Full-length rat amylin forms fibrils following substitution of single residues from human amylin

Journal of Molecular Biology

Volumn 326, Issue 4, 2003, Pages 1147-1156

  Green, Janelle ^a   Goldsbury, Claire ^b   Mini, Thierry ^a   Sunderji, Shabir ^c   Frey, Peter ^c   Kistler, Joerg ^d   Cooper, Garth ^d,e   Aebi, Ueli ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^c NOVARTIS PHARMA AG   (Switzerland)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Amylin; Amyloid; Islet amyloid polypeptide (IAPP); Proline residues; Type 2 diabetes

Indexed keywords

AMYLIN; PEPTIDE; PROLINE; THIOFLAVINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; ASSAY; BIOSYNTHESIS; CONTROLLED STUDY; ELECTRON MICROSCOPY; FIBER; FLUORESCENCE; HUMAN; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN VARIANT; RAT; SEDIMENTATION; STAINING;

EID: 0037470589     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01377-3     Document Type: Article

References (60)

1. Sipe J.D., Cohen A.S. Review: history of the amyloid fibril. J. Struct. Biol. 130:2000;88-98.
2. Clark A., Cooper G.J., Lewis C.E., Morris J.F., Willis A.C., Reid K.B., Turner R.C. Islet amyloid formed from diabetes-associated peptide may be pathogenic in type-2 diabetes. Lancet. 2:1987;231-234.
3. Cooper G.J., Willis A.C., Clark A., Turner R.C., Sim R.B., Reid K.B. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl Acad. Sci. USA. 84:1987;8628-8632.
4. Brain S.D., Williams T.J., Tippins J.R., Morris H.R., MacIntyre I. Calcitonin gene-related peptide is a potent vasodilator. Nature. 313:1985;54-56.
5. Bauerfeind P., Hof R., Hof A., Cucala M., Siegrist S., von Ritter C., Fischer J.A., Blum A.L. Effects of hCGRP I and II on gastric blood flow and acid secretion in anesthetized rabbits. Am. J. Physiol. 256:1989;G145-G149.
6. Cooper G.J. Amylin compared with calcitonin gene-related peptide: structure, biology, and relevance to metabolic disease. Endocr. Rev. 15:1994;163-201.
7. Cornish J., Callon K.E., King A.R., Cooper G.J., Reid I.R. Systemic administration of amylin increases bone mass, linear growth, and adiposity in adult male mice. Am. J. Physiol. 275:1998;E694-E699.
8. Hettiarachchi M., Chalkley S., Furler S.M., Choong Y.S., Heller M., Cooper G.J., Kraegen E.W. Rat amylin-(8-37) enhances insulin action and alters lipid metabolism in normal and insulin-resistant rats. Am. J. Physiol. 273:1997;E859-E867.
9. Leighton B., Cooper G.J. Pancreatic amylin and calcitonin gene-related peptide cause resistance to insulin in skeletal muscle in vitro. Nature. 335:1988;632-635.
10. Young A.A., Cooper G.J., Carlo P., Rink T.J., Wang M.W. Response to intravenous injections of amylin and glucagon in fasted, fed, and hypoglycemic rats. Am. J. Physiol. 264:1993;E943-E950.
11. DeArmond S.J., McKinley M.P., Barry R.A., Braunfeld M.B., McColloch J.R., Prusiner S.B. Identification of prion amyloid filaments in scrapie-infected brain. Cell. 41:1985;221-235.
12. Forloni G., Angeretti N., Chiesa R., Monzani E., Salmona M., Bugiani O., Tagliavini F. Neurotoxicity of a prion protein fragment. Nature. 362:1993;543-546.
13. Lorenzo A., Yankner B.A. Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red. Proc. Natl Acad. Sci. USA. 91:1994;12243-12247.
14. Schubert D., Behl C., Lesley R., Brack A., Dargusch R., Sagara Y., Kimura H. Amyloid peptides are toxic via a common oxidative mechanism. Proc. Natl Acad. Sci. USA. 92:1995;1989-1993.
15. Lorenzo A., Razzaboni B., Weir G.C., Yankner B.A. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature. 368:1994;756-760.
16. Janson J., Ashley R.H., Harrison D., McIntyre S., Butler P.C. The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes. 48:1999;491-498.
