Amyloid fibril; Double PHD finger 3 (DPF3); Intrinsically disordered protein; Protein aggregation; Spectroscopy; Amyloid; Intrinsically Disordered Proteins; Protein Isoforms; Transcription Factors; Amyloid/chemistry; Protein Isoforms/metabolism; Transcription Factors/metabolism; Zinc Fingers; Intrinsically Disordered Proteins/chemistry; Structural Biology; Biochemistry; Molecular Biology; General Medicine
Abstract :
[en] Double PHD fingers 3 (DPF3) is a zinc finger protein, found in the BAF chromatin remodelling complex, and is involved in the regulation of gene expression. Two DPF3 isoforms have been identified, respectively named DPF3b and DPF3a. Very limited structural information is available for these isoforms, and their specific functionality still remains poorly studied. In a previous work, we have demonstrated the first evidence of DPF3a being a disordered protein sensitive to amyloid fibrillation. Intrinsically disordered proteins (IDPs) lack a defined tertiary structure, existing as a dynamic conformational ensemble, allowing them to act as hubs in protein-protein interaction networks. In the present study, we have more thoroughly characterised DPF3a in vitro behaviour, as well as unravelled and compared the structural properties of the DPF3b isoform, using an array of predictors and biophysical techniques. Predictions, spectroscopy, and dynamic light scattering have revealed a high content in disorder: prevalence of random coil, aromatic residues partially to fully exposed to the solvent, and large hydrodynamic diameters. DPF3a appears to be more disordered than DPF3b, and exhibits more expanded conformations. Furthermore, we have shown that they both time-dependently aggregate into amyloid fibrils, as revealed by typical circular dichroism, deep-blue autofluorescence, and amyloid-dye binding assay fingerprints. Although spectroscopic and microscopic analyses have unveiled that they share a similar aggregation pathway, DPF3a fibrillates at a faster rate, likely through reordering of its C-terminal domain.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Mignon, Julien; Laboratoire de Chimie Physique des Biomolécules, UCPTS, University of Namur, 61 rue de Bruxelles, 5000 Namur, Belgium, Namur Institute of Structured Matter (NISM), University of Namur, Namur, Belgium, Namur Research Institute for Life Sciences (NARILIS), University of Namur, Namur, Belgium. Electronic address: julien.mignon@unamur.be
Mottet, Denis ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Leyder, Tanguy; Laboratoire de Chimie Physique des Biomolécules, UCPTS, University of Namur, 61 rue de Bruxelles, 5000 Namur, Belgium. Electronic address: tanguy.leyder@student.unamur.be
Uversky, Vladimir N; Department of Molecular Medicine, USF Health Byrd Alzheimer's Research Institute, Morsani College of Medicine, University of South Florida, Tampa, FL, United States. Electronic address: vuversky@usf.edu
Perpète, Eric A; Laboratoire de Chimie Physique des Biomolécules, UCPTS, University of Namur, 61 rue de Bruxelles, 5000 Namur, Belgium, Namur Research Institute for Life Sciences (NARILIS), University of Namur, Namur, Belgium, Institute of Life, Earth and Environment (ILEE), University of Namur, Namur, Belgium. Electronic address: eric.perpete@unamur.be
Michaux, Catherine; Laboratoire de Chimie Physique des Biomolécules, UCPTS, University of Namur, 61 rue de Bruxelles, 5000 Namur, Belgium, Namur Institute of Structured Matter (NISM), University of Namur, Namur, Belgium, Namur Research Institute for Life Sciences (NARILIS), University of Namur, Namur, Belgium. Electronic address: catherine.michaux@unamur.be
Language :
English
Title :
Structural characterisation of amyloidogenic intrinsically disordered zinc finger protein isoforms DPF3b and DPF3a.
