Interactions of IDPs with Membranes Using Dark-State Exchange NMR Spectroscopy.
Cell Membrane
/ metabolism
Darkness
Humans
Intrinsically Disordered Proteins
/ chemistry
Nuclear Magnetic Resonance, Biomolecular
/ methods
Protein Conformation
Research Design
Signal Processing, Computer-Assisted
Solutions
Specimen Handling
/ methods
alpha-Synuclein
/ chemistry
tau Proteins
/ chemistry
Dark-state exchange spectroscopy
IDP
Membrane interactions
NMR
Solution state
Tau
α-synuclein
Journal
Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969
Informations de publication
Date de publication:
2020
2020
Historique:
entrez:
23
7
2020
pubmed:
23
7
2020
medline:
16
3
2021
Statut:
ppublish
Résumé
Membrane interactions of proteins play a role in essential cellular processes in both physiological and disease states. The structural flexibility of intrinsically disordered proteins (IDPs) allows for interactions with multiple partners, including membranes. However, determining conformational states of IDPs when interacting with membranes can be challenging. Here we describe the use of nuclear magnetic resonance (NMR), including dark-state exchange saturation transfer (DEST), to probe IDP-membrane interactions in order to determine whether there is an interaction, which residues participate, and the extent/nature of the interaction between the protein and the membrane. Using α-synuclein and tau as typical examples, we provide protocols for how the membrane interactions of IDPs can be probed, including details of how the samples should be prepared and guidelines on how to interpret the results.
Identifiants
pubmed: 32696379
doi: 10.1007/978-1-0716-0524-0_30
pmc: PMC8185907
mid: NIHMS1706338
doi:
Substances chimiques
Intrinsically Disordered Proteins
0
Solutions
0
alpha-Synuclein
0
tau Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
585-608Subventions
Organisme : NIGMS NIH HHS
ID : P41 GM118302
Pays : United States
Organisme : NIA NIH HHS
ID : R37 AG019391
Pays : United States
Références
Duplâtre G, Ferreira Marques MF, Da Graça Miguel M (1996) Size of sodium dodecyl sulfate micelles in aqueous solutions as studied by positron annihilation lifetime spectroscopy. J Phys Chem 100:16608–16612
doi: 10.1021/jp960644m
Barré P, Eliezer D (2013) Structural transitions in tau k18 on micelle binding suggest a hierarchy in the efficacy of individual microtubule-binding repeats in filament nucleation. Protein Sci 22:1037–1048
doi: 10.1002/pro.2290
Bussell R, Eliezer D (2003) A structural and functional role for 11-mer repeats in α-synuclein and other exchangeable lipid binding proteins. J Mol Biol 329(4):763–778
doi: 10.1016/S0022-2836(03)00520-5
Snead D, Eliezer D (2018) Spectroscopic characterization of structure–function relationships in the intrinsically disordered protein complexin. In: Methods in enzymology. Elsevier, Amsterdam
Fawzi NL, Ying J, Torchia DA et al (2012) Probing exchange kinetics and atomic resolution dynamics in high-molecular-weight complexes using dark-state exchange saturation transfer NMR spectroscopy. Nat Protoc 7:1523–1533
doi: 10.1038/nprot.2012.077
Georgieva ER, Ramlall TF, Borbat PP et al (2010) The lipid-binding domain of wild type and mutant alpha-synuclein: compactness and interconversion between the broken and extended helix forms. J Biol Chem 285:28261–28274
doi: 10.1074/jbc.M110.157214
Georgieva ER, Ramlall TF, Borbat PP et al (2008) Membrane-bound alpha-synuclein forms an extended helix: long-distance pulsed ESR measurements using vesicles, bicelles, and rodlike micelles. J Am Chem Soc 130:12856–12857
