Phosphatidylethanolamine enhances amyloid fiber-dependent membrane fragmentation

Biochemistry

Volumn 51, Issue 39, 2012, Pages 7676-7684

  Sciacca, Michele F M ^a   Brender, Jeffrey R ^a   Lee, Dong Kuk ^a,b   Ramamoorthy, Ayyalusamy ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b Seoul National University of Science and Technology   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

FIBER FORMATION; IN-VITRO; MEMBRANE BINDING; MEMBRANE COMPOSITION; MEMBRANE DISRUPTION; MEMBRANE PERMEABILIZATION; MEMBRANE SURFACE; MODEL MEMBRANES; MODEL SYSTEM; PHOSPHATIDYLETHANOLAMINE; TYPE II;

CELL MEMBRANES; CYTOLOGY; GLYCOPROTEINS; LIPIDS; OLIGOMERS; PROTEINS; TOXICITY;

MEMBRANES;

AMYLIN; PHOSPHATIDYLETHANOLAMINE;

ARTICLE; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOTOXICITY; FRAGMENTATION REACTION; MEMBRANE BINDING; MEMBRANE DAMAGE; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION;

AMINO ACID SEQUENCE; CELL MEMBRANE; CIRCULAR DICHROISM; HUMANS; ISLET AMYLOID POLYPEPTIDE; LIPOSOMES; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PERMEABILITY; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES;

EID: 84867091546     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3009888     Document Type: Article

References (74)

