Structural characterization of heparin-induced glyceraldehyde-3-phosphate dehydrogenase protofibrils preventing α-synuclein oligomeric species toxicity

Journal of Biological Chemistry

Volumn 289, Issue 20, 2014, Pages 13838-13850

  Ávila, César L ^a   Torres Bugeau, Clarisa M ^a   Barbosa, Leandro R S ^b   Sales, Elisa Morandé ^b   Ouidja, Mohand O ^c,d   Socías, Sergio B ^c   Celej, M Soledad ^e   Raisman Vozari, Rita ^c   Papy Garcia, Dulce ^d   Itri, Rosangela ^b   Chehín, Rosana N ^a  

^a Instituto Superior de Investigaciones Biologicas   (Argentina)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^d UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^e UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASES; MASS SPECTROMETRY; OLIGOMERS;

ALL-ATOM MODEL; EXTRACELLULAR SPACE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; GLYCOSAMINOGLYCANS; PARKINSON DISEASE; SMALL ANGLE X-RAY SCATTERING; STRUCTURAL CHARACTERIZATION; THERAPEUTIC STRATEGY;

CELL CULTURE;

ALPHA SYNUCLEIN; DIMER; GAG PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEPARIN; OLIGOMER; CROSS LINKING REAGENT; NEUROPROTECTIVE AGENT;

ARTICLE; CELL SURVIVAL; DOPAMINERGIC NERVE CELL; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NEUROPROTECTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTOFIBRIL; RADIATION SCATTERING; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; MOLECULAR GENETICS; NERVE CELL; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; TOXICITY; TUMOR CELL LINE;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; CELL LINE, TUMOR; CELL SURVIVAL; CROSS-LINKING REAGENTS; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEPARIN; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEURONS; NEUROPROTECTIVE AGENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84900992806     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.544288     Document Type: Article

References (70)

