Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations

Research output: Contribution to journalJournal articleResearchpeer-review

Standard

Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations. / Tree, Julia A.; Turnbull, Jeremy E.; Buttigieg, Karen R.; Elmore, Michael J.; Coombes, Naomi; Hogwood, John; Mycroft-West, Courtney J.; Lima, Marcelo A.; Skidmore, Mark A.; Karlsson, Richard; Chen, Yen Hsi; Yang, Zhang; Spalluto, Cosma Mirella; Staples, Karl J.; Yates, Edwin A.; Gray, Elaine; Singh, Dave; Wilkinson, Tom; Page, Clive P.; Carroll, Miles W.

In: British Journal of Pharmacology, Vol. 178, No. 3, 2021, p. 626-635.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Tree, JA, Turnbull, JE, Buttigieg, KR, Elmore, MJ, Coombes, N, Hogwood, J, Mycroft-West, CJ, Lima, MA, Skidmore, MA, Karlsson, R, Chen, YH, Yang, Z, Spalluto, CM, Staples, KJ, Yates, EA, Gray, E, Singh, D, Wilkinson, T, Page, CP & Carroll, MW 2021, 'Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations', British Journal of Pharmacology, vol. 178, no. 3, pp. 626-635. https://doi.org/10.1111/bph.15304

APA

Tree, J. A., Turnbull, J. E., Buttigieg, K. R., Elmore, M. J., Coombes, N., Hogwood, J., Mycroft-West, C. J., Lima, M. A., Skidmore, M. A., Karlsson, R., Chen, Y. H., Yang, Z., Spalluto, C. M., Staples, K. J., Yates, E. A., Gray, E., Singh, D., Wilkinson, T., Page, C. P., & Carroll, M. W. (2021). Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations. British Journal of Pharmacology, 178(3), 626-635. https://doi.org/10.1111/bph.15304

Vancouver

Tree JA, Turnbull JE, Buttigieg KR, Elmore MJ, Coombes N, Hogwood J et al. Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations. British Journal of Pharmacology. 2021;178(3):626-635. https://doi.org/10.1111/bph.15304

Author

Tree, Julia A. ; Turnbull, Jeremy E. ; Buttigieg, Karen R. ; Elmore, Michael J. ; Coombes, Naomi ; Hogwood, John ; Mycroft-West, Courtney J. ; Lima, Marcelo A. ; Skidmore, Mark A. ; Karlsson, Richard ; Chen, Yen Hsi ; Yang, Zhang ; Spalluto, Cosma Mirella ; Staples, Karl J. ; Yates, Edwin A. ; Gray, Elaine ; Singh, Dave ; Wilkinson, Tom ; Page, Clive P. ; Carroll, Miles W. / Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations. In: British Journal of Pharmacology. 2021 ; Vol. 178, No. 3. pp. 626-635.

Bibtex

@article{2c6da736f2874518927b1688baff6e3c,
title = "Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations",
abstract = "Background and Purpose: Currently, there are no licensed vaccines and limited antivirals for the treatment of COVID-19. Heparin (delivered systemically) is currently used to treat anticoagulant anomalies in COVID-19 patients. Additionally, in the United Kingdom, Brazil and Australia, nebulised unfractionated heparin (UFH) is being trialled in COVID-19 patients as a potential treatment. A systematic comparison of the potential antiviral effect of various heparin preparations on live wild type SARS-CoV-2, in vitro, is needed. Experimental Approach: Seven different heparin preparations including UFH and low MW heparins (LMWH) of porcine or bovine origin were screened for antiviral activity against live SARS-CoV-2 (Australia/VIC01/2020) using a plaque inhibition assay with Vero E6 cells. Interaction of heparin with spike protein RBD was studied using differential scanning fluorimetry and the inhibition of RBD binding to human ACE2 protein using elisa assays was examined. Key Results: All the UFH preparations had potent antiviral effects, with IC50 values ranging between 25 and 41 μg·ml−1, whereas LMWHs were less inhibitory by ~150-fold (IC50 range 3.4–7.8 mg·ml−1). Mechanistically, we observed that heparin binds and destabilizes the RBD protein and furthermore, we show heparin directly inhibits the binding of RBD to the human ACE2 protein receptor. Conclusion and Implications: This comparison of clinically relevant heparins shows that UFH has significantly stronger SARS-CoV-2 antiviral activity compared to LMWHs. UFH acts to directly inhibit binding of spike protein to the human ACE2 protein receptor. Overall, the data strongly support further clinical investigation of UFH as a potential treatment for patients with COVID-19.",
keywords = "COVID-19, heparin, LMWH, nebulised, SARS-CoV-2, UFH",
author = "Tree, {Julia A.} and Turnbull, {Jeremy E.} and Buttigieg, {Karen R.} and Elmore, {Michael J.} and Naomi Coombes and John Hogwood and Mycroft-West, {Courtney J.} and Lima, {Marcelo A.} and Skidmore, {Mark A.} and Richard Karlsson and Chen, {Yen Hsi} and Zhang Yang and Spalluto, {Cosma Mirella} and Staples, {Karl J.} and Yates, {Edwin A.} and Elaine Gray and Dave Singh and Tom Wilkinson and Page, {Clive P.} and Carroll, {Miles W.}",
year = "2021",
doi = "10.1111/bph.15304",
language = "English",
volume = "178",
pages = "626--635",
journal = "British Journal of Pharmacology",
issn = "0007-1188",
publisher = "Wiley",
number = "3",

}

RIS

TY - JOUR

T1 - Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations

AU - Tree, Julia A.

