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Article ; Online: De Novo

Wang, Ruobing / Simone-Roach, Chantelle / Lindstrom-Vautrin, Jonathan / Wang, Feiya / Rollins, Stuart / Bawa, Pushpinder Singh / Lu, Junjie / Tang, Yang / Beermann, Mary Lou / Schlaeger, Thorsten / Mahoney, John / Rowe, Steven M / Hawkins, Finn J / Kotton, Darrell N

American journal of respiratory and critical care medicine

2023 Volume 207, Issue 9, Page(s) 1249–1253

MeSH term(s)	Humans ; Induced Pluripotent Stem Cells ; Cystic Fibrosis ; Cells, Cultured ; Cell Line ; Cystic Fibrosis Transmembrane Conductance Regulator ; Cell Differentiation
Chemical Substances	Cystic Fibrosis Transmembrane Conductance Regulator (126880-72-6)
Language	English
Publishing date	2023-02-21
Publishing country	United States
Document type	Letter ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1180953-x
ISSN	1535-4970 ; 0003-0805 ; 1073-449X
ISSN (online)	1535-4970
ISSN	0003-0805 ; 1073-449X
DOI	10.1164/rccm.202205-1010LE
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Article ; Online: Human airway lineages derived from pluripotent stem cells reveal the epithelial responses to SARS-CoV-2 infection.

Wang, Ruobing / Hume, Adam J / Beermann, Mary Lou / Simone-Roach, Chantelle / Lindstrom-Vautrin, Jonathan / Le Suer, Jake / Huang, Jessie / Olejnik, Judith / Villacorta-Martin, Carlos / Bullitt, Esther / Hinds, Anne / Ghaedi, Mahboobe / Rollins, Stuart / Werder, Rhiannon B / Abo, Kristine M / Wilson, Andrew A / Mühlberger, Elke / Kotton, Darrell N / Hawkins, Finn J

American journal of physiology. Lung cellular and molecular physiology

2022 Volume 322, Issue 3, Page(s) L462–L478

Abstract: There is an urgent need to understand how SARS-CoV-2 infects the airway epithelium and in a subset of individuals leads to severe illness or death. Induced pluripotent stem cells (iPSCs) provide a near limitless supply of human cells that can be ... ...

Abstract	There is an urgent need to understand how SARS-CoV-2 infects the airway epithelium and in a subset of individuals leads to severe illness or death. Induced pluripotent stem cells (iPSCs) provide a near limitless supply of human cells that can be differentiated into cell types of interest, including airway epithelium, for disease modeling. We present a human iPSC-derived airway epithelial platform, composed of the major airway epithelial cell types, that is permissive to SARS-CoV-2 infection. Subsets of iPSC-airway cells express the SARS-CoV-2 entry factors angiotensin-converting enzyme 2 (
MeSH term(s)	COVID-19 ; Epithelial Cells ; Humans ; Induced Pluripotent Stem Cells ; Pluripotent Stem Cells ; SARS-CoV-2
Language	English
Publishing date	2022-01-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1013184-x
ISSN	1522-1504 ; 1040-0605
ISSN (online)	1522-1504
ISSN	1040-0605
DOI	10.1152/ajplung.00397.2021
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Article ; Online: Human airway lineages derived from pluripotent stem cells reveal the epithelial responses to SARS-CoV-2 infection

Wang, Ruobing / Hume, Adam / Beermann, Mary Lou / Simone-Roach, Chantelle / Lindstrom-Vautrin, Jonathan / Le Suer, Jake / Huang, Jessie / Olejnik, Judith / Villacorta-Martin, Carlos / Bullitt, Esther / Hinds, Anne / Ghaedi, Mahboobe / Werder, Rhiannon / Abo, Kristine / Wilson, Andrew / Muhlberger, Elke / Kotton, Darrell N. / Hawkins, Finn J

bioRxiv

Abstract	There is an urgent need to understand how SARS-CoV-2 infects the airway epithelium and in a subset of individuals leads to severe illness or death. Induced pluripotent stem cells (iPSCs) provide a near limitless supply of human cells that can be differentiated into cell types of interest, including airway epithelium, for disease modeling. We present a human iPSC-derived airway epithelial platform, composed of the major airway epithelial cell types, that is permissive to SARS-CoV-2 infection. Subsets of iPSC-airway cells express the SARS-CoV-2 entry factors ACE2 and TMPRSS2. Multiciliated cells are the primary initial target of SARS-CoV-2 infection. Upon infection with SARS-CoV-2, iPSC-airway cells generate robust interferon and inflammatory responses and treatment with remdesivir or camostat methylate causes a decrease in viral propagation and entry, respectively. In conclusion, iPSC-derived airway cells provide a physiologically relevant in vitro model system to interrogate the pathogenesis of, and develop treatment strategies for, COVID-19 pneumonia.
Keywords	covid19
Language	English
Publishing date	2021-07-07
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2021.07.06.451340
Database	COVID19

