Selection for nonamyloidogenic mutants of islet Amyloid Polypeptide (IAPP) identifies an extended region for amyloidogenicity

Biochemistry

Volumn 49, Issue 36, 2010, Pages 7783-7789

  Fox, Ayano ^a   Snollaerts, Thibaut ^a   Errecart Casanova, Camille ^a   Calciano, Anastasia ^a   Nogaj, Luiza A ^b   Moffet, David A ^a  

^a LOYOLA MARYMOUNT UNIVERSITY   (United States)

^b Loyola University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; FLUORESCENCE; GLYCOPROTEINS; OLIGOMERS;

AMYLOIDOGENICITY; DOUBLE MUTATION; ENHANCED GREEN FLUORESCENT PROTEIN; FUSION PROTEINS; REPORTER PROTEIN; SINGLE MUTATION; TYPE II; WILD TYPES;

PROTEINS;

AMYLIN; ENHANCED GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MUTANT PROTEIN; PEPTIDE LIBRARY; AMYLOID; GREEN FLUORESCENT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; MUTATIONAL ANALYSIS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; WILD TYPE; AMINO ACID SEQUENCE; ATOMIC FORCE MICROSCOPY; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE;

ESCHERICHIA COLI;

AMINO ACID SEQUENCE; AMYLOID; GREEN FLUORESCENT PROTEINS; HUMANS; ISLET AMYLOID POLYPEPTIDE; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 77956395740     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100337p     Document Type: Article

References (42)