Publication date :
01 October 2022
Journal title :
International Journal of Biological Macromolecules
Authors are appreciative to the Research Unit in Biology of Microorganisms, as well as to the MaSUN, L.O.S., and Morph-Im platforms of the University of Namur. J. Mignon thanks the Belgian National Fund for Scientific Research (FNRS) for his FRIA PhD Student position. C. Michaux and D. Mottet also thank the FNRS for their Research Associate position. E. A. Perpète also thanks the FNRS for his Senior Research Associate position. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Tyagi, M., Imam, N., Verma, K., Patel, A.K., Chromatin remodelers: we are the drivers!!. Nucleus 7 (2016), 388–404, 10.1080/19491034.2016.1211217.
Lange, M., Kaynak, B., Forster, U.B., Tönjes, M., Fischer, J.J., Grimm, C., Schlesinger, J., Just, S., Dunkel, I., Krueger, T., Mebus, S., Lehrach, H., Lurz, R., Gobom, J., Rottbauer, W., Abdelilah-Seyfried, S., Sperling, S., Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev. 22 (2008), 2370–2384, 10.1101/gad.471408.
Ishizaka, A., Mizutani, T., Kobayashi, K., Tando, T., Sakurai, K., Fujiwara, T., Iba, H., Double plant homeodomain (PHD) finger proteins DPF3a and -3b are required as transcriptional co-activators in SWI/SNF complex-dependent activation of NF-κB RelA/p50 heterodimer. J. Biol. Chem. 287 (2012), 11924–11933, 10.1074/jbc.M111.322792.
Lessard, J., Wu, J.I., Ranish, J.A., Wan, M., Winslow, M.M., Staahl, B.T., Wu, H., Aebersold, R., Graef, I.A., Crabtree, G.R., An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55 (2007), 201–215, 10.1016/j.neuron.2007.06.019.
Zeng, L., Zhang, Q., Li, S., Plotnikov, A.N., Walsh, M.J., Zhou, M.M., Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466 (2010), 258–262, 10.1038/nature09139.
Li, W., Zhao, A., Tempel, W., Loppnau, P., Liu, Y., Crystal structure of DPF3b in complex with an acetylated histone peptide. J. Struct. Biol. 195 (2016), 365–372, 10.1016/j.jsb.2016.07.001.
Fu, K., Nakano, H., Morselli, M., Chen, T., Pappoe, H., Nakano, A., Pellegrini, M., A temporal transcriptome and methylome in human embryonic stem cell-derived cardiomyocytes identifies novel regulators of early cardiac development. Epigenetics. 13 (2018), 1013–1026, 10.1080/15592294.2018.1526029.
Cui, H., Schlesinger, J., Schoenhals, S., Tönjes, M., Dunkel, I., Meierhofer, D., Cano, E., Schulz, K., Berger, M.F., Haack, T., Abdelilah-Seyfried, S., Bulyk, M.L., Sauer, S., Sperling, S.R., Phosphorylation of the chromatin remodeling factor DPF3a induces cardiac hypertrophy through releasing HEY repressors from DNA. Nucleic Acids Res. 44 (2015), 2538–2553, 10.1093/nar/gkv1244.
Guanglei, W., Bingbing, W., Peixin, Y., Epigenetics in congenital heart disease. J. Am. Heart Assoc., 11, 2022, 10.1161/JAHA.121.025163.
Cui, H., Schlesinger, J., Schoenhals, S., Tönjes, M., Dunkel, I., Meierhofer, D., Cano, E., Schulz, K., Berger, M.F., Haack, T., Abdelilah-Seyfried, S., Bulyk, M.L., Sauer, S., Sperling, S.R., Phosphorylation of the chromatin remodeling factor DPF3a induces cardiac hypertrophy through releasing HEY repressors from DNA. Nucleic Acids Res. 44 (2015), 2538–2553, 10.1093/nar/gkv1244.
Hiramatsu, H., Kobayashi, K., Kobayashi, K., Haraguchi, T., Ino, Y., Todo, T., Iba, H., The role of the SWI/SNF chromatin remodeling complex in maintaining the stemness of glioma initiating cells. Sci. Rep., 7, 2017, 10.1038/s41598-017-00982-3.
