Kinetic stabilization of the native state by protein engineering: Implications for inhibition of transthyretin amyloidogenesis

Journal of Molecular Biology

Volumn 347, Issue 4, 2005, Pages 841-854

  Foss, Ted R ^a   Kelker, Matthew S ^a   Wiseman, R Luke ^a   Wilson, Ian A ^a   Kelly, Jeffery W ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Amyloid; Kinetic stability; Native state stabilization; Protein engineering; Transthyretin

Indexed keywords

GUANIDINE; MONOMER; PREALBUMIN; PROTEIN SUBUNIT; TETRAMER; THYROXINE; UREA;

AMYLOIDOGENESIS; ARTICLE; BINDING SITE; DENATURATION; DISSOCIATION; KINETICS; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFECT; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN STRUCTURE; THERMODYNAMICS;

EID: 14944368141     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.01.050     Document Type: Article

References (74)

1. J.W. Kelly The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways Curr. Opin. Struct. Biol. 8 1998 101 106
2. C.C. Blake, L.C. Serpell, M. Sunde, O. Sandgren, and E. Lundgren A molecular model of the amyloid fibril Ciba Found. Symp. 199 1996 6 21
3. J.N. Buxbaum The systemic amyloidoses Curr. Opin. Rheumatol. 16 2004 67 75
4. 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. USA 96 1999 3590 3594
5. C.M. Dobson The structural basis of protein folding and its links with human disease Phil. Trans. Roy. Soc. London 356 2001 133 145
6. 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
7. H.A. Lashuel, D. Hartley, B.M. Petre, T. Walz, and P.T. Lansbury Jr Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291
8. K.N. Dahlgren, A.M. Manelli, W.B. Stine Jr, L.K. Baker, G.A. Krafft, and M.J. LaDu Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability J. Biol. Chem. 277 2002 32046 32053
9. Y. Gong, L. Chang, K.L. Viola, P.N. Lacor, M.P. Lambert, and C.E. Finch Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss Proc. Natl Acad. Sci. USA 100 2003 10417 10422
10. H.J. Kim, S.C. Chae, D.K. Lee, B. Chromy, S.C. Lee, and Y.C. Park Selective neuronal degeneration induced by soluble oligomeric amyloid beta protein FASEB J. 17 2003 118 120
11. H.W. Wang, J.F. Pasternak, H. Kuo, H. Ristic, M.P. Lambert, and B. Chromy Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus Brain Res. 924 2002 133 140
12. M. Bucciantini, E. Giannoni, F. Chiti, F. Baroni, L. Formigli, and J. Zurdo Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 416 2002 507 511
13. N. Reixach, S. Deechongkit, X. Jiang, J.W. Kelly, and J.N. Buxbaum Tissue damage in the amyloidoses: transthyretin monomers and nonnative oligomers are the major cytotoxic species in tissue culture Proc. Natl Acad. Sci. USA 101 2004 2817 2822
14. M.M. Sousa, I. Cardoso, R. Fernandes, A. Guimaraes, and M.J. Saraiva Deposition of transthyretin in early stages of familial amyloidotic polyneuropathy: evidence for toxicity of nonfibrillar aggregates Am. J. Pathol. 159 2001 1993 2000
15. F.E. Cohen, and J.W. Kelly Therapeutic approaches to protein-misfolding diseases Nature 426 2003 905 909
16. P. Hammarstrom, F. Schneider, and J.W. Kelly Trans-suppression of misfolding in an amyloid disease Science 293 2001 2459 2462
17. P. Hammarstrom, R.L. Wiseman, E.T. Powers, and J.W. Kelly Prevention of transthyretin amyloid disease by changing protein misfolding energetics Science 299 2003 713 716
18. F. Chiti, N. Taddei, M. Stefani, C.M. Dobson, and G. Ramponi Reduction of the amyloidogenicity of a protein by specific binding of ligands to the native conformation Protein Sci. 10 2001 879 886
