Protease inhibitors targeting coronavirus and filovirus entry

•We identify vinylsulfones as lead candidate inhibitors of Ebola virus and SARS-CoV.•K11777 inhibited Ebola virus and SARS-CoV entry in the sub-nanomolar range.•Potent inhibition correlated with the presence of a basic piperazine ring at P3.•Serine protease inhibitor and K11777 blocked coronavirus e...

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Vydáno v:Antiviral research Ročník 116; s. 76 - 84
Hlavní autoři: Zhou, Yanchen, Vedantham, Punitha, Lu, Kai, Agudelo, Juliet, Carrion, Ricardo, Nunneley, Jerritt W., Barnard, Dale, Pöhlmann, Stefan, McKerrow, James H., Renslo, Adam R., Simmons, Graham
Médium: Journal Article
Jazyk:angličtina
Vydáno: Netherlands Elsevier B.V 01.04.2015
Published by Elsevier B.V
Témata:
ISSN:0166-3542, 1872-9096, 1872-9096
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Abstract •We identify vinylsulfones as lead candidate inhibitors of Ebola virus and SARS-CoV.•K11777 inhibited Ebola virus and SARS-CoV entry in the sub-nanomolar range.•Potent inhibition correlated with the presence of a basic piperazine ring at P3.•Serine protease inhibitor and K11777 blocked coronavirus entry into caco-2 cells.•Camostat protected 6 out of ten mice from lethal infection with SARS-CoV. In order to gain entry into cells, diverse viruses, including Ebola virus, SARS-coronavirus and the emerging MERS-coronavirus, depend on activation of their envelope glycoproteins by host cell proteases. The respective enzymes are thus excellent targets for antiviral intervention. In cell culture, activation of Ebola virus, as well as SARS- and MERS-coronavirus can be accomplished by the endosomal cysteine proteases, cathepsin L (CTSL) and cathepsin B (CTSB). In addition, SARS- and MERS-coronavirus can use serine proteases localized at the cell surface, for their activation. However, it is currently unclear which protease(s) facilitate viral spread in the infected host. We report here that the cysteine protease inhibitor K11777, ((2S)-N-[(1E,3S)-1-(benzenesulfonyl)-5-phenylpent-1-en-3-yl]-2-{[(E)-4-methylpiperazine-1-carbonyl]amino}-3-phenylpropanamide) and closely-related vinylsulfones act as broad-spectrum antivirals by targeting cathepsin-mediated cell entry. K11777 is already in advanced stages of development for a number of parasitic diseases, such as Chagas disease, and has proven to be safe and effective in a range of animal models. K11777 inhibition of SARS-CoV and Ebola virus entry was observed in the sub-nanomolar range. In order to assess whether cysteine or serine proteases promote viral spread in the host, we compared the antiviral activity of an optimized K11777-derivative with that of camostat, an inhibitor of TMPRSS2 and related serine proteases. Employing a pathogenic animal model of SARS-CoV infection, we demonstrated that viral spread and pathogenesis of SARS-CoV is driven by serine rather than cysteine proteases and can be effectively prevented by camostat. Camostat has been clinically used to treat chronic pancreatitis, and thus represents an exciting potential therapeutic for respiratory coronavirus infections. Our results indicate that camostat, or similar serine protease inhibitors, might be an effective option for treatment of SARS and potentially MERS, while vinyl sulfone-based inhibitors are excellent lead candidates for Ebola virus therapeutics.