17. Tenidis K., Waldner M., Bernhagen J., Fischle W., Bergmann M., Weber M., et al. Identification of a penta- and hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties. J. Mol. Biol. 295:2000;1055-1071.
18. Eanes E.D., Glenner G.G.X.-. ray diffraction studies on amyloid filaments. J. Histochem. Cytochem. 16:1968;673-677.
19. Geddes A.J., Parker K.D., Atkins E.D., Beighton E. "Cross-beta" conformation in proteins. J. Mol. Biol. 32:1968;343-358.
20. Shirahama T., Cohen A.S. High-resolution electron microscopic analysis of the amyloid fibril. J. Cell. Biol. 33:1967;679-708.
21. Blake C., Serpell L. Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous beta-sheet helix. Structure. 4:1996;989-998.
22. Cardoso I., Goldsbury C.S., Muller S.A., Olivieri V., Wirtz S., Damas A.M., et al. Transthyretin fibrillogenesis entails the assembly of monomers: a molecular model for in vitro assembled transthyretin amyloid-like fibrils. J. Mol. Biol. 317:2002;683-695.
23. Chaney M.O., Webster S.D., Kuo Y.M., Roher A.E. Molecular modeling of the Abeta1-42 peptide from Alzheimer's disease. Protein Eng. 11:1998;761-767.
24. Malinchik S.B., Inouye H., Szumowski K.E., Kirschner D.A. Structural analysis of Alzheimer's beta(1-40) amyloid: protofilament assembly of tubular fibrils. Biophys. J. 74:1998;537-545.
25. Serpell L.C., Sunde M., Benson M.D., Tennent G.A., Pepys M.B., Fraser P.E. The protofilament substructure of amyloid fibrils. J. Mol. Biol. 300:2000;1033-1039.
26. Shirahama T., Benson M.D., Cohen A.S., Tanaka A. Fibrillar assemblage of variable segments of immunoglobulin light chains: an electron microscopic study. J. Immunol. 110:1973;21-30.
27. Bauer H.H., Aebi U., Haner M., Hermann R., Muller M., Merkle H.P. Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin. J. Struct. Biol. 115:1995;1-15.
28. Cohen, A. S., Shirahama, T. & Skinner, M. (1982). Electron microscopy of amyloid. In Electron Microscopy of Protein (Harrid, I., ed.), vol. 3, pp. 165-205, Academic Press, London.
29. Goldsbury C.S., Cooper G.J., Goldie K.N., Muller S.A., Saafi E.L., Gruijters W.T., et al. Polymorphic fibrillar assembly of human amylin. J. Struct. Biol. 119:1997;17-27.
30. Goldsbury C., Goldie K., Pellaud J., Seelig J., Frey P., Muller S.A., et al. Amyloid fibril formation from full-length and fragments of amylin. J. Struct. Biol. 130:2000;352-362.
31. Goldsbury C.S., Wirtz S., Muller S.A., Sunderji S., Wicki P., Aebi U., Frey P. Studies on the in vitro assembly of a beta 1-40: implications for the search for a beta fibril formation inhibitors. J. Struct. Biol. 130:2000;217-231.
32. Harper J.D., Wong S.S., Lieber C.M., Lansbury P.T. Observation of metastable Abeta amyloid protofibrils by atomic force microscopy. Chem. Biol. 4:1997;119-125.
33. Kirschner D.A., Inouye H., Duffy L.K., Sinclair A., Lind M., Selkoe D.J. Synthetic peptide homologous to beta protein from Alzheimer disease forms amyloid-like fibrils in vitro. Proc. Natl Acad. Sci. USA. 84:1987;6953-6957.
34. Serpell L.C., Sunde M., Fraser P.E., Luther P.K., Morris E.P., Sangren O., et al. Examination of the structure of the transthyretin amyloid fibril by image reconstruction from electron micrographs. J. Mol. Biol. 254:1995;113-118.
35. Azriel R., Gazit E. Analysis of the minimal amyloid-forming fragment of the islet amyloid polypeptide. An experimental support for the key role of the phenylalanine residue in amyloid formation. J. Biol. Chem. 276:2001;34156-34161.
36. Glenner G.G., Eanes E.D., Wiley C.A. Amyloid fibrils formed from a segment of the pancreatic islet amyloid protein. Biochem. Biophys. Res. Commun. 155:1988;608-614.
37. Nilsson M.R., Raleigh D.P. Analysis of amylin cleavage products provides new insights into the amyloidogenic region of human amylin. J. Mol. Biol. 294:1999;1375-1385.
