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 Computational Biology

Volumn 9, Issue 8, 2013, Pages

  Wu, Chun ^a   Shea, Joan Emma ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CONFORMATIONS; GLYCOPROTEINS; MOLECULAR DYNAMICS; PHYSIOLOGICAL MODELS; PHYSIOLOGY; RATS;

AMINO ACID PEPTIDES; HAIRPIN CONFORMATION; HAIRPIN STRUCTURES; HELIX-COIL; INTRINSICALLY DISORDERED PROTEINS; ISLET AMYLOID POLYPEPTIDES; PEPTIDE HORMONES; STRUCTURAL DIFFERENCES; STRUCTURAL SIMILARITY; STRUCTURE-ACTIVITY RELATIONSHIPS;

PEPTIDES;

AMYLIN; AMYLOID; AMYLOID PRECURSOR PROTEIN; NON AMYLOIDOGENIC ISLET AMYLOID POLYPEPTIDE; OLIGOMER; PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; PATHOLOGY; PHYSIOLOGY; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIMULATION; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

RATTUS; SUIDAE;

EID: 84883418395     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003211     Document Type: Article

References (122)

1. Pittner RA, Albrandt K, Beaumont K, Gaeta LSL, Koda JE, et al. (1994) Molecular Physiology of Amylin. J Cell Biochem 55: 19-28.
2. Young AA, Vine W, Gedulin BR, Pittner R, Janes S, et al. (1996) Preclinical pharmacology of pramlintide in the rat: Comparisons with human and rat amylin. Drug Dev Res 37: 231-248.
3. Kruger DF, Gatcomb PM, Owen SK, (1999) Clinical implications of amylin and amylin deficiency. Diabetes Educ 25: 389-397.
4. Ratner RE, Dickey R, Fineman M, Maggs DG, Shen L, et al. (2004) Amylin replacement with pramlintide as an adjunct to insulin therapy improves long-term glycaemic and weight control in Type 1 diabetes mellitus: a 1-year, randomized controlled trial. Diabet Med 21: 1204-1212.
5. Cooper GJS, Day AJ, Willis AC, Roberts AN, Reid KBM, et al. (1989) Amylin and the Amylin Gene- Structure, Function and Relationship to Islet Amyloid and to Diabetes-Mellitus. Biochim Biophys Acta 1014: 247-258.
6. Wimalawansa SJ, (1997) Amylin, calcitonin gene-related peptide, calcitonin, and adrenomedullin: A peptide superfamily. Crit Rev Neurobiol 11: 167-239.
7. Poyner DR, Sexton PM, Marshall I, Smith DM, Quirion R, et al. (2002) International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev 54: 233-246.
8. Leighton B, Cooper GJS, (1988) Pancreatic Amylin and Calcitonin Gene-Related Peptide Cause Resistance to Insulin in Skeletal-Muscle Invitro. Nature 335: 632-635.
9. Roberts AN, Leighton B, Todd JA, Cockburn D, Schofield PN, et al. (1989) Molecular and Functional-Characterization of Amylin, a Peptide Associated with Type-2 Diabetes-Mellitus. Proc Natl Acad Sci U S A 86: 9662-9666.
10. Rink TJ, Beaumont K, Koda J, Young A, (1993) Structure and Biology of Amylin. Trends Pharmacol Sci 14: 113-118.
11. Westermark P, Wernstedt C, Wilander E, Hayden DW, Obrien TD, 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 U S A 84: 3881-3885.
12. Cooper GJS, Leighton B, Dimitriadis GD, Parrybillings M, Kowalchuk JM, et al. (1988) Amylin Found in Amyloid Deposits in Human Type-2 Diabetes-Mellitus May Be a Hormone That Regulates Glycogen-Metabolism in Skeletal-Muscle. Proc Natl Acad Sci U S A 85: 7763-7766.
13. Hayden MR, Karuparthi PR, Manrique CM, Lastra G, Habibi J, et al. (2007) Longitudinal ultrastructure study of islet amyloid in the HIP rat model of type 2 diabetes mellitus. Exp Biol Med 232: 772-779.
