Probing ion channel activity of human islet amyloid polypeptide (amylin)

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 12, 2012, Pages 3121-3130

  Zhao, Jun ^a   Luo, Yin ^a,b,c   Jang, Hyunbum ^d   Yu, Xiang ^a   Wei, Guanghong ^b,c   Nussinov, Ruth ^d,e   Zheng, Jie ^a  

^a The University of Akron   (United States)

^b and Key Laboratory of Micro and Nano Photonic Structures   (China)

^c FUDAN UNIVERSITY   (China)

^d NATIONAL CANCER INSTITUTE   (United States)

^e TEL AVIV UNIVERSITY   (Israel)

Author keywords

Directional permeability; hIAPP; Ion channel; Molecular dynamic

Indexed keywords

AMYLIN; AMYLOID BETA PROTEIN; BETA 2 MICROGLOBULIN; CALCIUM ION; CHLORIDE ION; DIOLEOYLPHOSPHATIDYLCHOLINE; POLYPEPTIDE ANTIBIOTIC AGENT; POTASSIUM ION; SODIUM ION;

ARTICLE; ATOMIC FORCE MICROSCOPY; BETA SHEET; BILAYER MEMBRANE; CHANNEL GATING; COMPUTER PROGRAM; CONFORMATION; HISTOGRAM; ION CONDUCTANCE; MEMBRANE PERMEABILITY; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE;

AMYLOID; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; HUMANS; INSULIN-SECRETING CELLS; ION CHANNELS; ISLET AMYLOID POLYPEPTIDE; LIPID BILAYERS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, TERTIARY;

EID: 84865652060     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.08.012     Document Type: Article

References (63)

