SOD1 exhibits allosteric frustration to facilitate metal binding affinity

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

Volumn 110, Issue 10, 2013, Pages 3871-3876

  Das, Atanu ^a   Plotkin, Steven S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Allosteric communication; Cooperativity; Frustrated contacts; Protein misfolding

Indexed keywords

COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; ZINC;

ALLOSTERISM; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA FINGERPRINTING; GENE MUTATION; GENETIC LINKAGE; GENETIC VARIABILITY; PRIORITY JOURNAL;

ALLOSTERIC REGULATION; AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; APOENZYMES; BIOMECHANICS; BIOPHYSICAL PHENOMENA; ENZYME STABILITY; GENETIC VARIATION; HUMANS; KINETICS; METALS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE DELETION; SUPEROXIDE DISMUTASE;

EID: 84874620335     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1216597110     Document Type: Article

References (40)

1. Monod J, Wyman J, Changeux J-P (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12:88-118.
2. Koshland DE, Jr., Némethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5(1): 365-385.
3. Weber G (1975) Energetics of ligand binding to proteins. Adv Protein Chem 29:1-83.
4. Gunasekaran K, Ma B, Nussinov R (2004) Is allostery an intrinsic property of all dynamic proteins? Proteins 57(3):433-443.
5. Ferreiro DU, Hegler JA, Komives EA, Wolynes PG (2011) On the role of frustration in the energy landscapes of allosteric proteins. Proc Natl Acad Sci USA 108(9):3499-3503.
6. Daily MD, Gray JJ (2007) Local motions in a benchmark of allosteric proteins. Proteins 67(2):385-399.
7. Gardino AK, et al. (2009) Transient non-native hydrogen bonds promote activation of a signaling protein. Cell 139(6):1109-1118.
8. Plotkin SS, Wolynes PG (2003) Buffed energy landscapes: Another solution to the kinetic paradoxes of protein folding. Proc Natl Acad Sci USA 100(8):4417-4422.
9. Christopoulos A (2002) Allosteric binding sites on cell-surface receptors: Novel targets for drug discovery. Nat Rev Drug Discov 1(3):198-210.
10. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366.
11. 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 160(2):181-217.
12. Bertini I, Manganl S, Viezzoli MS (1998) Structure and Properties of Copper-Zinc Superoxide Dismutases. Adv Inorg Chem, ed Sykes A (Academic, San Diego), Vol 45, pp 127-250.
13. Valentine JS, Doucette PA, Zittin Potter S (2005) Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu Rev Biochem 74:563-593.
14. Getzoff ED, et al. (1992) Faster superoxide dismutase mutants designed by enhancing electrostatic guidance. Nature 358(6384):347-351.
15. Bosco DA, et al. (2010) Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat Neurosci 13(11):1396-1403.
16. Forsberg K, et al. (2010) Novel antibodies reveal inclusions containing non-native SOD1 in sporadic ALS patients. PLoS ONE 5(7):e11552.
17. Chiti F, Dobson CM (2009) Amyloid formation by globular proteins under native conditions. Nat Chem Biol 5(1):15-22.
18. 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(27):10218-10223.
19. 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(6):461-467.
20. Banci L, et al. (2005) Fully metallated S134N Cu, Zn-superoxide dismutase displays abnormal mobility and intermolecular contacts in solution. J Biol Chem 280(43): 35815-35821.
21. Jonsson PA, et al. (2004) Minute quantities of misfolded mutant superoxide dismutase- 1 cause amyotrophic lateral sclerosis. Brain 127(Pt 1):73-88.
22. Grad LI, et al. (2011) Intermolecular transmission of superoxide dismutase 1 misfolding in living cells. Proc Natl Acad Sci USA 108(39):16398-16403.
23. Das A, Plotkin SS (2013) Mechanical probes of SOD1 predict systematic trends in metal and dimer affinity of ALS-associated mutants. J Mol Biol, 10.1016/j.jmb.2012.12.022.
24. Khare SD, Dokholyan NV (2006) Common dynamical signatures of familial amyotrophic lateral sclerosis-associated structurally diverse Cu, Zn superoxide dismutase mutants. Proc Natl Acad Sci USA 103(9):3147-3152.
25. 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(15):4575-4583.
26. Schuyler AD, Carlson HA, Feldman EL (2011) Computational methods for identifying a layered allosteric regulatory mechanism for ALS-causing mutations of Cu-Zn superoxide dismutase 1. Proteins 79(2):417-427.
27. Edwards SA, Wagner J, Gräter F (2012) Dynamic prestress in a globular protein. PLOS Comput Biol 8(5):e1002509.
28. Whitford PC, et al. (2009) An all-atom structure-based potential for proteins: Bridging minimal models with all-atom empirical forcefields. Proteins 75(2):430-441.
29. Furukawa Y, O'Halloran TV (2005) Amyotrophic lateral sclerosis mutations have the greatest destabilizing effect on the apo- and reduced form of SOD1, leading to unfolding and oxidative aggregation. J Biol Chem 280(17):17266-17274.
30. Hörnberg 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(2):333-342.
31. 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(32):9543-9553.
32. Bertini I, Piccioli M, Viezzoli MS, Chiu CY, Mullenbach GT (1994) A spectroscopic characterization of a monomeric analog of copper, zinc superoxide dismutase. Eur Biophys J 23(3):167-176.
33. Li L, Guest W, Huang A, Plotkin SS, Cashman NR (2009) Immunological mimicry of PrPC-PrPSc interactions: Antibody-induced PrP misfolding. Protein Eng Des Sel 22(8): 523-529.
34. Cheng H, et al. (2009) Autoinhibitory interactions between the PDZ2 and C-terminal domains in the scaffolding protein NHERF1. Structure 17(5):660-669.
35. Benson NC, Daggett V (2008) Dynameomics: Large-scale assessment of native protein flexibility. Protein Sci 17(12):2038-2050.
36. Jenik M, et al. (2012) Protein frustratometer: a tool to localize energetic frustration in protein molecules. Nucleic Acids Res 40:W348-W351.
37. Roberts BR, et al. (2007) Structural characterization of zinc-deficient human superoxide dismutase and implications for ALS. J Mol Biol 373(4):877-890.
38. Museth AK, Brorsson AC, Lundqvist M, Tibell LA, Jonsson BH (2009) The ALS-associated mutation G93A in human copper-zinc superoxide dismutase selectively destabilizes the remote metal binding region. Biochemistry 48(37):8817-8829.
39. Nordlund A, et al. (2009) Functional features cause misfolding of the ALS-provoking enzyme SOD1. Proc Natl Acad Sci USA 106(24):9667-9672.
40. Bryan PN (2000) Protein engineering of subtilisin. Biochim Biophys Acta 1543(2): 203-222.