α-Helical structures drive early stages of self-assembly of amyloidogenic amyloid polypeptide aggregate formation in membranes

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Pannuzzo, Martina ^a   Raudino, Antonio ^b   Milardi, Danilo ^c   La Rosa, Carmelo ^b   Karttunen, Mikko ^d  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF CATANIA   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLIN; RECOMBINANT PROTEIN;

ALGORITHM; ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; LIPID BILAYER; MEMBRANE; METABOLISM; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; THERMODYNAMICS;

ALGORITHMS; HUMANS; ISLET AMYLOID POLYPEPTIDE; LIPID BILAYERS; MEMBRANES; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; THERMODYNAMICS;

EID: 84885110787     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep02781     Document Type: Article

References (89)

1. Merlini, G. & Bellotti, V. Molecular mechanisms of amyloidosis. N. Engl. J. Med. 349, 583-596 (2003). (Pubitemid 36951371)
2. Hardy, J. & Selkoe, D. J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356 (2002). (Pubitemid 34790756)
3. Dickson, D. W. The pathogenesis of senile plaques. J. Neuropathol. Exp. Neurol. 56, 321-339 (1997). (Pubitemid 27465015)
4. Abedini, A. & Raleigh, D. P. A role for helical intermediates in amyloid formation by natively unfolded polypeptides? Phys. Biol. 6, 015005 (2009).
5. Miller, Y., Ma, B. & Nussinov, R. Polymorphism in Alzheimer Abeta amyloid organization reflects conformational selection in a rugged energy landscape. Chem. Rev. 110, 4820-4838 (2010).
6. Dupuis, N. F., Wu, C., Shea, J. & Bowers, M. T. Human islet amyloid polypeptide monomers form ordered beta-hairpins: a possible direct amyloidogenic precursor. J. Am. Chem. Soc. 131, 18283-18292 (2009).
7. Bernstein, S. L. et al. Amyloid-b protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nature Chem. 1, 326-331 (2009).
8. Hoppener, J. W., Ahren, B. & Lips, C. J. Islet amyloid and type 2 diabetes mellitus. N. Engl. J. Med. 343, 411-19 (2000). (Pubitemid 30626125)
9. Kahn, S. E., Andrikopoulos, S. & Verchere, C. B. Islet amyloid: a long-recognized but underappreciated pathological feature of type 2 diabetes. Diabetes 48, 241-253 (1999). (Pubitemid 29061094)
10. Haataja, L., Gurlo, T., Huang, C. J. & Butler, P. C. Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr. Rev. 29, 303-316 (2008). (Pubitemid 351679701)
11. Ramamoorthy, A. & Lim, M. H. Structural Characterization and Inhibition of Toxic Amyloid-b Oligomeric Intermediates. Biophys. J. 105, 287-288 (2013).
12. Milojevic, V. & Melacini, V. Stoichiometry and Affinity of the Human Serum Albumin-Alzheimer's Ab Peptide Interactions. Biophys. J. 100, 183-192 (2011).
13. Raditsis, V., Milojevic, V. & Melacini, V. Ab Association Inhibition by Transferrin. Biophys. J. 105, 473-480 (2013).
14. Glabe, C. G. Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol. of aging. 4, 570-575 (2006). (Pubitemid 43290525)
15. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003). (Pubitemid 36444329)
16. Demmester, N. et al. Apoptosis induced in neuronalcells by C-terminal amyloid fragments is correlated with theiraggregation properties in phospholipid membranes. Mol. Membr. Biol. 17, 219-228 (2000).
17. Kawahara, M., Kuroda, Y., Arispe, N. & Rojas, E. Alzheimer's amyloid, human islet amylin, and prion peptide fragment evoke intracellular free calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell line. J. Biol. Chem. 275, 14077-14083 (2000). (Pubitemid 30339682)
18. Lin, H., Bhatia, R. & Lal, R. Amyloid protein forms ion channels: implications for Alzheimer's disease pathology. FASEB. J. 15, 2433-2444 (2001). (Pubitemid 33063171)
19. Hebda, J. A. Miranker, A. D. The interplay of Catalysis and Toxicity by Amyloid intermediates on Lipid Bilayers: Insights from Type II Diabetes. Ann. Rev. Biophys. 38, 125-152 (2009).
20. Sciacca, M. F. et al. Two-Step Mechanism of Membrane Disruption by Ab through Membrane Fragmentation and Pore formation. Biophys. J. 103, 702-710 (2012).
21. Butterfield, S. M. & Lashuel, H. Amyloidogenic protein-membrane interactions: mechanistic insight from model systems. Angew. Chem. 49, 5628-5654 (2010).
