, 3-11.
41. McCord JM, &, Fridovich I, (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244, 6049-6055.
42. Kabsch W, (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26, 795-800.
43. Evans P, (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62, 72-82.
44. Collaborative Computational Project, Number 4 (1994) The CCP4 Suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760-763.
45. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, &, Read RJ, (2007) Phaser crystallographic software. J Appl Crystallogr 40, 658-674.
46. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213-221.
47. Emsley P, &, Cowtan K, (2004) Coot: mode-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
48. Laskowski RA, MacArthur MW, Moss DS, &, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283-291.
49. Cohen GH, (1997) ALIGN: a program to superimpose protein coordinates, accounting for insertions and deletions. J Appl Crystallogr 30, 1160-1161.
50. DeLano WL, (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
51. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, &, Ferrin TE, (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.