1. Carrell, R. W. and Lomas, D. A. (1997) Conformational disease Lancet 350, 134-138
2. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75, 333-366
3. Westermark, P., Wernstedt, C., Wilander, E., Hayden, D. W., Obrien, T. D., and Johnson, K. H. (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
4. Woods, S. C., Lutz, T. A., Geary, N., and Langhans, W. (2006) Pancreatic signals controlling food intake; insulin, glucagon and amylin Philos. Trans. R. Soc. London, Ser. B 361, 1219-1235
5. Westermark, P., Andersson, A., and Westermark, G. T. (2011) Islet amyloid polypeptide, islet amyloid, and diabetes mellitus Physiol. Rev. 91, 795-826
6. Kayed, R., Sokolov, Y., Edmonds, B., McIntire, T. M., Milton, S. C., Hall, J. E., and Glabe, C. G. (2004) Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J. Biol. Chem. 279, 46363-46366
7. Haataja, L., Gurlo, T., Huang, C. J., and Butler, P. C. (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis Endocr. Rev. 29, 302-316
8. Hebda, J. A. and Miranker, A. D. (2009) The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: Insights from type II diabetes Annu. Rev. Biophys. Biomol. Struct. 38, 125-152
9. Last, N. B., Rhoades, E., and Miranker, A. D. (2011) Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity Proc. Natl. Acad. Sci. U.S.A. 108, 9460-9465
10. Lashuel, H. A. and Lansbury, P. T. (2006) Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q. Rev. Biophys. 39, 167-201
11. Anguiano, M., Nowak, R. J., and Lansbury, P. T. (2002) Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes Biochemistry 41, 11338-11343
12. La Rosa, C., Scalisi, S., Sciacca, M. F. M., Zhavnerko, G., Grasso, D. M., and Marletta, G. (2010) Self-assembling pathway of hIAPP fibrils within lipid bilayers ChemBioChem 11, 1856-1859
13. Sparr, E., Engel, M. F. M., Sakharov, D. V., Sprong, M., Jacobs, J., de Kruijff, B., Hoppener, J. W. M., and Killian, J. A. (2004) Islet amyloid polypeptide-induced membrane leakage involves uptake of lipids by forming amyloid fibers FEBS Lett. 577, 117-120
14. Engel, M. F., Khemtemourian, L., Kleijer, C. C., Meeldijk, H. J., Jacobs, J., Verkleij, A. J., de Kruijff, B., Killian, J. A., and Hoppener, J. W. (2008) Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane Proc. Natl. Acad. Sci. U.S.A. 105, 6033-6038
15. Green, J. D., Kreplak, L., Goldsbury, C., Blatter, X. L., Stolz, M., Cooper, G. S., Seelig, A., Kist-Ler, J., and Aebi, U. (2004) Atomic force microscopy reveals defects within mica supported lipid bilayers induced by the amyloidogenic human amylin peptide J. Mol. Biol. 342, 877-887
16. Brender, J. R., Salamekh, S., and 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
17. Knight, J. D., Hebda, J. A., and Miranker, A. D. (2006) Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide Biochemistry 45, 9496-9508
18. Knight, J. D. and Miranker, A. D. (2004) Phospholipid catalysis of diabetic amyloid assembly J. Mol. Biol. 341, 1175-1187
19. Evers, F., Jeworrek, C., Tiemeyer, S., Weise, K., Sellin, D., Paulus, M., Struth, B., Tolan, M., and Winter, R. (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
20. Sellin, D., Yan, L. M., Kapurniotu, A., and Winter, R. (2010) Suppression of IAPP fibrillation at anionic lipid membranes via IAPP-derived amyloid inhibitors and insulin Biophys. Chem. 150, 73-79
21. Engel, M. F. M., Yigittop, H., Elgersma, R. C., Rijkers, D. T. S., Liskamp, R. M. J., de Kruijff, B., Hoppener, J. W. M., and Killian, J. A. (2006) Islet amyloid polypelptide inserts into phospholipid monolayers as monomer J. Mol. Biol. 356, 783-789
22. Brender, J. R., Lee, E. L., Cavitt, M. A., Gafni, A., Steel, D. G., and Ramamoorthy, A. (2008) 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
23. Brender, J. R., Hartman, K., Reid, K. R., Kennedy, R. T., and Ramamoorthy, A. (2008) A single mutation in the nonamyloidogenic region of islet amyloid polypeptide greatly reduces toxicity Biochemistry 47, 12680-12688
24. Brender, J. R., Lee, E. L., Hartman, K., Wong, P. T., Ramamoorthy, A., Steel, D. G., and Gafni, A. (2011) Biphasic effects of insulin on islet amyloid polypeptide membrane disruption Biophys. J. 100, 685-692
25. Jayasinghe, S. A. and Langen, R. (2005) Lipid membranes modulate the structure of islet amyloid polypeptide Biochemistry 44, 12113-12119
26. Grudzielanek, S., Smirnovas, V., and Winter, R. (2007) The effects of various membrane physical-chemical properties on the aggregation kinetics of insulin Chem. Phys. Lipids 149, 28-39
27. Jo, E. J., McLaurin, J., Yip, C. M., St George-Hyslop, P., and Fraser, P. E. (2000) α-Synuclein membrane interactions and lipid specificity J. Biol. Chem. 275, 34328-34334
