Increased α-synuclein aggregation following limited cleavage by certain matrix metalloproteinases

Experimental Neurology

Volumn 215, Issue 1, 2009, Pages 201-208

  Levin, Johannes ^a   Giese, Armin ^b   Boetzel, Kai ^a   Israel, Lars ^b   Högen, Tobias ^b   Nübling, Georg ^b   Kretzschmar, Hans ^b   Lorenzl, Stefan ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

synuclein; Aggregate; FCS; Mass spectrometry; MMP; Oligomer; Parkinson's disease; Proteinase K; SIFT; Trypsin

Indexed keywords

ALPHA SYNUCLEIN; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; OLIGOMER; PROTEINASE; PROTEINASE K; STROMELYSIN; TRYPSIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE CROSS CORRELATION SPECTROSCOPY; GEL ELECTROPHORESIS; IN VITRO STUDY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PARKINSON DISEASE; PATHOGENESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; QUANTITATIVE ASSAY; SCANNING FOR INTENSELY FLUORESCENTLY TARGET; SPECTROSCOPY; TECHNIQUE;

ALPHA-SYNUCLEIN; BIOPHYSICAL PROCESSES; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPECTRUM ANALYSIS;

EID: 57449109485     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.10.010     Document Type: Article

References (63)

1. Apetri M.M., Maiti N.C., Zagorski M.G., Carey P.R., and Anderson V.E. Secondary structure of alpha-synuclein oligomers: characterization by raman and atomic force microscopy. J. Mol. Biol. 355 (2006) 63-71
2. Asahina M., Yoshiyama Y., and Hattori T. Expression of matrix metalloproteinase-9 and urinary-type plasminogen activator in Alzheimer's disease brain. Clin. Neuropathol. 20 (2001) 60-63
3. Baba M., Nakajo S., Tu P.H., Tomita T., Nakaya K., Lee V.M., Trojanowski J.Q., and Iwatsubo T. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 152 (1998) 879-884
4. Behrends C., Langer C.A., Boteva R., Bottcher U.M., Stemp M.J., Schaffar G., Rao B.V., Giese A., Kretzschmar H., Siegers K., and Hartl F.U. Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers. Mol. Cell 23 (2006) 887-897
5. Beuche W., Yushchenko M., Mader M., Maliszewska M., Felgenhauer K., and Weber F. Matrix metalloproteinase-9 is elevated in serum of patients with amyotrophic lateral sclerosis. NeuroReport 11 (2000) 3419-3422
6. Beyer K. Mechanistic aspects of Parkinson's disease: alpha-synuclein and the biomembrane. Cell Biochem. Biophys. 47 (2007) 285-299
7. Bieschke J., Giese A., Schulz-Schaeffer W., Zerr I., Poser S., Eigen M., and Kretzschmar H. Ultrasensitive detection of pathological prion protein aggregates by dual-color scanning for intensely fluorescent targets. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 5468-5473
8. Braak H., Rub U., Gai W.P., and Del T.K. Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J. Neural Transm. 110 (2003) 517-536
9. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., Taddei N., Ramponi G., Dobson C.M., and Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
10. Campbell B.C., McLean C.A., Culvenor J.G., Gai W.P., Blumbergs P.C., Jakala P., Beyreuther K., Masters C.L., and Li Q.X. The solubility of alpha-synuclein in multiple system atrophy differs from that of dementia with Lewy bodies and Parkinson's disease. J. Neurochem. 76 (2001) 87-96
11. Chartier-Harlin M.C., Kachergus J., Roumier C., Mouroux V., Douay X., Lincoln S., Levecque C., Larvor L., Andrieux J., Hulihan M., Waucquier N., Defebvre L., Amouyel P., Farrer M., and Destee A. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 364 (2004) 1167-1169
