α-Synuclein in Central Nervous System and from Erythrocytes, Mammalian Cells, and Escherichia coli Exists Predominantly as Disordered Monomer

Journal of Biological Chemistry - Tập 287 Số 19 - Trang 15345-15364 - 2012
Bruno Fauvet1, Martial Mbefo1, Mohamed-Bilal Fares1, Carole Desobry1, Sarah Michael2, Mustafa T. Ardah3, Elpida Tsika4, Philippe Coune5, Michel Prudent6, Niels Lion6, David Eliezer7, Darren J. Moore4, Bernard L. Schneider5, Patrick Aebischer5, Omar M. A. El‐Agnaf3, Eliezer Masliah2, Hilal A. Lashuel1
1Laboratory of Molecular and Chemical Biology of Neurodegeneration, Brain Mind Institute, Station 19, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland,
2Department of Neurosciences, School of Medicine, University of California at San Diego, La Jolla, California 92093,
3Department of Biochemistry, Faculty of Medicine and Health Sciences, United Arab Emirates University, Al Ain 15551, United Arab Emirates,
4Laboratory of Molecular Neurodegenerative Research, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland
5Neurodegenerative Disease Laboratory, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland,
6Service Régional Vaudois de Transfusion Sanguine, Route de la Corniche 2, 1066 Epalinges, Switzerland, and
7Department of Biochemistry and Program in Structural Biology, Weill Cornell Medical College, New York, New York 10065

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Bartels, 2011, α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation, Nature, 477, 107, 10.1038/nature10324

Wang, 2011, A soluble α-synuclein construct forms a dynamic tetramer, Proc. Natl. Acad. Sci., 108, 17797, 10.1073/pnas.1113260108

Spillantini, 1998, α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson disease and dementia with Lewy bodies, Proc. Natl. Acad. Sci., 95, 6469, 10.1073/pnas.95.11.6469

Baba, 1998, Aggregation of α-synuclein in Lewy bodies of sporadic Parkinson disease and dementia with Lewy bodies, Am. J. Pathol., 152, 879

Cookson, 2009, α-Synuclein and neuronal cell death, Mol. Neurodegener., 4, 9, 10.1186/1750-1326-4-9

Weinreb, 1996, NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded, Biochemistry, 35, 13709, 10.1021/bi961799n

Conway, 1998, Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson disease, Nat. Med., 4, 1318, 10.1038/3311

Chartier-Harlin, 2004, α-Synuclein locus duplication as a cause of familial Parkinson disease, Lancet, 364, 1167, 10.1016/S0140-6736(04)17103-1

Singleton, 2003, α-Synuclein locus triplication causes Parkinson disease, Science, 302, 841, 10.1126/science.1090278

Polymeropoulos, 1997, Mutation in the α-synuclein gene identified in families with Parkinson disease, Science, 276, 2045, 10.1126/science.276.5321.2045

Zarranz, 2004, The new mutation, E46K, of α-synuclein causes Parkinson and Lewy body dementia, Ann. Neurol., 55, 164, 10.1002/ana.10795

Muñoz, 1997, Identification of Spanish familial Parkinson disease and screening for the A53T mutation of the α-synuclein gene in early onset patients, Neurosci. Lett., 235, 57, 10.1016/S0304-3940(97)00710-6

Duda, 2000, Widespread nitration of pathological inclusions in neurodegenerative synucleinopathies, Am. J. Pathol., 157, 1439, 10.1016/S0002-9440(10)64781-5

Giasson, 2000, Oxidative damage linked to neurodegeneration by selective α-synuclein nitration in synucleinopathy lesions, Science, 290, 985, 10.1126/science.290.5493.985

Souza, 2000, Dityrosine cross-linking promotes formation of stable α-synuclein polymers. Implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies, J. Biol. Chem., 275, 18344, 10.1074/jbc.M000206200

Yamin, 2003, Nitration inhibits fibrillation of human α-synuclein in vitro by formation of soluble oligomers, FEBS Lett., 542, 147, 10.1016/S0014-5793(03)00367-3

Binolfi, 2006, Interaction of α-synuclein with divalent metal ions reveals key differences: a link between structure, binding specificity, and fibrillation enhancement, J. Am. Chem. Soc., 128, 9893, 10.1021/ja0618649

Santner, 2010, Metalloproteomics and metal toxicology of α-synuclein, Metallomics, 2, 378, 10.1039/b926659c

Lücking, 2000, α-Synuclein and Parkinson disease, Cell. Mol. Life Sci., 57, 1894, 10.1007/PL00000671

Uversky, 2009, Biophysics of Parkinson disease. Structure and aggregation of α-synuclein, Curr. Protein Pept. Sci., 10, 483, 10.2174/138920309789351921

Ringrose, 2008, Highly efficient depletion strategy for the two most abundant erythrocyte-soluble proteins improves proteome coverage dramatically, J. Proteome Res., 7, 3060, 10.1021/pr8001029

Han, 2010, A comparative study of common techniques used to measure hemolysis in stored red cell concentrates, Vox Sang., 98, 116, 10.1111/j.1423-0410.2009.01249.x

