The IRE1α-XBP1 arm of the unfolded protein response is a host factor activated in SARS-CoV-2 infection

SARS-CoV-2 infection can cause severe pneumonia, wherein exacerbated inflammation plays a major role. This is reminiscent of the process commonly termed cytokine storm, a condition dependent on a disproportionated production of cytokines. This state involves the activation of the innate immune respo...

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Published inBiochimica et biophysica acta. Molecular basis of disease Vol. 1870; no. 5; p. 167193
Main Authors Fernández, Jose Javier, Marín, Arturo, Rosales, Romel, Penrice-Randal, Rebekah, Mlcochova, Petra, Alvarez, Yolanda, Villalón-Letelier, Fernando, Yildiz, Soner, Pérez, Enrique, Rathnasinghe, Raveen, Cupic, Anastasija, Kehrer, Thomas, Uccellini, Melissa B., Alonso, Sara, Martínez, Fernando, McGovern, Briana Lynn, Clark, Jordan J., Sharma, Parul, Bayón, Yolanda, Alonso, Andrés, Albrecht, Randy A., White, Kris M., Schotsaert, Michael, Miorin, Lisa, Stewart, James P., Hiscox, Julian A., Gupta, Ravindra K., Irigoyen, Nerea, García-Sastre, Adolfo, Crespo, Mariano Sánchez, Fernández, Nieves
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 01.06.2024
Subjects
Animals
COVID-19
COVID-19 - immunology
COVID-19 - metabolism
COVID-19 - pathology
COVID-19 - virology
Cytokines
Cytokines - metabolism
Endoribonucleases - genetics
Endoribonucleases - metabolism
Female
Fluvoxamine
Humans
Mesocricetus
Mice
Mice, Inbred C57BL
Pneumonia
Protein Serine-Threonine Kinases - genetics
Protein Serine-Threonine Kinases - metabolism
SARS-CoV-2 - metabolism
Signal Transduction
TLR
Transcription factors
Unfolded Protein Response
Variants of concern
Viral sepsis
Virus Replication
X-Box Binding Protein 1 - genetics
X-Box Binding Protein 1 - metabolism
COVID-19
Viral sepsis
Pneumonia
Transcription factors
Cytokines
Variants of concern
TLR
Fluvoxamine
Unfolded protein response
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Abstract SARS-CoV-2 infection can cause severe pneumonia, wherein exacerbated inflammation plays a major role. This is reminiscent of the process commonly termed cytokine storm, a condition dependent on a disproportionated production of cytokines. This state involves the activation of the innate immune response by viral patterns and coincides with the biosynthesis of the biomass required for viral replication, which may overwhelm the capacity of the endoplasmic reticulum and drive the unfolded protein response (UPR). The UPR is a signal transduction pathway composed of three branches that is initiated by a set of sensors: inositol-requiring protein 1 (IRE1), protein kinase RNA-like ER kinase (PERK), and activating transcription factor 6 (ATF6). These sensors control adaptive processes, including the transcriptional regulation of proinflammatory cytokines. Based on this background, the role of the UPR in SARS-CoV-2 replication and the ensuing inflammatory response was investigated using in vivo and in vitro models of infection. Mice and Syrian hamsters infected with SARS-CoV-2 showed a sole activation of the Ire1α-Xbp1 arm of the UPR associated with a robust production of proinflammatory cytokines. Human lung epithelial cells showed the dependence of viral replication on the expression of UPR-target proteins branching on the IRE1α-XBP1 arm and to a lower extent on the PERK route. Likewise, activation of the IRE1α-XBP1 branch by Spike (S) proteins from different variants of concern was a uniform finding. These results show that the IRE1α-XBP1 system enhances viral replication and cytokine expression and may represent a potential therapeutic target in SARS-CoV-2 severe pneumonia. [Display omitted] •SARS-CoV-2 infection of mice and Syrian hamsters activates the Ire1α-Xbp1 arm of UPR.•Ire1α-Xbp1 arm activity is associated with proinflammatory cytokine production.•SARS-CoV-2 leverages the Ire1α-Xbp1 arm for replication in lung epithelial cells.•The IRE1α-XBP1 arm is activated by Spike proteins from different variants of concern.
