Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 16, 2008, Pages 6033-6038

  Engel, Maarten F M ^a,b   Khemtémourian, Lucie ^b   Kleijer, Cécile C ^b   Meeldijk, Hans J D ^c   Jacobs, Jet ^a   Verkleij, Arie J ^c   De Kruijff, Ben ^b   Killian, J Antoinette ^b   Höppener, Jo W M ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Amylin; Amyloid cytotoxicity; Large unilamellar vesicles; Protein membrane interaction; Type 2 diabetes mellitus

Indexed keywords

AMYLIN; AMYLOID; INSULIN;

ARTICLE; CELL GROWTH; CELL SURFACE; ELECTRON MICROSCOPY; FIBER; KINETICS; MEMBRANE DAMAGE; MOLECULAR MECHANICS; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN INTERACTION; ANIMAL; CELL MEMBRANE; DRUG EFFECT; HUMAN; METABOLISM; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PATHOLOGY; ULTRASTRUCTURE;

AMYLOID; ANIMALS; CELL MEMBRANE; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN; INSULIN-SECRETING CELLS; KINETICS; MICE; MICROSCOPY, ELECTRON;

EID: 43149118349     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0708354105     Document Type: Article

References (48)

1. Höppener JWM, Ahrén B, Lips CJM (2000) Islet amyloid and type 2 diabetes mellitus. N Engl J Med 343:411-419.
2. Mirzabekov TA, Lin MC, Kagan, BL (1996) Pore formation by the cytotoxic islet amyloid peptide amylin. J Biol Chem 271:1988-1992.
3. Quist A, et al. (2005) Amyloid ion channels: A common structural link for protein-misfolding disease. Proc Natl Acad Sci USA 102:10427-10432.
4. Anguiano M, Nowak RJ, Lansbury PT, Jr (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.
5. Porat Y, Kolusheva S, Jelinek R, Gazit E (2003) The human islet amyloid polypeptide forms transient membrane-active prefibrillar assemblies. Biochemistry 42:10971-10977.
6. Kayed R, et al. (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. Janson J, et al. (1999) The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 48:491-498.
8. Meier JJ, et al. (2006) Inhibition of hIAPP fibril formation does not prevent beta-cell death: Evidence for distinct actions of oligomers and fibrils of hIAPP. Am J Physiol 291:E1317-E1324.
9. Knight JD, Hebda JA, Miranker AD (2006) Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide. Biochemistry 45:9496-9508.
10. Kourie JI, et al. (2002) Heterogeneous amyloid-formed ion channels as a common cytotoxic mechanism: Implications for therapeutic strategies against amyloidosis. Cell Biochem Biophys 36:191-207.
11. Arispe N, Pollard HB, Rojas E (1993) Giant multilevel cation channels formed by Alzheimer disease amyloid β-protein [Aβ P-(1- 40)] in bilayer membranes. Proc Natl Acad Sci USA 90:10573-10577.
12. Sparr E, et al. (2004) Islet amyloid polypeptide-induced membrane leakage involves uptake of lipids by forming amyloid fibers. FEBS Lett 577:117-120.
13. Demuro A, et al. (2005) Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J Biol Chem 280:17294-17300.
14. Green JD, et al. (2004) Atomic force microscopy reveals defects within mica supported lipid bilayers induced by the amyloidogenic human amylin peptide. J Mol Biol 342:877-887.
15. Brender JR, et al. (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.
16. Okada T, Wakabayashi M, Ikeda K, Matsuzaki K (2007) Formation of toxic fibrils of Alzheimer's amyloid β-protein-(1- 40) by monosialoganglioside GM1, a neuronal membrane component. J Mol Biol 371:481-489.
17. Novitskaya V, Bocharova OV, Bronstein I, Baskakov IV (2006) Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. J Biol Chem 281:13828-13836.
18. Gharibyan AL, et al. (2006) Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways. J Mol Biol 365:1337-1349.
19. McLaurin J, Chakrabartty A (1996) Membrane disruption by Alzheimer β-amyloid peptides mediated through specific binding to either phospholipids or gangliosides: Implications for neurotoxicity. J Biol Chem 271:26482-26489.
20. LeVine H, III (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T. Methods Enzymol 309:274-284.
