High-content analysis of α-synuclein aggregation and cell death in a cellular model of Parkinson's disease

Journal of Neuroscience Methods

Volumn 261, Issue , 2016, Pages 117-127

  Macchi, Francesca ^a   Deleersnijder, Angélique ^a   Van den Haute, Chris ^a,c   Munck, Sebastian ^b   Pottel, Hans ^a   Michiels, Annelies ^a,c   Debyser, Zeger ^d   Gerard, Melanie ^a   Baekelandt, Veerle ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c KU LEUVEN   (Belgium)

^d DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

Author keywords

Aggregation; Alpha synuclein; Cell death; High content analysis; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE METHYL ESTER; PROTEIN FARNESYLTRANSFERASE INHIBITOR; 4',6 DIAMIDINO 2 PHENYLINDOLE; INDOLE DERIVATIVE; SNCA PROTEIN, HUMAN; THIAZOLE DERIVATIVE; THIOFLAVINE;

APOPTOSIS; ARTICLE; AUTOMATION; CELL DEATH; CELL FREE SYSTEM; CELL VIABILITY; DRUG SCREENING; GENOTOXICITY; HUMAN; HUMAN CELL; NERVE CELL; NEUROBLASTOMA CELL; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; SINGLE CELL ANALYSIS; VALIDATION PROCESS; CELL COUNT; CELL CULTURE TECHNIQUE; CELL SURVIVAL; CHEMISTRY; FLUORESCENCE MICROSCOPY; GENE VECTOR; GENETICS; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; LENTIVIRINAE; METABOLISM; PARKINSONISM; PATHOLOGY; PROCEDURES; PROTEIN MULTIMERIZATION; PROTEINOSIS; SOFTWARE; TUMOR CELL LINE; VALIDATION STUDY; WESTERN BLOTTING;

ALPHA-SYNUCLEIN; APOPTOSIS; BLOTTING, WESTERN; CELL COUNT; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL SURVIVAL; GENETIC VECTORS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INDOLES; LENTIVIRUS; MICROSCOPY, FLUORESCENCE; OXIDATIVE STRESS; PARKINSONIAN DISORDERS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN MULTIMERIZATION; SOFTWARE; THIAZOLES;

EID: 84954290559     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2015.11.009     Document Type: Article

References (61)