19. S.A. Peterson, T. Klabunde, H.A. Lashuel, H. Purkey, J.C. Sacchettini, and J.W. Kelly Inhibiting transthyretin conformational changes that lead to amyloid fibril formation Proc. Natl Acad. Sci. USA 95 1998 12956 12960
20. P. Westermark, K. Sletten, B. Johansson, and G.G. Cornwell III Fibril in senile systemic amyloidosis is derived from normal transthyretin Proc. Natl Acad. Sci. USA 87 1990 2843 2845
21. L.H. Connors, A. Lim, T. Prokaeva, V.A. Roskens, and C.E. Costello Tabulation of human transthyretin (TTR) variants, 2003 Amyloid 10 2003 160 184
22. M.J. Saraiva Transthyretin mutations in health and disease Hum. Mutat. 5 1995 191 196
23. C.C. Blake, I.D. Swan, C. Rerat, J. Berthou, A. Laurent, and B. Rerat An X-ray study of the subunit structure of prealbumin J. Mol. Biol. 61 1971 217 224
24. C.J. Terry, A.M. Damas, P. Oliveira, M.J. Saraiva, I.L. Alves, and P.P. Costa Structure of Met30 variant of transthyretin and its amyloidogenic implications EMBO J. 12 1993 735 741
25. M.P. Sebastiao, M.J. Saraiva, and A.M. Damas The crystal structure of amyloidogenic Leu55→Pro transthyretin variant reveals a possible pathway for transthyretin polymerization into amyloid fibrils J. Biol. Chem. 273 1998 24715 24722
26. A. Hornberg, T. Eneqvist, A. Olofsson, E. Lundgren, and A.E. Sauer-Eriksson A comparative analysis of 23 structures of the amyloidogenic protein transthyretin J. Mol. Biol. 302 2000 649 669
27. X. Jiang, C.S. Smith, H.M. Petrassi, P. Hammarstrom, J.T. White, J.C. Sacchettini, and J.W. Kelly An engineered transthyretin monomer that is nonamyloidogenic, unless it is partially denatured Biochemistry 40 2001 11442 11452
28. M.P. Sebastiao, V. Lamzin, M.J. Saraiva, and A.M. Damas Transthyretin stability as a key factor in amyloidogenesis: X-ray analysis at atomic resolution J. Mol. Biol. 306 2001 733 744
29. A. Hornberg, A. Olofsson, T. Eneqvist, E. Lundgren, and A.E. Sauer-Eriksson The beta-strand D of transthyretin trapped in two discrete conformations Biochim. Biophys. Acta 1700 2004 93 104
30. G.J. Miroy, Z. Lai, H.A. Lashuel, S.A. Peterson, C. Strang, and J.W. Kelly Inhibiting transthyretin amyloid fibril formation via protein stabilization Proc. Natl Acad. Sci. USA 93 1996 15051 15056
31. H. Razavi, S.K. Palaninathan, E.T. Powers, R.L. Wiseman, H.E. Purkey, and N.N. Mohamedmohaideen Benzoxazoles as transthyretin amyloid fibril inhibitors: synthesis, evaluation, and mechanism of action Angew. Chem. Int. Ed. Engl. 42 2003 2758 2761
32. H.M. Petrassi, T. Klabunde, J. Sacchettini, and J.W. Kelly Structure-based design of N-phenyl phenoxazine transthyretin amyloid fibril inhibitors J. Am. Chem. Soc. 122 2000 2178 2192
33. V.B. Oza, C. Smith, P. Raman, E.K. Koepf, H.A. Lashuel, and H.M. Petrassi Synthesis, structure, and activity of diclofenac analogues as transthyretin amyloid fibril formation inhibitors J. Med. Chem. 45 2002 321 332
34. N.S. Green, S.K. Palaninathan, J.C. Sacchettini, and J.W. Kelly Synthesis and characterization of potent bivalent amyloidosis inhibitors that bind prior to transthyretin tetramerization J. Am. Chem. Soc. 125 2003 13404 13414
35. S.L. Adamski-Werner, S.K. Palaninathan, J.C. Sacchettini, and J.W. Kelly Diflunisal analogues stabilize the native state of transthyretin. Potent inhibition of amyloidogenesis J. Med. Chem. 47 2004 355 374
36. W. Colon, and J.W. Kelly Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro Biochemistry 31 1992 8654 8660
