Age-related oxidative modifications of transthyretin modulate its amyloidogenicity

Biochemistry

Volumn 52, Issue 11, 2013, Pages 1913-1926

  Zhao, Lei ^a   Buxbaum, Joel N ^a   Reixach, Natàlia ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID FIBRIL FORMATION; AMYLOIDOGENICITY; HOMOTETRAMERIC PROTEIN TRANSTHYRETIN; OXIDATIVE MODIFICATION; PERIPHERAL NERVES; PROTEIN MISFOLDING; PROTEIN OXIDATION; SMALL MOLECULES;

AMINO ACIDS; CELL CULTURE; DEPOSITION; OLIGOMERS; OXIDATION; PROTEINS; TISSUE;

AGGREGATES;

AMYLOID; PREALBUMIN; RESVERATROL;

AGE; ALKYLATION; ARTICLE; CARBONYLATION; CELL VIABILITY; CYTOTOXICITY; DENATURATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; OXIDATION; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONTENT; PROTEIN MODIFICATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RENATURATION; RISK FACTOR; SITE DIRECTED MUTAGENESIS; TURBIDITY;

AGE FACTORS; AGING; AMYLOID; AMYLOIDOSIS; CELL LINE; HUMANS; MYOCYTES, CARDIAC; OXIDATION-REDUCTION; POINT MUTATION; PREALBUMIN; PROTEIN CARBONYLATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STILBENES; THIAZOLES;

EID: 84875426278     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301313b     Document Type: Article

References (59)