12. Chen M., Margittai M., Chen J., and Langen R. Investigation of alpha-synuclein fibril structure by site-directed spin labeling. J. Biol. Chem. 282 (2007) 24970-24979
13. Choi D.H., Kim E.M., Son H.J., Joh T., Kim D., Kim Y.S., Beal M.F., and Hwang O. A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J. Neurochem. 106 (2008) 405-415
14. Cole N.B., Murphy D.D., Lebowitz J., Di N.L., Levine R.L., and Nussbaum R.L. Metal-catalyzed oxidation of alpha-synuclein: helping to define the relationship between oligomers, protofibrils, and filaments. J. Biol. Chem. 280 (2005) 9678-9690 11-3-
15. Crowther R.A., Jakes R., Spillantini M.G., and Goedert M. Synthetic filaments assembled from C-terminally truncated alpha-synuclein. FEBS Lett. 436 (1998) 309-312
16. Danzer K.M., Haasen D., Karow A.R., Moussaud S., Habeck M., Giese A., Kretzschmar H., Hengerer B., and Kostka M. Different species of alpha-synuclein oligomers induce calcium influx and seeding. J. Neurosci. 27 (2007) 9220-9232
17. El-Agnaf O.M., Paleologou K.E., Greer B., Abogrein A.M., King J.E., Salem S.A., Fullwood N.J., Benson F.E., Hewitt R., Ford K.J., Martin F.L., Harriott P., Cookson M.R., and Allsop D. A strategy for designing inhibitors of alpha-synuclein aggregation and toxicity as a novel treatment for Parkinson's disease and related disorders. FASEB J. 18 (2004) 1315-1317
18. Evert B.O., Araujo J., Vieira-Saecker A.M., de Vos R.A., Harendza S., Klockgether T., and Wullner U. Ataxin-3 represses transcription via chromatin binding, interaction with histone deacetylase 3, and histone deacetylation. J. Neurosci. 26 (2006) 11474-11486
19. Giese A., Bieschke J., Eigen M., and Kretzschmar H.A. Putting prions into focus: application of single molecule detection to the diagnosis of prion diseases. Arch. Virol., Suppl. (2000) 161-171
20. Giese A., Levin J., Bertsch U., and Kretzschmar H. Effect of metal ions on de novo aggregation of full-length prion protein. Biochem. Biophys. Res. Commun. 320 (2004) 1240-1246
21. Giese A., Bader B., Bieschke J., Schaffar G., Odoy S., Kahle P.J., Haass C., and Kretzschmar H. Single particle detection and characterization of synuclein co-aggregation. Biochem. Biophys. Res. Commun. 333 (2005) 1202-1210
22. Goldberg M.S., and Lansbury Jr. P.T. Is there a cause-and-effect relationship between alpha-synuclein fibrillization and Parkinson's disease?. Nat. Cell Biol. 2 (2000) E115-E119
23. Haustein E., and Schwille P. Fluorescence correlation spectroscopy: novel variations of an established technique. Annu. Rev. Biophys. Biomol. Struct. 36 151-69 (2007) 151-169
24. Ibanez P., Bonnet A.M., Debarges B., Lohmann E., Tison F., Pollak P., Agid Y., Durr A., and Brice A. Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease. Lancet 364 (2004) 1169-1171
25. Iwai A., Masliah E., Yoshimoto M., Ge N., Flanagan L., de Silva H.A., Kittel A., and Saitoh T. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14 (1995) 467-475
26. Iwai A., Yoshimoto M., Masliah E., and Saitoh T. Non-A beta component of Alzheimer's disease amyloid (NAC) is amyloidogenic. Biochemistry 34 (1995) 10139-10145
27. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
28. Kiaei M., Kipiani K., Calingasan N.Y., Wille E., Chen J., Heissig B., Rafii S., Lorenzl S., and Beal M.F. Matrix metalloproteinase-9 regulates TNF-alpha and FasL expression in neuronal, glial cells and its absence extends life in a transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 205 (2007) 74-81
