Quantification of quaternary structure stability in aggregation-prone proteins under physiological conditions: The transthyretin case

Biochemistry

Volumn 53, Issue 41, 2014, Pages 6496-6510

  Robinson, Lei Z ^a   Reixach, Natàlia ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTROPHORESIS; PHYSIOLOGY;

AMYLOID DEPOSITION; BINDING ENERGETICS; CLINICAL DEVELOPMENT; HOMOTETRAMERIC PROTEIN TRANSTHYRETIN; KINETIC STABILITY; PHYSIOLOGICAL CONDITION; POLYACRYLAMIDE GEL ELECTROPHORESIS; QUATERNARY STRUCTURE;

PROTEINS;

AMYLOID; GLUTARALDEHYDE; PREALBUMIN; PROTEIN INHIBITOR; RESVERATROL; SOM 0226; UNCLASSIFIED DRUG; BENZOPHENONE DERIVATIVE; BENZOXAZOLE DERIVATIVE; FLUORESCENT DYE; MUTANT PROTEIN; NEW DRUG; NITROPHENOL; NOOTROPIC AGENT; RECOMBINANT PROTEIN; TAFAMIDIS; TOLCAPONE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG BINDING; DRUG POTENCY; HIGH TEMPERATURE; METHODOLOGY; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; PH; PRESSURE; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN UNFOLDING; THERMODYNAMICS; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; FAMILIAL AMYLOIDOSIS; GENETICS; HUMAN; KINETICS; METABOLISM; PROTEINOSIS;

AMINO ACID SUBSTITUTION; AMYLOID; AMYLOIDOSIS, FAMILIAL; BENZOPHENONES; BENZOXAZOLES; BINDING SITES; DRUGS, INVESTIGATIONAL; FLUORESCENT DYES; HUMANS; KINETICS; MODELS, MOLECULAR; MUTANT PROTEINS; NITROPHENOLS; NOOTROPIC AGENTS; PREALBUMIN; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN UNFOLDING; RECOMBINANT PROTEINS; THERMODYNAMICS;

EID: 84908216706     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500739q     Document Type: Article

References (48)