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Article: SARS-CoV-2 Infection of Pluripotent Stem Cell-derived Human Lung Alveolar Type 2 Cells Elicits a Rapid Epithelial-Intrinsic Inflammatory Response.

bioRxiv : the preprint server for biology

2020

Abstract: The most severe and fatal infections with SARS-CoV-2 result in the acute respiratory distress syndrome, a clinical phenotype of coronavirus disease 2019 (COVID-19) that is associated with virions targeting the epithelium of the distal lung, particularly ... ...

Abstract	The most severe and fatal infections with SARS-CoV-2 result in the acute respiratory distress syndrome, a clinical phenotype of coronavirus disease 2019 (COVID-19) that is associated with virions targeting the epithelium of the distal lung, particularly the facultative progenitors of this tissue, alveolar epithelial type 2 cells (AT2s). Little is known about the initial responses of human lung alveoli to SARS-CoV-2 infection due in part to inability to access these cells from patients, particularly at early stages of disease. Here we present an
Keywords	covid19
Language	English
Publishing date	2020-08-06
Publishing country	United States
Document type	Preprint
DOI	10.1101/2020.06.30.175695
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Article ; Online: SARS-CoV-2 Infection of Pluripotent Stem Cell-Derived Human Lung Alveolar Type 2 Cells Elicits a Rapid Epithelial-Intrinsic Inflammatory Response.

Cell stem cell

2020 Volume 27, Issue 6, Page(s) 962–973.e7

Abstract: A hallmark of severe COVID-19 pneumonia is SARS-CoV-2 infection of the facultative progenitors of lung alveoli, the alveolar epithelial type 2 cells (AT2s). However, inability to access these cells from patients, particularly at early stages of disease, ... ...

Abstract	A hallmark of severe COVID-19 pneumonia is SARS-CoV-2 infection of the facultative progenitors of lung alveoli, the alveolar epithelial type 2 cells (AT2s). However, inability to access these cells from patients, particularly at early stages of disease, limits an understanding of disease inception. Here, we present an in vitro human model that simulates the initial apical infection of alveolar epithelium with SARS-CoV-2 by using induced pluripotent stem cell-derived AT2s that have been adapted to air-liquid interface culture. We find a rapid transcriptomic change in infected cells, characterized by a shift to an inflammatory phenotype with upregulation of NF-κB signaling and loss of the mature alveolar program. Drug testing confirms the efficacy of remdesivir as well as TMPRSS2 protease inhibition, validating a putative mechanism used for viral entry in alveolar cells. Our model system reveals cell-intrinsic responses of a key lung target cell to SARS-CoV-2 infection and should facilitate drug development.
MeSH term(s)	Adenosine Monophosphate/analogs & derivatives ; Adenosine Monophosphate/pharmacology ; Alanine/analogs & derivatives ; Alanine/pharmacology ; Alveolar Epithelial Cells/virology ; Animals ; Antiviral Agents/pharmacology ; COVID-19/virology ; Cells, Cultured ; Drug Development ; Enzyme Inhibitors/pharmacology ; Humans ; Inflammation/virology ; Models, Biological ; Pluripotent Stem Cells/cytology ; Pluripotent Stem Cells/virology ; RNA-Seq ; SARS-CoV-2/physiology ; Serine Endopeptidases/metabolism ; Virus Replication
Chemical Substances	Antiviral Agents ; Enzyme Inhibitors ; remdesivir (3QKI37EEHE) ; Adenosine Monophosphate (415SHH325A) ; Serine Endopeptidases (EC 3.4.21.-) ; TMPRSS2 protein, human (EC 3.4.21.-) ; Alanine (OF5P57N2ZX)
Keywords	covid19
Language	English
Publishing date	2020-09-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2375354-7
ISSN	1875-9777 ; 1934-5909
ISSN (online)	1875-9777
ISSN	1934-5909
DOI	10.1016/j.stem.2020.09.013
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Article ; Online: Derivation of Airway Basal Stem Cells from Human Pluripotent Stem Cells.