doi: 10.1021/ja804517m
Jao CC, Hegde BG, Chen J et al (2008) Structure of membrane-bound alpha-synuclein from site-directed spin labeling and computational refinement. Proc Natl Acad Sci U S A 105:19666–19671
doi: 10.1073/pnas.0807826105
Eliezer D (2012) Distance information for disordered proteins from NMR and ESR measurements using paramagnetic spin labels. Methods Mol Biol 895:127–138
doi: 10.1007/978-1-61779-927-3_10
Georgieva ER, Xiao S, Borbat PP et al (2014) Tau binds to lipid membrane surfaces via short amphipathic helices located in its microtubule-binding repeats. Biophys J 107:1441–1452
doi: 10.1016/j.bpj.2014.07.046
Brandt R, Léger J, Lee G (1995) Interaction of tau with the neural plasma membrane mediated by tau’s amino-terminal projection domain. J Cell Biol 131(5):1327–1340
doi: 10.1083/jcb.131.5.1327
Gauthier-Kemper A, Weissmann C, Golovyashkina N et al (2011) The frontotemporal dementia mutation R406W blocks tau’s interaction with the membrane in an annexin A2-dependent manner. J Cell Biol 192(4):647–661
doi: 10.1083/jcb.201007161
Shea TB (1997) Phospholipids alter tau conformation, phosphorylation, proteolysis, and association with microtubules: implication for tau function under normal and degenerative conditions. J Neurosci Res 50:114–122
doi: 10.1002/(SICI)1097-4547(19971001)50:1<114::AID-JNR12>3.0.CO;2-B
Gray EG, Paula-Barbosa M, Roher A (1987) Alzheimer’s disease: paired helical filaments and cytomembranes. Neuropathol Appl Neurobiol 13:91–110
doi: 10.1111/j.1365-2990.1987.tb00174.x
Barré P, Eliezer D (2006) Folding of the repeat domain of tau upon binding to lipid surfaces. J Mol Biol 362:312–326
doi: 10.1016/j.jmb.2006.07.018
Emanuele M, Chieregatti E (2015) Mechanisms of alpha-synuclein action on neurotransmission: cell-autonomous and non-cell autonomous role. Biomolecules 5(2):865–892
doi: 10.3390/biom5020865
Das T, Eliezer D (2019) Membrane interactions of intrinsically disordered proteins: the example of alpha-synuclein. Biochim Biophys Acta Proteins Proteom 1867:879–889
doi: 10.1016/j.bbapap.2019.05.001
Gonzalez-Horta A, Gonzalez Hernandez B, Chavez-Montes A (2013) Fluorescence as a tool to study lipid-protein interactions: the case of α-Synuclein. Open J Biophys 3:112–119
doi: 10.4236/ojbiphy.2013.31A014
Das T, Eliezer D (2019) Probing structural changes in alpha-synuclein by nuclear magnetic resonance spectroscopy. Methods Mol Biol 1948:157–181
doi: 10.1007/978-1-4939-9124-2_13
Fawzi NL, Ying J, Ghirlando R et al (2011) Atomic resolution dynamics on the surface of amyloid β protofibrils probed by solution NMR. Nature 480:268–272
doi: 10.1038/nature10577
Delaglio F, Grzesiek S, Vuister GW et al (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277–293
doi: 10.1007/BF00197809
Eliezer D, Barré P, Kobaslija M et al (2005) Residual structure in the repeat domain of tau: Echoes of microtubule binding and paired helical filament formation. Biochemistry 44(3):1026–1036
doi: 10.1021/bi048953n
Harbison NW, Bhattacharya S, Eliezer D (2012) Assigning backbone NMR resonances for full length tau isoforms: efficient compromise between manual assignments and reduced dimensionality. PLoS One 7:e34679
doi: 10.1371/journal.pone.0034679
Anthis NJ, Clore GM (2015) Visualizing transient dark states by NMR spectroscopy. Q Rev Biophys 48:35–116
doi: 10.1017/S0033583514000122
Maltsev AS, Chen J, Levine RL et al (2013) Site-specific interaction between α-synuclein and membranes probed by NMR-observed methionine oxidation rates. J Am Chem Soc 135:2943–2946
doi: 10.1021/ja312415q