Parallel use of human stem cell lung and heart models provide insights for SARS-CoV-2 treatment
et al., Stem Cell Reports, doi:10.1016/j.stemcr.2023.05.007, Jun 2023
HCQ for COVID-19
1st treatment shown to reduce risk in
March 2020, now with p < 0.00000000001 from 424 studies, used in 59 countries.
No treatment is 100% effective. Protocols
combine treatments.
6,200+ studies for
200+ treatments. c19early.org
|
In vitro study showing that SARS-CoV-2 cell entry differs across cell types. ACE2 was required for infection in both lung and cardiac cells, but TMPRSS2 cleavage was required in lung cells, while the endosomal pathway was required in cardiac cells.
Authors show that antiviral activity and cytotoxicity can be significantly different in cardiac and lung cells, and in the commonly used African monkey kidney-derived Vero cells.
These results highlight that, especially after SARS-CoV-2 spreads beyond the upper respiratory tract, a combination of treatments affecting different pathways may be more effective.
39 preclinical studies support the efficacy of HCQ for COVID-19:
Study covers HCQ, remdesivir, and favipiravir.
1.
Shang et al., Identification of Cathepsin L as the molecular target of hydroxychloroquine with chemical proteomics, Molecular & Cellular Proteomics, doi:10.1016/j.mcpro.2025.101314.
2.
González-Paz et al., Biophysical Analysis of Potential Inhibitors of SARS-CoV-2 Cell Recognition and Their Effect on Viral Dynamics in Different Cell Types: A Computational Prediction from In Vitro Experimental Data, ACS Omega, doi:10.1021/acsomega.3c06968.
3.
Alkafaas et al., A study on the effect of natural products against the transmission of B.1.1.529 Omicron, Virology Journal, doi:10.1186/s12985-023-02160-6.
4.
Guimarães Silva et al., Are Non-Structural Proteins From SARS-CoV-2 the Target of Hydroxychloroquine? An in Silico Study, ACTA MEDICA IRANICA, doi:10.18502/acta.v61i2.12533.
5.
Nguyen et al., The Potential of Ameliorating COVID-19 and Sequelae From Andrographis paniculata via Bioinformatics, Bioinformatics and Biology Insights, doi:10.1177/11779322221149622.
7.
Yadav et al., Repurposing the Combination Drug of Favipiravir, Hydroxychloroquine and Oseltamivir as a Potential Inhibitor Against SARS-CoV-2: A Computational Study, Research Square, doi:10.21203/rs.3.rs-628277/v1.
8.
Hussein et al., Molecular Docking Identification for the efficacy of Some Zinc Complexes with Chloroquine and Hydroxychloroquine against Main Protease of COVID-19, Journal of Molecular Structure, doi:10.1016/j.molstruc.2021.129979.
9.
Baildya et al., Inhibitory capacity of Chloroquine against SARS-COV-2 by effective binding with Angiotensin converting enzyme-2 receptor: An insight from molecular docking and MD-simulation studies, Journal of Molecular Structure, doi:10.1016/j.molstruc.2021.129891.
10.
Noureddine et al., Quantum chemical studies on molecular structure, AIM, ELF, RDG and antiviral activities of hybrid hydroxychloroquine in the treatment of COVID-19: molecular docking and DFT calculations, Journal of King Saud University - Science, doi:10.1016/j.jksus.2020.101334.
11.
Tarek et al., Pharmacokinetic Basis of the Hydroxychloroquine Response in COVID-19: Implications for Therapy and Prevention, European Journal of Drug Metabolism and Pharmacokinetics, doi:10.1007/s13318-020-00640-6.
12.
Rowland Yeo et al., Impact of Disease on Plasma and Lung Exposure of Chloroquine, Hydroxychloroquine and Azithromycin: Application of PBPK Modeling, Clinical Pharmacology & Therapeutics, doi:10.1002/cpt.1955.
13.
Hitti et al., Hydroxychloroquine attenuates double-stranded RNA-stimulated hyper-phosphorylation of tristetraprolin/ZFP36 and AU-rich mRNA stabilization, Immunology, doi:10.1111/imm.13835.
14.
Yan et al., Super-resolution imaging reveals the mechanism of endosomal acidification inhibitors against SARS-CoV-2 infection, ChemBioChem, doi:10.1002/cbic.202400404.
15.
Mohd Abd Razak et al., In Vitro Anti-SARS-CoV-2 Activities of Curcumin and Selected Phenolic Compounds, Natural Product Communications, doi:10.1177/1934578X231188861.
16.
Alsmadi et al., The In Vitro, In Vivo, and PBPK Evaluation of a Novel Lung-Targeted Cardiac-Safe Hydroxychloroquine Inhalation Aerogel, AAPS PharmSciTech, doi:10.1208/s12249-023-02627-3.
17.
Wen et al., Cholinergic α7 nAChR signaling suppresses SARS-CoV-2 infection and inflammation in lung epithelial cells, Journal of Molecular Cell Biology, doi:10.1093/jmcb/mjad048.
18.
Kamga Kapchoup et al., In vitro effect of hydroxychloroquine on pluripotent stem cells and their cardiomyocytes derivatives, Frontiers in Pharmacology, doi:10.3389/fphar.2023.1128382.
19.
Milan Bonotto et al., Cathepsin inhibitors nitroxoline and its derivatives inhibit SARS-CoV-2 infection, Antiviral Research, doi:10.1016/j.antiviral.2023.105655.
20.