28. Zhu, M., Li, J., and Fink, A. L. (2003) The association of α-synuclein with membranes affects bilayer structure, stability, and fibril formation J. Biol. Chem. 278, 40186-40197
29. Sciacca, M. F., Kotler, S. A., Brender, J. R., Chen, J., Lee, D. K., and Ramamoorthy, A. (2012) Two-step mechanism of membrane disruption by Aβ through membrane fragmentation and pore formation Biophys. J. 103, 702-710
30. Radovan, D., Opitz, N., and Winter, R. (2009) Fluorescence microscopy studies on islet amyloid polypeptide fibrillation at heterogeneous and cellular membrane interfaces and its inhibition by resveratrol FEBS Lett. 583, 1439-1445
31. Weise, K., Radovan, D., Gohlke, A., Opitz, N., and Winter, R. (2010) Interaction of hIAPP with model raft membranes and pancreatic β-cells: Cytotoxicity of hIAPP oligomers ChemBioChem 11, 1280-1290
32. Wakabayashi, M. and Matsuzaki, K. (2009) Ganglioside-induced amyloid formation by human islet amyloid polypeptide in lipid rafts FEBS Lett. 583, 2854-2858
33. Cho, W. J., Trikha, S., and Jeremic, A. M. (2009) Cholesterol regulates assembly of human islet amyloid polypeptide on model membranes J. Mol. Biol. 393, 765-775
34. Trikha, S. and Jeremic, A. M. (2011) Clustering and internalization of toxic amylin oligomers in pancreatic cells require plasma membrane cholesterol J. Biol. Chem. 286, 36086-36097
35. Morita, M., Vestergaard, M., Hamada, T., and Takagi, M. (2010) Real-time observation of model membrane dynamics induced by Alzheimer's amyloid β Biophys. Chem. 147, 81-86
36. Domanov, Y. A. and Kinnunen, P. K. J. (2008) Islet amyloid polypeptide forms rigid lipid-protein amyloid fibrils on supported phospholipid bilayers J. Mol. Biol. 376, 42-54
37. Lundbaek, J. A., Collingwood, S. A., Ingolfsson, H. I., Kapoor, R., and Andersen, O. S. (2010) Lipid bilayer regulation of membrane protein function: Gramicidin channels as molecular force probes J. R. Soc., Interface 7, 373-395
38. Smith, P. E. S., Brender, J. R., and Ramamoorthy, A. (2009) Induction of negative curvature as a mechanism of cell toxicity by amyloidogenic peptides: The case of islet amyloid polypeptide J. Am. Chem. Soc. 131, 4470-4478
39. Cazzaniga, E., Bulbarelli, A., Lonati, E., Orlando, A., Re, F., Gregori, M., and Masserini, M. (2011) Aβ peptide toxicity is reduced after treatments decreasing phosphatidylethanolamine content in differentiated neuroblastoma cells Neurochem. Res. 36, 863-869
40. Janmey, P. A. and Kinnunen, P. K. J. (2006) Biophysical properties of lipids and dynamic membranes Trends Cell Biol. 16, 538-546
41. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo Nature 416, 535-539
42. Lin, C. Y., Gurlo, T., Kayed, R., Butler, A. E., Haataja, L., Glabe, C. G., and Butler, P. C. (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
43. Vance, J. E. (2008) Thematic review series: Glycerolipids. Phosphatidylserine and phosphatidylethanolamine in mammalian cells: Two metabolically related aminophospholipids J. Lipid Res. 49, 1377-1387
44. Brender, J. R., Hartman, K., Nanga, R. P., Popovych, N., de la Salud Bea, R., Vivekanandan, S., Marsh, E. N., and Ramamoorthy, A. (2010) Role of zinc in human islet amyloid polypeptide aggregation J. Am. Chem. Soc. 132, 8973-8983
45. Soong, R., Brender, J. R., Macdonald, P. M., and Ramamoorthy, A. (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
46. Brender, J. R., Durr, U. H. N., Heyl, D., Budarapu, M. B., and Ramamoorthy, A. (2007) Membrane fragmentation by an amyloidogenic fragment of human islet amyloid polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes Biochim. Biophys. Acta 1768, 2026-2029
47. Muller, P., Schiller, S., Wieprecht, T., Dathe, M., and Herrmann, A. (2000) Continuous measurement of rapid transbilayer movement of a pyrene-labeled phospholipid analogue Chem. Phys. Lipids 106, 89-99
48. Stewart, J. C. (1980) Colorimetric determination of phospholipids with ammonium ferrothiocyanate Anal. Biochem. 104, 10-14
49. Kodaka, M. (2004) Requirements for generating sigmoidal time-course aggregation in nucleation-dependent polymerization model Biophys. Chem. 107, 243-253
50. Magzoub, M. and Miranker, A. D. (2012) Concentration-dependent transitions govern the subcellular localization of islet amyloid polypeptide FASEB J. 26, 1228-1238
51. Bechinger, B. and Lohner, K. (2006) Detergent-like actions of linear amphipathic cationic antimicrobial peptides Biochim. Biophys. Acta 1758, 1529-1539
52. Reynolds, N. P., Soragni, A., Rabe, M., Verdes, D., Liverani, E., Handschin, S., Riek, R., and Seeger, S. (2011) Mechanism of membrane interaction and disruption by α-synuclein J. Am. Chem. Soc. 133, 19366-19375
