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Article: Macrophages control pathological interferon responses during viral respiratory infection.

Hoagland, Daisy A / Rodríguez-Morales, Patricia / Mann, Alexander O / Yu, Shuang / Lai, Alicia / Vazquez, Alan Baez / Pope, Scott D / Lim, Jaechul / Li, Shun / Zhang, Xian / Li, Ming O / Medzhitov, Ruslan / Franklin, Ruth A

bioRxiv : the preprint server for biology

2023

Abstract: Antiviral immune mediators, including interferons and their downstream effectors, are critical for host defense yet can become detrimental when uncontrolled. Here, we identify a macrophage-mediated anti-inflammatory mechanism that limits type I ... ...

Abstract	Antiviral immune mediators, including interferons and their downstream effectors, are critical for host defense yet can become detrimental when uncontrolled. Here, we identify a macrophage-mediated anti-inflammatory mechanism that limits type I interferon (IFN-I) responses. Specifically, we found that cellular stress and pathogen recognition induce Oncostatin M (OSM) production by macrophages. OSM-deficient mice succumbed to challenge with influenza or a viral mimic due to heightened IFN-I activation. Macrophage-derived OSM restricted excessive IFN-I production by lung epithelial cells following viral stimulation. Furthermore, reconstitution of OSM in the respiratory tract was sufficient to protect mice lacking macrophage-derived OSM against morbidity, indicating the importance of local OSM production. This work reveals a host strategy to dampen inflammation in the lung through the negative regulation of IFN-I by macrophages.
Language	English
Publishing date	2023-12-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.12.16.572019
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Article: Disruption of nuclear architecture as a cause of COVID-19 induced anosmia.

Zazhytska, Marianna / Kodra, Albana / Hoagland, Daisy A / Fullard, John F / Shayya, Hani / Omer, Arina / Firestein, Stuart / Gong, Qizhi / Canoll, Peter D / Goldman, James E / Roussos, Panos / tenOever, Benjamin R / Overdevest, Jonathan B / Lomvardas, Stavros

bioRxiv : the preprint server for biology

2021

Abstract: Olfaction relies on a coordinated partnership between odorant flow and neuronal communication. Disruption in our ability to detect odors, or anosmia, has emerged as a hallmark symptom of infection with SARS-CoV-2, yet the mechanism behind this abrupt ... ...

Abstract	Olfaction relies on a coordinated partnership between odorant flow and neuronal communication. Disruption in our ability to detect odors, or anosmia, has emerged as a hallmark symptom of infection with SARS-CoV-2, yet the mechanism behind this abrupt sensory deficit remains elusive. Here, using molecular evaluation of human olfactory epithelium (OE) from subjects succumbing to COVID-19 and a hamster model of SARS-CoV-2 infection, we discovered widespread downregulation of olfactory receptors (ORs) as well as key components of their signaling pathway. OR downregulation likely represents a non-cell autonomous effect, since SARS-CoV-2 detection in OSNs is extremely rare both in human and hamster OEs. A likely explanation for the reduction of OR transcription is the striking reorganization of nuclear architecture observed in the OSN lineage, which disrupts multi-chromosomal compartments regulating OR expression in humans and hamsters. Our experiments uncover a novel molecular mechanism by which a virus with a very selective tropism can elicit persistent transcriptional changes in cells that evade it, contributing to the severity of COVID-19.
Language	English
Publishing date	2021-02-09
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.02.09.430314
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Article ; Online: Leveraging the antiviral type I interferon system as a first line of defense against SARS-CoV-2 pathogenicity.

Hoagland, Daisy A / Møller, Rasmus / Uhl, Skyler A / Oishi, Kohei / Frere, Justin / Golynker, Ilona / Horiuchi, Shu / Panis, Maryline / Blanco-Melo, Daniel / Sachs, David / Arkun, Knarik / Lim, Jean K / tenOever, Benjamin R

Immunity

2021 Volume 54, Issue 3, Page(s) 557–570.e5

Abstract: The emergence and spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has resulted in significant global morbidity, mortality, and societal disruption. A better understanding of virus-host interactions may potentiate therapeutic ... ...

