A fluorescence resonance energy transfer assay for monitoring α- synclein aggregation in a caenorhabditis elegans model for Parkinson’s disease

CNS and Neurological Disorders - Drug Targets

Volumn 14, Issue 8, 2015, Pages 1054-1068

  Nagarajan, Archana ^a   Bodhicharla, Rakesh ^b   Winter, Jody ^c   Anbalagan, Charumathi ^d   Morgan, Kevin ^e   Searle, Mark ^e   Nazir, Aamir ^f   Adenle, Ademola ^g   Fineberg, April ^e   Brady, Declan ^e   Vere, Kelly ^e   Richens, Jo ^e   Oshea, Paul ^e   Bell, David ^h   Depomerai, David ^e  

^a UNIVERSITY OF STAVANGER   (Norway)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^d Duke University   (United States)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^f CENTRAL DRUG RESEARCH INSTITUTE   (India)

^g UNITED NATIONS UNIVERSITY   (Japan)

^h EUROPEAN CHEMICALS AGENCY   (Finland)

Author keywords

Aggregation; C. elegans; Fluorescent proteins; FRET; Pollutants; synuclein

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; CHLORPYRIFOS; CYAN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 70; HUNTINGTIN INTERACTING PROTEIN 1; HYBRID PROTEIN; MERCURY; MTL 1 PROTEIN; PROTEIN; PROTEOLIPID PROTEIN; THIOFLAVINE; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN; BACTERIAL PROTEIN; PHOTOPROTEIN; PROTEIN AGGREGATE; SNCA PROTEIN, HUMAN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAENORHABDITIS ELEGANS; CIRCULAR DICHROISM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; GENE EXPRESSION REGULATION; HIGH THROUGHPUT SCREENING; HUMAN; MOLECULAR CLONING; NONHUMAN; PARKINSON DISEASE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSGENIC ORGANISM; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; WORM; ANIMAL; ANTAGONISTS AND INHIBITORS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PARKINSONISM; PHYSIOLOGY; PROCEDURES; PROTEINOSIS; TRANSGENIC ANIMAL;

ALPHA-SYNUCLEIN; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BACTERIAL PROTEINS; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CIRCULAR DICHROISM; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; PARKINSONIAN DISORDERS; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; RNA INTERFERENCE;

EID: 84945334222     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/1871527314666150821110538     Document Type: Article

References (61)