14. Toukatly MN, Jurgens C, Kahn SE, Hull RL, (2010) Human type 2 diabetes is associatied with islet amyloid deposition, decreased β-cell area, and increased β-cell apoptosis. J Investig Med 58: 109.
15. Chakraborty S, Chatterjee B, Basu S, (2012) A mechanistic insight into the amyloidogenic structure of hIAPP peptide revealed from sequence analysis and molecular dynamics simulation. Biophys Chem 168-169: 1-9.
16. Conchillo-Sole O, de Groot NS, Aviles FX, Vendrell J, Daura X, et al. (2007) AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. Bmc Bioinformatics 8: 65.
17. Butler AE, Jang J, Gurlo T, Carty MD, Soeller WC, et al. (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.
18. Matveyenko AV, Butler PC, (2006) Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes. Ilar Journal 47: 225-233.
19. Soeller WC, Janson J, Hart SE, Parker JC, Carty MD, et al. (1998) Islet amyloid-associated diabetes in obese Avy/a mice expressing human islet amyloid polypeptide. Diabetes 47: 743-750.
20. Hull RL, Andrikopoulos S, Verchere CB, Vidal J, Wang F, et al. (2003) Increased dietary fat promotes islet amyloid formation and β-cell secretory dysfunction in a transgenic mouse model of islet amyloid. Diabetes 52: 372-379.
21. Hoppener JWM, Oosterwijk C, Nieuwenhuis MG, Posthuma G, Thijssen JHH, et al. (1999) Extensive islet amyloid formation is induced by development of type II diabetes mellitus and contributes to its progression: pathogenesis of diabetes in a mouse model. Diabetologia 42: 427-434.
22. Watanabe T, Takada M, Hiroshima O, Tachibana S, (1989) Peptide Chemistry; Uski M, editor. Osaka, Japan: Protein Research Foundation pp. 235-238.
23. Cao P, Tu LH, Abedini A, Levsh O, Akter R, et al. (2012) Sensitivity of Amyloid Formation by Human Islet Amyloid Polypeptide to Mutations at Residue 20. J Mol Biol 421: 282-295.
24. Wang M, Yang JP, Wang JY, Wang XJ, (2012) Structural Effects of L16Q, S20G, and L16Q-S20G Mutations on hIAPP: A Comparative Molecular Dynamics Study. Chin J Chem 30: 241-248.
25. Seino S, (2001) S20G mutation of the amylin gene is associated with Type II diabetes in Japanese. Diabetologia 44: 906-909.
26. Ma Z, Westermark GT, Sakagashira S, Sanke T, Gustavsson A, et al. (2001) Enhanced in vitro production of amyloid-like fibrils from mutant (S20G) islet amyloid polypeptide. Amyloid 8: 242-249.
27. Potter KJ, Abedini A, Marek P, Klimek AM, Butterworth S, et al. (2010) Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts. Proc Natl Acad Sci U S A 107: 4305-4310.
28. Udayasankar J, Kodama K, Hull RL, Zraika S, Aston-Mourney K, et al. (2009) Amyloid formation results in recurrence of hyperglycaemia following transplantation of human IAPP transgenic mouse islets. Diabetologia 52: 145-153.
29. Westermark GT, Westermark P, Berne C, Korsgren O, (2008) Widespread amyloid deposition in transplanted human pancreatic islets. N Engl J Med 359: 977-979.
30. Bohman S, Westermark GT, (2012) Extensive amyloid formation in transplanted microencapsulated mouse and human islets. Amyloid 19: 87-93.
31. Lorenzo A, Razzaboni B, Weir GC, Yankner BA, (1994) Pancreatic-Islet Cell Toxicity of Amylin Associated with Type-2 Diabetes-Mellitus. Nature 368: 756-760.
32. Janson J, Ashley RH, Harrison D, McIntyre S, Butler PC, (1999) The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 48: 491-498.
33. Ritzel RA, Butler PC, (2003) Replication increases β-cell vulnerability to human islet amyloid polypeptide-induced apoptosis. Diabetes 52: 1701-1708.
