The Amyloid Fibril-Forming β-Sheet Regions of Amyloid β and α-Synuclein Preferentially Interact with the Molecular Chaperone 14-3-3ζ
Abstract
:1. Introduction
2. Results and Discussion
2.1. Interaction of 14-3-3ζ with Amyloid β Peptides
2.2. Interaction of 14-3-3ζ with α-Synuclein
3. Materials and Methods
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Sample Availability
References
- Chiti, F.; Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 2006, 75, 333–366. [Google Scholar] [CrossRef] [Green Version]
- Knowles, T.P.; Vendruscolo, M.; Dobson, C.M. The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 2014, 15, 384–396. [Google Scholar] [CrossRef]
- Powers, E.T.; Morimoto, R.I.; Dillin, A.; Kelly, J.W.; Balch, W.E. Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 2009, 78, 959–991. [Google Scholar] [CrossRef] [Green Version]
- Walther, D.M.; Kasturi, P.; Zheng, M.; Pinkert, S.; Vecchi, G.; Ciryam, P.; Morimoto, R.I.; Dobson, C.M.; Vendruscolo, M.; Mann, M.; et al. Widespread proteome remodeling and aggregation in aging C. elegans. Cell 2015, 161, 919–932. [Google Scholar] [CrossRef] [Green Version]
- Treweek, T.M.; Meehan, S.; Ecroyd, H.; Carver, J.A. Small heat-shock proteins: Important players in regulating cellular proteostasis. Cell. Mol. Life Sci. 2015, 72, 429–451. [Google Scholar] [CrossRef] [PubMed]
- Hayashi, J.; Carver, J.A. The multifaceted nature of alphaB-crystallin. Cell Stress Chaperones 2020, 25, 639–654. [Google Scholar] [CrossRef] [PubMed]
- Yano, M.; Nakamuta, S.; Wu, X.; Okumura, Y.; Kido, H. A novel function of 14-3-3 protein: 14-3-3zeta is a heat-shock-related molecular chaperone that dissolves thermal-aggregated proteins. Mol. Biol. Cell 2006, 17, 4769–4779. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Williams, D.M.; Ecroyd, H.; Goodwin, K.L.; Dai, H.; Fu, H.; Woodcock, J.M.; Zhang, L.; Carver, J.A. NMR spectroscopy of 14-3-3zeta reveals a flexible C-terminal extension: Differentiation of the chaperone and phosphoserine-binding activities of 14-3-3zeta. Biochem. J. 2011, 437, 493–503. [Google Scholar] [CrossRef] [PubMed]
- Pair, F.S.; Yacoubian, T.A. 14-3-3 proteins: Novel pharmacological targets in neurodegenerative diseases. Trends Pharmacol. Sci. 2021, 42, 226–238. [Google Scholar] [CrossRef]
- Sluchanko, N.N.; Gusev, N.B. Moonlighting chaperone-like activity of the universal regulatory 14-3-3 proteins. FEBS J. 2017, 284, 1279–1295. [Google Scholar] [CrossRef] [Green Version]
- Kaplan, A.; Bueno, M.; Fournier, A.E. Extracellular functions of 14-3-3 adaptor proteins. Cell Signal. 2017, 31, 26–30. [Google Scholar] [CrossRef]
- Cox, D.; Carver, J.A.; Ecroyd, H. Preventing alpha-synuclein aggregation: The role of the small heat-shock molecular chaperone proteins. Biochim. Biophys. Acta 2014, 1842, 1830–1843. [Google Scholar] [CrossRef] [Green Version]
- Foote, M.; Zhou, Y. 14-3-3 proteins in neurological disorders. Int. J. Biochem. Mol. Biol. 2012, 3, 152–164. [Google Scholar] [PubMed]
- LeVine, H., 3rd. Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymool. 1999, 309, 274–284. [Google Scholar]
- Jarrett, J.T.; Berger, E.P.; Lansbury, P.T., Jr. The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimer’s disease. Biochemistry 1993, 32, 4693–4697. [Google Scholar] [CrossRef] [PubMed]
- Hudson, S.A.; Ecroyd, H.; Dehle, F.C.; Musgrave, I.F.; Carver, J.A. (−)-Epigallocatechin-3-gallate (EGCG) maintains kappa-casein in its pre-fibrillar state without redirecting its aggregation pathway. J. Mol. Biol. 2009, 392, 689–700. [Google Scholar] [CrossRef] [Green Version]
