Ribosylation rapidly induces α-synuclein to form highly cytotoxic molten globules of advanced glycation end products

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  Chen, Lan ^a   Wei, Yan ^a,c   Wang, Xueqing ^a   He, Rongqiao ^a,b,c  

^a INSTITUTE OF BIOPHYSICS   (China)

^b INSTITUTE OF PSYCHOLOGY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ALPHA SYNUCLEIN; GLOBULAR PROTEIN; GLUCOSE; LACTATE DEHYDROGENASE; LYSINE; REACTIVE OXYGEN METABOLITE; RIBOSE; THIOFLAVINE; TRYPSIN;

AMINO TERMINAL SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; CYTOTOXICITY; DIMERIZATION; ENZYME RELEASE; FLUORESCENCE; GLYCATION; INCUBATION TIME; LIGHT SCATTERING; MOLTEN GLOBULE; MORPHOLOGY; NONHUMAN; OXIDATIVE STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN POLYMERIZATION; PROTEIN SECONDARY STRUCTURE; RIBOSYLATION; SEQUENCE ANALYSIS; WESTERN BLOTTING; APOPTOSIS; CELL SURVIVAL; CHEMISTRY; DOSE RESPONSE; DRUG EFFECT; HUMAN; INTRACELLULAR SPACE; KINETICS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; SPECTROFLUOROMETRY; TIME; TUMOR CELL LINE;

ALPHA-SYNUCLEIN; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CIRCULAR DICHROISM; DOSE-RESPONSE RELATIONSHIP, DRUG; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; INTRACELLULAR SPACE; KINETICS; LYSINE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; REACTIVE OXYGEN SPECIES; RIBOSE; SPECTROMETRY, FLUORESCENCE; TIME FACTORS;

EID: 77949359499     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009052     Document Type: Article

References (75)

1. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
2. Barzilai A, Melamed E (2003) Molecular mechanisms of selective dopaminergic neuronal death in Parkinson's disease. Trends Mol Med 9: 126-132.
3. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, et al. (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science 302: 841.
4. Iwatsubo T, Yamaguchi H, Fujimuro M, Yokosawa H, Ihara Y, et al. (1996) Purification and characterization of Lewy bodies from the brains of patients with diffuse Lewy body disease. Am J Pathol 148: 1517-1529.
5. Iwatsubo T (2007) Pathological biochemistry of alpha-synucleinopathy. Neuropathology 27: 474-478.
6. Shults CW (2006) Lewy bodies. Proc Natl Acad Sci U S A 103: 1661-1668.
7. Zimran A, Neudorfer O, Elstein D (2005) The glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N Engl J Med 352: 728-731; author reply 728-731.
8. Sandal M, Valle F, Tessari I, Mammi S, Bergantino E, et al. (2008) Conformational equilibria in monomeric alpha-synuclein at the single-molecule level. PLoS Biol 6: e6.
9. Munch G, Luth HJ, Wong A, Arendt T, Hirsch E, et al. (2000) Crosslinking of alpha-synuclein by advanced glycation endproducts-an early pathophysiological step in Lewy body formation? J Chem Neuroanat 20: 253-257.
10. Dorval V, Fraser PE (2006) Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alpha-synuclein. J Biol Chem 281: 9919-9924.
11. Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, et al. (2002) alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4: 160-164.
12. Shaikh S, Nicholson LF (2008) Advanced glycation end products induce in vitro cross-linking of alpha-synuclein and accelerate the process of intracellular inclusion body formation. J Neurosci Res 86: 2071-2082.
13. Dalfo E, Portero-Otin M, Ayala V, Martinez A, Pamplona R, et al. (2005) Evidence of oxidative stress in the neocortex in incidental Lewy body disease. J Neuropathol Exp Neurol 64: 816-830.
14. Seuffer R (1977) [A new method for the determination of sugars in cerebrospinal fluid (author's transl)]. J Clin Chem Clin Biochem 15: 663-668.
15. Garlick RL, Mazer JS, Higgins PJ, Bunn HF (1983) Characterization of glycosylated hemoglobins. Relevance to monitoring of diabetic control and analysis of other proteins. J Clin Invest 71: 1062-1072.
16. Shaklai N, Garlick RL, Bunn HF (1984) Nonenzymatic glycosylation of human serum albumin alters its conformation and function. J Biol Chem 259: 3812-3817.
17. Mendez DL, Jensen RA, McElroy LA, Pena JM, Esquerra RM (2005) The effect of non-enzymatic glycation on the unfolding of human serum albumin. Arch Biochem Biophys 444: 92-99.
18. James PE, Lang D, Tufnell-Barret T, Milsom AB, Frenneaux MP (2004) Vasorelaxation by red blood cells and impairment in diabetes: reduced nitric oxide and oxygen delivery by glycated hemoglobin. Circ Res 94: 976-983.
19. Necula M, Kuret J (2004) Pseudophosphorylation and glycation of tau protein enhance but do not trigger fibrillization in vitro. J Biol Chem 279: 49694-49703.
20. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M (1998) 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: 6469-6473.
21. Stefani M, Dobson CM (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 81: 678-699.
22. Lansbury PT, Lashuel HA (2006) A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443: 774-779.
23. Sanghera N, Wall M, Venien-Bryan C, Pinheiro TJ (2008) Globular and prefibrillar prion aggregates are toxic to neuronal cells and perturb their electrophysiology. Biochim Biophys Acta 1784: 873-881.
24. Tabner BJ, El-Agnaf OM, German MJ, Fullwood NJ, Allsop D (2005) Protein aggregation, metals and oxidative stress in neurodegenerative diseases. Biochem Soc Trans 33: 1082-1086.
25. Chromy BA, Nowak RJ, Lambert MP, Viola KL, Chang L, et al. (2003) Self-assembly of Abeta(1-42) into globular neurotoxins. Biochemistry 42: 12749-12760.
26. Bucciantini M, Calloni G, Chiti F, Formigli L, Nosi D, et al. (2004) Prefibrillar amyloid protein aggregates share common features of cytotoxicity. J Biol Chem 279: 31374-31382.
27. Sattarahmady N, Moosavi-Movahedi AA, Ahmad F, Hakimelahi GH, Habibi-Rezaei M, et al. (2007) Formation of the molten globule-like state during prolonged glycation of human serum albumin. Biochim Biophys Acta 1770: 933-942.
