Accelerated fibrillation of α-synuclein induced by the combined action of macromolecular crowding and factors inducing partial folding

Current Alzheimer Research

Volumn 6, Issue 3, 2009, Pages 252-260

  Munishkina, L A ^a   Finka, A L ^a   Uversky, V N ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

synuclein; Aggregation; Crowding; Fibrillation; GAGs; Metals; Organic solvent; Parkinson's disease; Pesticides; Polycations

Indexed keywords

ALCOHOL; ALPHA SYNUCLEIN; GLYCOSAMINOGLYCAN; MACROGOL; METAL; ORGANIC SOLVENT; PESTICIDE; POLYANION; POLYCATION;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE;

ALPHA-SYNUCLEIN; ANIMALS; ANIONS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ESCHERICHIA COLI; GLYCOSAMINOGLYCANS; HYDROGEN-ION CONCENTRATION; MACROMOLECULAR SUBSTANCES; METALS; METHYLAMINES; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; OXIDANTS; PHYSICOCHEMICAL PHENOMENA; POLYETHYLENE GLYCOLS; PROTEIN BINDING; STATIC ELECTRICITY; TIME FACTORS;

EID: 67149087384     PISSN: 15672050     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720509788486491     Document Type: Article

References (58)

1. Maroteaux L, Campanelli JT, Scheller RH. Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J Neurosci 8: 2804-2815 (1988). (Pubitemid 18219069)
2. Jakes R, Spillantini MG, Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett 345: 27-32 (1994). (Pubitemid 24154659)
3. Iwai A, Masliah E, Yoshimoto M, Ge N, Flanagan L, de Silva HA, et al. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14: 467-475 (1995).
4. Weinreb PH, Zhen W, Poon AW, Conway KA, Lansbury PT, Jr. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35: 13709-13715 (1996). (Pubitemid 26363912)
5. Uversky VN, Li J, Fink AL. Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J Biol Chem 276: 10737-10744 (2001). (Pubitemid 38089246)
6. Eliezer D, Kutluay E, Bussell R, Jr., Browne G. Conformational properties of alpha-synuclein in its free and lipid-associated states. J Mol Biol 307: 1061-1073 (2001). (Pubitemid 33029953)
7. Uversky VN, Gillespie JR, Fink AL. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41: 415-427 (2000).
8. Uversky VN. Natively unfolded proteins: a point where biology waits for physics. Protein Sci 11: 739-756 (2002). (Pubitemid 34241284)
9. Uversky VN. What does it mean to be natively unfolded? Eur J Biochem 269: 2-12 (2002).
10. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M. alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc Natl Acad Sci USA 95: 6469-6473 (1998). (Pubitemid 28249037)
11. Spillantini MG, Goedert M. The alpha-synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. Ann N Y Acad Sci 920: 16-27 (2000). (Pubitemid 32056547)
12. Tofaris GK, Spillantini MG. Alpha-synuclein dysfunction in Lewy body diseases. Mov Disord 20 (Suppl 12): S37-44 (2005). (Pubitemid 41419553)
13. Trojanowski JQ, Goedert M, Iwatsubo T, Lee VM. Fatal attractions: abnormal protein aggregation and neuron death in Parkinson's disease and Lewy body dementia. Cell Death Differ 5: 832-837 (1998). (Pubitemid 28484393)
14. Galvin JE, Lee VM, Schmidt ML, Tu PH, Iwatsubo T, Trojanowski JQ. Pathobiology of the Lewy body. Adv Neurol 80: 313-324 (1999).
15. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci 2: 492-501 (2001).
16. Goedert M. Parkinson's disease and other alpha-synucleinopathies. Clin Chem Lab Med 39: 308-312 (2001).
17. Uversky VN. Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation. J Neurochem 103: 17-37 (2007).
