Nonnative SOD1 trimer is toxic to motor neurons in a model of amyotrophic lateral sclerosis

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

Volumn 113, Issue 3, 2016, Pages 614-619

  Proctor, Elizabeth A ^a,b   Fee, Lanette ^b   Tao, Yazhong ^b   Redler, Rachel L ^b   Fay, James M ^b   Zhang, Yuliang ^c   Lv, Zhengjian ^c   Mercer, Ian P ^b   Deshmukh, Mohanish ^b   Lyubchenko, Yuri L ^c   Dokholyan, Nikolay V ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MUTANT PROTEIN; OLIGOMER; PROTEIN AGGREGATE; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME STABILITY; METHODOLOGY; MOTONEURON; NERVE CELL NECROSIS; NEUROTOXICITY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN MISFOLDING; STOICHIOMETRY; ANIMAL; BIOLOGICAL MODEL; CELL DEATH; CELL LINE; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; MOLECULAR MODEL; MUTATION; PATHOLOGY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL DEATH; CELL LINE; ENZYME STABILITY; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOTOR NEURONS; MUTANT PROTEINS; MUTATION; PROTEIN AGGREGATES; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SUPEROXIDE DISMUTASE;

EID: 84955062355     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516725113     Document Type: Article

References (53)

1. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: Deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2(11):806-819.
2. Rothstein JD (2009) Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol 65(Suppl 1):S3-S9.
3. Walker LC, LeVine H, 3rd (2012) Corruption and spread of pathogenic proteins in neurodegenerative diseases. J Biol Chem 287(40):33109-33115.
4. Redler RL, Dokholyan NV (2012) The complex molecular biology of amyotrophic lateral sclerosis (ALS). Prog Mol Biol Transl Sci 107:215-262.
5. Zetterström P, et al. (2007) Soluble misfolded subfractions of mutant superoxide dismutase-1s are enriched in spinal cords throughout life in murine ALS models. Proc Natl Acad Sci USA 104(35):14157-14162.
6. Kirkitadze MD, Bitan G, Teplow DB (2002) Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: The emerging role of oligomeric assemblies. J Neurosci Res 69(5):567-577.
7. Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431(7010):805-810.
8. Caughey B, Lansbury PT (2003) Protofibrils, pores, fibrils, and neurodegeneration: Separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 26:267-298.
9. Bieschke J, et al. (2012) Small-molecule conversion of toxic oligomers to nontoxic β-sheet-rich amyloid fibrils. Nat Chem Biol 8(1):93-101.
10. Rakhit R, et al. (2007) An immunological epitope selective for pathological monomermisfolded SOD1 in ALS. Nat Med 13(6):754-759.
11. Jonsson PA, et al. (2004) Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain 127(Pt 1):73-88.
12. Israelson A, et al. (2010) Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron 67(4):575-587.
13. Pedrini S, et al. (2010) ALS-linked mutant SOD1 damages mitochondria by promoting conformational changes in Bcl-2. Hum Mol Genet 19(15):2974-2986.
14. Nishitoh H, et al. (2008) ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 22(11):1451-1464.
15. Redler RL, Fee L, Fay JM, Caplow M, Dokholyan NV (2014) Non-native soluble oligomers of Cu/Zn superoxide dismutase (SOD1) contain a conformational epitope linked to cytotoxicity in amyotrophic lateral sclerosis (ALS). Biochemistry 53(14):2423-2432.
16. 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.
17. Brotherton TE, et al. (2012) Localization of a toxic form of superoxide dismutase 1 protein to pathologically affected tissues in familial ALS. Proc Natl Acad Sci USA 109(14):5505-5510.
18. Rotunno MS, et al. (2014) Identification of a misfolded region in superoxide dismutase 1 that is exposed in amyotrophic lateral sclerosis. J Biol Chem 289(41):28527-28538.
19. 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(27):11263-11267.
20. Banci L, et al. (2008) SOD1 and amyotrophic lateral sclerosis: mutations and oligomerization. PloS One 3(2):e1677.
21. Luchinat E, et al. (2014) In-cell NMR reveals potential precursor of toxic species from SOD1 fALS mutants. Nat Commun 5:5502.
22. Auclair JR, Boggio KJ, Petsko GA, Ringe D, Agar JN (2010) Strategies for stabilizing superoxide dismutase (SOD1), the protein destabilized in the most common form of familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 107(50):21394-21399.
23. Korzhnev DM, Religa TL, Banachewicz W, Fersht AR, Kay LE (2010) A transient and lowpopulated protein-folding intermediate at atomic resolution. Science 329(5997):1312-1316.
