Electron tomography reveals the fibril structure and lipid interactions in amyloid deposits

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

Volumn 113, Issue 20, 2016, Pages 5604-5609

  Kollmer, Marius ^a   Meinhardt, Katrin ^a   Haupt, Christian ^a   Liberta, Falk ^a   Wulff, Melanie ^a   Linder, Julia ^a   Handl, Lisa ^a   Heinrich, Liesa ^b   Loos, Cornelia ^a   Schmidt, Matthias ^a   Syrovets, Tatiana ^a   Simmet, Thomas ^a   Westermark, Per ^c   Westermark, Gunilla T ^d   Horn, Uwe ^b   Schmidt, Volker ^a   Walther, Paul ^a   Fändrich, Marcus ^a  

^a UNIVERSITY OF ULM   (Germany)

^b HANS KNÖLL INSTITUTE   (Germany)

^c UPPSALA UNIVERSITY   (Sweden)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

Aggregation; Conformational disease; Electron tomography; Prion; Protein assembly

Indexed keywords

AMYLOID A PROTEIN; LIPID; AMYLOID; LIPID BILAYER; SAA1 PROTEIN, HUMAN; SERUM AMYLOID A;

AMYLOIDOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CELL INCLUSION; CELL STRUCTURE; ELECTRON TOMOGRAPHY; FEMALE; LIPID BILAYER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SCANNING TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CHEMISTRY; PROCEDURES; ULTRASTRUCTURE;

AMYLOID; ANIMALS; CELLS, CULTURED; ELECTRON MICROSCOPE TOMOGRAPHY; FEMALE; LIPID BILAYERS; LIPIDS; MICE; SERUM AMYLOID A PROTEIN;

EID: 84970016674     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1523496113     Document Type: Article

References (52)

1. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366.
2. Sipe JD, et al. (2014) Nomenclature 2014: Amyloid fibril proteins and clinical classification of the amyloidosis. Amyloid 21(4):221-224.
3. Hazenberg BP (2013) Amyloidosis: A clinical overview. Rheum Dis Clin North Am 39(2): 323-345.
4. Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148(6):1188-1203.
5. Fändrich M, Schmidt M, Grigorieff N (2011) Recent progress in understanding Alzheimer's β-amyloid structures. Trends Biochem Sci 36(6):338-345.
6. Pepys MB (2006) Amyloidosis. Annu Rev Med 57:223-241.
7. Obici L, Merlini G (2012) AA amyloidosis: Basic knowledge, unmet needs and future treatments. Swiss Med Wkly 142:w13580.
8. Bergström J, et al. (2005) Amyloid deposits in transthyretin-derived amyloidosis: Cleaved transthyretin is associated with distinct amyloid morphology. J Pathol 206(2):224-232.
9. Thal DR, Walter J, Saido TC, Fändrich M (2015) Neuropathology and biochemistry of Aβ and its aggregates in Alzheimer's disease. Acta Neuropathol 129(2):167-182.
10. Baumeister W (2004) Mapping molecular landscapes inside cells. Biol Chem 385(10):865-872.
11. Shirahama T, et al. (1990) Amyloid enhancing factor-loaded macrophages in amyloid fibril formation. Lab Invest 62(1):61-68.
12. Kluve-Beckerman B, Manaloor J, Liepnieks JJ (2001) Binding, trafficking and accumulation of serum amyloid A in peritoneal macrophages. Scand J Immunol 53(4):393-400.
13. Elimova E, Kisilevsky R, Szarek WA, Ancsin JB (2004) Amyloidogenesis recapitulated in cell culture: A peptide inhibitor provides direct evidence for the role of heparan sulfate and suggests a new treatment strategy. FASEB J 18(14):1749-1751.
14. Westermark GT, Fändrich M, Westermark P (2015) AA amyloidosis: Pathogenesis and targeted therapy. Annu Rev Pathol 10:321-344.
15. Kluve-Beckerman B, Liepnieks JJ, Wang L, Benson MD (1999) A cell culture system for the study of amyloid pathogenesis. Amyloid formation by peritoneal macrophages cultured with recombinant serum amyloid A. Am J Pathol 155(1):123-133.
16. Gellermann GP, et al. (2005) Raft lipids as common components of human extracellular amyloid fibrils. Proc Natl Acad Sci USA 102(18):6297-6302.
17. Röcken C, Shakespeare A (2002) Pathology, diagnosis and pathogenesis of AA amyloidosis. Virchows Arch 440(2):111-122.
18. Derebe MG, et al. (2014) Serum amyloid A is a retinol binding protein that transports retinol during bacterial infection. eLife 3:e03206.
19. Lu J, Yu Y, Zhu I, Cheng Y, Sun PD (2014) Structural mechanism of serum amyloid A-mediated inflammatory amyloidosis. Proc Natl Acad Sci USA 111(14):5189-5194.
20. Haupt C, et al. (2011) Pattern recognition with a fibril-specific antibody fragment reveals the surface variability of natural amyloid fibrils. J Mol Biol 408(3):529-540.
21. Curtis H, Barnes SN (1989) Biology (Worth Publishers, New York), 5th Ed.
22. Hine R (1999) Membrane. The Facts on File Dictionary of Biology (Checkmark, New York), 3rd Ed.
23. Kuchel PW, Ralston GB (1988) Theory and Problems of Biochemistry, Schaum's Outlines (McGraw-Hill, New York).
24. Sorenson GD, Bari WA (1968) Murine amyloid deposits and cellular relationships. Amyloidosis, eds Mandema E, Ruinen L, Scholten JH, Cohen AS (Excerpta Medica, Amsterdam), pp 58-73.
25. Butterfield SM, Lashuel HA (2010) Amyloidogenic protein-membrane interactions: Mechanistic insight from model systems. Angew Chem Int Ed Engl 49(33):5628-5654.
26. Meier C, Weil T, Kirchhoff F, Münch J (2014) Peptide nanofibrils as enhancers of retroviral gene transfer. Wiley Interdiscip Rev Nanomed Nanobiotechnol 6(5):438-451.
27. Westermark P (2015) Localized amyloidoses and amyloidoses associated with aging outside the central nervous system. Amyloid and Related Disorders Current Clinical Pathology, eds Picken MM, et al. (Springer, Cham, Switzerland), pp 95-120.
28. Wisniewski HM, Wegiel J, Wang KC, Lach B (1992) Ultrastructural studies of the cells forming amyloid in the cortical vessel wall in Alzheimer's disease. Acta Neuropathol 84(2):117-127.
29. Gondo T, et al. (1993) Localized amyloidosis in squamous cell carcinoma of uterine cervix: electron microscopic features of nodular and star-like amyloid deposits. Virchows Arch A Pathol Anat Histopathol 422(3):225-231.
30. Romhányi G (1949) Ueber die submikroskopische Struktur des Amyloids. Schweiz Z Pathol Bakteriol 12(3):253-262. German.
31. Shirahama T, Cohen AS (1973) An analysis of the close relationship of lysosomes to early deposits of amyloid. Ultrastructural evidence in experimental mouse amyloidosis. Am J Pathol 73(1):97-114.
32. Stalder M, Deller T, Staufenbiel M, Jucker M (2001) 3D-Reconstruction of microglia and amyloid in APP23 transgenic mice: No evidence of intracellular amyloid. Neurobiol Aging 22(3):427-434.
33. Saibil HR, et al. (2012) Heritable yeast prions have a highly organized three-dimensional architecture with interfiber structures. Proc Natl Acad Sci USA 109(37):14906-14911.
34. Hurbain I, et al. (2008) Electron tomography of early melanosomes: Implications for melanogenesis and the generation of fibrillar amyloid sheets. Proc Natl Acad Sci USA 105(50):19726-19731.
35. Mangione PP, et al. (2013) Structure, folding dynamics, and amyloidogenesis of D76N β2-microglobulin: Roles of shear flow, hydrophobic surfaces, and α-crystallin. J Biol Chem 288(43):30917-30930.
36. Cohlberg JA, Li J, Uversky VN, Fink AL (2002) Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from α-synuclein in vitro. Biochemistry 41(5):1502-1511.
37. Galvagnion C, et al. (2015) Lipid vesicles trigger α-synuclein aggregation by stimulating primary nucleation. Nat Chem Biol 11(3):229-234.
38. Cohen SI, Vendruscolo M, Dobson CM, Knowles TP (2012) From macroscopic measurements to microscopic mechanisms of protein aggregation. J Mol Biol 421(2-3):160-171.
39. Andersen CB, et al. (2009) Branching in amyloid fibril growth. Biophys J 96(4):1529-1536.
40. Ban T, et al. (2006) Real-time and single fibril observation of the formation of amyloid beta spherulitic structures. J Biol Chem 281(44):33677-33683.
41. Krebs MR, Domike KR, Donald AM (2009) Protein aggregation: More than just fibrils. Biochem Soc Trans 37(Pt 4):682-686.
42. Schmidt M, et al. (2015) Peptide dimer structure in an Aβ(1-42) fibril visualized with cryo-EM. Proc Natl Acad Sci USA 112(38):11858-11863.
43. Milanesi L, et al. (2012) Direct three-dimensional visualization of membrane disruption by amyloid fibrils. Proc Natl Acad Sci USA 109(50):20455-20460.
44. Vauthey S, Santoso S, Gong H, Watson N, Zhang S (2002) Molecular self-assembly of surfactant-like peptides to form nanotubes and nanovesicles. Proc Natl Acad Sci USA 99(8):5355-5360.
45. Cherny I, Gazit E (2008) Amyloids: Not only pathological agents but also ordered nanomaterials. Angew Chem Int Ed Engl 47(22):4062-4069.
46. Bolisetty S, Mezzenga R (2016) Amyloid-carbon hybrid membranes for universal water purification. Nat Nanotechnol 11(4):365-371.
47. Kelley CT (1995) Iterative Methods for Linear and Nonlinear Equations (SIAM, Philadelphia).
48. Lundmark K, Vahdat Shariatpanahi A, Westermark GT (2013) Depletion of spleen macrophages delays AA amyloid development: A study performed in the rapid mouse model of AA amyloidosis. PLoS One 8(11):e79104.
49. Ganowiak K, Hultman P, Engström U, Gustavsson A, Westermark P (1994) Fibrils from synthetic amyloid-related peptides enhance development of experimental AA-amyloidosis in mice. Biochem Biophys Res Commun 199(1):306-312.
50. Silverman BW (1986) Density Estimation for Statistics and Data Analysis (CRC, London).
51. Scott DW (2015) Multivariate Density Estimation: Theory, Practice and Visualization (Wiley, New York), 2nd Ed.
52. Snyder JP (1987) Map Projections - A Working Manual (U.S. Government Publishing Office, Washington, DC).