- Lindner, R.A.; Treweek, T.M.; Carver, J.A. The molecular chaperone alpha-crystallin is in kinetic competition with aggregation to stabilize a monomeric molten-globule form of alpha-lactalbumin. Biochem. J. 2001, 354, 79–87. [Google Scholar] [CrossRef]
- Carver, J.A.; Lindner, R.A.; Lyon, C.; Canet, D.; Hernandez, H.; Dobson, C.M.; Redfield, C. The interaction of the molecular chaperone alpha-crystallin with unfolding alpha-lactalbumin: A structural and kinetic spectroscopic study. J. Mol. Biol. 2002, 318, 815–827. [Google Scholar] [CrossRef]
- Treweek, T.M.; Rekas, A.; Lindner, R.A.; Walker, M.J.; Aquilina, J.A.; Robinson, C.V.; Horwitz, J.; Perng, M.D.; Quinlan, R.A.; Carver, J.A. R120G alphaB-crystallin promotes the unfolding of reduced alpha-lactalbumin and is inherently unstable. FEBS J. 2005, 272, 711–724. [Google Scholar] [CrossRef] [Green Version]
- Kulig, M.; Ecroyd, H. The small heat-shock protein alphaB-crystallin uses different mechanisms of chaperone action to prevent the amorphous versus fibrillar aggregation of alpha-lactalbumin. Biochem. J. 2012, 448, 343–352. [Google Scholar] [CrossRef] [Green Version]
- Cox, D.; Selig, E.; Griffin, M.D.; Carver, J.A.; Ecroyd, H. Small heat-shock proteins prevent alpha-synuclein aggregation via transient interactions and their efficacy is affected by the rate of aggregation. J. Biol. Chem. 2016, 291, 22618–22629. [Google Scholar] [CrossRef] [Green Version]
- Mori, H.; Takio, K.; Ogawara, M.; Selkoe, D.J. Mass spectrometry of purified amyloid beta protein in Alzheimer’s disease. J. Biol. Chem. 1992, 267, 17082–17086. [Google Scholar] [CrossRef]
- Kollmer, M.; Close, W.; Funk, L.; Rasmussen, J.; Bsoul, A.; Schierhorn, A.; Schmidt, M.; Sigurdson, C.J.; Jucker, M.; Fandrich, M. Cryo-EM structure and polymorphism of Abeta amyloid fibrils purified from Alzheimer’s brain tissue. Nat. Commun. 2019, 10, 4760. [Google Scholar] [CrossRef] [Green Version]
- Hou, L.; Zagorski, M.G. NMR reveals anomalous copper(II) binding to the amyloid Abeta peptide of Alzheimer’s disease. J. Am. Chem. Soc. 2006, 128, 9260–9261. [Google Scholar] [CrossRef] [PubMed]
- Narayan, P.; Meehan, S.; Carver, J.A.; Wilson, M.R.; Dobson, C.M.; Klenerman, D. Amyloid-beta oligomers are sequestered by both intracellular and extracellular chaperones. Biochemistry 2012, 51, 9270–9276. [Google Scholar] [CrossRef] [Green Version]
- Petkova, A.T.; Ishii, Y.; Balbach, J.J.; Antzutkin, O.N.; Leapman, R.D.; Delaglio, F.; Tycko, R. A structural model for Alzheimer’s beta-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. USA 2002, 99, 16742–16747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paravastu, A.K.; Qahwash, I.; Leapman, R.D.; Meredith, S.C.; Tycko, R. Seeded growth of beta-amyloid fibrils from Alzheimer’s brain-derived fibrils produces a distinct fibril structure. Proc. Natl. Acad. Sci. USA 2009, 106, 7443–7448. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carver, J.A.; Ecroyd, H.; Truscott, R.J.W.; Thorn, D.C.; Holt, C. Proteostasis and the regulation of intra- and extracellular protein aggregation by ATP-independent molecular chaperones: Lens alpha-crystallins and milk caseins. Acc. Chem. Res. 2018, 51, 745–752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Friedrich, R.P.; Tepper, K.; Ronicke, R.; Soom, M.; Westermann, M.; Reymann, K.; Kaether, C.; Fandrich, M. Mechanism of amyloid plaque formation suggests an intracellular basis of Abeta pathogenicity. Proc. Natl. Acad. Sci. USA 2010, 107, 1942–1947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Conway, K.A.; Harper, J.D.; Lansbury, P.T. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med. 1998, 4, 1318–1320. [Google Scholar] [CrossRef]