34. Cooper GJS, Aitken JF, Zhang S, (2010) Is type 2 diabetes an amyloidosis and does it really matter (to patients)? Diabetologia 53: 1011-1016.
35. Ritzel RA, Meier JJ, Lin CY, Veldhuis JD, Butler PC, (2007) Human islet amyloid polypeptide oligomers disrupt cell coupling, induce apoptosis, and impair insulin secretion in isolated human islets. Diabetes 56: 65-71.
36. Lin CY, Gurlo T, Kayed R, Butler AE, Haataja L, et al. (2007) Toxic human islet amyloid polypeptide (h-IAPP) oligomers are intracellular, and vaccination to induce anti-toxic oligomer antibodies does not prevent h-IAPP-induced β-cell apoptosis in h-IAPP transgenic mice. Diabetes 56: 1324-1332.
37. Haataja L, Gurlo T, Huang CJ, Butler PC, (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr Rev 29: 303-316.
38. Gurlo T, Ryazantsev S, Huang CJ, Yeh MW, Reber HA, et al. (2010) Evidence for Proteotoxicity in β-Cells in Type 2 Diabetes Toxic Islet Amyloid Polypeptide Oligomers Form Intracellularly in the Secretory Pathway. Am J Pathol 176: 861-869.
39. Rivera JF, Gurlo T, Daval M, Huang CJ, Matveyenko AV, et al. (2011) Human-IAPP disrupts the autophagy/lysosomal pathway in pancreatic β-cells: protective role of p62-positive cytoplasmic inclusions. Cell Death Differ 18: 415-426.
40. Ritzel RA, Jayasinghe S, Hansen JB, Sturis J, Langen R, et al. (2010) β-cell selective K-ATP-channel activation protects β-cells and human islets from human islet amyloid polypeptide induced toxicity. Regul Pept 165: 158-162.
41. Quist A, Doudevski L, Lin H, Azimova R, Ng D, et al. (2005) Amyloid ion channels: A common structural link for protein-misfolding disease. Proc Natl Acad Sci U S A 102: 10427-10432.
42. Seeliger J, Weise K, Opitz N, Winter R, (2012) The Effect of Aβ on IAPP Aggregation in the Presence of an Isolated β-Cell Membrane. J Mol Biol 421: 348-363.
43. Yan LM, Tatarek-Nossol M, Velkova A, Kazantzis A, Kapurniotu A, (2006) Design of a mimic of nonamyloidogenic and bioactive human islet amyloid polypeptide (IAPP) as nanomolar affinity inhibitor of IAPP cytotoxic fibrillogenesis. Proc Natl Acad Sci U S A 103: 2046-2051.
44. Meng FL, Raleigh DP, Abedini A, (2010) Combination of Kinetically Selected Inhibitors in Trans Leads to Highly Effective Inhibition of Amyloid Formation. J Am Chem Soc 132: 14340-14342.
45. Cao P, Meng F, Abedini A, Raleigh DP, (2010) The Ability of Rodent Islet Amyloid Polypeptide To Inhibit Amyloid Formation by Human Islet Amyloid Polypeptide Has Important Implications for the Mechanism of Amyloid Formation and the Design of Inhibitors. Biochemistry (Mosc) 49: 872-881.
46. Abedini A, Meng FL, Raleigh DP, (2007) A single-point mutation converts the highly amyloidogenic human islet amyloid polypeptide into a potent fibrillization inhibitor. J Am Chem Soc 129: 11300-11301.
47. Meng FL, Abedini A, Plesner A, Verchere CB, Raleigh DP, (2010) The Flavanol (-)-Epigallocatechin 3-Gallate Inhibits Amyloid Formation by Islet Amyloid Polypeptide, Disaggregates Amyloid Fibrils, and Protects Cultured Cells against IAPP-Induced Toxicity. Biochemistry (Mosc) 49: 8127-8133.
