Mechanisms of Severe Acute Respiratory Syndrome Coronavirus-Induced Acute Lung Injury
Abstract
Systems biology offers considerable promise in uncovering novel pathways by which viruses and other microbial pathogens interact with host signaling and expression networks to mediate disease severity. In this study, we have developed an unbiased modeling approach to identify new pathways and network connections mediating acute lung injury, using severe acute respiratory syndrome coronavirus (SARS-CoV) as a model pathogen. We utilized a time course of matched virologic, pathological, and transcriptomic data within a novel methodological framework that can detect pathway enrichment among key highly connected network genes. This unbiased approach produced a high-priority list of 4 genes in one pathway out of over 3,500 genes that were differentially expressed following SARS-CoV infection. With these data, we predicted that the urokinase and other wound repair pathways would regulate lethal versus sublethal disease following SARS-CoV infection in mice. We validated the importance of the urokinase pathway for SARS-CoV disease severity using genetically defined knockout mice, proteomic correlates of pathway activation, and pathological disease severity. The results of these studies demonstrate that a fine balance exists between host coagulation and fibrinolysin pathways regulating pathological disease outcomes, including diffuse alveolar damage and acute lung injury, following infection with highly pathogenic respiratory viruses, such asmore »
- Authors:
-
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- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Epidemiology
- Oregon Health Sciences Univ., Portland, OR (United States). Dept. of Medical Informatics and Clinical Epidemiology. Division of Bioinformatics and Computational Biology
- Univ. of Washington, Seattle, WA (United States). School of Medicine. Dept. of Microbiology
- Oregon Health Sciences Univ., Portland, OR (United States). Oregon Clinical and Translational Research Inst.
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Genetics
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Microbiology and Immunology
- Univ. of Washington, Seattle, WA (United States). School of Medicine. Dept. of Microbiology; Univ. of Washington, Seattle, WA (United States). Washington National Primate Research Center
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Microbiology and Immunology; Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Epidemiology
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1626096
- Grant/Contract Number:
- AC06-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 4; Journal Issue: 4; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology (ASM)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology
Citation Formats
Gralinski, Lisa E., Bankhead, Armand, Jeng, Sophia, Menachery, Vineet D., Proll, Sean, Belisle, Sarah E., Matzke, Melissa, Webb-Robertson, Bobbie-Jo M., Luna, Maria L., Shukla, Anil K., Ferris, Martin T., Bolles, Meagan, Chang, Jean, Aicher, Lauri, Waters, Katrina M., Smith, Richard D., Metz, Thomas O., Law, G. Lynn, Katze, Michael G., McWeeney, Shannon, and Baric, Ralph S. Mechanisms of Severe Acute Respiratory Syndrome Coronavirus-Induced Acute Lung Injury. United States: N. p., 2013.
Web. doi:10.1128/mbio.00271-13.
Gralinski, Lisa E., Bankhead, Armand, Jeng, Sophia, Menachery, Vineet D., Proll, Sean, Belisle, Sarah E., Matzke, Melissa, Webb-Robertson, Bobbie-Jo M., Luna, Maria L., Shukla, Anil K., Ferris, Martin T., Bolles, Meagan, Chang, Jean, Aicher, Lauri, Waters, Katrina M., Smith, Richard D., Metz, Thomas O., Law, G. Lynn, Katze, Michael G., McWeeney, Shannon, & Baric, Ralph S. Mechanisms of Severe Acute Respiratory Syndrome Coronavirus-Induced Acute Lung Injury. United States. https://doi.org/10.1128/mbio.00271-13
Gralinski, Lisa E., Bankhead, Armand, Jeng, Sophia, Menachery, Vineet D., Proll, Sean, Belisle, Sarah E., Matzke, Melissa, Webb-Robertson, Bobbie-Jo M., Luna, Maria L., Shukla, Anil K., Ferris, Martin T., Bolles, Meagan, Chang, Jean, Aicher, Lauri, Waters, Katrina M., Smith, Richard D., Metz, Thomas O., Law, G. Lynn, Katze, Michael G., McWeeney, Shannon, and Baric, Ralph S. Tue .