1. Buxbaum, J. N. (2004) The systemic amyloidoses Curr. Opin. Rheumatol. 16, 67-75
2. Sipe, J. D., Benson, M. D., Buxbaum, J. N., Ikeda, S., Merlini, G., Saraiva, M. J., and Westermark, P. (2010) Amyloid fibril protein nomenclature: 2010 recommendations from the nomenclature committee of the International Society of Amyloidosis Amyloid 17, 101-104
3. Li, X., Masliah, E., Reixach, N., and Buxbaum, J. N. (2011) Neuronal production of transthyretin in human and murine Alzheimer's disease: Is it protective? J. Neurosci. 31, 12483-12490
4. Buxbaum, J. N. and Reixach, N. (2009) Transthyretin: The servant of many masters Cell. Mol. Life Sci. 66, 3095-3101
5. Cornwell, G. G., III, Murdoch, W. L., Kyle, R. A., Westermark, P., and Pitkanen, P. (1983) Frequency and distribution of senile cardiovascular amyloid. A clinicopathologic correlation Am. J. Med. 75, 618-623
6. Tanskanen, M., Peuralinna, T., Polvikoski, T., Notkola, I. L., Sulkava, R., Hardy, J., Singleton, A., Kiuru-Enari, S., Paetau, A., Tienari, P. J., and Myllykangas, L. (2008) Senile systemic amyloidosis affects 25% of the very aged and associates with genetic variation in α2-macroglobulin and tau: A population-based autopsy study Ann. Med. 40, 232-239
7. Jacobson, D. R., Pastore, R., Pool, S., Malendowicz, S., Kane, I., Shivji, A., Embury, S. H., Ballas, S. K., and Buxbaum, J. N. (1996) Revised transthyretin Ile 122 allele frequency in African-Americans Hum. Genet. 98, 236-238
8. Buxbaum, J., Jacobson, D. R., Tagoe, C., Alexander, A., Kitzman, D. W., Greenberg, B., Thaneemit-Chen, S., and Lavori, P. (2006) Transthyretin V122I in African Americans with congestive heart failure J. Am. Coll. Cardiol. 47, 1724-1725
9. Jacobson, D. R., Pastore, R. D., Yaghoubian, R., Kane, I., Gallo, G., Buck, F. S., and Buxbaum, J. N. (1997) Variant-sequence transthyretin (isoleucine 122) in late-onset cardiac amyloidosis in black Americans N. Engl. J. Med. 336, 466-473
10. Kelly, J. W. (1998) The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways Curr. Opin. Struct. Biol. 8, 101-106
11. Hurshman, A. R., White, J. T., Powers, E. T., and Kelly, J. W. (2004) Transthyretin aggregation under partially denaturing conditions is a downhill polymerization Biochemistry 43, 7365-7381
12. Hammarstrom, P., Jiang, X., Hurshman, A. R., Powers, E. T., and Kelly, J. W. (2002) Sequence-dependent denaturation energetics: A major determinant in amyloid disease diversity Proc. Natl. Acad. Sci. U.S.A. 99 (Suppl. 4) 16427-16432
13. Sekijima, Y., Wiseman, R. L., Matteson, J., Hammarstrom, P., Miller, S. R., Sawkar, A. R., Balch, W. E., and Kelly, J. W. (2005) The biological and chemical basis for tissue-selective amyloid disease Cell 121, 73-85
14. Stadtman, E. R. (2006) Protein oxidation and aging Free Radical Res. 40, 1250-1258
15. Stadtman, E. R. and Levine, R. L. (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins Amino Acids 25, 207-218
16. Fedorova, M., Kuleva, N., and Hoffmann, R. (2010) Identification of cysteine, methionine and tryptophan residues of actin oxidized in vivo during oxidative stress J. Proteome Res. 9, 1598-1609
17. Poole, L. B. (2004) Formation and functions of protein sulfenic acids. Current Protocols in Toxicology, Chapter 17, Unit 17, Wiley, New York.
18. Hoshi, T. and Heinemann, S. (2001) Regulation of cell function by methionine oxidation and reduction J. Physiol. 531, 1-11
19. Shacter, E. (2000) Quantification and significance of protein oxidation in biological samples Drug Metab. Rev. 32, 307-326
20. Amici, A., Levine, R. L., Tsai, L., and Stadtman, E. R. (1989) Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions J. Biol. Chem. 264, 3341-3346
21. Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A., and Colombo, R. (2003) Protein carbonyl groups as biomarkers of oxidative stress Clin. Chim. Acta 329, 23-38
22. Levine, R. L. (2002) Carbonyl modified proteins in cellular regulation, aging, and disease Free Radical Biol. Med. 32, 790-796