1. Buxbaum, J. N. (2004) The systemic amyloidoses Curr. Opin. Rheumatol. 16, 67-75
2. Buxbaum, J. N. (2008) in Rheumatology (Hochberg, M. C., Silman, A. J., Smolen, J. S., Weinblatt, M. E., and Weisman, M. H., Eds.) pp 1671-1681, Elsevier, London.
3. Buxbaum, J. N. and Reixach, N. (2009) Transthyretin: the servant of many masters Cell. Mol. Life Sci. 66, 3095-3101
4. 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
5. 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
6. 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
7. 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 alpha2-macroglobulin and tau: a population-based autopsy study Ann. Med. 40, 232-239
8. 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
9. 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
10. Adams, D., Theaudin, M., Cauquil, C., Algalarrondo, V., and Slama, M. (2014) FAP neuropathy and emerging treatments Curr. Neurol. Neurosci. Rep. 14, 435
11. Sekijima, Y. (2014) Recent progress in the understanding and treatment of transthyretin amyloidosis J. Clin. Pharm. Ther. 39, 225-233
12. 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
13. 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, 37-38
14. Hammarström, 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, 16427-16432
15. Schneider, F., Hammarstrom, P., and Kelly, J. W. (2001) Transthyretin slowly exchanges subunits under physiological conditions: a convenient chromatographic method to study subunit exchange in oligomeric proteins Protein Sci. 10, 1606-1613
16. Wiseman, R. L., Green, N. S., and Kelly, J. W. (2005) Kinetic stabilization of an oligomeric protein under physiological conditions demonstrated by a lack of subunit exchange: implications for transthyretin amyloidosis Biochemistry 44, 9265-9274
17. 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
18. Centellas, M., Planas, A., Reig, N., Gavalda, N., and Insa, R. (2013) SOM0226: a reprofiled drug intended for the prevention and treatment of familial transthyretin amyloidosis, in Proceedings of the XIIIth International Symposium on Amyloidosis: From Misfolded Proteins to Well-Designed Treatment (Hazenberg, B. P. C. and Bijzet, J., Eds.) pp 451-453, May 6-10, Groningen, The Netherlands.
19. 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
20. 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
21. Zhao, L., Buxbaum, J. N., and Reixach, N. (2013) Age-related oxidative modifications of transthyretin modulate its amyloidogenicity Biochemistry 52, 1913-1926
22. 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
23. Penchala, S. C., Connelly, S., Wang, Y., Park, M. S., Zhao, L., Baranczak, A., Rappley, I., Vogel, H., Liedtke, M., Witteles, R. M., Powers, E. T., Reixach, N., Chan, W. K., Wilson, I. A., Kelly, J. W., Graef, I. A., and Alhamadsheh, M. M. (2013) AG10 inhibits amyloidogenesis and cellular toxicity of the familial amyloid cardiomyopathy-associated V122I transthyretin Proc. Natl. Acad. Sci. U.S.A. 110, 9992-9997
24. 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
25. LeVine, H., III (1999) Quantification of beta-sheet amyloid fibril structures with thioflavin T Methods Enzymol. 309, 274-284
26. 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
27. 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
28. Hurshman Babbes, A. R., Powers, E. T., and Kelly, J. W. (2008) Quantification of the thermodynamically linked quaternary and tertiary structural stabilities of transthyretin and its disease-associated variants: the relationship between stability and amyloidosis Biochemistry 47, 6969-6984
29. 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
30. Tagoe, C., Reixach, N., Friske, L., Mustra, D., French, D., Gallo, G., and Buxbaum, J. N. (2007) In vivo stabilization of mutant human transthyretin in transgenic mice Amyloid 14, 227-236
31. Mizuguchi, M., Yokoyama, T., Nabeshima, Y., Kawano, K., Tanaka, I., and Niimura, N. (2012) Quaternary structure, aggregation and cytotoxicity of transthyretin Amyloid 19, 5-7
32. Rappley, I., Monteiro, C., Novais, M., Baranczak, A., Solis, G., Wiseman, R. L., Helmke, S., Maurer, M. S., Coelho, T., Powers, E. T., and Kelly, J. W. (2014) Quantification of transthyretin kinetic stability in human plasma using subunit exchange Biochemistry 53, 1993-2006
33. Johnson, S. M., Wiseman, R. L., Sekijima, Y., Green, N. S., Adamski-Werner, S. L., and Kelly, J. W. (2005) Native state kinetic stabilization as a strategy to ameliorate protein misfolding diseases: a focus on the transthyretin amyloidoses Acc. Chem. Res. 38, 911-921
34. Colon, W. and Kelly, J. W. (1992) Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro Biochemistry 31, 8654-8660
35. Lai, Z., Colon, W., and Kelly, J. W. (1996) The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid Biochemistry 35, 6470-6482
36. Coelho, T., Carvalho, M., Saraiva, M., Alves, I., Almeida, M. R., and Costa, P. P. (1993) A strikingly benign evolution of FAP in an individual found to be a compound heterozygote for two TTR mutations: TTR MET 30 and TTR MET 119 J. Rheumatol. 20, 179
37. Hammarstrom, P., Schneider, F., and Kelly, J. W. (2001) Trans-suppression of misfolding in an amyloid disease Science 293, 2459-2462
38. Longo, A. I., Hays, M. T., and Saraiva, M. J. (1997) Comparative stability and clearance of [Met30]transthyretin and [Met119]transthyretin Eur. J. Biochem. 249, 662-668
39. Dolado, I., Nieto, J., Saraiva, M. J., Arsequell, G., Valencia, G., and Planas, A. (2005) Kinetic assay for high-throughput screening of in vitro transthyretin amyloid fibrillogenesis inhibitors J. Comb. Chem. 7, 246-252
40. Cardoso, I., Goldsbury, C. S., Muller, S. A., Olivieri, V., Wirtz, S., Damas, A. M., Aebi, U., and Saraiva, M. J. (2002) Transthyretin fibrillogenesis entails the assembly of monomers: a molecular model for in vitro assembled transthyretin amyloid-like fibrils J. Mol. Biol. 317, 683-695
41. Teng, M. H., Yin, J. Y., Vidal, R., Ghiso, J., Kumar, A., Rabenou, R., Shah, A., Jacobson, D. R., Tagoe, C., Gallo, G., and Buxbaum, J. (2001) Amyloid and nonfibrillar deposits in mice transgenic for wild-type human transthyretin: a possible model for senile systemic amyloidosis Lab Invest. 81, 385-396
42. Sousa, M. M., Cardoso, I., Fernandes, R., Guimaraes, A., and Saraiva, M. J. (2001) Deposition of transthyretin in early stages of familial amyloidotic polyneuropathy: evidence for toxicity of nonfibrillar aggregates Am. J. Pathol. 159, 1993-2000
43. 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
44. Alhamadsheh, M. M., Connelly, S., Cho, A., Reixach, N., Powers, E. T., Pan, D. W., Wilson, I. A., Kelly, J. W., and Graef, I. A. (2011) Potent kinetic stabilizers that prevent transthyretin-mediated cardiomyocyte proteotoxicity Sci. Transl. Med. 3, 97ra81
45. Wiseman, R. L., Johnson, S. M., Kelker, M. S., Foss, T., Wilson, I. A., and Kelly, J. W. (2005) Kinetic stabilization of an oligomeric protein by a single ligand binding event J. Am. Chem. Soc. 127, 5540-5551
46. Gavrin, L. K., Denny, R. A., and Saiah, E. (2012) Small molecules that target protein misfolding J. Med. Chem. 55, 10823-10843
47. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J. P., and Deng, H. X. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Nature 362, 59-62
48. Vassall, K. A., Stubbs, H. R., Primmer, H. A., Tong, M. S., Sullivan, S. M., Sobering, R., Srinivasan, S., Briere, L. A., Dunn, S. D., Colon, W., and Meiering, E. M. (2011) Decreased stability and increased formation of soluble aggregates by immature superoxide dismutase do not account for disease severity in ALS Proc. Natl. Acad. Sci. U.S.A. 108, 2210-2215