28. He RQ, Yang MD, Zheng X, Zhou JX (1995) Isolation and some properties of glycated D-glyceraldehyde-3-phosphate dehydrogenase from rabbit muscle. Biochem J 309 ( Pt1): 133-139.
29. He RQ, Li YG, Wu XQ, Li L (1995) Inactivation and conformation changes of the glycated and non-glycated D-glyceraldehyde-3-phosphate dehydrogenase during guanidine-HCl denaturation. Biochim Biophys Acta 1253: 47-56.
30. Sheng Z, Liu Y, Chen L, He R (2008) Nonenzymatic Glycation of α-Synuclein and Changes in Its Conformation. Progress in Biochemistry and Biophysics 35: 1202-1208.
31. Wei Y, Chen L, Chen J, Ge L, He R (2009) Rapid glycation with D-ribose induces globular amyloid-like aggregations of BSA with high cytotoxicity to SH-SY5Y cells. BMC Cell Biol 10: 10.
32. Chen L, Wei Y, Wang X, He R (2009) D-Ribosylated Tau forms globular aggregates with high cytotoxicity. Cell Mol Life Sci 66: 2559-2571.
33. Nie CL, Wei Y, Chen X, Liu YY, Dui W, et al. (2007) Formaldehyde at low concentration induces protein tau into globular amyloid-like aggregates in vitro and in vivo. PLoS ONE 2: e629.
34. Liu X, Metzger LE (2007) Application of fluorescence spectroscopy for monitoring changes in nonfat dry milk during storage. J Dairy Sci 90: 24-37.
35. Ikeda K, Higashi T, Sano H, Jinnouchi Y, Yoshida M, et al. (1996) N (epsilon)-(carboxymethyl)lysine protein adduct is a major immunological epitope in proteins modified with advanced glycation end products of the Maillard reaction. Biochemistry 35: 8075-8083.
36. Mosca A, Carenini A, Zoppi F, Carpinelli A, Banfi G, et al. (1987) Plasma protein glycation as measured by fructosamine assay. Clin Chem 33: 1141-1146.
37. Baker JR, Metcalf PA, Johnson RN, Newman D, Rietz P (1985) Use of protein-based standards in automated colorimetric determinations of fructosamine in serum. Clin Chem 31: 1550-1554.
38. Bertoncini CW, Jung YS, Fernandez CO, Hoyer W, Griesinger C, et al. (2005) Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein. Proc Natl Acad Sci U S A 102: 1430-1435.
39. Matulis D, Lovrien R (1998) 1-Anilino-8-naphthalene sulfonate anion-protein binding depends primarily on ion pair formation. Biophys J 74: 422-429.
40. Semisotnov GV, Rodionova NA, Razgulyaev OI, Uversky VN, Gripas AF, et al. (1991) Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 31: 119-128.
41. Hoyer W, Antony T, Cherny D, Heim G, Jovin TM, et al. (2002) Dependence of alpha-synuclein aggregate morphology on solution conditions. J Mol Biol 322: 383-393.
42. Naiki H, Higuchi K, Hosokawa M, Takeda T (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal Biochem 177: 244-249.
43. Cheon M, Chang I, Mohanty S, Luheshi LM, Dobson CM, et al. (2007) Structural reorganisation and potential toxicity of oligomeric species formed during the assembly of amyloid fibrils. PLoS Comput Biol 3: 1727-1738.
44. Eriksen JL, Dawson TM, Dickson DW, Petrucelli L (2003) Caught in the act: alpha-synuclein is the culprit in Parkinson's disease. Neuron 40: 453-456.
45. Hasegawa Y, Suehiro A, Higasa S, Namba M, Kakishita E (2002) Enhancing effect of advanced glycation end products on serotonin-induced platelet aggregation in patients with diabetes mellitus. Thromb Res 107: 319-323.
46. Koga K, Yamagishi S, Okamoto T, Inagaki Y, Amano S, et al. (2002) Serum levels of glucose-derived advanced glycation end products are associated with the severity of diabetic retinopathy in type 2 diabetic patients without renal dysfunction. Int J Clin Pharmacol Res 22: 13-17.
47. Scott ML, Nesheim MC, Young RJ (1982) Nutrition of the Chicken. M.L. Scott and Associates, Ithaca, New York. pp 100-102.
48. Pliml W, von Arnim T, Stablein A, Hofmann H, Zimmer HG, et al. (1992) Effects of ribose on exercise-induced ischaemia in stable coronary artery disease. Lancet 340: 507-510.
49. Weinreb PH, Zhen W, Poon AW, Conway KA, Lansbury PT Jr (1996) NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35: 13709-13715.
50. Mak W, Cheng TS, Chan KH, Cheung RT, Ho SL (2005) Cerebrospinal fluid to serum glucose ratio in non-hypoglycorrhachic neurological conditions. Hong Kong Med J 11: 457-462.