Miao et al., SIM imaging resolves endocytosis of SARS-CoV-2 spike RBD in living cells, Cell Chemical Biology, doi:10.1016/j.chembiol.2023.02.001.
21.
Yuan et al., Hydroxychloroquine blocks SARS-CoV-2 entry into the endocytic pathway in mammalian cell culture, Communications Biology, doi:10.1038/s42003-022-03841-8.
22.
Faísca et al., Enhanced In Vitro Antiviral Activity of Hydroxychloroquine Ionic Liquids against SARS-CoV-2, Pharmaceutics, doi:10.3390/pharmaceutics14040877.
23.
Delandre et al., Antiviral Activity of Repurposing Ivermectin against a Panel of 30 Clinical SARS-CoV-2 Strains Belonging to 14 Variants, Pharmaceuticals, doi:10.3390/ph15040445.
24.
Purwati et al., An in vitro study of dual drug combinations of anti-viral agents, antibiotics, and/or hydroxychloroquine against the SARS-CoV-2 virus isolated from hospitalized patients in Surabaya, Indonesia, PLOS One, doi:10.1371/journal.pone.0252302.
25.
Zhang et al., SARS-CoV-2 spike protein dictates syncytium-mediated lymphocyte elimination, Cell Death & Differentiation, doi:10.1038/s41418-021-00782-3.
26.
Dang et al., Structural basis of anti-SARS-CoV-2 activity of hydroxychloroquine: specific binding to NTD/CTD and disruption of LLPS of N protein, bioRxiv, doi:10.1101/2021.03.16.435741.
27.
Shang (B) et al., Inhibitors of endosomal acidification suppress SARS-CoV-2 replication and relieve viral pneumonia in hACE2 transgenic mice, Virology Journal, doi:10.1186/s12985-021-01515-1.
28.
Wang et al., Chloroquine and hydroxychloroquine as ACE2 blockers to inhibit viropexis of 2019-nCoV Spike pseudotyped virus, Phytomedicine, doi:10.1016/j.phymed.2020.153333.
29.
Sheaff, R., A New Model of SARS-CoV-2 Infection Based on (Hydroxy)Chloroquine Activity, bioRxiv, doi:10.1101/2020.08.02.232892.
30.
Ou et al., Hydroxychloroquine-mediated inhibition of SARS-CoV-2 entry is attenuated by TMPRSS2, PLOS Pathogens, doi:10.1371/journal.ppat.1009212.
31.
Andreani et al., In vitro testing of combined hydroxychloroquine and azithromycin on SARS-CoV-2 shows synergistic effect, Microbial Pathogenesis, doi:10.1016/j.micpath.2020.104228.
32.
Clementi et al., Combined Prophylactic and Therapeutic Use Maximizes Hydroxychloroquine Anti-SARS-CoV-2 Effects in vitro, Front. Microbiol., 10 July 2020, doi:10.3389/fmicb.2020.01704.
33.
Liu et al., Hydroxychloroquine, a less toxic derivative of chloroquine, is effective in inhibiting SARS-CoV-2 infection in vitro, Cell Discovery 6, 16 (2020), doi:10.1038/s41421-020-0156-0.
34.
Yao et al., In Vitro Antiviral Activity and Projection of Optimized Dosing Design of Hydroxychloroquine for the Treatment of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), Clin. Infect. Dis., 2020 Mar 9, doi:10.1093/cid/ciaa237.
Rudraraju et al., 1 Jun 2023, Australia, peer-reviewed, 28 authors.
Contact: enzo.porrello@mcri.edu.au (corresponding author), jose.polo@monash.edu, sean.humphrey@mcri.edu.au, mirana.ramialison@mcri.edu.au, david.elliott@mcri.edu.au, kanta.subbarao@influenzacentre.org.
In vitro studies are an important part of preclinical research, however results may be very different in vivo.
Parallel use of human stem cell lung and heart models provide insights for SARS-CoV-2 treatment
Stem Cell Reports, doi:10.1016/j.stemcr.2023.05.007
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) primarily infects the respiratory tract, but pulmonary and cardiac complications occur in severe coronavirus disease 2019 . To elucidate molecular mechanisms in the lung and heart, we conducted paired experiments in human stem cell-derived lung alveolar type II (AT2) epithelial cell and cardiac cultures infected with SARS-CoV-2. With CRISPR-Cas9-mediated knockout of ACE2, we demonstrated that angiotensin-converting enzyme 2 (ACE2) was essential for SARS-CoV-2 infection of both cell types but that further processing in lung cells required TMPRSS2, while cardiac cells required the endosomal pathway. Host responses were significantly different; transcriptome profiling and phosphoproteomics responses depended strongly on the cell type. We identified several antiviral compounds with distinct antiviral and toxicity profiles in lung AT2 and cardiac cells, highlighting the importance of using several relevant cell types for evaluation of antiviral drugs. Our data provide new insights into rational drug combinations for effective treatment of a virus that affects multiple organ systems.
EXPERIMENTAL PROCEDURES
Resource availability Corresponding authors Enzo R. Porrello, Jose M. Polo, Sean J. Humphrey, Mirana Ramialison, David A. Elliott or Kanta Subbarao are the corresponding authors for this paper.