22. Brender, J. R. et al. 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, 6424-6429 (2008). (Pubitemid 351706103)
23. Sciacca, M. F. M. et al. Cations as Switches of Amyloid-Mediated Membrane Disruption Mechanisms: Calcium and IAPP. Biophys. J. 104, 172-184 (2013).
24. Brender, J. R., Salamekh, S. & Ramamoorthy, A. Membrane Disruption and Early Events in the Aggregation of the Diabetes Related Peptide IAPP from aMolecular Perspective. Acc. Chem Res. 45, 454-462 (2012).
25. Cooper, G. J. et al. Purification and characterization of a peptide from amyloidrich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. USA 84, 8628-8632 (1987). (Pubitemid 18033465)
26. Westermark, P., Andersson, A. & Westermark, G. T. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 91, 795-826 (2011).
27. Harroun, T. A., Bradshaw, J. P. & Ashley, R. H. Inhibitors can arrest the membrane activity of human islet amyloid polypeptide independently of amyloid formation. FEBS. Lett. 507, 200-204 (2001). (Pubitemid 33001542)
28. Hirakura, Y., Yiu, W. W., Yamamoto, A. Kagan, B. L. Amyloid peptide channels: blockade by zinc and inhibition by Congo red (amyloid channel block). Amyloid 7, 194-199 (2000).
29. Mirzabekov, T. A., Lin, M. C. & Kagan, B. L. Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem. 271, 1988-1992 (1996). (Pubitemid 26047780)
30. Anguiano, M., Nowak, R. J. & Lansbury, P. T. Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes. Biochemistry 41, 11338-11343 (2002).
31. Kawahara, M., Kuroda, Y., Arispe, N. & Rojas, E. Alzheimer's beta-amyloid, human islet amylin, and prion protein fragment evoke intracellular free calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell line. J. Biol. Chem. 275, 14077-14083 (2000). (Pubitemid 30339682)
32. Weise, K., Radovan, D., Gohlke, A., Opitz, N. Winter, R. Interaction of hIAPP with model raft membranes and pancreatic beta-cells: cytotoxicity of hIAPP oligomers. ChemBioChem. 11, 1280-1290 (2010).
33. Meier, J. J. et al. Inhibition of human IAPP fibril formation does not prevent betacell death: evidence for distinct actions of oligomers and fibrils of human IAPP. Am. J. Physiol. Endocrinol. Metab. 291, E1317-24 (2006). (Pubitemid 44904040)
34. Nath, A.,Miranker, A. D. Rhoades, E. Amembrane-bound antiparallel dimer of rat islet amyloid polypeptide. Angew. Chem. 50, 10859-10862 (2011).
35. Quist, A. et al. Amyloids form membrane pores: a common structural link for protein-misfolding disease. Proc. Natl. Acad. Sci. USA 102, 10427-10432 (2005). (Pubitemid 41061570)
36. Engel, M. F. M. et al. Islet amyloid polypeptide inserts into phospholipid monolayers as monomer. J. Mol. Biol. 356, 783-789 (2006). (Pubitemid 43139337)
37. Prakash, R., 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 1808, 2337-2342 (2011).
38. Laghaei, R., Mousseau, N. & Wei, G. Effect of the disulfide bond on the monomeric structure of human amylin studied by combined Hamiltonian and temperature replica exchange molecular dynamics simulations. J. Phys. Chem. B 114, 7071-7077 (2010).
39. Dupuis, N. F., Wu, C., Shea, J. E. & Bowers, M. T. The amyloid formation mechanism in human IAPP: dimers have b-strand monomer-monomer interfaces. J. Am. Chem. Soc. 133, 7240-7243 (2011).
40. Reddy, A. S. et al. Stable and metastable states of human amylin in solution. Biophys. J. 99, 2208-2216 (2010).
41. Andrews, M. N. Winter, R. Comparing the structural properties of human and rat islet amyloid polypeptide by MD computer simulations. Biophys. Chem. 156, 43-50 (2011).
42. Rivera, E., Straub, J. & Thirumalai, D. Sequence and crowding effects in the aggregation of a 10-residue fragment derived from islet amyloid polypeptide. Biophys. J. 96, 4552-4560 (2009).
43. Xu,W., Wei, G., Su, H., Nordenskio?d, L. & Mu, Y. Effects of cholesterol on pore formation in lipid bilayers induced by human islet amyloid polypeptide fragments: A coarse-grained molecular dynamics study. Phys. Rev. E 84, 1-8 (2011).
