Direct detection of transient α-helical states in islet amyloid polypeptide

Protein Science

Volumn 16, Issue 1, 2007, Pages 110-117

  Williamson, Jessica A ^a   Miranker, Andrew D ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

helix; Amylin; Amyloid; IAPP; Intrinsic disorder; NMR; Protein folding; Type 2 diabetes

Indexed keywords

AMYLIN; AMYLOID;

ALPHA HELIX; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; NONHUMAN; PANCREAS ISLET; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTON NUCLEAR MAGNETIC RESONANCE; RAT;

AMINO ACID SEQUENCE; AMYLOID; ANIMALS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; RATS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 33845960266     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062486907     Document Type: Article

References (63)

1. Abedini, A. and Raleigh, D.P. 2006. Destabilization of human IAPP amyloid fibrils by proline mutations outside of the putative amyloidogenic domain: Is there a critical amyloidogenic domain in human IAPP? J. Mol. Biol. 355: 274-281.
2. Aurora, R. and Rose, G.D. 1998. Helix capping. Protein Sci. 7: 21-38.
3. 1H NMR and distance geometry with restrained molecular dynamics. Biochemistry 30: 575-582.
4. Butler, A.E., Jang, J., Gurlo, T., Carty, M.D., Soeller, W.C., and Butler, P.C. 2004. Diabetes due to a progressive defect in β-cell mass in rats transgenic for human islet amyloid polypeptide (HIP Rat): A new model for type 2 diabetes. Diabetes 53: 1509-1516.
5. Chiti, F. and Dobson, C.M. 2006. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75: 333-366.
6. Cierpicki, T. and Otlewski, J. 2001. Amide proton temperature coefficients as hydrogen bond indicators in proteins. J. Biomol. NMR 21: 249-261.
7. Cooper, G.J. 1994. Amylin compared with calcitonin gene-related peptide: Structure, biology, and relevance to metabolic disease. Endocr. Rev. 15: 163-201.
8. Cort, J., Liu, Z., Lee, G., Harris, S.M., Prickett, K.S., Gaeta, L.S., and Andersen, N.H. 1994. β-structure in human amylin and two designer β-peptides: CD and NMR spectroscopic comparisons suggest soluble β-oligomers and the absence of significant populations of β-strand dimers. Biochem. Biophys. Res. Commun. 204: 1088-1095.
9. Cottingham, I.R., Millar, A., Emslie, E., Colman, A., Schnieke, A.E., and McKee, C. 2001. A method for the amidation of recombinant peptides expressed as intein fusion proteins in Escherichia coli. Nat. Biotechnol. 19: 974-977.
10. Creighton, T.E. 1993. Proteins: Structures and molecular properties, 2d ed. W.H. Freeman and Company, New York.
11. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. 1995. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6: 277-293.
12. Dobeli, H., Draeger, N., Huber, G., Jakob, P., Schmidt, D., Seilheimer, B., Stuber, D., Wipf, B., and Zulauf, M. 1995. A biotechnological method provides access to aggregation competent monomeric Alzheimer's 1-42 residue amyloid peptide. Biotechnology (N.Y.) 13: 988-993.
13. Dunker, A.K., Lawson, J.D., Brown, C.J., Williams, R.M., Romero, P., Oh, J.S., Oldfield, C.J., Campen, A.M., Ratliff, C.M., Hipps, K.W., et al. 2001. Intrinsically disordered protein. J. Mol. Graph. Model. 19: 26-59.
14. Dyson, H.J. and Wright, P.E. 2001. Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. Methods Enzymol. 339: 258-270.
15. Eakin, C.M., Berman, A.J., and Miranker, A.D. 2006. A native to amyloidogenic transition regulated by a backbone trigger. Nat. Struct. Mol. Biol. 13: 202-208.
16. Gehman, J.D. 2003. Theoretical macromolecular structure elucidation using solid state nuclear magnetic resonance. In Chemistry, pp. 160-188. Yale University, New Haven, CT.
17. Green, J., Goldsbury, C., Mini, T., Sunderji, S., Frey, P., Kistler, J., Cooper, G., and Aebi, U. 2003. Full-length rat amylin forms fibrils following substitution of single residues from human amylin. J. Mol. Biol. 326: 1147-1156.