29. Kim Y.S., Choi D.H., Block M.L., Lorenzl S., Yang L., Kim Y.J., Sugama S., Cho B.P., Hwang O., Browne S.E., Kim S.Y., Hong J.S., Beal M.F., and Joh T.H. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J. 21 (2007) 179-187
30. Kostka M., Hogen T., Danzer K.M., Levin J., Habeck M., Wirth A., Wagner R., Glabe C.G., Finger S., Heinzelmann U., Garidel P., Duan W., Ross C.A., Kretzschmar H., and Giese A. Single-particle characterization of iron-induced pore-forming alpha-synuclein oligomers. J. Biol. Chem. 283 (2008) 10992-11003
31. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J.T., Schols L., and Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18 (1998) 106-108
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
33. Lansbury P.T., and Lashuel H.A. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 19 443 (2006) 774-779
34. Lee M.K., Stirling W., Xu Y., Xu X., Qui D., Mandir A.S., Dawson T.M., Copeland N.G., Jenkins N.A., and Price D.L. Human alpha-synuclein-harboring familial Parkinson's disease-linked Ala-53 -> Thr mutation causes neurodegenerative disease with alpha-synuclein aggregation in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 8968-8973
35. Lee S.J. Origins and effects of extracellular alpha-synuclein: implications in Parkinson's disease. J. Mol. Neurosci. 34 (2008) 17-22
36. Levin J., Bertsch U., Kretzschmar H., and Giese A. Single particle analysis of manganese-induced prion protein aggregates. Biochem. Biophys. Res. Commun. 329 (2005) 1200-1207
37. Lewy F.H. Handbuch der Neurologie (1912) 920-933
38. Li W., West N., Colla E., Pletnikova O., Troncoso J.C., Marsh L., Dawson T.M., Jakala P., Hartmann T., Price D.L., and Lee M.K. Aggregation promoting C-terminal truncation of alpha-synuclein is a normal cellular process and is enhanced by the familial Parkinson's disease-linked mutations. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 2162-2167
39. Lorenzl S., Albers D.S., Narr S., Chirichigno J., and Beal M.F. Expression of MMP-2, MMP-9, and MMP-1 and their endogenous counterregulators TIMP-1 and TIMP-2 in postmortem brain tissue of Parkinson's disease. Exp. Neurol. 178 (2002) 13-20
40. Lorenzl S., Albers D.S., Relkin N., Ngyuen T., Hilgenberg S.L., Chirichigno J., Cudkowicz M.E., and Beal M.F. Increased plasma levels of matrix metalloproteinase-9 in patients with Alzheimer's disease. Neurochem. Int. 43 (2003) 191-196
41. Lorenzl S., Albers D.S., Chirichigno J.W., Augood S.J., and Beal M.F. Elevated levels of matrix metalloproteinases-9 and -1 and of tissue inhibitors of MMPs, TIMP-1 and TIMP-2 in postmortem brain tissue of progressive supranuclear palsy. J. Neurol. Sci. 218 (2004) 39-45
42. Lorenzl S., Calingasan N., Yang L., Albers D.S., Shugama S., Gregorio J., Krell H.W., Chirichigno J., Joh T., and Beal M.F. Matrix metalloproteinase-9 is elevated in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism in mice. Neuromol. Med. 5 (2004) 119-132
43. Lorenzl S., Narr S., Angele B., Krell H.W., Gregorio J., Kiaei M., Pfister H.W., and Beal M.F. The matrix metalloproteinases inhibitor Ro 28-2653 [correction of Ro 26-2853] extends survival in transgenic ALS mice. Exp. Neurol. 200 (2006) 166-171
44. Lukacova V., Zhang Y., Mackov M., Baricic P., Raha S., Calvo J.A., and Balaz S. Similarity of binding sites of human matrix metalloproteinases. J. Biol. Chem. 279 (2004) 14194-14200