Cells African green monkey kidney epithelial (Vero cells, ATCC Cat. CCL-81), Vero hSLAM (Merck, Cat. 04091501), Calu-3 (ATCC, Cat. HTB-55), and VeroE6-TMPRSS2 (CellBank Australia, Cat. JCRB1819) cells were cultured at 37 C and 5% CO 2. Vero cell media: minimum essential medium (MEM; Media Preparation Unit, Peter Doherty Institute) supplemented with 5% fetal bovine serum (FBS; Bovogen, Cat. SFBS), 50 U/mL penicillin and 50 mg/mL streptomycin (PenStrep, Thermo Fisher Scientific, Cat. 15070-063), 2 mM GlutaMAX (Thermo Fisher Scientific, Cat. 35050061), and 15 mM HEPES (Thermo Fisher Scientific, Cat. 15630130) . Vero hSLAM cell media: MEM supplemented with 7% FBS, PenStrep, 2 mM GlutaMAX, 15 mM HEPES, and 0.4 mg/mL G418 Sulfate (Gibco, Cat. 10131027). Calu-3 cell media: MEM containing L-glutamine and sodium bicarbonate (Sigma, Cat. M4655) supplemented with 10% FBS, PenStrep, 13 non-essential amino acids (Gibco, Cat. 11140050), and sodium pyruvate (Fisher Scientific, Cat. BP356-100). VeroE6-TMPRSS2 cell media: Dulbecco's MEM (DMEM; Media Preparation Unit, Peter Doherty Institute) supplemented with 10% FBS, PenStrep, 2 mM GlutaMAX, and 1 mg/ mL G418 Sulfate. (Hou et al., 2020) . SARS-CoV-2 VIC01 was propagated in Vero and Vero hSLAM cells in Vero infection..
References
Anderson, Kaplan, Bell, Koutsis, Haynes et al., NKX2-5 regulates human cardiomyogenesis via a HEY2 dependent transcriptional network, Nat. Commun, doi:10.1038/s41467-018-03714-x
Bailey, Dmytrenko, Greenberg, Bredemeyer, Ma et al., SARS-CoV-2 infects human engineered heart tissues and models COVID-19 myocarditis, JACC Basic Transl Sci, doi:10.1016/j.jacbts.2021.01.002
Bojkova, Wagner, Shumliakivska, Aslan, Saleem et al., SARS-CoV-2 infects and induces cytotoxic effects in human cardiomyocytes, Cardiovasc. Res, doi:10.1093/cvr/cvaa267
Bouhaddou, Memon, Meyer, White, Rezelj et al., The global phosphorylation landscape of SARS-CoV-2 infection, Cell, doi:10.1016/j.cell.2020.06.034
Chen, Bobrovitz, Premji, Koopmans, Fisman et al., SARS-CoV-2 shedding dynamics across the respiratory tract, sex, and disease severity for adult and pediatric COVID-19, Elife, doi:10.7554/eLife.70458
Chen, Gao, Wang, Wei, An iTSCderived placental model of SARS-CoV-2 infection reveals ACE2-dependent susceptibility in syncytiotrophoblasts, bioRxiv, doi:10.1101/2021.10.27.465224
Deinhardt-Emmer, Wittschieber, Sanft, Kleemann, Elschner et al., Early postmortem mapping of SARS-CoV-2 RNA in patients with COVID-19 and the correlation with tissue damage, Elife, doi:10.7554/eLife.60361
Dobin, Davis, Schlesinger, Drenkow, Zaleski et al., STAR: ultrafast universal RNA-seq aligner, Bioinformatics, doi:10.1093/bioinformatics/bts635
Elliott, Braam, Koutsis, Ng, Jenny et al., NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes, Nat. Methods, doi:10.1038/nmeth.1740
Goyal, Choi, Pinheiro, Schenck, Chen et al., Clinical characteristics of Covid-19 in New York City, N. Engl. J. Med, doi:10.1056/NEJMc2010419
Gunst, Staerke, Pahus, Kristensen, Bodilsen et al., Efficacy of the TMPRSS2 inhibitor camostat mesilate in patients hospitalized with Covid-19-a double-blind randomized controlled trial, EClinicalMedicine, doi:10.1016/j.eclinm.2021.100849
Hamming, Timens, Bulthuis, Lely, Navis et al., Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis, J. Pathol, doi:10.1002/path.1570
Hoffmann, Kleine-Weber, Schroeder, Kru ¨ger, Herrler et al., SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor, Cell, doi:10.1016/j.cell.2020.05.042
Howe, Achuthan, Allen, Allen, Alvarez-Jarreta et al., Ensembl 2021, Nucleic Acids Res, doi:10.1093/nar/gkaa942
Huang, Hume, Abo, Werder, Villacorta-Martin et al., 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, doi:10.1016/j.stem.2020.09.013
Humphrey, Karayel, James, Mann, High-throughput and high-sensitivity phosphoproteomics with the EasyPhos platform, Nat. Protoc, doi:10.1038/s41596-018-0014-9
Jacob, Morley, Hawkins, Mccauley, Jean et al., Differentiation of human pluripotent stem cells into functional lung alveolar epithelial cells, Cell Stem Cell, doi:10.1016/j.stem.2017.08.014
