Evidence for a partially structured state of the amylin monomer

Biophysical Journal

Volumn 97, Issue 11, 2009, Pages 2948-2957

  Vaiana, Sara M ^a,c   Best, Robert B ^b   Yau, Wai Ming ^a   Eaton, William A ^a   Hofrichter, James ^a  

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

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLIN; CALCITONIN RECEPTOR; DISULFIDE; GUANIDINE; TRYPTOPHAN;

ARTICLE; HYDROGEN BOND; HYDROPHILICITY; MOLECULAR DYNAMICS; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN STRUCTURE; SIMULATION;

RATTUS;

EID: 72549109010     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.08.041     Document Type: Article

References (47)

1. Westermark, P., C. Wernstedt, E. Wilander, D. W. Hayden, T. D. Obrien, et al. 1987. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. USA. 84:3881-3885.
2. Cooper, G. J. S., A. C. Willis, A. Clark, R. C. Turner, R. B. Sim, et al. 1987. Purification and characterization of a peptide from amyloid-rich pancreases of type-2 diabetic patients. Proc. Natl. Acad. Sci. USA. 84:8628-8632.
3. Jayasinghe, S. A., and R. Langen. 2005. Lipid membranes modulate the structure of islet amyloid polypeptide. Biochemistry. 44:12113-12119.
4. Kayed, R., J. Bernhagen, N. Greenfield, K. Sweimeh, H. Brunner, et al. 1999. Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro. J. Mol. Biol. 287:781-796.
5. Hoppener, J. W. M., and C. J. M. Lips. 2006. Role of islet amyloid in type 2 diabetes mellitus. Int. J. Biochem. Cell Biol. 38:726-736.
6. Lansbury, P. T., and H. A. Lashuel. 2006. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature. 443:774-779.
7. Lorenzo, A., B. Razzaboni, G. C. Weir, and B. A. Yankner. 1994. Pancreatic-islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature. 368:756-760. (Pubitemid 24153418)
8. Kapurniotu, A. 2001. Arnyloidogenicity and cytotoxicity of islet amyloid polypeptide. Biopolymers. 60:438-459. (Pubitemid 35000911)
9. Jaikaran, E. T. A. S., and A. Clark. 2001. Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochim. Biophys. Acta. 1537:179-203.
10. Hay, D. L., G. Christopoulos, A. Christopoulos, D. R. Poyner, and P. M. Sexton. 2005. Pharmacological discrimination of calcitonin receptor: receptor activity-modifying protein complexes. Mol. Pharmacol. 67:1655-1665.
11. Hay, D. L., G. Christopoulos, A. Christopoulos, and P. M. Sexton. 2004. Amylin receptors: molecular composition and pharmacology. Biochem. Soc. Trans. 32:865-867.
12. Conner, A. C., J. Simms, J. Barwell, M. Wheatley, and D. R. Poyner. 2007. Ligand binding and activation of the CGRP receptor. Biochem. Soc. Trans. 35:729-732.
13. Williamson, J. A., and A. D. Miranker. 2007. Direct detection of transient α-helical states in islet amyloid polypeptide. Protein Sci. 16: 110-117.
14. Yonemoto, I. T., G. J. A. Kroon, H. J. Dyson, W. E. Balch, and J. W. Kelly. 2008. Amylin proprotein processing generates progressively more amyloidogenic peptides that initially sample the helical state. Biochemistry. 47:9900-9910.
15. Jayasinghe, S. A., and R. Langen. 2007. Membrane interaction of islet amyloid polypeptide. Biochim. Biophys. Acta. 1768:2002-2009.
16. Nanga, R. P. R., J. R. Brender, J. Xu, G. Veglia, and A. Ramamoorthy. 2008. Structures of rat and human islet amyloid polypeptide IAPP(1-19) in micelles by NMR spectroscopy. Biochemistry. 47:12689-12697.
17. Knight, J. D., and A. D. Miranker. 2004. Phospholipid catalysis of diabetic amyloid assembly. J. Mol. Biol. 341:1175-1187.
18. Knight, J. D., J. A. Hebda, and A. D. Miranker. 2006. Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide. Biochemistry. 45:9496-9508.
19. Engel, M. F. M., L. Khemtemourian, C. C. Kleijer, H. J. D. Meeldijk, J. Jacobs, et al. 2008. Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane. Proc. Natl. Acad. Sci. USA. 105:6033-6038.
20. Brender, J. R., K. Hartman, K. R. Reid, R. T. Kennedy, and A. Ramamoorthy. 2008. A single mutation in the nonamyloidogenic region of islet amyloid polypeptide greatly reduces toxicity. Biochemistry. 47:12680-12688.
21. Luca, S., W. M. Yau, R. Leapman, and R. Tycko. 2007. Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR. Biochemistry. 46:13505-13522. (Pubitemid 350209947)