"Mechanisms of Severe Acute Respiratory Syndrome Coronavirus-Induced Acute Lung Injury". United States. https://doi.org/10.1128/mbio.00271-13. https://www.osti.gov/servlets/purl/1626096.
@article{osti_1626096,
title = {Mechanisms of Severe Acute Respiratory Syndrome Coronavirus-Induced Acute Lung Injury},
author = {Gralinski, Lisa E. and Bankhead, Armand and Jeng, Sophia and Menachery, Vineet D. and Proll, Sean and Belisle, Sarah E. and Matzke, Melissa and Webb-Robertson, Bobbie-Jo M. and Luna, Maria L. and Shukla, Anil K. and Ferris, Martin T. and Bolles, Meagan and Chang, Jean and Aicher, Lauri and Waters, Katrina M. and Smith, Richard D. and Metz, Thomas O. and Law, G. Lynn and Katze, Michael G. and McWeeney, Shannon and Baric, Ralph S.},
abstractNote = {Systems biology offers considerable promise in uncovering novel pathways by which viruses and other microbial pathogens interact with host signaling and expression networks to mediate disease severity. In this study, we have developed an unbiased modeling approach to identify new pathways and network connections mediating acute lung injury, using severe acute respiratory syndrome coronavirus (SARS-CoV) as a model pathogen. We utilized a time course of matched virologic, pathological, and transcriptomic data within a novel methodological framework that can detect pathway enrichment among key highly connected network genes. This unbiased approach produced a high-priority list of 4 genes in one pathway out of over 3,500 genes that were differentially expressed following SARS-CoV infection. With these data, we predicted that the urokinase and other wound repair pathways would regulate lethal versus sublethal disease following SARS-CoV infection in mice. We validated the importance of the urokinase pathway for SARS-CoV disease severity using genetically defined knockout mice, proteomic correlates of pathway activation, and pathological disease severity. The results of these studies demonstrate that a fine balance exists between host coagulation and fibrinolysin pathways regulating pathological disease outcomes, including diffuse alveolar damage and acute lung injury, following infection with highly pathogenic respiratory viruses, such as SARS-CoV.},
doi = {10.1128/mbio.00271-13},
journal = {mBio (Online)},
number = 4,
volume = 4,
place = {United States},
year = {Tue Aug 06 00:00:00 EDT 2013},
month = {Tue Aug 06 00:00:00 EDT 2013}
}
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- Proceedings of the American Thoracic Society, Vol. 3, Issue 4
Nonhomogeneous immunostaining of hyaline membranes in different manifestations of diffuse alveolar damage
journal, January 2006
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Synthetic Reconstruction of Zoonotic and Early Human Severe Acute Respiratory Syndrome Coronavirus Isolates That Produce Fatal Disease in Aged Mice
text, January 2007
- David, Kelvin,; Mark, Heise,; Amy, Sims,
- The University of North Carolina at Chapel Hill University Libraries
H5N1-Infected Cells in Lung with Diffuse Alveolar Damage in Exudative Phase from a Fatal Case in Vietnam
journal, March 2008
- Liem, Nguyen Thanh; Nakajima, Noriko; Phat, Le Phuc
- Japanese Journal of Infectious Diseases, Vol. 61, Issue 2
Works referencing / citing this record:
Sm017
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Severe Acute Respiratory Syndrome Coronaviruses with Mutations in the E Protein Are Attenuated and Promising Vaccine Candidates
journal, January 2015
- Regla-Nava, Jose A.; Nieto-Torres, Jose L.; Jimenez-Guardeño, Jose M.
- Journal of Virology, Vol. 89, Issue 7
Broad-spectrum antiviral GS-5734 inhibits both epidemic and zoonotic coronaviruses
journal, June 2017
- Sheahan, Timothy P.; Sims, Amy C.; Graham, Rachel L.