Katsura, Sontake, Tata, Kobayashi, Edwards et al., Human lung stem cell-based alveolospheres provide insights into SARS-CoV-2-mediated interferon responses and pneumocyte dysfunction, Cell Stem Cell, doi:10.1016/j.stem.2020.10.005
Lazzerini, Laghi-Pasini, Boutjdir, Capecchi, Inflammatory cytokines and cardiac arrhythmias: the lesson from COVID-19, Nat. Rev. Immunol, doi:10.1038/s41577-022-00714-3
Lee, Huang, Rastegari, Rengganaten, Liu et al., Tumor necrosis factor-alpha exacerbates viral entry in SARS-CoV2-infected iPSC-derived cardiomyocytes, Int. J. Mol. Sci, doi:10.3390/ijms22189869
Lei, Dong, Ma, Wang, Xiao et al., Activation and evasion of type I interferon responses by SARS-CoV-2, Nat. Commun, doi:10.1038/s41467-020-17665-9
Li, Renner, Comar, Whelan, Reyes et al., SARS-CoV-2 induces double-stranded RNAmediated innate immune responses in respiratory epithelialderived cells and cardiomyocytes, doi:10.1073/pnas.2022643118
Liao, Smyth, Shi, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, doi:10.1093/bioinformatics/btt656
Lopes, Garcia-Herna ´ndez, Lorenzini, Futema, Chumakova et al., Alpha-protein kinase 3 (ALPK3) truncating variants are a cause of autosomal dominant hypertrophic cardiomyopathy, Eur. Heart J, doi:10.1093/eurheartj/ehab424
Marchiano, Hsiang, Khanna, Higashi, Whitmore et al., SARS-CoV-2 infects human pluripotent stem cellderived cardiomyocytes, impairing electrical and mechanical function, Stem Cell Rep, doi:10.1016/j.stemcr.2021.02.008
Mills, Titmarsh, Koenig, Parker, Ryall et al., Functional screening in human cardiac organoids reveals a metabolic mechanism for cardiomyocyte cell cycle arrest, Proc. Natl. Acad. Sci. USA, doi:10.1073/pnas.1707316114
Montaser, Lalmanach, Mach, CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells, Biol. Chem, doi:10.1515/BC.2002.147
Mulay, Konda, Garcia, Jr, Yao et al., SARS-CoV-2 infection of primary human lung epithelium for COVID-19 modeling and drug discovery, Cell Rep, doi:10.1016/j.celrep.2021.109055
Muus, Luecken, Eraslan, Sikkema, Waghray et al., Single-cell meta-analysis of SARS-CoV-2 entry genes across tissues and demographics, Nat. Med, doi:10.1038/s41591-020-01227-z
Nalbandian, Sehgal, Gupta, Madhavan, Mcgroder et al., Post-acute COVID-19 syndrome, Nat. Med, doi:10.1038/s41591-021-01283-z
Navaratnarajah, Pease, Halfmann, Taye, Barkhymer et al., Highly efficient SARS-CoV-2 infection of human cardiomyocytes: spike protein-mediated cell fusion and its inhibition, J. Virol, doi:10.1128/JVI.01368-21
Ou, Liu, Lei, Li, Mi et al., Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV, Nat. Commun, doi:10.1038/s41467-020-15562-9
Perez-Bermejo, Kang, Rockwood, Simoneau, Joy et al., SARS-CoV-2 infection of human iPSC-derived cardiac cells reflects cytopathic features in hearts of patients with COVID-19, Sci. Transl. Med, doi:10.1126/scitranslmed.abf7872
Phelan, Anderson, Howden, Wong, Hickey et al., ALPK3-deficient cardiomyocytes generated from patientderived induced pluripotent stem cells and mutant human embryonic stem cells display abnormal calcium handling and establish that ALPK3 deficiency underlies familial cardiomyopathy, Eur. Heart J, doi:10.1093/eurheartj/ehw160
Pruijssers, George, Scha ¨fer, Leist, Gralinksi et al., Remdesivir inhibits SARS-CoV-2 in human lung cells and chimeric SARS-CoV expressing the SARS-CoV-2 RNA polymerase in mice, Cell Rep, doi:10.1016/j.celrep.2020.107940
Puntmann, Carerj, Wieters, Fahim, Arendt et al., Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19), JAMA Cardiol, doi:10.1001/jamacardio.2020.3557
Qi, Qian, Zhang, Zhang, Single cell RNA sequencing of 13 human tissues identify cell types and receptors of human coronaviruses, Biochem. Biophys. Res. Commun, doi:10.1016/j.bbrc.2020.03.044
Robinson, Alkass, Bergmann, Maguire, Roderick et al., Genes encoding ACE2, TMPRSS2 and related proteins mediating SARS-CoV-2 viral entry are upregulated with age in human cardiomyocytes, J. Mol. Cell. Cardiol, doi:10.1016/j.yjmcc.2020.08.009
Robinson, Mccarthy, Smyth, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, doi:10.1093/bioinformatics/btp616
