Phosphatidylethanolamine enhances amyloid fiber-dependent membrane fragmentation.

The toxicity of amyloid-forming peptides has been hypothesized to reside in the ability of protein oligomers to interact with and disrupt the cell membrane. Much of the evidence for this hypothesis comes from in vitro experiments using model membranes. However, the accuracy of this approach depends on the ability of the model membrane to accurately mimic the cell membrane. The effect of membrane composition has been overlooked in many studies of amyloid toxicity in model systems. By combining measurements of membrane binding, membrane permeabilization, and fiber formation, we show that lipids with the phosphatidylethanolamine (PE) headgroup strongly modulate the membrane disruption induced by IAPP (islet amyloid polypeptide protein), an amyloidogenic protein involved in type II diabetes. Our results suggest that PE lipids hamper the interaction of prefibrillar IAPP with membranes but enhance the membrane disruption correlated with the growth of fibers on the membrane surface via a detergent-like mechanism. These findings provide insights into the mechanism of membrane disruption induced by IAPP, suggesting a possible role of PE and other amyloids involved in other pathologies.

[1]  P. Magistretti,et al.  A42 Neurotoxicity Is Mediated by Ongoing Nucleated Polymerization Process Rather than by Discrete , 2011 .

[2]  Roland Winter,et al.  Elucidating the mechanism of lipid membrane-induced IAPP fibrillogenesis and its inhibition by the red wine compound resveratrol: a synchrotron X-ray reflectivity study. , 2009, Journal of the American Chemical Society.

[3]  R. Epand,et al.  Relationship of membrane curvature to the formation of pores by magainin 2. , 1998, Biochemistry.

[4]  P. Butler,et al.  Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. , 2008, Endocrine reviews.

[5]  N. Opitz,et al.  Fluorescence microscopy studies on islet amyloid polypeptide fibrillation at heterogeneous and cellular membrane interfaces and its inhibition by resveratrol , 2009, FEBS letters.

[6]  S. Jayasinghe,et al.  Structure of α-Helical Membrane-bound Human Islet Amyloid Polypeptide and Its Implications for Membrane-mediated Misfolding* , 2008, Journal of Biological Chemistry.

[7]  Maarten F. M. Engel,et al.  Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane , 2008, Proceedings of the National Academy of Sciences.

[8]  J. Vance Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids. , 2008, Journal of lipid research.

[9]  W. K. Cullen,et al.  Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo , 2002, Nature.

[10]  Gianluigi Veglia,et al.  Structures of rat and human islet amyloid polypeptide IAPP(1-19) in micelles by NMR spectroscopy. , 2008, Biochemistry.

[11]  Masato Kodaka,et al.  Requirements for generating sigmoidal time-course aggregation in nucleation-dependent polymerization model. , 2004, Biophysical chemistry.

[12]  D. W. Hayden,et al.  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. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Ayyalusamy Ramamoorthy,et al.  Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment. , 2011, Biochimica et biophysica acta.

[14]  Ayyalusamy Ramamoorthy,et al.  Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective. , 2012, Accounts of chemical research.

[15]  R. Winter,et al.  The effects of various membrane physical-chemical properties on the aggregation kinetics of insulin. , 2007, Chemistry and physics of lipids.

[16]  B. Kagan,et al.  Amyloid peptide pores and the beta sheet conformation. , 2010, Advances in experimental medicine and biology.

[17]  A. Miranker,et al.  Phospholipid catalysis of diabetic amyloid assembly. , 2004, Journal of molecular biology.

[18]  W. Cho,et al.  Cholesterol regulates assembly of human islet amyloid polypeptide on model membranes. , 2009, Journal of molecular biology.

[19]  Kevin Hartman,et al.  A single mutation in the nonamyloidogenic region of islet amyloid polypeptide greatly reduces toxicity. , 2008, Biochemistry.

[20]  Q. Fan,et al.  A Novel Action of Alzheimer's Amyloid β-Protein (Aβ): Oligomeric Aβ Promotes Lipid Release , 2001, The Journal of Neuroscience.

[21]  A. Miranker,et al.  The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes. , 2009, Annual review of biophysics.

[22]  Per Westermark,et al.  Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. , 2011, Physiological reviews.

[23]  Yen Sun,et al.  How type II diabetes-related islet amyloid polypeptide damages lipid bilayers. , 2012, Biophysical journal.

