JBB2026, Dec 2, Amyloid structure and assembly
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1 JBB2026, Dec 2, Amyloid structure and assembly Disordered Folded? Douglas and Dillin, 2010, J. Cell. Biol. Cell death Loss of organ function Disease pathogenesis Vendruscolo et al, Cold Spring Harbor Perspectives, 2011
2 Amyloid Macroscopic deposits of beta-sheet rich protein aggregates, classically extracellular. Also refers to a specific fibrillar protein architecture (cross-beta) observed in amyloid deposits. Originally described as being similar to starch (amylum), on the basis of iodine staining (Rudolph Virchow, 1854) Shown to be protein deposits in tissue (Friedreich and Kekule, 1859) Fibrillar protein deposits observed in brains of dementia patients (Alois Alzheimer, 1907) Congo red staining introduced as a diagnostic method (Bennhold, 1922) Electron microscopy reveals the fibrillar structure of amyloid (Cohen and Calkins, 1959) X-ray diffraction used to show the beta-pleated sheet structure of amyloid fibrils (Eanes and Glenner, 1968) High resolution structural details of amyloids begin to emerge (2000 present, numerous groups)
3 Amyloid diseases Tau filaments in CTE (chronic traumatic enchephalitis) Spongiosis as a result of PrP misfolding In prion diseases (here CJD) Β-islet cell death in type II diabetes (amyloid aggregation of amylin) Deposition of beta-2 microglobulin In dialysis-related amyloidosis
4 Human amyloid diseases
5 Structural diversity of disease related amyloid proteins Jahn & Radford (2008) Arch. Biochem. Biophys. 469:
6 Amyloid fibrils from diverse proteins share a common architecture NH 2 ISFLIF-COOH -synuclein fibrils (Parkinson s) Lashuel et al. (2002) J. Mol. Biol. Cross-beta structure beta strands perpendicular to the long axis of the fibril Tycko, Biochemistry, 2006
7 Functional amyloids Pmel17 amyloid plays a key role in melanocyte and melanin deposition Neuronal cytoplasmic polyadenylation element binding protein (CPEB) protein from Aplysia can form prion/amyloid like assemblies in yeast that provide self-perpetuating biochemical memories Heinrich & Lindquist (2011) PNAS 108, Pfefferkorn et al. (2010) PNAS 107, Similarly, amyloid-like oligomers formed by the Drosophila Orb2 protein play a role in the persistence of memory Majumdar et al., 2012, Cell 148:
8 Functional amyloids Adhesion molecules from bacterial (eg. E. coli curli filaments) and yeast pathogens contain amyloid architecture. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Prion proteins in yeast are capable of forming infectious amyloid structures and have also been assigned to biological functions. Li et al (2012) Cell 150,
9 Amyloid fibrils are significantly more stable than the native state Jahn & Radford (2008) Arch. Biochem. Biophys. 469: It has recently been shown that the native folds of proteins are metastable relative to amyloid fibrils. In other words, amyloid fibrils are the state with the lowest ΔG. To understand why this is true, we need to look at the atomic structures of amyloid fibrils.
10 Structural details of amyloid fibrils Low resolution morphological information can be obtained using transmission electron microscopy or atomic force microscopy (in some cases negative stain TEM or AFM can provide information regarding twisting or bundling of fibrils). Higher resolution techniques are required to obtain molecular details of amyloid structure. AFM of 2-microglubulin fibrils TEM of A (1-42) fibrils
11 Congo red Congo Red The classic diagnostic tool for amyloid deposition in tissue is staining with Congo Red. Planar aromatic molecules of this type are though to bind in an ordered fashion to the extended cross- structure, altering spectroscopic properties. In addition to staining red, CR bound to amyloid exhibits a green-gold birefingence under polarized light. SAA amyloidosis of the trachea Turkstra et al., 2008, Clin. Rheumatol. 27:
12 FTIR is a useful tool for monitoring secondary structure
13 Structural details of amyloid fibrils X ray fibre diffraction Vanderbilt U.
14 Structural details of amyloid fibrils X ray crystallography Vanderbilt U.
15 Structural details of amyloid fibrils X ray fibre diffraction Can only report on regular repeating units primarily interstrand and intersheet spacing. Diagnostic test for the presence of cross- architecture due to the characteristic reflections. Greenwald & Riek, 2010, Structure 18:
16 Structural details of amyloid fibrils X-ray crystallography Landau et al., 2011, PLoS Biol, 9:e So far, crystal structures have been limited to amyloid peptides 6-8 residues in length. Absolute requirement for homogeneous structure/packing throughout the crystal. Assumption is that crystal packing recapitulates protofibril architecture (in at least one case this has been proven false). Has allowed very high resolution details of cross-beta core structure to be observed.