24. Laganowsky A, et al. (2012) Atomic view of a toxic amyloid small oligomer. Science 335(6073):1228-1231.
25. Khare SD, Caplow M, Dokholyan NV (2004) The rate and equilibrium constants for a multistep reaction sequence for the aggregation of superoxide dismutase in amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 101(42):15094-15099.
26. Wilcox KC, et al. (2009) Modifications of superoxide dismutase (SOD1) in human erythrocytes: A possible role in amyotrophic lateral sclerosis. J Biol Chem 284(20):13940-13947.
27. Hubbard SJ, Campbell SF, Thornton JM (1991) Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. J Mol Biol 220(2):507-530.
28. Rakhit R, et al. (2004) Monomeric Cu, Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis. J Biol Chem 279(15):15499-15504.
29. Ding F, Tsao D, Nie H, Dokholyan NV (2008) Ab initio folding of proteins with all-atom discrete molecular dynamics. Structure 16(7):1010-1018.
30. Deng HX, et al. (1993) Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science 261(5124):1047-1051.
31. Juneja T, Pericak-Vance MA, Laing NG, Dave S, Siddique T (1997) Prognosis in familial amyotrophic lateral sclerosis: Progression and survival in patients with glu100gly and ala4val mutations in Cu,Zn superoxide dismutase. Neurology 48(1):55-57.
32. Bruijn LI, Miller TM, Cleveland DW (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci 27:723-749.
33. Joyce PI, Fratta P, Fisher EMC, Acevedo-Arozena A (2011) SOD1 and TDP-43 animal models of amyotrophic lateral sclerosis: Recent advances in understanding disease toward the development of clinical treatments. Mamm Genome 22(7-8):420-448.
34. Rotunno MS, Bosco DA (2013) An emerging role for misfolded wild-type SOD1 in sporadic ALS pathogenesis. Front Cell Neurosci 7:253.
35. Shibata N, Asayama K, Hirano A, Kobayashi M (1996) Immunohistochemical study on superoxide dismutases in spinal cords from autopsied patients with amyotrophic lateral sclerosis. Dev Neurosci 18(5-6):492-498.
36. Shibata N, et al. (1994) Cu/Zn superoxide dismutase-like immunoreactivity in Lewy body-like inclusions of sporadic amyotrophic lateral sclerosis. Neurosci Lett 179(1-2): 149-152.
37. Gruzman A, et al. (2007) Common molecular signature in SOD1 for both sporadic and familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 104(30):12524-12529.
38. Goscin SA, Fridovich I (1972) The purification and properties of superoxide dismutase from Saccharomyces cerevisiae. Biochim Biophys Acta 289(2):276-283.
39. Shlyakhtenko LS, Gall AA, Lyubchenko YL (2013) Mica functionalization for imaging of DNA and protein-DNA complexes with atomic force microscopy. Methods Mol Biol 931:295-312.
40. Portillo AM, Krasnoslobodtsev AV, Lyubchenko YL (2012) Effect of electrostatics on aggregation of prion protein Sup35 peptide. J Phys Condens Matter 24(16):164205.
41. Miyagi A, Ando T, Lyubchenko YL (2011) Dynamics of nucleosomes assessed with time-lapse high-speed atomic force microscopy. Biochemistry 50(37):7901-7908.
42. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20(18):3551-3567.
43. Go N, Abe H (1981) Noninteracting local-structure model of folding and unfolding transition in globular proteins. I. Formulation. Biopolymers 20(5):991-1011.
44. Hubbard SJ, Eisenmenger F, Thornton JM (1994) Modeling studies of the change in conformation required for cleavage of limited proteolytic sites. Protein Sci 3(5): 757-768.
45. Ding F, Borreguero JM, Buldyrey SV, Stanley HE, Dokholyan NV (2003) Mechanism for the alpha-helix to beta-hairpin transition. Proteins 53(2):220-228.
46. 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(2):215-218.
47. Dokholyan NV, Buldyrev SV, Stanley HE, Shakhnovich EI (1998) Discrete molecular dynamics studies of the folding of a protein-like model. Fold Des 3(6):577-587.
48. Zhou Y, Karplus M (1997) Folding thermodynamics of a model three-helix-bundle protein. Proc Natl Acad Sci USA 94(26):14429-14432.
49. Okamoto Y (2004) Generalized-ensemble algorithms: enhanced sampling techniques for Monte Carlo and molecular dynamics simulations. J Mol Graph Model 22(5): 425-439.
50. Ramachandran S, Kota P, Ding F, Dokholyan NV (2011) Automated minimization of steric clashes in protein structures. Proteins 79(1):261-270.
51. Kota P, Ding F, Ramachandran S, Dokholyan NV (2011) Gaia: Automated quality assessment of protein structure models. Bioinformatics 27(16):2209-2215.
52. Yin S, Ding F, Dokholyan NV (2007) Modeling backbone flexibility improves protein stability estimation. Structure 15(12):1567-1576.
53. Yin S, Ding F, Dokholyan NV (2007) Eris: An automated estimator of protein stability. Nat Methods 4(6):466-467.