22. Vaiana, S. M., R. Ghirlando, W. M. Yau, W. A. Eaton, and J. Hofrichter. 2008. Sedimentation studies on human amylin fail to detect low-molecular-weight oligomers. Biophys. J. 94:L45-L47.
23. Buscaglia, M., J. Kubelka, W. A. Eaton, and J. Hofrichter. 2005. Determination of ultrafast protein folding rates from loop formation dynamics. J. Mol. Biol. 347:657-664.
24. Buscaglia, M., B. Schuler, L. J. Lapidus, W. A. Eaton, and J. Hofrichter. 2003. Kinetics of intramolecular contact formation in a denatured protein. J. Mol. Biol. 332:9-12.
25. Lapidus, L. J., W. A. Eaton, and J. Hofrichter. 2000. Measuring the rate of intramolecular contact formation in polypeptides. Proc. Natl. Acad. Sci. USA. 97:7220-7225.
26. Lapidus, L. J., W. A. Eaton, and J. Hofrichter. 2002. Measuring dynamic flexibility of the coil state of a helix-forming peptide. J. Mol. Biol. 319:19-25.
27. Buscaglia, M., L. J. Lapidus, W. A. Eaton, and J. Hofrichter. 2006. Effects of denaturants on the dynamics of loop formation in polypeptides. Biophys. J. 91:276-288. (Pubitemid 44018055)
28. Lapidus, L. J., P. J. Steinbach, W. A. Eaton, A. Szabo, and J. Hofrichter. 2002. Effects of chain stiffness on the dynamics of loop formation in polypeptides. Appendix: testing a 1-dimensional diffusion model for peptide dynamics. J. Phys. Chem. B. 106:11628-11640.
29. Lapidus, L. J., W. A. Eaton, and J. Hofrichter. 2001. Dynamics of intramolecular contact formation in polypeptides: distance dependence of quenching rates in a room-temperature glass. Phys. Rev. Lett. 87:258101.
30. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
31. Sorin, E. J., and V. S. Pande. 2005. Exploring the helix-coil transition via all-atom equilibrium ensemble simulations. Biophys. J. 88:2472-2493.
32. Jorgensen, W. L., J. Chandrasekhar, and J. D. Madura. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
33. Hoover, W. G. 1985. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A. 31:1695-1697.
34. Nosé, S. 1984. A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys. 52:255-268.
35. Parinello, M., and A. Rahman. 1981. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52:7182-7190.
36. Gonnelli, M., and G. B. Strambini. 1995. Phosphorescence lifetime of tryptophan in proteins. Biochemistry. 34:13847-13857.
37. Moglich, A., K. Joder, and T. Kiefhaber. 2006. End-to-end distance distributions and intrachain diffusion constants in unfolded polypeptide chains indicate intramolecular hydrogen bond formation. Proc. Natl. Acad. Sci. USA. 103:12394-12399.
38. Moglich, A., F. Krieger, and T. Kiefhaber. 2005. Molecular basis for the effect of urea and guanidinium chloride on the dynamics of unfolded polypeptide chains. J. Mol. Biol. 345:153-162.
39. Soong, R., J. R. Brender, P. M. Macdonald, and A. Ramamoorthy. 2009. Association of highly compact type II diabetes related islet amyloid polypeptide intermediate species at physiological temperature revealed by diffusion NMR spectroscopy. J. Am. Chem. Soc. 131:7079-7085.
40. Bolen, D. W., and G. D. Rose. 2008. Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu. Rev. Biochem. 77:339-362.
41. Fiebig, K. M., and K. A. Dill. 1993. Protein core assembly processes. J. Chem. Phys. 98:3475-3487.
42. Dill, K. A., K. M. Fiebig, and H. S. Chan. 1993. Cooperativity in protein-folding kinetics. Proc. Natl. Acad. Sci. USA. 90:1942-1946.
43. Henry, E. R., and W. A. Eaton. 2004. Combinatorial modeling of protein folding kinetics: free energy profiles and rates. Chem. Phys. 307:163-185.
44. Koo, B. W., and A. D. Miranker. 2005. Contribution of the intrinsic disulfide to the assembly mechanism of islet amyloid. Protein Sci. 14:231-239.
45. Thirumalai, D., D. K. Klimov, and R. I. Dima. 2003. Emerging ideas on the molecular basis of protein and peptide aggregation. Curr. Opin. Struct. Biol. 13:146-159.
46. Dima, R. I., and D. Thirumalai. 2002. Exploring protein aggregation and self-propagation using lattice models: phase diagram and kinetics. Protein Sci. 11:1036-1049.
47. 28 salt bridge on the conformational fluctuations of monomers and dimers of Aβ peptides with implications for rates of fibril formation. J. Phys. Chem. B. 113:1162-1172.