AbstractList • We identify vinylsulfones as lead candidate inhibitors of Ebola virus and SARS-CoV. • K11777 inhibited Ebola virus and SARS-CoV entry in the sub-nanomolar range. • Potent inhibition correlated with the presence of a basic piperazine ring at P3. • Serine protease inhibitor and K11777 blocked coronavirus entry into caco-2 cells. • Camostat protected 6 out of ten mice from lethal infection with SARS-CoV. In order to gain entry into cells, diverse viruses, including Ebola virus, SARS-coronavirus and the emerging MERS-coronavirus, depend on activation of their envelope glycoproteins by host cell proteases. The respective enzymes are thus excellent targets for antiviral intervention. In cell culture, activation of Ebola virus, as well as SARS- and MERS-coronavirus can be accomplished by the endosomal cysteine proteases, cathepsin L (CTSL) and cathepsin B (CTSB). In addition, SARS- and MERS-coronavirus can use serine proteases localized at the cell surface, for their activation. However, it is currently unclear which protease(s) facilitate viral spread in the infected host. We report here that the cysteine protease inhibitor K11777, ((2S)-N-[(1E,3S)-1-(benzenesulfonyl)-5-phenylpent-1-en-3-yl]-2-{[(E)-4-methylpiperazine-1-carbonyl]amino}-3-phenylpropanamide) and closely-related vinylsulfones act as broad-spectrum antivirals by targeting cathepsin-mediated cell entry. K11777 is already in advanced stages of development for a number of parasitic diseases, such as Chagas disease, and has proven to be safe and effective in a range of animal models. K11777 inhibition of SARS-CoV and Ebola virus entry was observed in the sub-nanomolar range. In order to assess whether cysteine or serine proteases promote viral spread in the host, we compared the antiviral activity of an optimized K11777-derivative with that of camostat, an inhibitor of TMPRSS2 and related serine proteases. Employing a pathogenic animal model of SARS-CoV infection, we demonstrated that viral spread and pathogenesis of SARS-CoV is driven by serine rather than cysteine proteases and can be effectively prevented by camostat. Camostat has been clinically used to treat chronic pancreatitis, and thus represents an exciting potential therapeutic for respiratory coronavirus infections. Our results indicate that camostat, or similar serine protease inhibitors, might be an effective option for treatment of SARS and potentially MERS, while vinyl sulfone-based inhibitors are excellent lead candidates for Ebola virus therapeutics.
In order to gain entry into cells, diverse viruses, including Ebola virus, SARS-coronavirus and the emerging MERS-coronavirus, depend on activation of their envelope glycoproteins by host cell proteases. The respective enzymes are thus excellent targets for antiviral intervention. In cell culture, activation of Ebola virus, as well as SARS- and MERS-coronavirus can be accomplished by the endosomal cysteine proteases, cathepsin L (CTSL) and cathepsin B (CTSB). In addition, SARS- and MERS-coronavirus can use serine proteases localized at the cell surface, for their activation. However, it is currently unclear which protease(s) facilitate viral spread in the infected host. We report here that the cysteine protease inhibitor K11777, ((2S)-N-[(1E,3S)-1-(benzenesulfonyl)-5-phenylpent-1-en-3-yl]-2-{[( E )-4-methylpiperazine-1-carbonyl]amino}-3-phenylpropanamide) and closely-related vinylsulfones act as broad-spectrum antivirals by targeting cathepsin-mediated cell entry. K11777 is already in advanced stages of development for a number of parasitic diseases, such as Chagas disease, and has proven to be safe and effective in a range of animal models. K11777 inhibition of SARS-CoV and Ebola virus entry was observed in the sub-nanomolar range. In order to assess whether cysteine or serine proteases promote viral spread in the host, we compared the antiviral activity of an optimized K11777-derivative with that of camostat, an inhibitor of TMPRSS2 and related serine proteases. Employing a pathogenic animal model of SARS-CoV infection, we demonstrated that viral spread and pathogenesis of SARS-CoV is driven by serine rather than cysteine proteases and can be effectively prevented by camostat. Camostat has been clinically used to treat chronic pancreatitis, and thus represents an exciting potential therapeutic for respiratory coronavirus infections. Our results indicate that camostat, or similar serine protease inhibitors, might be an effective option for treatment of SARS and potentially MERS, while vinyl sulfone-based inhibitors are excellent lead candidates for Ebola virus therapeutics.