1. L. Khemtémourian, J.A. Killian, J.W.M. Höppener, and M.F.M. Engel Recent insights in islet amyloid polypeptide-induced membrane disruption and its role in beta-cell death in type 2 diabetes mellitus Exp. Diabetes Res. 2008 2008 1 9
2. B. Åkesson, G. Panagiotidis, P. Westermark, and I. Lundquist Islet amyloid polypeptide inhibits glucagon release and exerts a dual action on insulin release from isolated islets Regul. Pept. 111 2003 55 60
3. T.K. Reda, A. Geliebter, and F.X. Pi-Sunyer Amylin, food Intake, and obesity Obesity 10 2002 1087 1091
4. L. Haataja, T. Gurlo, C.J. Huang, and P.C. Butler Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis Endocr. Rev. 29 2008 303 316
5. S. Luca, W.-M. Yau, R. Leapman, and R. Tycko Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR Biochemistry 46 2007 13505 13522
6. A. Quist, I. Doudevski, H. Lin, R. Azimova, D. Ng, B. Frangione, B. Kagan, J. Ghiso, and R. Lal Amyloid ion channels: a common structural link for protein-misfolding disease PNAS 102 2005 10427 10432
7. J. Zhao, X. Yu, G. Liang, and J. Zheng Heterogeneous triangular structures of human islet amyloid polypeptide (amylin) with internal hydrophobic cavity and external wrapping morphology reveal the polymorphic nature of amyloid fibrils Biomacromolecules 12 2011 1781 1794
8. J. Zhao, X. Yu, G. Liang, and J. Zheng Structural polymorphism of human islet amyloid polypeptide (hIAPP) oligomers highlights the importance of interfacial residue interactions Biomacromolecules 12 2011 210 220
9. J.R. Brender, S. Salamekh, and A. Ramamoorthy Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective Acc. Chem. Res. 45 2012 454 462
10. J.A. Hebda, and A.D. Miranker The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes Annu. Rev. Biophys. 38 2009 125 152
11. D.R. Poyner, P.M. Sexton, I. Marshall, D.M. Smith, R. Quirion, W. Born, R. Muff, J.A. Fischer, and S.M. Foord International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors Pharmacol. Rev. 54 2002 233 246
12. G. Christopoulos, K.J. Perry, M. Morfis, N. Tilakaratne, Y.Y. Gao, N.J. Fraser, M.J. Main, S.M. Foord, and P.M. Sexton Multiple amylin receptors arise from receptor activity-modifying protein interaction with the calcitonin receptor gene product Mol. Pharmacol. 56 1999 235 242
13. J.H. Jhamandas, and D. MacTavish beta-Amyloid protein (A beta) and human amylin regulation of apoptotic genes occurs through the amylin receptor Apoptosis 17 2012 37 47
14. S. Casas, A. Novials, F. Reimann, R. Gomis, and F.M. Gribble Calcium elevation in mouse pancreatic beta cells evoked by extracellular human islet amyloid polypeptide involves activation of the mechanosensitive ion channel TRPV4 Diabetologia 51 2008 2252 2262
15. J.R. Brender, U.H.N. Dürr, D. Heyl, M.B. Budarapu, and A. Ramamoorthy Membrane fragmentation by an amyloidogenic fragment of human islet amyloid polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes Biomembranes 1768 2007 2026 2029
16. S.M. Butterfield, and H.A. Lashuel Amyloidogenic protein-membrane interactions: mechanistic insight from model systems Angew. Chem. Int. Ed. 49 2010 5628 5654
17. P.E.S. Smith, J.R. Brender, and A. Ramamoorthy Induction of negative curvature as a mechanism of cell toxicity by amyloidogenic peptides: the case of islet amyloid polypeptide J. Am. Chem. Soc. 131 2009 4470 4478
18. T.A. Mirzabekov, M.-C. Lin, and B.L. Kagan Pore formation by the cytotoxic islet amyloid peptide amylin J. Biol. Chem. 271 1996 1988 1992
19. H. Jang, J. Zheng, and R. Nussinov Models of {beta}-amyloid ion-channels in the membrane suggest that channel formation in the bilayer is a dynamic process Biophys. J. 93 2007 1938 1949
20. H. Jang, J. Zheng, R. Lal, and R. Nussinov New structures help the modeling of toxic amyloid-[beta] ion channels Trends Biochem. Sci. 33 2008 91 100
21. H. Jang, F.T. Arce, S. Ramachandran, R. Capone, R. Azimova, B.L. Kagan, R. Nussinov, and R. Lal Truncated beta-amyloid peptide channels provide an alternative mechanism for Alzheimer's disease and Down syndrome Proc. Natl. Acad. Sci. U. S. A. 107 2010 6538 6543