- Plotegher, N.; Kumar, D.; Tessari, I.; Brucale, M.; Munari, F.; Tosatto, L.; Belluzzi, E.; Greggio, E.; Bisaglia, M.; Capaldi, S.; et al. The chaperone-like protein 14-3-3eta interacts with human alpha-synuclein aggregation intermediates rerouting the amyloidogenic pathway and reducing alpha-synuclein cellular toxicity. Hum. Mol. Genet. 2014, 23, 5615–5629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rekas, A.; Adda, C.G.; Aquilina, J.A.; Barnham, K.J.; Sunde, M.; Galatis, D.; Williamson, N.A.; Masters, C.L.; Anders, R.F.; Robinson, C.V.; et al. Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: Effects on amyloid fibril formation and chaperone activity. J. Mol. Biol. 2004, 340, 1167–1183. [Google Scholar] [CrossRef]
- Rekas, A.; Jankova, L.; Thorn, D.C.; Cappai, R.; Carver, J.A. Monitoring the prevention of amyloid fibril formation by alpha-crystallin. Temperature dependence and the nature of the aggregating species. FEBS J. 2007, 274, 6290–6304. [Google Scholar] [CrossRef]
- Sluchanko, N.N.; Tugaeva, K.V.; Greive, S.J.; Antson, A.A. Chimeric 14-3-3 proteins for unraveling interactions with intrinsically disordered partners. Sci. Rep. 2017, 7, 12014. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dedmon, M.M.; Christodoulou, J.; Wilson, M.R.; Dobson, C.M. Heat shock protein 70 inhibits alpha-synuclein fibril formation via preferential binding to prefibrillar species. J. Biol. Chem. 2005, 280, 14733–14740. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burmann, B.M.; Gerez, J.A.; Matecko-Burmann, I.; Campioni, S.; Kumari, P.; Ghosh, D.; Mazur, A.; Aspholm, E.E.; Sulskis, D.; Wawrzyniuk, M.; et al. Regulation of alpha-synuclein by chaperones in mammalian cells. Nature 2020, 577, 127–132. [Google Scholar] [CrossRef] [PubMed]
- Ostrerova, N.; Petrucelli, L.; Farrer, M.; Mehta, N.; Choi, P.; Hardy, J.; Wolozin, B. Alpha-synuclein shares physical and functional homology with 14-3-3 proteins. J. Neurosci. 1999, 19, 5782–5791. [Google Scholar] [CrossRef] [Green Version]
- Wang, B.; Underwood, R.; Kamath, A.; Britain, C.; McFerrin, M.B.; McLean, P.J.; Volpicelli-Daley, L.A.; Whitaker, R.H.; Placzek, W.J.; Becker, K.; et al. 14-3-3 proteins reduce cell-to-cell transfer and propagation of pathogenic alpha-synuclein. J. Neurosci. 2018, 38, 8211–8232. [Google Scholar] [CrossRef] [Green Version]
- Doherty, C.P.A.; Ulamec, S.M.; Maya-Martinez, R.; Good, S.C.; Makepeace, J.; Khan, G.N.; van Oosten-Hawle, P.; Radford, S.E.; Brockwell, D.J. A short motif in the N-terminal region of alpha-synuclein is critical for both aggregation and function. Nat. Struct. Mol. Biol. 2020, 27, 249–259. [Google Scholar] [CrossRef]
- Guerrero-Ferreira, R.; Taylor, N.M.; Mona, D.; Ringler, P.; Lauer, M.E.; Riek, R.; Britschgi, M.; Stahlberg, H. Cryo-EM structure of alpha-synuclein fibrils. Elife 2018, 7, e36402. [Google Scholar] [CrossRef]
- Guerrero-Ferreira, R.; Taylor, N.M.; Arteni, A.A.; Kumari, P.; Mona, D.; Ringler, P.; Britschgi, M.; Lauer, M.E.; Makky, A.; Verasdonck, J.; et al. Two new polymorphic structures of human full-length alpha-synuclein fibrils solved by cryo-electron microscopy. Elife 2019, 8, e48907. [Google Scholar] [CrossRef]
- Schweighauser, M.; Shi, Y.; Tarutani, A.; Kametani, F.; Murzin, A.G.; Ghetti, B.; Matsubara, T.; Tomita, T.; Ando, T.; Hasegawa, K.; et al. Structures of alpha-synuclein filaments from multiple system atrophy. Nature 2020, 585, 464–469. [Google Scholar] [CrossRef]
