Insights into the molecular mechanism of protein native-like aggregation upon glycation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 6, 2013, Pages 1010-1022

  Oliveira, Luis M A ^a,d   Gomes, Ricardo A ^a,b   Yang, Dennis ^c   Dennison, Sarah R ^e   Família, Carlos ^a   Lages, Ana ^a   Coelho, Ana V ^b   Murphy, Regina M ^c   Phoenix, David A ^f   Quintas, Alexandre ^a  

^a INSTITUTO SUPERIOR DE CIÊNCIAS DA SAÚDE EGAS MONIZ   (Portugal)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF LISBON   (Portugal)

^e UNIVERSITY OF CENTRAL LANCASHIRE   (United Kingdom)

^f UNIVERSITY OF CENTRAL LANCASHIRE   (United Kingdom)

Author keywords

Conformational disease; Cytochrome c; Glycation; Lipid monolayer; Methylglyoxal; Native like aggregation

Indexed keywords

AMYLOID; CYTOCHROME C;

ARTICLE; CONTROLLED STUDY; GLYCATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; AMYLOID; ANIMALS; CYTOCHROMES C; GLYCOSYLATION; HORSES; KINETICS; MEMBRANE LIPIDS; PROTEIN CONFORMATION; PROTEIN FOLDING; PYRUVALDEHYDE; THERMODYNAMICS;

EID: 84878106220     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.12.001     Document Type: Article

References (63)

1. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366
2. M. Sunde, and C. Blake The structure of amyloid fibrils by electron microscopy and X-ray diffraction Adv. Protein Chem. 50 1997 123 159
3. W.S. Gosal, S.L. Myers, S.E. Radford, and N.H. Thomson Amyloid under the atomic force microscope Protein Pept. Lett. 13 2006 261 270
4. M.R. Nilsson Techniques to study amyloid fibril formation in vitro Methods 34 2004 151 160
5. M.R. Krebs, E.H. Bromley, and A.M. Donald The binding of thioflavin-T to amyloid fibrils: Localisation and implications J. Struct. Biol. 149 2005 30 37
6. M.A. Smith, S. Taneda, P.L. Richey, S. Miyata, S.D. Yan, D. Stern, L.M. Sayre, V.M. Monnier, and G. Perry Advanced Maillard reaction end products are associated with Alzheimer disease pathology Proc. Natl. Acad. Sci. U.S.A. 91 1994 5710 5714
7. S.D. Yan, X. Chen, A.M. Schmidt, J. Brett, G. Godman, Y.S. Zou, C.W. Scott, C. Caputo, T. Frappier, and M.A. Smith Glycated tau protein in Alzheimer disease: A mechanism for induction of oxidant stress Proc. Natl. Acad. Sci. U.S.A. 91 1994 7787 7791
8. R. Castellani, M.A. Smith, P.L. Richey, and G. Perry Glycoxidation and oxidative stress in Parkinson disease and diffuse Lewy body disease Brain Res. 737 1996 195 200
9. G. Munch, H.J. Luth, A. Wong, T. Arendt, E. Hirsch, R. Ravid, and P. Riederer Crosslinking of alpha-synuclein by advanced glycation endproducts - an early pathophysiological step in Lewy body formation? J. Chem. Neuroanat. 20 2000 253 257
10. R. Gomes, M. Sousa Silva, A. Quintas, C. Cordeiro, A. Freire, P. Pereira, A. Martins, E. Monteiro, E. Barroso, and A. Ponces Freire Argpyrimidine, a methylglyoxal-derived advanced glycation end-product in familial amyloidotic polyneuropathy Biochem. J. 385 2005 339 345
11. M. Brownlee Advanced protein glycosylation in diabetes and aging Annu. Rev. Med. 46 1995 223 234
12. A. Bierhaus, T. Fleming, S. Stoyanov, A. Leffler, A. Babes, C. Neacsu, S.K. Sauer, M. Eberhardt, M. Schnolzer, F. Lasitschka, W.L. Neuhuber, T.I. Kichko, I. Konrade, R. Elvert, W. Mier, V. Pirags, I.K. Lukic, M. Morcos, T. Dehmer, N. Rabbani, P.J. Thornalley, D. Edelstein, C. Nau, J. Forbes, P.M. Humpert, M. Schwaninger, D. Ziegler, D.M. Stern, M.E. Cooper, U. Haberkorn, M. Brownlee, P.W. Reeh, and P.P. Nawroth Methylglyoxal modification of Nav1.8 facilitates nociceptive neuron firing and causes hyperalgesia in diabetic neuropathy Nat. Med. 18 2012 926 933
13. B. Duran-Jimenez, D. Dobler, S. Moffatt, N. Rabbani, C.H. Streuli, P.J. Thornalley, D.R. Tomlinson, and N.J. Gardiner Advanced glycation end products in extracellular matrix proteins contribute to the failure of sensory nerve regeneration in diabetes Diabetes 58 2009 2893 2903
14. M. Fukunaga, S. Miyata, S. Higo, Y. Hamada, S. Ueyama, and M. Kasuga Methylglyoxal induces apoptosis through oxidative stress-mediated activation of p38 mitogen-activated protein kinase in rat Schwann cells Ann. N. Y. Acad. Sci. 1043 2005 151 157
15. S. Ohkawara, T. Tanaka-Kagawa, Y. Furukawa, and H. Jinno Methylglyoxal activates the human transient receptor potential ankyrin 1 channel J. Toxicol. Sci. 37 2012 831 835
16. B.M. Radu, D.I. Dumitrescu, C.C. Mustaciosu, and M. Radu Dual effect of methylglyoxal on the intracellular Ca2 + signaling and neurite outgrowth in mouse sensory neurons Cell. Mol. Neurobiol. 32 2012 1047 1057
17. Y.G. Choi, J.I. Kim, Y.C. Jeon, S.J. Park, E.K. Choi, R. Rubenstein, R.J. Kascsak, R.I. Carp, and Y.S. Kim Nonenzymatic glycation at the N terminus of pathogenic prion protein in transmissible spongiform encephalopathies J. Biol. Chem. 279 2004 30402 30409
18. D. Lee, C.W. Park, S.R. Paik, and K.Y. Choi The modification of alpha-synuclein by dicarbonyl compounds inhibits its fibril-forming process Biochim. Biophys. Acta 1794 2009 421 430
19. L.M. Oliveira, A. Lages, R.A. Gomes, H. Neves, C. Familia, A.V. Coelho, and A. Quintas Insulin glycation by methylglyoxal results in native-like aggregation and inhibition of fibril formation BMC Biochem. 12 2011 41