Sampaio, Chauveau, Hertzog, Bridgeman, Fowler et al., The RNA sensor MDA5 detects SARS-CoV-2 infection, Sci. Rep, doi:10.1038/s41598-021-92940-3
Schneider, Pease, Navaratnarajah, Halfmann, Clemens et al., SARS-CoV-2 direct cardiac damage through spike-mediated cardiomyocyte fusion
Shang, Wan, Luo, Ye, Geng et al., Cell entry mechanisms of SARS-CoV-2, Proc. Natl. Acad. Stem Cell Reports j
Shao, Shang, Luo, Shi, Zhao et al., Myocardial injury is associated with higher mortality in patients
Sharma, Garcia, Jr, Wang, Plummer et al., Human iPSCderived cardiomyocytes are susceptible to SARS-CoV-2 infection, Cell Rep. Med, doi:10.1016/j.xcrm.2020.100052
Shemesh, Aktepe, Deerain, Mcauley, Audsley et al., SARS-CoV-2 suppresses IFNbeta production mediated by NSP1, 5, 6, 15, ORF6 and ORF7b but does not suppress the effects of added interferon, PLoS Pathog, doi:10.1371/journal.ppat.1009800
Shi, Qin, Shen, Cai, Liu et al., Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, JAMA Cardiol, doi:10.1001/jamacardio.2020.0950
Sungnak, Huang, Be ´cavin, Berg, Queen et al., SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes, Nat. Med, doi:10.1038/s41591-020-0868-6
Tiwari, Wang, Smith, Carlin, Revealing tissue-specific SARS-CoV-2 infection and host responses using human stem cell-derived lung and cerebral organoids, Stem Cell Rep, doi:10.1016/j.stemcr.2021.02.005
Tohyama, Hattori, Sano, Hishiki, Nagahata et al., Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes, Cell Stem Cell, doi:10.1016/j.stem.2012.09.013
Uhle ´n, Fagerberg, Hallstro ¨m, Lindskog, Oksvold et al., Proteomics. Tissue-based map of the human proteome, Science, doi:10.1126/science.1260419
Wang, Mannan, Xiao, Abdulfatah, Qiao et al., Characterization of SARS-CoV-2 and host entry factors distribution in a COVID-19 autopsy series, Commun. Med. 1, doi:10.1038/s43856-021-00025-z
Williams, Colzani, Macrae, Robinson, Bloor et al., Human embryonic stem cell-derived cardiomyocyte platform screens inhibitors of SARS-CoV-2 infection, Commun. Biol, doi:10.1038/s42003-021-02453-y
Xia, Cao, Xie, Zhang, Chen et al., Evasion of type I interferon by SARS-CoV-2, Cell Rep, doi:10.1016/j.celrep.2020.108234
Yang, Chen, Zhou, Mediators of SARS-CoV-2 entry are preferentially enriched in cardiomyocytes, Hereditas, doi:10.1186/s41065-020-00168-4
Yaron, Heaton, Levy, Johnson, Jordan et al., The FDA-approved drug Alectinib compromises SARS-CoV-2 nucleocapsid phosphorylation and inhibits viral infection in vitro, bioRxiv, doi:10.1101/2020.08.14.251207
Youk, Kim, Evans, Jeong, Hur et al., Three-dimensional human alveolar stem cell culture models reveal infection response to SARS-CoV-2, Cell Stem Cell, doi:10.1016/j.stem.2020.10.004
Zhang, Bastard, Liu, Le Pen, Moncada-Velez et al., Inborn errors of type I IFN immunity in patients with life-threatening COVID-19, Science, doi:10.1126/science.abd4570
Zhou, Yang, Wang, Hu, Zhang et al., Addendum: a pneumonia outbreak associated with a new coronavirus of probable bat origin, Nature, doi:10.1038/s41586-020-2951-z
Zhou, Zhou, Pache, Chang, Khodabakhshi et al., Metascape provides a biologist-oriented resource for the analysis of systems-level datasets, Nat. Commun, doi:10.1038/s41467-019-09234-6
Zou, Chen, Zou, Han, Hao et al., Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection, Front. Med, doi:10.1007/s11684-020-0754-0
DOI record:
{
"DOI": "10.1016/j.stemcr.2023.05.007",
"ISSN": [
"2213-6711"
],
"URL": "http://dx.doi.org/10.1016/j.stemcr.2023.05.007",
"alternative-id": [
"S2213671123001856"
],
"assertion": [
{
"label": "This article is maintained by",
"name": "publisher",
"value": "Elsevier"
},
{
"label": "Article Title",
"name": "articletitle",
"value": "Parallel use of human stem cell lung and heart models provide insights for SARS-CoV-2 treatment"
},
{
"label": "Journal Title",
"name": "journaltitle",
"value": "Stem Cell Reports"
},
{
"label": "CrossRef DOI link to publisher maintained version",
"name": "articlelink",
"value": "https://doi.org/10.1016/j.stemcr.2023.05.007"
},
{
"label": "Content Type",
"name": "content_type",
"value": "article"
},
{
"label": "Copyright",
"name": "copyright",
"value": "© 2023 The Authors."
