Residual Structures in the Acid-Unfolded States of Vλ6 Proteins Affect Amyloid Fibrillation

Journal of Molecular Biology

Volumn 392, Issue 4, 2009, Pages 1033-1043

  Mishima, Tomonori ^a   Ohkuri, Takatoshi ^a   Monji, Akira ^b   Kanemaru, Takaaki ^c   Abe, Yoshito ^a   Ueda, Tadashi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY HOSPITAL   (Japan)

Author keywords

amyloid fibril; disulfide bond; hydrophobic interaction; NMR relaxation; residual structure

Indexed keywords

ACID PROTEIN; AMYLOID; AMYLOID PROTEIN; IMMUNOGLOBULIN LIGHT CHAIN; JTO PROTEIN; LAMBDA 6 VARIABLE DOMAIN PROTEIN; UNCLASSIFIED DRUG; WIL PROTEIN;

AMINO ACID SEQUENCE; AMYLOIDOSIS; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; HYDROPHOBICITY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; WILD TYPE;

EID: 69749122031     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.07.078     Document Type: Article

References (68)

1. Uversky V.N. A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders. J. Biomol. Struct. Dyn. 21 (2003) 211-234
2. Chakraborty C., Nandi S., and Jana S. Prion disease: a deadly disease for protein misfolding. Curr. Pharm. Biotechnol. 6 (2005) 167-177
3. Veerhuis R., Boshuizen R.S., and Familian A. Amyloid associated proteins in Alzheimer's and prion disease. Curr. Drug Targets CNS Neurol. Disord. 4 (2005) 235-248
4. Sunde M., Serpell L.C., Bartlam M., Fraser P.E., Pepys M.B., and Blake C.C. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273 (1997) 729-739
5. Guijarro J.I., Sunde M., Jones J.A., Campbell I.D., and Dobson C.M. Amyloid fibril formation by an SH3 domain. Proc. Natl Acad. Sci. USA 95 (1998) 4224-4228
6. Konno T., Murata K., and Nagayama K. Amyloid-like aggregates of a plant protein: a case of a sweet-tasting protein, monellin. FEBS Lett. 454 (1999) 122-126
7. Damaschun G., Damaschun H., Fabian H., Gast K., Krober R., Wieske M., and Zirwer D. Conversion of yeast phosphoglycerate kinase into amyloid-like structure. Proteins 39 (2000) 204-211
8. Pertinhez T.A., Bouchard M., Tomlinson E.J., Wain R., Ferguson S.J., Dobson C.M., and Smith L.J. Amyloid fibril formation by a helical cytochrome. FEBS Lett. 495 (2001) 184-186
9. Fandrich M., Fletcher M.A., and Dobson C.M. Amyloid fibrils from muscle myoglobin. Nature 410 (2001) 165-166
10. Pavlov N.A., Cherny D.I., Heim G., Jovin T.M., and Subramaniam V. Amyloid fibrils from the mammalian protein prothymosin alpha. FEBS Lett. 517 (2002) 37-40
11. Dobson C.M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 24 (1999) 329-332
12. Uversky V.N., and Fink A.L. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim. Biophys. Acta 1698 (2004) 131-153
13. Kelly J.W. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8 (1998) 101-106
14. Ross C.A., and Poirier M.A. Protein aggregation and neurodegenerative disease. Nat. Med. 10 (2004) S10-S17
15. Teplow D.B. Structural and kinetic features of amyloid beta-protein fibrillogenesis. Amyloid 5 (1998) 121-142
16. Lopez De La Paz M., Goldie K., Zurdo J., Lacroix E., Dobson C.M., Hoenger A., and Serrano L. De novo designed peptide-based amyloid fibrils. Proc. Natl Acad. Sci. USA 99 (2002) 16052-16057
17. Tjernberg L., Hosia W., Bark N., Thyberg J., and Johansson J. Charge attraction and beta propensity are necessary for amyloid fibril formation from tetrapeptides. J. Biol. Chem. 277 (2002) 43243-43246
18. de Groot N.S., Parella T., Aviles F.X., Vendrell J., and Ventura S. Ile-phe dipeptide self-assembly: clues to amyloid formation. Biophys. J. 92 (2007) 1732-1741
19. Schwalbe H., Fiebig K.M., Buck M., Jones J.A., Grimshaw S.B., Spencer A., et al. Structural and dynamical properties of a denatured protein. Heteronuclear 3D NMR experiments and theoretical simulations of lysozyme in 8 M urea. Biochemistry 36 (1997) 8977-8991
20. Schwarzinger S., Wright P.E., and Dyson H.J. Molecular hinges in protein folding: the urea-denatured state of apomyoglobin. Biochemistry 41 (2002) 12681-12686
21. Platt G.W., McParland V.J., Kalverda A.P., Homans S.W., and Radford S.E. Dynamics in the unfolded state of beta2-microglobulin studied by NMR. J. Mol. Biol. 346 (2005) 279-294