48. Aitken JF, Loomes KM, Scott DW, Reddy S, Phillips ARJ, et al. (2010) Tetracycline Treatment Retards the Onset and Slows the Progression of Diabetes in Human Amylin/Islet Amyloid Polypeptide Transgenic Mice. Diabetes 59: 161-171.
49. Evers F, Jeworrek C, Tiemeyer S, Weise K, Sellin D, et al. (2009) Elucidating the Mechanism of Lipid Membrane-Induced IAPP Fibrillogenesis and Its Inhibition by the Red Wine Compound Resveratrol: A Synchrotron X-ray Reflectivity Study. J Am Chem Soc 131: 9516-9521.
50. Padrick SB, Miranker AD, (2001) Islet amyloid polypeptide: Identification of long-range contacts and local order on the fibrillogenesis pathway. J Mol Biol 308: 783-794.
51. Higham CE, Jaikaran ETAS, Fraser PE, Gross M, Clark A, (2000) Preparation of synthetic human islet amyloid polypeptide (IAPP) in a stable conformation to enable study of conversion to amyloid-like fibrils. FEBS Lett 470: 55-60.
52. Goldsbury C, Goldie K, Pellaud J, Seelig J, Frey P, et al. (2000) Amyloid fibril formation from full-length and fragments of amylin. J Struct Biol 130: 352-362.
53. Jaikaran ETAS, Higham CE, Serpell LC, Zurdo J, Gross M, et al. (2001) Identification of a novel human islet amyloid polypeptide β-sheet domain and factors influencing fibrillogenesis. J Mol Biol 308: 515-525.
54. Williamson JA, Miranker AD, (2007) Direct detection of transient α-helical states in islet amyloid polypeptide. Protein Sci 16: 110-117.
55. Yonemoto IT, Kroon GJA, Dyson HJ, Balch WE, Kelly JW, (2008) Amylin proprotein processing generates progressively more amyloidogenic peptides that initially sample the helical state. Biochemistry (Mosc) 47: 9900-9910.
56. Nanga RPR, Brender JR, Xu JD, Veglia G, Ramamoorthy A, (2008) Structures of Rat and Human Islet Amyloid Polypeptide IAPP(1-19) in Micelles by NMR Spectroscopy. Biochemistry (Mosc) 47: 12689-12697.
57. Wiltzius J, Sievers S, Sawaya M, 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.
58. Cort JR, Liu ZH, Lee GM, Huggins KNL, Janes S, et al. (2009) Solution state structures of human pancreatic amylin and pramlintide. Protein Eng Desi Select 22: 497-513.
59. Nanga RPR, Brender JR, Xu JD, Hartman K, Subramanian V, et al. (2009) 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.
60. Nanga RPR, Brender JR, Vivekanandan S, Ramamoorthy A, (2011) Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment. Biochim Biophys Acta: Biomembranes 1808: 2337-2342.
61. Kayed R, Bernhagen J, Greenfield N, Sweimeh K, Brunner H, et al. (1999) Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro. J Mol Biol 287: 781-796.
62. Dupuis NF, Wu C, Shea J-E, Bowers MT, (2009) Human Islet Amyloid Polypeptide Monomers Form Ordered β-hairpins: A Possible Direct Amyloidogenic Precursor. J Am Chem Soc 131: 18283-18292.
63. Dupuis NF, Wu C, Shea JE, Bowers MT, (2011) The Amyloid Formation Mechanism in Human IAPP: Dimers Have β-Strand Monomer-Monomer Interfaces. J Am Chem Soc 133: 7240-7243.
64. Reddy AS, Wang L, Lin YS, Ling Y, Chopra M, et al. (2010) Solution Structures of Rat Amylin Peptide: Simulation, Theory, and Experiment. Biophys J 98: 443-451.
65. Reddy AS, Wang L, Singh S, Ling Y, Buchanan L, et al. (2010) Stable and metastable states of human amylin in solution. Biophys J 99: 2208-2216.
66. Murphya RD, Conlona J, Mansoora T, Lucac S, Vaianad SM, et al. (2012) Conformational dynamics of human IAPP monomers. Biophys Chem 167: 1-7.
