Mechanism for transforming cytosolic SOD1 into integral membrane proteins of organelles by ALS-causing mutations

Biochimica et Biophysica Acta - Biomembranes

Volumn , Issue Part A, 2015, Pages 1-7

  Lim, Liangzhong ^a   Lee, Xiaowen ^a   Song, Jianxing ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Amphiphilicity; Amyotrophic lateral sclerosis (ALS); Membrane protein; NMR spectroscopy; Superoxide dismutase 1 (SOD1)

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; DISULFIDE; MEMBRANE PROTEIN; ZINC; SUPEROXIDE DISMUTASE;

AMPHIPHILICITY; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CELLULAR PARAMETERS; CYTOSOL; DEPLETION; ENZYME CONFORMATION; ENZYME STRUCTURE; GENE; GENE MUTATION; GENETIC ASSOCIATION; GENETIC TRANSFORMATION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SOD1 GENE; ZINC DEPLETION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; MOLECULAR GENETICS; MUTATION; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; CYTOSOL; DISULFIDES; HUMANS; INTRACELLULAR MEMBRANES; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; ORGANELLES; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; SUPEROXIDE DISMUTASE; ZINC;

EID: 84988220726     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.10.002     Document Type: Article

References (37)

1. L.I. Bruijn, T.M. Miller, and D.W. Cleveland Unraveling the mechanisms involved in motor neuron degeneration in ALS Annu. Rev. Neurosci. 27 2004 723 749
2. S. Da Cruz, and D.W. Cleveland Understanding the role of TDP-43 and FUS/TLS in ALS and beyond Curr. Opin. Neurobiol. 21 6 2011 904 919
3. M.S. Rotunno, and D.A. Bosco An emerging role for misfolded wild-type SOD1 in sporadic ALS pathogenesis Front. Cell. Neurosci. 7 2013 253
4. D.R. Rosen, T. Siddique, D. Patterson, D.A. Figlewicz, and P. Sapp Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Nature 362 6415 1993 59 62
5. O. Abel, J.F. Powell, P.M. Andersen, and A. Al-Chalabi ALSoD: a user-friendly online bioinformatics tool for amyotrophic lateral sclerosis genetics Hum. Mutat. 33 9 2012 1345 1351
6. J.J. Perry, D.S. Shin, E.D. Getzoff, and J.A. Tainer The structural biochemistry of the superoxide dismutases Biochim. Biophys. Acta 1804 2 2010 245 262
7. P. Zetterström, H.G. Stewart, D. Bergemalm, P.A. Jonsson, and K.S. Graffmo Soluble misfolded subfractions of mutant superoxide dismutase-1s are enriched in spinal cords throughout life in murine ALS models Proc. Natl. Acad. Sci. U. S. A. 104 35 2007 14157 14162
8. T.E. Brotherton, Y. Li, and J.D. Glass Cellular toxicity of mutant SOD1 protein is linked to an easily soluble, non-aggregated form in vitro Neurobiol. Dis. 49C 2012 49 56
9. P.K. Auluck, G. Caraveo, and S. Lindquist α-Synuclein: membrane interactions and toxicity in Parkinson's disease Annu. Rev. Cell Dev. Biol. 26 2010 211 233
10. R.A. Bodner, T.F. Outeiro, S. Altmann, M.M. Maxwell, and S.H. Cho Pharmacological promotion of inclusion formation: a therapeutic approach for Huntington's and Parkinson's diseases Proc. Natl. Acad. Sci. U. S. A. 103 11 2006 4246 4251
11. C. Vande Velde, T.M. Miller, N.R. Cashman, and D.W. Cleveland Selective association of misfolded ALS-linked mutant SOD1 with the cytoplasmic face of mitochondria Proc. Natl. Acad. Sci. U. S. A. 105 10 2008 4022 4027
12. J. Liu, C. Lillo, P.A. Jonsson, C. Vande Velde, and C.M. Ward Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria Neuron 43 1 2004 5 17
13. A. Israelson, N. Arbel, S. Da Cruz, H. Ilieva, and K. Yamanaka Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS Neuron 67 4 2010 575 587
14. K. Homma, T. Fujisawa, N. Tsuburaya, N. Yamaguchi, and H. Kadowaki SOD1 as a molecular switch for initiating the homeostatic ER stress response under zinc deficiency Mol. Cell 52 1 2013 75 86