1. Dobson CM. Protein folding and misfolding. Nature 2003; 426: 884-90.
2. Uversky VN. Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation. J Neurochem 2007; 103: 17-37.
3. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997; 388: 839-40.
4. Polymeropoulos MH, Lavedan C, Leroy E, et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997; 276: 2045-7.
5. Kruger R, Kuhn W, Muller T, et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 1998; 18: 106-8.
6. Li J, Uversky VN, Fink AL. Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein. Biochemistry 2001; 40: 11604-13.
7. Uversky VN, Li J, Souillac P, et al. Biophysical properties of the synucleins and their propensities to fibrillate: inhibition of alphasynuclein assembly by beta- and gamma-synucleins. J Biol Chem 2002; 277: 11970-8.
8. Goers J, Uversky VN, Fink AL. Polycation-induced oligomerization and accelerated fibrillation of human alphasynuclein in vitro. Protein Sci 2003; 12: 702-7.
9. Munishkina LA, Henriques J, Uversky VN, Fink AL. Role of protein-water interactions and electrostatics in alpha-synuclein fibril formation. Biochemistry 2004; 43: 3289-300.
10. van Ham TJ, Thijssen KL, Breitling R, Hofstra RM, Plasterk RH, Nollen EA. C. elegans model identifies genetic modifiers of alphasynuclein inclusion formation during aging. PLoS Genet 2008; 4: e1000027.
11. van Ham TJ, Esposito A, Kumita JR, et al. Towards multiparametric fluorescent imaging of amyloid formation: studies of a YFP model of alpha-synuclein aggregation. J Mol Biol 2010; 395: 627-42.
12. Lakso M, Vartiainen S, Moilanen AM, et al. Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J Neurochem 2003; 86: 165-72.
13. Hamamichi S, Rivas RN, Knight AL, Cao S, Caldwell KA, Caldwell GA. Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson's disease model. Proc Natl Acad Sci USA 2008; 105: 728-33.
14. Roodveldt C, Bertoncini C, Andersson A, et al. Chaperone proteostasis in Parkinson's disease: stabilization of the Hsp70/alpha-synuclein complex by Hip. EMBO J 2009; 28: 3758- 70.
15. Link CD, Cypser JR, Johnson CJ, Johnson TE. Direct observation of stress response in Caenorhabditis elegans using a reporter transgene. Cell Stress Chaperones 1999; 4: 235-42.
16. McColl G, Roberts BR, Gunn AP, et al. The Caenorhabditis elegans A beta 1-42 model of Alzheimer disease predominantly expresses A beta 3-42. J Biol Chem 2009; 284: 22697-702.
17. Satyal SH, Schmidt E, Kitagawa K, et al. Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans. Proc Natl Acad Sci USA 2000; 97: 5750-5.
18. Nollen EA, Garcia SM, van Haaften G, et al. Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc Natl Acad Sci USA 2004; 101: 6403-8.
19. Brignull HR, Moore FE, Tang SJ, Morimoto RI. Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a pan-neuronal Caenorhabditis elegans model. J Neurosci 2006; 26: 7597-606.
20. Bodhicharla R, Nagarajan A, Winter J, et al. Effects of alphasynuclein overexpression in transgenic Caenorhabditis elegans strains. CNS Neurol Disord Drug Targets 2012; 11: 965-75.
21. Kaminski Schierle GS, Bertoncini CW, Chan FT, et al. A FRET sensor for non-invasive imaging of amyloid formation in vivo. Chemphyschemistry 2011; 12: 673-80.
22. Anbalagan C, Lafayette I, Antoniou-Kourounioti M, et al. Transgenic nematodes as biosensors for metal stress in soil pore water samples. Ecotoxicology 2012; 21: 439-55.
23. Hunt-Newbury R, Viveiros R, Johnsen R, et al. High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 2007; 5: e237.
24. Rekas A, Adda CG, Andrew Aquilina J, et al. Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol 2004; 340: 1167-83.
25. Rizzo MA, Springer GH, Granada B, Piston DW. An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 2004; 22: 445-9.
26. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 2002; 20: 87-90.
27. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-5.
28. Reinhart BJ, Ruvkun G. Isoform-specific mutations in the Caenorhabditis elegans heterochronic gene lin-14 affect stagespecific patterning. Genetics 2001; 157: 199-209.
29. de Pomerai DI, Ip WK, McLaughlin M, Perry KC. Expression in non-lens tissues of an enzyme activity related to the 'lens-specific' protein, delta crystallin. Development 1991; 111: 181-90.
30. LeVine H, 3rd. Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci 1993; 2: 404-10.
31. Williams PL, Dusenbery DB. Aquatic toxicity testing using the nematode, Caenorhabditis elegans. Environ Toxicol Chem 1990; 9: 1285-90.
32. Mutwakil MHAZ, Steele TJG, Lowe KC, de Pomerai DI. Surfactant stimulation of growth in the nematode Caenorhabditis elegans. Enzyme Microb Technol 1997; 20: 462-70.
33. Kamath RS, Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003; 30: 313-21.
34. de Pomerai DI, Smith B, Dawe A, et al. Microwave radiation can alter protein conformation without bulk heating. FEBS Lett 2003; 543: 93-7.