67. Liang GZ, Zhao J, Yu X, Zheng J, (2013) Comparative Molecular Dynamics Study of Human IAPP and Rat IAPP Oligomers. Biochemistry (Mosc) 52: 1089-1100.
68. Roth JD, Roland BL, Cole RL, Trevaskis JL, Weyer C, et al. (2008) Leptin responsiveness restored by amylin agonism in diet-induced obesity: Evidence from nonclinical and clinical studies. Proc Natl Acad Sci U S A 105: 7257-7262.
69. D'Ursi AM, Armenante MR, Guerrini R, Salvadori S, Sorrentino G, et al. (2004) Solution structure of amyloid β-peptide (25-35) in different media. J Med Chem 47: 4231-4238.
70. Daidone I, Simona F, Roccatano D, Broglia RA, Tiana G, et al. (2004) β-hairpin conformation of fibrillogenic peptides: Structure and α-β transition mechanism revealed by molecular dynamics simulations. Proteins: Struct, Funct, Bioinfo 57: 198-204.
71. Shanmugam G, Polavarapu PL, (2004) Structure of Aβ(25-35) peptide in different environments. Biophys J 87: 622-630.
72. Lazo ND, Grant MA, Condron MC, Rigby AC, Teplow DB, (2005) On the nucleation of amyloid β-protein monomer folding. Protein Sci 14: 1581-1596.
73. Wei GH, Shea JE, (2006) Effects of solvent on the structure of the Alzheimer amyloid-β(25-35) peptide. Biophys J 91: 1638-1647.
74. Baumketner A, Shea JE, (2006) Folding landscapes of the Alzheimer amyloid-β(12-28) peptide. J Mol Biol 362: 567-579.
75. Baumketner A, Bernstein SL, Wyttenbach T, Lazo ND, Teplow DB, et al. (2006) Structure of the 21-30 fragment of amyloid β-protein. Protein Sci 15: 1239-1247.
76. Baumketner A, Shea J-E, (2007) The structure of the Alzheimer amyloid b 10-35 peptide probed through replica-exchange molecular dynamics simulations in explicit solvent. J Mol Biol 366: 275-285.
77. Yang MF, Teplow DB, (2008) Amyloid β-Protein Monomer Folding: Free-Energy Surfaces Reveal Alloform-Specific Differences. J Mol Biol 384: 450-464.
78. Itoh SG, Okamoto Y, (2008) Amyloid-β(29-42) dimer formations studied by a multicanonical-multioverlap molecular dynamics simulation. J Phys Chem B 112: 2767-2770.
79. Cerf E, Sarroukh R, Tamamizu-Kato S, Breydo L, Derclaye S, et al. (2009) Antiparallel β-sheet: a signature structure of the oligomeric amyloid β-peptide. Biochem J 421: 415-423.
80. Lu Y, Derreumaux P, Guo Z, Mousseau N, Wei GH, (2009) Thermodynamics and dynamics of amyloid peptide oligomerization are sequence dependent. Proteins: Struct, Funct, Bioinfo 75: 954-963.
81. Wei GH, Jewett AI, Shea JE, (2010) Structural diversity of dimers of the Alzheimer amyloid-β(25-35) peptide and polymorphism of the resulting fibrils. Phys Chem Chem Phys 12: 3622-3629.
82. Lu Y, Wei GH, Derreumaux P, (2011) Effects of G33A and G33I Mutations on the Structures of Monomer and Dimer of the Amyloid-β Fragment 29-42 by Replica Exchange Molecular Dynamics Simulations. J Phys Chem B 115: 1282-1288.
83. Larini L, Shea JE, (2012) Role of β-Hairpin Formation in Aggregation: The Self-Assembly of the Amyloid-β(25-35) Peptide. Biophys J 103: 576-586.
84. Grabenauer M, Wu C, Soto P, Shea J-E, Bowers MT, (2010) Oligomers of the prion protein fragment 106-126 are likely assembled from β-hairpins in solution, and methionine oxidation inhibits assembly without altering the peptide's monomeric conformation. J Am Chem Soc 132: 532-539.
