The GB1 amyloid fibril: Recruitment of the peripheral β-strands of the domain swapped dimer into the polymeric interface

Journal of Molecular Biology

Volumn 348, Issue 3, 2005, Pages 687-698

  Louis, John M ^a   Byeon, In Ja L ^a   Baxa, Ulrich ^b   Gronenborn, Angela M ^a,c  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Amyloid; Cross linking; Domain swapping; fibril; Immunoglobulin binding domain B1

Indexed keywords

AMYLOID; CYSTEINE DERIVATIVE; DIMER; IMMUNOGLOBULIN BINDING DOMAIN B1 OF STREPTOCOCCAL PROTEIN G; MUTANT PROTEIN; POLYMER; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL BOND; FIBER; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN VARIANT; REVERTANT;

EID: 17144382523     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.02.071     Document Type: Article

References (58)

1. J.D. Sipe Amyloidosis Crit. Rev. Clin. Lab. Sci. 31 1994 325 354
2. R.W. Carrell, and D.A. Lomas Conformational diseases Lancet 350 1997 134 138
3. J.W. Kelly The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways Curr. Opin. Struct. Biol. 8 1998 101 106
4. R.W. Carrell, and B. Gooptu Conformational changes and disease- serpins, prions and Alzheimer's Curr. Opin. Struct. Biol. 8 1998 799 809
5. C.M. Dobson Protein misfolding, evolution and disease Trends Biochem. Sci. 24 1999 329 332
6. J.C. Rochet, and P.T. Lansbury Jr Amyloid fibrillogenesis: themes and variations Curr. Opin. Struct. Biol. 10 2000 60 68
7. Wetzel, R., ed. (1999). Amyloid, prions and other aggregates. Methods in Enzymol. 309, Academic Press, San Diego.
8. V.N. Uversky, and A.L. Fink Conformational constraints for amyloid fibrillation: the importance of being unfolded Biochim. Biophys. Acta 1698 2004 131 153
9. P.E. Wright, and H.J. Dyson Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm J. Mol. Biol. 293 1999 321 331
10. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins: Struct. Funct. Genet. 41 2000 415 427
11. A.K. Dunker, J.D. Lawson, C.J. Brown, R.M. Williams, P. Romero, and J.S. Oh Intrinsically disordered protein J. Mol. Graph. Model. 19 2001 26 59
12. P. Tompa Intrinsically unstructured proteins Trends Biochem. Sci. 27 2002 527 533
13. J.L. Jiminez, J.I. Guijarro, E. Orlova, J. Zurdo, C.M. Dobson, and M. Sunde Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing EMBO J. 18 1999 815 821
14. L.C. Serpell Alzheimer's amyloid fibrils: structure and assembly Biochim. Biophys. Acta 1502 2000 16 30
15. J.D. Sipe, and A.S. Cohen Review: history of the amyloid fibril J. Struct. Biol. 130 2000 88 98
16. R. Wetzel Ideas of order for amyloid fibril structure Structure 10 2002 1031 1036
17. M.F. Perutz, J.T. Finch, J. Berriman, and A. Lesk Amyloid fibers are water-filled nanotubes Proc. Natl Acad. Sci. USA 99 2002 5591 5595
18. A.T. Petkova, Y. Ishii, J.J. Balbach, O.N. Antzutkin, R.D. Leapman, and F. Delaglio A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl Acad. Sci. USA 99 2002 16742 16747
19. M. Sunde, L.C. Serpell, M. Bartlam, P.E. Fraser, M.B. Pepys, and C.C.F. Blake Common core structure of amyloid fibrils by synchrotron X-ray diffraction J. Mol. Biol. 273 1997 729 739
20. A.M. Gronenborn, D.R. Filpula, N.Z. Essig, A. Achari, M. Whitlow, P.T. Wingfield, and G.M. Clore A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G Science 253 1991 657 661
21. A. Achari, S.P. Hale, A.J. Howard, G.M. Clore, A.M. Gronenborn, K.D. Hardman, and M. Whitlow 1.67 Å X-ray structure of the B2 immunoglobulin-binding domain of streptococcal protein G and comparison to the NMR structure of the B1 domain Biochemistry 31 1992 10449 10457
22. O. Tcherkasskaya, J.R. Knutson, S.A. Bowley, M.K. Frank, and A.M. Gronenborn Nanosecond dynamics of the single tryptophan reveals multi-state equilibrium unfolding of protein GB1 Biochemistry 39 2000 11216 11226
23. M.K. Frank, F. Dyda, A. Dobrodumov, and A.M. Gronenborn Core mutations switch monomeric protein GB1 into an intertwined tetramer Nature Struct. Biol. 9 2002 877 885
24. I.-J.L. Byeon, J.M. Louis, and A.M. Gronenborn A protein contortionist: core mutations of GB1 that induce dimerization and domain swapping J. Mol. Biol. 333 2003 141 152
25. K. Ding, J.M. Louis, and A.M. Gronenborn Insights into conformation and dynamics of protein GB1 during folding and unfolding by NMR J. Mol. Biol. 335 2004 1299 1307
26. I.-J.L. Byeon, J.M. Louis, and A.M. Gronenborn A captured folding intermediate involved in dimerization and domain-swapping of GB1 J. Mol. Biol. 340 2004 615 625
27. H.J. Dyson, and P.E. Wright Unfolded proteins and protein folding studied by NMR Chem. Rev. 104 2004 3607 3622
28. M.P. Schlunegger, M.J. Bennett, and D. Eisenberg Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly Advan. Protein Chem. 50 1997 61 122
29. Y. Liu, and D. Eisenberg 3D domain swapping: as domains continue to swap Protein Sci 11 2002 1285 1299