In order to gain entry into cells, diverse viruses, including Ebola virus, SARS-coronavirus and the emerging MERS-coronavirus, depend on activation of their envelope glycoproteins by host cell proteases. The respective enzymes are thus excellent targets for antiviral intervention. In cell culture, activation of Ebola virus, as well as SARS- and MERS-coronavirus can be accomplished by the endosomal cysteine proteases, cathepsin L (CTSL) and cathepsin B (CTSB). In addition, SARS- and MERS-coronavirus can use serine proteases localized at the cell surface, for their activation. However, it is currently unclear which protease(s) facilitate viral spread in the infected host. We report here that the cysteine protease inhibitor K11777, ((2S)-N-[(1E,3S)-1-(benzenesulfonyl)-5-phenylpent-1-en-3-yl]-2-{[(E)-4-methylpiperazine-1-carbonyl]amino}-3-phenylpropanamide) and closely-related vinylsulfones act as broad-spectrum antivirals by targeting cathepsin-mediated cell entry. K11777 is already in advanced stages of development for a number of parasitic diseases, such as Chagas disease, and has proven to be safe and effective in a range of animal models. K11777 inhibition of SARS-CoV and Ebola virus entry was observed in the sub-nanomolar range. In order to assess whether cysteine or serine proteases promote viral spread in the host, we compared the antiviral activity of an optimized K11777-derivative with that of camostat, an inhibitor of TMPRSS2 and related serine proteases. Employing a pathogenic animal model of SARS-CoV infection, we demonstrated that viral spread and pathogenesis of SARS-CoV is driven by serine rather than cysteine proteases and can be effectively prevented by camostat. Camostat has been clinically used to treat chronic pancreatitis, and thus represents an exciting potential therapeutic for respiratory coronavirus infections. Our results indicate that camostat, or similar serine protease inhibitors, might be an effective option for treatment of SARS and potentially MERS, while vinyl sulfone-based inhibitors are excellent lead candidates for Ebola virus therapeutics.In order to gain entry into cells, diverse viruses, including Ebola virus, SARS-coronavirus and the emerging MERS-coronavirus, depend on activation of their envelope glycoproteins by host cell proteases. The respective enzymes are thus excellent targets for antiviral intervention. In cell culture, activation of Ebola virus, as well as SARS- and MERS-coronavirus can be accomplished by the endosomal cysteine proteases, cathepsin L (CTSL) and cathepsin B (CTSB). In addition, SARS- and MERS-coronavirus can use serine proteases localized at the cell surface, for their activation. However, it is currently unclear which protease(s) facilitate viral spread in the infected host. We report here that the cysteine protease inhibitor K11777, ((2S)-N-[(1E,3S)-1-(benzenesulfonyl)-5-phenylpent-1-en-3-yl]-2-{[(E)-4-methylpiperazine-1-carbonyl]amino}-3-phenylpropanamide) and closely-related vinylsulfones act as broad-spectrum antivirals by targeting cathepsin-mediated cell entry. K11777 is already in advanced stages of development for a number of parasitic diseases, such as Chagas disease, and has proven to be safe and effective in a range of animal models. K11777 inhibition of SARS-CoV and Ebola virus entry was observed in the sub-nanomolar range. In order to assess whether cysteine or serine proteases promote viral spread in the host, we compared the antiviral activity of an optimized K11777-derivative with that of camostat, an inhibitor of TMPRSS2 and related serine proteases. Employing a pathogenic animal model of SARS-CoV infection, we demonstrated that viral spread and pathogenesis of SARS-CoV is driven by serine rather than cysteine proteases and can be effectively prevented by camostat. Camostat has been clinically used to treat chronic pancreatitis, and thus represents an exciting potential therapeutic for respiratory coronavirus infections. Our results indicate that camostat, or similar serine protease inhibitors, might be an effective option for treatment of SARS and potentially MERS, while vinyl sulfone-based inhibitors are excellent lead candidates for Ebola virus therapeutics.
