Kinetic control in protein folding for light chain amyloidosis and the differential effects of somatic mutations

Journal of Molecular Biology

Volumn 426, Issue 2, 2014, Pages 347-361

  Blancas Mejía, Luis M ^a   Tischer, Alexander ^a,b   Thompson, James R ^a   Tai, Jonathan ^c   Wang, Lin ^a   Auton, Matthew ^a,b   Ramirez Alvarado, Marina ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

amyloid fibril formation; kinetic two state model; light chain amyloidosis; protein thermodynamic and kinetic stability; scan rate dependence and hysteresis

Indexed keywords

AMYLOID; IMMUNOGLOBULIN LIGHT CHAIN; MUTANT PROTEIN; PROLINE;

AMYLOIDOSIS; ARTICLE; CELL INCLUSION; CIS TRANS ISOMERISM; CLONING; CONTROLLED STUDY; CRYSTAL STRUCTURE; FIBER; HUMAN; HUMAN TISSUE; HYSTERESIS; IN VITRO STUDY; ISOMERIZATION; LIGHT CHAIN; LIGHT CHAIN AMYLOIDOSIS; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN UNFOLDING; SOMATIC MUTATION; TEMPERATURE DEPENDENCE; THERMODYNAMICS; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY;

AMYLOID FIBRIL FORMATION; CDR; COMPLEMENTARITY-DETERMINING REGION; KINETIC TWO-STATE MODEL; LIGHT CHAIN AMYLOIDOSIS; PROTEIN THERMODYNAMIC AND KINETIC STABILITY; SCAN RATE DEPENDENCE AND HYSTERESIS; THIOFLAVIN T; THT;

AMYLOIDOSIS; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOGLOBULIN LIGHT CHAINS; KINETICS; MUTATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; TEMPERATURE;

EID: 84891836578     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.10.016     Document Type: Article

References (43)