18. Grzesiek, S. and Bax, A. 1992a. Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114: 6291-6293.
19. Grzesiek, S. and Bax, A. 1992b. An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins. J. Magn. Reson. 99: 201-207.
20. Hay, D.L., Christopoulos, G., Christopoulos, A., and Sexton, P.M. 2004. Amylin receptors: Molecular composition and pharmacology. Biochem. Soc. Trans. 32: 865-867.
21. Hoppener, J.W., Ahren, B., and Lips, C.J. 2000. Islet amyloid and type 2 diabetes mellitus. N. Engl. J. Med. 343: 411-419.
22. Howitt, S.G., Kilk, K., Wang, Y., Smith, D.M., Langel, U., and Poyner, D.R. 2003. The role of the 8-18 helix of CGRP8-37 in mediating high affinity binding to CGRP receptors; coulombic and steric interactions. Br. J. Pharmacol. 138: 325-332.
23. Hull, R.L., Westermark, G.T., Westermark, P., and Kahn, S.E. 2004. Islet amyloid: A critical entity in the pathogenesis of type 2 diabetes. J. Clin. Endocrinol. Metab. 89: 3629-3643.
24. 15N spectra of proteins: Heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29: 4659-4667.
25. Jaikaran, E.T. and Clark, A. 2001. Islet amyloid and type 2 diabetes: From molecular misfolding to islet pathophysiology. Biochim. Biophys. Acta 1537: 179-203.
26. Jaikaran, E.T., Higham, C.E., Serpell, L.C., Zurdo, J., Gross, M., Clark, A., and Fraser, P.E. 2001. Identification of a novel human islet amyloid polypeptide β-sheet domain and factors influencing fibrillogenesis. J. Mol. Biol 308: 515-525.
27. Kay, L.E., Keifer, P., and Saarinen, T. 1992. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc 114: 10663-10665.
28. Kayed, R., Bernhagen, J., Greenfield, N., Sweimeh, K., Brunner, H., Voelter, W., and Kapurniotu, A. 1999. Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro. J. Mol. Biol 287: 781-796.
29. Kessler, J.C., Rochet, J.C., and Lansbury Jr., P.T. 2003. The N-terminal repeat domain of α-synuclein inhibits β-sheet and amyloid fibril formation. Biochemistry 42: 672-678.
30. Kirkitadze, M.D., Condron, M.M., and Teplow, D.B. 2001. Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis. J. Mol. Biol. 312: 1103-1119.
31. Knight, J.D., Hebda, J.A., and Miranker, A.D. 2006. Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide. Biochemistry 45: 9496-9508.
32. Lopes, D.H., Colin, C., Degaki, T.L., de Sousa, A.C., Vieira, M.N., Sebollela, A., Martinez, A.M., Bloch Jr., C., Ferreira, S.T., and Sogayar, M.C. 2004. Amyloidogenicity and cytotoxicity of recombinant mature human islet amyloid polypeptide (rhIAPP). J. Biol. Chem. 279: 42803-42810.
33. Lopez de la Paz, M., de Mori, G.M., Serrano, L., and Colombo, G. 2005. Sequence dependence of amyloid fibril formation: Insights from molecular dynamics simulations. J. Mol. Biol. 349: 583-596.
34. MacArthur, M.W. and Thornton, J.M. 1991. Influence of proline residues on protein conformation. J. Mol. Biol. 218: 397-412.
35. Matveyenko, A.V. and Butler, P.C. 2006. β-Cell deficit due to increased apoptosis in the human islet amyloid polypeptide transgenic (HIP) rat recapitulates the metabolic defects present in type 2 diabetes. Diabetes 55: 2106-2114.
36. Mazor, Y., Gilead, S., Benhar, I., and Gazit, E. 2002. Identification and characterization of a novel molecular-recognition and self-assembly domain within the islet amyloid polypeptide. J. Mol. Biol. 322: 1013-1024.
37. McNulty, B.C., Young, G.B., and Pielak, G.J. 2006. Macromolecular crowding in the Escherichia coli periplasm maintains α-synuclein disorder. J. Mol. Biol. 355: 893-897.
38. 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR 5: 14-24.
39. Muff, R., Born, W., Lutz, T.A., and Fischer, J.A. 2004. Biological importance of the peptides of the calcitonin family as revealed by disruption and transfer of corresponding genes. Peptides 25: 2027-2038.