[24]  P. Devaux,et al.  High-resolution 31P-1H two-dimensional Nuclear Magnetic Resonance spectra of unsonicated lipid mixtures spinning at the magic-angle , 1996, European Biophysics Journal.

[25]  Sara M. Butterfield,et al.  Amyloidogenic Protein—Membrane Interactions: Mechanistic Insight from Model Systems , 2010 .

[26]  J. Brender,et al.  Induction of negative curvature as a mechanism of cell toxicity by amyloidogenic peptides: the case of islet amyloid polypeptide. , 2009, Journal of the American Chemical Society.

[27]  J. Brender,et al.  Membrane fragmentation by an amyloidogenic fragment of human Islet Amyloid Polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes. , 2007, Biochimica et biophysica acta.

[28]  J. Brender,et al.  Biphasic effects of insulin on islet amyloid polypeptide membrane disruption. , 2011, Biophysical journal.

[29]  Ruth Nussinov,et al.  β-Barrel topology of Alzheimer's β-amyloid ion channels. , 2010, Journal of molecular biology.

[30]  R. Riek,et al.  Mechanism of membrane interaction and disruption by α-synuclein. , 2011, Journal of the American Chemical Society.

[31]  P. Kinnunen,et al.  Islet amyloid polypeptide forms rigid lipid-protein amyloid fibrils on supported phospholipid bilayers. , 2008, Journal of molecular biology.

[32]  Ayyalusamy Ramamoorthy,et al.  Two-step mechanism of membrane disruption by Aβ through membrane fragmentation and pore formation. , 2012, Biophysical journal.

[33]  J. Kistler,et al.  The aggregation potential of human amylin determines its cytotoxicity towards islet β‐cells , 2006, The FEBS journal.

[34]  S. Jayasinghe,et al.  Lipid membranes modulate the structure of islet amyloid polypeptide. , 2005, Biochemistry.

[35]  A. Ramamoorthy,et al.  MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain. , 2003, Biophysical journal.

[36]  A. Miranker,et al.  Conserved and cooperative assembly of membrane-bound alpha-helical states of islet amyloid polypeptide. , 2006, Biochemistry.

[37]  Norbert Opitz,et al.  Interaction of hIAPP with Model Raft Membranes and Pancreatic β‐Cells: Cytotoxicity of hIAPP Oligomers , 2010, Chembiochem : a European journal of chemical biology.

[38]  D. Lomas,et al.  Conformational disease , 1997, The Lancet.

[39]  Helgi I. Ingólfsson,et al.  Lipid bilayer regulation of membrane protein function: gramicidin channels as molecular force probes , 2010, Journal of The Royal Society Interface.

[40]  A. Miranker,et al.  Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity , 2011, Proceedings of the National Academy of Sciences.

[41]  P. Lansbury,et al.  Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? , 2006, Quarterly Reviews of Biophysics.

[42]  S. Woods,et al.  Pancreatic signals controlling food intake; insulin, glucagon and amylin , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[43]  J. Brender,et al.  Association of highly compact type II diabetes related islet amyloid polypeptide intermediate species at physiological temperature revealed by diffusion NMR spectroscopy. , 2009, Journal of the American Chemical Society.

[44]  Chia-yu Lin,et al.  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 , 2007, Diabetes.

[45]  S. Ludtke,et al.  Effect of changing the size of lipid headgroup on peptide insertion into membranes. , 1997, Biophysical journal.

[46]  A. Jeremic,et al.  Clustering and Internalization of Toxic Amylin Oligomers in Pancreatic Cells Require Plasma Membrane Cholesterol* , 2011, The Journal of Biological Chemistry.

[47]  J C Stewart,et al.  Colorimetric determination of phospholipids with ammonium ferrothiocyanate. , 1980, Analytical biochemistry.

[48]  J. Brender,et al.  NMR structure in a membrane environment reveals putative amyloidogenic regions of the SEVI precursor peptide PAP(248-286). , 2009, Journal of the American Chemical Society.

[49]  Mun'delanji C. Vestergaard,et al.  Real-time observation of model membrane dynamics induced by Alzheimer's amyloid beta. , 2010, Biophysical chemistry.

[50]  A. Miranker,et al.  Concentration‐dependent transitions govern the subcellular localization of islet amyloid polypeptide , 2012, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[51]  A. Herrmann,et al.  Continuous measurement of rapid transbilayer movement of a pyrene-labeled phospholipid analogue. , 2000, Chemistry and physics of lipids.