- Science Translational Medicine, Vol. 9, Issue 396
Scl011
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Infection with MERS-CoV Causes Lethal Pneumonia in the Common Marmoset
journal, August 2014
- Falzarano, Darryl; de Wit, Emmie; Feldmann, Friederike
- PLoS Pathogens, Vol. 10, Issue 8
Sm010
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm014
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm020
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia
journal, April 2020
- Arachchillage, Deepa R. J.; Laffan, Mike
- Journal of Thrombosis and Haemostasis, Vol. 18, Issue 5
Sm036
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm038
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm004
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Molecular pathology of emerging coronavirus infections
journal, December 2014
- Gralinski, Lisa E.; Baric, Ralph S.
- The Journal of Pathology, Vol. 235, Issue 2
MERS-CoV and H5N1 influenza virus antagonize antigen presentation by altering the epigenetic landscape
journal, January 2018
- Menachery, Vineet D.; Schäfer, Alexandra; Burnum-Johnson, Kristin E.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 5
Sm039
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Annotation of long non-coding RNAs expressed in Collaborative Cross founder mice in response to respiratory virus infection reveals a new class of interferon-stimulated transcripts
journal, June 2014
- Josset, Laurence; Tchitchek, Nicolas; Gralinski, Lisa E.
- RNA Biology, Vol. 11, Issue 7
Annotation of long non-coding RNAs expressed in Collaborative Cross founder mice in response to respiratory virus infection reveals a new class of interferon-stimulated transcripts
text, January 2014
- S., Baric, Ralph; J., Eisfeld, Amie; J., Thomas, Matthew
- The University of North Carolina at Chapel Hill University Libraries
Attenuation and Restoration of Severe Acute Respiratory Syndrome Coronavirus Mutant Lacking 2'-O-Methyltransferase Activity
journal, January 2014
- Menachery, V. D.; Yount, B. L.; Josset, L.
- Journal of Virology, Vol. 88, Issue 8
Sm008
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm028
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm033
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Pneumonia, Acute Respiratory Distress Syndrome and Early Immune-Modulator Therapy
preprint, November 2016
- Lee, Kyung-Yil
Sm005
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm001
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Molecular pathology of emerging coronavirus infections
text, January 2014
- Baric, Ralph S.; Gralinski, Lisa E.
- Wiley Online Library
Sm021
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Conditioned Medium of Human Adipose Mesenchymal Stem Cells Increases Wound Closure and Protects Human Astrocytes Following Scratch Assay In Vitro
journal, September 2017
- Baez-Jurado, Eliana; Hidalgo-Lanussa, Oscar; Guio-Vega, Gina
- Molecular Neurobiology, Vol. 55, Issue 6
Scl004
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Genome Wide Identification of SARS-CoV Susceptibility Loci Using the Collaborative Cross
text, January 2015
- Leonard, McMillan,; A., Churchill, Gary; R., Miller, Darla
- The University of North Carolina at Chapel Hill University Libraries
Sm013
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm019
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
New Metrics for Evaluating Viral Respiratory Pathogenesis
text, January 2015
- D., Menachery, Vineet; S., Baric, Ralph; T., Ferris, Martin
- The University of North Carolina at Chapel Hill University Libraries
Broad-spectrum antiviral GS-5734 inhibits both epidemic and zoonotic coronaviruses
text, January 2017
- Y., Feng, Joy; Yeojin, Park,; L., MacKman, Richard
- The University of North Carolina at Chapel Hill University Libraries
Sm029
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
A decade after SARS: strategies for controlling emerging coronaviruses
text, January 2013
- Graham, Rachel L.; Donaldson, Eric F.; Baric, Ralph S.
- Macmillan Publishers
Scl010
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm034
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm009
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
New Metrics for Evaluating Viral Respiratory Pathogenesis
journal, June 2015
- Menachery, Vineet D.; Gralinski, Lisa E.; Baric, Ralph S.
- PLOS ONE, Vol. 10, Issue 6
Combination Attenuation Offers Strategy for Live Attenuated Coronavirus Vaccines
journal, July 2018
- Menachery, Vineet D.; Gralinski, Lisa E.; Mitchell, Hugh D.