20. B. Caughey, and P.T. Lansbury Protofibrils, pores, fibrils, and neurodegeneration: Separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 26 2003 267 298
21. D.C. Crowther, K.J. Kinghorn, E. Miranda, R. Page, J.A. Curry, F.A. Duthie, D.C. Gubb, and D.A. Lomas Intraneuronal Abeta, non-amyloid aggregates and neurodegeneration in a Drosophila model of Alzheimer's disease Neuroscience 132 2005 123 135
22. K.M. Danzer, D. Haasen, A.R. Karow, S. Moussaud, M. Habeck, A. Giese, H. Kretzschmar, B. Hengerer, and M. Kostka Different species of alpha-synuclein oligomers induce calcium influx and seeding J. Neurosci. 27 2007 9220 9232
23. J. Lauren, D.A. Gimbel, H.B. Nygaard, J.W. Gilbert, and S.M. Strittmatter Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers Nature 457 2009 1128 1132
24. J.I. Guijarro, M. Sunde, J.A. Jones, I.D. Campbell, and C.M. Dobson Amyloid fibril formation by an SH3 domain Proc. Natl. Acad. Sci. U.S.A. 95 1998 4224 4228
25. F. Chiti, P. Webster, N. Taddei, A. Clark, M. Stefani, G. Ramponi, and C.M. Dobson Designing conditions for in vitro formation of amyloid protofilaments and fibrils Proc. Natl. Acad. Sci. U.S.A. 96 1999 3590 3594
26. V. Villegas, J. Zurdo, V.V. Filimonov, F.X. Aviles, C.M. Dobson, and L. Serrano Protein engineering as a strategy to avoid formation of amyloid fibrils Protein Sci. 9 2000 1700 1708
27. M.K. Chow, A.M. Ellisdon, L.D. Cabrita, and S.P. Bottomley Polyglutamine expansion in ataxin-3 does not affect protein stability: Implications for misfolding and disease J. Biol. Chem. 279 2004 47643 47651
28. J.S. Pedersen, G. Christensen, and D.E. Otzen Modulation of S6 fibrillation by unfolding rates and gatekeeper residues J. Mol. Biol. 341 2004 575 588
29. G. Plakoutsi, N. Taddei, M. Stefani, and F. Chiti Aggregation of the acylphosphatase from Sulfolobus solfataricus: The folded and partially unfolded states can both be precursors for amyloid formation J. Biol. Chem. 279 2004 14111 14119
30. F. Bemporad, and F. Chiti "Native-like aggregation" of the acylphosphatase from Sulfolobus solfataricus and its biological implications FEBS Lett. 583 2009 2630 2638
31. S.M. Singh, R.L. Hutchings, and K.M. Mallela Mechanisms of m-cresol-induced protein aggregation studied using a model protein cytochrome c J. Pharm. Sci. 2011
32. J. Gobom, E. Nordhoff, E. Mirgorodskaya, R. Ekman, and P. Roepstorff Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry J. Mass Spectrom. 34 1999 105 116
33. R.A. Gomes, H. Vicente Miranda, M.S. Silva, G. Graca, A.V. Coelho, A.E. Ferreira, C. Cordeiro, and A.P. Freire Yeast protein glycation in vivo by methylglyoxal. Molecular modification of glycolytic enzymes and heat shock proteins FEBS J. 273 2006 5273 5287
34. R.A. Gomes, L.M. Oliveira, M. Silva, C. Ascenso, A. Quintas, G. Costa, A.V. Coelho, M. Sousa Silva, A.E. Ferreira, A. Ponces Freire, and C. Cordeiro Protein glycation in vivo: Functional and structural effects on yeast enolase Biochem. J. 416 2008 317 326
35. C.M. Wilson Studies and critique of Amido Black 10B, Coomassie Blue R, and Fast Green FCF as stains for proteins after polyacrylamide gel electrophoresis Anal. Biochem. 96 1979 263 278
36. W.C. Johnson Analyzing protein circular dichroism spectra for accurate secondary structures Proteins 35 1999 307 312
37. L. Whitmore, and B.A. Wallace DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32 2004 W668 W673
38. L. Whitmore, and B.A. Wallace Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases Biopolymers 89 2008 392 400
39. R.A. Demel Monolayers - description of use and interaction Methods Enzymol. 32 1974 539 544
40. R.A. Demel, W. Jordi, H. Lambrechts, H. van Damme, R. Hovius, and B. de Kruijff Differential interactions of apo- and holocytochrome c with acidic membrane lipids in model systems and the implications for their import into mitochondria J. Biol. Chem. 264 1989 3988 3997