Hao Lin, W., Gang Dai, W., Dong Xu, X., Hua Yu, Q., Zhang, B., Li, J., H., Ping Li, Downregulation of DPF3 promotes the proliferation and motility of breast cancer cells through activating JAK2/STAT3 signaling. Biochem. Biophys. Res. Commun. 514 (2019), 639–644, 10.1016/j.bbrc.2019.04.170.
Colli, L.M., Jessop, L., Myers, T.A., Camp, S.Y., Machiela, M.J., Choi, J., Cunha, R., Onabajo, O., Mills, G.C., Schmid, V., Brodie, S.A., Delattre, O., Mole, D.R., Purdue, M.P., Yu, K., Brown, K.M., Chanock, S.J., Altered regulation of DPF3, a member of the SWI/SNF complexes, underlies the 14q24 renal cancer susceptibility locus. Am. J. Hum. Genet. 108 (2021), 1590–1610, 10.1016/j.ajhg.2021.07.009.
Protze, J., Naas, S., Krüger, R., Stöhr, C., Kraus, A., Grampp, S., Wiesener, M., Schiffer, M., Hartmann, A., Wullich, B., Schödel, J., The renal cancer risk allele at 14q24.2 activates a novel hypoxia-inducible transcription factor-binding enhancer of DPF3 expression. J. Biol. Chem., 298, 2022, 10.1016/j.jbc.2022.101699.
Kosova, G., Hotaling, J.M., Ohlander, S., Niederberger, C., Prins, G.S., Ober, C., Variants in DPF3 and DSCAML1 are associated with sperm morphology. J. Assist. Reprod. Genet. 31 (2014), 131–137, 10.1007/s10815-013-0140-9.
Liu, S.Y., Zhang, C.J., Peng, H.Y., Sun, H., Lin, K.Q., Huang, X.Q., Huang, K., Chu, J.Y., Yang, Z.Q., Strong association of SLC1A1 and DPF3 gene variants with idiopathic male infertility in Han Chinese. Asian J. Androl. 18 (2016), 486–492, 10.4103/1008-682X.178850.
Sato, Y., Hasegawa, C., Tajima, A., Nozawa, S., Yoshiike, M., Koh, E., Kanaya, J., Namiki, M., Matsumiya, K., Tsujimura, A., Komatsu, K., Itoh, N., Eguchi, J., Yamauchi, A., Iwamoto, T., Association of TUSC1 and DPF3 gene polymorphisms with male infertility. J. Assist. Reprod. Genet. 35 (2018), 257–263, 10.1007/s10815-017-1052-x.
Local, A., Huang, H., Albuquerque, C.P., Singh, N., Lee, A.Y., Wang, W., Wang, C., Hsia, J.E., Shiau, A.K., Ge, K., Corbett, K.D., Wang, D., Zhou, H., Ren, B., Identification of H3K4me1-associated proteins at mammalian enhancers. Nat. Genet. 50 (2018), 73–82, 10.1038/s41588-017-0015-6.
El Hadidy, N., Uversky, V.N., Intrinsic disorder of the baf complex: roles in chromatin remodeling and disease development. Int. J. Mol. Sci., 20, 2019, 10.3390/ijms20215260.
Mignon, J., Mottet, D., Verrillo, G., Matagne, A., Perpète, E.A., Michaux, C., Revealing intrinsic disorder and aggregation properties of the DPF3a zinc finger protein. ACS Omega. 6 (2021), 18793–18801, 10.1021/acsomega.1c01948.
Kulkarni, P., Bhattacharya, S., Achuthan, S., Behal, A., Jolly, M.K., Kotnala, S., Mohanty, A., Rangarajan, G., Salgia, R., Uversky, V., Intrinsically disordered proteins: critical components of the wetware. Chem. Rev. 122 (2022), 6614–6633, 10.1021/acs.chemrev.1c00848.
Uversky, V.N., Intrinsically disordered proteins: targets for the future ?. Renaud, J.-P., (eds.) Structural Biology in Drug Discovery: Methods, Techniques, and Practices, First Edit, 2020, John Wiley & Sons Inc, 587–612.