23. Conrad, C. C., Marshall, P. L., Talent, J. M., Malakowsky, C. A., Choi, J., and Gracy, R. W. (2000) Oxidized proteins in Alzheimer's plasma Biochem. Biophys. Res. Commun. 275, 678-681
24. Choi, J., Malakowsky, C. A., Talent, J. M., Conrad, C. C., and Gracy, R. W. (2002) Identification of oxidized plasma proteins in Alzheimer's disease Biochem. Biophys. Res. Commun. 293, 1566-1570
25. Floor, E. and Wetzel, M. G. (1998) Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay J. Neurochem. 70, 268-275
26. Madian, A. G. and Regnier, F. E. (2010) Profiling carbonylated proteins in human plasma J. Proteome Res. 9, 1330-1343
27. Guidi, F., Magherini, F., Gamberi, T., Bini, L., Puglia, M., Marzocchini, R., Ranaldi, F., Modesti, P. A., Gulisano, M., and Modesti, A. (2011) Plasma protein carbonylation and physical exercise Mol. BioSyst. 7, 640-650
28. D'Aguanno, S., Franciotta, D., Lupisella, S., Barassi, A., Pieragostino, D., Lugaresi, A., Centonze, D., D'Eril, G. M., Bernardini, S., Federici, G., and Urbani, A. (2010) Protein profiling of Guillain-Barre syndrome cerebrospinal fluid by two-dimensional electrophoresis and mass spectrometry Neurosci. Lett. 485, 49-54
29. Ando, Y., Nyhlin, N., Suhr, O., Holmgren, G., Uchida, K., el Sahly, M., Yamashita, T., Terasaki, H., Nakamura, M., Uchino, M., and Ando, M. (1997) Oxidative stress is found in amyloid deposits in systemic amyloidosis Biochem. Biophys. Res. Commun. 232, 497-502
30. Maleknia, S. D., Reixach, N., and Buxbaum, J. N. (2006) Oxidation inhibits amyloid fibril formation of transthyretin FEBS J. 273, 5400-5406
31. Sousa, M. M., Fernandes, R., Palha, J. A., Taboada, A., Vieira, P., and Saraiva, M. J. (2002) Evidence for early cytotoxic aggregates in transgenic mice for human transthyretin Leu55Pro Am. J. Pathol. 161, 1935-1948
32. Bourgault, S., Choi, S., Buxbaum, J. N., Kelly, J. W., Price, J. L., and Reixach, N. (2011) Mechanisms of transthyretin cardiomyocyte toxicity inhibition by resveratrol analogs Biochem. Biophys. Res. Commun. 410, 707-713
33. Reixach, N., Deechongkit, S., Jiang, X., Kelly, J. W., and Buxbaum, J. N. (2004) Tissue damage in the amyloidoses: Transthyretin monomers and nonnative oligomers are the major cytotoxic species in tissue culture Proc. Natl. Acad. Sci. U.S.A. 101, 2817-2822
34. Kingsbury, J. S., Klimtchuk, E. S., Theberge, R., Costello, C. E., and Connors, L. H. (2007) Expression, purification, and in vitro cysteine-10 modification of native sequence recombinant human transthyretin Protein Expression Purif. 53, 370-377
35. Noble, R. W. and Gibson, Q. H. (1970) The reaction of ferrous horseradish peroxidase with hydrogen peroxide J. Biol. Chem. 245, 2409-2413
36. Maisonneuve, E., Ducret, A., Khoueiry, P., Lignon, S., Longhi, S., Talla, E., and Dukan, S. (2009) Rules governing selective protein carbonylation PLoS One 4, e7269
37. Reixach, N., Foss, T. R., Santelli, E., Pascual, J., Kelly, J. W., and Buxbaum, J. N. (2007) Human-murine transthyretin heterotetramers are kinetically stable and non-amyloidogenic: A lesson in the generation of transgenic models of diseases involving oligomeric proteins J. Biol. Chem. 283, 2098-2107
38. Davidson, M. M., Nesti, C., Palenzuela, L., Walker, W. F., Hernandez, E., Protas, L., Hirano, M., and Isaac, N. D. (2005) Novel cell lines derived from adult human ventricular cardiomyocytes J. Mol. Cell. Cardiol. 39, 133-147
39. Stadtman, E. R., Van, R. H., Richardson, A., Wehr, N. B., and Levine, R. L. (2005) Methionine oxidation and aging Biochim. Biophys. Acta 1703, 135-140
40. Lai, Z., McCulloch, J., Lashuel, H. A., and Kelly, J. W. (1997) Guanidine hydrochloride-induced denaturation and refolding of transthyretin exhibits a marked hysteresis: Equilibria with high kinetic barriers Biochemistry 36, 10230-10239
41. Colon, W. and Kelly, J. W. (1992) Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro Biochemistry 31, 8654-8660
42. Jiang, X., Buxbaum, J. N., and Kelly, J. W. (2001) The V122I cardiomyopathy variant of transthyretin increases the velocity of rate-limiting tetramer dissociation, resulting in accelerated amyloidosis Proc. Natl. Acad. Sci. U.S.A. 98, 14943-14948
