dGAE(297-391) Tau Fragment Promotes Formation of Chronic Traumatic Encephalopathy-Like Tau Filaments
Language English Country Germany Media print-electronic
Document type Journal Article
Grant support
lzp-2019/1-0244
Latvijas Zinātnes Padome
VPP-EM-BIOMEDICĪNA-2022/1-0001
Latvijas Zinātnes Padome
873127
H2020 Marie Skłodowska-Curie Actions
101038074
H2020 Marie Skłodowska-Curie Actions
PubMed
39183704
PubMed Central
PMC11586700
DOI
10.1002/anie.202407821
Knihovny.cz E-resources
- Keywords
- NMR spectroscopy, dGAE fragment, filamentous aggregates, tau protein, tauopathies,
- MeSH
- Chronic Traumatic Encephalopathy * metabolism pathology MeSH
- HEK293 Cells MeSH
- Humans MeSH
- tau Proteins * metabolism chemistry MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- tau Proteins * MeSH
The microtubule-associated protein tau forms disease-specific filamentous aggregates in several different neurodegenerative diseases. In order to understand how tau undergoes misfolding into a specific filament type and to control this process for drug development purposes, it is crucial to study in vitro tau aggregation methods and investigate the structures of the obtained filaments at the atomic level. Here, we used the tau fragment dGAE, which aggregates spontaneously, to seed the formation of full-length tau filaments. The structures of dGAE and full-length tau filaments were investigated by magic-angle spinning (MAS) solid-state NMR, showing that dGAE allows propagation of a chronic traumatic encephalopathy (CTE)-like fold to the full-length tau. The obtained filaments efficiently seeded tau aggregation in HEK293T cells. This work demonstrates that in vitro preparation of disease-specific types of full-length tau filaments is feasible.
CEITEC MU Masaryk University Kamenice 753 5 625 00 Brno Czech Republic
Department of Chemistry Faculty of Science Masaryk University Kamenice 5 625 00 Brno Czech Republic
Institute of Neuroimmunology Slovak Academy of Sciences Dubravska cesta 9 845 10 Bratislava Slovakia
Latvian Institute of Organic Synthesis Aizkraukles 21 Riga LV 1006 Latvia
See more in PubMed
Chiti F., Dobson C. M., Annu. Rev. Biochem. 2006, 75, 333–366. PubMed
Wang Y., Mandelkow E., Nat. Rev. Neurosci. 2015, 17, 22–35. PubMed
Sibille N., Sillen A., Leroy A., Wieruszeski J.-M., Mulloy B., Landrieu I., Lippens G., Biochemistry 2006, 45, 12560–12572. PubMed
Fitzpatrick A. W. P., Falcon B., He S., Murzin A. G., Murshudov G., Garringer H. J., Crowther R. A., Ghetti B., Goedert M., Scheres S. H. W., Nature 2017, 547, 185–190. PubMed PMC
Zhang W., Tarutani A., Newell K. L., Murzin A. G., Matsubara T., Falcon B., Vidal R., Garringer H. J., Shi Y., Ikeuchi T., Murayama S., Ghetti B., Hasegawa M., Goedert M., Scheres S. H. W., Nature 2020, 580, 283–287. PubMed PMC
Falcon B., Zivanov J., Zhang W., Murzin A. G., Garringer H. J., Vidal R., Crowther R. A., Newell K. L., Ghetti B., Goedert M., Scheres S. H. W., Nature 2019, 568, 420–423. PubMed PMC
Falcon B., Zhang W., Murzin A. G., Murshudov G., Garringer H. J., Vidal R., Crowther R. A., Ghetti B., Scheres S. H. W., Goedert M., Nature 2018, 561, 137–140. PubMed PMC
Shi Y., Zhang W., Yang Y., Murzin A. G., Falcon B., Kotecha A., van Beers M., Tarutani A., Kametani F., Garringer H. J., Vidal R., Hallinan G. I., Lashley T., Saito Y., Murayama S., Yoshida M., Tanaka H., Kakita A., Ikeuchi T., Robinson A. C., Nature 2021, 598, 359–363. PubMed PMC
Goedert M., Masuda-Suzukake M., Falcon B., Brain 2016, 140, 266–278. PubMed
Kitoka K., Skrabana R., Gasparik N., Hritz J., Jaudzems K., Front. Mol. Biosci. 2021, 8, 761227. PubMed PMC
Scheres S. H., Zhang W., Falcon B., Goedert M., Curr. Opin. Struct. Biol. 2020, 64, 17–25. PubMed