35. Mitchell DH, Stiles JW, Santelli J, Sanadi DR. Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol 1979; 34: 28-36.
36. Golding C, Senior S, Wilson MT, O'Shea, P. Time resolution of binding and membrane insertion of a mitochondrial signal peptide: correlation with structural changes and evidence for cooperativity. Biochemistry 1996; 35: 10931-7.
37. Visser NV, Hink MA, Borst JW, van der Krogt GN, Visser AJ. Circular dichroism spectroscopy of fluorescent proteins. FEBS Lett 2002; 521: 31-5.
38. Uversky VN, Li J, Fink AL. Pesticides directly accelerate the rate of alpha-synuclein fibril formation: a possible factor in Parkinson's disease. FEBS Lett 2001; 500: 105-8.
39. Patterson G, Day RN, Piston D. Fluorescent protein spectra. J Cell Sci 2001; 114: 837-8.
40. Pollok BA, Heim R. Using GFP in FRET-based applications. Trends Cell Biol 1999; 9: 57-60.
41. Chadborn N, Bryant J, Bain AJ, O'Shea P. Ligand-dependent conformational equilibria of serum albumin revealed by tryptophan fluorescence quenching. Biophys J 1999; 76: 2198-207.
42. Zdinak LJ, Greenberg IB, Szewczyk N, et al. Transgene-coded chimeric proteins as reporters of intracellular proteolysis: starvation- induced catabolism of a lacZ fusion protein in muscle cells of Caenorhabditis elegans. J Cell Biochem 1997; 67: 143-5.
43. Giasson BI, Murray IV, Trojanowski JQ, Lee VM. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J Biol Chem 2001; 276: 2380-6.
44. Murray IV, Giasson BI, Quinn S, et al. Role of alpha-synuclein carboxy-terminus on fibril formation in vitro. Biochemistry 2003; 42: 8530-40.
45. McLean PJ, Kawamata H, Hyman BT. Alpha-synuclein-enhanced green fluorescent protein fusion proteins form proteasome sensitive inclusions in primary neurons. Neuroscience 2001; 104: 901-12.
46. Rockenstein E, Schwach G, Ingolic E, et al. Lysosomal pathology associated with alpha-synuclein accumulation in transgenic models using an eGFP fusion protein. J Neurosci Res 2005; 80: 247-59.
47. Leroux MR, Melki R, Gordon B, Batelier G, Candido EP. Structure-function studies on small heat shock protein oligomeric assembly and interaction with unfolded polypeptides. J Biol Chem 1997; 272: 24646-56.
48. Anbalagan C, Lafayette I, Antoniou-Kourounioti M, et al. Use of transgenic GFP reporter strains of the nematode Caenorhabditis elegans to investigate the patterns of stress responses induced by pesticides and by organic extracts from agricultural soils. Ecotoxicology 2013; 22: 72-85.
49. Link CD. Transgenic invertebrate models of age-associated neurodegenerative diseases. Mech Ageing Dev 2001; 122: 1639- 49.
50. Masters TA, Marsh RJ, Armoogum DA, Nicolaou N, Larijani B, Bain AJ. Restricted state selection in fluorescent protein Forster resonance energy transfer. J Am Chem Soc 2013; 135: 7883-90.
51. Robinson D, Besley NA, O'Shea P, Hirst JD. Di-8-ANEPPS emission spectra in phospholipid/cholesterol membranes: a theoretical study. J Phys Chem B 2011; 115: 4160-7.
52. Uversky VN, Li J, Bower K, Fink AL. Synergistic effects of pesticides and metals on the fibrillation of alpha-synuclein: implications for Parkinson's disease. Neurotoxicology 2002; 23: 527-36.
53. Fernagut PO, Hutson CB, Fleming SM, et al. Behavioral and histopathological consequences of paraquat intoxication in mice: effects of alpha-synuclein over-expression. Synapse 2007; 61: 991- 1001.
54. Sun F, Anantharam V, Latchoumycandane C, Kanthasamy A, Kanthasamy AG. Dieldrin induces ubiquitin-proteasome dysfunction in alpha-synuclein overexpressing dopaminergic neuronal cells and enhances susceptibility to apoptotic cell death. J Pharmacol Exp Ther 2005; 315: 69-79.
55. Brown DR. Metal binding to alpha-synuclein peptides and its contribution to toxicity. Biochem Biophys Res Commun 2009; 380: 377-81.
56. Drago D, Bolognin S, Zatta P. Role of metal ions in the abeta oligomerization in Alzheimer's disease and in other neurological disorders. Curr Alzheimer Res 2008; 5: 500-7.
57. Ryu J, Girigoswami K, Ha C, Ku SH, Park CB Influence of multiple metal ions on beta-amyloid aggregation and dissociation on a solid surface. Biochemistry 2008; 47: 5328-35.
58. Allsop D, Mayes J, Moore S, Masad A, Tabner BJ. Metaldependent generation of reactive oxygen species from amyloid proteins implicated in neurodegenerative disease. Biochem Soc Trans 2008; 36: 1293-8.
59. Kritzer JA, Hamamichi S, McCaffery JM, et al. Rapid selection of cyclic peptides that reduce alpha-synuclein toxicity in yeast and animal models. Nat Chem Biol 2009; 5: 655-63.
60. Jadiya P, Khan A, Sammi SR, Kaur S, Mir SS, Nazir A. Anti- Parkinsonian effects of Bacopa monnieri: insights from transgenic and pharmacological Caenorhabditis elegans models of Parkinson's disease. Biochem Biophys Res Commun 2011; 413: 605-10.
61. Roberti MJ, Jovin TM, Jares-Erijman E. Confocal fluorescence anisotropy and FRAP imaging of alpha-synuclein amyloid aggregates in living cells. PLoS One 2011; 6: e23338.