}
],
"author": [
{
"affiliation": [],
"family": "Rudraraju",
"given": "Rajeev",
"sequence": "first"
},
{
"affiliation": [],
"family": "Gartner",
"given": "Matthew J.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Neil",
"given": "Jessica A.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Stout",
"given": "Elizabeth S.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Chen",
"given": "Joseph",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Needham",
"given": "Elise J.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "See",
"given": "Michael",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Mackenzie-Kludas",
"given": "Charley",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Yang Lee",
"given": "Leo Yi",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Wang",
"given": "Mingyang",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Pointer",
"given": "Hayley",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Karavendzas",
"given": "Kathy",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Abu-Bonsrah",
"given": "Dad",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Drew",
"given": "Damien",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Yang Sun",
"given": "Yu Bo",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Tan",
"given": "Jia Ping",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Sun",
"given": "Guizhi",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Salavaty",
"given": "Abbas",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Charitakis",
"given": "Natalie",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Nim",
"given": "Hieu T.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Currie",
"given": "Peter D.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Tham",
"given": "Wai-Hong",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Porrello",
"given": "Enzo",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Polo",
"given": "Jose M.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Humphrey",
"given": "Sean J.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Ramialison",
"given": "Mirana",
"sequence": "additional"
},
{
"ORCID": "http://orcid.org/0000-0003-1052-7407",
"affiliation": [],
"authenticated-orcid": false,
"family": "Elliott",
"given": "David A.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Subbarao",
"given": "Kanta",
"sequence": "additional"
}
],
"container-title": "Stem Cell Reports",
"container-title-short": "Stem Cell Reports",
"content-domain": {
"crossmark-restriction": true,
"domain": [
"cell.com",
"elsevier.com",
"sciencedirect.com"
]
},
"created": {
"date-parts": [
[
2023,
6,
13
]
],
"date-time": "2023-06-13T14:50:01Z",
"timestamp": 1686667801000
},
"deposited": {
"date-parts": [
[
2023,
6,
16
]
],
"date-time": "2023-06-16T21:43:53Z",
"timestamp": 1686951833000
},
"indexed": {
"date-parts": [
[
2023,
6,
17
]
],
"date-time": "2023-06-17T04:22:28Z",
"timestamp": 1686975748920
},
"is-referenced-by-count": 0,
"issue": "6",
"issued": {
"date-parts": [
[
2023,
6
]
]
},
"journal-issue": {
"issue": "6",
"published-print": {
"date-parts": [
[
2023,
6
]
]
}
},
"language": "en",
"license": [
{
"URL": "https://www.elsevier.com/tdm/userlicense/1.0/",
"content-version": "tdm",
"delay-in-days": 0,
"start": {
"date-parts": [
[
2023,
6,
1
]
],
"date-time": "2023-06-01T00:00:00Z",
"timestamp": 1685577600000
}
},
{
"URL": "http://creativecommons.org/licenses/by-nc-nd/4.0/",
"content-version": "vor",
"delay-in-days": 0,
"start": {
"date-parts": [
[
2023,
5,
11
]
],
"date-time": "2023-05-11T00:00:00Z",
"timestamp": 1683763200000
}
}
],
"link": [
{
"URL": "https://api.elsevier.com/content/article/PII:S2213671123001856?httpAccept=text/xml",
"content-type": "text/xml",
"content-version": "vor",
"intended-application": "text-mining"
},
{
"URL": "https://api.elsevier.com/content/article/PII:S2213671123001856?httpAccept=text/plain",
"content-type": "text/plain",
"content-version": "vor",
"intended-application": "text-mining"
}
],
"member": "78",
"original-title": [],
"page": "1308-1324",
"prefix": "10.1016",
"published": {
"date-parts": [
[
2023,
6
]
]
},
"published-print": {
"date-parts": [
[
2023,
6
]
]
},
"publisher": "Elsevier BV",
"reference": [
{
"DOI": "10.1038/s41467-018-03714-x",
"article-title": "NKX2-5 regulates human cardiomyogenesis via a HEY2 dependent transcriptional network",
"author": "Anderson",
"doi-asserted-by": "crossref",
"first-page": "1373",
"journal-title": "Nat. Commun.",
"key": "10.1016/j.stemcr.2023.05.007_bib1",
"volume": "9",
"year": "2018"
},
{
"DOI": "10.1016/j.jacbts.2021.01.002",
"article-title": "SARS-CoV-2 infects human engineered heart tissues and models COVID-19 myocarditis",
"author": "Bailey",
"doi-asserted-by": "crossref",
"first-page": "331",
"journal-title": "JACC Basic Transl Sci",
"key": "10.1016/j.stemcr.2023.05.007_bib2",
"volume": "6",
"year": "2021"
},
{
"DOI": "10.1093/cvr/cvaa267",
"article-title": "SARS-CoV-2 infects and induces cytotoxic effects in human cardiomyocytes",
"author": "Bojkova",
"doi-asserted-by": "crossref",
"first-page": "2207",
"journal-title": "Cardiovasc. Res.",
"key": "10.1016/j.stemcr.2023.05.007_bib3",
"volume": "116",
"year": "2020"
},
{
"DOI": "10.1016/j.cell.2020.06.034",
"article-title": "The global phosphorylation landscape of SARS-CoV-2 infection",
"author": "Bouhaddou",