Kuipers, B.J.H., Gruppen, H., Prediction of molar extinction coefficients of proteins and peptides using UV absorption of the constituent amino acids at 214 nm to enable quantitative reverse phase high-performance liquid chromatography-mass spectrometry analysis. J. Agric. Food Chem. 55 (2007), 5445–5451, 10.1021/jf070337l.
Williams, R.M., Obradovi, Z., Mathura, V., Braun, W., Garner, E.C., Takayama, S., Brown, C.J., Dunker, A.K., The protein non-folding problem: amino acid determinants of intrinsic order and disorder. Pac. Symp. Biocomp., 2001, 89–100.
Peng, K., Vucetic, S., Radivojac, P., Brown, C.J., Dunker, A.K., Obradovic, Z., Optimizing long intrinsic disorder predictors with protein evolutionary information. J. Bioinforma. Comput. Biol. 3 (2005), 35–60, 10.1142/s0219720005000886.
Garner, Romero, Dunker, Brown, Obradovic, Predicting Binding Regions Within Disordered Proteins. Genome Informatics. Workshop on Genome Informatics, 10, 1999, 41–50.
Walsh, I., Martin, A.J.M., Tosatto, S.C.E., Di domenico, T., Espritz: Accurate and fast prediction of protein disorder. Bioinformatics 28 (2012), 503–509, 10.1093/bioinformatics/btr682.
Ishida, T., Kinoshita, K., PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res. 35 (2007), 460–464, 10.1093/nar/gkm363.
Erdos, G., Pajkos, M., Dosztányi, Z., IUPred3: prediction of protein disorder enhanced with unambiguous experimental annotation and visualization of evolutionary conservation. Nucleic Acids Res. 49 (2021), 297–303, 10.1093/nar/gkab408.
Emenecker, R.J., Griffith, D., Holehouse, A.S., Metapredict: a fast, accurate, and easy-to-use predictor of consensus disorder and structure. Biophys. J. 120 (2021), 4312–4319, 10.1016/j.bpj.2021.08.039.
Bernhofer, M., Dallago, C., Karl, T., Satagopam, V., Heinzinger, M., Littmann, M., Olenyi, T., Qiu, J., Schütze, K., Yachdav, G., Ashkenazy, H., Ben-Tal, N., Bromberg, Y., Goldberg, T., Kajan, L., O'Donoghue, S., Sander, C., Schafferhans, A., Schlessinger, A., Vriend, G., Mirdita, M., Gawron, P., Gu, W., Jarosz, Y., Trefois, C., Steinegger, M., Schneider, R., Rost, B., PredictProtein - predicting protein structure and function for 29 years. Nucleic Acids Res. 49 (2021), 535–540, 10.1093/nar/gkab354.
Wang, S., Ma, J., Xu, J., AUCpreD: proteome-level protein disorder prediction by AUC-maximized deep convolutional neural fields. Bioinformatics 32 (2016), i672–i679, 10.1093/bioinformatics/btw446.
Dass, R., Mulder, F.A.A., Nielsen, J.T., ODiNPred: comprehensive prediction of protein order and disorder. Sci. Rep., 10, 2020, 10.1038/s41598-020-71716-1.
Holehouse, A.S., Das, R.K., Ahad, J.N., Richardson, M.O.G., Pappu, R.V., CIDER: resources to analyze sequence-ensemble relationships of intrinsically disordered proteins. Biophys. J. 112 (2017), 16–21, 10.1016/j.bpj.2016.11.3200.
Letunic, I., Khedkar, S., Bork, P., SMART: recent updates, new developments and status in 2020. Nucleic Acids Res. 49 (2021), D458–D460, 10.1093/nar/gkaa937.
Jarnot, P., Ziemska-Legiecka, J., Dobson, L., Merski, M., Mier, P., Andrade-Navarro, M.A., Hancock, J.M., Dosztányi, Z., Paladin, L., Necci, M., Piovesan, D., Tosatto, S.C.E., Promponas, V.J., Grynberg, M., Gruca, A., PlaToLoCo: the first web meta-server for visualization and annotation of low complexity regions in proteins. Nucleic Acids Res. 48 (2020), W77–W84, 10.1093/NAR/GKAA339.