AbstractList SARS-CoV-2 infection can cause severe pneumonia, wherein exacerbated inflammation plays a major role. This is reminiscent of the process commonly termed cytokine storm, a condition dependent on a disproportionated production of cytokines. This state involves the activation of the innate immune response by viral patterns and coincides with the biosynthesis of the biomass required for viral replication, which may overwhelm the capacity of the endoplasmic reticulum and drive the unfolded protein response (UPR). The UPR is a signal transduction pathway composed of three branches that is initiated by a set of sensors: inositol-requiring protein 1 (IRE1), protein kinase RNA-like ER kinase (PERK), and activating transcription factor 6 (ATF6). These sensors control adaptive processes, including the transcriptional regulation of proinflammatory cytokines. Based on this background, the role of the UPR in SARS-CoV-2 replication and the ensuing inflammatory response was investigated using in vivo and in vitro models of infection. Mice and Syrian hamsters infected with SARS-CoV-2 showed a sole activation of the Ire1α-Xbp1 arm of the UPR associated with a robust production of proinflammatory cytokines. Human lung epithelial cells showed the dependence of viral replication on the expression of UPR-target proteins branching on the IRE1α-XBP1 arm and to a lower extent on the PERK route. Likewise, activation of the IRE1α-XBP1 branch by Spike (S) proteins from different variants of concern was a uniform finding. These results show that the IRE1α-XBP1 system enhances viral replication and cytokine expression and may represent a potential therapeutic target in SARS-CoV-2 severe pneumonia. [Display omitted] •SARS-CoV-2 infection of mice and Syrian hamsters activates the Ire1α-Xbp1 arm of UPR.•Ire1α-Xbp1 arm activity is associated with proinflammatory cytokine production.•SARS-CoV-2 leverages the Ire1α-Xbp1 arm for replication in lung epithelial cells.•The IRE1α-XBP1 arm is activated by Spike proteins from different variants of concern.
SARS-CoV-2 infection can cause severe pneumonia, wherein exacerbated inflammation plays a major role. This is reminiscent of the process commonly termed cytokine storm, a condition dependent on a disproportionated production of cytokines. This state involves the activation of the innate immune response by viral patterns and coincides with the biosynthesis of the biomass required for viral replication, which may overwhelm the capacity of the endoplasmic reticulum and drive the unfolded protein response (UPR). The UPR is a signal transduction pathway composed of three branches that is initiated by a set of sensors: inositol-requiring protein 1 (IRE1), protein kinase RNA-like ER kinase (PERK), and activating transcription factor 6 (ATF6). These sensors control adaptive processes, including the transcriptional regulation of proinflammatory cytokines. Based on this background, the role of the UPR in SARS-CoV-2 replication and the ensuing inflammatory response was investigated using in vivo and in vitro models of infection. Mice and Syrian hamsters infected with SARS-CoV-2 showed a sole activation of the Ire1α-Xbp1 arm of the UPR associated with a robust production of proinflammatory cytokines. Human lung epithelial cells showed the dependence of viral replication on the expression of UPR-target proteins branching on the IRE1α-XBP1 arm and to a lower extent on the PERK route. Likewise, activation of the IRE1α-XBP1 branch by Spike (S) proteins from different variants of concern was a uniform finding. These results show that the IRE1α-XBP1 system enhances viral replication and cytokine expression and may represent a potential therapeutic target in SARS-CoV-2 severe pneumonia.SARS-CoV-2 infection can cause severe pneumonia, wherein exacerbated inflammation plays a major role. This is reminiscent of the process commonly termed cytokine storm, a condition dependent on a disproportionated production of cytokines. This state involves the activation of the innate immune response by viral patterns and coincides with the biosynthesis of the biomass required for viral replication, which may overwhelm the capacity of the endoplasmic reticulum and drive the unfolded protein response (UPR). The UPR is a signal transduction pathway composed of three branches that is initiated by a set of sensors: inositol-requiring protein 1 (IRE1), protein kinase RNA-like ER kinase (PERK), and activating transcription factor 6 (ATF6). These sensors control adaptive processes, including the transcriptional regulation of proinflammatory cytokines. Based on this background, the role of the UPR in SARS-CoV-2 replication and the ensuing inflammatory response was investigated using in vivo and in vitro models of infection. Mice and Syrian hamsters infected with SARS-CoV-2 showed a sole activation of the Ire1α-Xbp1 arm of the UPR associated with a robust production of proinflammatory cytokines. Human lung epithelial cells showed the dependence of viral replication on the expression of UPR-target proteins branching on the IRE1α-XBP1 arm and to a lower extent on the PERK route. Likewise, activation of the IRE1α-XBP1 branch by Spike (S) proteins from different variants of concern was a uniform finding. These results show that the IRE1α-XBP1 system enhances viral replication and cytokine expression and may represent a potential therapeutic target in SARS-CoV-2 severe pneumonia.