37. A.R. Hurshman, J.T. White, E.T. Powers, and J.W. Kelly Transthyretin aggregation under partially denaturing conditions is a downhill polymerization Biochemistry 43 2004 7365 7381
38. P. Hammarstrom, X. Jiang, A.R. Hurshman, E.T. Powers, and J.W. Kelly Sequence-dependent denaturation energetics: a major determinant in amyloid disease diversity Proc. Natl Acad. Sci. USA 99 2002 16427 16432
39. K. Liu, H.S. Cho, H.A. Lashuel, J.W. Kelly, and D.E. Wemmer A glimpse of a possible amyloidogenic intermediate of transthyretin Nature Struct. Biol. 7 2000 754 757
40. H.A. Lashuel, C. Wurth, L. Woo, and J.W. Kelly The most pathogenic transthyretin variant, L55P, forms amyloid fibrils under acidic conditions and protofilaments under physiological conditions Biochemistry 38 1999 13560 13573
41. H.A. Lashuel, Z. Lai, and J.W. Kelly Characterization of the transthyretin acid denaturation pathways by analytical ultracentrifugation: implications for wild-type, V30M, and L55P amyloid fibril formation Biochemistry 37 1998 17851 17864
42. Z. Lai, J. McCulloch, H.A. Lashuel, and J.W. Kelly Guanidine hydrochloride-induced denaturation and refolding of transthyretin exhibits a marked hysteresis: equilibria with high kinetic barriers Biochemistry 36 1997 10230 10239
43. J.W. Kelly, W. Colon, Z. Lai, H.A. Lashuel, J. McCulloch, and S.L. McCutchen Transthyretin quaternary and tertiary structural changes facilitate misassembly into amyloid Advan. Protein Chem. 50 1997 161 181
44. Z. Lai, W. Colon, and J.W. Kelly The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid Biochemistry 35 1996 6470 6482
45. S.L. McCutchen, Z. Lai, G.J. Miroy, J.W. Kelly, and W. Colon Comparison of lethal and nonlethal transthyretin variants and their relationship to amyloid disease Biochemistry 34 1995 13527 13536
46. S.L. McCutchen, W. Colon, and J.W. Kelly Transthyretin mutation Leu-55-Pro significantly alters tetramer stability and increases amyloidogenicity Biochemistry 32 1993 12119 12127
47. P. Hammarstrom, Y. Sekijima, J.T. White, R.L. Wiseman, A. Lim, and C.E. Costello D18G transthyretin is monomeric, aggregation prone, and not detectable in plasma and cerebrospinal fluid: a prescription for central nervous system amyloidosis? Biochemistry 42 2003 6656 6663
48. A. Quintas, M.J. Saraiva, and R.M. Brito The amyloidogenic potential of transthyretin variants correlates with their tendency to aggregate in solution FEBS Letters 418 1997 297 300
49. A. Quintas, M.J. Saraiva, and R.M. Brito The tetrameric protein transthyretin dissociates to a non-native monomer in solution. A novel model for amyloidogenesis J. Biol. Chem. 274 1999 32943 32949
50. Y. Sekijima, P. Hammarstrom, M. Matsumura, Y. Shimizu, M. Iwata, and T. Tokuda Energetic characteristics of the new transthyretin variant A25T may explain its a typical central nervous system pathology Lab. Invest. 83 2003 409 417
51. P. Hammarstrom, X. Jiang, S. Deechongkit, and J.W. Kelly Anion shielding of electrostatic repulsions in transthyretin modulates stability and amyloidosis: insight into the chaotrope unfolding dichotomy Biochemistry 40 2001 11453 11459
52. T. Coelho, M. Carvalho, M.J. Saraiva, I.L. Alves, M.R. Almeida, and P.P. Costa A strinkingly benign evolution of FAP in an individual compound heterzygote for two TTR mutations: TTR Met30 and TTR Met119 J. Rheumatol. 20 1993 179