Wischik C. M., Novak M., Edwards P. C., Klug A., Tichelaar W., Crowther R. A., Proc. Natl. Acad. Sci. USA 1988, 85, 4884–4888. PubMed PMC
Sillen A., Wieruszeski J.-M., Leroy A., Younes A. B., Landrieu I., Lippens G., J. Am. Chem. Soc. 2005, 127, 10138–10139. PubMed
Wegmann S., Medalsy I. D., Mandelkow E., Müller D. J., Proc. Natl. Acad. Sci. USA 2012, 110, E313–E321. PubMed PMC
Lövestam S., Koh F. A., van Knippenberg B., Kotecha A., Murzin A. G., Goedert M., Scheres S. H., eLife 2022, 11, e76494. PubMed PMC
Lövestam S., Li D., Wagstaff J. L., Kotecha A., Kimanius D., McLaughlin S. H., Murzin A. G., Freund S. M. V., Goedert M., Scheres S. H. W., Nature 2023, 625, 119–125. PubMed PMC
Jayan P., Vahid A. A., Kizhakkeduth S. T., Muhammed S. O. H., Shibina A. B., Vijayan V., ChemBioChem 2021, 22, 2093–2097. PubMed
Chakraborty P., Rivière G., Liu S., de Opakua A. I., Dervişoğlu R., Hebestreit A., Andreas L. B., Vorberg I. M., Zweckstetter M., Nat. Commun. 2021, 12, 4231. PubMed PMC
Al-Hilaly Y. K., Hurt C., Rickard J. E., Harrington C. R., Storey J. M. D., Wischik C. M., Serpell L. C., Siemer A. B., Frontiers in Neuroscience 2022, 16, DOI 10.3389/fnins.2022.988074. PubMed DOI PMC
Duan P., Dregni A. J., El Mammeri Nadia, Hong M., Proc. Natl. Acad. Sci. USA 2023, 120,DOI 10.1073/pnas.2310067120. PubMed DOI PMC
Goedert M., Jakes R., Spillantini M. G., Hasegawa M., Smith M. J., Crowther R. A., Nature 1996, 383, 550–553. PubMed
Fichou Y., Lin Y., Rauch J. N., Vigers M., Zeng Z., Srivastava M., Keller T. J., Freed J. H., Kosik K. S., Han S., Proc. Natl. Acad. Sci. USA 2018, 115, 13234–13239. PubMed PMC
Andronesi O. C., von Bergen M., Biernat J., Seidel K., Griesinger C., Mandelkow E., Baldus M., J. Am. Chem. Soc. 2008, 130, 5922–5928. PubMed
Daebel V., Chinnathambi S., Biernat J., Schwalbe M., Habenstein B., Loquet A., Akoury E., Tepper K., Müller H., Baldus M., Griesinger C., Zweckstetter M., Mandelkow E., Vijayan V., Lange A., J. Am. Chem. Soc. 2012, 134, 13982–13989. PubMed
Xiang S., Kulminskaya N., Habenstein B., Biernat J., Tepper K., Paulat M., Griesinger C., Becker S., Lange A., Mandelkow E., Linser R., J. Am. Chem. Soc. 2017, 139, 2639–2646. PubMed
Dregni A. J., Mandala V. S., Wu H., Elkins M. R., Wang H. K., Hung I., DeGrado W. F., Hong M., Proc. Natl. Acad. Sci. USA 2019, 116, 16357–16366. PubMed PMC
Savastano A., Jaipuria G., Andreas L., Mandelkow E., Zweckstetter M., Sci. Rep. 2020, 10, 21210. PubMed PMC
Dregni A. J., Wang H. K., Wu H., Duan P., Jin J., DeGrado W. F., Hong M., J. Am. Chem. Soc. 2021, 143, 7839–7851. PubMed PMC
Zhang W., Falcon B., Murzin A. G., Fan J., Crowther R. A., Goedert M., Scheres S. H., eLife 2019, 8, e43584. PubMed PMC
McMillan P. J., Kraemer B. C., Robinson L., Leverenz J. B., Raskind M., Schellenberg G., J. Neuropathol. Exp. Neurol. 2011, 70, 1006–1019. PubMed PMC
Mena R., Edwards P. C., Harrington C. R., Mukaetova-Ladinska E. B., Wischik C. M., Acta Neuropathol. 1996, 91, 633–641. PubMed
Abraha A., Ghoshal N., Clark Gamblin T., Cryns V. L., Stephen Berry R., Kuret J., Binder L. I., J. Cell Sci. 2000, 113, 3737–3745. PubMed
Cohen S. I. A., Linse S., Luheshi L. M., Hellstrand E., White D. A., Rajah L., Otzen D. E., Vendruscolo M., Dobson C. M., Knowles T. P. J., Proc. Natl. Acad. Sci. USA 2013, 110, 9758–9763. PubMed PMC
Siemer A. B., Solid State Nucl. Magn. Reson. 2020, 106, 101643. PubMed PMC
Holmes B. B., Furman J. L., Mahan T. E., Yamasaki T. R., Mirbaha H., Eades W. C., Belaygorod L., Cairns N. J., Holtzman D. M., Diamond M. I., Proc. Natl. Acad. Sci. USA 2014, 111, E4376–E4385. PubMed PMC
Al-Hilaly Y. K., Pollack S. J., Vadukul D. M., Citossi F., Rickard J. E., Simpson M., Storey J. M. D., Harrington C. R., Wischik C. M., Serpell L. C., J. Mol. Biol. 2017, 429, 3650–3665. PubMed