85. Daidone I, Di Nola A, Smith JC, (2011) Molecular Origin of Gerstmann-Straussler-Scheinker Syndrome: Insight from Computer Simulation of an Amyloidogenic Prion Peptide. Biophys J 100: 3000-3007.
86. Tycko R, (2006) Molecular structure of amyloid fibrils: Insights from solid-state NMR. Q Rev Biophys 39: 1-55.
87. Andreetto E, Yan L, Tatarek-Nossol M, Velkova A, Frank R, et al. (2010) Identification of Hot Regions of the Aβ-IAPP Interaction Interface as High-Affinity Binding Sites in both Cross- and Self-Association. Angew Chem Int Ed 49: 3081-3085.
88. Laghaei R, Mousseau N, Wei GH, (2011) Structure and Thermodynamics of Amylin Dimer Studied by Hamiltonian-Temperature Replica Exchange Molecular Dynamics Simulations. J Phys Chem B 115: 3146-3154.
89. Kapurniotu A, Schmauder A, Tenidis K, (2002) Structure-based design and study of non-amyloidogenic, double N-methylated IAPP amyloid core sequences as inhibitors of IAPP amyloid formation and cytotoxicity. J Mol Biol 315: 339-350.
90. Tatarek-Nossol M, Yan LM, Schmauder A, Tenidis K, Westermark G, et al. (2005) Inhibition of hIAPP amyloid-fibril formation and apoptotic cell death by a designed hIAPP amyloid-core-containing hexapeptide. Chem Biol 12: 797-809.
91. Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, et al. (2007) Intrinsic Disorder and Functional Proteomics. Biophys J 92: 1439-1456.
92. Riddle M, Frias J, Zhang B, Maier H, Brown C, et al. (2007) Pramlintide improved glycemic control and reduced weight in patients with type 2 diabetes using basal insulin. Diabetes Care 30: 2794-2799.
93. Wang L, Middleton CT, Singh S, Reddy AS, Woys AM, et al. (2011) 2DIR Spectroscopy of Human Amylin Fibrils Reflects Stable β-Sheet Structure. J Am Chem Soc 133: 16062-16071.
94. Middleton CT, Marek P, Cao P, Chiu CC, Singh S, et al. (2012) Two-dimensional infrared spectroscopy reveals the complex behaviour of an amyloid fibril inhibitor. Nat Chem 4: 355-360.
95. Milton NGN, Harris JR, (2013) Fibril formation and toxicity of the non-amyloidogenic rat amylin peptide. Micron 44: 246-253.
96. Abedini A, Raleigh D, (2009) A role for helical intermediates in amyloid formation by natively unfolded polypeptides? Phys Biol 6: 015005.
97. Brender JR, Salamekh S, Ramamoorthy A, (2012) Membrane Disruption and Early Events in the Aggregation of the Diabetes Related Peptide IAPP from a Molecular Perspective. Acc Chem Res 45: 454-462.
98. Brender JR, Hartman K, Reid KR, Kennedy RT, Ramamoorthy A, (2008) A Single Mutation in the Nonamyloidogenic Region of Islet Amyloid Polypeptide Greatly Reduces Toxicity. Biochemistry (Mosc) 47: 12680-12688.
99. Jang H, Arce FT, Ramachandran S, Capone R, Azimova R, et al. (2010) Truncated β-amyloid peptide channels provide an alternative mechanism for Alzheimer's Disease and Down syndrome. Proc Natl Acad Sci U S A 107: 6538-6543.
100. Jang H, Arce FT, Ramachandran S, Capone R, Lal R, et al. (2010) β-Barrel Topology of Alzheimer's β-Amyloid Ion Channels. J Mol Biol 404: 917-934.
101. Zhao J, Luo Y, Jang HB, Yu X, Wei GH, et al. (2012) Probing ion channel activity of human islet amyloid polypeptide (amylin). Biochim Biophys Acta: Biomembranes 1818: 3121-3130.
102. Laganowsky A, Liu C, Sawaya MR, Whitelegge JP, Park J, et al. (2012) Atomic View of a Toxic Amyloid Small Oligomer. Science 335: 1228-1231.