"doi-asserted-by": "crossref",
"first-page": "685",
"journal-title": "Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib4",
"volume": "182",
"year": "2020"
},
{
"article-title": "An iTSC-derived placental model of SARS-CoV-2 infection reveals ACE2-dependent susceptibility in syncytiotrophoblasts",
"author": "Chen",
"journal-title": "bioRxiv",
"key": "10.1016/j.stemcr.2023.05.007_bib5",
"year": "2021"
},
{
"DOI": "10.7554/eLife.70458",
"article-title": "SARS-CoV-2 shedding dynamics across the respiratory tract, sex, and disease severity for adult and pediatric COVID-19",
"author": "Chen",
"doi-asserted-by": "crossref",
"first-page": "e70458",
"journal-title": "Elife",
"key": "10.1016/j.stemcr.2023.05.007_bib6",
"volume": "10",
"year": "2021"
},
{
"DOI": "10.7554/eLife.60361",
"article-title": "Early postmortem mapping of SARS-CoV-2 RNA in patients with COVID-19 and the correlation with tissue damage",
"author": "Deinhardt-Emmer",
"doi-asserted-by": "crossref",
"first-page": "e60361",
"journal-title": "Elife",
"key": "10.1016/j.stemcr.2023.05.007_bib7",
"volume": "10",
"year": "2021"
},
{
"DOI": "10.1093/bioinformatics/bts635",
"article-title": "STAR: ultrafast universal RNA-seq aligner",
"author": "Dobin",
"doi-asserted-by": "crossref",
"first-page": "15",
"journal-title": "Bioinformatics",
"key": "10.1016/j.stemcr.2023.05.007_bib8",
"volume": "29",
"year": "2013"
},
{
"DOI": "10.1038/nmeth.1740",
"article-title": "NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes",
"author": "Elliott",
"doi-asserted-by": "crossref",
"first-page": "1037",
"journal-title": "Nat. Methods",
"key": "10.1016/j.stemcr.2023.05.007_bib9",
"volume": "8",
"year": "2011"
},
{
"DOI": "10.1056/NEJMc2010419",
"article-title": "Clinical characteristics of Covid-19 in New York City",
"author": "Goyal",
"doi-asserted-by": "crossref",
"first-page": "2372",
"journal-title": "N. Engl. J. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib10",
"volume": "382",
"year": "2020"
},
{
"DOI": "10.1016/j.eclinm.2021.100849",
"article-title": "Efficacy of the TMPRSS2 inhibitor camostat mesilate in patients hospitalized with Covid-19-a double-blind randomized controlled trial",
"author": "Gunst",
"doi-asserted-by": "crossref",
"first-page": "100849",
"journal-title": "EClinicalMedicine",
"key": "10.1016/j.stemcr.2023.05.007_bib11",
"volume": "35",
"year": "2021"
},
{
"DOI": "10.1002/path.1570",
"article-title": "Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis",
"author": "Hamming",
"doi-asserted-by": "crossref",
"first-page": "631",
"journal-title": "J. Pathol.",
"key": "10.1016/j.stemcr.2023.05.007_bib12",
"volume": "203",
"year": "2004"
},
{
"DOI": "10.1016/j.cell.2020.02.052",
"article-title": "SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor",
"author": "Hoffmann",
"doi-asserted-by": "crossref",
"first-page": "271",
"journal-title": "Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib13",
"volume": "181",
"year": "2020"
},
{
"DOI": "10.1016/j.cell.2020.05.042",
"article-title": "SARS-CoV-2 reverse genetics reveals a variable infection gradient in the respiratory tract",
"author": "Hou",
"doi-asserted-by": "crossref",
"first-page": "429",
"journal-title": "Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib14",
"volume": "182",
"year": "2020"
},
{
"DOI": "10.1093/nar/gkaa942",
"article-title": "Ensembl 2021",
"author": "Howe",
"doi-asserted-by": "crossref",
"first-page": "D884",
"journal-title": "Nucleic Acids Res.",
"key": "10.1016/j.stemcr.2023.05.007_bib15",
"volume": "49",
"year": "2021"
},
{
"DOI": "10.1016/j.stem.2020.09.013",
"article-title": "SARS-CoV-2 infection of pluripotent stem cell-derived human lung alveolar type 2 cells elicits a rapid epithelial-intrinsic inflammatory response",
"author": "Huang",
"doi-asserted-by": "crossref",
"first-page": "962",
"journal-title": "Cell Stem Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib16",
"volume": "27",
"year": "2020"
},
{
"DOI": "10.1038/s41596-018-0014-9",
"article-title": "High-throughput and high-sensitivity phosphoproteomics with the EasyPhos platform",
"author": "Humphrey",
"doi-asserted-by": "crossref",
"first-page": "1897",
"journal-title": "Nat. Protoc.",
"key": "10.1016/j.stemcr.2023.05.007_bib17",
"volume": "13",
"year": "2018"
},
{
"DOI": "10.1016/j.stem.2017.08.014",
"article-title": "Differentiation of human pluripotent stem cells into functional lung alveolar epithelial cells",
"author": "Jacob",
"doi-asserted-by": "crossref",
"first-page": "472",
"journal-title": "Cell Stem Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib18",
"volume": "21",
"year": "2017"
},
{
"DOI": "10.1016/j.stem.2020.10.005",
"article-title": "Human lung stem cell-based alveolospheres provide insights into SARS-CoV-2-mediated interferon responses and pneumocyte dysfunction",
"author": "Katsura",
"doi-asserted-by": "crossref",
"first-page": "890",
"journal-title": "Cell Stem Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib19",
"volume": "27",
"year": "2020"
},
{
"DOI": "10.1038/s41577-022-00714-3",
"article-title": "Inflammatory cytokines and cardiac arrhythmias: the lesson from COVID-19",
"author": "Lazzerini",
"doi-asserted-by": "crossref",
"first-page": "270",
"journal-title": "Nat. Rev. Immunol.",
"key": "10.1016/j.stemcr.2023.05.007_bib20",
"volume": "22",
"year": "2022"
},
{