22. Lietzow M.A., Jamin M., Jane Dyson H.J., and Wright P.E. Mapping long-range contacts in a highly unfolded protein. J. Mol. Biol. 322 (2002) 655-662
23. Shortle D., and Ackerman M.S. Persistence of native-like topology in a denatured protein in 8 M urea. Science 293 (2001) 487-489
24. Mohana-Borges R., Goto N.K., Kroon G.J., Dyson H.J., and Wright P.E. Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings. J. Mol. Biol. 340 (2004) 1131-1142
25. Klein-Seetharaman J., Oikawa M., Grimshaw S.B., Wirmer J., Duchardt E., Ueda T., et al. Long-range interactions within a nonnative protein. Science 295 (2002) 1719-1722
26. Wirmer J., Schlorb C., Klein-Seetharaman J., Hirano R., Ueda T., Imoto T., and Schwalbe H. Modulation of compactness and long-range interactions of unfolded lysozyme by single point mutations. Angew. Chem., Int. Ed. Engl. 43 (2004) 5780-5785
27. Ohkuri T., Shioi S., Imoto T., and Ueda T. Effect of the structure of the denatured state of lysozyme on the aggregation reaction at the early stages of folding from the reduced form. J. Mol. Biol. 347 (2005) 159-168
28. Mishima T., Ohkuri T., Monji A., Imoto T., and Ueda T. Amyloid formation in denatured single-mutant lysozymes where residual structures are modulated. Protein Sci. 15 (2006) 2448-2452
29. Bertoncini C.W., Jung Y.S., Fernandez C.O., Hoyer W., Griesinger C., Jovin T.M., and Zweckstetter M. Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein. Proc. Natl Acad. Sci. USA 102 (2005) 1430-1435
30. Sipe J.D. Amyloidosis. Annu. Rev. Biochem. 61 (1992) 947-975
31. Bellotti V., Mangione P., and Merlini G. Review: immunoglobulin light chain amyloidosis-the archetype of structural and pathogenic variability. J. Struct. Biol. 130 (2000) 280-289
32. Solomon A., Frangione B., and Franklin E.C. Bence Jones proteins and light chains of immunoglobulins. Preferential association of the V lambda VI subgroup of human light chains with amyloidosis AL (lambda). J. Clin. Invest. 70 (1982) 453-460
33. Pokkuluri P.R., Solomon A., Weiss D.T., Stevens F.J., and Schiffer M. Tertiary structure of human lambda 6 light chains. Amyloid 6 (1999) 165-171
34. Wall J., Schell M., Murphy C., Hrncic R., Stevens F.J., and Solomon A. Thermodynamic instability of human lambda 6 light chains: correlation with fibrillogenicity. Biochemistry 38 (1999) 14101-14108
35. Wall J.S., Gupta V., Wilkerson M., Schell M., Loris R., Adams P., 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
36. del Pozo Yauner L., Ortiz E., Sanchez R., Sanchez-Lopez R., Guereca L., Murphy C.L., et al. Influence of the germline sequence on the thermodynamic stability and fibrillogenicity of human lambda 6 light chains. Proteins 72 (2008) 684-692
37. Ahn H.C., Le Y.T., Nagchowdhuri P.S., Derose E.F., Putnam-Evans C., London R.E., et al. NMR characterizations of an amyloidogenic conformational ensemble of the PI3K SH3 domain. Protein Sci. 15 (2006) 2552-2557
38. Cao A., Hu D., and Lai L. Formation of amyloid fibrils from fully reduced hen egg white lysozyme. Protein Sci. 13 (2004) 319-324
39. Katou H., Kanno T., Hoshino M., Hagihara Y., Tanaka H., Kawai T., et al. The role of disulfide bond in the amyloidogenic state of beta(2)-microglobulin studied by heteronuclear NMR. Protein Sci. 11 (2002) 2218-2229
40. Dyson H.J., and Wright P.E. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 104 (2004) 3607-3622
41. LeVine III H. Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci. 2 (1993) 404-410
42. Pedersen J.S., Dikov D., Flink J.L., Hjuler H.A., Christiansen G., and Otzen D.E. The changing face of glucagon fibrillation: structural polymorphism and conformational imprinting. J. Mol. Biol. 355 (2006) 501-523
43. Pedersen J.S., and Otzen D.E. Amyloid-a state in many guises: survival of the fittest fibril fold. Protein Sci. 17 (2008) 2-10
44. Kelly J.W., Colon W., Lai Z., Lashuel H.A., McCulloch J., McCutchen S.L., et al. Transthyretin quaternary and tertiary structural changes facilitate misassembly into amyloid. Adv. Protein Chem. 50 (1997) 161-181