1. S.K. Kumar, M.A. Gertz, M.Q. Lacy, D. Dingli, S.R. Hayman, and F.K. Buadi et al. Recent improvements in survival in primary systemic amyloidosis and the importance of an early mortality risk score Mayo Clin Proc 86 2011 12 18
2. J. Clarke, E. Cota, S.B. Fowler, and S.J. Hamill Folding studies of immunoglobulin-like β-sandwich proteins suggest that they share a common folding pathway Structure 7 1999 1145 1153
3. P. Bork, L. Holm, and C. Sander The immunoglobulin fold: structural classification, sequence patterns and common core J Mol Biol 242 1994 309 320
4. E.M. Baden, E.G. Randles, A.K. Aboagye, J.R. Thompson, and M. Ramirez-Alvarado Structural insights into the role of mutations in amyloidogenesis J Biol Chem 283 2008 30950 30956
5. C.M. Chung, J.D. Chiu, L.H. Connors, O. Gursky, A. Lim, and A.B. Dykstra et al. Thermodynamic stability of a κI immunoglobulin light chain: relevance to multiple myeloma Biophys J 88 2005 4232 4242
6. L. Del Pozo Yauner, E. Ortiz, R. Sanchez, R. Sanchez-Lopez, L. Guereca, and C.L. Murphy et al. Influence of the germline sequence on the thermodynamic stability and fibrillogenicity of human lambda 6 light chains Proteins 72 2008 684 692
7. L.R. Helms, and R. Wetzel Specificity of abnormal assembly in immunoglobulin light chain deposition disease and amyloidosis J Mol Biol 257 1996 77 86
8. M.R. Hurle, L.R. Helms, L. Li, W. Chan, and R. Wetzel A role for destabilizing amino acid replacements in light-chain amyloidosis Proc Natl Acad Sci U S A 91 1994 5446 5450
9. P.W. Stevens, R. Raffen, D.K. Hanson, Y.-L. Deng, M. Berrios-Hammond, and F.A. Westholm et al. Recombinant immunoglobulin variable domains generated from synthetic genes provide a system for in vitro characterization of light-chain amyloid proteins Protein Sci 4 1995 421 432
10. J. Wall, M. Schell, C. Murphy, R. Hrncic, F.J. Stevens, and A. Solomon Thermodynamic instability of human lambda 6 light chains: correlation with fibrillogenicity Biochemistry 38 1999 14101 14108
11. J.S. Wall, V. Gupta, M. Wilkerson, M. Schell, R. Loris, and P. Adams et al. Structural basis of light chain amyloidogenicity: comparison of the thermodynamic properties, fibrillogenic potential and tertiary structural features of four Vlambda6 proteins J Mol Recognit 17 2004 323 331
12. R. Wetzel Domain stability in immunoglobulin light chain deposition disorders Adv Protein Chem 50 1997 183 242
13. Y. Kim, J.S. Wall, J. Meyer, C. Murphy, T.W. Randolph, and M.C. Manning et al. Thermodynamic modulation of light chain amyloid fibril formation J Biol Chem 275 2000 1570 1574
14. R. Raffen, L.J. Dieckman, M. Szpunar, C. Wunschl, P.R. Pokkuluri, and P. Dave et al. Physicochemical consequences of amino acid variations that contribute to fibril formation by immunoglobulin light chains Protein Sci 8 1999 509 517
15. F. Chiti, P. Webster, N. Taddei, A. Clark, M. Stefani, and G. Ramponi et al. Designing conditions for in vitro formation of amyloid protofilaments and fibrils Proc Natl Acad Sci U S A 96 1999 3590 3594
16. Y.S. Kim, S.P. Cape, E. Chi, R. Raffen, P. Wilkins-Stevens, and F.J. Stevens et al. Counteracting effects of renal solutes on amyloid fibril formation by immunoglobulin light chains J Biol Chem 276 2001 1626 1633
17. R. Khurana, J.R. Gillespie, A. Talapatra, L.J. Minert, C. Ionescu-Zanetti, and I. Millett et al. Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates Biochemistry 40 2001 3525 3535
18. P.O. Souillac, V.N. Uversky, I.S. Millett, R. Khurana, S. Doniach, and A.L. Fink Effect of association state and conformational stability on the kinetics of immunoglobulin light chain amyloid fibril formation at physiological pH J Biol Chem 277 2002 12657 12665
19. P.O. Souillac, V.N. Uversky, I.S. Millett, R. Khurana, S. Doniach, and A.L. Fink Elucidation of the molecular mechanism during the early events in immunoglobulin light chain amyloid fibrillation. Evidence for an off-pathway oligomer at acidic pH J Biol Chem 277 2002 12666 12679
20. R.W. McLaughlin, J.K. De Stigter, L.A. Sikkink, E.M. Baden, and M. Ramirez-Alvarado The effects of sodium sulfate, glycosaminoglycans, and Congo red on the structure, stability, and amyloid formation of an immunoglobulin light-chain protein Protein Sci 15 2006 1710 1722
21. L.A. Sikkink, and M. Ramirez-Alvarado Biochemical and aggregation analysis of Bence Jones proteins from different light chain diseases Amyloid 15 2008 29 39
22. L.A. Sikkink, and M. Ramirez-Alvarado Salts enhance both protein stability and amyloid formation of an immunoglobulin light chain Biophys Chem 135 2008 25 31
23. X. Meng, A.L. Fink, and V.N. Uversky The effect of membranes on the in vitro fibrillation of an amyloidogenic light-chain variable-domain SMA J Mol Biol 381 2008 989 999
24. L.M. Blancas-Mejia, L.A. Tellez, L. del Pozo-Yauner, B. Becerril, J.M. Sanchez-Ruiz, and D.A. Fernandez-Velasco Thermodynamic and kinetic characterization of a germ line human λ6 light-chain protein: the relation between unfolding and fibrillogenesis J Mol Biol 386 2009 1153 1166
25. D.J. Martin, and M. Ramirez-Alvarado Comparison of amyloid fibril formation by two closely related immunoglobulin light chain variable domains Amyloid 17 2010 129 136
26. D.J. Martin, and M. Ramirez-Alvarado Glycosaminoglycans promote fibril formation by amyloidogenic immunoglobulin light chains through a transient interaction Biophys Chem 158 2011 81 89
27. A.C. DiCostanzo, J.R. Thompson, F.C. Peterson, B.F. Volkman, and M. Ramirez-Alvarado Tyrosine residues mediate fibril formation in a dynamic light chain dimer interface J Biol Chem 287 2012 27997 28006
28. E.G. Randles, J.R. Thompson, D.J. Martin, and M. Ramirez-Alvarado Structural alterations within native amyloidogenic immunoglobulin light chains J Mol Biol 389 2009 199 210
29. E.M. Baden, B.A. Owen, F.C. Peterson, B.F. Volkman, M. Ramirez-Alvarado, and J.R. Thompson Altered dimer interface decreases stability in an amyloidogenic protein J Biol Chem 283 2008 15853 15860
30. F.C. Peterson, E.M. Baden, B.A. Owen, B.F. Volkman, and M. Ramirez-Alvarado A single mutation promotes amyloidogenicity through a highly promiscuous dimer interface Structure 18 2010 563 570
31. D. Fasshauer, W. Antonin, V. Subramaniam, and R. Jahn SNARE assembly and disassembly exhibit a pronounced hysteresis Nat Struct Biol 9 2002 144 151
32. A. Tischer, M.A. Cruz, and M. Auton The linker between the D3 and A1 domains of vWF suppresses A1-GPIbα catch bonds by site specific binding to the A1 domain Protein Sci 22 2013 1049 1059
33. J.A. Fauerbach, D.A. Yushchenko, S.H. Shahmoradian, W. Chiu, T.M. Jovin, and E.A. Jares-Erijman Supramolecular non-amyloid intermediates in the early stages of α-synuclein aggregation Biophys J 102 2012 1127 1136
34. J.M. Sanchez-Ruiz Protein kinetic stability Biophys Chem 148 2010 1 15
35. J.R. Lepock, K.P. Ritchie, M.C. Kolios, A.M. Rodahl, K.A. Heinz, and J. Kruuv Influence of transition rates and scan rate on kinetic simulations of differential scanning calorimetry profiles of reversible and irreversible protein denaturation Biochemistry 31 1992 12706 12712
36. K. Mizuno, S.P. Boudko, J. Engel, and H.P. Bachinger Kinetic hysteresis in collagen folding Biophys J 98 2010 3004 3014
37. C. Freund, A. Honegger, P. Hunziker, T.A. Holak, and A. Plückthun Folding nuclei of the scFv fragment of an antibody Biochemistry 35 1996 8457 8464
38. M. Jäger, and A. Plückthun The rate-limiting steps for the folding of an antibody scFv fragment FEBS Lett 418 1997 106 110
39. M. Jager, and A. Pluckthun Folding and assembly of an antibody Fv fragment, a heterodimer stabilized by antigen J Mol Biol 285 1999 2005 2019
40. E.R. Simpson, E.M. Herold, and J. Buchner The folding pathway of the antibody V(L) domain J Mol Biol 392 2009 1326 1338
41. M.J. Feige, L.M. Hendershot, and J. Buchner How antibodies fold Trends Biochem Sci 35 2010 189 198
42. M.R. Eftink Use of multiple spectroscopic methods to monitor equilibrium unfolding of proteins Methods Enzymol 259 1995 487 512
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