Insights into the cross-amyloid aggregation of Aβ40 and its N-terminal truncated peptide Aβ11-40 affected by epigallocatechin gallate

doi:10.1016/j.cjche.2021.04.018

Abstract

Abstract: Inhibition of protein misfolding and aggregation is a great challenge in the field of biochemical and biopharmaceutical engineering. Alzheimer's disease (AD) is a protein-misfolding disease, and the interactions between 40-amino-acid-residue β-amyloid peptide (Aβ₄₀) and its N-terminal truncated peptide Aβ_11-40 demonstrate that Aβ_11-40 may play an important role in the pathological process of AD. However, the effect of inhibitors on Aβ_11-40 aggregation and on the cross-amyloid aggregation (co-assembly) between Aβ₄₀ and Aβ_11-40 has never been studied. Herein, coaggregation and seeding interactions between Aβ₄₀ and Aβ_11-40 as well as the effect of epigallocatechin gallate (EGCG), a small molecule inhibitor, on the cross-amyloid aggregation have been investigated by extensive analyses. It is found that Aβ_11-40 participates in the aggregation of Aβ₄₀ and leads to the formation of coaggregates that contain less β-sheet structures than pure Aβ₄₀ aggregates. The aggregation kinetics along with morphologies and secondary structures of the coaggregates are also significantly affected by the Aβ₄₀/Aβ_11-40 ratio. EGCG accelerates the nucleation of Aβ₄₀ but retards that of Aβ_11-40 by affecting their elongation and secondary nucleation processes in solution and on solid surfaces. Meanwhile, EGCG makes the conformations of the seeding-induced Aβ aggregates more compact, especially for the homologous seedings. Isothermal titration calorimetry measurement indicates that hydrophobic interactions mainly contribute to the inhibition of the two Aβ isoforms by EGCG. The findings of this research have provided new insights into Aβ aggregation and the effect of an important inhibitor and the results would benefit in the development of potent inhibitors against co-assembly of different amyloid proteins.

Key words: Protein, Aggregation, Kinetics, Nucleation, Elongation, Molecular interactions

摘要： Inhibition of protein misfolding and aggregation is a great challenge in the field of biochemical and biopharmaceutical engineering. Alzheimer's disease (AD) is a protein-misfolding disease, and the interactions between 40-amino-acid-residue β-amyloid peptide (Aβ₄₀) and its N-terminal truncated peptide Aβ_11-40 demonstrate that Aβ_11-40 may play an important role in the pathological process of AD. However, the effect of inhibitors on Aβ_11-40 aggregation and on the cross-amyloid aggregation (co-assembly) between Aβ₄₀ and Aβ_11-40 has never been studied. Herein, coaggregation and seeding interactions between Aβ₄₀ and Aβ_11-40 as well as the effect of epigallocatechin gallate (EGCG), a small molecule inhibitor, on the cross-amyloid aggregation have been investigated by extensive analyses. It is found that Aβ_11-40 participates in the aggregation of Aβ₄₀ and leads to the formation of coaggregates that contain less β-sheet structures than pure Aβ₄₀ aggregates. The aggregation kinetics along with morphologies and secondary structures of the coaggregates are also significantly affected by the Aβ₄₀/Aβ_11-40 ratio. EGCG accelerates the nucleation of Aβ₄₀ but retards that of Aβ_11-40 by affecting their elongation and secondary nucleation processes in solution and on solid surfaces. Meanwhile, EGCG makes the conformations of the seeding-induced Aβ aggregates more compact, especially for the homologous seedings. Isothermal titration calorimetry measurement indicates that hydrophobic interactions mainly contribute to the inhibition of the two Aβ isoforms by EGCG. The findings of this research have provided new insights into Aβ aggregation and the effect of an important inhibitor and the results would benefit in the development of potent inhibitors against co-assembly of different amyloid proteins.

关键词: Protein, Aggregation, Kinetics, Nucleation, Elongation, Molecular interactions

Yue Liang, Wenjuan Wang, Yan Sun, Xiaoyan Dong. Insights into the cross-amyloid aggregation of Aβ₄₀ and its N-terminal truncated peptide Aβ_11-40 affected by epigallocatechin gallate[J]. Chinese Journal of Chemical Engineering, 2022, 45(5): 284-293.