•We identify vinylsulfones as lead candidate inhibitors of Ebola virus and SARS-CoV.•K11777 inhibited Ebola virus and SARS-CoV entry in the sub-nanomolar range.•Potent inhibition correlated with the presence of a basic piperazine ring at P3.•Serine protease inhibitor and K11777 blocked coronavirus entry into caco-2 cells.•Camostat protected 6 out of ten mice from lethal infection with SARS-CoV. In order to gain entry into cells, diverse viruses, including Ebola virus, SARS-coronavirus and the emerging MERS-coronavirus, depend on activation of their envelope glycoproteins by host cell proteases. The respective enzymes are thus excellent targets for antiviral intervention. In cell culture, activation of Ebola virus, as well as SARS- and MERS-coronavirus can be accomplished by the endosomal cysteine proteases, cathepsin L (CTSL) and cathepsin B (CTSB). In addition, SARS- and MERS-coronavirus can use serine proteases localized at the cell surface, for their activation. However, it is currently unclear which protease(s) facilitate viral spread in the infected host. We report here that the cysteine protease inhibitor K11777, ((2S)-N-[(1E,3S)-1-(benzenesulfonyl)-5-phenylpent-1-en-3-yl]-2-{[(E)-4-methylpiperazine-1-carbonyl]amino}-3-phenylpropanamide) and closely-related vinylsulfones act as broad-spectrum antivirals by targeting cathepsin-mediated cell entry. K11777 is already in advanced stages of development for a number of parasitic diseases, such as Chagas disease, and has proven to be safe and effective in a range of animal models. K11777 inhibition of SARS-CoV and Ebola virus entry was observed in the sub-nanomolar range. In order to assess whether cysteine or serine proteases promote viral spread in the host, we compared the antiviral activity of an optimized K11777-derivative with that of camostat, an inhibitor of TMPRSS2 and related serine proteases. Employing a pathogenic animal model of SARS-CoV infection, we demonstrated that viral spread and pathogenesis of SARS-CoV is driven by serine rather than cysteine proteases and can be effectively prevented by camostat. Camostat has been clinically used to treat chronic pancreatitis, and thus represents an exciting potential therapeutic for respiratory coronavirus infections. Our results indicate that camostat, or similar serine protease inhibitors, might be an effective option for treatment of SARS and potentially MERS, while vinyl sulfone-based inhibitors are excellent lead candidates for Ebola virus therapeutics.
Author Simmons, Graham
Zhou, Yanchen
McKerrow, James H.
Lu, Kai
Barnard, Dale
Carrion, Ricardo
Vedantham, Punitha
Agudelo, Juliet
Nunneley, Jerritt W.
Pöhlmann, Stefan
Renslo, Adam R.
AuthorAffiliation b Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA 94118, USA
a Blood Systems Research Institute, San Francisco, CA 94118, USA
d Texas Biomedical Research Institute, San Antonio, TX 78227, USA
g Department of Pathology and Center for Discovery and Innovation in Parasitic Diseases, University of California, San Francisco, San Francisco, CA 94158, USA
e Institute for Antiviral Research, Department of Animal, Dairy and Veterinary Science, Utah State University, Logan, UT 84322, USA
c Small Molecule Discovery Center and Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA
f Infection Biology Unit, German Primate Center, 37077 Göttingen, Germany
AuthorAffiliation_xml – name: g Department of Pathology and Center for Discovery and Innovation in Parasitic Diseases, University of California, San Francisco, San Francisco, CA 94158, USA
– name: a Blood Systems Research Institute, San Francisco, CA 94118, USA
– name: b Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA 94118, USA
– name: c Small Molecule Discovery Center and Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA
– name: f Infection Biology Unit, German Primate Center, 37077 Göttingen, Germany
– name: d Texas Biomedical Research Institute, San Antonio, TX 78227, USA
– name: e Institute for Antiviral Research, Department of Animal, Dairy and Veterinary Science, Utah State University, Logan, UT 84322, USA
Author_xml – sequence: 1
  givenname: Yanchen
  surname: Zhou
  fullname: Zhou, Yanchen
  organization: Blood Systems Research Institute, San Francisco, CA 94118, USA
– sequence: 2
  givenname: Punitha
  surname: Vedantham
  fullname: Vedantham, Punitha
  organization: Small Molecule Discovery Center and Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA
– sequence: 3
  givenname: Kai
  surname: Lu
  fullname: Lu, Kai
  organization: Blood Systems Research Institute, San Francisco, CA 94118, USA
– sequence: 4
  givenname: Juliet
  surname: Agudelo
  fullname: Agudelo, Juliet
  organization: Blood Systems Research Institute, San Francisco, CA 94118, USA
– sequence: 5
  givenname: Ricardo
  surname: Carrion
  fullname: Carrion, Ricardo
  organization: Texas Biomedical Research Institute, San Antonio, TX 78227, USA
– sequence: 6
  givenname: Jerritt W.