53. T. Coelho, R. Chorao, A. Sousa, I.L. Alves, M.F. Torres, and M.J. Saraiva Compound heterozygotes of transthretin Met30 and transthyretin Met119 are protected from the devastating effects of Familial Amyloid Polyneuropathy Neuromuscul. Disord. 6 1996 27 32
54. M. Manning, and W. Colon Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward beta-sheet structure Biochemistry 43 2004 11248 11254
55. E. Subbian, Y. Yabuta, and U. Shinde Positive selection dictates the choice between kinetic and thermodynamic protein folding and stability in subtilases Biochemistry 43 2004 14348 14360
56. E.L. Cunningham, S.S. Jaswal, J.L. Sohl, and D.A. Agard Kinetic stability as a mechanism for protease longevity Proc. Natl Acad. Sci. USA 96 1999 11008 11014
57. S.S. Jaswal, J.L. Sohl, J.H. Davis, and D.A. Agard Energetic landscape of alpha-lytic protease optimizes longevity through kinetic stability Nature 415 2002 343 346
58. S.M. Truhlar, E.L. Cunningham, and D.A. Agard The folding landscape of Streptomyces griseus protease B reveals the energetic costs and benefits associated with evolving kinetic stability Protein Sci. 13 2004 381 390
59. P. Forrer, C. Chang, D. Ott, A. Wlodawer, and A. Pluckthun Kinetic stability and crystal structure of the viral capsid protein SHP J. Mol. Biol. 344 2004 179 193
60. C.R. Robinson, and R.T. Sauer Equilibrium stability and sub-millisecond refolding of a designed single-chain Arc repressor Biochemistry 35 1996 13878 13884
61. C.R. Robinson, and R.T. Sauer Covalent attachment of Arc repressor subunits by a peptide linker enhances affinity for operator DNA Biochemistry 35 1996 109 116
62. C.R. Robinson, and R.T. Sauer Optimizing the stability of single-chain proteins by linker length and composition mutagenesis Proc. Natl Acad. Sci. USA 95 1998 5929 5934
63. G.W. Farr, K. Furtak, M.B. Rowland, N.A. Ranson, H.R. Saibil, T. Kirchhausen, and A.L. Horwich Multivalent binding of nonnative substrate proteins by the chaperonin GroEL Cell 100 2000 561 573
64. F. Schneider, P. Hammarstrom, and J.W. Kelly Transthyretin slowly exchanges subunits under physiological conditions: a convenient chromatographic method to study subunit exchange in oligomeric proteins Protein Sci. 10 2001 1606 1613
65. Wiseman, R. L. J., S. L., Kelker, M. S., Foss, T. R., Wilson, I. A. & Kelly, J. W. (2005). Kinetic stabilization of an oligomeric protein by a single ligand binding event. J. Am. Chem. Soc. In the press.
66. J.S. Philo A method for directly fitting the time derivative of sedimentation velocity data and an alternative algorithm for calculating sedimentation coefficient distribution functions Anal. Biochem. 279 2000 151 163
67. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78 2000 1606 1619
68. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
69. T. Klabunde, H.M. Petrassi, V.B. Oza, P. Raman, J.W. Kelly, and J.C. Sacchettini Rational design of potent human transthyretin amyloid disease inhibitors Nature Struct. Biol. 7 2000 312 321
70. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
71. T.A. Jones, J.Y. Zou, S.W. Cowan, and M. Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallog. sect. A 47 1991 110 119
72. M.D. Winn, M.N. Isupov, and G.N. Murshudov Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallog. sect. D 57 2001 122 133
73. R.A. Laskowski, D.S. Moss, and J.M. Thornton Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231 1993 1049 1067
74. A. Fersht Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding vol. 1 1999 W.H. Freeman and Company New York