References

[1] R. M. Murphy, B. S. Kendrick, Protein misfolding and aggregation, Biotechnol. Progr. 23 (2007) 548-552
[2] C. A. Ross, M. A. Poirier, Protein aggregation and neurodegenerative disease, Nat. Med. 10 Suppl (2004) S10-S17
[3] J. Hardy, D. J. Selkoe, The amyloid hypothesis of Alzheimer's disease-progress and problems on the road to therapeutics, Science 297 (2002) 353-356
[4] V. Fodera, F. Librizzi, M. Groenning, M. Van De Weert, M. Leone, Secondary nucleation and accessible surface in insulin amyloid fibril formation, J. Phys. Chem. B 112 (2008) 3853-3858
[5] L. Xu, Y. Chen, X. Wang, Assembly of amyloid β peptides in the presence of fibril seeds:one-pot coarse-grained molecular dynamics simulations, J. Phys. Chem. B 118 (31) (2014) 9238-9246
[6] P. Seubert, C. Vigo-Pelfrey, F. Esch, M. Lee, H. Dovey, D. Davis, S. Sinha, M. Schlossmacher, J. Whaley, C. Swindlehurst, R. Mccormack, R. Wolfert, D. Selkoe, I. Lieberburg, D. Schenk, Isolation and quantification of soluble Alzheimer's β-peptide form biological fluids, Nature 359 (1992) 325-327
[7] L. Miravalle, M. Calero, M. Takao, A. E. Roher, B. Ghetti, R. Vidal, Amino-terminally truncated Aβ peptide species are the main component of cotton wool plaques, Biochemistry 44 (2005) 10810-10821
[8] D. L. Milller, I. A. Papayannopoulos, J. Styles, S. A. Bobin, Y. Y. Lin, K. Biemann, K. Iqbal, Peptide compositions of the cerebrovascular and senile plaque core amyloid deposits of Alzheimer's disease, Arch. Biochem. Biophys. 301 (1993) 41-52
[9] J. Naslund, A. Schierhorn, U. Hellman, L. Lannfelt, A. D. Roses, L. O. Tjernberg, J. Silberring, S. E. Gandy, B. Winblad, P. Greengard, C. Nordtedt, L. Terenius, Relative abundance of Alzheimer Aβ amyloid peptide variants in AD and normal aging P. Natl. Acad. Sci. 91 (1994) 8378-8382
[10] K. Liu, I. Solano, D. Mann, C. Lemere, M. Mercken, J. Q. Trojanowski, V. M. Lee, Characterization of Aβ11-40/42 peptide deposition in Alzheimer's disease and young Down's syndrome brains:implication of N-terminally truncated Aβ species in the pathogenesis of Alzheimer's disease, Acta Neuropathol. 112 (2) (2006) 163-174
[11] J. D. Barritt, N. D. Younan, J. H. Viles, N-terminally truncated amyloid-β(11-40/42) cofibrillizes with its full-length counterpart:implications for Alzheimer's disease, Angew. Chem. Int. Edtt. 56 (33) (2017) 9816-9819
[12] X. Hao, J. Zheng, Y. Sun, X. Dong, Seeding and cross-seeding aggregations of Aβ40 and its N-terminal-truncated peptide Aβ11-40, Langmuir 35 (7) (2019) 2821-2831
[13] T. A. Mirzabekov, M. Lin, B. L. Kagan, Pore formation by the cytotoxic islet amyloid peptide amylin, J. Biol. Chem. 271 (1996) 1988-1992
[14] H. Ogi, Y. Fukunishi, T. Yanagida, H. Yagi, Y. Goto, M. Fukushima, K. Uesugi, M. Hirao, Seed-dependent deposition behavior of Aβ peptides studied with wireless quartz-crystal-microbalance biosensor, Anal. Chem. 83 (12) (2011) 4982-4988
[15] K. A. Marx, Quartz crystal microbalance:a useful tool for studying thin polymer films and complex biomolecular systems at the solution-surface interface, Biomacromolecules 4 (2003) 1099-1120
[16] D. J. Selkoe, J. Hardy, The amyloid hypothesis of Alzheimer's disease at 25 years, EMBO Mol. Med. 8 (6) (2016) 595-608
[17] X. Han, G. He, Toward a rational design to regulate β-amyloid fibrillation for Alzheimer's disease treatment, ACS Chem. Neurosci. 9 (2) (2018) 198-210