- Woodcock, J.M.; Coolen, C.; Goodwin, K.L.; Baek, D.J.; Bittman, R.; Samuel, M.S.; Pitson, S.M.; Lopez, A.F. Destabilisation of dimeric 14-3-3 proteins as a novel approach to anti-cancer therapeutics. Oncotarget 2015, 6, 14522–14536. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Woodcock, J.M.; Goodwin, K.L.; Sandow, J.J.; Coolen, C.; Perugini, M.A.; Webb, A.I.; Pitson, S.M.; Lopez, A.F.; Carver, J.A. Role of salt bridges in the dimer interface of 14-3-3zeta in dimer dynamics, N-terminal alpha-helical order, and molecular chaperone activity. J. Biol. Chem. 2018, 293, 89–99. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Narhi, L.; Wood, S.J.; Steavenson, S.; Jiang, Y.; Wu, G.M.; Anafi, D.; Kaufman, S.A.; Martin, F.; Sitney, K.; Denis, P.; et al. Both familial Parkinson’s disease mutations accelerate alpha-synuclein aggregation. J. Biol. Chem. 1999, 274, 9843–9846. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Macao, B.; Hoyer, W.; Sandberg, A.; Brorsson, A.C.; Dobson, C.M.; Hard, T. Recombinant amyloid beta-peptide production by coexpression with an affibody ligand. BMC Biotechnol. 2008, 8, 82. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Provencher, S.W. CONTIN: A general purpose constrained regularization program for inverting noisy linear algebraic and integral equations. Comput. Phys. Commun. 1982, 27, 229–242. [Google Scholar] [CrossRef]
- Koppel, D.E. Analysis of macromolecular polydispersity in intensity correlation spectroscopy: The method of cumulants. J. Chem. Phys. 1972, 57, 4814–4820. [Google Scholar] [CrossRef]
- Cavanagh, J.; Fairbrother, W.J.; Palmer, A.G.; Rance, M.; Skelton, N.J. Heteronuclear NMR experiments. In Protein NMR Spectroscopy; Cavanagh, J., Fairbrother, W.J., Palmer, A.G., Rance, M., Skelton, N.J., Eds.; Academic Press: Burlington, MA, USA, 2007; pp. 533–678. [Google Scholar]
- Delaglio, F.; Grzesiek, S.; Vuister, G.W.; Zhu, G.; Pfeifer, J.; Bax, A. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 1995, 6, 277–293. [Google Scholar] [CrossRef]
- Goddard, T.D.; Kneller, D.G. SPARKY 3; University of California: San Francisco, CA, USA, 2008. [Google Scholar]
- Bussell, R., Jr.; Eliezer, D. Residual structure and dynamics in Parkinson’s disease-associated mutants of alpha-synuclein. J. Biol. Chem. 2001, 276, 45996–46003. [Google Scholar] [CrossRef] [Green Version]
- Wishart, D.S.; Bigam, C.G.; Holm, A.; Hodges, R.S.; Sykes, B.D. 1H, 13C and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 1995, 5, 67–81. [Google Scholar] [CrossRef] [PubMed]
- Shammas, S.L.; Waudby, C.A.; Wang, S.; Buell, A.K.; Knowles, T.P.; Ecroyd, H.; Welland, M.E.; Carver, J.A.; Dobson, C.M.; Meehan, S. Binding of the molecular chaperone alphaB-crystallin to Abeta amyloid fibrils inhibits fibril elongation. Biophys. J. 2011, 101, 1681–1689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Williams, D.M.; Thorn, D.C.; Dobson, C.M.; Meehan, S.; Jackson, S.E.; Woodcock, J.M.; Carver, J.A. The Amyloid Fibril-Forming β-Sheet Regions of Amyloid β and α-Synuclein Preferentially Interact with the Molecular Chaperone 14-3-3ζ. Molecules 2021, 26, 6120. https://doi.org/10.3390/molecules26206120
Williams DM, Thorn DC, Dobson CM, Meehan S, Jackson SE, Woodcock JM, Carver JA. The Amyloid Fibril-Forming β-Sheet Regions of Amyloid β and α-Synuclein Preferentially Interact with the Molecular Chaperone 14-3-3ζ. Molecules. 2021; 26(20):6120. https://doi.org/10.3390/molecules26206120
Chicago/Turabian StyleWilliams, Danielle M., David C. Thorn, Christopher M. Dobson, Sarah Meehan, Sophie E. Jackson, Joanna M. Woodcock, and John A. Carver. 2021. "The Amyloid Fibril-Forming β-Sheet Regions of Amyloid β and α-Synuclein Preferentially Interact with the Molecular Chaperone 14-3-3ζ" Molecules 26, no. 20: 6120. https://doi.org/10.3390/molecules26206120