1. Apostolidou, M., Jayasinghe, S. A., and Langen, R. (2008) Structure of alpha-helical membrane-bound human islet amyloid polypeptide and its implications for membrane-mediated misfolding J. Biol. Chem. 283, 17205-17210
2. 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
3. Kahn, S. E., Andrikopoulos, S., and Verchere, C. B. (1999) Islet amyloid: A long-recognized but underappreciated pathological feature of type 2 diabetes Diabetes 48, 241-253
4. Ritzel, R. A., Meier, J. J., Lin, C. Y., Veldhuis, J. D., and Butler, P. C. (2007) Human islet amyloid polypeptide oligomers disrupt cell coupling, induce apoptosis, and impair insulin secretion in isolated human islets Diabetes 56, 65-71
5. Matveyenko, A. V. and Butler, P. C. (2006) Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes ILAR J. 47, 225-233
6. 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. U.S.A. 87, 5036-5040
7. Nanga, R. P., Brender, J. R., Xu, J., Veglia, G., and Ramamoorthy, A. (2008) Structures of rat and human islet amyloid polypeptide IAPP(1-19) in micelles by NMR spectroscopy Biochemistry 47, 12689-12697
8. Gazit, E. (2005) Mechanisms of amyloid fibril self-assembly and inhibition FEBS J. 272, 5971-5978
9. 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
10. Marek, P., Abedini, A., Song, B. B., Kanungo, M., Johnson, M. E., Gupta, R., Zaman, W., Wong, S. S., and Raleigh, D. P. (2007) Aromatic interactions are not required for amyloid fibril formation by islet amyloid polypeptide but do influence the rate of fibril formation and fibril morphology Biochemistry 46, 3255-3261
11. Abedini, A., Meng, F. L., and Raleigh, D. P. (2007) A single-point mutation converts the highly amyloidogenic human islet amyloid polypeptide into a potent fibrillization inhibitor J. Am. Chem. Soc. 129, 11300
12. Abedini, A. and Raleigh, D. P. (2005) The role of His-18 in amyloid formation by human islet amyloid polypeptide Biochemistry 44, 16284-16291
13. Koo, B. W., Hebda, J. A., and Miranker, A. D. (2008) Amide inequivalence in the fibrillar assembly of islet amyloid polypeptide Protein Eng., Des. Sel. 21, 147-154
14. Scrocchi, L. A., Chen, Y., Waschuk, S., Wang, F., Cheung, S., Darabie, A. A., McLaurin, J., and Fraser, P. E. (2002) Design of peptide-based inhibitors of human islet amyloid polypeptide fibrillogenesis J. Mol. Biol. 318, 697-706
15. Tracz, S. M., Abedini, A., Driscoll, M., and Raleigh, D. P. (2004) Role of aromatic interactions in amyloid formation by peptides derived from human Amylin Biochemistry 43, 15901-15908
16. Waldo, G. S., Standish, B. M., Berendzen, J., and Terwilliger, T. C. (1999) Rapid protein-folding assay using green fluorescent protein Nat. Biotechnol. 17, 691-695
17. Baine, M., Georgie, D. S., Shiferraw, E. Z., Nguyen, T. P. T., Nogaj, L. A., and Moffet, D. A. (2009) Inhibition of A beta 42 aggregation using peptides selected from combinatorial libraries J.Pept. Sci. 15, 499-503
18. Sharma, R. C. and Schimke, R. T. (1996) Preparation of electro-competent E. coli using salt-free growth medium BioTechniques 20, 42-44
19. de Groot, N. S., Aviles, F. X., Vendrell, J., and Ventura, S. (2006) Mutagenesis of the central hydrophobic cluster in A beta 42 Alzheimers pepticle - Side-chain properties correlate with aggregation propensities FEBS J. 273, 658-668
20. Kim, W., Kim, Y., Min, J., Kim, D. J., Chang, Y. T., and Hecht, M. H. (2006) A high-throughput screen for compounds that inhibit aggregation of the Alzheimers peptide ACS Chem. Biol. 1, 461-469
21. Wurth, C., Guimard, N. K., and Hecht, M. H. (2002) Mutations that reduce aggregation of the Alzheimers Abeta42 peptide: An unbiased search for the sequence determinants of Abeta amyloidogenesis J. Mol. Biol. 319, 1279-1290
22. Wurth, C., Kim, W., and Hecht, M. H. (2006) Combinatorial approaches to probe the sequence determinants of protein aggregation and amyloidogenicity Protein Pept. Lett. 13, 279-286
23. Kim, W. and Hecht, M. H. (2006) Generic hydrophobic residues are sufficient to promote aggregation of the Alzheimers A beta 42 peptide Proc. Natl. Acad. Sci. U.S.A. 103, 15824-15829
24. Kim, W. and Hecht, M. H. (2008) Mutations enhance the aggregation propensity of the Alzheimers A beta peptide J. Mol. Biol. 377, 565-574
25. Yamin, G., Ruchala, P., and Teplow, D. B. (2009) A peptide hairpin inhibitor of amyloid beta-protein oligomerization and fibrillogenesis Biochemistry 48, 11329-11331
26. Ahn, J. S., Lee, J. H., Kim, J. H., and Paik, S. R. (2007) Novel method for quantitative determination of amyloid fibrils of alpha-synuclein and amyloid beta/A4 protein by using resveratrol Anal. Biochem. 367, 259-265
27. Gilead, S. and Gazit, E. (2008) The role of the 14-20 domain of the islet amyloid polypeptide in amyloid formation Exp. Diabetes Res. 2008, 256954
28. Gilead, S., Wolfenson, H., and Gazit, E. (2006) Molecular mapping of the recognition interface between the islet amyloid polypeptide and insulin Angew. Chem., Int. Ed. Engl. 45, 6476-6480
29. 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
30. Wiltzius, J. J. W., Sievers, S. A., Sawaya, M. R., and Eisenberg, D. (2009) Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process Protein Sci. 18, 1521-1530
31. Williamson, J. A., Loria, J. P., and Miranker, A. D. (2009) Helix stabilization precedes aqueous and bilayer-catalyzed fiber formation in islet amyloid polypeptide J. Mol. Biol. 393, 383-396
32. Williamson, J. A. and Miranker, A. D. (2007) Direct detection of transient alpha-helical states in islet amyloid polypeptide Protein Sci. 16, 110-117
33. Yonemoto, I. T., Kroon, G. J., Dyson, H. J., Balch, W. E., and Kelly, J. W. (2008) Amylin proprotein processing generates progressively more amyloidogenic peptides that initially sample the helical state Biochemistry 47, 9900-9910
34. Sakagashira, S., Hiddinga, H. J., Tateishi, K., Sanke, T., Hanabusa, T., Nanjo, K., and Eberhardt, N. L. (2000) S20G mutant amylin exhibits increased in vitro amyloidogenicity and increased intracellular cytotoxicity compared to wild-type amylin Am. J. Pathol. 157, 2101-2109
35. Hortschansky, P., Schroeckh, V., Christopeit, T., Zandomeneghi, G., and Fandrich, M. (2005) The aggregation kinetics of Alzheimers beta-amyloid peptide is controlled by stochastic nucleation Protein Sci. 14, 1753-1759
36. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 424, 805-808
37. Nielsen, L., Khurana, R., Coats, A., Frokjaer, S., Brange, J., Vyas, S., Uversky, V. N., and Fink, A. L. (2001) Effect of environmental factors on the kinetics of insulin fibril formation: Elucidation of the molecular mechanism Biochemistry 40, 6036-6046
38. Fernandez-Escamilla, A. M., Rousseau, F., Schymkowitz, J., and Serrano, L. (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins Nat. Biotechnol. 22, 1302-1306
39. Linding, R., Schymkowitz, J., Rousseau, F., Diella, F., and Serrano, L. (2004) A comparative study of the relationship between protein structure and beta-aggregation in globular and intrinsically disordered proteins J. Mol. Biol. 342, 345-353
40. Rousseau, F., Schymkowitz, J., and Serrano, L. (2006) Protein aggregation and amyloidosis: Confusion of the kinds? Curr. Opin. Struct. Biol. 16, 118-126
41. Koo, B. W. and Miranker, A. D. (2005) Contribution of the intrinsic disulfide to the assembly mechanism of islet amyloid Protein Sci. 14, 231-239
42. Chang, H. C., Kaiser, C. M., Hartl, F. U., and Barral, J. M. (2005) De novo folding of GFP fusion proteins: High efficiency in eukaryotes but not in bacteria J. Mol. Biol. 353, 397-409