103. Sciacca MFM, Brender JR, Lee DK, Ramamoorthy A, (2012) Phosphatidylethanolamine Enhances Amyloid Fiber-Dependent Membrane Fragmentation. Biochemistry (Mosc) 51: 7676-7684.
104. Westermark GT, Westermark P, (2008) Importance of Aggregated Islet Amyloid Polypeptide for the Progressive β-Cell Failure in Type 2 Diabetes and in Transplanted Human Islets. Experimental Diabetes Research pp. 1-2.
105. Zraika S, Hull RL, Verchere CB, Clark A, Potter KJ, et al. (2010) Toxic oligomers and islet β-cell death: guilty by association or convicted by circumstantial evidence? Diabetologia 53: 1046-1056.
106. Hull RL, Westermark GT, Westermark P, Kahn SE, (2004) Islet amyloid: A critical entity in the pathogenesis of type 2 diabetes. J Clin Endocrinol Metab 89: 3629-3643.
107. Obrien TD, Butler PC, Westermark P, Johnson KH, (1993) Islet Amyloid Polypeptide- a Review of Its Biology and Potential Roles in the Pathogenesis of Diabetes-Mellitus. Vet Pathol 30: 317-332.
108. Case DA, Cheatham TE, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
109. Sugita Y, Okamoto Y, (1999) Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 314: 141-151.
110. Gunsteren WFv, Weiner PK, Wilkinson T (1997) Computer simulation of biomolecular systems. Boston: Kluwer Academic Publishers.
111. Shell MS, Ritterson R, Dill KA, (2008) A test on peptide stability of AMBER force fields with implicit solvation. J Phys Chem B 112: 6878-6886.
112. Ozkan SB, Wu GA, Chodera JD, Dill KA, (2007) Protein folding by zipping and assembly. Proc Natl Acad Sci U S A 104: 11987-11992.
113. Wu C, Shea JE, (2010) On the Origins of the Weak Folding Cooperativity of a Designed bba Ultrafast Protein FSD-1. Plos Computational Biology 6: e1000998.
114. Voelz V, Bowman G, Beauchamp K, Pande V, (2010) Molecular Simulation of ab Initio Protein Folding for a Millisecond Folder NTL9(1-39). J Am Chem Soc 132: 1526-1528.
115. Voelz V, Singh V, Wedemeyer W, Lapidus L, Pande V, (2010) Unfolded-State Dynamics and Structure of Protein L Characterized by Simulation and Experiment. J Am Chem Soc 132: 4702-4709.
116. Wang XQ, Wu C, Vu A, Shea JE, Dahlquist FW, (2012) Computational and Experimental Analyses Reveal the Essential Roles of Inter-domain Linkers in the Biological Function of Chemotaxis Histidine Kinase CheA. J Am Chem Soc 134: 16107-16110.
117. Wu C, Murray MM, Bernstein SL, Condron MM, Bitan G, et al. (2009) The structure of Aβ42 C-terminal fragments probed by a combined experimental and theoretical study. J Mol Biol 387: 492-501.
118. Ryckaert JP, Ciccotti G, Berendsen HJC, (1977) Numerical-Integration of Cartesian Equations of Motion of a System with Constraints- Molecular-Dynamics of N-Alkanes. J Comput Phys 23: 327-341.
119. Procacci P, Berne BJ, (1994) Multiple Time-Scale Methods for Constant-Pressure Molecular-Dynamics Simulations of Molecular-Systems. Mol Phys 83: 255-272.
120. Frishman D, Argos P, (1995) Knowledge-based protein secondary structure assignment. Proteins: Struct, Funct, Genet 23: 566-579.
121. Daura X, van Gunsteren WF, Mark AE, (1999) Folding-unfolding thermodynamics of a β-heptapeptide from equilibrium simulations. Proteins: Struct, Funct, Genet 34: 269-280.
122. Kongsted J, Soderhjelm P, Ryde U, (2009) How accurate are continuum solvation models for drug-like molecules? J Comput Aided Mol Des 23: 395-409.