44. Lee, C., Sun, Y. & Huang, H. W. How Type II Diabetes-Related Islet Amyloid Polypeptide Damages Lipid Bilayers. Biophys. J. 102, 1059-1068 (2012).
45. Scalisi, S. et al. Self-Assembling Pathway of HiApp Fibrils within Lipid Bilayers. ChemBiochem 11, 1856-1859 (2010).
46. Sajith, A., Jayasinghe, S. A. & Langen, R. Membrane interaction of islet amyloid polypeptide. Biochim. Biophys. Acta 1768, 2002-2009 (2007). (Pubitemid 47125849)
47. Soong, R., Brender, J. R., Macdonald, P. M. & Ramamoorthy, A. 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 (2009).
48. Nanga, R. P. R., Brender, J. R., Xu, J., Veglia, G. & Ramamoorthy, A. Structures of Rat and Human Islet Amyloid Polypeptide IAPP1-19 in Micelles by NMR Spectroscopy. Biochemistry 47, 12689-12697 (2008).
49. Oelschlaeger, C., Schopferer, M., Scheffold, F. & Willenbacher, N. Linear-to-Branched Micelles Transition: A Rheometry and Diffusing Wave Spectroscopy (DWS) Study. Langmuir 25, 716-723 (2009).
50. Tang, M. & Carter,W. C. Branching Mechanisms in Surfactants Micellar Growth. J. Phys. Chem. B 117, 2898-2905 (2013).
51. Pannuzzo, M., Milardi, D., Raudino, A., Karttunen, M. & La Rosa, C. Analytical model and multiscale simulations of Ab peptide aggregation in lipid membranes: towards a unifying description of conformational transitions, oligomerization and membrane damage. Phys.Chem. Chem. Phys. 15, 8940-8951 (2013).
52. Zimmerberg, J. & Kozlov, M. M. How proteins produce cellular membrane curvature. Nature Rev. Mol. Cell. Biol. 7, 9-19 (2006). (Pubitemid 43361568)
53. Bahrami, A. H. & Jalali, M. A. Vesicle deformations by clusters of transmembrane proteins. J. Chem. Phys. 134, 085106 (2011).
54. Dommersnes, P. G. & Fournier, J. B. N-body study of anisotropic membrane inclusions: Membrane mediated interactions and ordered aggregation. Eur. Phys. J. B. 12, 9-12 (1999). (Pubitemid 129640352)
55. Iglic, A. et al.On the role of anisotropy ofmembrane constituents in formation of a membrane neck during budding of amulticomponentmembrane. J. Biomech. 40, 579-585 (2007). (Pubitemid 46127486)
56. Ramamoorthy, A., Thennarasu, S., Lee, D-K., Tan, A. & Maloy, L. Solid-State NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J. 91, 206-216 (2006). (Pubitemid 44015320)
57. Sciacca, M. F. M., Pappalardo, M., Milardi, D., Grasso, D. M. & La Rosa, C. Calcium-activated membrane interaction of the islet amyloid polypeptide: Implications in the pathogenesis of type II diabetes mellitus. Arch. Biochem. Biophys. 477, 291-298 (2008).
58. Sciacca, M. F. M. et al. Are fibril growth and membrane damage linked processes? An experimental and computational study of IAPP(12-18) and IAPP(21-27) peptides. New J. Chem. 34, 200-207 (2010).
59. Seifert, U. & Lipowsky, R. The morphology of vesicles. In Lipowsky, R. & Sackmann, E. editors 0Structure and Dynamics of Membranes.0 p.403-463. Elsevier, Amsterdam (1995).
60. Straub, J. E. Thirumalai, D. Toward amolecular theory of early and late events in monomer to amyloid fibril formation. Ann. Rev. Phys. Chem. 62, 437-463 (2011).
61. Pappalardo,M. et al. A molecular dynamics study on the conformational stability of prp 180-193 helix ii prion fragment. Chem. Phys. Lett. 390, 511-516 (2004).
62. Milardi, D., Pappalardo,M., Pannuzzo,M., La Rosa, C. Grasso, D. M. The role of the Cys2-Cys7 disulfide bridge on the early steps of Islet Amyloid Polypeptide aggregation. Chem. Phys. Lett. 463, 396-399 (2008).
63. Last, N. B., Rhoades, E. Miranker, A. D. Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity. Proc. Natl. Acad. Sci. USA 108, 9460-9465 (2011).
64. Gregory, S. M., Cavenaugh, A., Journigan, V., Pokorny, A. & Almeida, P. F. F. A quantitative model for the all-or-none permeabilization of phospholipid vesicles by the antimicrobial peptide cecropin A. Biophys. J. 94, 1667-1680 (2008).
