The effect of Aβ on IAPP aggregation in the presence of an isolated β-cell membrane

Journal of Molecular Biology

Volumn 421, Issue 2-3, 2012, Pages 348-363

  Seeliger, Janine ^a   Weise, Katrin ^a   Opitz, Norbert ^b   Winter, Roland ^a  

^a TU DORTMUND UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

AFM; amyloid; ATR FTIR spectroscopy; fluorescence microscopy; peptide membrane interaction

Indexed keywords

AMYLIN; AMYLOID BETA PROTEIN; ANION;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ISOLATION; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; COMPLEX FORMATION; FLUORESCENCE MICROSCOPY; INFRARED SPECTROSCOPY; INSULINOMA; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; RAT;

RATTUS;

EID: 84863983553     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.01.048     Document Type: Article

References (46)

1. Dobson C.M. Protein folding and misfolding Nature 426 2003 884 890
2. Morgado I., and Fändrich M. Assembly of Alzheimer's Aβ peptide into nanostructured amyloid fibrils Curr. Opin. Colloid Interface Sci. 16 2001 508 514
3. Eichner T., and Radford S.E. A diversity of assembly mechanisms of a generic amyloid fold Mol. Cell 43 2011 8 18
4. Westermark P. Aspects on human amyloid forms and their fibril polypeptides FEBS J. 272 2005 5942 5949
5. DeToma A.S., Salamekh S., Ramamoorthy A., and Lim M.H. Misfolded proteins in Alzheimer's disease and type II diabetes Chem. Soc. Rev. 41 2012 608 621
6. Westermark P., Wernstedt C., Wilander E., Hayden D.W., O'Brien T.D., and Johnson K.H. 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. USA 84 1987 3881 3885
7. Cooper G.J.S., Willis A.C., Clark A., Turner R.C., Sim R.B., and Reid K.B.M. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients Proc. Natl Acad. Sci. USA 84 1987 8628 8632
8. Nishi M., Sanke T., Nagamatsu S., Bell G.I., and Steiner D.F. Islet amyloid polypeptide - a new β cell secretory product related to islet amyloid deposits J. Biol. Chem. 265 1990 4173 4176
9. Glenner G.G., and Wong C.W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein Biochem. Biophys. Res. Commun. 120 1984 885 890
10. Selkoe D.J., Abraham C.R., Podlisny M.B., and Duffy L.K. Isolation of low-molecular-weight proteins from amyloid plaque fibers in Alzheimer's disease J. Neurochem. 146 1986 1820 1834
11. Khemtémourian L., Killian J.A., Höppener J.W.M., and Engel M.F.M. Recent insights in islet amyloid polypeptide-induced membrane disruption and its role in β-cell death in type 2 diabetes mellitus Exp. Diabetes Res. 2008 10.1155/2008/421287
12. Höppener J.W., and Lips C.J. Role of islet amyloid in type 2 diabetes mellitus Int. J. Biochem. Cell Biol. 38 2006 726 736
13. Janson J., Laedtke T., Parisi J.E., O'Brien P., Petersen R.C., and Butler P.C. Increased risk of type 2 diabetes in Alzheimer disease Diabetes 53 2004 474 481
14. Sims-Robinson C., Kim B., Rosko A., and Feldman E.L. How does diabetes accelerate Alzheimer disease pathology? Nat. Rev., Neurol. 6 2010 551 559
15. O'Nuallain B., Williams A.D., Westermark P., and Wetzel R. Seeding specificity in amyloid growth induced by heterologous fibrils J. Biol. Chem. 279 2004 17490 17499
16. Yan L.M., Velkova A., Tatarek-Nossol M., Andreetto E., and Kapurniotu A. IAPP mimic blocks Aβ cytotoxic self-assembly: cross-suppression of amyloid toxicity of Aβ and IAPP suggests a molecular link between Alzheimer's disease and type II diabetes Angew. Chem., Int. Ed. 46 2007 1246 1252
17. Turk J., Wolf B.A., Lefkowith J.B., Stump W.T., and McDaniel M.L. Glucose-induced phospholipid hydrolysis in isolated pancreatic islets: quantitative effects on the phospholipid content of arachidonate and other fatty acids Biochim. Biophys. Acta 879 1986 399 409
18. Hallberg A. Effects of starvation and different culture conditions on the phospholipid content of isolated pancreatic islets Biochim. Biophys. Acta 796 1984 328 335
19. Reis O., Winter R., and Zerda T.W. The effect of high external pressure on DPPC-cholesterol multilamellar vesicles: a pressure-tuning Fourier transform infrared spectroscopy study Biochim. Biophys. Acta, Biomembr. 1279 1996 5 16
20. Reis O., and Winter R. Pressure and temperature effects on conformational and hydrational properties of lamellar and bicontinuous cubic phases of the fully hydrated monoacylglyceride monoelaidin - a Fourier transform-infrared spectroscopy study using the diamond anvil technique Langmuir 14 1998 2903 2909
21. Wong P.T., Schauerte J.A., Wisser K.C., Ding H., Lee E.L., Steel D.G., and Gafni A. Amyloid-β membrane binding and permeabilization are distinct processes influenced separately by membrane charge and fluidity J. Mol. Biol. 286 2009 81 96