- Journal of Virology, Vol. 92, Issue 17
Allelic Variation in the Toll-Like Receptor Adaptor Protein Ticam2 Contributes to SARS-Coronavirus Pathogenesis in Mice
journal, June 2017
- Gralinski, Lisa E.; Menachery, Vineet D.; Morgan, Andrew P.
- G3 Genes|Genomes|Genetics, Vol. 7, Issue 6
A decade after SARS: strategies for controlling emerging coronaviruses
journal, November 2013
- Graham, Rachel L.; Donaldson, Eric F.; Baric, Ralph S.
- Nature Reviews Microbiology, Vol. 11, Issue 12
MERS-CoV and H5N1 influenza virus antagonize antigen presentation by altering the epigenetic landscape
text, January 2018
- M., Webb-Robertson, Bobbie-Jo; D., Nicora, Carrie; O., Metz, Thomas
- The University of North Carolina at Chapel Hill University Libraries
A comprehensive collection of systems biology data characterizing the host response to viral infection
journal, October 2014
- Aevermann, Brian D.; Pickett, Brett E.; Kumar, Sanjeev
- Scientific Data, Vol. 1, Issue 1
Sm018
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Sm031
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
The effect of inhibition of PP1 and TNFα signaling on pathogenesis of SARS coronavirus
journal, September 2016
- McDermott, Jason E.; Mitchell, Hugh D.; Gralinski, Lisa E.
- BMC Systems Biology, Vol. 10, Issue 1
Pneumonia, Acute Respiratory Distress Syndrome, and Early Immune-Modulator Therapy
journal, February 2017
- Lee, Kyung-Yil
- International Journal of Molecular Sciences, Vol. 18, Issue 2
Sm011
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Genome Wide Identification of SARS-CoV Susceptibility Loci Using the Collaborative Cross
journal, October 2015
- Gralinski, Lisa E.; Ferris, Martin T.; Aylor, David L.
- PLOS Genetics, Vol. 11, Issue 10
Coronavirus susceptibility to the antiviral remdesivir (GS-5734) is mediated by the viral polymerase and the proofreading exoribonuclease
text, January 2018
- R., Denison, Mark; Dustin, Siegel,; S., Ray, Adrian
- The University of North Carolina at Chapel Hill University Libraries
Sm007
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Attenuation and Restoration of Severe Acute Respiratory Syndrome Coronavirus Mutant Lacking 2'-O-Methyltransferase Activity
text, January 2014
- Agnihothram, Sudhakar; Katze, Michael G.; Josset, Laurence
- American Society for Microbiology
Sm015
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Combination Attenuation Offers Strategy for Live Attenuated Coronavirus Vaccines
text, January 2018
- T., McAnarney, Eileen; M., Waters, Katrina; E., Gralinski, Lisa
- The University of North Carolina at Chapel Hill University Libraries
Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia
journal, April 2020
- Tang, Ning; Li, Dengju; Wang, Xiong
- Journal of Thrombosis and Haemostasis, Vol. 18, Issue 4
Sm023
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Broad-spectrum coronavirus antiviral drug discovery
journal, February 2019
- Totura, Allison L.; Bavari, Sina
- Expert Opinion on Drug Discovery, Vol. 14, Issue 4
Sm035
dataset, January 2020
- Waters, Katrina; Anderson, Lindsey; McDermott, Jason
- Pacific Northwest National Laboratory 2; EMSL; PNNL
Molecular pathology of emerging coronavirus infections
journal, December 2014
- Gralinski, Lisa E.; Baric, Ralph S.
- The Journal of Pathology, Vol. 235, Issue 2
SARS-CoV-Encoded Small RNAs Contribute to Infection-Associated Lung Pathology
journal, March 2017
- Morales, Lucía; Oliveros, Juan Carlos; Fernandez-Delgado, Raúl
- Cell Host & Microbe, Vol. 21, Issue 3
Systems approaches to coronavirus pathogenesis
journal, June 2014
- Schäfer, Alexandra; Baric, Ralph S.; Ferris, Martin T.