65. Axelsen, P. H. A chaotic pore model of polypeptide antibiotic action. Biophys. J. 94, 1549-1550 (2008).
66. Bond, P. & Sansom, M. S. P. Insertion and assembly of membrane proteins via simulation. J. Am. Chem. Soc. 128, 2697-2704 (2006). (Pubitemid 43327948)
67. Zhao, J., Yu, X., Liang, G. & Zheng, J. 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, 1781-94 (2011).
68. Mo, Y., Lu, Y., Wei, G. Derreumaux, P. Structural diversity of the soluble trimers of the human amylin(20-29) peptide revealed by molecular dynamics simulations. J. Chem. Phys. 130, 125101 (2009).
69. Dias, C. L., Karttunen, M. & Chan, H. S. hydrophobic interactions in the formation of secondary structures in small peptides. Phys. Rev. E 84, 041931 (2011).
70. Magzoub, J. & Miranker, A. D. Concentration-dependent transitions govern the subcellular localization of islet amyloid polypeptide. FASEB J. 26, 1228 (2012).
71. Yu, S. P., Farhangrazi, Z. S., Ying,H. S., Yeh, C.-H. & Choi, D. W. Enhancement of Outward Potassium Current May Participate in b-Amyloid Peptide-Induced Cortical Neuronal Death. Neurobiol. Dis. 5, 81-88 (1998). (Pubitemid 28430718)
72. Rzepiela, et al. Reconstruction of atomistic details from coarse grained structures. J. Comp. Chem. 31, 1333-1343 (2010).
73. Patil, S. M., Xu, S., Sheftic, S. R. & Alexandrescu, A. T. Dynamic alpha-helix structure of micelle-bound human amylin. J. Biol. Chem. 284, 11982-11991 (2009).
74. 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).
75. Hess, B., Kutzner, C., Van der Spoel, D. & Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J. Chem. Theory. Comput. 4, 435-447 (2008).
76. Wong-ekkabut, J., Miettinen, M. S., Dias, C. Karttunen, M. Static charges cannot drive a continuous flow of water molecules through a carbon nanotube. Nature Nanotech. 5, 555-557 (2010).
77. Oostenbrink, C., Soares, T. A., van der Vegt, N. F. & van Gunsteren, W. F. Validation of the 53A6 GROMOS force field. Biophys. J. 34, 273-284 (2005). (Pubitemid 40884072)
78. Wong-ekkabut, J. & Karttunen, M. Assessment of common simulation protocols for simulations of nanopores, membrane proteins & channels. J. Chem. Theory Comput. 8, 2905-2911 (2012).
79. Cino, E. A., Choy, W.-Y. & Karttunen, M. Comparison of secondary structure formation using 10 different force fields in microsecond molecular dynamics simulations. J. Chem. Theory Comput. 8, 2725-2740 (2012).
80. Monticelli, L. et al. The MARTINI coarse grained force field: extension to proteins. J. Chem. Theory Comp. 4, 819-834 (2008).
81. Marrink, S. J., Risselada, H. J., Yefimov, S., Tieleman, D. P. & de Vries, A. H. The MARTINI forcefield: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812-7824 (2007). (Pubitemid 47169693)
82. Marrink, S. J., de Vries, A. H. & Mark, A. E. Coarse grained model for semiquantitative lipid simulations. J. Phys. Chem. B 108, 750-760 (2004).
83. de Jong, D. H., Singh, G., Bennett, W. F. D., Arnarez, C.,Wassenaar, T. A., Scha?er, L. V., Periole, X., Tieleman, D. P. & Marrink, S. J. Improved parameters for the Martini coarse-grained protein force field. J. Chem. Theory Comput. 9, 687-697 (2013). Parameters at http://md.chem.rug.nl/cgmartini/index. php/force-fieldparameters/lipids.
84. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F. & Hermans, J. Interaction Models for Water in Relation to Protein Hydration, in Intermolecular Forces, edited by Pullman, B. 331-342 D. Reidel Publishing Company, Dordrecht (1981).
85. Nose? S. A. Unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 81, 511 (1984).
86. Hoover, W. Canonical dynamics: Equilibrium phase-space distributions. Phys. Rev. A 31, 1695-1697 (1985).
87. Parrinello, M. & Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys. 52, 7182-7190 (1981). (Pubitemid 12456820)
88. Darden, T., York, D. & Pedersen, L. Particle mesh Ewald: An Nlog(N)method for Ewald sums in large systems. J. Chem. Phys. 98, 10089 (1993).
89. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A. & Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690 (1984).