Al-Hilaly Y. K., Foster B. E., Biasetti L., Lutter L., Pollack S. J., Rickard J. E., Storey J. M. D., Harrington C. R., Xue W., Wischik C. M., Serpell L. C., FEBS Lett. 2019, 594, 944–950. PubMed PMC
Lutter L., Al-Hilaly Y. K., Serpell C. J., Tuite M. F., Wischik C. M., Serpell L. C., Xue W.-F., J. Mol. Biol. 2022, 434, 167466. PubMed PMC
Skrabana R., Dvorsky R., Sevcik J., Novak M., J. Struct. Biol. 2010, 171, 74–81. PubMed
Sevcik J., Skrabana R., Dvorsky R., Csokova N., Iqbal K., Novak M., FEBS Lett. 2007, 581, 5872–5878. PubMed
Qi C., Verheijen B. M., Kokubo Yasumasa, Shi Y., Tetter S., Murzin A. G., Nakahara A., Morimoto S., Vermulst M., Sasaki R., Aronica E., Hirokawa Y., Oyanagi Kiyomitsu, Kakita Akiyoshi, Ryskeldi-Falcon B., Yoshida M., Hasegawa M., Scheres Sjors H. W., Goedert M., Proc. Natl. Acad. Sci. USA 2023, 120, DOI 10.1073/pnas.2306767120. PubMed DOI PMC
Qi C., Hasegawa M., Takao M., Sakai M., Sasaki M., Mizutani M., Akagi A., Iwasaki Y., Miyahara H., Yoshida M., Scheres Sjors H W, Goedert M., Acta Neuropathologica Communications 2023, 11, 74. PubMed PMC
Schweers O., Mandelkow E. M., Biernat J., Mandelkow E., Proc. Natl. Acad. Sci. USA 1995, 92, 8463–8467. PubMed PMC
Stöhr J., Wu H., Nick M., Wu Y., Bhate M., Condello C., Johnson N., Rodgers J., Lemmin T., Acharya S., Becker J., Robinson K., Kelly M. J. S., Gai F., Stubbs G., Prusiner S. B., DeGrado W. F., Nat. Chem. 2017, 9, 874–881. PubMed PMC
Novak P., Cehlar O., Skrabana R., Novak M., Journal of Alzheimer's disease: JAD 2018, 64, S535–S546. PubMed
Katsumoto A., Takeuchi H., Tanaka F., Frontiers in Neurology 2019, 10, 980. PubMed PMC
Taniguchi-Watanabe Sayuri, Arai T., Kametani Fuyuki, Nonaka T., Masami, Masuda-Suzukake, Tarutani Airi, Murayama S., Saito Y., Arima K., Yoshida M., Akiyama H., Robinson A., Takeshi Iwatsubo David, Hasegawa M., Acta Neuropathol. 2016, 131, 267–280. PubMed PMC
Wesseling H., Mair W., Kumar M., Schlaffner C. N., Tang S., Beerepoot P., Fatou B., Guise A. J., Cheng L., Takeda S., Muntel J., Rotunno M. S., Dujardin S., Davies P., Kosik K. S., Miller B. L., Berretta S., Hedreen J. C., Grinberg L. T., Seeley W. W., Cell 2020, 183, 1699–1713.e13. PubMed PMC
Lacabanne D., Meier B. H., Böckmann A., J. Biomol. NMR 2017, 71, 141–150. PubMed
Wiegand T., Lacabanne D., Keller K., Cadalbert R., Lecoq L., Yulikov M., Terradot L., Jeschke G., Meier B. H., Böckmann A., Angew. Chem. Int. Ed. 2017, 56, 3369–3373. PubMed
Meisl Georg, Kirkegaard J. B., Arosio Paolo, Vendruscolo Thomas M., Linse S., Knowles J., Nature Protocols 2016, 11, 252–272. PubMed
Skinner S. P., Fogh R. H., Boucher W., Ragan T. J., Mureddu L. G., Vuister G. W., J. Biomol. NMR 2016, 66, 111–124. PubMed PMC
Wang Y., Protein Sci. 2002, 11, 852–861. PubMed PMC
Zech S. G., Wand A. J., McDermott A. E., J. Am. Chem. Soc. 2005, 127, 8618–8626. PubMed
Marulanda D., Tasayco María Luisa, McDermott A. E., Cataldi M., Arriaran V., Polenova T., J. Am. Chem. Soc. 2004, 126, 16608–16620. PubMed
Zhang Y., Doherty T., Li J., Lu W., Barinka C., Lubkowski Jacek, Hong M., J. Mol. Biol. 2010, 397, 408–422. PubMed PMC
Baker P. R., Chalkley R. J., Molecular Cellular Proteomics 2014, 13, 1392–1396. PubMed PMC
Weisová P., Cehlár O., Škrabana R., Žilková M., Filipčík P., Kováčech B., Prčina M., Wojčiaková Ľ., Fialová Ľ., Smolek T., Kontseková E., Žilka N., Novák M., Acta Neuropathologica Communications 2019, 7. PubMed PMC
Holmes B. B., Furman J. L., Mahan T. E., Yamasaki T. R., Mirbaha H., Eades W. C., Belaygorod L., Cairns N. J., Holtzman D. M., Diamond M. I., Proc. Natl. Acad. Sci. USA 2014, 111, E4376–E4385. PubMed PMC