1. Aelvoet S-A., Ibrahimi A., Macchi F., Gijsbers R., Van den Haute C., Debyser Z., et al. Noninvasive bioluminescence imaging of α-synuclein oligomerization in mouse brain using split firefly luciferase reporters. J Neurosci 2014, 34:16518-16532.
2. Appel-Cresswell S., Vilarino-Guell C., Encarnacion M., Sherman H., Yu I., Shah B., et al. Alpha-synuclein p.H50Q, a novel pathogenic mutation for Parkinson's disease. Movement Disorders 2013, 28:811-813.
3. Bidinosti M., Shimshek D.R., Mollenhauer B., Marcellin D., Schweizer T., Lotz G.P., et al. Novel one-step immunoassays to quantify α-synuclein: applications for biomarker development and high-throughput screening. J Biol Chem 2012, 287:33691-33705.
4. Blackmore M.G., Moore D.L., Smith R.P., Goldberg J.L., Bixby J.L., Lemmon V.P. High content screening of cortical neurons identifies novel regulators of axon growth. Mol Cell Neurosci 2010, 44:43-54.
5. Boyd J.D., Lee P., Feiler M.S., Zauur N., Liu M., Concannon J., et al. A high content screen identifies novel compounds that inhibit stress-induced TDP-43 cellular aggregation and associated cytotoxicity. J Biomol Screening 2014, 19:44-56.
6. Chartier-Harlin M.C., Kachergus J., Roumier C., Mouroux V., Douay X., Lincoln S., et al. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 2004, 364:1167-1169.
7. Deleersnijder A., Gerard M., Debyser Z., Baekelandt V. The remarkable conformational plasticity of alpha-synuclein: blessing or curse. Trends Mol Med 2013, 19:368-377.
8. Deleersnijder A., Van Rompuy A.S., Desender L., Pottel H., Buee L., Debyser Z., et al. Comparative analysis of different peptidyl-prolyl isomerases reveals FK506-binding protein 12 as the most potent enhancer of alpha-synuclein aggregation. J Biol Chem 2011, 286:26687-26701.
9. Denner P., Schmalowsky J., Prechtl S. High-content analysis in preclinical drug discovery. Comb Chem High Throughput Screen 2008, 11:216-230.
10. Dragunow M. High-content analysis in neuroscience. Nat Rev Neurosci 2008, 9:779-788.
11. Dragunow M., Greenwood J.M., Cameron R.E., Narayan P.J., O'Carroll S.J., Pearson A.G., et al. Valproic acid induces caspase 3-mediated apoptosis in microglial cells. Neuroscience 2006, 140:1149-1156.
12. Elbaz A., Levecque C., Clavel J., Vidal J.S., Richard F., Correze J.R., et al. S18Y polymorphism in the UCH-L1 gene and Parkinson's disease: evidence for an age-dependent relationship. Mov Disord 2003, 18:130-137.
13. Eslamboli A., Romero-Ramos M., Burger C., Bjorklund T., Muzyczka N., Mandel R.J., et al. Long-term consequences of human alpha-synuclein overexpression in the primate ventral midbrain. Brain 2007, 130:799-815.
14. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature 2000, 404:394-398.
15. Fennell M., Chan H., Wood A. Multiparameter measurement of caspase 3 activation and apoptotic cell death in NT2 neuronal precursor cells using high-content analysis. J Biomol Screen 2006, 11:296-302.
16. Fitzgerald J.C., Gao G.P., Reyes-Sandoval A., Pavlakis G.N., Xiang Z.Q., Wlazlo A.P., et al. A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag. J Immunol 2003, 170:1416-1422.
17. Gasser T. Molecular pathogenesis of Parkinson disease: insights from genetic studies. Expert Rev Mol Med 2009, 11:e22.
18. Geraerts M., Michiels M., Baekelandt V., Debyser Z., Gijsbers R. Upscaling of lentiviral vector production by tangential flow filtration. J Gene Med 2005, 7:1299-1310.
19. Gerard M., Deleersnijder A., Daniels V., Schreurs S., Munck S., Reumers V., et al. Inhibition of FK506 binding proteins reduces alpha-synuclein aggregation and Parkinson's disease-like pathology. J Neurosci 2010, 30:2454-2463.
20. Grimsey N.L., Narayan P.J., Dragunow M., Glass M. A novel high-throughput assay for the quantitative assessment of receptor trafficking. Clin Exp Pharmacol Physiol 2008, 35:1377-1382.
21. Hansen C., Angot E., Bergstrom A.L., Steiner J.A., Pieri L., Paul G., et al. alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 2011, 121:715-725.
22. Harper J.D., Lansbury P.T. Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 1997, 66:385-407.
23. Hasson S.A., Kane L.A., Yamano K., Huang C-H., Sliter D.A., Buehler E., et al. High-content genome-wide RNAi screens identify regulators of parkin upstream of mitophagy. Nature 2013, 504:291-295.
24. Ibanez P., Bonnet A.M., Debarges B., Lohmann E., Tison F., Pollak P., et al. Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease. Lancet 2004, 364:1169-1171.
25. Iversen P.W., Beck B., Chen Y.F., et al. HTS assay validation. Assay guidance manual 2012, Eli Lilly & Company and the National Center for Advancing Translational Sciences, Bethesda, USA, [Internet]. G.S. Sittampalam, C.N. Nelson (Eds.).
26. Kirik D., Annett L.E., Burger C., Muzyczka N., Mandel R.J., Bjorklund A. Nigrostriatal alpha-synucleinopathy induced by viral vector-mediated overexpression of human alpha-synuclein: a new primate model of Parkinson's disease. Proc Natl Acad Sci USA 2003, 100:2884-2889.
27. Kirik D., Rosenblad C., Burger C., Lundberg C., Johansen T.E., Muzyczka N., et al. Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. J Neurosci 2002, 22:2780-2791.
28. Kroemer G., Galluzzi L., Vandenabeele P., Abrams J., Alnemri E.S., Baehrecke E.H., et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009, 16:3-11.
29. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 1998, 18:106-108.
30. Lakso M., Vartiainen S., Moilanen A.M., Sirvio J., Thomas J.H., Nass R., et al. Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J Neurochem 2003, 86:165-172.
31. Lauwers E., Debyser Z., Van Dorpe J., De Strooper B., Nuttin B., Baekelandt V. Neuropathology and neurodegeneration in rodent brain induced by lentiviral vector-mediated overexpression of alpha-synuclein. Brain Pathol 2003, 13:364-372.