Hawkins, Finn J / Suzuki, Shingo / Beermann, Mary Lou / Barillà, Cristina / Wang, Ruobing / Villacorta-Martin, Carlos / Berical, Andrew / Jean, J C / Le Suer, Jake / Matte, Taylor / Simone-Roach, Chantelle / Tang, Yang / Schlaeger, Thorsten M / Crane, Ana M / Matthias, Nadine / Huang, Sarah X L / Randell, Scott H / Wu, Joshua / Spence, Jason R /

Carraro, Gianni / Stripp, Barry R / Rab, Andras / Sorsher, Eric J / Horani, Amjad / Brody, Steven L / Davis, Brian R / Kotton, Darrell N

Cell stem cell

2020 Volume 28, Issue 1, Page(s) 79–95.e8

Abstract: The derivation of tissue-specific stem cells from human induced pluripotent stem cells (iPSCs) would have broad reaching implications for regenerative medicine. Here, we report the directed differentiation of human iPSCs into airway basal cells ("iBCs"), ...

Abstract	The derivation of tissue-specific stem cells from human induced pluripotent stem cells (iPSCs) would have broad reaching implications for regenerative medicine. Here, we report the directed differentiation of human iPSCs into airway basal cells ("iBCs"), a population resembling the stem cell of the airway epithelium. Using a dual fluorescent reporter system (NKX2-1
MeSH term(s)	Cell Differentiation ; Epithelial Cells ; Humans ; Induced Pluripotent Stem Cells ; Lung ; Pluripotent Stem Cells ; Trachea
Language	English
Publishing date	2020-10-23
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2375354-7
ISSN	1875-9777 ; 1934-5909
ISSN (online)	1875-9777
ISSN	1934-5909
DOI	10.1016/j.stem.2020.09.017
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Article: SARS-CoV-2 Infection of Pluripotent Stem Cell-derived Human Lung Alveolar Type 2 Cells Elicits a Rapid Epithelial-Intrinsic Inflammatory Response

Abstract	The most severe and fatal infections with SARS-CoV-2 result in the acute respiratory distress syndrome, a clinical phenotype of coronavirus disease 2019 (COVID-19) that is associated with virions targeting the epithelium of the distal lung, particularly the facultative progenitors of this tissue, alveolar epithelial type 2 cells (AT2s) Little is known about the initial responses of human lung alveoli to SARS-CoV-2 infection due in part to inability to access these cells from patients, particularly at early stages of disease Here we present an in vitro human model that simulates the initial apical infection of the distal lung epithelium with SARS-CoV-2, using AT2s that have been adapted to air-liquid interface culture after their derivation from induced pluripotent stem cells (iAT2s) We find that SARS-CoV-2 induces a rapid global transcriptomic change in infected iAT2s characterized by a shift to an inflammatory phenotype predominated by the secretion of cytokines encoded by NF-kB target genes, delayed epithelial interferon responses, and rapid loss of the mature lung alveolar epithelial program Over time, infected iAT2s exhibit cellular toxicity that can result in the death of these key alveolar facultative progenitors, as is observed in vivo in COVID-19 lung autopsies Importantly, drug testing using iAT2s confirmed the efficacy of TMPRSS2 protease inhibition, validating putative mechanisms used for viral entry in human alveolar cells Our model system reveals the cell-intrinsic responses of a key lung target cell to infection, providing a platform for further drug development and facilitating a deeper understanding of COVID-19 pathogenesis
Keywords	covid19
Publisher	WHO
Document type	Article
Note	WHO #Covidence: #637839
Database	COVID19

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Article: SARS-CoV-2 Infection of Pluripotent Stem Cell-Derived Human Lung Alveolar Type 2 Cells Elicits a Rapid Epithelial-Intrinsic Inflammatory Response

Cell stem cell (Online)