22. M. Mustata, R. Capone, H. Jang, F.T. Arce, S. Ramachandran, R. Lal, and R. Nussinov K3 fragment of amyloidogenic beta(2)-microglobulin forms ion channels: implication for dialysis related amyloidosis J. Am. Chem. Soc. 131 2009 14938 14945
23. H. Jang, F.T. Arce, S. Ramachandran, R. Capone, R. Lal, and R. Nussinov Structural convergence among diverse, toxic beta-sheet ion channels J. Phys. Chem. B 114 2010 9445 9451
24. M. Kawahara, and Y. Kuroda Molecular mechanism of neurodegeneration induced by Alzheimer's [beta]-amyloid protein: channel formation and disruption of calcium homeostasis Brain Res. Bull. 53 2000 389 397
25. A. Demuro, E. Mina, R. Kayed, S.C. Milton, I. Parker, and C.G. Glabe Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers J. Biol. Chem. 280 2005 17294 17300
26. N. Arispe, H.B. Pollard, and E. Rojas Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein [Abeta P-(1-40)] in bilayer membranes PNAS 90 1993 10573 10577
27. H. Lin, R. Bhatia, and R. Lal Amyloid beta protein forms ion channels: implications for Alzheimer's disease pathophysiology FASEB J. 15 2001 2433 2444
28. Y. Hirakura, and B.L. Kagan Pore formation by beta-2-microglobulin: a mechanism for the pathogenesis of dialysis associated amyloidosis Amyloid 8 2001 94 100
29. A. Mascioni, F. Porcelli, U. Ilangovan, A. Ramamoorthy, and G. Veglia Conformational preferences of the amylin nucleation site in SDS micelles: an NMR study Biopolymers 69 2003 29 41
30. U. Ilangovan, and A. Ramamoorthy Conformational studies of human islet amyloid peptide using molecular dynamics and simulated annealing methods Biopolymers 45 1998 9 20
31. R.P.R. Nanga, J.R. Brender, S. Vivekanandan, and A. Ramamoorthy Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment Biochim. Biophys. Acta, Biomembr. 1808 2011 2337 2342
32. S.M. Patil, S. Xu, S.R. Sheftic, and A.T. Alexandrescu Dynamic alpha-helix structure of micelle-bound human amylin J. Biol. Chem. 284 2009 11982 11991
33. S. Jo, T. Kim, and W. Im Automated builder and database of protein/membrane complexes for molecular dynamics simulations PLoS One 2 2007 e880
34. H.I. Petrache, S. Tristram-Nagle, K. Gawrisch, D. Harries, V.A. Parsegian, and J.F. Nagle Structure and fluctuations of charged phosphatidylserine bilayers in the absence of salt Biophys. J. 86 2004 1574 1586
35. L. Kale, R. Skeel, M. Bhandarkar, R. Brunner, A. Gursoy, N. Krawetz, J. Phillips, A. Shinozaki, K. Varadarajan, and K. Schulten NAMD2: greater scalability for parallel molecular dynamics J. Comput. Phys. 151 1999 283 312
36. A.D. MacKerell, D. Bashford, M. Bellott, R.L. Dunbrack, J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F.T.K. Lau, C. Mattos, S. Michnick, T. Ngo, D.T. Nguyen, B. Prodhom, W.E. Reiher, B. Roux, M. Schlenkrich, J.C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
37. H. Jang, F.T. Arce, R. Capone, S. Ramachandran, R. Lal, and R. Nussinov Misfolded amyloid ion channels present mobile beta-sheet subunits in contrast to conventional ion channels Biophys. J. 97 2009 3029 3037
38. H. Jang, B. Ma, R. Lal, and R. Nussinov Models of toxic beta-sheet channels of protegrin-1 suggest a common subunit organization motif shared with toxic alzheimer beta-amyloid ion channels Biophys. J. 95 2008 4631 4642
39. O.S. Smart, J.M. Goodfellow, and B.A. Wallace The pore dimensions of gramicidin A Biophys. J. 65 1993 2455 2460
40. W. Humphrey, A. Dalke, and K. Schulten VMD - visual molecular dynamics J. Mol. Graphics 14 1996 33 38
41. D. Frishman, and P. Argos Knowledge-based protein secondary structure assignment Proteins: Struct. Funct. Genet. 23 1995 566 579
42. P. Westermark, U. Engstrom, K.H. Johnson, G.T. Westermark, and C. Betsholtz Islet amyloid polypeptide-pinpointing amino acid residues linked to amyloid fibril formation Proc. Natl. Acad. Sci. U. S. A. 87 1990 5036 5040