  surname: Nunneley
  fullname: Nunneley, Jerritt W.
  organization: Texas Biomedical Research Institute, San Antonio, TX 78227, USA
– sequence: 7
  givenname: Dale
  surname: Barnard
  fullname: Barnard, Dale
  organization: Institute for Antiviral Research, Department of Animal, Dairy and Veterinary Science, Utah State University, Logan, UT 84322, USA
– sequence: 8
  givenname: Stefan
  surname: Pöhlmann
  fullname: Pöhlmann, Stefan
  organization: Infection Biology Unit, German Primate Center, 37077 Göttingen, Germany
– sequence: 9
  givenname: James H.
  surname: McKerrow
  fullname: McKerrow, James H.
  organization: Department of Pathology and Center for Discovery and Innovation in Parasitic Diseases, University of California, San Francisco, San Francisco, CA 94158, USA
– sequence: 10
  givenname: Adam R.
  surname: Renslo
  fullname: Renslo, Adam R.
  organization: Small Molecule Discovery Center and Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA
– sequence: 11
  givenname: Graham
  surname: Simmons
  fullname: Simmons, Graham
  email: gsimmons@bloodsystems.org
  organization: Blood Systems Research Institute, San Francisco, CA 94118, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25666761$$D View this record in MEDLINE/PubMed
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Keywords Cathepsin
Coronavirus
Filovirus
Vinylsulfones
Language English
License Copyright © 2015. Published by Elsevier B.V.
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Snippet •We identify vinylsulfones as lead candidate inhibitors of Ebola virus and SARS-CoV.•K11777 inhibited Ebola virus and SARS-CoV entry in the sub-nanomolar...
In order to gain entry into cells, diverse viruses, including Ebola virus, SARS-coronavirus and the emerging MERS-coronavirus, depend on activation of their...
• We identify vinylsulfones as lead candidate inhibitors of Ebola virus and SARS-CoV. • K11777 inhibited Ebola virus and SARS-CoV entry in the sub-nanomolar...
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StartPage 76
SubjectTerms Animals
Antiviral Agents - pharmacology
Cathepsin
Cathepsins - metabolism
Cell Line, Tumor
Coronavirus
Coronavirus - drug effects
Coronavirus - physiology
Coronavirus Infections - drug therapy
Dipeptides - pharmacology
Ebola virus
Ebolavirus - drug effects
Ebolavirus - physiology
Filoviridae - drug effects
Filoviridae - physiology
Filovirus
Gabexate - analogs & derivatives
Gabexate - pharmacology
Humans
Mice
Mice, Inbred BALB C
Protease Inhibitors - pharmacology
SARS coronavirus
SARS Virus - drug effects
SARS Virus - physiology
Serine Endopeptidases - metabolism
Serine Proteinase Inhibitors - pharmacology
Vinyl Compounds - pharmacology
Vinylsulfones
Virus Internalization - drug effects
Title Protease inhibitors targeting coronavirus and filovirus entry
URI https://dx.doi.org/10.1016/j.antiviral.2015.01.011
https://www.ncbi.nlm.nih.gov/pubmed/25666761
https://www.proquest.com/docview/1662638541
https://www.proquest.com/docview/1732831823
https://pubmed.ncbi.nlm.nih.gov/PMC4774534
Volume 116
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