30. M.E. Newcomer Trading places Nature Struct. Biol. 8 2001 282 284
31. M.E. Newcomer Protein folding and three-dimensional domain swapping: a strained relationship? Curr. Opin. Struct. Biol. 12 2002 48 53
32. R. Janowski, M. Kozak, E. Jankowska, Z. Grzonka, A. Grubb, and M. Abrahamson Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping Nature Struct. Biol. 8 2001 316 320
33. K.J. Knaus, M. Morillas, W. Swietnicki, M. Malone, W.K. Surewicz, and V.C. Yee Crystal structure of the human prion protein reveals a mechanism for oligomerization Nature Struct. Biol. 8 2001 770 774
34. R.A. Staniforth, S. Giannini, L.D. Higgins, M.J. Conroy, A.M. Hounslow, and R. Jerala Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily EMBO J. 20 2001 4774 4781
35. C.A. Bewley, K.R. Gustafson, M.R. Boyd, D.G. Covell, A. Bax, G.M. Clore, and A.M. Gronenborn Solution structure of cyanovirin-N, a potent HIV-inactivating protein Nature Struct. Biol. 5 1998 571 578
36. F. Yang, C.A. Bewley, J.M. Louis, K.R. Gustafson, M.R. Boyd, and A.M. Gronenborn Crystal structure of cyanovirin-N, a potent HIV-inactivating protein, shows unexpected domain-swapping J. Mol. Biol. 288 1999 403 412
37. L.G. Barrientos, J.M. Louis, I. Botos, T. Mori, Z.Z. Han, and B.R. O'Keefe The domain-swapped dimer of cyanovirin-N is in a metastable folded state: reconciliation of X-ray and NMR structures Structure 10 2002 673 686
38. L.G. Barrientos, F. Lasala, R. Delgado, A. Sanchez, and A.M. Gronenborn Flipping the switch from monomeric to dimeric CV-N has little effect on antiviral activity Structure 12 2004 1799 1807
39. P.G. DeGennes Brownian motions of flexible polymer-chains Nature 282 1979 367 370
40. M. Ramirez-Alvarado, J.S. Merkel, and L. Regan 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
41. M. Ramirez-Alvarado, and L. Regan Does the location of a mutation determine the ability to form amyloid fibrils? J. Mol. Biol. 323 2002 17 22
42. C.S. Goldsbury, S. Wirtz, S.A. Muller, S. Sunderji, P. Wicki, and U. Aebi Studies on the in vitro assembly of Aβ1-40: implications for the search for Aβ fibril formation inhibitors J. Struct. Biol. 130 2000 217 231
43. J.L. Jimenez, E.J. Nettleton, M. Bouchard, C.V. Robinson, C.M. Dobson, and H.R. Saibil The protofilament structure of insulin amyloid fibrils Proc. Natl Acad. Sci. USA 99 2002 9196 9201
44. R. Khurana, C. Ionescu-Zanetti, M. Pope, J. Li, L. Nielson, and M. Ramirez-Alvarado A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy Biophys. J. 85 2003 1135 1144
45. 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
46. T. Gallagher, P. Alexander, P. Bryan, and G.L. Gilliland Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR Biochemistry 33 1994 4721 4729
47. J.L. Jimenez, J.L. Guijarro, E. Orlova, J. Zurdo, C.M. Dobson, and M. Sunde Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing EMBO J. 18 1999 815 821
48. J.R. Glover, A.S. Kowal, E.C. Schirmer, M.M. Patino, J.J. Liu, and S. Lindquist Self-seeded fibers formed by Sup35, the protein determinant of [PSI+], a heritable prion-like factor of S-cerevisiae Cell 89 1997 811 819
49. A.V. Kajava, U. Baxa, R.B. Wickner, and A.C. Steven A model for Ure2p prion filaments and other amyloids: the parallel superpleated beta-structure Proc. Natl Acad. Sci. USA 101 2004 7885 7890
50. A.J. Modler, K. Gast, G. Lutsch, and G. Damaschun Assembly of amyloid protofibrils via critical oligomers - a novel pathway of amyloid formation J. Mol. Biol. 325 2003 135 148
51. A. Sanders, C.J. Craven, L.D. Higgins, S. Giannini, M.J. Conroy, and A.M. Hounslow Cystatin forms a tetramer through structural rearrangement of domain-swapped dimers prior to amyloidogenesis J. Mol. Biol. 336 2004 165 178
52. M.J. Bennett, M.P. Schlunegger, and D. Eisenberg 3D domain swapping - a mechanism for oligomer assembly Protein Sci. 4 1995 2455 2468
53. S. Lee, and D. Eisenberg Seeded conversion of recombinant prion protein to a disulfide-bonded oligomer by a reduction-oxidation process Nature Struct. Biol. 10 2003 725 730
54. J.S. Pedersen, G. Christensen, and D.E. Otzen Modulation of S6 fibrillation by unfolding rates and gatekeeper residues J. Mol. Biol. 341 2004 575 588
55. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRpipe-a multidimensional spectral processing system based on Unix Pipes J. Biomol. NMR 6 1995 277 293
56. D.S. Garrett, R. Powers, A.M. Gronenborn, and G.M. Clore A Common-sense approach to peak picking in 2-dimensional, 3-dimensional, and 4-dimensional spectra using automatic computer analysis of contour diagrams J. Magn. Reson. 95 1991 214 220
57. C.D. Schwieters, J.J. Kuszewski, N. Tjandra, and G.M. Clore The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160 2003 65 73
58. A.T. Brünger X-PLOR: Version 3.1: A System for X-ray Crystallography and NMR 1992 Yale University Press New Haven, CT