Malhis, N., Jacobson, M., Gsponer, J., MoRFchibi SYSTEM: software tools for the identification of MoRFs in protein sequences. Nucleic Acids Res. 44 (2016), W488–W493, 10.1093/NAR/GKW409.
Kaleel, M., Torrisi, M., Mooney, C., Pollastri, G., PaleAle 5.0: prediction of protein relative solvent accessibility by deep learning. Amino Acids 51 (2019), 1289–1296, 10.1007/s00726-019-02767-6.
Sormanni, P., Vendruscolo, M., Protein solubility predictions using the camsol method in the study of protein homeostasis. Cold Spring Harb. Perspect. Biol., 11, 2019, 10.1101/cshperspect.a033845.
Tsolis, A.C., Papandreou, N.C., Iconomidou, V.A., Hamodrakas, S.J., A consensus method for the prediction of “aggregation-prone” peptides in globular proteins. PLoS ONE, 8, 2013, 10.1371/journal.pone.0054175.
Micsonai, A., Wien, F., Bulyáki, É., Kun, J., Moussong, É., Lee, Y.H., Goto, Y., Réfrégiers, M., Kardos, J., BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra. Nucleic Acids Res. 46 (2018), 315–322, 10.1093/nar/gky497.
Zhang, W., Xu, C., Bian, C., Tempel, W., Crombet, L., MacKenzie, F., Min, J., Liu, Z., Qi, C., Crystal structure of the Cys2His2-type zinc finger domain of human DPF2. Biochem. Biophys. Res. Commun. 413 (2011), 58–61, 10.1016/j.bbrc.2011.08.043.
Van Der Lee, R., Buljan, M., Lang, B., Weatheritt, R.J., Daughdrill, G.W., Dunker, A.K., Fuxreiter, M., Gough, J., Gsponer, J., Jones, D.T., Kim, P.M., Kriwacki, R.W., Oldfield, C.J., Pappu, R.V., Tompa, P., Uversky, V.N., Wright, P.E., Babu, M.M., Classification of intrinsically disordered regions and proteins. Chem. Rev. 114 (2014), 6589–6631, 10.1021/cr400525m.
Uversky, V.N., Intrinsically disordered proteins and their “mysterious” (meta)physics. Front. Phys. 7 (2019), 8–23, 10.3389/fphy.2019.00010.
Xue, B., Oldfield, C.J., Dunker, A.K., Uversky, V.N., CDF it all: consensus prediction of intrinsically disordered proteins based on various cumulative distribution functions. FEBS Lett. 583 (2009), 1469–1474, 10.1016/j.febslet.2009.03.070.
Uversky, V.N., Gillespie, J.R., Fink, A.L., Why are “natively unfolded” proteins unstructured under physiologic conditions?. Proteins 41 (2000), 415–427, 10.1002/1097-0134(20001115)41:3<415::AID-PROT130>3.0.CO;2-7.
Kyte, J., Doolittle, R.F., A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 (1982), 105–132, 10.1016/0022-2836(82)90515-0.
Das, R.K., Pappu, R.V., Conformations of intrinsically disordered proteins are influenced by linear sequence distributions of oppositely charged residues. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 13392–13397, 10.1073/pnas.1304749110.
Martin, E.W., Holehouse, A.S., Grace, C.R., Hughes, A., Pappu, R.V., Mittag, T., Sequence determinants of the conformational properties of an intrinsically disordered protein prior to and upon multisite phosphorylation. J. Am. Chem. Soc. 138 (2016), 15323–15335, 10.1021/jacs.6b10272.
Das, R.K., Ruff, K.M., Pappu, R.V., Relating sequence encoded information to form and function of intrinsically disordered proteins. Curr. Opin. Struct. Biol. 32 (2015), 102–112, 10.1016/j.sbi.2015.03.008.
Fung, H.Y.J., Birol, M., Rhoades, E., IDPs in macromolecular complexes: the roles of multivalent interactions in diverse assemblies. Curr. Opin. Struct. Biol. 49 (2018), 36–43, 10.1016/j.sbi.2017.12.007.