AU - Turnbull, Jeremy E.

AU - Buttigieg, Karen R.

AU - Elmore, Michael J.

AU - Coombes, Naomi

AU - Hogwood, John

AU - Mycroft-West, Courtney J.

AU - Lima, Marcelo A.

AU - Skidmore, Mark A.

AU - Karlsson, Richard

AU - Chen, Yen Hsi

AU - Yang, Zhang

AU - Spalluto, Cosma Mirella

AU - Staples, Karl J.

AU - Yates, Edwin A.

AU - Gray, Elaine

AU - Singh, Dave

AU - Wilkinson, Tom

AU - Page, Clive P.

AU - Carroll, Miles W.

PY - 2021

Y1 - 2021

N2 - Background and Purpose: Currently, there are no licensed vaccines and limited antivirals for the treatment of COVID-19. Heparin (delivered systemically) is currently used to treat anticoagulant anomalies in COVID-19 patients. Additionally, in the United Kingdom, Brazil and Australia, nebulised unfractionated heparin (UFH) is being trialled in COVID-19 patients as a potential treatment. A systematic comparison of the potential antiviral effect of various heparin preparations on live wild type SARS-CoV-2, in vitro, is needed. Experimental Approach: Seven different heparin preparations including UFH and low MW heparins (LMWH) of porcine or bovine origin were screened for antiviral activity against live SARS-CoV-2 (Australia/VIC01/2020) using a plaque inhibition assay with Vero E6 cells. Interaction of heparin with spike protein RBD was studied using differential scanning fluorimetry and the inhibition of RBD binding to human ACE2 protein using elisa assays was examined. Key Results: All the UFH preparations had potent antiviral effects, with IC50 values ranging between 25 and 41 μg·ml−1, whereas LMWHs were less inhibitory by ~150-fold (IC50 range 3.4–7.8 mg·ml−1). Mechanistically, we observed that heparin binds and destabilizes the RBD protein and furthermore, we show heparin directly inhibits the binding of RBD to the human ACE2 protein receptor. Conclusion and Implications: This comparison of clinically relevant heparins shows that UFH has significantly stronger SARS-CoV-2 antiviral activity compared to LMWHs. UFH acts to directly inhibit binding of spike protein to the human ACE2 protein receptor. Overall, the data strongly support further clinical investigation of UFH as a potential treatment for patients with COVID-19.

AB - Background and Purpose: Currently, there are no licensed vaccines and limited antivirals for the treatment of COVID-19. Heparin (delivered systemically) is currently used to treat anticoagulant anomalies in COVID-19 patients. Additionally, in the United Kingdom, Brazil and Australia, nebulised unfractionated heparin (UFH) is being trialled in COVID-19 patients as a potential treatment. A systematic comparison of the potential antiviral effect of various heparin preparations on live wild type SARS-CoV-2, in vitro, is needed. Experimental Approach: Seven different heparin preparations including UFH and low MW heparins (LMWH) of porcine or bovine origin were screened for antiviral activity against live SARS-CoV-2 (Australia/VIC01/2020) using a plaque inhibition assay with Vero E6 cells. Interaction of heparin with spike protein RBD was studied using differential scanning fluorimetry and the inhibition of RBD binding to human ACE2 protein using elisa assays was examined. Key Results: All the UFH preparations had potent antiviral effects, with IC50 values ranging between 25 and 41 μg·ml−1, whereas LMWHs were less inhibitory by ~150-fold (IC50 range 3.4–7.8 mg·ml−1). Mechanistically, we observed that heparin binds and destabilizes the RBD protein and furthermore, we show heparin directly inhibits the binding of RBD to the human ACE2 protein receptor. Conclusion and Implications: This comparison of clinically relevant heparins shows that UFH has significantly stronger SARS-CoV-2 antiviral activity compared to LMWHs. UFH acts to directly inhibit binding of spike protein to the human ACE2 protein receptor. Overall, the data strongly support further clinical investigation of UFH as a potential treatment for patients with COVID-19.

KW - COVID-19

KW - heparin

KW - LMWH

KW - nebulised

KW - SARS-CoV-2

KW - UFH

U2 - 10.1111/bph.15304

DO - 10.1111/bph.15304

M3 - Journal article

C2 - 33125711

AN - SCOPUS:85096138013

VL - 178

SP - 626

EP - 635

JO - British Journal of Pharmacology

JF - British Journal of Pharmacology

SN - 0007-1188

IS - 3

ER -

ID: 256264301