21. Padrick SB, Miranker AD (2002) Islet amyloid: Phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis. Biochemistry 41:4694-4703.
22. Jayasinghe SA, Langen R (2005) Lipid membranes modulate the structure of islet amyloid polypeptide. Biochemistry 44:12113-12119.
23. Ruschak AM, Miranker AD (2007) Fiber-dependent amyloid formation as catalysis of an existing reaction pathway. Proc Natl Acad Sci USA 104:12341-12346.
24. Ferrone FA, Hofrichter J, Eaton WA (1985) Kinetics of sickle hemoglobin polymerization. II. A double nucleation mechanism. J Mol Biol 183:611-631.
25. Harper JD, Lansbury PT (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 66:385-407.
26. Knight JD, Miranker AD (2004) Phospholipid catalysis of diabetic amyloid assembly. J Mol Biol 341:1175-1187.
27. O'Nuallain B, Williams AD, Westermark P, Wetzel R (2004) Seeding specificity in amyloid growth induced by heterologous fibrils. J Biol Chem 279:17490-17499.
28. Kelly JW (2000) Mechanisms of amyloidogenesis. Nat Struct Biol 7:824-826.
29. Westermark P, et al. (1996) Effects of beta cell granule components on human islet amyloid polypeptide fibril formation. FEBS Lett 379:203-206.
30. Jaikaran ETAS, Nilsson MR, Clark A (2004) Pancreatic beta-cell granule peptides form heteromolecular complexes which inhibit islet amyloid polypeptide fibril formation. Biochem J 377:709-716.
31. Kudva YC, Mueske C, Butler PC, Eberhardt NL (1998) A novel assay in vitro of human islet amyloid polypeptide amyloidogenesis and effects of insulin secretory vesicle peptides on amyloid formation. Biochem J 331:809-813.
32. Gilead S, Wolfenson H, Gazit E (2006) Molecular mapping of the recognition interface between the islet amyloid polypeptide and insulin. Angew Chem Int Ed 45:6476-6480.
33. Sumner Makin O, Serpell LC (2004) Structural characterisation of islet amyloid polypeptide fibrils. J Mol Biol 335:1279-1288.
34. Goldsbury C, et al. (2000) Amyloid fibril formation from full-length and fragments of amylin. J Struct Biol 130:352-362.
35. Kayed R, et al. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489.
36. Engel MFM, et al. (2006) Islet amyloid polypeptide inserts into phospholipid monolayers as monomer. J Mol Biol 356:783-789.
37. Lopes DHJ, et al. (2007) Mechanism of IAPP fibrillation at lipid interfaces studied by infrared reflection absorption spectroscopy (IRRAS). Biophys J 93:3132-3141.
38. Zhao H, Tuominen EKJ, Kinnunen PKJ (2004) Formation of amyloid fibers triggered by phosphatidylserine-containing membranes. Biochemistry 43:10302-10307.
39. Gellermann GP, et al. (2005) Raft lipids as common components of human extracellular amyloid fibrils. Proc Natl Acad Sci USA 102:6297-6302.
40. Rustenbeck I, Matthies A, Lenzen S (1994) Lipid composition of glucose-stimulated pancreatic islets and insulin-secreting tumor cells. Lipids 29:685-692.
41. Rensink AAM, et al. (2004) Insulin inhibits amyloid β-induced cell death in cultured human brain pericytes. Neurobiol Aging 25:93-103.
42. Westermark P (1973) Fine structure of islets of Langerhans in insular amyloidosis. Virchows Archiv A Pathol Anat Histopathol 359:1-18.
43. Clark A, et al. (1987) Islet amyloid formed from diabetes-associated peptide may be pathogenic in type 2 diabetes. Lancet 330:231-234.
44. Lorenzo A, Razzaboni B, Weir GC, Yankner BA (1994) Pancreatic islet cell toxicity of amylin associated with type 2 diabetes mellitus. Nature 368:756-760.
45. O'Brien TD, et al. (1995) Human islet amyloid polypeptide expression in COS-1 cells: A model of intracellular amyloidogenesis. Am J Pathol 147:609-616.
46. Hiddinga HJ, Eberhardt NL (1999) Intracellular amyloidogenesis by human islet amyloid polypeptide induces apoptosis in COS-1 cells. Am J Pathol 154:1077-1088.
47. Saafi EL, et al. (2001) Ultrastructural evidence that apoptosis is the mechanism by which human amylin evokes death in RINm5F pancreatic islet beta-cells. Cell Biol Int 25:339-350.
48. Hasper HE, et al. (2006) An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science 313:1636-1637.