18. Uversky VN, Fink AL. Biophysical properties of human alpha-synuclein and its role in Parkinson's disease. In: Pandalai SG, 'Recent Research Developments in Proteins'.(Pandalai SG.Pandalai SGs). Kerala, India: Transworld Research Network, p. 153-186 (2002).
19. Uversky VN. A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders. J Biomol Struct Dyn 21: 211-234 (2003). (Pubitemid 37204199)
20. Uversky VN, Li J, Fink AL. Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J Biol Chem 276: 44284-44296 (2001). (Pubitemid 37384003)
21. 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 23: 527-536 (2002). (Pubitemid 36527673)
22. Uversky VN, Li J and Fink AL. Pesticides directly accelerate the rate of alpha-synuclein fibril formation: a possible factor in Parkinson's disease. FEBS Lett 500: 105-108 (2001). (Pubitemid 32607541)
23. Manning-Bog AB, McCormack AL, Li J, Uversky VN, Fink AL and Di Monte DA. The herbicide paraquat causes up-regulation, aggregation of alpha-synuclein in mice: paraquat and alpha-synuclein. J Biol Chem 277: 1641-1644 (2002). (Pubitemid 34968732)
24. Cohlberg JA, Li J, Uversky VN and Fink AL. Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from alpha-synuclein in vitro. Biochemistry 41: 1502-1511 (2002). (Pubitemid 34112739)
25. Goers J, Manning-Bog AB, McCormack AL, Millett IS, Doniach S, Di Monte DA, et al. Nuclear localization of alpha-synuclein , its interaction with histones. Biochemistry 42: 8465-8471 (2003).
26. Goers J, Uversky VN, Fink AL. Polycation-induced oligomerization and accelerated fibrillation of human alpha-synuclein in vitro. Protein Sci 12: 702-707 (2003). (Pubitemid 36348457)
27. Munishkina LA, Phelan C, Uversky VN , Fink AL. Conformational behavior and aggregation of alpha-synuclein in organic solvents: modeling the effects of membranes. Biochemistry 42: 2720-2730 (2003). (Pubitemid 36330626)
28. Uversky VN, Li J, Fink AL. Trimethylamine-N-oxide-induced folding of alpha-synuclein. FEBS Lett 509: 31-35 (2001).
29. Zimmerman SB, Trach SO. Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222: 599-620 (1991).
30. Zimmerman SB, Minton AP. Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22: 27-65 (1993). (Pubitemid 23180316)
31. Fulton AB. How crowded is the cytoplasm? Cell 30: 345-347 (1982).
32. Minton AP. Influence of excluded volume upon macromolecular structure and associations in 'crowded' media. Curr Opin Biotechnol 8: 65-69 (1997).
33. Ellis RJ. Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26: 597-604 (2001). (Pubitemid 32925190)
34. Minton AP. Implications of macromolecular crowding for protein assembly. Curr Opin Struct Biol 10: 34-39 (2000). (Pubitemid 30099324)
35. Minton AP. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276: 10577-10580 (2001). (Pubitemid 38089223)
36. Minton AP. Protein folding: Thickening the broth. Curr Biol 10: R97-99 (2000). (Pubitemid 30115733)
37. Eggers DK , Valentine JS. Crowding and hydration effects on protein conformation: a study with sol-gel encapsulated proteins. J Mol Biol 314: 911-922 (2001). (Pubitemid 34087857)
38. Eggers DK, Valentine JS. Molecular confinement influences protein structure and enhances thermal protein stability. Protein Sci 10: 250-261 (2001). (Pubitemid 32229119)
39. Bismuto E, Martelli PL, De Maio A, Mita DG, Irace G , Casadio R. Effect of molecular confinement on internal enzyme dynamics: frequency domain fluorometry and molecular dynamics simulation studies. Biopolymers 67: 85-95 (2002). (Pubitemid 34712095)