1. Spillantini, M. G., Crowther, R. A., Jakes, R., Hasegawa, M., and Goedert, M. (1998) α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U.S.A. 95, 6469-6473
2. Lee, H. J., Patel, S., and Lee, S. J. (2005) Intravesicular localization and exocytosis of α-synuclein and its aggregates. J. Neurosci. 25, 6016-6024
3. Lee, H. J., Suk, J. E., Bae, E. J., and Lee, S. J. (2008) Clearance and deposition of extracellular α-synuclein aggregates in microglia. Biochem. Biophys. Res. Commun. 372, 423-428
4. Lee, S. J. (2008) Origins and effects of extracellular α-synuclein: implications in Parkinson's disease. J. Mol. Neurosci. 34, 17-22
5. Chai, Y. J., Kim, D., Park, J., Zhao, H., Lee, S. J., and Chang, S. (2013) The secreted oligomeric form of α-synuclein affects multiple steps of membrane trafficking. FEBS Lett. 587, 452-459
6. Steiner, J. A., Angot, E., and Brundin, P. (2011) A deadly spread: cellular mechanisms of α-synuclein transfer. Cell Death Differ. 18, 1425-1433
7. Wood, S. J., Wypych, J., Steavenson, S., Louis, J. C., Citron, M., and Biere, A. L. (1999) α-Synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 274, 19509-19512
8. Conway, K. A., Harper, J. D., and Lansbury, P. T., Jr. (2000) Fibrils formed in vitro from α-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry 39, 2552-2563
9. Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366
10. Caughey, B., and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298
11. Cremades, N., Cohen, S. I., Deas, E., Abramov, A. Y., Chen, A. Y., Orte, A., Sandal, M., Clarke, R. W., Dunne, P., Aprile, F. A., Bertoncini, C. W., Wood, N. W., Knowles, T. P., Dobson, C. M., and Klenerman, D. (2012) Direct observation of the interconversion of normal and toxic forms of αsynuclein. Cell 149, 1048-1059
12. Butterfield, S. M., and Lashuel, H. A. (2010) Amyloidogenic protein-membrane interactions: mechanistic insight from model systems. Angew Chem. Int. Ed. Engl. 49, 5628-5654
13. Tsuchiya, K., Tajima, H., Kuwae, T., Takeshima, T., Nakano, T., Tanaka, M., Sunaga, K., Fukuhara, Y., Nakashima, K., Ohama, E., Mochizuki, H., Mizuno, Y., Katsube, N., and Ishitani, R. (2005) Pro-apoptotic protein glyceraldehyde-3-phosphate dehydrogenase promotes the formation of Lewy body-like inclusions. Eur. J. Neurosci. 21, 317-326
14. Leverenz, J. B., Umar, I., Wang, Q., Montine, T. J., McMillan, P. J., Tsuang, D. W., Jin, J., Pan, C., Shin, J., Zhu, D., and Zhang, J. (2007) Proteomic identification of novel proteins in cortical Lewy bodies. Brain Pathol. 17, 139-145
15. Sirover, M.A. (2011) On the functional diversity of glyceraldehyde-3- phosphate dehydrogenase: biochemical mechanisms and regulatory control. Biochim. Biophys. Acta 1810, 741-751
16. Zheng, L., Roeder, R. G., and Luo, Y. (2003) S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114, 255-266
17. Engel, M., Seifert, M., Theisinger, B., Seyfert, U., and Welter, C. (1998) Glyceraldehyde-3-phosphate dehydrogenase and Nm23-H1/nucleoside diphosphate kinase A. Two old enzymes combine for the novel Nm23 protein phosphotransferase function. J. Biol. Chem. 273, 20058-20065
18. Kumagai, H., and Sakai, H. (1983) A porcine brain protein (35 K protein) which bundles microtubules and its identification as glyceraldehyde 3-phosphate dehydrogenase. J. Biochem. 93, 1259-1269
19. Xu, K. Y., and Becker, L. C. (1998) Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesicles. J. Histochem. Cytochem. 46, 419-427
20. Lin, H., Zhu, Y. J., and Lal, R. (1999) Amyloid β protein(1-40) forms calcium-permeable, Zn2+-sensitive channel in reconstituted lipid vesicles. Biochemistry 38, 11189-11196
21. Hara, M. R., Agrawal, N., Kim, S. F., Cascio, M. B., Fujimuro, M., Ozeki, Y., Takahashi, M., Cheah, J. H., Tankou, S. K., Hester, L. D., Ferris, C. D., Hayward, S. D., Snyder, S. H., and Sawa, A. (2005) S-Nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7, 665-674
22. Butterfield, D. A., Hardas, S. S., and Lange, M. L. (2010) Oxidatively modified glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and Alzheimer's disease: many pathways to neurodegeneration. J. Alzheimers Dis. 20, 369-393
23. Allen, M., Cox, C., Belbin, O., Ma, L., Bisceglio, G. D., Wilcox, S. L., Howell, C. C., Hunter, T. A., Culley, O., Walker, L. P., Carrasquillo, M. M., Dickson, D. W., Petersen, R. C., Graff-Radford, N. R., Younkin, S. G., and Ertekin-Taner, N. (2010) Association and heterogeneity at the GAPDH locus in Alzheimer's disease. Neurobiol. Aging 33, 203 e225-e233
24. Díaz-Nido, J., Wandosell, F., and Avila, J. (2002) Glycosaminoglycans and β-amyloid, prion and tau peptides in neurodegenerative diseases. Peptides 23, 1323-1332