Abstract	The emergence and spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has resulted in significant global morbidity, mortality, and societal disruption. A better understanding of virus-host interactions may potentiate therapeutic insights toward limiting this infection. Here we investigated the dynamics of the systemic response to SARS-CoV-2 in hamsters by histological analysis and transcriptional profiling. Infection resulted in consistently high levels of virus in the upper and lower respiratory tracts and sporadic occurrence in other distal tissues. A longitudinal cohort revealed a wave of inflammation, including a type I interferon (IFN-I) response, that was evident in all tissues regardless of viral presence but was insufficient to prevent disease progression. Bolstering the antiviral response with intranasal administration of recombinant IFN-I reduced viral disease, prevented transmission, and lowered inflammation in vivo. This study defines the systemic host response to SARS-CoV-2 infection and supports use of intranasal IFN-I as an effective means of early treatment.
MeSH term(s)	Animals ; Biopsy ; COVID-19/genetics ; COVID-19/immunology ; COVID-19/metabolism ; COVID-19/virology ; Cricetinae ; Cytokines/genetics ; Cytokines/metabolism ; Disease Models, Animal ; Gene Expression Profiling ; Host-Pathogen Interactions/immunology ; Humans ; Immunity, Innate ; Interferon Type I/genetics ; Interferon Type I/metabolism ; Lung/immunology ; Lung/metabolism ; Lung/pathology ; Lung/virology ; Organ Specificity/immunology ; SARS-CoV-2/physiology ; Virulence ; Virus Replication/immunology
Chemical Substances	Cytokines ; Interferon Type I
Language	English
Publishing date	2021-01-29
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1217235-2
ISSN	1097-4180 ; 1074-7613
ISSN (online)	1097-4180
ISSN	1074-7613
DOI	10.1016/j.immuni.2021.01.017
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Article ; Online: SARS-CoV-2 infection in hamsters and humans results in lasting and unique systemic perturbations after recovery.

Science translational medicine

2022 Volume 14, Issue 664, Page(s) eabq3059

Abstract: The host response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection can result in prolonged pathologies collectively referred to as post-acute sequalae of COVID-19 (PASC) or long COVID. To better understand the mechanism ... ...

Abstract	The host response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection can result in prolonged pathologies collectively referred to as post-acute sequalae of COVID-19 (PASC) or long COVID. To better understand the mechanism underlying long COVID biology, we compared the short- and long-term systemic responses in the golden hamster after either SARS-CoV-2 or influenza A virus (IAV) infection. Results demonstrated that SARS-CoV-2 exceeded IAV in its capacity to cause permanent injury to the lung and kidney and uniquely affected the olfactory bulb (OB) and olfactory epithelium (OE). Despite a lack of detectable infectious virus, the OB and OE demonstrated myeloid and T cell activation, proinflammatory cytokine production, and an interferon response that correlated with behavioral changes extending a month after viral clearance. These sustained transcriptional changes could also be corroborated from tissue isolated from individuals who recovered from COVID-19. These data highlight a molecular mechanism for persistent COVID-19 symptomology and provide a small animal model to explore future therapeutics.
MeSH term(s)	Animals ; COVID-19/complications ; Cricetinae ; Humans ; Interferons ; Mesocricetus ; SARS-CoV-2 ; Post-Acute COVID-19 Syndrome
Chemical Substances	Interferons (9008-11-1)
Language	English
Publishing date	2022-09-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2518854-9
ISSN	1946-6242 ; 1946-6234
ISSN (online)	1946-6242
ISSN	1946-6234
DOI	10.1126/scitranslmed.abq3059
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Article ; Online: Non-cell-autonomous disruption of nuclear architecture as a potential cause of COVID-19-induced anosmia.