41. W. Jordi, L.X. Zhou, M. Pilon, R.A. Demel, and B. de Kruijff The importance of the amino terminus of the mitochondrial precursor protein apocytochrome c for translocation across model membranes J. Biol. Chem. 264 1989 2292 2301
42. C.N. Pace Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131 1986 266 280
43. D.W. Bolen, and M.M. Santoro Unfolding free energy changes determined by the linear extrapolation method. 2. Incorporation of delta G degrees N-U values in a thermodynamic cycle Biochemistry 27 1988 8069 8074
44. M.M. Santoro, and D.W. Bolen Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27 1988 8063 8068
45. C. Park, and S. Marqusee Analysis of the stability of multimeric proteins by effective DeltaG and effective m-values Protein Sci. 13 2004 2553 2558
46. M. Caracotsios, and W.E. Stewart Sensitivity analysis of initial value problems with mixed ODEs and algebraic equations Comput. Chem. Eng. 9 1985 359 365
47. M. Caracotsios, and W.E. Stewart Computer-aided Modeling of Reactive Systems 2008 Wiley Hoboken, NJ
48. W.E. Stewart, M. Caracotsios, and J.P. Sorensen Parameter estimation from multiresponse data AICHE J. 38 1992 641 650
49. H. Akaike A new look at the statistical model identification IEEE Trans. Autom. Control 19 1974 716 723
50. N. Sreerama, and R.W. Woody Computation and analysis of protein circular dichroism spectra Methods Enzymol. 383 2004 318 351
51. R. GhoshMoulick, J. Bhattacharya, S. Roy, S. Basak, and A.K. Dasgupta Compensatory secondary structure alterations in protein glycation Biochim. Biophys. Acta 1774 2007 233 242
52. J.F. Calvert, J.L. Hill, and A. Dong Redox-dependent conformational changes are common structural features of cytochrome c from various species Arch. Biochem. Biophys. 346 1997 287 293
53. B. Hammack, K. Attfield, D. Clayton, E. Dec, A. Dong, C. Sarisky, and B.E. Bowler The magnitude of changes in guanidine-HCl unfolding m-values in the protein, iso-1-cytochrome c, depends upon the substructure containing the mutation Protein Sci. 7 1998 1789 1795
54. I. Bartalesi, I. Bertini, K. Ghosh, A. Rosato, and P. Turano The unfolding of oxidized c-type cytochromes: The instructive case of Bacillus pasteurii J. Mol. Biol. 321 2002 693 701
55. A. Quintas, and L.M.A. Oliveira Protein hierarchy levels of structural organization for amyloidogenesis: Biochemical and biophysical aspects underlying misfolding and disease T.F. Outeiro, Protein Misfolding in Biology and Disease 2008 Transworld Research Network 1 34
56. F. Chiti, and C.M. Dobson Amyloid formation by globular proteins under native conditions Nat. Chem. Biol. 5 2009 15 22
57. D. Canet, A.M. Last, P. Tito, M. Sunde, A. Spencer, D.B. Archer, C. Redfield, C.V. Robinson, and C.M. Dobson Local cooperativity in the unfolding of an amyloidogenic variant of human lysozyme Nat. Struct. Biol. 9 2002 308 315
58. L. Banci, I. Bertini, N. D'Amelio, E. Gaggelli, E. Libralesso, I. Matecko, P. Turano, and J.S. Valentine Fully metallated S134N Cu, Zn-superoxide dismutase displays abnormal mobility and intermolecular contacts in solution J. Biol. Chem. 280 2005 35815 35821
59. T.W. Lo, M.E. Westwood, A.C. McLellan, T. Selwood, and P.J. Thornalley Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N alpha-acetylarginine, N alpha-acetylcysteine, and N alpha-acetyllysine, and bovine serum albumin J. Biol. Chem. 269 1994 32299 32305
60. J.W. Baynes, N.G. Watkins, C.I. Fisher, C.J. Hull, J.S. Patrick, M.U. Ahmed, J.A. Dunn, and S.R. Thorpe The Amadori product on protein: Structure and reactions Prog. Clin. Biol. Res. 304 1989 43 67
61. M.B. Johansen, L. Kiemer, and S. Brunak Analysis and prediction of mammalian protein glycation Glycobiology 16 2006 844 853
62. N. Ahmed, D. Dobler, M. Dean, and P.J. Thornalley Peptide mapping identifies hotspot site of modification in human serum albumin by methylglyoxal involved in ligand binding and esterase activity J. Biol. Chem. 280 2005 5724 5732
63. T.E. Creighton Proteins: Structures and Molecular Properties 1993 W. H. Freeman and Company New York