17 Steric zipper motifs define packing modes within hydrophobic core Based on possible arrangements of the beta-strands within a fibril, Sawaya et al. proposed a set of 8 possible packing motifs. These are termed steric zippers due to the exclusion of water. Interfaces are stabilized by backbone hydrogen bonding along the fibril axis and optimal van der Waals packing between sheets. Polar residues are either located on the outer (non dehydrated) face, or involved in extensive hydrogen bonding. Sawaya et al., 2007, Nature 447:
18 Steric zipper motifs define packing modes within hydrophobic core Eisenberg and Jucker, 2012, Cell 148:
19 Structural details of amyloid fibrils cryo electron microscopy Application of single-particle analysis techniques allows averaging of electron density along the length of amyloid fibrils, providing detailed maps with nm resolution. NMR structures can be docked into these to provide complete picture of fibril structure. -2-microglobulin fibrils White et al., 2009, J. Mol. Biol. 389:48-57
20 Structural details of amyloid fibrils cryo electron microscopy Mature fibril composed of 2 protofilaments Morgado and Fandrich, 2011, Curr. Opin. Coll. Int. Sci.
21 NMR spectroscopy + 1 H- 1 H distances - 2 o, 3 o, 4 o structure Chemical shifts = 2 o structure ps second dynamics
22 Structural details of amyloid fibrils solution NMR spectroscopy H/D exchange of A beta 1-42 fibrils, detected by NMR Luhrs et al., 2005, Proc. Natl. Acad. Sci. USA
23 Structural details of amyloid fibrils solution NMR spectroscopy Luhrs et al., 2005, Proc. Natl. Acad. Sci. USA
24 Amyloid fibrils Structural details of amyloid fibrils solid state NMR KTNMKHMAGAAAAGAVVGGLG High resolution NMR of solids
25 Structural details of amyloid fibrils solid state NMR B o We can improve NMR resolution in solid samples by imposing: a) Order (eg. single crystals, planar membranes) b) Rapid axial motion 13 C Spectrum of solid Valine HCl static Sample 2.5 khz MAS In static solids, nuclei are anisotropic - fixed in different orientation Orientation-dependent interactions based on a (3cos 2 θ -1) term. Under MAS (θ = 54.7), 3cos 2 θ -1 = 0 and reintroduces isotropy. 5 khz MAS 10 khz MAS CO C C C
26 Structural details of amyloid fibrils solid state NMR Structural restraints from solid state NMR allow high resolution structures of peptides and protofilaments within amyloid fibrils. Limitation is spectral resolution. 13 C, 15 N, ( 1 H) Chemical shifts secondary structure. 13 C- 13 C, 13 C- 15 N, 15 N- 15 N dipolar couplings tertiary and quaternary structure. Yau and Sharpe, 2012, J. Struct. Biol.
27 Structural details of amyloid fibrils solid state NMR HET-S prion ( ) of Podospora anserina beta helix structure Two different fibrillar forms of the Alzheimer s A (1-40) protein Tycko, 2011, Annu. Rev. Phys. Chem. Wasmer et al. (2008) Science 319:
28 Amyloid fibrils are significantly more stable than the native state NNQNTF ISFLIF NVGSNTY Greenwald & Riek, 2010, Structure 18: Cross- core is stabilized by van der Waals interactions and interstrand hydrogen bonds. The intersheet steric zipper stability is enhanced by side chain hydrogen binds or salt bridges as appropriate. Aromatic rings stack favorably along long axis, as do networks of hydrogen bonds between polar residues (e.g. in poly Q expansions seen in Huntington s disease).
29 What prevents spontaneous conversion to amyloid fibrils? Thioflavin T The fluorescent dye ThT binds to amyloid structures and exhibits a characteristic shift in its emission maximum to ~ 480 nm, allowing us to monitor fibrillization kinetics. In vitro kinetic studies reveal a lag phase preceding fibril growth. This suggests a kinetic barrier which is overcome once aggregation begins (nucleated assembly process). In vivo, the presence of kinetic barriers as well as cellular control over folding, misfolding and aggregation, prevents amyloid fibril formation under most conditions. Mutation, age, or other confounding factors override these barriers and promote fibrillization.
30 Nucleation / seeding Kumar and Walter, 2011, Aging 3: Addition of fragmented fibrils, or seeds significantly reduces the lag phase. It also promotes formation of the same structure/strain/morphology present in the seeds. This has recently been used to investigate the structure of A fibrils in Alzheimer s brains.
31 Multiple pathways for nucleation / seeding Knowles et al., 2014 Nat. Rev. Mol. Cell. Biol. 15:
32 Structural heterogeneity of amyloid fibrils Rugged energy landscape on the aggregated side - leads to structural heterogeneity of amyloid fibrils, strain behaviour in prions. Also see non-fibrillar oligomers as less stable, but populated during misfolding and aggregation.
33 Structural heterogeneity of amyloid fibrils Jahn and Radford, 2008, Arch. Biochem. Biophys.
34 Functional heterogeneity of amyloid fibrils - strains Strains can be reliably propagated in vitro (seeding) or in vivo (infection) In yeast prions, strains are associated with structural integrity/fragmentation of fibrils and their associations with chaperones. This has led to the hypothesis that strains are determined by the structure and stability of the amyloid form of the protein.
35 Evidence for templating of amyloid structure from seeds Petkova et al., 2005 Science
36 Structures of A fibrils seeded from patient differ from in vitro Yu et al., 2013, Cell
37 Patients with different symptoms and pathology have different fibril structures Yu et al., 2013, Cell
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