Mapping of functional SARS-CoV-2 receptors in human lungs establishes differences in variant binding and SLC1A5 as a viral entry modulator of hACE2.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Jan 2023
Historique:
received: 16 07 2021
revised: 15 11 2022
accepted: 17 11 2022
pubmed: 31 12 2022
medline: 21 1 2023
entrez: 30 12 2022
Statut: ppublish

Résumé

The COVID-19 pandemic is an infectious disease caused by SARS-CoV-2. The first step of SARS-CoV-2 infection is the recognition of angiotensin-converting enzyme 2 (ACE2) receptors by the receptor-binding domain (RBD) of the viral Spike (S) glycoprotein. Although the molecular and structural bases of the SARS-CoV-2-RBD/hACE2 interaction have been thoroughly investigated in vitro, the relationship between hACE2 expression and in vivo infection is less understood. Here, we developed an efficient SARS-CoV-2-RBD binding assay suitable for super resolution microscopy and simultaneous hACE2 immunodetection and mapped the correlation between hACE2 receptor abundance and SARS-CoV-2-RBD binding, both in vitro and in human lung biopsies. Next, we explored the specific proteome of SARS-CoV-2-RBD/hACE2 through a comparative mass spectrometry approach. We found that only a minority of hACE2 positive spots are actually SARS-CoV-2-RBD binding sites, and that the relationship between SARS-CoV-2-RBD binding and hACE2 presence is variable, suggesting the existence of additional factors. Indeed, we found several interactors that are involved in receptor localization and viral entry and characterized one of them: SLC1A5, an amino acid transporter. High-resolution receptor-binding studies showed that co-expression of membrane-bound SLC1A5 with hACE2 predicted SARS-CoV-2 binding and entry better than hACE2 expression alone. SLC1A5 depletion reduces SARS-CoV-2 binding and entry. Notably, the Omicron variant is more efficient in binding hACE2 sites, but equally sensitive to SLC1A5 downregulation. We propose a method for mapping functional SARS-CoV-2 receptors in vivo. We confirm the existence of hACE2 co-factors that may contribute to differential sensitivity of cells to infection. This work was supported by an unrestricted grant from "Fondazione Romeo ed Enrica Invernizzi" to Stefano Biffo and by AIRC under MFAG 2021 - ID. 26178 project - P.I. Manfrini Nicola.

Sections du résumé

BACKGROUND BACKGROUND
The COVID-19 pandemic is an infectious disease caused by SARS-CoV-2. The first step of SARS-CoV-2 infection is the recognition of angiotensin-converting enzyme 2 (ACE2) receptors by the receptor-binding domain (RBD) of the viral Spike (S) glycoprotein. Although the molecular and structural bases of the SARS-CoV-2-RBD/hACE2 interaction have been thoroughly investigated in vitro, the relationship between hACE2 expression and in vivo infection is less understood.
METHODS METHODS
Here, we developed an efficient SARS-CoV-2-RBD binding assay suitable for super resolution microscopy and simultaneous hACE2 immunodetection and mapped the correlation between hACE2 receptor abundance and SARS-CoV-2-RBD binding, both in vitro and in human lung biopsies. Next, we explored the specific proteome of SARS-CoV-2-RBD/hACE2 through a comparative mass spectrometry approach.
FINDINGS RESULTS
We found that only a minority of hACE2 positive spots are actually SARS-CoV-2-RBD binding sites, and that the relationship between SARS-CoV-2-RBD binding and hACE2 presence is variable, suggesting the existence of additional factors. Indeed, we found several interactors that are involved in receptor localization and viral entry and characterized one of them: SLC1A5, an amino acid transporter. High-resolution receptor-binding studies showed that co-expression of membrane-bound SLC1A5 with hACE2 predicted SARS-CoV-2 binding and entry better than hACE2 expression alone. SLC1A5 depletion reduces SARS-CoV-2 binding and entry. Notably, the Omicron variant is more efficient in binding hACE2 sites, but equally sensitive to SLC1A5 downregulation.
INTERPRETATION CONCLUSIONS
We propose a method for mapping functional SARS-CoV-2 receptors in vivo. We confirm the existence of hACE2 co-factors that may contribute to differential sensitivity of cells to infection.
FUNDING BACKGROUND
This work was supported by an unrestricted grant from "Fondazione Romeo ed Enrica Invernizzi" to Stefano Biffo and by AIRC under MFAG 2021 - ID. 26178 project - P.I. Manfrini Nicola.

Identifiants

pubmed: 36584595
pii: S2352-3964(22)00572-2
doi: 10.1016/j.ebiom.2022.104390
pmc: PMC9795807
pii:
doi:

Substances chimiques

Receptors, Virus 0
SLC1A5 protein, human 0
Minor Histocompatibility Antigens 0
Amino Acid Transport System ASC 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104390

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors report no conflict of interest.

Auteurs

Annarita Miluzio (A)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Alessandro Cuomo (A)

Department of Experimental Oncology, IEO, European Institute of Oncology IRCCS, 20141, Milan, Italy.

Chiara Cordiglieri (C)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Lorena Donnici (L)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Elisa Pesce (E)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Mauro Bombaci (M)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Matteo Conti (M)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Alessandra Fasciani (A)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Luigi Terracciano (L)

Institute of Pathology, University Hospital Basel, 4031, Basel, Switzerland.

Lara Manganaro (L)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Mirco Toccafondi (M)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Alessandra Scagliola (A)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Stefania Oliveto (S)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Sara Ricciardi (S)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy; Department of Biosciences, University of Milan, 20133, Milan, Italy.

Renata Grifantini (R)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy.

Raffaele De Francesco (R)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy; Department of Pharmacological and Biomolecular Sciences, University of Milan, 20133, Milan, Italy.

Sergio Abrignani (S)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy; Department of Clinical Sciences and Community Health, University of Milan, 20122, Milan, Italy.

Nicola Manfrini (N)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy; Department of Biosciences, University of Milan, 20133, Milan, Italy. Electronic address: manfrini@ingm.org.

Stefano Biffo (S)

National Institute of Molecular Genetics, "Fondazione Romeo ed Enrica Invernizzi", INGM, 20122, Milan, Italy; Department of Biosciences, University of Milan, 20133, Milan, Italy. Electronic address: biffo@ingm.org.

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Classifications MeSH