Zazhytska, Marianna / Kodra, Albana / Hoagland, Daisy A / Frere, Justin / Fullard, John F / Shayya, Hani / McArthur, Natalie G / Moeller, Rasmus / Uhl, Skyler / Omer, Arina D / Gottesman, Max E / Firestein, Stuart / Gong, Qizhi / Canoll, Peter D / Goldman, James E / Roussos, Panos / tenOever, Benjamin R / Jonathan B Overdevest / Lomvardas, Stavros

Cell

2022 Volume 185, Issue 6, Page(s) 1052–1064.e12

Abstract: SARS-CoV-2 infects less than 1% of cells in the human body, yet it can cause severe damage in a variety of organs. Thus, deciphering the non-cell-autonomous effects of SARS-CoV-2 infection is imperative for understanding the cellular and molecular ... ...

Abstract	SARS-CoV-2 infects less than 1% of cells in the human body, yet it can cause severe damage in a variety of organs. Thus, deciphering the non-cell-autonomous effects of SARS-CoV-2 infection is imperative for understanding the cellular and molecular disruption it elicits. Neurological and cognitive defects are among the least understood symptoms of COVID-19 patients, with olfactory dysfunction being their most common sensory deficit. Here, we show that both in humans and hamsters, SARS-CoV-2 infection causes widespread downregulation of olfactory receptors (ORs) and of their signaling components. This non-cell-autonomous effect is preceded by a dramatic reorganization of the neuronal nuclear architecture, which results in dissipation of genomic compartments harboring OR genes. Our data provide a potential mechanism by which SARS-CoV-2 infection alters the cellular morphology and the transcriptome of cells it cannot infect, offering insight to its systemic effects in olfaction and beyond.
MeSH term(s)	Animals ; Anosmia ; COVID-19 ; Cricetinae ; Down-Regulation ; Humans ; Receptors, Odorant ; SARS-CoV-2 ; Smell
Chemical Substances	Receptors, Odorant
Language	English
Publishing date	2022-02-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2022.01.024
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Zs.A 1167: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Cardiomyocytes recruit monocytes upon SARS-CoV-2 infection by secreting CCL2.

Yang, Liuliu / Nilsson-Payant, Benjamin E / Han, Yuling / Jaffré, Fabrice / Zhu, Jiajun / Wang, Pengfei / Zhang, Tuo / Redmond, David / Houghton, Sean / Møller, Rasmus / Hoagland, Daisy / Carrau, Lucia / Horiuchi, Shu / Goff, Marisa / Lim, Jean K / Bram, Yaron / Richardson, Chanel / Chandar, Vasuretha / Borczuk, Alain /

Huang, Yaoxing / Xiang, Jenny / Ho, David D / Schwartz, Robert E / tenOever, Benjamin R / Evans, Todd / Chen, Shuibing

Stem cell reports

2021 Volume 16, Issue 10, Page(s) 2565

Language	English
Publishing date	2021-10-06
Publishing country	United States
Document type	Published Erratum
ZDB-ID	2720528-9
ISSN	2213-6711 ; 2213-6711
ISSN (online)	2213-6711
ISSN	2213-6711
DOI	10.1016/j.stemcr.2021.09.008
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Article ; Online: Disruption of nuclear architecture as a cause of COVID-19 induced anosmia

Zazhytska, Marianna / Kodra, Albana / Hoagland, Daisy A. / Fullard, John / Shayya, Hani J. / Omer, Arina / Firestein, Stuart / Gong, Qizhi / Canoll, Peter / Goldman, James E. / Roussos, Panos / tenOever, Benjamin R. / Overdevest, Jonathan B / Lomvardas, Stavros