40. Morar AS, Olteanu A, Young GB , Pielak GJ. Solvent-induced collapse of alpha-synuclein and acid-denatured cytochrome c. Protein Sci 10: 2195-2199 (2001). (Pubitemid 32988636)
41. Hatters DM, Minton AP, Howlett GJ. Macromolecular crowding accelerates amyloid formation by human apolipoprotein C-II. J Biol Chem 277: 7824-7830 (2002). (Pubitemid 34968230)
42. Uversky VN, Cooper EM, Bower KS, Li J, Fink AL. Accelerated alpha-synuclein fibrillation in crowded milieu. FEBS Lett 515: 99-103 (2002). (Pubitemid 34273905)
43. Shtilerman MD, Ding TT, Lansbury PT Jr. Molecular crowding accelerates fibrillization of alpha-synuclein: could an increase in the cytoplasmic protein concentration induce Parkinson's disease? Biochemistry 41: 3855-3860 (2002).
44. Nielsen L, Khurana R, Coats A, Frokjaer S, Brange J, Vyas S, et al. Effect of environmental factors on the kinetics of insulin fibril formation: elucidation of the molecular mechanism. Biochemistry 40: 6036-6046 (2001).
45. Yamin G, Glaser CB, Uversky VN , Fink AL. Certain metals trigger fibrillation of methionine-oxidized alpha-synuclein. J Biol Chem 278: 27630-27635 (2003). (Pubitemid 36899949)
46. Munishkina LA, Henriques J, Uversky VN, Fink AL. Role of protein-water interactions and electrostatics in alpha-synuclein fibril formation. Biochemistry 43: 3289-3300 (2004). (Pubitemid 38352279)
47. Tanner CM. The role of environmental toxins in the etiology of Parkinson's disease. Trends Neurosci 12: 49-54 (1989). (Pubitemid 19054583)
48. Hirsch EC, Brandel JP, Galle P, Javoy-Agid F, Agid Y. Iron and aluminum increase in the substantia nigra of patients with Parkinson's disease: an X-ray microanalysis. J Neurochem 56: 446-451 (1991). (Pubitemid 21901982)
49. Good PF, Olanow CW, Perl DP. Neuromelanin-containing neurons of the substantia nigra accumulate iron and aluminum in Parkinson's disease: a LAMMA study. Brain Res 593: 343-346 (1992).
50. Yasui M, Kihira T, Ota K. Calcium, magnesium and aluminum concentrations in Parkinson's disease. Neurotoxicology 13: 593-600 (1992).
51. Hertzman C, Wiens M, Snow B, Kelly S, Calne D. A case-control study of Parkinson's disease in a horticultural region of British Columbia. Mov Disord 9: 69-75 (1994). (Pubitemid 24022617)
52. Gorell JM, Johnson CC, Rybicki BA, Peterson EL, Richardson RJ. The risk of Parkinson's disease with exposure to pesticides, farming, well water, and rural living. Neurology 50: 1346-1350 (1998). (Pubitemid 28240350)
53. Gorell JM, Johnson CC, Rybicki BA, Peterson EL, Kortsha GX, Brown GG, et al. Occupational exposure to manganese, copper, lead, iron, mercury and zinc and the risk of Parkinson's disease. Neurotoxicology 20: 239-247 (1999).
54. Gorell JM, Rybicki BA, Johnson CC, Peterson EL. Occupational metal exposures and the risk of Parkinson's disease. Neuroepidemiology 18: 303-308 (1999). (Pubitemid 29493517)
55. Altschuler E. Aluminum-containing antacids as a cause of idiopathic Parkinson's disease. Med Hypotheses 53: 22-23 (1999). (Pubitemid 29391318)
56. Le Couteur DG, McLean AJ, Taylor MC, Woodham BL, Board PG. Pesticides and Parkinson's disease. Biomed Pharmacother 53: 122-130 (1999).
57. Cardin AD, Weintraub HJ. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9: 21-32 (1989). (Pubitemid 19046087)
58. Bolen DW, Baskakov IV. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 310: 955-963 (2001). (Pubitemid 32738368)