45. Munishkina L.A., Phelan C., Uversky V.N., and Fink A.L. Conformational behavior and aggregation of alpha-synuclein in organic solvents: modeling the effects of membranes. Biochemistry 42 (2003) 2720-2730
46. Murray I.V., Giasson B.I., Quinn S.M., Koppaka V., Axelsen P.H., Ischiropoulos H., Trojanowski J.Q., and Lee V.M. Role of alpha-synuclein carboxy-terminus on fibril formation in vitro. Biochemistry 42 (2003) 8530-8540
47. Nagase H., and Woessner Jr. J.F. Matrix metalloproteinases. J. Biol. Chem. 274 (1999) 21491-21494
48. Page L.J., Suk J.Y., Huff M.E., Lim H.J., Venable J., Yates J., Kelly J.W., and Balch W.E. Metalloendoprotease cleavage triggers gelsolin amyloidogenesis. EMBO J. 24 (2005) 4124-4132
49. Park S.M., Hwang I.K., Kim S.Y., Lee S.J., Park K.S., and Lee S.T. Characterization of plasma gelsolin as a substrate for matrix metalloproteinases. Proteomics 6 (2006) 1192-1199
50. Peress N., Perillo E., and Zucker S. Localization of tissue inhibitor of matrix metalloproteinases in Alzheimer's disease and normal brain. J. Neuropathol. Exp. Neurol. 54 (1995) 16-22
51. Periquet M., Fulga T., Myllykangas L., Schlossmacher M.G., and Feany M.B. Aggregated alpha-synuclein mediates dopaminergic neurotoxicity in vivo. J. Neurosci. 27 (2007) 3338-3346
52. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di I.G., Golbe L.I., and Nussbaum R.L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 (1997) 2045-2047
53. Rochet J.C., Outeiro T.F., Conway K.A., Ding T.T., Volles M.J., Lashuel H.A., Bieganski R.M., Lindquist S.L., and Lansbury P.T. Interactions among alpha-synuclein, dopamine, and biomembranes: some clues for understanding neurodegeneration in Parkinson's disease. J. Mol. Neurosci. 23 (2004) 23-34
54. Schwille P., Meyer-Almes F.J., and Rigler R. Dual-color fluorescence cross-correlation spectroscopy for multicomponent diffusional analysis in solution. Biophys. J. 72 (1997) 1878-1886
55. Serpell L.C., Berriman J., Jakes R., Goedert M., and Crowther R.A. Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4897-4902
56. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., and Goedert M. Alpha-synuclein in Lewy bodies. Nature 388 (1997) 839-840
57. Spillantini M.G., Crowther R.A., Jakes R., Hasegawa M., and Goedert M. alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 6469-6473
58. Sung J.Y., Park S.M., Lee C.H., Um J.W., Lee H.J., Kim J., Oh Y.J., Lee S.T., Paik S.R., and Chung K.C. Proteolytic cleavage of extracellular secreted {alpha}-synuclein via matrix metalloproteinases. J. Biol. Chem. 280 (2005) 25216-25224
59. Tolosa E., Wenning G., and Poewe W. The diagnosis of Parkinson's disease. Lancet Neurol. 5 (2006) 75-86
60. Turk B.E., Huang L.L., Piro E.T., and Cantley L.C. Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat. Biotechnol. 19 (2001) 661-667
61. Ueda K., Fukushima H., Masliah E., Xia Y., Iwai A., Yoshimoto M., Otero D.A., Kondo J., Ihara Y., and Saitoh T. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 11282-11286
62. Vos C.M., Sjulson L., Nath A., McArthur J.C., Pardo C.A., Rothstein J., and Conant K. Cytotoxicity by matrix metalloprotease-1 in organotypic spinal cord and dissociated neuronal cultures. Exp. Neurol. 163 (2000) 324-330
63. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., Vidal L., Hoenicka J., Rodriguez O., Atares B., Llorens V., Gomez T.E., del S.T., Munoz D.G., and de Yebenes J.G. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 55 (2004) 164-173