Eliezer, 2001, Conformational properties of α-synuclein in its free and lipid-associated states, J. Mol. Biol., 307, 1061, 10.1006/jmbi.2001.4538

Delaglio, 1995, NMRPipe. A multidimensional spectral processing system based on UNIX pipes, J Biomol NMR, 6, 277, 10.1007/BF00197809

Johnson, 1994, NMR View. A Computer Program for the Visualization and Analysis of NMR Data, J. Biomol. NMR, 4, 603, 10.1007/BF00404272

Wishart, 1995, 1H, 13C, and 15N chemical shift referencing in biomolecular NMR, J. Biomol. NMR, 6, 135, 10.1007/BF00211777

Tinsley, 2010, Sensitive and specific detection of α-synuclein in human plasma, J. Neurosci. Res., 88, 2693, 10.1002/jnr.22417

Perrin, 2003, Epitope mapping and specificity of the anti-α-synuclein monoclonal antibody Syn-1 in mouse brain and cultured cell lines, Neurosci. Lett., 349, 133, 10.1016/S0304-3940(03)00781-X

Mbefo, 2010, Phosphorylation of synucleins by members of the Polo-like kinase family, J. Biol. Chem., 285, 2807, 10.1074/jbc.M109.081950

Lee, 2002, Human α-synuclein-harboring familial Parkinson disease-linked Ala-53 → Thr mutation causes neurodegenerative disease with α-synuclein aggregation in transgenic mice, Proc. Natl. Acad. Sci., 99, 8968, 10.1073/pnas.132197599

Rockenstein, 1995, Levels and alternative splicing of amyloid β protein precursor (APP) transcripts in brains of APP transgenic mice and humans with Alzheimer disease, J. Biol. Chem., 270, 28257, 10.1074/jbc.270.47.28257

Dusonchet, 2009, Targeted overexpression of the parkin substrate Pael-R in the nigrostriatal system of adult rats to model Parkinson disease, Neurobiol Dis, 35, 32, 10.1016/j.nbd.2009.03.013

Lennox, 1989, Diffuse Lewy body disease. Correlative neuropathology using anti-ubiquitin immunocytochemistry, J. Neurol. Neurosurg. Psychiatry, 52, 1236, 10.1136/jnnp.52.11.1236

Pham, 2010, Progressive accumulation of amyloid-α oligomers in Alzheimer disease and in amyloid precursor protein transgenic mice is accompanied by selective alterations in synaptic scaffold proteins, FEBS J., 277, 3051, 10.1111/j.1742-4658.2010.07719.x

Anderson, 2006, Phosphorylation of Ser-129 is the dominant pathological modification of α-synuclein in familial and sporadic Lewy body disease, J. Biol. Chem., 281, 29739, 10.1074/jbc.M600933200

Ohrfelt, 2011, Identification of novel α-synuclein isoforms in human brain tissue by using an online nanoLC-ESI-FTICR-MS method, Neurochem. Res., 36, 2029, 10.1007/s11064-011-0527-x

Uéda, 1993, Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease, Proc. Natl. Acad. Sci., 90, 11282, 10.1073/pnas.90.23.11282

Jakes, 1994, Identification of two distinct synucleins from human brain, FEBS Lett., 345, 27, 10.1016/0014-5793(94)00395-5

Anderson, 2010, Identification of a helical intermediate in trifluoroethanol-induced α-synuclein aggregation, Proc. Natl. Acad. Sci., 107, 18850, 10.1073/pnas.1012336107

Bussell, 2001, Residual structure and dynamics in Parkinson disease-associated mutants of α-synuclein, J. Biol. Chem., 276, 45996, 10.1074/jbc.M106777200

Georgieva, 2008, Membrane-bound α-synuclein forms an extended helix. Long distance pulsed ESR measurements using vesicles, bicelles, and rod-like micelles, J. Am. Chem. Soc., 130, 12856, 10.1021/ja804517m

Georgieva, 2010, The lipid-binding domain of wild type and mutant α-synuclein. Compactness and interconversion between the broken and extended helix forms, J. Biol. Chem., 285, 28261, 10.1074/jbc.M110.157214

Paleologou, 2010, Phosphorylation at Ser-87 is enhanced in synucleinopathies, inhibits α-synuclein oligomerization, and influences synuclein-membrane interactions, J. Neurosci., 30, 3184, 10.1523/JNEUROSCI.5922-09.2010

Paleologou, 2008, Phosphorylation at Ser-129 but not the phosphomimics S129E/D inhibits the fibrillation of α-synuclein, J. Biol. Chem., 283, 16895, 10.1074/jbc.M800747200

Rospigliosi, 2009, E46K Parkinson-linked mutation enhances C-terminal to N-terminal contacts in α-synuclein, J. Mol. Biol., 388, 1022, 10.1016/j.jmb.2009.03.065

Sung, 2007, Residual structure, backbone dynamics, and interactions within the synuclein family, J. Mol. Biol., 372, 689, 10.1016/j.jmb.2007.07.008

