A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate

Here, we report the engineering of a Bioluminescence Resonance Energy Transfer (BRET)-based SARS-CoV-2 main protease (Mpro) biosensor containing the Mpro N-terminal autocleavage sequence in tandem and a nanobody that shows an enhanced rate of Mpro-mediated proteolytic cleavage. Specifically, we desi...

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Main Author: Geethakumari, Anupriya M (author)
Other Authors: Sultana, Asfia (author), Fatima, Asma (author), Uddin, S M Nasir (author), Abdulhakim, Somaiya (author), Mohamed, Amera (author), Rahman, Samiha (author), Al-Buainain, Khaloud (author), Yassine, Hadi M (author), Khatib, Hebah A Al (author), Biswas, Kabir H (author)
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Published: 2025
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Online Access:http://dx.doi.org/10.1016/j.snr.2025.100315
https://www.sciencedirect.com/science/article/pii/S2666053925000335
http://hdl.handle.net/10576/65127
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author Geethakumari, Anupriya M
author2 Sultana, Asfia
Fatima, Asma
Uddin, S M Nasir
Abdulhakim, Somaiya
Mohamed, Amera
Rahman, Samiha
Al-Buainain, Khaloud
Yassine, Hadi M
Khatib, Hebah A Al
Biswas, Kabir H
author2_role author
author
author
author
author
author
author
author
author
author
author_facet Geethakumari, Anupriya M
Sultana, Asfia
Fatima, Asma
Uddin, S M Nasir
Abdulhakim, Somaiya
Mohamed, Amera
Rahman, Samiha
Al-Buainain, Khaloud
Yassine, Hadi M
Khatib, Hebah A Al
Biswas, Kabir H
author_role author
dc.creator.none.fl_str_mv Geethakumari, Anupriya M
Sultana, Asfia
Fatima, Asma
Uddin, S M Nasir
Abdulhakim, Somaiya
Mohamed, Amera
Rahman, Samiha
Al-Buainain, Khaloud
Yassine, Hadi M
Khatib, Hebah A Al
Biswas, Kabir H
dc.date.none.fl_str_mv 2025-05-22T09:57:08Z
2025-06-30
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://dx.doi.org/10.1016/j.snr.2025.100315
26660539
https://www.sciencedirect.com/science/article/pii/S2666053925000335
http://hdl.handle.net/10576/65127
9
dc.language.none.fl_str_mv en
dc.publisher.none.fl_str_mv Elsevier
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biosensor
BRET
Molecular dynamics simulation
Mpro
Nanobody
SARS-CoV-2
dc.title.none.fl_str_mv A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
dc.type.none.fl_str_mv Article
info:eu-repo/semantics/publishedVersion
info:eu-repo/semantics/article
description Here, we report the engineering of a Bioluminescence Resonance Energy Transfer (BRET)-based SARS-CoV-2 main protease (Mpro) biosensor containing the Mpro N-terminal autocleavage sequence in tandem and a nanobody that shows an enhanced rate of Mpro-mediated proteolytic cleavage. Specifically, we designed Mpro biosensors containing 2×, 4× and 8× repeats of Mpro N-terminal autocleavage sequences and a combination of Mpro cleavage sequences containing a total of 12 cleavage sites sandwiched between mNeonGreen (mNG) and NanoLuc (NLuc). Gaussian accelerated molecular dynamics (GaMD) simulations of the predicted alpha-helical synthetic Mpro cleavage sequences revealed a dynamic nature of the cleavage sequences, which is critical for their efficient cleavage, and a relatively short end-to-end distances, which is required for high BRET. Live cell assays revealed a cleavage sequence length-dependent resonance energy transfer, except for the 12× -syn cleavage site, and an increased rate of cleavage and a decreased pharmacological inhibitor efficacy for the Mpro biosensor containing 2× cleavage sequences. Further, mutational analysis revealed a requirement for both cleavage sites to be intact for increased cleavage rate. Importantly, the inclusion of an Mpro-binding, but non-inhibiting, NB2E3 nanobody at the N-terminal further increased the cleavage rate of the 2× cleavage sequence-containing Mpro biosensor. We envisage that the NB2E3 nanobody-2× Mpro biosensor engineered here will be useful in drug discovery and functional characterization of Mpro mutants in newly emerging SARS-CoV-2 variants as well as in detecting SARS-CoV-2 infection in a point-of-care testing (POCT) format.