Das, S., Pal, U., Das, S., Bagga, K., Roy, A., Mrigwani, A., Maiti, N.C., Sequence complexity of amyloidogenic regions in intrinsically disordered human proteins. PLoS ONE, 9, 2014, 10.1371/journal.pone.0089781.
Morris, O.M., Torpey, J.H., Isaacson, R.L., Intrinsically disordered proteins: modes of binding with emphasis on disordered domains. Open Biol., 11, 2021, 10.1098/rsob.210222.
Tcherkasskaya, O., Uversky, V.N., Denatured collapsed states in protein folding: Example of apomyoglobin. Proteins 44 (2001), 244–254, 10.1002/prot.1089.
Nygaard, M., Kragelund, B.B., Papaleo, E., Lindorff-Larsen, K., An efficient method for estimating the hydrodynamic radius of disordered protein conformations. Biophys. J. 113 (2017), 550–557, 10.1016/j.bpj.2017.06.042.
Vivian, J.T., Callis, P.R., Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80 (2001), 2093–2109, 10.1016/S0006-3495(01)76183-8.
Lakowicz, J.R., Principles of Fluorescence Spectroscopy. Third Edit, 2006, Springer Science.
Noronha, M., Lima, J.C., Lamosa, P., Santos, H., Maycock, C., Ventura, R., Maçanita, A.L., Intramolecular fluorescence quenching of tyrosine by the peptide α-carbonyl group revisited. J. Phys. Chem. A 108 (2004), 2155–2166, 10.1021/jp037125l.
Davis, K.B., Zhang, Z., Karpova, E.A., Zhang, J., Application of tyrosine-tryptophan fluorescence resonance energy transfer in monitoring protein size changes. Anal. Biochem. 557 (2018), 142–150, 10.1016/j.ab.2018.07.022.
Davis, K.B., Zhang, Z., Karpova, E.A., Zhang, J., Application of tyrosine-tryptophan fluorescence resonance energy transfer in monitoring protein size changes. Anal. Biochem. 557 (2018), 142–150, 10.1016/j.ab.2018.07.022.
Biter, A.B., Pollet, J., Chen, W.H., Strych, U., Hotez, P.J., Bottazzi, M.E., A method to probe protein structure from UV absorbance spectra. Anal. Biochem., 587, 2019, 10.1016/j.ab.2019.113450.
Ghosh, D., Singh, P.K., Sahay, S., Jha, N.N., Jacob, R.S., Sen, S., Kumar, A., Riek, R., Maji, S.K., Structure based aggregation studies reveal the presence of helix-rich intermediate during α-synuclein aggregation. Sci. Rep., 5, 2015, 10.1038/srep09228.
Noronha, M., Lima, J.C., Lamosa, P., Santos, H., Maycock, C., Ventura, R., Maçanita, A.L., Intramolecular fluorescence quenching of tyrosine by the peptide α-carbonyl group revisited. J. Phys. Chem. A 108 (2004), 2155–2166, 10.1021/jp037125l.
Wieczorek, E., Bezara, P., Ożyhar, A., Deep blue autofluorescence reveals the instability of human transthyretin. Int. J. Biol. Macromol. 191 (2021), 492–499, 10.1016/j.ijbiomac.2021.09.107.
Ziaunys, M., Sneideris, T., Smirnovas, V., Exploring the potential of deep-blue autofluorescence for monitoring amyloid fibril formation and dissociation. PeerJ, 2019, 10.7717/peerj.7554.
Jesus, C.S.H., Soares, H.T., Piedade, A.P., Cortes, L., Serpa, C., Using amyloid autofluorescence as a biomarker for lysozyme aggregation inhibition. Analyst 146 (2021), 2383–2391, 10.1039/d0an02260h.
Niyangoda, C., Miti, T., Breydo, L., Uversky, V., Muschol, M., Carbonyl-based blue autofluorescence of proteins and amino acids. PLoS ONE., 12, 2017, 10.1371/journal.pone.0176983.