[52]  J. Hofrichter,et al.  Sedimentation studies on human amylin fail to detect low-molecular-weight oligomers. , 2008, Biophysical journal.

[53]  J. Brender,et al.  Role of zinc in human islet amyloid polypeptide aggregation. , 2010, Journal of the American Chemical Society.

[54]  C. Dobson,et al.  Protein misfolding, functional amyloid, and human disease. , 2006, Annual review of biochemistry.

[55]  C. Tribet,et al.  Permeabilization of lipid membranes and cells by a light-responsive copolymer. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[56]  J. Brender,et al.  Helical conformation of the SEVI precursor peptide PAP248-286, a dramatic enhancer of HIV infectivity, promotes lipid aggregation and fusion. , 2009, Biophysical journal.

[57]  B. Bechinger,et al.  Detergent-like actions of linear amphipathic cationic antimicrobial peptides. , 2006, Biochimica et biophysica acta.

[58]  K. Matsuzaki,et al.  Ganglioside‐induced amyloid formation by human islet amyloid polypeptide in lipid rafts , 2009, FEBS letters.

[59]  T. Sparrman,et al.  Association of amyloid-β peptide with membrane surfaces monitored by solid state NMR , 2002 .

[60]  R. Nussinov,et al.  New structures help the modeling of toxic amyloidbeta ion channels. , 2008, Trends in biochemical sciences.

[61]  R. Winter,et al.  Suppression of IAPP fibrillation at anionic lipid membranes via IAPP-derived amyloid inhibitors and insulin. , 2010, Biophysical chemistry.

[62]  P. Lansbury,et al.  Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes. , 2002, Biochemistry.

[63]  F. Kirchhoff,et al.  Semen-Derived Amyloid Fibrils Drastically Enhance HIV Infection , 2007, Cell.

[64]  Maarten F. M. Engel,et al.  Islet amyloid polypeptide‐induced membrane leakage involves uptake of lipids by forming amyloid fibers , 2004, FEBS letters.

[65]  T. Rephann,et al.  Association , 1973, ACM SIGSPATIAL International Workshop on Advances in Geographic Information Systems.

[66]  R. Kayed,et al.  Permeabilization of Lipid Bilayers Is a Common Conformation-dependent Activity of Soluble Amyloid Oligomers in Protein Misfolding Diseases* , 2004, Journal of Biological Chemistry.

[67]  M. Masserini,et al.  Abeta Peptide Toxicity is Reduced After Treatments Decreasing Phosphatidylethanolamine Content in Differentiated Neuroblastoma Cells , 2011, Neurochemical Research.

[68]  P. S. St George-Hyslop,et al.  α-Synuclein Membrane Interactions and Lipid Specificity* , 2000, The Journal of Biological Chemistry.

[69]  Amedeo Caflisch,et al.  Amyloid aggregation on lipid bilayers and its impact on membrane permeability. , 2009 .

[70]  J. Brender,et al.  Amyloid fiber formation and membrane disruption are separate processes localized in two distinct regions of IAPP, the type-2-diabetes-related peptide. , 2008, Journal of the American Chemical Society.

[71]  S. Ji,et al.  Intra-membrane Oligomerization and Extra-membrane Oligomerization of Amyloid-β Peptide Are Competing Processes as a Result of Distinct Patterns of Motif Interplay* , 2011, The Journal of Biological Chemistry.

[72]  Maarten F. M. Engel,et al.  Islet amyloid polypeptide inserts into phospholipid monolayers as monomer. , 2006, Journal of molecular biology.

[73]  Jie Li,et al.  The Association of α-Synuclein with Membranes Affects Bilayer Structure, Stability, and Fibril Formation* , 2003, Journal of Biological Chemistry.

[74]  C. La Rosa,et al.  Self‐Assembling Pathway of HiApp Fibrils within Lipid Bilayers , 2010, Chembiochem : a European journal of chemical biology.

[75]  U. Aebi,et al.  Atomic force microscopy reveals defects within mica supported lipid bilayers induced by the amyloidogenic human amylin peptide. , 2004, Journal of molecular biology.

[76]  P. Janmey,et al.  Biophysical properties of lipids and dynamic membranes. , 2006, Trends in cell biology.