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language_invalid_str_mv en
network_acronym_str qu
network_name_str Qatar University repository
oai_identifier_str oai:qspace.qu.edu.qa:10576/65127
publishDate 2025
publisher.none.fl_str_mv Elsevier
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rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
spelling A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rateGeethakumari, Anupriya MSultana, AsfiaFatima, AsmaUddin, S M NasirAbdulhakim, SomaiyaMohamed, AmeraRahman, SamihaAl-Buainain, KhaloudYassine, Hadi MKhatib, Hebah A AlBiswas, Kabir HBiosensorBRETMolecular dynamics simulationMproNanobodySARS-CoV-2Here, we report the engineering of a Bioluminescence Resonance Energy Transfer (BRET)-based SARS-CoV-2 main protease (Mpro) biosensor containing the Mpro N-terminal autocleavage sequence in tandem and a nanobody that shows an enhanced rate of Mpro-mediated proteolytic cleavage. Specifically, we designed Mpro biosensors containing 2×, 4× and 8× repeats of Mpro N-terminal autocleavage sequences and a combination of Mpro cleavage sequences containing a total of 12 cleavage sites sandwiched between mNeonGreen (mNG) and NanoLuc (NLuc). Gaussian accelerated molecular dynamics (GaMD) simulations of the predicted alpha-helical synthetic Mpro cleavage sequences revealed a dynamic nature of the cleavage sequences, which is critical for their efficient cleavage, and a relatively short end-to-end distances, which is required for high BRET. Live cell assays revealed a cleavage sequence length-dependent resonance energy transfer, except for the 12× -syn cleavage site, and an increased rate of cleavage and a decreased pharmacological inhibitor efficacy for the Mpro biosensor containing 2× cleavage sequences. Further, mutational analysis revealed a requirement for both cleavage sites to be intact for increased cleavage rate. Importantly, the inclusion of an Mpro-binding, but non-inhibiting, NB2E3 nanobody at the N-terminal further increased the cleavage rate of the 2× cleavage sequence-containing Mpro biosensor. We envisage that the NB2E3 nanobody-2× Mpro biosensor engineered here will be useful in drug discovery and functional characterization of Mpro mutants in newly emerging SARS-CoV-2 variants as well as in detecting SARS-CoV-2 infection in a point-of-care testing (POCT) format.This work is supported by the Undergraduate Research Experience Program (UREP) grant (# 28–264–3–092) awarded by the Qatar National Research Foundation (QNRF), Qatar Foundation and an internal funding from the College of Health & Life Sciences (CHLS), Hamad Bin Khalifa University (HBKU), a member of the Qatar Foundation. Some of the computational research work reported in the manuscript were performed using high-performance computer resources and services provided by the Research Computing group in Texas A&M University at Qatar. Research Computing is funded by the Qatar Foundation for Education, Science and Community Development (http://www.qf.org.qa). A.M.G. was supported by a postdoctoral fellowship from CHLS/HBKU. A.S., A.F., and S.M.N.U. were supported by scholarships from CHLS/HBKU.Elsevier2025-05-22T09:57:08Z2025-06-30Articleinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://dx.doi.org/10.1016/j.snr.2025.10031526660539https://www.sciencedirect.com/science/article/pii/S2666053925000335http://hdl.handle.net/10576/651279enhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:qspace.qu.edu.qa:10576/651272025-05-22T19:06:58Z
spellingShingle A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
Geethakumari, Anupriya M
Biosensor
BRET
Molecular dynamics simulation
Mpro
Nanobody
SARS-CoV-2
status_str publishedVersion
title A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
title_full A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
title_fullStr A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
title_full_unstemmed A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
title_short A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
title_sort A BRET-based Mpro biosensor containing a nanobody and tandem cleavage sites shows an increased cleavage rate
topic Biosensor
BRET
Molecular dynamics simulation
Mpro
Nanobody
SARS-CoV-2
url http://dx.doi.org/10.1016/j.snr.2025.100315
https://www.sciencedirect.com/science/article/pii/S2666053925000335
http://hdl.handle.net/10576/65127