40. Munoz, V. and Serrano, L. 1997. Development of the multiple sequence approximation within the AGADIR model of α-helix formation: Comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers 41: 495-509.
41. Murray, N.E., Brammar, W.J., and Murray, K. 1977. Lambdoid phages that simplify the recovery of in vitro recombinants. Mol. Gen. Genet. 150: 53-61.
42. Neidhardt, F.C., Bloch, P.L., and Smith, D.F. 1974. Culture medium for enterobacteria. J. Bacteriol. 119: 736-747.
43. Nelson, R., Sawaya, M.R., Balbirnie, M., Madsen, A.O., Riekel, C., Grothe, R., and Eisenberg, D. 2005. Structure of the cross-β spine of amyloid-like fibrils. Nature 435: 773-778.
44. Padrick, S.B. and Miranker, A.D. 2001. Islet amyloid polypeptide: Identification of long-range contacts and local order on the fibrillogenesis pathway. J. Mol. Biol. 308: 783-794.
45. Padrick, S.B. and Miranker, A.D. 2002. Islet amyloid: Phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis. Biochemistry 41: 4694-4703.
46. Pauling, L., Corey, R.B., and Branson, H.R. 1951. The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain. Proc. Natl. Acad. Sci. 37: 205-211.
47. Petkova, A.T., Leapman, R.D., Guo, Z., Yau, W.M., Mattson, M.P., and Tycko, R. 2005. Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science 307: 262-265.
48. Schwarzinger, S., Kroon, G.J., Foss, T.R., Wright, P.E., and Dyson, H.J. 2000. Random coil chemical shifts in acidic 8 M urea: Implementation of random coil shift data in NMRView. J. Biomol. NMR 18: 43-48.
49. Schwarzinger, S., Kroon, G.J., Foss, T.R., Chung, J., Wright, P.E., and Dyson, H.J. 2001. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc. 123: 2970-2978.
50. Seavey, B.R., Farr, E.A., Westler, W.M., and Markley, J.L. 1991. A relational database for sequence-specific protein NMR data. J. Biomol. NMR 1: 217-236.
51. Shao, H., Jao, S., Ma, K., and Zagorski, M.G. 1999. Solution structures of micelle-bound amyloid β-(1-40) and β-(1-42) peptides of Alzheimer's disease. J. Mol. Biol. 285: 755-773.
52. Studier, F.W. and Moffatt, B.A. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189: 113-130.
53. Uversky, V.N. and Fink, A.L. 2004. Conformational constraints for amyloid fibrillation: The importance of being unfolded. Biochim. Biophys. Acta 1698: 131-153.
54. Wang, F., Hull, R.L., Vidal, J., Cnop, M., and Kahn, S.E. 2001. Islet amyloid develops diffusely throughout the pancreas before becoming severe and replacing endocrine cells. Diabetes 50: 2514-2520.
55. Westermark, G.T., Gebre-Medhin, S., Steiner, D.F., and Westermark, P. 2000. Islet amyloid development in a mouse strain lacking endogenous islet amyloid polypeptide (IAPP) but expressing human IAPP. Mol. Med. 6: 998-1007.
56. Westermark, P., Engstrom, U., Johnson, K.H., Westermark, G.T., and Betsholtz, C. 1990. Islet amyloid polypeptide: Pinpointing amino acid residues linked to amyloid fibril formation. Proc. Natl. Acad. Sci. 87: 5036-5040.
57. Wishart, D.S. and Sykes, B.D. 1994. Chemical shifts as a tool for structure determination. Methods Enzymol. 239: 363-392.
58. Wishart, D.S., Sykes, B.D., and Richards, F.M. 1991. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222: 311-333.
59. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 5: 67-81.
60. Yao, J., Chung, J., Eliezer, D., Wright, P.E., and Dyson, H.J. 2001. NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding. Biochemistry 40: 3561-3571.
61. Zhang, O. and Forman-Kay, J.D. 1997. NMR studies of unfolded states of an SH3 domain in aqueous solution and denaturing conditions. Biochemistry 36: 3959-3970.
62. 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J. Biomol. NMR 4: 845-858.
63. Zhang, X., Xu, Y., Zhang, J., Wu, J., and Shi, Y. 2005. Structural and dynamic characterization of the acid-unfolded state of hUBF HMG box 1 provides clues for the early events in protein folding. Biochemistry 44: 8117-8125.