Saraiva, M.A., Interpretation of α-synuclein UV absorption spectra in the peptide bond and the aromatic regions. J. Photochem. Photobiol. B Biol., 212, 2020, 10.1016/j.jphotobiol.2020.112022.
Niyangoda, C., Miti, T., Breydo, L., Uversky, V., Muschol, M., Carbonyl-based blue autofluorescence of proteins and amino acids. PLoS ONE, 12, 2017, 10.1371/journal.pone.0176983.
Biancalana, M., Koide, S., Molecular mechanism of Thioflavin-T binding to amyloid fibrils. Biochim. Biophys. Acta, Proteins Proteomics 1804 (2010), 1405–1412, 10.1016/j.bbapap.2010.04.001.
Xue, C., Lin, T.Y., Chang, D., Guo, Z., Thioflavin T as an amyloid dye: fibril quantification, optimal concentration and effect on aggregation. R. Soc. Open Sci., 4, 2017, 10.1098/rsos.160696.
Yakupova, E.I., Bobyleva, L.G., Vikhlyantsev, I.M., Bobylev, A.G., Congo red and amyloids: history and relationship. Biosci. Rep., 39, 2019, 10.1042/BSR20181415.
Bush, A.I., Copper, zinc, and the metallobiology of Alzheimer disease. Alzheimer Dis. Assoc. Disord. 17 (2003), 147–150.
Breydo, L., Uversky, V.N., Role of metal ions in aggregation of intrinsically disordered proteins in neurodegenerative diseases. Metallomics 3 (2011), 1163–1180, 10.1039/c1mt00106j.
Gras, S.L., Waddington, L.J., Goldie, K.N., Transmission electron microscopy of amyloid fibrils. Methods Mol. Biol. 752 (2011), 197–214, 10.1007/978-1-60327-223-0_13.
Xu, S., Brunden, K.R., Trojanowski, J.Q., Lee, V.M.Y., Characterization of tau fibrillization in vitro. Alzheimers Dement. 6 (2010), 110–117, 10.1016/j.jalz.2009.06.002.
Willbold, D., Strodel, B., Schröder, G.F., Hoyer, W., Heise, H., Amyloid-type protein aggregation and prion-like properties of amyloids. Chem. Rev. 121 (2021), 8285–8307, 10.1021/acs.chemrev.1c00196.
Close, W., Neumann, M., Schmidt, A., Hora, M., Annamalai, K., Schmidt, M., Reif, B., Schmidt, V., Grigorieff, N., Fändrich, M., Physical basis of amyloid fibril polymorphism. Nat. Commun., 9, 2018, 10.1038/s41467-018-03164-5.
Wegmann, S., Yu, J.J., Chinnathambi, S., Mandelkow, E.M., Mandelkow, E., Muller, D.J., Human tau isoforms assemble into ribbon-like fibrils that display polymorphic structure and stability. J. Biol. Chem. 285 (2010), 27302–27313, 10.1074/jbc.M110.145318.
Kurouski, D., Supramolecular organization of amyloid fibrils. Exploring New Findings on Amyloidosis, 2016, 73–98, 10.5772/62672.
Maeda, S., Sahara, N., Saito, Y., Murayama, M., Yoshiike, Y., Kim, H., Miyasaka, T., Murayama, S., Ikai, A., Takashima, A., Granular tau oligomers as intermediates of tau filaments. Biochemistry 46 (2007), 3856–3861, 10.1021/bi061359o.
Rauch, R., Hofbeck, M., Zweier, C., Koch, A., Zink, S., Trautmann, U., Hoyer, J., Kaulitz, R., Singer, H., Rauch, A., Comprehensive genotype-phenotype analysis in 230 patients with tetralogy of fallot. J. Med. Genet. 47 (2010), 321–331, 10.1136/jmg.2009.070391.
Sha, Y.W., Xu, X., Bin Mei, L., Li, P., Su, Z.Y., He, X.Q., Li, L., A homozygous CEP135 mutation is associated with multiple morphological abnormalities of the sperm flagella (MMAF). Gene 633 (2017), 48–53, 10.1016/j.gene.2017.08.033.