43. LeVine, H., III (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T Methods Enzymol. 309, 274-284
44. Jiang, X., Smith, C. S., Petrassi, H. M., Hammarstrom, P., White, J. T., Sacchettini, J. C., and Kelly, J. W. (2001) An engineered transthyretin monomer that is nonamyloidogenic, unless it is partially denatured Biochemistry 40, 11442-11452
45. Klabunde, T., Petrassi, H. M., Oza, V. B., Raman, P., Kelly, J. W., and Sacchettini, J. C. (2000) Rational design of potent human transthyretin amyloid disease inhibitors Nat. Struct. Biol. 7, 312-321
46. Hammarstrom, P., Jiang, X., Deechongkit, S., and Kelly, J. W. (2001) Anion shielding of electrostatic repulsions in transthyretin modulates stability and amyloidosis: Insight into the chaotrope unfolding dichotomy Biochemistry 40, 11453-11459
47. Bennion, B. J. and Daggett, V. (2003) The molecular basis for the chemical denaturation of proteins by urea Proc. Natl. Acad. Sci. U.S.A. 100, 5142-5147
48. Lundberg, E., Olofsson, A., Westermark, G. T., and Sauer-Eriksson, A. E. (2009) Stability and fibril formation properties of human and fish transthyretin, and of the Escherichia coli transthyretin-related protein FEBS J. 276, 1999-2011
49. Lindgren, M., Sorgjerd, K., and Hammarstrom, P. (2005) Detection and characterization of aggregates, prefibrillar amyloidogenic oligomers, and protofibrils using fluorescence spectroscopy Biophys. J. 88, 4200-4212
50. Miller, S. R., Sekijima, Y., and Kelly, J. W. (2004) Native state stabilization by NSAIDs inhibits transthyretin amyloidogenesis from the most common familial disease variants Lab. Invest. 84, 545-552
51. Zhang, Q. and Kelly, J. W. (2003) Cys10 mixed disulfides make transthyretin more amyloidogenic under mildly acidic conditions Biochemistry 42, 8756-8761
52. Hou, L., Kang, I., Marchant, R. E., and Zagorski, M. G. (2002) Methionine 35 oxidation reduces fibril assembly of the amyloid Aβ-(1-42) peptide of Alzheimer's disease J. Biol. Chem. 277, 40173-40176
53. Breydo, L., Bocharova, O. V., Makarava, N., Salnikov, V. V., Anderson, M., and Baskakov, I. V. (2005) Methionine oxidation interferes with conversion of the prion protein into the fibrillar proteinase K-resistant conformation Biochemistry 44, 15534-15543
54. Uversky, V. N., Yamin, G., Souillac, P. O., Goers, J., Glaser, C. B., and Fink, A. L. (2002) Methionine oxidation inhibits fibrillation of human α-synuclein in vitro FEBS Lett. 517, 239-244
55. Binger, K. J., Griffin, M. D., and Howlett, G. J. (2008) Methionine oxidation inhibits assembly and promotes disassembly of apolipoprotein C-II amyloid fibrils Biochemistry 47, 10208-10217
56. Herlenius, G., Wilczek, H. E., Larsson, M., and Ericzon, B. G. (2004) Ten years of international experience with liver transplantation for familial amyloidotic polyneuropathy: Results from the Familial Amyloidotic Polyneuropathy World Transplant Registry Transplantation 77, 64-71
57. Coelho, T., Maia, L. F., Martins da, S. A., Waddington, C. M., Plante-Bordeneuve, V., Lozeron, P., Suhr, O. B., Campistol, J. M., Conceicao, I. M., Schmidt, H. H., Trigo, P., Kelly, J. W., Labaudiniere, R., Chan, J., Packman, J., Wilson, A., and Grogan, D. R. (2012) Tafamidis for transthyretin familial amyloid polyneuropathy: A randomized, controlled trial Neurology 79, 785-792
58. Bulawa, C. E., Connelly, S., Devit, M., Wang, L., Weigel, C., Fleming, J. A., Packman, J., Powers, E. T., Wiseman, R. L., Foss, T. R., Wilson, I. A., Kelly, J. W., and Labaudiniere, R. (2012) Tafamidis, a potent and selective transthyretin kinetic stabilizer that inhibits the amyloid cascade Proc. Natl. Acad. Sci. U.S.A. 109, 9629-9634
59. Berk, J. L., Suhr, O. B., Sekijima, Y., Yamashita, T., Heneghan, M., Zeldenrust, S. R., Ando, Y., Ikeda, S., Gorevic, P., Merlini, G., Kelly, J. W., Skinner, M., Bisbee, A. B., Dyck, P. J., and Obici, L. (2012) The Diflunisal Trial: Study accrual and drug tolerance Amyloid 19 (Suppl. 1) 37-38