bioRxiv

Abstract	Olfaction relies on a coordinated partnership between odorant flow and neuronal communication. Disruption in our ability to detect odors, or anosmia, has emerged as a hallmark symptom of infection with SARS-CoV-2 and yet the mechanism behind this abrupt sensory deficit remains elusive. Here, using molecular evaluation of human olfactory epithelium (OE) from subjects succumbing to COVID-19 and a hamster model of SARS-CoV-2 infection, we discovered widespread downregulation of olfactory receptors (ORs) and key components of their signaling pathway. OR downregulation likely represents a non-cell autonomous effect, since SARS-CoV-2 detection in OSNs is extremely rare both in human and hamster OEs. A likely explanation for the reduction of OR transcription is the striking reorganization of nuclear architecture observed in the OSN lineage, which disrupts multi-chromosomal compartments regulating OR expression in humans and hamsters. Our experiments uncover a novel molecular mechanism by which a virus with a very selective tropism can elicit persistent transcriptional changes in cells that evade it, contributing to the severity of COVID-19.
Keywords	covid19
Language	English
Publishing date	2021-02-09
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2021.02.09.430314
Database	COVID19

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Article ; Online: Imbalanced Host Response to SARS-CoV-2 Drives Development of COVID-19.

Blanco-Melo, Daniel / Nilsson-Payant, Benjamin E / Liu, Wen-Chun / Uhl, Skyler / Hoagland, Daisy / Møller, Rasmus / Jordan, Tristan X / Oishi, Kohei / Panis, Maryline / Sachs, David / Wang, Taia T / Schwartz, Robert E / Lim, Jean K / Albrecht, Randy A / tenOever, Benjamin R

Cell

2020 Volume 181, Issue 5, Page(s) 1036–1045.e9

Abstract: Viral pandemics, such as the one caused by SARS-CoV-2, pose an imminent threat to humanity. Because of its recent emergence, there is a paucity of information regarding viral behavior and host response following SARS-CoV-2 infection. Here we offer an in- ... ...

Abstract	Viral pandemics, such as the one caused by SARS-CoV-2, pose an imminent threat to humanity. Because of its recent emergence, there is a paucity of information regarding viral behavior and host response following SARS-CoV-2 infection. Here we offer an in-depth analysis of the transcriptional response to SARS-CoV-2 compared with other respiratory viruses. Cell and animal models of SARS-CoV-2 infection, in addition to transcriptional and serum profiling of COVID-19 patients, consistently revealed a unique and inappropriate inflammatory response. This response is defined by low levels of type I and III interferons juxtaposed to elevated chemokines and high expression of IL-6. We propose that reduced innate antiviral defenses coupled with exuberant inflammatory cytokine production are the defining and driving features of COVID-19.
MeSH term(s)	Animals ; Betacoronavirus/physiology ; COVID-19 ; Cells, Cultured ; Chemokines/genetics ; Chemokines/immunology ; Coronavirus Infections/genetics ; Coronavirus Infections/immunology ; Disease Models, Animal ; Host-Pathogen Interactions ; Humans ; Immunity, Innate ; Inflammation/virology ; Interferons/genetics ; Interferons/immunology ; Pandemics ; Pneumonia, Viral/genetics ; Pneumonia, Viral/immunology ; RNA Viruses/classification ; RNA Viruses/immunology ; SARS-CoV-2 ; Transcription, Genetic
Chemical Substances	Chemokines ; Interferons (9008-11-1)
Keywords	covid19
Language	English
Publishing date	2020-05-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2020.04.026
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Article: Non-cell-autonomous disruption of nuclear architecture as a potential cause of COVID-19-induced anosmia

Zazhytska, Marianna / Kodra, Albana / Hoagland, Daisy A. / Frere, Justin / Fullard, John F. / Shayya, Hani / McArthur, Natalie G. / Moeller, Rasmus / Uhl, Skyler / Omer, Arina D. / Gottesman, Max E. / Firestein, Stuart / Gong, Qizhi / Canoll, Peter D. / Goldman, James E. / Roussos, Panos / tenOever, Benjamin R. / Jonathan B. Overdevest / Lomvardas, Stavros

