High-resolution photocatalytic mapping of SARS-CoV-2 spike interactions on the cell surface

Suprama Datta; Da Yuan Chen; Alexander H. Tavares; Tamara Reyes-Robles; Keun Ah Ryu; Nazimuddin Khan; Tyler J. Bechtel; Jayde M. Bertoch; Cory H. White; Daria J. Hazuda; Kalpit A. Vora; Erik C. Hett; Olugbeminiyi O. Fadeyi; Rob C. Oslund; Andrew Emili; Mohsan Saeed

doi:10.1016/j.chembiol.2023.06.028

High-resolution photocatalytic mapping of SARS-CoV-2 spike interactions on the cell surface

Suprama Datta, Da Yuan Chen, Alexander H. Tavares, Tamara Reyes-Robles, Keun Ah Ryu, Nazimuddin Khan, Tyler J. Bechtel, Jayde M. Bertoch, Cory H. White, Daria J. Hazuda, Kalpit A. Vora, Erik C. Hett, Olugbeminiyi O. Fadeyi, Rob C. Oslund, Andrew Emili, Mohsan Saeed

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

2 Scopus citations

Abstract

Identifying virus-host interactions on the cell surface can improve our understanding of viral entry and pathogenesis. SARS-CoV-2, the causative agent of the COVID-19 disease, uses ACE2 as a receptor to enter cells. Yet the full repertoire of cell surface proteins that contribute to viral entry is unknown. We developed a photocatalyst-based viral-host protein microenvironment mapping platform (ViraMap) to probe the molecular neighborhood of the SARS-CoV-2 spike protein on the human cell surface. Application of ViraMap to ACE2-expressing cells captured ACE2, the established co-receptor NRP1, and several novel cell surface proteins. We systematically analyzed the relevance of these candidate proteins to SARS-CoV-2 entry by knockdown and overexpression approaches in pseudovirus and authentic infection models and identified PTGFRN and EFNB1 as bona fide viral entry factors. Our results highlight additional host targets that participate in SARS-CoV-2 infection and showcase ViraMap as a powerful platform for defining viral interactions on the cell surface.

Original language	English (US)
Pages (from-to)	1313-1322.e7
Journal	Cell Chemical Biology
Volume	30
Issue number	10
DOIs	https://doi.org/10.1016/j.chembiol.2023.06.028
State	Published - Oct 19 2023
Externally published	Yes

Keywords

SARS-CoV-2
photocatalysis
proximity labeling
viral entry
viral-host interactome

ASJC Scopus subject areas

Biochemistry
Molecular Medicine
Molecular Biology
Pharmacology
Drug Discovery
Clinical Biochemistry

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10.1016/j.chembiol.2023.06.028

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Datta, S., Chen, D. Y., Tavares, A. H., Reyes-Robles, T., Ryu, K. A., Khan, N., Bechtel, T. J., Bertoch, J. M., White, C. H., Hazuda, D. J., Vora, K. A., Hett, E. C., Fadeyi, O. O., Oslund, R. C., Emili, A., & Saeed, M. (2023). High-resolution photocatalytic mapping of SARS-CoV-2 spike interactions on the cell surface. Cell Chemical Biology, 30(10), 1313-1322.e7. https://doi.org/10.1016/j.chembiol.2023.06.028

Datta, S, Chen, DY, Tavares, AH, Reyes-Robles, T, Ryu, KA, Khan, N, Bechtel, TJ, Bertoch, JM, White, CH, Hazuda, DJ, Vora, KA, Hett, EC, Fadeyi, OO, Oslund, RC, Emili, A & Saeed, M 2023, 'High-resolution photocatalytic mapping of SARS-CoV-2 spike interactions on the cell surface', Cell Chemical Biology, vol. 30, no. 10, pp. 1313-1322.e7. https://doi.org/10.1016/j.chembiol.2023.06.028

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abstract = "Identifying virus-host interactions on the cell surface can improve our understanding of viral entry and pathogenesis. SARS-CoV-2, the causative agent of the COVID-19 disease, uses ACE2 as a receptor to enter cells. Yet the full repertoire of cell surface proteins that contribute to viral entry is unknown. We developed a photocatalyst-based viral-host protein microenvironment mapping platform (ViraMap) to probe the molecular neighborhood of the SARS-CoV-2 spike protein on the human cell surface. Application of ViraMap to ACE2-expressing cells captured ACE2, the established co-receptor NRP1, and several novel cell surface proteins. We systematically analyzed the relevance of these candidate proteins to SARS-CoV-2 entry by knockdown and overexpression approaches in pseudovirus and authentic infection models and identified PTGFRN and EFNB1 as bona fide viral entry factors. Our results highlight additional host targets that participate in SARS-CoV-2 infection and showcase ViraMap as a powerful platform for defining viral interactions on the cell surface.",

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AU - Chen, Da Yuan

AU - Tavares, Alexander H.

AU - Reyes-Robles, Tamara

AU - Ryu, Keun Ah

AU - Khan, Nazimuddin

AU - Bechtel, Tyler J.

AU - Bertoch, Jayde M.

AU - White, Cory H.

AU - Hazuda, Daria J.

AU - Vora, Kalpit A.

AU - Hett, Erik C.

AU - Fadeyi, Olugbeminiyi O.

AU - Oslund, Rob C.

AU - Emili, Andrew

AU - Saeed, Mohsan

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N2 - Identifying virus-host interactions on the cell surface can improve our understanding of viral entry and pathogenesis. SARS-CoV-2, the causative agent of the COVID-19 disease, uses ACE2 as a receptor to enter cells. Yet the full repertoire of cell surface proteins that contribute to viral entry is unknown. We developed a photocatalyst-based viral-host protein microenvironment mapping platform (ViraMap) to probe the molecular neighborhood of the SARS-CoV-2 spike protein on the human cell surface. Application of ViraMap to ACE2-expressing cells captured ACE2, the established co-receptor NRP1, and several novel cell surface proteins. We systematically analyzed the relevance of these candidate proteins to SARS-CoV-2 entry by knockdown and overexpression approaches in pseudovirus and authentic infection models and identified PTGFRN and EFNB1 as bona fide viral entry factors. Our results highlight additional host targets that participate in SARS-CoV-2 infection and showcase ViraMap as a powerful platform for defining viral interactions on the cell surface.

AB - Identifying virus-host interactions on the cell surface can improve our understanding of viral entry and pathogenesis. SARS-CoV-2, the causative agent of the COVID-19 disease, uses ACE2 as a receptor to enter cells. Yet the full repertoire of cell surface proteins that contribute to viral entry is unknown. We developed a photocatalyst-based viral-host protein microenvironment mapping platform (ViraMap) to probe the molecular neighborhood of the SARS-CoV-2 spike protein on the human cell surface. Application of ViraMap to ACE2-expressing cells captured ACE2, the established co-receptor NRP1, and several novel cell surface proteins. We systematically analyzed the relevance of these candidate proteins to SARS-CoV-2 entry by knockdown and overexpression approaches in pseudovirus and authentic infection models and identified PTGFRN and EFNB1 as bona fide viral entry factors. Our results highlight additional host targets that participate in SARS-CoV-2 infection and showcase ViraMap as a powerful platform for defining viral interactions on the cell surface.

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High-resolution photocatalytic mapping of SARS-CoV-2 spike interactions on the cell surface

Abstract

Keywords

ASJC Scopus subject areas

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