15. J.S. Zu, H.X. Deng, T.P. Lo, H. Mitsumoto, and M.S. Ahmed Exon 5 encoded domain is not required for the toxic function of mutant SOD1 but essential for the dismutase activity: identification and characterization of two new SOD1 mutations associated with familial amyotrophic lateral sclerosis Neurogenetics 1 1 1997 65 71
16. J. Song Insight into "insoluble proteins" with pure water FEBS Lett. 583 6 2009 953 959
17. J. Song Why do proteins aggregate? "Intrinsically insoluble proteins" and "dark mediators" revealed by studies on "insoluble proteins" solubilized in pure water F1000Res. 2 2013 94
18. H. Qin, L. Lim, Y. Wei, G. Gupta, and J. Song Resolving the paradox for protein aggregation diseases: a common mechanism for aggregated proteins to initially attack membranes without needing aggregates F1000Res. 2 2013 221
19. H. Qin, W. Wang, and J. Song ALS-causing P56S mutation and splicing variation on the hVAPB MSP domain transform its β-sandwich fold into lipid-interacting helical conformations Biochem. Biophys. Res. Commun. 431 3 2013 398 403
20. H.J. Dyson, and P.E. Wright Unfolded proteins and protein folding studied by NMR Chem. Rev. 104 8 2004 3607 3622
21. L. Banci, I. Bertini, F. Cantini, N. D'Amelio, and E. Gaggelli Human SOD1 before harboring the catalytic metal: solution structure of copper-depleted, disulfide-reduced form J. Biol. Chem. 281 4 2006 2333 2337
22. C.K. Bruns, and R.R. Kopito Impaired post-translational folding of familial ALS-linked Cu, Zn superoxide dismutase mutants EMBO J. 26 3 2007 855 866
23. S.H. White, and W.C. Wimley Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365
24. A.S. Ladokhin, and S.H. White Folding of amphipathic alpha-helices on membranes: energetics of helix formation by melittin J. Mol. Biol. 285 4 1999 1363 1369
25. R. Bussell Jr., T.F. Ramlall, and D. Eliezer Helix periodicity, topology, and dynamics of membrane-associated alpha-synuclein Protein Sci. 14 4 2005 862 872
26. T.S. Ulmer, A. Bax, N.B. Cole, and R.L. Nussbaum Structure and dynamics of micelle-bound human alpha-synuclein J. Biol. Chem. 280 10 2005 9595 9603
27. P. Mazumder, J.E. Suk, and T.S. Ulmer Insight into α-synuclein plasticity and misfolding from differential micelle binding J. Phys. Chem. B 117 39 2013 11448 11459
28. S.Y. Lee, and W. Parker Amphiphilic α-helical potential: a putative folding motif adding few constraints to protein evolution J. Mol. Evol. 73 3-4 2011 166 180
29. R. Jahn, and T.C. Südhof Membrane fusion and exocytosis Annu. Rev. Biochem. 68 1999 863 911
30. M.C. Lee, L. Orci, S. Hamamoto, E. Futai, M. Ravazzola, and R. Schekman Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle Cell 122 4 2005 605 617
31. K. Elfrink, J. Ollesch, J. Stöhr, D. Willbold, and D. Riesner Structural changes of membrane-anchored native PrP(C) Proc. Natl. Acad. Sci. U. S. A. 105 31 2008 10815 10819
32. H. Shao, S. Jao, K. Ma, and M.G. Zagorski Solution structures of micelle-bound amyloid beta-(1-40) and beta-(1-42) peptides of Alzheimer's disease J. Mol. Biol. 285 2 1999 755 773
33. G. Künze, P. Barré, H.A. Scheidt, and D. Eliezer Binding of the three-repeat domain of tau to phospholipid membranes induces an aggregated-like state of the protein Biochim. Biophys. Acta 1818 9 2012 2302 2313
34. K.B. Kegel, E. Sapp, J. Yoder, B. Cuiffo, and L. Sobin Huntingtin associates with acidic phospholipids at the plasma membrane J. Biol. Chem. 280 43 2005 36464 36473
35. J.R. Brender, S. Salamekh, and A. Ramamoorthy Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective Acc. Chem. Res. 45 3 2012 454 462
36. B.L. Kagan, H. Jang, R. Capone, F. Teran Arce, and S. Ramachandran Antimicrobial properties of amyloid peptides Mol. Pharm. 9 4 2012 708 717
37. Z. Jiang, M. de Messieres, and J.C. Lee Membrane remodeling by α-synuclein and effects on amyloid formation J. Am. Chem. Soc. 135 43 2013 15970 15973