[18] S. H. Wang, X. Y. Dong, Y. Sun, Thermodynamic analysis of the molecular interactions between amyloid β-protein fragments and (-)-epigallocatechin-3-gallate, J. Phys. Chem. B 116 (20) (2012) 5803-5809
[19] J. Bieschke, J. Russ, R. P. Friedrich, D. E. Ehrnhoefer, H. Wobst, K. Neugebauer, E. E. Wanker, EGCG remodels mature α-synuclein and amyloid-β fibrils and reduces cellular toxicity, Proc. Natl. Acad. Sci.107 (17) (2010) 7710-7715
[20] D. E. Ehrnhoefer, J. Bieschke, A. Boeddrich, M. Herbst, L. Masino, R. Lurz, S. Engemann, A. Pastore, E. E. Wanker, EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers, Nat. Struct. Mol. Biol. 15 (6) (2008) 558-566
[21] S. Chan, S. Kantham, V. M. Rao, M. K. Palanivelu, H. L. Pham, P. N. Shaw, R. P. Mcgeary, B. P. Ross, Metal chelation, radical scavenging and inhibition of Aβ(42) fibrillation by food constituents in relation to Alzheimer's disease, Food Chem. 199 (2016) 185-194
[22] S. A. Mandel, T. Amit, L. Kalfon, L. Reznichenko, M. B. H. Youdim, Targeting multiple neurodegenerative diseases etiologies with multimodal-acting green tea catechins, J. Nutr. 138 (2008) 1578S-1583S
[23] N. Dragicevic, A. Smith, X. Lin, F. Yuan, N. Copes, V. Delic, J. Tan, C. Cao, R. D. Shytle, P. C. Bradshaw, Green tea epigallocatechin-3-gallate (EGCG) and other flavonoids reduce Alzheimer's amyloid-induced mitochondrial dysfunction, J. Alzheimers Dis. 26 (3) (2011) 507-521
[24] Q. Wang, N. Shah, J. Zhao, C. Wang, C. Zhao, L. Liu, L. Li, F. Zhou, J. Zheng, Structural, morphological, and kinetic studies of β-amyloid peptide aggregation on self-assembled monolayers, Phys. Chem. Chem. Phys. 13 (33) (2011) 15200-15210
[25] C. Streich, L. Akkari, C. Decker, J. Bormann, C. Rehbock, A. Muller-Schiffmann, F. C. Niemeyer, L. Nagel-Steger, D. Willbold, B. Sacca, C. Korth, T. Schrader, S. Barcikowski, Characterizing the effect of multivalent conjugates composed of Aβ-specific ligands and metal nanoparticles on neurotoxic fibrillar aggregation, ACS Nano 10 (8) (2016) 7582-7597
[26] C. Wang, L. Xu, F. Cheng, H. Wang, L. Jia, Curcumin induces structural change and reduces the growth of amyloid-β fibrils:a QCM-D study, RSC Adv. 5 (38) (2015) 30197-30205
[27] M. V. Voinova, M. Rodahl, M. Jonson, B. Kasemo, Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces:continuum mechanics approach, Phys. Scr. 59 (1999)
[28] J. D. Barritt, J. H. Viles, Truncated amyloid-β(11-40/42) from Alzheimer disease binds Cu²⁺ with a femtomolar affinity and influences fiber assembly, J. Biol. Chem. 290 (46) (2015) 27791-27802
[29] T. Weiffert, G. Meisl, P. Flagmeier, S. De, C. J. R. Dunning, B. Frohm, H. Zetterberg, K. Blennow, E. Portelius, D. Klenerman, C. M. Dobson, T. P. J. Knowles, S. Linse, Increased secondary nucleation underlies accelerated aggregation of the four-residue N-terminally truncated Aβ42 species Aβ5-42, ACS Chem. Neurosci. 10 (5) (2019) 2374-2384
[30] D. Meral, B. Urbanc, Discrete molecular dynamics study of oligomer formation by N-terminally truncated amyloid β-protein, J. Mol. Biol. 425 (12) (2013) 2260-2275
[31] M. M. Murray, S. L. Bernstein, V. Nyugen, M. M. Condron, D. B. Teplow, M. T. Bowers, Amyloid β protein:Aβ40 inhibits Aβ42 oligomerization, J. Am. Chem. Soc. 131 (2009) 6316-6137
[32] J. Seeliger, K. Weise, N. Opitz, R. Winter, The effect of Aβ on IAPP aggregation in the presence of an isolated β-cell membrane, J. Mol. Biol. 421 (2-3) (2012) 348-363
