Inhibition of IAPP aggregation by insulin depends on the insulin oligomeric state regulated by zinc ion concentration

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Nedumpully Govindan, Praveen ^a   Ding, Feng ^a  

^a CLEMSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLIN; INSULIN; PROTEIN BINDING; ZINC;

ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEINOSIS; RAT;

ANIMALS; HUMANS; INSULIN; ISLET AMYLOID POLYPEPTIDE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; RATS; ZINC;

EID: 84951305423     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08240     Document Type: Article

References (52)

1. Westermark, P., Andersson, A.&Westermark, G. T. Is aggregated IAPP a cause of beta-cell failure in transplanted human pancreatic islets? Curr. Diab. Rep. 5, 184-188 (2005).
2. Götz, J., Ittner, L. M. & Lim, Y.-A. Common features between diabetes mellitus and Alzheimer's disease. Cell. Mol. Life Sci. 66, 1321-1325 (2009).
3. Konarkowska, B., Aitken, J. F., Kistler, J., Zhang, S. & Cooper, G. J. S. The aggregation potential of human amylin determines its cytotoxicity towards islet bcells. FEBS J. 273, 3614-3624 (2006).
4. Hebda, J. A.&Miranker, A. D. The Interplay of Catalysis and Toxicity by Amyloid Intermediates on Lipid Bilayers: Insights from Type II Diabetes. Annu. Rev. Biophys. 38, 125-152 (2009).
5. Sladek, R. et al. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445, 881-885 (2007).
6. Flannick, J. et al. Loss-of-function mutations in SLC30A8 protect against type 2 diabetes. Nat. Genet. 46, 357-363 (2014).
7. Ritzel, R. A., Meier, J. J., Lin, C.-Y., Veldhuis, J. D. & Butler, P. C. Human Islet Amyloid Polypeptide Oligomers Disrupt Cell Coupling, Induce Apoptosis, and Impair Insulin Secretion in Isolated Human Islets. Diabetes 56, 65-71 (2007).
8. Sakagashira, S. et al. S20G Mutant Amylin Exhibits Increased in Vitro Amyloidogenicity and Increased Intracellular Cytotoxicity Compared to Wild-Type Amylin. Am. J. Pathol. 157, 2101-2109 (2000).
9. Janson, J., Ashley, R. H.,Harrison, D.,McIntyre, S. & Butler, P. C. The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediatesized toxic amyloid particles. Diabetes 48, 491-498 (1999).
10. Chakraborty, S., Chatterjee, B. & Basu, S. A mechanistic insight into the amyloidogenic structure of hIAPP peptide revealed from sequence analysis and molecular dynamics simulation. Biophys. Chem. 168-169, 1-9 (2012).
11. Abedini, A., Meng, F. & Raleigh, D. P. A Single-Point Mutation Converts the Highly Amyloidogenic Human Islet Amyloid Polypeptide into a Potent Fibrillization Inhibitor. J. Am. Chem. Soc. 129, 11300-11301 (2007).
12. Seino, S. S20G mutation of the amylin gene is associated with Type II diabetes in Japanese. Study Group of Comprehensive Analysis of Genetic Factors in Diabetes Mellitus. Diabetologia 44, 906-909 (2001).
13. Padrick, S. B. &Miranker, A. D. Islet Amyloid: Phase Partitioning and Secondary Nucleation Are Central to the Mechanism of Fibrillogenesis. Biochemistry (Mosc.) 41, 4694-4703 (2002).
14. Hutton, J. C. The insulin secretory granule. Diabetologia 32, 271-281 (1989).
15. Jha, S. et al. pH Dependence of Amylin Fibrillization. Biochemistry (Mosc.) 53, 300-310 (2014).