Cell. 2022 Mar. 17, v. 185, no. 6

2022

Abstract	SARS-CoV-2 infects less than 1% of cells in the human body, yet it can cause severe damage in a variety of organs. Thus, deciphering the non-cell-autonomous effects of SARS-CoV-2 infection is imperative for understanding the cellular and molecular disruption it elicits. Neurological and cognitive defects are among the least understood symptoms of COVID-19 patients, with olfactory dysfunction being their most common sensory deficit. Here, we show that both in humans and hamsters, SARS-CoV-2 infection causes widespread downregulation of olfactory receptors (ORs) and of their signaling components. This non-cell-autonomous effect is preceded by a dramatic reorganization of the neuronal nuclear architecture, which results in dissipation of genomic compartments harboring OR genes. Our data provide a potential mechanism by which SARS-CoV-2 infection alters the cellular morphology and the transcriptome of cells it cannot infect, offering insight to its systemic effects in olfaction and beyond.
Keywords	COVID-19 infection ; Severe acute respiratory syndrome coronavirus 2 ; cognition ; genomics ; humans ; neurons ; olfactory disorders ; smell ; transcriptome
Language	English
Dates of publication	2022-0317
Size	p. 1052-1064.e12.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2022.01.024
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Common Genetic Variation in Humans Impacts In Vitro Susceptibility to SARS-CoV-2 Infection.

Dobrindt, Kristina / Hoagland, Daisy A / Seah, Carina / Kassim, Bibi / O'Shea, Callan P / Murphy, Aleta / Iskhakova, Marina / Fernando, Michael B / Powell, Samuel K / Deans, P J Michael / Javidfar, Ben / Peter, Cyril / Møller, Rasmus / Uhl, Skyler A / Garcia, Meilin Fernandez / Kimura, Masaki / Iwasawa, Kentaro / Crary, John F / Kotton, Darrell N /

Takebe, Takanori / Huckins, Laura M / tenOever, Benjamin R / Akbarian, Schahram / Brennand, Kristen J

Stem cell reports

2021 Volume 16, Issue 3, Page(s) 505–518

Abstract: The host response to SARS-CoV-2, the etiologic agent of the COVID-19 pandemic, demonstrates significant interindividual variability. In addition to showing more disease in males, the elderly, and individuals with underlying comorbidities, SARS-CoV-2 can ... ...

Abstract	The host response to SARS-CoV-2, the etiologic agent of the COVID-19 pandemic, demonstrates significant interindividual variability. In addition to showing more disease in males, the elderly, and individuals with underlying comorbidities, SARS-CoV-2 can seemingly afflict healthy individuals with profound clinical complications. We hypothesize that, in addition to viral load and host antibody repertoire, host genetic variants influence vulnerability to infection. Here we apply human induced pluripotent stem cell (hiPSC)-based models and CRISPR engineering to explore the host genetics of SARS-CoV-2. We demonstrate that a single-nucleotide polymorphism (rs4702), common in the population and located in the 3' UTR of the protease FURIN, influences alveolar and neuron infection by SARS-CoV-2 in vitro. Thus, we provide a proof-of-principle finding that common genetic variation can have an impact on viral infection and thus contribute to clinical heterogeneity in COVID-19. Ongoing genetic studies will help to identify high-risk individuals, predict clinical complications, and facilitate the discovery of drugs.
MeSH term(s)	3' Untranslated Regions/genetics ; Adolescent ; Adult ; Animals ; COVID-19/genetics ; COVID-19/virology ; Cell Line ; Chlorocebus aethiops ; Clustered Regularly Interspaced Short Palindromic Repeats/genetics ; Female ; Furin/genetics ; Genetic Predisposition to Disease/genetics ; Host-Pathogen Interactions/genetics ; Humans ; Induced Pluripotent Stem Cells/virology ; Male ; Neurons/virology ; Peptide Hydrolases/genetics ; Polymorphism, Single Nucleotide/genetics ; SARS-CoV-2/pathogenicity ; Vero Cells
Chemical Substances	3' Untranslated Regions ; Peptide Hydrolases (EC 3.4.-) ; Furin (EC 3.4.21.75)
Language	English
Publishing date	2021-02-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2720528-9
ISSN	2213-6711 ; 2213-6711
ISSN (online)	2213-6711
ISSN	2213-6711
DOI	10.1016/j.stemcr.2021.02.010
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