43. M.-T. Lee, W.-C. Hung, F.-Y. Chen, and H.W. Huang Mechanism and kinetics of pore formation in membranes by water-soluble amphipathic peptides Proc. Natl. Acad. Sci. U. S. A. 105 2008 5087 5092
44. M. Manna, and C. Mukhopadhyay Cause and effect of melittin-induced pore formation: a computational approach Langmuir 25 2009 12235 12242
45. S. Jha, D. Sellin, R. Seidel, and R. Winter Amyloidogenic propensities and conformational properties of ProIAPP and IAPP in the presence of lipid bilayer membranes J. Mol. Biol. 389 2009 907 920
46. K. Weise, D. Radovan, A. Gohlke, N. Opitz, and R. Winter Interaction of hIAPP with model raft membranes and pancreatic beta-cells: cytotoxicity of hIAPP oligomers ChemBioChem 11 2010 1280 1290
47. M. Wakabayashi, and K. Matsuzaki Ganglioside-induced amyloid formation by human islet amyloid polypeptide in lipid rafts FEBS Lett. 583 2009 2854 2858
48. X. Yu, and J. Zheng Cholesterol promotes the interaction of Alzheimer β-amyloid monomer with lipid bilayer J. Mol. Biol. 421 2012 561 571
49. H.A. Lashuel, and P.T. Lansbury Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q. Rev. Biophys. 39 2006 167 201
50. J.R. Brender, E.L. Lee, M.A. Cavitt, A. Gafni, D.G. Steel, and A. Ramamoorthy Amyloid fiber formation and membrane disruption are separate processes localized in two distinct regions of IAPP, the type-2-diabetes-related peptide J. Am. Chem. Soc. 130 2008 6424 6429
51. N.B. Last, E. Rhoades, and A.D. Miranker Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity Proc. Natl. Acad. Sci. U. S. A. 108 2011 9460 9465
52. J.D. Knight, J.A. Hebda, and A.D. Miranker Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide Biochemistry 45 2006 9496 9508
53. P.E.S. Smith, J.R. Brender, and A. Ramamoorthy Induction of negative curvature as a mechanism of cell toxicity by amyloidogenic peptides: the case of islet amyloid polypeptide J. Am. Chem. Soc. 131 2009 4470 4478
54. Z. Chang, Y. Luo, Y. Zhang, and G. Wei Interactions of A beta 25-35 beta-barrel-like oligomers with anionic lipid bilayer and resulting membrane leakage: an all-atom molecular dynamics study J. Phys. Chem. B 115 2011 1165 1174
55. Y. Shafrir, S.R. Durell, A. Anishkin, and H.R. Guy Beta-barrel models of soluble amyloid beta oligomers and annular protofibrils Proteins Struct. Funct. Bioinform. 78 2010 3458 3472
56. S. Chimon, M.A. Shaibat, C.R. Jones, D.C. Calero, B. Aizezi, and Y. Ishii Evidence of fibril-like [beta]-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's [beta]-amyloid Nat. Struct. Mol. Biol. 14 2007 1157 1164
57. H.A. Scheidt, I. Morgado, S. Rothemund, D. Huster, and M. Fändrich Solid-state NMR spectroscopic investigation of Aβ protofibrils: implication of a β-sheet remodeling upon maturation into terminal amyloid fibrils Angew. Chem. Int. Ed. 50 2011 2837 2840
58. J.C. Stroud, C. Liu, P.K. Teng, and D. Eisenberg Toxic fibrillar oligomers of amyloid-β have cross-β structure Proc. Natl. Acad. Sci. U. S. A. 109 2012 7717 7722
59. R. Sarroukh, E. Cerf, S. Derclaye, Y.F. Dufrêne, E. Goormaghtigh, J.M. Ruysschaert, and V. Raussens Transformation of amyloid β(1-40) oligomers into fibrils is characterized by a major change in secondary structure Cell Mol. Life Sci. 68 2011 1429 1438
60. J. Zhao, Q. Wang, G. Liang, and J. Zheng Molecular dynamics simulations of low-ordered Alzheimer beta-Amyloid oligomers from dimer to hexamer on self-assembled monolayers Langmuir 27 2011 14876 14887
61. S. Kumar, J.M. Rosenberg, D. Bouzida, R.H. Swendsen, and P.A. Kollman The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 13 1992 1011 1021
62. J.S. Hub, B.L. de Groot, and D. van der Spoel g-wham - a free weighted histogram analysis implementation including robust error and autocorrelation estimates J. Chem. Theory Comput. 6 2010 3713 3720
63. P. Gkeka, and L. Sarkisov Interactions of phospholipid bilayers with several classes of amphiphilic α-helical peptides: insights from coarse-grained molecular dynamics simulations J. Phys. Chem. B 114 2009 826 839