32. Lesage S., Anheim M., Letournel F., Bousset L., Honoré A., Rozas N., et al. G51D α-synuclein mutation causes a novel Parkinsonian-pyramidal syndrome. Ann Neurol 2013, 73:459-471. for the French Parkinson's Disease Genetics Study G.
33. Liu Z., Meray R.K., Grammatopoulos T.N., Fredenburg R.A., Cookson M.R., Liu Y., et al. Membrane-associated farnesylated UCH-L1 promotes alpha-synuclein neurotoxicity and is a therapeutic target for Parkinson's disease. Proc Natl Acad Sci USA 2009, 106:4635-4640.
34. Lubbe S., Morris H. Recent advances in Parkinson's disease genetics. J Neurol 2014, 261:259-266.
35. Lundvig D., Lindersson E., Jensen P.H. Pathogenic effects of alpha-synuclein aggregation. Brain Res Mol Brain Res 2005, 134:3-17.
36. Maraganore D.M., Lesnick T.G., Elbaz A., Chartier-Harlin M.C., Gasser T., Kruger R., et al. UCHL1 is a Parkinson's disease susceptibility gene. Ann Neurol 2004, 55:512-521.
37. Mizuno Y., Hattori N., Kubo S., Sato S., Nishioka K., Hatano T., et al. Progress in the pathogenesis and genetics of Parkinson's disease. Philos. Trans. R. Soc. London, B: Biol. Sci. 2008, 363:2215-2227.
38. Momose Y., Murata M., Kobayashi K., Tachikawa M., Nakabayashi Y., Kanazawa I., et al. Association studies of multiple candidate genes for Parkinson's disease using single nucleotide polymorphisms. Ann Neurol 2002, 51:133-136.
39. Narayan P.J., Gibbons H.M., Mee E.W., Faull R.L., Dragunow M. High throughput quantification of cells with complex morphology in mixed cultures. J Neurosci Methods 2007, 164:339-349.
40. Naze P., Vuillaume I., Destee A., Pasquier F., Sablonniere B. Mutation analysis and association studies of the ubiquitin carboxy-terminal hydrolase L1 gene in Huntington's disease. Neurosci Lett 2002, 328:1-4.
41. Olanow C.W., Brundin P. Parkinson's disease and alpha synuclein is Parkinson's disease a prion-like disorder?. Mov Disord 2013, 28:31-40.
42. Oliveras-Salvá M., Macchi F., Coessens V., Deleersnijder A., Gérard M., Van der Perren A., et al. Alpha-synuclein-induced neurodegeneration is exacerbated in PINK1 knockout mice. Neurobiol Aging 2014, 35:2625-2636.
43. Oliveras-Salva M., Van der Perren A., Casadei N., Stroobants S., Nuber S., D'Hooge R., et al. rAAV2/7 vector-mediated overexpression of alpha-synuclein in mouse substantia nigra induces protein aggregation and progressive dose-dependent neurodegeneration. Mol Neurodegener 2013, 8:44.
44. Ostrerova-Golts N., Petrucelli L., Hardy J., Lee J.M., Farer M., Wolozin B. The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. J Neurosci 2000, 20:6048-6054.
45. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997, 276:2045-2047.
46. Radio N. Neurite outgrowth assessment using high content analysis methodology. Neurotrophic factors 2012, 247-260. Humana Press, New York City, USA. S.D. Skaper (Ed.).
47. Rausch O. Use of high-content analysis for compound screening and target selection. IDrugs 2005, 8:573-577.
48. Reyes J.F., Olsson T.T., Lamberts J.T., Devine M.J., Kunath T., Brundin P. A cell culture model for monitoring α-synuclein cell-to-cell transfer. Neurobiol Dis 2015, 77:266-275.
49. Schmandke A., Schmandke A., Pietro M.A., Schwab M.E. An open source based high content screening method for cell biology laboratories investigating cell spreading and adhesion. PLoS ONE 2013, 8:e78212.
50. Scotter E.L., Narayan P., Glass M., Dragunow M. High throughput quantification of mutant huntingtin aggregates. J Neurosci Methods 2008, 171:174-179.
51. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., et al. Alpha-synuclein locus triplication causes Parkinson's disease. Science 2003, 302:841.
52. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997, 388:839-840.
53. Teboul O., Feki A., Dubois A., Bozon B., Faure A., Hantraye P., et al. A standardized method to automatically segment amyloid plaques in Congo Red stained sections from Alzheimer transgenic mice. Conf Proc IEEE Eng Med Biol Soc 2007, 2007:5593-5596.
54. Vallotton P., Lagerstrom R., Sun C., Buckley M., Wang D., De S.M., et al. Automated analysis of neurite branching in cultured cortical neurons using HCA-Vision. Cytometry A 2007, 71:889-895.
55. Van der Perren A., Toelen J., Casteels C., Macchi F., Van Rompuy A.-S., Sarre S., et al. Longitudinal follow-up and characterization of a robust rat model for Parkinson's disease based on over expression of alpha-synuclein with adeno-associated viral vectors. Neurobiol Aging 2015, 36:1543-1558.
56. Van der Veken P., Fülöp V., Rea D., Gerard M., Van Elzen R., Joossens J., et al. P2-Substituted N-acylprolylpyrrolidine inhibitors of prolyl oligopeptidase: biochemical evaluation, binding mode determination, and assessment in a cellular model of synucleinopathy. J Med Chem 2012, 55:9856-9867.
57. Varma H., Lo D.C., Stockwell B.R. High throughput screening for neurodegeneration and complex disease phenotypes. Comb Chem High Throughput Screen 2008, 11:238-248.
58. Wang D., Lagerstrom R., Sun C., Bishof L., Valotton P., Götte M. HCA-vision. Automated neurite outgrowth analysis. J Biomol Screening 2010, 15:1165-1170.
59. Wintermeyer P., Kruger R., Kuhn W., Muller T., Woitalla D., Berg D., et al. Mutation analysis and association studies of the UCHL1 gene in German Parkinson's disease patients. NeuroReport 2000, 11:2079-2082.
60. Xue S., Jia J. Genetic association between ubiquitin carboxy-terminal hydrolase-L1 gene S18Y polymorphism and sporadic Alzheimer's disease in a Chinese Han population. Brain Res 2006, 1087:28-32.
61. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., et al. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 2004, 55:164-173.