Croke, 2008, Hydrogen exchange of monomeric α-synuclein shows unfolded structure persists at physiological temperature and is independent of molecular crowding in Escherichia coli, Protein Sci., 17, 1434, 10.1110/ps.033803.107

Fernández, 2004, NMR of α-synuclein-polyamine complexes elucidates the mechanism and kinetics of induced aggregation, EMBO J., 23, 2039, 10.1038/sj.emboj.7600211

Li, 2009, 19F NMR studies of α-synuclein conformation and fibrillation, Biochemistry, 48, 8578, 10.1021/bi900872p

McNulty, 2006, Temperature-induced reversible conformational change in the first 100 residues of α-synuclein, Protein Sci., 15, 602, 10.1110/ps.051867106

Rasia, 2005, Structural characterization of copper(II) binding to α-synuclein. Insights into the bioinorganic chemistry of Parkinson disease, Proc. Natl. Acad. Sci., 102, 4294, 10.1073/pnas.0407881102

Segers-Nolten, 2008, Tissue transglutaminase modulates α-synuclein oligomerization, Protein Sci., 17, 1395, 10.1110/ps.036103.108

Wu, 2009, Structural reorganization of α-synuclein at low pH observed by NMR and REMD simulations, J. Mol. Biol., 391, 784, 10.1016/j.jmb.2009.06.063

Azeredo da Silveira, 2009, Phosphorylation does not prompt, nor prevent, the formation of α-synuclein toxic species in a rat model of Parkinson disease, Hum. Mol. Genet., 18, 872

El-Agnaf, 2006, Detection of oligomeric forms of α-synuclein protein in human plasma as a potential biomarker for Parkinson's disease, FASEB J., 20, 419, 10.1096/fj.03-1449com

Lee, 2001, Self-oligomerization and protein aggregation of α-synuclein in the presence of Coomassie Brilliant Blue, Eur. J. Biochem., 268, 295, 10.1046/j.1432-1033.2001.01877.x

Paik, 1999, Copper(II)-induced self-oligomerization of α-synuclein, Biochem. J., 340, 821, 10.1042/bj3400821

Cole, 2002, Lipid droplet binding and oligomerization properties of the Parkinson disease protein α-synuclein, J. Biol. Chem., 277, 6344, 10.1074/jbc.M108414200

Shaikh, 2008, Advanced glycation end products induce in vitro cross-linking of α-synuclein and accelerate the process of intracellular inclusion body formation, J. Neurosci. Res., 86, 2071, 10.1002/jnr.21644

Walker, 2002, 57

Selkoe, 2011, Nondenaturing purification of α-synuclein from erythrocytes, Protocol Exchange

Smith, 1988, Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase, Gene, 67, 31, 10.1016/0378-1119(88)90005-4

Lim, 1994, Three-dimensional structure of Schistosoma japonicum glutathione S-transferase fused with a six-amino acid conserved neutralizing epitope of gp41 from HIV, Protein Sci., 3, 2233, 10.1002/pro.5560031209

Parker, 1990, Crystallization of glutathione S-transferase from human placenta, J. Mol. Biol., 213, 221, 10.1016/S0022-2836(05)80183-4

Ji, 1992, The three-dimensional structure of a glutathione S-transferase from the mu gene class. Structural analysis of the binary complex of isoenzyme 3–3 and glutathione at 2.2-Å resolution, Biochemistry, 31, 10169, 10.1021/bi00157a004

Ferguson, 1964, Starch gel electrophoresis. Application to the classification of pituitary proteins and polypeptides, Metabolism, 13, 985, 10.1016/S0026-0495(64)80018-4

Wu, 2008, Characterization of conformational and dynamic properties of natively unfolded human and mouse α-synuclein ensembles by NMR. Implication for aggregation, J. Mol. Biol., 378, 1104, 10.1016/j.jmb.2008.03.017

Marsh, 2006, Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein. Implications for fibrillation, Protein Sci., 15, 2795, 10.1110/ps.062465306

Bertoncini, 2005, Familial mutants of α-synuclein with increased neurotoxicity have a destabilized conformation, J. Biol. Chem., 280, 30649, 10.1074/jbc.C500288200

Kang, 2003, Enhanced oligomerization of the α-synuclein mutant by the Cu,Zn-superoxide dismutase and hydrogen peroxide system, Mol. Cells, 15, 87, 10.1016/S1016-8478(23)13712-5

Krishnan, 2003, Oxidative dimer formation is the critical rate-limiting step for Parkinson disease α-synuclein fibrillogenesis, Biochemistry, 42, 829, 10.1021/bi026528t

Dedmon, 2005, Mapping long range interactions in α-synuclein using spin-label NMR and ensemble molecular dynamics simulations, J. Am. Chem. Soc., 127, 476, 10.1021/ja044834j

Oueslati, 2012, Mimicking phosphorylation at serine 87 inhibits the aggregation of human α-synuclein and protects against its toxicity in a rat model of Parkinson disease, J. Neurosci., 32, 1536, 10.1523/JNEUROSCI.3784-11.2012