53. Jan, A., Adolfsson, O., Allaman, I., Buccarello, A. L., Magistretti, P. J., Pfeifer, A., Muhs, A., and Lashuel, H. A. (2011) Aβ42 neurotoxicity is mediated by ongoing nucleated polymerization process rather than by discrete Aβ42 species J. Biol. Chem. 286, 8585-8596
54. Pellarin, R., Friedman, R., and Caflisch, A. (2009) Amyloid aggregation on lipid bilayers and its impact on membrane permeability J. Mol. Biol. 387, 407-415
55. Michikawa, M., Gong, J. S., Fan, Q. W., Sawamura, N., and Yanagisawa, K. (2001) A novel action of Alzheimer's amyloid β-protein (Aβ): Oligomeric Aβ promotes lipid release J. Neurosci. 21, 7226-7235
56. Kagan, B. L. and Thundimadathil, J. (2010) Amyloid peptide pores and the β sheet conformation Proteins 677, 150-167
57. Jang, H. B., Zheng, J., Lal, R., and Nussinov, R. (2008) New structures help the modeling of toxic amyloid β ion channels Trends Biochem. Sci. 33, 91-100
58. Apostolidou, M., Jayasinghe, S. A., and Langen, R. (2008) Structure of α-helical membrane-bound hIAPP and its implications for membrane-mediated misfolding J. Biol. Chem. 283, 17205-17210
59. Matsuzaki, K., Sugishita, K., Ishibe, N., Ueha, M., Nakata, S., Miyajima, K., and Epand, R. M. (1998) Relationship of membrane curvature to the formation of pores by magainin 2 Biochemistry 37, 11856-11863
60. Konarkowska, B., Aitken, J. F., Kistler, J., Zhang, S. P., and Cooper, G. J. S. (2006) The aggregation potential of human amylin determines its cytotoxicity towards islet β-cells FEBS J. 273, 3614-3624
61. Warschawski, D. E., Fellmann, P., and Devaux, P. F. (1996) High resolution p-31-h-1 two-dimensional nuclear magnetic resonance spectra of unsonicated lipid mixtures spinning at the magic-angle Eur. Biophys. J. Biophys. Lett. 25, 131-137
62. Lindstrom, F., Bokvist, M., Sparrman, T., and Grobner, G. (2002) Association of amyloid-β peptide with membrane surfaces monitored by solid state NMR Phys. Chem. Chem. Phys. 4, 5524-5530
63. Butterfield, S. M. and Lashuel, H. A. (2010) Amyloidogenic protein membrane interactions: Mechanistic insight from model systems Angew. Chem., Int. Ed. 49, 5628-5654
64. Hallock, K. J., Lee, D. K., and Ramamoorthy, A. (2003) MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain Biophys. J. 84, 3052-3060
65. Heller, W. T., He, K., Ludtke, S. J., Harroun, T. A., and Huang, H. W. (1997) Effect of changing the size of lipid headgroup on peptide insertion into membranes Biophys. J. 73, 239-244
66. Nanga, R. P. R., Brender, J. R., Xu, J. D., Veglia, G., and Ramamoorthy, A. (2008) Structures of rat and human islet amyloid polypeptide IAPP(1-19) in micelles by NMR spectroscopy Biochemistry 47, 12689-12697
67. Nanga, R. P. R., Brender, J. R., Vivekanandan, S., Popovych, N., and Ramamoorthy, A. (2009) NMR structure in a membrane environment reveals putative amyloidogenic regions of the SEVI precursor peptide PAP(248-286) J. Am. Chem. Soc. 131, 17972-17979
68. Brender, J. R., Hartman, K., Gottler, L. M., Cavitt, M. E., Youngstrom, D. W., and Ramamoorthy, A. (2009) Helical conformation of the SEVI precursor peptide PAP(248-286), a dramatic enhancer of HIV infectivity, promotes lipid aggregation and fusion Biophys. J. 97, 2474-2483
69. Munch, J., Rucker, E., Standker, L., Adermann, K., Goffinet, C., Schindler, M., Wildum, S., Chinnadurai, R., Rajan, D., Specht, A., Gimenez-Gallego, G., Sanchez, P. C., Fowler, D. M., Koulov, A., Kelly, J. W., Mothes, W., Grivel, J. C., Margolis, L., Keppler, O. T., Forssmann, W. G., and Kirchhoff, F. (2007) Semen-derived amyloid fibrils drastically enhance HIV infection Cell 131, 1059-1071
70. Nanga, R. P. R., Brender, J. R., Vivekanandan, S., and Ramamoorthy, A. (2011) Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment Biochim. Biophys. Acta 1808, 2337-2342
71. Jang, H., Arce, F. T., Ramachandran, S., Capone, R., Lal, R., and Nussinov, R. (2010) β-Barrel topology of Alzheimer's β-amyloid ion channels J. Mol. Biol. 404, 917-934
72. Vaiana, S. M., Ghirlando, R., Yau, W. M., Eaton, W. A., and Hofrichter, J. (2008) Sedimentation studies on human amylin fail to detect low-molecular-weight oligomers Biophys. J. 94, L45-L47
73. Zhang, Y. J., Shi, J. M., Bai, C. J., Wang, H., Li, H. Y., Wu, Y., and Ji, S. R. (2012) Intra-membrane oligomerization and extra-membrane oligomerization of amyloid-β peptide are competing processes as a result of distinct patterns of motif interplay J. Biol. Chem. 287, 748-756
74. Lee, C. C., Sun, Y., and Huang, H. W. (2012) How type II diabetes-related islet amyloid polypeptide damages lipid bilayers Biophys. J. 102, 1059-1068