16. Hull, R. L., Westermark, G. T., Westermark, P. & Kahn, S. E. Islet Amyloid: A Critical Entity in the Pathogenesis of Type 2 Diabetes. J. Clin. Endocrinol. Metab. 89, 3629-3643 (2004).
17. Westermark, P., Li, Z.-C., Westermark, G. T., Leckström, A. & Steiner, D. F. Effects of beta cell granule components on human islet amyloid polypeptide fibril formation. FEBS Lett. 379, 203-206 (1996).
18. Larson, J. L.&Miranker, A. D. TheMechanism of Insulin Action on Islet Amyloid Polypeptide Fiber Formation. J. Mol. Biol. 335, 221-231 (2004).
19. Knight, J. D.,Williamson, J. A.&Miranker, A. D. Interaction of membrane-bound islet amyloid polypeptide with soluble and crystalline insulin. Protein Sci. 17, 1850-1856 (2008).
20. Wei, L. et al. Residual Structure in Islet Amyloid Polypeptide Mediates Its Interactions with Soluble Insulin. Biochemistry (Mosc.) 48, 2368-2376 (2009).
21. Jiang, P.,Wei, L., Pervushin, K. & Mu, Y. pH-Dependent Interactions of Human Islet Amyloid Polypeptide Segments with Insulin Studied by Replica Exchange Molecular Dynamics Simulations. J. Phys. Chem. B 114, 10176-10183 (2010).
22. Chimienti, F., Devergnas, S., Favier, A. & Seve, M. Identification and Cloning of a b-Cell-Specific Zinc Transporter, ZnT-8, Localized Into Insulin Secretory Granules. Diabetes 53, 2330-2337 (2004).
23. Nicolson, T. J. et al. Insulin Storage and Glucose Homeostasis in Mice Null for the Granule Zinc Transporter ZnT8 and Studies of the Type 2 Diabetes-Associated Variants. Diabetes 58, 2070-2083 (2009).
24. Lemaire, K. et al. Insulin crystallization depends on zinc transporter ZnT8 expression, but is not required for normal glucose homeostasis in mice. Proc. Natl. Acad. Sci. 106, 14872-14877 (2009).
25. Pound, L. D. et al. Deletion of the mouse Slc30a8 gene encoding zinc transporter-8 results in impaired insulin secretion. Biochem. J. 421, 371-376 (2009).
26. Dunn, M. F. Zinc-Ligand Interactions Modulate Assembly and Stability of the Insulin Hexamer-A Review. Biometals 18, 295-303 (2005).
27. Miller, C., Zerze, G. H. & Mittal, J. Molecular Simulations Indicate Marked Differences in the Structure of Amylin Mutants, Correlated with Known Aggregation Propensity. J. Phys. Chem. B 117, 16066-16075 (2013).
28. Singh, S., Chiu, C., Reddy, A. S. & Pablo, J. J. de. a-helix to b-hairpin transition of human amylin monomer. J. Chem. Phys. 138, 155101 (2013).
29. Dupuis, N. F., Wu, C., Shea, J.-E. & Bowers, M. T. The Amyloid Formation Mechanism in Human IAPP: Dimers Have b-Strand Monomer2Monomer Interfaces. J. Am. Chem. Soc. 133, 7240-7243 (2011).
30. Laghaei, R., Mousseau, N. & Wei, G. Structure and Thermodynamics of Amylin Dimer Studied by Hamiltonian-Temperature Replica Exchange Molecular Dynamics Simulations. J. Phys. Chem. B 115, 3146-3154 (2011).
31. Wu, C. & Shea, J.-E. Structural Similarities and Differences between Amyloidogenic and Non-Amyloidogenic Islet Amyloid Polypeptide (IAPP) Sequences and Implications for the Dual Physiological and Pathological Activities of These Peptides. PLoS Comput Biol 9, e1003211 (2013).
32. Susa, A. C. et al. Defining the Molecular Basis of Amyloid Inhibitors: Human Islet Amyloid Polypeptide-Insulin Interactions. J. Am. Chem. Soc. 136, 12912-12919 (2014).