25. Holmes, B. B., DeVos, S. L., Kfoury, N., Li, M., Jacks, R., Yanamandra, K., Ouidja, M. O., Brodsky, F. M., Marasa, J., Bagchi, D. P., Kotzbauer, P. T., Miller, T. M., Papy-Garcia, D., and Diamond, M. I. (2013) Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc. Natl. Acad. Sci. U.S.A. 110, E3138-E3147
26. Motamedi-Shad, N., Monsellier, E., Torrassa, S., Relini, A., and Chiti, F. (2009) Kinetic analysis of amyloid formation in the presence of heparan sulfate: faster unfolding and change of pathway. J. Biol. Chem. 284, 29921-29934
27. Torres-Bugeau, C. M., Ávila, C. L., Raisman-Vozari, R., Papy-Garcia, D., Itri, R., Barbosa, L. R., Cortez, L. M., Sim, V. L., and Chehín, R. N. (2012) Characterization of heparin-induced glyceraldehyde-3-phosphate dehydrogenase early amyloid-like oligomers and their implication in α-synuclein aggregation. J. Biol. Chem. 287, 2398-2409
28. Hoyer, W., Antony, T., Cherny, D., Heim, G., Jovin, T. M., and Subramaniam, V. (2002) Dependence of α-synuclein aggregate morphology on solution conditions. J. Mol. Biol. 322, 383-393
29. Kaylor, J., Bodner, N., Edridge, S., Yamin, G., Hong, D. P., and Fink, A. L. (2005) Characterization of oligomeric intermediates in α-synuclein fibrillation: FRET studies of Y125W/Y133F/Y136F α-synuclein. J. Mol. Biol. 353, 357-372
30. Danzer, K. M., Haasen, D., Karow, A. R., Moussaud, S., Habeck, M., Giese, A., Kretzschmar, H., Hengerer, B., and Kostka, M. (2007) Different species of αsynuclein oligomers induce calcium influx and seeding. J. Neurosci. 27, 9220-9232
31. Arrondo, J. L., Castresana, J., Valpuesta, J. M., and Goñi, F. M. (1994) Structure and thermal denaturation of crystalline and noncrystalline cytochrome oxidase as studied by infrared spectroscopy. Biochemistry 33, 11650-11655
32. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
33. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509
34. Finer, E. G., Flook, A. G., and Hauser, H. (1972) Mechanism of sonication of aqueous egg yolk lecithin dispersions and nature of the resultant particles. Biochim. Biophys. Acta 260, 49-58
35. Kendall, D. A., and MacDonald, R. C. (1982) A fluorescence assay to monitor vesicle fusion and lysis. J. Biol. Chem. 257, 13892-13895
36. Barbosa, L. R., Spinozzi, F., Mariani, P., and Itri, R. (2013) in Proteins in Solution and at Interfaces (Ruso, J. M., and Piñeiro, A., eds) pp. 49-72, John Wiley & Sons, Inc., New York
37. Ortore, M. G., Spinozzi, F., Mariani, P., Paciaroni, A., Barbosa, L. R., Amenitsch, H., Steinhart, M., Ollivier, J., and Russo, D. (2009) Combining structure and dynamics: nondenaturing high-pressure effect on lysozyme in solution. J.R. Soc. Interface 6, S619-S634
38. Barbosa, L. R., Ortore, M. G., Spinozzi, F., Mariani, P., Bernstorff, S., and Itri, R. (2010) The importance of protein-protein interactions on the pHinduced conformational changes of bovine serum albumin: a small-angle x-ray scattering study. Biophys. J. 98, 147-157
39. Fournet, G., and Guinier, A. (1955) Small Angle Scattering of X-rays (translated by Walker, C. B., and Yudowitch, K. L.) pp. 7-78, John Wiley& Sons, Inc., New York
40. Fancy, D. A., Denison, C., Kim, K., Xie, Y., Holdeman, T., Amini, F., and Kodadek, T. (2000) Scope, limitations and mechanistic aspects of the photo-induced cross-linking of proteins by water-soluble metal complexes. Chem. Biol. 7, 697-708
41. Fancy, D. A., and Kodadek, T. (1999) Chemistry for the analysis of proteinprotein interactions: rapid and efficient cross-linking triggered by long wavelength light. Proc. Natl. Acad. Sci. U.S.A. 96, 6020-6024
42. Weber, K., and Osborn, M. (1969) The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J. Biol. Chem. 244, 4406-4412
43. Schneidman-Duhovny, D., Inbar, Y., Nussinov, R., and Wolfson, H. J. (2005) Geometry-based flexible and symmetric protein docking. Proteins 60, 224-231
44. Cowan-Jacob, S. W., Kaufmann, M., Anselmo, A. N., Stark, W., and Grütter, M. G. (2003) Structure of rabbit-muscle glyceraldehyde-3-phosphate dehydrogenase. Acta Crystallogr. D. Biol. Crystallogr. 59, 2218-2227
45. Marrink, S. J., Risselada, H. J., Yefimov, S., Tieleman, D. P., and de Vries, A. H. (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B. 111, 7812-7824
46. Monticelli, L., Kandasamy, S. K., Periole, X., Larson, R. G., Tieleman, D. P., and Marrink, S.-J. (2008) The MARTINI coarse-grained force field: Extension to proteins. J. Chem. Theory Comput. 4, 819-834
47. Periole, X., Cavalli, M., Marrink, S.-J., and Ceruso, M.A. (2009) Combining an elastic network with a coarse-grained molecular force field: Structure, dynamics, and intermolecular recognition. J. Chem. Theory Comput. 5, 2531-2543
48. Rzepiela, A. J., Schäfer, L. V., Goga, N., Risselada, H. J., De Vries, A. H., and Marrink, S. J. (2010) Reconstruction of atomistic details from coarsegrained structures. J. Comput. Chem. 31, 1333-1343
