The viral protein corona directs viral pathogenesis and amyloid aggregation

Kariem Ezzat; Maria Pernemalm; Sandra Pålsson; Thomas C. Roberts; Peter Järver; Aleksandra Dondalska; Burcu Bestas; Michal J. Sobkowiak; Bettina Levänen; Magnus Sköld; Elizabeth A. Thompson; Osama Saher; Otto K. Kari; Tatu Lajunen; Eva Sverremark Ekström; Caroline Nilsson; Yevheniia Ishchenko; Tarja Malm; Matthew J.A. Wood; Ultan F. Power; Sergej Masich; Anders Lindén; Johan K. Sandberg; Janne Lehtiö; Anna Lena Spetz; Samir EL Andaloussi

doi:10.1038/s41467-019-10192-2

The viral protein corona directs viral pathogenesis and amyloid aggregation

Kariem Ezzat, Maria Pernemalm, Sandra Pålsson, Thomas C. Roberts, Peter Järver, Aleksandra Dondalska, Burcu Bestas, Michal J. Sobkowiak, Bettina Levänen, Magnus Sköld, Elizabeth A. Thompson, Osama Saher, Otto K. Kari, Tatu Lajunen, Eva Sverremark Ekström, Caroline Nilsson, Yevheniia Ishchenko, Tarja Malm, Matthew J.A. Wood, Ultan F. PowerSergej Masich, Anders Lindén, Johan K. Sandberg, Janne Lehtiö, Anna Lena Spetz, Samir EL Andaloussi

Research output: Contribution to journal › Article › peer-review

Abstract

Artificial nanoparticles accumulate a protein corona layer in biological fluids, which significantly influences their bioactivity. As nanosized obligate intracellular parasites, viruses share many biophysical properties with artificial nanoparticles in extracellular environments and here we show that respiratory syncytial virus (RSV) and herpes simplex virus type 1 (HSV-1) accumulate a rich and distinctive protein corona in different biological fluids. Moreover, we show that corona pre-coating differentially affects viral infectivity and immune cell activation. In addition, we demonstrate that viruses bind amyloidogenic peptides in their corona and catalyze amyloid formation via surface-assisted heterogeneous nucleation. Importantly, we show that HSV-1 catalyzes the aggregation of the amyloid β-peptide (Aβ₄₂), a major constituent of amyloid plaques in Alzheimer’s disease, in vitro and in animal models. Our results highlight the viral protein corona as an acquired structural layer that is critical for viral–host interactions and illustrate a mechanistic convergence between viral and amyloid pathologies.

Original language	English (US)
Article number	2331
Journal	Nature communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-10192-2
State	Published - Dec 1 2019
Externally published	Yes

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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Ezzat, K., Pernemalm, M., Pålsson, S., Roberts, T. C., Järver, P., Dondalska, A., Bestas, B., Sobkowiak, M. J., Levänen, B., Sköld, M., Thompson, E. A., Saher, O., Kari, O. K., Lajunen, T., Sverremark Ekström, E., Nilsson, C., Ishchenko, Y., Malm, T., Wood, M. J. A., ... EL Andaloussi, S. (2019). The viral protein corona directs viral pathogenesis and amyloid aggregation. Nature communications, 10(1), Article 2331. https://doi.org/10.1038/s41467-019-10192-2

Ezzat, K, Pernemalm, M, Pålsson, S, Roberts, TC, Järver, P, Dondalska, A, Bestas, B, Sobkowiak, MJ, Levänen, B, Sköld, M, Thompson, EA, Saher, O, Kari, OK, Lajunen, T, Sverremark Ekström, E, Nilsson, C, Ishchenko, Y, Malm, T, Wood, MJA, Power, UF, Masich, S, Lindén, A, Sandberg, JK, Lehtiö, J, Spetz, AL & EL Andaloussi, S 2019, 'The viral protein corona directs viral pathogenesis and amyloid aggregation', Nature communications, vol. 10, no. 1, 2331. https://doi.org/10.1038/s41467-019-10192-2

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title = "The viral protein corona directs viral pathogenesis and amyloid aggregation",

abstract = "Artificial nanoparticles accumulate a protein corona layer in biological fluids, which significantly influences their bioactivity. As nanosized obligate intracellular parasites, viruses share many biophysical properties with artificial nanoparticles in extracellular environments and here we show that respiratory syncytial virus (RSV) and herpes simplex virus type 1 (HSV-1) accumulate a rich and distinctive protein corona in different biological fluids. Moreover, we show that corona pre-coating differentially affects viral infectivity and immune cell activation. In addition, we demonstrate that viruses bind amyloidogenic peptides in their corona and catalyze amyloid formation via surface-assisted heterogeneous nucleation. Importantly, we show that HSV-1 catalyzes the aggregation of the amyloid β-peptide (Aβ42), a major constituent of amyloid plaques in Alzheimer{\textquoteright}s disease, in vitro and in animal models. Our results highlight the viral protein corona as an acquired structural layer that is critical for viral–host interactions and illustrate a mechanistic convergence between viral and amyloid pathologies.",

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AU - Ezzat, Kariem

AU - Pernemalm, Maria

AU - Pålsson, Sandra

AU - Roberts, Thomas C.

AU - Järver, Peter

AU - Dondalska, Aleksandra

AU - Bestas, Burcu

AU - Sobkowiak, Michal J.

AU - Levänen, Bettina

AU - Sköld, Magnus

AU - Thompson, Elizabeth A.

AU - Saher, Osama

AU - Kari, Otto K.

AU - Lajunen, Tatu

AU - Sverremark Ekström, Eva

AU - Nilsson, Caroline

AU - Ishchenko, Yevheniia

AU - Malm, Tarja

AU - Wood, Matthew J.A.

AU - Power, Ultan F.

AU - Masich, Sergej

AU - Lindén, Anders

AU - Sandberg, Johan K.

AU - Lehtiö, Janne

AU - Spetz, Anna Lena

AU - EL Andaloussi, Samir

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Artificial nanoparticles accumulate a protein corona layer in biological fluids, which significantly influences their bioactivity. As nanosized obligate intracellular parasites, viruses share many biophysical properties with artificial nanoparticles in extracellular environments and here we show that respiratory syncytial virus (RSV) and herpes simplex virus type 1 (HSV-1) accumulate a rich and distinctive protein corona in different biological fluids. Moreover, we show that corona pre-coating differentially affects viral infectivity and immune cell activation. In addition, we demonstrate that viruses bind amyloidogenic peptides in their corona and catalyze amyloid formation via surface-assisted heterogeneous nucleation. Importantly, we show that HSV-1 catalyzes the aggregation of the amyloid β-peptide (Aβ42), a major constituent of amyloid plaques in Alzheimer’s disease, in vitro and in animal models. Our results highlight the viral protein corona as an acquired structural layer that is critical for viral–host interactions and illustrate a mechanistic convergence between viral and amyloid pathologies.

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The viral protein corona directs viral pathogenesis and amyloid aggregation

Abstract

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