33. Ding, F.&Dokholyan,N.V. Emergence of Protein Fold Families through Rational Design. PLoS Comput Biol 2, e85 (2006).
34. Shirvanyants, D., Ding, F., Tsao, D., Ramachandran, S. & Dokholyan, N. V. Discrete Molecular Dynamics: An Efficient And Versatile Simulation Method For Fine Protein Characterization. J. Phys. Chem. B 116, 8375-8382 (2012).
35. Ding, F., Tsao, D., Nie, H. & Dokholyan, N. V. Ab Initio Folding of Proteins with All-Atom Discrete Molecular Dynamics. Structure 16, 1010-1018 (2008).
36. Dagliyan, O., Proctor, E. A., D'Auria, K. M., Ding, F. & Dokholyan, N. V. Structural and Dynamic Determinants of Protein-Peptide Recognition. Structure 19, 1837-1845 (2011).
37. Kimura, S., Caldarini, M., Broglia, R. A., Dokholyan, N. V. & Tiana, G. The maturation of HIV-1 protease precursor studied by discrete molecular dynamics. Proteins Struct. Funct. Bioinforma. 82, 633-639 (2014).
38. Nanga, R. P. R., Brender, J. R., Vivekanandan, S. & Ramamoorthy, A. Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment. Biochim. Biophys. Acta BBA-Biomembr. 1808, 2337-2342 (2011).
39. Kumar, S., Rosenberg, J. M., Bouzida, D., Swendsen, R. H. & Kollman, P. A. THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13, 1011-1021 (1992).
40. Nanga, R. P. R. et al. Three-Dimensional Structure and Orientation of Rat Islet Amyloid Polypeptide Protein in a Membrane Environment by Solution NMR Spectroscopy. J. Am. Chem. Soc. 131, 8252-8261 (2009).
41. Wiltzius, J. J. W., Sievers, S. A., Sawaya, M. R. &Eisenberg, D. Atomic structures of IAPP (amylin) fusions suggest amechanism for fibrillation and the role of insulin in the process. Protein Sci. 18, 1521-1530 (2009).
42. Barton, G. J. OC-A cluster analysis program. (University of Dundee, UK, 1993).
43. Maurer-Stroh, S. et al. Exploring the sequence determinants of amyloid structure using position-specific scoring matrices. Nat. Methods 7, 237-242 (2010).
44. Luca, S., Yau, W.-M., Leapman, R. & Tycko, R. Peptide Conformation and Supramolecular Organization in Amylin Fibrils: Constraints from Solid-State NMR. Biochemistry (Mosc.) 46, 13505-13522 (2007).
45. Brender, J. R. et al. Role of Zinc in Human Islet Amyloid Polypeptide Aggregation. J. Am. Chem. Soc. 132, 8973-8983 (2010).
46. Salamekh, S. et al. A Two-Site Mechanism for the Inhibition of IAPP Amyloidogenesis by Zinc. J. Mol. Biol. 410, 294-306 (2011).
47. Ciszak, E. & Smith, G. D. Crystallographic Evidence for Dual Coordination Around Zinc in the T3R3 Human Insulin Hexamer. Biochemistry (Mosc.) 33, 1512-1517 (1994).
48. Lazaridis, T. & Karplus, M. Effective energy function for proteins in solution. Proteins Struct. Funct. Bioinforma. 35, 133-152 (1999).
49. Ding, F., Borreguero, J. M., Buldyrey, S. V., Stanley, H. E. & Dokholyan, N. V. Mechanism for the a-helix to b-hairpin transition. Proteins Struct. Funct. Bioinforma. 53, 220-228 (2003).
50. Ding, F., Furukawa, Y., Nukina, N. & Dokholyan, N. V. Local unfolding of Cu, Zn superoxide dismutase monomer determines the morphology of fibrillar aggregates. J. Mol. Biol. 421, 548-560 (2012).
51. Andersen, H. C. Molecular dynamics simulations at constant pressure and/or temperature. J. Chem. Phys. 72, 2384-2393 (1980).
52. Sugita, Y. & Okamoto, Y. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 314, 141-151 (1999).