49. Vendruscolo, M., Najmanovich, R., and Domany, E. (1999) Protein folding in contact map space. Phys. Rev. Lett. 82, 656-659
50. Chennamsetty, N., Voynov, V., Kayser, V., Helk, B., and Trout, B. L. (2009) Design of therapeutic proteins with enhanced stability. Proc. Natl. Acad. Sci. U.S.A. 106, 11937-11942
51. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38
52. Black, S. D., and Mould, D. R. (1991) Development of hydrophobicity parameters to analyze proteins which bear post- or cotranslational modifications. Anal. Biochem. 193, 72-82
53. Yang, W. H., Yang, C., Xue, Y. Q., Lu, T., Reiser, J., Zhao, L. R., and Duan, W. M. (2013) Regulated expression of lentivirus-mediated GDNF in human bone marrow-derived mesenchymal stem cells and its neuroprotection on dopaminergic cells in vitro. PLoS One 8, e64389
54. Kim, H. Y., Cho, M. K., Kumar, A., Maier, E., Siebenhaar, C., Becker, S., Fernandez, C. O., Lashuel, H. A., Benz, R., Lange, A., and Zweckstetter, M. (2009) Structural properties of pore-forming oligomers of αsynuclein. J. Am. Chem. Soc. 131, 17482-17489
55. Glabe, C. G. (2008) Structural classification of toxic amyloid oligomers. J. Biol. Chem. 283, 29639-29643
56. Kayed, R., Sokolov, Y., Edmonds, B., McIntire, T. M., Milton, S. C., Hall, J. E., and Glabe, C. G. (2004) Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279, 46363-46366
57. Volles, M. J., Lee, S. J., Rochet, J. C., Shtilerman, M. D., Ding, T. T., Kessler, J. C., and Lansbury, P. T., Jr. (2001) Vesicle permeabilization by protofibrillar α-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry 40, 7812-7819
58. van Rooijen, B. D., Claessens, M. M., and Subramaniam, V. (2010) Membrane permeabilization by oligomeric α-synuclein: in search of the mechanism. PLoS One 5, e14292
59. Morero, R. D., Viñals, A. L., Bloj, B., and Farías, R. N. (1985) Fusion of phospholipid vesicles induced by muscle glyceraldehyde-3- phosphate dehydrogenase in the absence of calcium. Biochemistry 24, 1904-1909
60. Oliveira, C. L., Behrens, M.A., Pedersen, J. S., Erlacher, K., and Otzen, D. (2009) A SAXS study of glucagon fibrillation. J. Mol. Biol. 387, 147-161
61. Giehm, L., Svergun, D. I., Otzen, D. E., and Vestergaard, B. (2011) Lowresolution structure of a vesicle disrupting-synuclein oligomer that accumulates during fibrillation. Proc. Natl. Acad. Sci. U.S.A. 108, 3246-3251
62. Spinozzi, F., Mariani, P., Saturni, L., Carsughi, F., Bernstorff, S., Cinelli, S., and Onori, G. (2007) Met-myoglobin association in dilute solution during pressure-induced denaturation: an analysis at pH 4.5 by high-pressure small-angle x-ray scattering. J. Phys. Chem. B. 111, 3822-3830
63. Ortore, M. G., Spinozzi, F., Vilasi, S., Sirangelo, I., Irace, G., Shukla, A., Narayanan, T., Sinibaldi, R., and Mariani, P. (2011) Time-resolved smallangle x-ray scattering study of the early stage of amyloid formation of an apomyoglobin mutant. Phys. Rev. E. Stat. Nonlin. Soft Matter Phys. 84, 061904
64. Kodali, R., and Wetzel, R. (2007) Polymorphism in the intermediates and products of amyloid assembly. Curr. Opin. Struct. Biol. 17, 48-57
65. El-Agnaf, O. M., Salem, S. A., Paleologou, K. E., Cooper, L. J., Fullwood, N. J., Gibson, M. J., Curran, M. D., Court, J. A., Mann, D. M., Ikeda, S., Cookson, M. R., Hardy, J., and Allsop, D. (2003) α-Synuclein implicated in Parkinson's disease is present in extracellular biological fluids, including human plasma. FASEB J. 17, 1945-1947
66. El-Agnaf, O. M., Salem, S. A., Paleologou, K. E., Curran, M. D., Gibson, M. J., Court, J. A., Schlossmacher, M. G., and Allsop, D. (2006) Detection of oligomeric forms of α-synuclein protein in human plasma as a potential biomarker for Parkinson's disease. FASEB J. 20, 419-425
67. Luk, K. C., Song, C., O'Brien, P., Stieber, A., Branch, J.R., Brunden, K. R., Trojanowski, J. Q., and Lee, V. M. (2009) Exogenous α-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc. Natl. Acad. Sci. U.S.A. 106, 20051-20056
68. Sacino, A. N., and Giasson, B. I. (2012) Does a prion-like mechanism play a major role in the apparent spread of αsynuclein pathology? Alzheimers Res. Ther. 4, 48
69. Huynh, M. B., Morin, C., Carpentier, G., Garcia-Filipe, S., Talhas-Perret, S., Barbier-Chassefière, V., van Kuppevelt, T. H., Martelly, I., Albanese, P., and Papy-Garcia, D. (2012) Age-related changes in rat myocardium involve altered capacities of glycosaminoglycans to potentiate growth factor functions and heparan sulfate-altered sulfation. J. Biol. Chem. 287, 11363-11373
70. Carlile, G. W., Chalmers-Redman, R. M., Tatton, N. A., Pong, A., Borden, K. E., and Tatton, W. G. (2000) Reduced apoptosis after nerve growth factor and serum withdrawal: conversion of tetrameric glyceraldehyde-3-phosphate dehydrogenase to a dimer. Mol. Pharmacol. 57, 2-12