SARS-CoV-2 infection can cause severe pneumonia, wherein exacerbated inflammation plays a major role. This is reminiscent of the process commonly termed cytokine storm, a condition dependent on a disproportionated production of cytokines. This state involves the activation of the innate immune response by viral patterns and coincides with the biosynthesis of the biomass required for viral replication, which may overwhelm the capacity of the endoplasmic reticulum and drive the unfolded protein response (UPR). The UPR is a signal transduction pathway composed of three branches that is initiated by a set of sensors: inositol-requiring protein 1 (IRE1), protein kinase RNA-like ER kinase (PERK), and activating transcription factor 6 (ATF6). These sensors control adaptive processes, including the transcriptional regulation of proinflammatory cytokines. Based on this background, the role of the UPR in SARS-CoV-2 replication and the ensuing inflammatory response was investigated using in vivo and in vitro models of infection. Mice and Syrian hamsters infected with SARS-CoV-2 showed a sole activation of the Ire1α-Xbp1 arm of the UPR associated with a robust production of proinflammatory cytokines. Human lung epithelial cells showed the dependence of viral replication on the expression of UPR-target proteins branching on the IRE1α-XBP1 arm and to a lower extent on the PERK route. Likewise, activation of the IRE1α-XBP1 branch by Spike (S) proteins from different variants of concern was a uniform finding. These results show that the IRE1α-XBP1 system enhances viral replication and cytokine expression and may represent a potential therapeutic target in SARS-CoV-2 severe pneumonia.
ArticleNumber 167193
Author García-Sastre, Adolfo
White, Kris M.
Uccellini, Melissa B.
Alonso, Sara
Clark, Jordan J.
Fernández, Nieves
Crespo, Mariano Sánchez
Rathnasinghe, Raveen
Cupic, Anastasija
Sharma, Parul
Alonso, Andrés
Alvarez, Yolanda
Pérez, Enrique
Fernández, Jose Javier
Yildiz, Soner
Bayón, Yolanda
Gupta, Ravindra K.
Hiscox, Julian A.
Rosales, Romel
McGovern, Briana Lynn
Albrecht, Randy A.
Stewart, James P.
Penrice-Randal, Rebekah
Kehrer, Thomas
Mlcochova, Petra
Villalón-Letelier, Fernando
Miorin, Lisa
Marín, Arturo
Schotsaert, Michael
Irigoyen, Nerea
Martínez, Fernando
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Issue 5
Keywords COVID-19
Viral sepsis
Pneumonia
Transcription factors
Cytokines
Variants of concern
TLR
Fluvoxamine
Unfolded protein response
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elsevier_sciencedirect_doi_10_1016_j_bbadis_2024_167193
PublicationCentury 2000
PublicationDate June 2024
2024-Jun
2024-06-00
20240601
PublicationDateYYYYMMDD 2024-06-01
PublicationDate_xml – month: 06
  year: 2024
  text: June 2024
PublicationDecade 2020
PublicationPlace Netherlands
PublicationPlace_xml – name: Netherlands
PublicationTitle Biochimica et biophysica acta. Molecular basis of disease
PublicationTitleAlternate Biochim Biophys Acta Mol Basis Dis
PublicationYear 2024
Publisher Elsevier B.V
Publisher_xml – name: Elsevier B.V
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Snippet SARS-CoV-2 infection can cause severe pneumonia, wherein exacerbated inflammation plays a major role. This is reminiscent of the process commonly termed...
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SubjectTerms Animals
COVID-19
COVID-19 - immunology
COVID-19 - metabolism
COVID-19 - pathology
COVID-19 - virology
Cytokines
Cytokines - metabolism
Endoribonucleases - genetics
Endoribonucleases - metabolism
Female
Fluvoxamine
Humans
Mesocricetus
Mice
Mice, Inbred C57BL
Pneumonia
Protein Serine-Threonine Kinases - genetics
Protein Serine-Threonine Kinases - metabolism
SARS-CoV-2 - metabolism
Signal Transduction
TLR
Transcription factors
Unfolded Protein Response
Variants of concern
Viral sepsis
Virus Replication
X-Box Binding Protein 1 - genetics
X-Box Binding Protein 1 - metabolism
Title The IRE1α-XBP1 arm of the unfolded protein response is a host factor activated in SARS-CoV-2 infection
URI https://dx.doi.org/10.1016/j.bbadis.2024.167193
https://www.ncbi.nlm.nih.gov/pubmed/38648902
https://www.proquest.com/docview/3045115834
Volume 1870
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