51. Ptitsyn OB, Pain RH, Semisotnov GV, Zerovnik E, Razgulyaev OI (1990) Evidence for a molten globule state as a general intermediate in protein folding. FEBS Lett 262: 20-24.
52. Fink AL, Oberg KA, Seshadri S (1998) Discrete intermediates versus molten globule models for protein folding: characterization of partially folded intermediates of apomyoglobin. Fold Des 3: 19-25.
53. Ohgushi M, Wada A (1983) 'Molten-globule state': a compact form of globular proteins with mobile side-chains. FEBS Lett 164: 21-24.
54. Pande VS, Rokhsar DS (1998) Is the molten globule a third phase of proteins? Proc Natl Acad Sci U S A 95: 1490-1494.
55. Ceru S, Zerovnik E (2008) Similar toxicity of the oligomeric molten globule state and the prefibrillar oligomers. FEBS Lett 582: 203-209.
56. Yan SD, Chen X, Schmidt AM, Brett J, Godman G, et al. (1994) Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc Natl Acad Sci U S A 91: 7787-7791.
57. Degenhardt TP, Thorpe SR, Baynes JW (1998) Chemical modification of proteins by methylglyoxal. Cell Mol Biol (Noisy-le-grand) 44: 1139-1145.
58. McCance DR, Dyer DG, Dunn JA, Bailie KE, Thorpe SR, et al. (1993) Maillard reaction products and their relation to complications in insulin-dependent diabetes mellitus. J Clin Invest 91: 2470-2478.
59. Ko LW, Ko EC, Nacharaju P, Liu WK, Chang E, et al. (1999) An immunochemical study on tau glycation in paired helical filaments. Brain Res 830: 301-313.
60. Matiacevich SB, Buera MP (2006) A critical evaluation of fluorescence as a potential marker for the Maillard reaction. Food Chem 95: 423-430.
61. Moreaux V, Birlouez-Aragon I (1997) Degradation of tryptophan in heated β-lactoglobulin-lactose mixtures is associated with intense Maillard reaction. J Agric Food Chem 45: 1905-1910.
62. Ferrer E, Alegria A, Farre R, Clemente G, Calvo C (2005) Fluorescence, browning index, and color in infant formulas during storage. J Agric Food Chem 53: 4911-4917.
63. Munch G, Kuhla B, Luth HJ, Arendt T, Robinson SR (2003) Anti-AGEing defences against Alzheimer's disease. Biochem Soc Trans 31: 1397-1399.
64. Huang C, Ren G, Zhou H, Wang CC (2005) A new method for purification of recombinant human alpha-synuclein in Escherichia coli. Protein Expr Purif 42: 173-177.
65. Syrovy I (1994) Glycation of albumin: reaction with glucose, fructose, galactose, ribose or glyceraldehyde measured using four methods. J Biochem Biophys Methods 28: 115-121.
66. Xu YJ, Wu XQ, Liu W, Lin XH, Chen JW, et al. (2002) A convenient assay of glycoserum by nitroblue tetrazolium with iodoacetamide. Clin Chim Acta 325: 127-131.
67. Coussons PJ, Jacoby J, McKay A, Kelly SM, Price NC, et al. (1997) Glucose modification of human serum albumin: a structural study. Free Radic Biol Med 22: 1217-1227.
68. Nie CL, Wang XS, Liu Y, Perrett S, He RQ (2007) Amyloid-like aggregates of neuronal tau induced by formaldehyde promote apoptosis of neuronal cells. BMC Neurosci 8: 9.
69. Mayo L, Stein R (2007) Characterization of LPS and interferon-gamma triggered activation-induced cell death in N9 and primary microglial cells: induction of the mitochondrial gateway by nitric oxide. Cell Death Differ 14: 183-186.
70. Racher AJ, Looby D, Griffiths JB (1990) Use of lactate dehydrogenase release to assess changes in culture viability. Cytotechnology 3: 301-307.
71. Legrand C, Bour JM, Jacob C, Capiaumont J, Martial A, et al. (1992) Lactate dehydrogenase (LDH) activity of the cultured eukaryotic cells as marker of the number of dead cells in the medium [corrected]. J Biotechnol 25: 231-243.
72. Smith WW, Norton DD, Gorospe M, Jiang H, Nemoto S, et al. (2005) Phosphorylation of p66Shc and forkhead proteins mediates Abeta toxicity. J Cell Biol 169: 331-339.
73. Xu Z, Xu RX, Liu BS, Jiang XD, Huang T, et al. (2005) Time window characteristics of cultured rat hippocampal neurons subjected to ischemia and reperfusion. Chin J Traumatol 8: 179-182.
74. Tsou CL (1988) Folding of the nascent peptide chain into a biologically active protein. Biochemistry 27: 1809-1812.
75. Reim DF, Speicher DW (1994) A method for high-performance sequence analysis using polyvinylidene difluoride membranes with a biphasic reaction column sequencer. Anal Biochem 216: 213-222.