45. Booth D.R., Sunde M., Bellotti V., Robinson C.V., Hutchinson W.L., Fraser P.E., et al. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385 (1997) 787-793
46. Ramirez-Alvarado M., Merkel J.S., and Regan L. A systematic exploration of the influence of the protein stability on amyloid fibril formation in vitro. Proc. Natl Acad. Sci. USA 97 (2000) 8979-8984
47. McParland V.J., Kalverda A.P., Homans S.W., and Radford S.E. Structural properties of an amyloid precursor of beta(2)-microglobulin. Nat. Struct. Biol. 9 (2002) 326-331
48. Fandrich M., Forge V., Buder K., Kittler M., Dobson C.M., and Diekmann S. Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments. Proc. Natl Acad. Sci. USA 100 (2003) 15463-15468
49. Platt G.W., Routledge K.E., Homans S.W., and Radford S.E. Fibril growth kinetics reveal a region of beta2-microglobulin important for nucleation and elongation of aggregation. J. Mol. Biol. 378 (2008) 251-263
50. Routledge K.E., Tartaglia G.G., Platt G.W., Vendruscolo M., and Radford S.E. Competition between intramolecular and intermolecular interactions in an amyloid-forming protein. J. Mol. Biol. 389 (2009) 776-786
51. Mishima T., Ohkuri T., Monji A., Imoto T., and Ueda T. A particular hydrophobic cluster in the residual structure of reduced lysozyme drastically affects the amyloid fibrils formation. Biochem. Biophys. Res. Commun. 356 (2007) 769-772
52. Ropson I.J., and Frieden C. Dynamic NMR spectral analysis and protein folding: identification of a highly populated folding intermediate of rat intestinal fatty acid-binding protein by 19F NMR. Proc. Natl Acad. Sci. USA 89 (1992) 7222-7226
53. Neri D., Billeter M., Wider G., and Wuthrich K. NMR determination of residual structure in a urea-denatured protein, the 434-repressor. Science 257 (1992) 1559-1563
54. Saab-Rincon G., Gualfetti P.J., and Matthews C.R. Mutagenic and thermodynamic analyses of residual structure in the alpha subunit of tryptophan synthase. Biochemistry 35 (1996) 1988-1994
55. Jarrett J.T., and Lansbury Jr. P.T. Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry 31 (1992) 12345-12352
56. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
57. Abedini A., Tracz S.M., Cho J.H., and Raleigh D.P. Characterization of the heparin binding site in the N-terminus of human pro-islet amyloid polypeptide: implications for amyloid formation. Biochemistry 45 (2006) 9228-9237
58. Hoyer W., Cherny D., Subramaniam V., and Jovin T.M. Impact of the acidic C-terminal region comprising amino acids 109-140 on alpha-synuclein aggregation in vitro. Biochemistry 43 (2004) 16233-16242
59. Smith D.P., and Radford S.E. Role of the single disulphide bond of beta(2)-microglobulin in amyloidosis in vitro. Protein Sci. 10 (2001) 1775-1784
60. Hurle M.R., Helms L.R., Li L., Chan W., and Wetzel R. A role for destabilizing amino acid replacements in light-chain amyloidosis. Proc. Natl Acad. Sci. USA 91 (1994) 5446-5450
61. Raffen R., Dieckman L.J., Szpunar M., Wunschl C., Pokkuluri P.R., Dave P., et al. Physicochemical consequences of amino acid variations that contribute to fibril formation by immunoglobulin light chains. Protein Sci. 8 (1999) 509-517
62. Kim Y., Wall J.S., Meyer J., Murphy C., Randolph T.W., Manning M.C., et al. Thermodynamic modulation of light chain amyloid fibril formation. J. Biol. Chem. 275 (2000) 1570-1574
63. Randles E.G., Thompson J.R., Martin D.J., and Ramirez-Alvarado M. Structural alterations within native amyloidogenic immunoglobulin light chains. J. Mol. Biol. 389 (2009) 199-210
64. Ignatovich O., Tomlinson I.M., Jones P.T., and Winter G. The creation of diversity in the human immunoglobulin V(lambda) repertoire. J. Mol. Biol. 268 (1997) 69-77
65. Market E., and Papavasiliou F.N. V(D)J recombination and the evolution of the adaptive immune system. PLoS Biol. 1 (2003) E16
66. Li Z., Woo C.J., Iglesias-Ussel M.D., Ronai D., and Scharff M.D. The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 18 (2004) 1-11
67. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28 (1989) 8972-8979
68. 15N NMR spectroscopy. Biochemistry 31 (1992) 4856-4866