- Current Opinion in Virology, Vol. 6
Systems analysis of West Nile virus infection
journal, June 2014
- Suthar, Mehul S.; Pulendran, Bali
- Current Opinion in Virology, Vol. 6
A decade after SARS: strategies for controlling emerging coronaviruses
journal, November 2013
- Graham, Rachel L.; Donaldson, Eric F.; Baric, Ralph S.
- Nature Reviews Microbiology, Vol. 11, Issue 12
MERS-CoV and H5N1 influenza virus antagonize antigen presentation by altering the epigenetic landscape
journal, January 2018
- Menachery, Vineet D.; Schäfer, Alexandra; Burnum-Johnson, Kristin E.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 5
Broad-spectrum antiviral GS-5734 inhibits both epidemic and zoonotic coronaviruses
journal, June 2017
- Sheahan, Timothy P.; Sims, Amy C.; Graham, Rachel L.
- Science Translational Medicine, Vol. 9, Issue 396
Toll-Like Receptor 3 Signaling via TRIF Contributes to a Protective Innate Immune Response to Severe Acute Respiratory Syndrome Coronavirus Infection
journal, May 2015
- Totura, Allison L.; Whitmore, Alan; Agnihothram, Sudhakar
- mBio, Vol. 6, Issue 3
Complement Activation Contributes to Severe Acute Respiratory Syndrome Coronavirus Pathogenesis
journal, October 2018
- Gralinski, Lisa E.; Sheahan, Timothy P.; Morrison, Thomas E.
- mBio, Vol. 9, Issue 5
Pulmonary vascular dysfunction in ARDS
journal, August 2014
- Ryan, Donal; Frohlich, Stephen; McLoughlin, Paul
- Annals of Intensive Care, Vol. 4, Issue 1
Genome Wide Identification of SARS-CoV Susceptibility Loci Using the Collaborative Cross
journal, October 2015
- Gralinski, Lisa E.; Ferris, Martin T.; Aylor, David L.
- PLOS Genetics, Vol. 11, Issue 10
The PDZ-Binding Motif of Severe Acute Respiratory Syndrome Coronavirus Envelope Protein Is a Determinant of Viral Pathogenesis
journal, August 2014
- Jimenez-Guardeño, Jose M.; Nieto-Torres, Jose L.; DeDiego, Marta L.
- PLoS Pathogens, Vol. 10, Issue 8
An Epithelial Integrin Regulates the Amplitude of Protective Lung Interferon Responses against Multiple Respiratory Pathogens
journal, August 2016
- Meliopoulos, Victoria A.; Van de Velde, Lee-Ann; Van de Velde, Nicholas C.
- PLOS Pathogens, Vol. 12, Issue 8
Host resilience to emerging coronaviruses
journal, July 2016
- Jamieson, Amanda M.
- Future Virology, Vol. 11, Issue 7
The Role of EGFR in Influenza Pathogenicity: Multiple Network-Based Approaches to Identify a Key Regulator of Non-lethal Infections
journal, September 2019
- Mitchell, Hugh D.; Eisfeld, Amie J.; Stratton, Kelly G.
- Frontiers in Cell and Developmental Biology, Vol. 7
Multi-omic network signatures of disease
journal, January 2014
- Gibbs, David L.; Gralinski, Lisa; Baric, Ralph S.
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SARS-CoV-2 Infection with Different Radiological Insights
journal, May 2020
- Brogna, Barbara; Brogna, Claudia; Martino, Alberigo
- Diagnostics, Vol. 10, Issue 5
Annotation of long non-coding RNAs expressed in Collaborative Cross founder mice in response to respiratory virus infection reveals a new class of interferon-stimulated transcripts
journal, June 2014
- Josset, Laurence; Tchitchek, Nicolas; Gralinski, Lisa E.
- RNA Biology, Vol. 11, Issue 7