Functional features cause misfolding of the ALS-provoking enzyme SOD1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 24, 2009, Pages 9667-9672

  Nordlund, Anna ^a   Leinartaite, Lina ^a   Saraboji, Kadhirvel ^a,b   Aisenbrey, Christopher ^c   Gröbner, Gerhard ^c   Zetterström, Per ^c   Danielsson, Jens ^a   Logan, Derek T ^b   Oliveberg, Mikael ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

Functional evolution; Protein disease; Protein misfolding

Indexed keywords

COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; ZINC;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY;

AMYOTROPHIC LATERAL SCLEROSIS; HUMANS; LIGANDS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; SUPEROXIDE DISMUTASE;

EID: 67649852607     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0812046106     Document Type: Article

References (35)

1. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366. (Pubitemid 44118036)
2. Lindberg MJ, Byström R, Boknäs N, Andersen PM, Oliveberg M (2005) Systematically perturbed folding patterns of amyotrophic lateral sclerosis (ALS)-associated SOD1 mutants. Proc Natl Acad Sci USA 102:9754-9759. (Pubitemid 40993641)
3. 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. (Pubitemid 46199198)
4. Estevez AG, et al. (1999) Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 286:2498-2500. (Pubitemid 129515968)
5. Lindberg MJ, Normark J, Holmgren A, Oliveberg M (2004) Folding of human superoxide dismutase: Disulfide reduction prevents dimerization and produces marginally stable monomers. Proc Natl Acad Sci USA 101:15893-15898. (Pubitemid 39507898)
6. Banci L, et al. (2007) Metal-free superoxide dismutase forms soluble oligomers under physiological conditions: A possible general mechanism for familial ALS. Proc Natl Acad Sci USA 104:11263-11267. (Pubitemid 47175129)
7. Rumfeldt JA, Lepock JR, Meiering EM (2009) Unfolding and folding kinetics of amyotrophic lateral sclerosis-associated mutant Cu,Zn superoxide dismutases. J Mol Biol 385:278-298.
8. Kayatekin C, Zitzewitz JA, Matthews CR (2008) Zinc binding modulates the entire folding free energy surface of human Cu,Zn superoxide dismutase. J Mol Biol 384:540-555.
9. Stroppolo ME, Malvezzi-Campeggi F, Mei G, Rosato N, Desideri A (2000) Role of the tertiary and quaternary structures in the stability of dimeric copper, zinc superoxide dismutases. Arch Biochem Biophys 377:215-218. (Pubitemid 30331880)
10. Mulligan VK, Kerman A, Ho S, Chakrabartty A (2008) Denaturational stress induces formation of zinc-deficient monomers of Cu,Zn superoxide dismutase: Implications for pathogenesis in amyotrophic lateral sclerosis. J Mol Biol 383:424-436.
11. Roberts BR, et al. (2007) Structural characterization of zinc-deficient human superoxide dismutase and implications for ALS. J Mol Biol 373:877-890. (Pubitemid 47505245)
12. Lamb AL, Torres AS, O'Halloran TV, Rosenzweig AC (2001) Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat Struct Biol 8:751-755. (Pubitemid 32803590)
13. Svensson AK, Bilsel O, Kondrashkina E, Zitzewitz JA, Matthews CR (2006) Mapping the folding free energy surface for metal-free human Cu,Zn superoxide dismutase. J Mol Biol 364:1084-1102. (Pubitemid 44765032)
14. Lindberg M, Tȧngrot J, Oliveberg M (2002) Complete change of the protein folding transition state upon circular permutation. Nat Struct Biol 9:818-822.
15. Banci L, Bertini I, Cramaro F, Del Conte R, Viezzoli MS (2003) Solution structure of Apo Cu,Zn superoxide dismutase: Role of metal ions in protein folding. Biochemistry 42:9543-9553. (Pubitemid 37006303)
16. Fersht AR (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (WH Freeman, New York).