38. Moriarty D.F., Raleigh D.P. Effects of sequential proline substitutions on amyloid formation by human amylin 20-29. Biochemistry. 38:1999;1811-1818.
39. Westermark P., Engstrom U., Johnson K.H., Westermark G.T., Betsholtz C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc. Natl Acad. Sci. USA. 87:1990;5036-5040.
40. Chou P.Y., Fasman G.D. Empirical predictions of protein conformation. Annu. Rev. Biochem. 47:1978;251-276.
41. Minor D.L. Jr, Kim P.S. Measurement of the beta-sheet-forming propensities of amino acids. Nature. 367:1994;660-663.
42. Jaikaran E.T., Higham C.E., Serpell L.C., Zurdo J., Gross M., Clark A., Fraser P.E. Identification of a novel human islet amyloid polypeptide beta-sheet domain and factors influencing fibrillogenesis. J. Mol. Biol. 308:2001;515-525.
43. Jaikaran E.T., Clark A. Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochim. Biophys. Acta. 1537:2001;179-203.
44. Padrick S.B., Miranker A.D. Islet amyloid polypeptide: identification of long-range contacts and local order on the fibrillogenesis pathway. J. Mol. Biol. 308:2001;783-794.
45. Betsholtz C., Christmanson L., Engstrom U., Rorsman F., Jordan K., O'Brien T.D., et al. Structure of cat islet amyloid polypeptide and identification of amino acid residues of potential significance for islet amyloid formation. Diabetes. 39:1990;118-122.
46. LeVine H. Thioflavin T interations with amyloid beta-sheet structures. Amyloid: Int. J. Exp. Clin. Invest. 2:1995;1-6.
47. Goldsbury C., Kistler J., Aebi U., Arvinte T., Cooper G.J. Watching amyloid fibrils grow by time-lapse atomic force microscopy. J. Mol. Biol. 285:1999;33-39.
48. Hutchinson E.G., Thornton J.M. A revised set of potentials for beta-turn formation in proteins. Protein Sci. 3:1994;2207-2216.
49. Richardson J.S. The anatomy and taxonomy of protein structure. Advan. Protein Chem. 34:1981;167-339.
50. Rose G.D., Gierasch L.M., Smith J.A. Turns in peptides and proteins. Advan. Protein Chem. 37:1985;1-109.
51. Curtain C.C., Ali F., Volitakis I., Cherny R.A., Norton R.S., Beyreuther K., et al. Alzheimer's disease amyloid-beta binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits. J. Biol. Chem. 276:2001;20466-20473.
52. Fraser P.E., McLachlan D.R., Surewicz W.K., Mizzen C.A., Snow A.D., Nguyen J.T., Kirschner D.A. Conformation and fibrillogenesis of Alzheimer A beta peptides with selected substitution of charged residues. J. Mol. Biol. 244:1994;64-73.
53. Huang X., Atwood C.S., Moir R.D., Hartshorn M.A., Vonsattel J.P., Tanzi R.E., Bush A.I. Zinc-induced Alzheimer's Abeta1-40 aggregation is mediated by conformational factors. J. Biol. Chem. 272:1997;26464-26470.
54. Yang D.S., McLaurin J., Qin K., Westaway D., Fraser P.E. Examining the zinc binding site of the amyloid-beta peptide. Eur. J. Biochem. 267:2000;6692-6698.
55. Gazit E. A possible role for pi-stacking in the self-assembly of amyloid fibrils. Faseb J. 16:2002;77-83.
56. Chiti F., Calamai M., Taddei N., Stefani M., Ramponi G., Dobson C.M. Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proc. Natl Acad. Sci. USA. 2002.
57. Chiti F., Taddei N., Baroni F., Capanni C., Stefani M., Ramponi G., Dobson C.M. Kinetic partitioning of protein folding and aggregation. Nature Struct. Biol. 9:2002;137-143.
58. Taddei N., Capanni C., Chiti F., Stefani M., Dobson C.M., Ramponi G. Folding and aggregation are selectively influenced by the conformational preferences of the alpha-helices of muscle acylphosphatase. J. Biol. Chem. 276:2001;37149-37154.
59. Stolz M., Stoffler D., Aebi U., Goldsbury C. Monitoring biomolecular interactions by time-lapse atomic force microscopy. J. Struct. Biol. 131:2000;171-180.
60. Bremer, A., Haner, M. & Aebi, U. (1997). Negative staining. In Cell Biology: A Laboratory Hand Book (Celis, J. E., ed.), 2nd edit., vol. 3, pp. 277-284, Academic Press, New York.