[33] X. Ge, Y. Yang, Y. Sun, W. Cao, F. Ding, Islet amyloid polypeptide promotes amyloid-beta aggregation by binding-induced helix-unfolding of the amyloidogenic core, ACS Chem. Neurosci. 9 (5) (2018) 967-975
[34] A. I. Ilitchev, M. J. Giammona, C. Olivas, S. L. Claud, K. L. Lazar Cantrell, C. Wu, S. K. Buratto, M. T. Bowers, Hetero-oligomeric amyloid assembly and mechanism:prion fragment PrP(106-126) catalyzes the islet amyloid polypeptide β-hairpin, J. Am. Chem. Soc. 140 (30) (2018) 9685-9695
[35] K. Pauwels, T. L. Williams, K. L. Morris, W. Jonckheere, A. Vandersteen, G. Kelly, J. Schymkowitz, F. Rousseau, A. Pastore, L. C. Serpell, K. Broersen, Structural basis for increased toxicity of pathological Aβ42:Aβ40 ratios in Alzheimer disease, J. Biol. Chem. 287 (8) (2012) 5650-5660
[36] C. A. Soldner, H. Sticht, A. H. C. Horn, Role of the N-terminus for the stability of an amyloid-β fibril with three-fold symmetry, PLoS One 12 (10) (2017) e0186347
[37] Y. Miura, K. Yasuda, K. Yamamoto, M. Koike, Y. Nishida, K. Kobayashi, Inhibition of Alzheimer amyloid aggregation with sulfated glycopolymers, Biomacromolecules 8 (2007) 2129-2134
[38] K. Matsuzaki, K. Kato, K. Yanagisawa, Aβ polymerization through interaction with membrane gangliosides, Biochim. Biophys. Acta 1801 (8) (2010) 868-877
[39] P. Arosio, T. P. Knowles, S. Linse, On the lag phase in amyloid fibril formation, Phys. Chem. Chem. Phys. 17 (12) (2015) 7606-7618
[40] S. T. Ngo, D. T. Truong, N. M. Tam, M. T. Nguyen, EGCG inhibits the oligomerization of amyloid beta (16-22) hexamer:theoretical studies, J. Mol. Graph. Model. 76 (2017) 1-10
[41] S. J. Hyung, A. S. Detoma, J. R. Brender, S. Lee, S. Vivekanandan, A. Kochi, J. S. Choi, A. Ramamoorthy, B. T. Ruotolo, M. H. Lim, Insights into antiamyloidogenic properties of the green tea extract (-)-epigallocatechin-3-gallate toward metal-associated amyloid-β species, Proc. Natl. Acad. Sci. 110 (10) (2013) 3743-3748
[42] Q. Chen, S. Xu, Q. Liu, J. Masliyah, Z. Xu, QCM-D study of nanoparticle interactions, Adv. Colloid Interface 233 (2016) 94-114
[43] S. H. Wang, F. F. Liu, X. Y. Dong, Y. Sun, Thermodynamic analysis of the molecular interactions between amyloid β- peptide 42 and (-)-epigallocatechin-3-gallate, J. Phys. Chem. B 114 (2010) 11576-11583
[44] P. D. Ross, S. Subramanian, Thermodynamics of protein association reactions:forces contributing to stability, Biochemistry 20 (11) (1981) 3096-3102
[45] J. M. Sturtevant, Heat capacity and entropy changes in processes involving proteins, P. Natl. Acad. Sci. 74 (6) (1977) 2236-2240
[46] J. M. Lopez Del Amo, U. Fink, M. Dasari, G. Grelle, E. E. Wanker, J. Bieschke, B. Reif, Structural properties of EGCG-induced, nontoxic Alzheimer's disease Aβ oligomers, J. Mol. Biol. 421 (4-5) (2012) 517-524
[47] J. Wang, T. Yamamoto, J. Bai, S. J. Cox, K. J. Korshavn, M. Monette, A. Ramamoorthy, Real-time monitoring of the aggregation of Alzheimer's amyloid-β via(1)H magic angle spinning NMR spectroscopy, Chem. Commun. 54 (16) (2018) 2000-2003

Insights into the cross-amyloid aggregation of Aβ₄₀ and its N-terminal truncated peptide Aβ_11-40 affected by epigallocatechin gallate

Insights into the cross-amyloid aggregation of Aβ₄₀ and its N-terminal truncated peptide Aβ_11-40 affected by epigallocatechin gallate

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