Abstract	A hallmark of severe COVID-19 pneumonia is SARS-CoV-2 infection of the facultative progenitors of lung alveoli, the alveolar epithelial type 2 cells (AT2s). However, inability to access these cells from patients, particularly at early stages of disease, limits an understanding of disease inception. Here, we present an in vitro human model that simulates the initial apical infection of alveolar epithelium with SARS-CoV-2 by using induced pluripotent stem cell-derived AT2s that have been adapted to air-liquid interface culture. We find a rapid transcriptomic change in infected cells, characterized by a shift to an inflammatory phenotype with upregulation of NF-κB signaling and loss of the mature alveolar program. Drug testing confirms the efficacy of remdesivir as well as TMPRSS2 protease inhibition, validating a putative mechanism used for viral entry in alveolar cells. Our model system reveals cell-intrinsic responses of a key lung target cell to SARS-CoV-2 infection and should facilitate drug development.
Keywords	covid19
Publisher	WHO
Document type	Article
Note	WHO #Covidence: #779662
Database	COVID19

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Article ; Online: SARS-CoV-2 Infection of Pluripotent Stem Cell-Derived Human Lung Alveolar Type 2 Cells Elicits a Rapid Epithelial-Intrinsic Inflammatory Response

Cell Stem Cell ; ISSN 1934-5909

2020

Keywords	Molecular Medicine ; Genetics ; Cell Biology ; covid19
Language	English
Publisher	Elsevier BV
Publishing country	us
Document type	Article ; Online
DOI	10.1016/j.stem.2020.09.013
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: The Epithelial Sodium Channel Is a Modifier of the Long-Term Nonprogressive Phenotype Associated with F508del CFTR Mutations.

Agrawal, Pankaj B / Wang, Ruobing / Li, Hongmei Lisa / Schmitz-Abe, Klaus / Simone-Roach, Chantelle / Chen, Jingxin / Shi, Jiahai / Louie, Tin / Sheng, Shaohu / Towne, Meghan C / Brainson, Christine F / Matthay, Michael A / Kim, Carla F / Bamshad, Michael / Emond, Mary J / Gerard, Norma P / Kleyman, Thomas R / Gerard, Craig

American journal of respiratory cell and molecular biology

2017 Volume 57, Issue 6, Page(s) 711–720

Abstract: Cystic fibrosis (CF) remains the most lethal genetic disease in the Caucasian population. However, there is great variability in clinical phenotypes and survival times, even among patients harboring the same genotype. We identified five patients with CF ... ...

Abstract	Cystic fibrosis (CF) remains the most lethal genetic disease in the Caucasian population. However, there is great variability in clinical phenotypes and survival times, even among patients harboring the same genotype. We identified five patients with CF and a homozygous F508del mutation in the CFTR gene who were in their fifth or sixth decade of life and had shown minimal changes in lung function over a longitudinal period of more than 20 years. Because of the rarity of this long-term nonprogressive phenotype, we hypothesized these individuals may carry rare genetic variants in modifier genes that ameliorate disease severity. Individuals at the extremes of survival time and lung-function trajectory underwent whole-exome sequencing, and the sequencing data were filtered to include rare missense, stopgain, indel, and splicing variants present with a mean allele frequency of <0.2% in general population databases. Epithelial sodium channel (ENaC) mutants were generated via site-directed mutagenesis and expressed for Xenopus oocyte assays. Four of the five individuals carried extremely rare or never reported variants in the SCNN1D and SCNN1B genes of the ENaC. Separately, an independently enriched rare variant in SCNN1D was identified in the Exome Variant Server database associated with a milder pulmonary disease phenotype. Functional analysis using Xenopus oocytes revealed that two of the three variants in δ-ENaC encoded by SCNN1D exhibited hypomorphic channel activity. Our data suggest a potential role for δ-ENaC in controlling sodium reabsorption in the airways, and advance the plausibility of ENaC as a therapeutic target in CF.
MeSH term(s)	Amino Acid Sequence ; Animals ; Cystic Fibrosis/genetics ; Cystic Fibrosis/metabolism ; Cystic Fibrosis Transmembrane Conductance Regulator/genetics ; Cystic Fibrosis Transmembrane Conductance Regulator/metabolism ; Epithelial Sodium Channels/genetics ; Epithelial Sodium Channels/metabolism ; Female ; Humans ; Male ; Sequence Deletion ; Xenopus ; Xenopus laevis
Chemical Substances	CFTR protein, human ; Epithelial Sodium Channels ; SCNN1B protein, human ; SCNN1D protein, human ; Cystic Fibrosis Transmembrane Conductance Regulator (126880-72-6)
Language	English
Publishing date	2017-07-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	1025960-0
ISSN	1535-4989 ; 1044-1549
ISSN (online)	1535-4989
ISSN	1044-1549
DOI	10.1165/rcmb.2017-0166OC
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