22. Valincius G., Heinrich F., Budvytyte R., Vanderah D.J., McGillivray D.J., and Sokolov Y. Soluble amyloid β-oligomers affect dielectric membrane properties by bilayer insertion and domain formation: implications for cell toxicity Biophys. J. 95 2008 4845 4861
23. Kapoor S., Werkmüller A., Denter C., Zhai Y., Markgraf J., and Weise K. Temperature-pressure phase diagram of a heterogeneous anionic model biomembrane system: results from a combined calorimetry, spectroscopy and microscopy study Biochim. Biophys. Acta, Biomembr. 1808 2011 1187 1195
24. Seeliger J., Evers F., Jeworrek C., Kapoor S., Weise K., and Andreetto E. Cross-amyloid interaction of Aβ and IAPP at lipid membranes Angew. Chem., Int. Ed. 51 2012 679 683
25. Weise K., Radovan D., Gohlke A., Opitz N., and Winter R. Interaction of hIAPP with model raft membranes and pancreatic β-cells: cytotoxicity of hIAPP oligomers ChemBioChem 11 2010 1280 1290
26. Knight J.D., and Miranker A.D. Phospholipid catalysis of diabetic amyloid assembly J. Mol. Biol. 341 2004 1175 1187
27. Jha S., Sellin D., Seidel R., and Winter R. Amyloidogenic propensities and conformational properties of ProIAPP and IAPP in the presence of lipid bilayer membranes J. Mol. Biol. 389 2009 907 920
28. Hebda J.A., and Miranker A.D. The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes Annu. Rev. Biophys. 38 2009 125 152
29. Evers F., Jeworrek C., Tiemeyer S., Weise K., Sellin D., and Paulus M. 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 2009 9516 9521
30. Lopes D.H.J., Meister A., Gohlke A., Hauser A., Blume A., and Winter R. Mechanism of islet amyloid polypeptide fibrillation at lipid interfaces studied by infrared reflection absorption spectroscopy Biophys. J. 93 2007 3132 3141
31. Jayasinghe S.A., and Langen R. Lipid membranes modulate the structure of islet amyloid polypeptide Biochemistry 44 2005 12113 12119
32. McLaurin J., and Chakrabartty A. Characterization of the interactions of Alzheimer β-amyloid peptides with phospholipid membranes Eur. J. Biochem. 245 1997 355 363
33. Williams T.L., and Serpell L.C. Membrane and surface interactions of Alzheimer's Aβ peptide - insights into the mechanism of cytotoxicity FEBS J. 278 2011 3905 3917
34. Sani M.A., Gehman J.D., and Separovic F. Lipid matrix plays a role in Abeta fibril kinetics and morphology FEBS Lett. 585 2011 749 754
35. Curtain C.C., Ali F.E., Smith D.G., Bush A.I., Masters C.L., and Barnham K.J. Metal ions, pH, and cholesterol regulate the interactions of Alzheimer's disease amyloid-β peptide with membrane lipid J. Biol. Chem. 278 2003 2977 2982
36. Andreetto E., Yan L.M., Tatarek-Nossol M., Velkova A., Frank R., and Kapurniotu A. 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 2010 3081 3085
37. Merglen A., Theander S., Rubi B., Chaffard G., Wollheim C.B., and Maechler P. Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells Endocrinology 145 2004 667 678
38. Bligh E.G., and Dyer W.J. A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
39. Bartlett G.R. Colorimetric assay methods for free and phosphorylated glyceric acids J. Biol. Chem. 234 1959 469 471
40. Tatulian S.A. Attenuated total reflection Fourier transform infrared spectroscopy: a method of choice for studying membrane proteins and lipids Biochemistry 42 2003 11898 11907
41. Cordeiro Y., Kraineva J., Suarez M.C., Tempesta A.G., Kelly J.W., and Silva J.L. Fourier transform infrared spectroscopy provides a fingerprint for the tetramer and for the aggregates of transthyretin Biophys. J. 91 2006 957 967
42. Cordeiro Y., Kraineva J., Gomes M.P.B., Lopes M.H., Martins V.R., and Lima L.M.T.R. The amino-terminal PrP domain is crucial to modulate prion misfolding and aggregation Biophys. J. 89 2005 2667 2676
43. Angelova M.J., and Dimitrov D.S. Liposome electroformation Faraday Discuss. Chem. Soc. 81 1987 303 311
44. Dimitrov D.S., and Angelova M.J. Lipid swelling and liposome formation mediated by electric fields Bioelectrochem. Bioenerg. 19 1988 323 333
45. Ambroggio E.E., and Bagatolli L.A. Giant unilamellar vesicles, fluorescence microscopy and lipid-peptide interactions M.A.R.B. Castanho, Membrane-Active Peptides: Methods and Results on Structure and Function 2009 International University Line La Jolla, CA 169
46. Nielsen L., Khurana R., Coats A., Frokjaer S., Brange J., and Vyas S. Effect of environmental factors on the kinetics of insulin fibril formation: elucidation of the molecular mechanism Biochemistry 40 2001 6036 6046