17. Nordlund A, Oliveberg M (2006) Folding of Cu/Zn superoxide dismutase suggests structural hotspots for gain of neurotoxic function in ALS: Parallels to precursors in amyloid disease. Proc Natl Acad Sci USA 103:10218-10223. (Pubitemid 44051147)
18. Oliveberg M, Wolynes PG (2005) The experimental survey of protein-folding energy landscapes. Q Rev Biophys 38:245-288. (Pubitemid 44268537)
19. Ferreiro DU, Hegler JA, Komives EA, Wolynes PG (2007) Localizing frustration in native proteins and protein assemblies. Proc Natl Acad Sci USA 104:19819-19824.
20. Gosavi S, Whitford PC, Jennings PA, Onuchic JN (2008) Extracting function from a beta-trefoil folding motif. Proc Natl Acad Sci USA 105:10384-10389.
21. Friel CT, Smith AD, Vendruscolo M, Gsponer G, Radford SE (2009) The mechanism of folding of Im7 reveals competition between functional and kinetic evolutionary constraints. Nat Struct Mol Biol 16:318-324.
22. Wilson CJ, Apiyo D, Wittung-Stafshede P (2004) Role of cofactors in metalloprotein folding Q Rev Biophys 37:285-314. (Pubitemid 41379757)
23. Pandit AD, Krantz BA, Dothager RS, Sosnick TR (2007) Characterizing protein folding transition States using Psi-analysis. Methods Mol Biol 350:83-104.
24. Ferraroni M, et al. (1999) The crystal structure of the monomeric human SOD mutant F50E/G51E/E133Q at atomic resolution. The enzyme mechanism revisited J Mol Biol 288:413-426. (Pubitemid 29221811)
25. Crow JP, Sampson JB, Zhuang Y, Thompson JA, Beckman JS (1997) Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J Neurochem 69:1936-1944. (Pubitemid 27452740)
26. Elam JS, et al. (2003) Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS. Nat Struct Biol 10:461-467. (Pubitemid 36637644)
27. Mäler L, Kowalewski, J (2006) Nuclear Spin Relaxations in Liquids. Theory, Experimnets and Applications. (Taylor and Francis, New York).
28. Brändén CI, Tooze J (1991) Introduction to Protein Structure (Garland, New York).
29. Hornberg A, Logan DT, Marklund SL, Oliveberg M (2007) The coupling between disulphide status, metallation and dimer interface strength in Cu/Zn superoxide dismutase J Mol Biol 365:333-342. (Pubitemid 44838707)
30. Potter SZ, et al. (2007) Binding of a single zinc ion to one subunit of copper-zinc superoxide dismutase apoprotein substantially influences the structure and stability of the entire homodimeric protein. J Am Chem Soc 129:4575-4583. (Pubitemid 46648756)
31. Sandelin E, Nordlund A, Andersen PM, Marklund SS, Oliveberg M (2007) Amyotrophic lateral sclerosis-associated copper/zinc superoxide dismutase mutations preferentially reduce the repulsive charge of the proteins. J Biol Chem 282:21230-21236. (Pubitemid 47099916)
32. Valentine JS, Pantoliano MW, McDonnell PJ, Burger AR, Lippard SJ (1979) pH-dependent migration of copper(II) to the vacant zinc-binding site of zinc-free bovine erythrocyte superoxide dismutase. Proc Natl Acad Sci USA 76:4245-4249.
33. Ahl IM, Lindberg MJ, Tibell LA (2004) Coexpression of yeast copper chaperone (yCCS) and CuZn-superoxide dismutases in Escherichia coli yields protein with high copper contents. Protein Expr Purif 37:311-319.
34. Oliveberg M, Vuilleumier S, Fersht AR (1994) Thermodynamic study of the acid denaturation of barnase and its dependence on ionic strength: Evidence for residual electrostatic interactions in the acid/thermally denatured state. Biochemistry 33:8826-8832. (Pubitemid 24255078)
35. Banci L, Bertini I, Cantini F, D'Onofrio M, Viezzoli MS (2002) Structure and dynamics of copper-free SOD: The protein before binding copper. Protein Sci 11:2479-2492. (Pubitemid 35050673)