"DOI": "10.3390/ijms22189869",
"article-title": "Tumor necrosis factor-alpha exacerbates viral entry in SARS-CoV2-infected iPSC-derived cardiomyocytes",
"author": "Lee",
"doi-asserted-by": "crossref",
"first-page": "9869",
"journal-title": "Int. J. Mol. Sci.",
"key": "10.1016/j.stemcr.2023.05.007_bib21",
"volume": "22",
"year": "2021"
},
{
"DOI": "10.1038/s41467-020-17665-9",
"article-title": "Activation and evasion of type I interferon responses by SARS-CoV-2",
"author": "Lei",
"doi-asserted-by": "crossref",
"first-page": "3810",
"journal-title": "Nat. Commun.",
"key": "10.1016/j.stemcr.2023.05.007_bib22",
"volume": "11",
"year": "2020"
},
{
"article-title": "SARS-CoV-2 induces double-stranded RNA-mediated innate immune responses in respiratory epithelial-derived cells and cardiomyocytes",
"author": "Li",
"journal-title": "Proc. Natl. Acad. Sci. USA",
"key": "10.1016/j.stemcr.2023.05.007_bib23",
"volume": "118",
"year": "2021"
},
{
"DOI": "10.1093/bioinformatics/btt656",
"article-title": "featureCounts: an efficient general purpose program for assigning sequence reads to genomic features",
"author": "Liao",
"doi-asserted-by": "crossref",
"first-page": "923",
"journal-title": "Bioinformatics",
"key": "10.1016/j.stemcr.2023.05.007_bib24",
"volume": "30",
"year": "2014"
},
{
"DOI": "10.1093/eurheartj/ehab424",
"article-title": "Alpha-protein kinase 3 (ALPK3) truncating variants are a cause of autosomal dominant hypertrophic cardiomyopathy",
"author": "Lopes",
"doi-asserted-by": "crossref",
"first-page": "3063",
"journal-title": "Eur. Heart J.",
"key": "10.1016/j.stemcr.2023.05.007_bib25",
"volume": "42",
"year": "2021"
},
{
"DOI": "10.1016/j.stemcr.2021.02.008",
"article-title": "SARS-CoV-2 infects human pluripotent stem cell-derived cardiomyocytes, impairing electrical and mechanical function",
"author": "Marchiano",
"doi-asserted-by": "crossref",
"first-page": "478",
"journal-title": "Stem Cell Rep.",
"key": "10.1016/j.stemcr.2023.05.007_bib26",
"volume": "16",
"year": "2021"
},
{
"DOI": "10.1073/pnas.1707316114",
"article-title": "Functional screening in human cardiac organoids reveals a metabolic mechanism for cardiomyocyte cell cycle arrest",
"author": "Mills",
"doi-asserted-by": "crossref",
"first-page": "E8372",
"journal-title": "Proc. Natl. Acad. Sci. USA",
"key": "10.1016/j.stemcr.2023.05.007_bib27",
"volume": "114",
"year": "2017"
},
{
"DOI": "10.1515/BC.2002.147",
"article-title": "CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells",
"author": "Montaser",
"doi-asserted-by": "crossref",
"first-page": "1305",
"journal-title": "Biol. Chem.",
"key": "10.1016/j.stemcr.2023.05.007_bib28",
"volume": "383",
"year": "2002"
},
{
"DOI": "10.1016/j.celrep.2021.109055",
"article-title": "SARS-CoV-2 infection of primary human lung epithelium for COVID-19 modeling and drug discovery",
"author": "Mulay",
"doi-asserted-by": "crossref",
"first-page": "109055",
"journal-title": "Cell Rep.",
"key": "10.1016/j.stemcr.2023.05.007_bib29",
"volume": "35",
"year": "2021"
},
{
"DOI": "10.1038/s41591-020-01227-z",
"article-title": "Single-cell meta-analysis of SARS-CoV-2 entry genes across tissues and demographics",
"author": "Muus",
"doi-asserted-by": "crossref",
"first-page": "546",
"journal-title": "Nat. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib30",
"volume": "27",
"year": "2021"
},
{
"DOI": "10.1038/s41591-021-01283-z",
"article-title": "Post-acute COVID-19 syndrome",
"author": "Nalbandian",
"doi-asserted-by": "crossref",
"first-page": "601",
"journal-title": "Nat. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib31",
"volume": "27",
"year": "2021"
},
{
"DOI": "10.1128/JVI.01368-21",
"article-title": "Highly efficient SARS-CoV-2 infection of human cardiomyocytes: spike protein-mediated cell fusion and its inhibition",
"author": "Navaratnarajah",
"doi-asserted-by": "crossref",
"first-page": "e0136821",
"journal-title": "J. Virol.",
"key": "10.1016/j.stemcr.2023.05.007_bib32",
"volume": "95",
"year": "2021"
},
{
"DOI": "10.1038/s41467-020-15562-9",
"article-title": "Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV",
"author": "Ou",
"doi-asserted-by": "crossref",
"first-page": "1620",
"journal-title": "Nat. Commun.",
"key": "10.1016/j.stemcr.2023.05.007_bib33",
"volume": "11",
"year": "2020"
},
{
"DOI": "10.1126/scitranslmed.abf7872",
"article-title": "SARS-CoV-2 infection of human iPSC-derived cardiac cells reflects cytopathic features in hearts of patients with COVID-19",
"author": "Perez-Bermejo",
"doi-asserted-by": "crossref",
"first-page": "eabf7872",
"journal-title": "Sci. Transl. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib34",
"volume": "13",
"year": "2021"
},
{
"DOI": "10.1093/eurheartj/ehw160",
"article-title": "ALPK3-deficient cardiomyocytes generated from patient-derived induced pluripotent stem cells and mutant human embryonic stem cells display abnormal calcium handling and establish that ALPK3 deficiency underlies familial cardiomyopathy",
"author": "Phelan",
"doi-asserted-by": "crossref",
"first-page": "2586",
"journal-title": "Eur. Heart J.",
"key": "10.1016/j.stemcr.2023.05.007_bib35",
"volume": "37",
"year": "2016"
},
{
"DOI": "10.1016/j.celrep.2020.107940",
"article-title": "Remdesivir inhibits SARS-CoV-2 in human lung cells and chimeric SARS-CoV expressing the SARS-CoV-2 RNA polymerase in mice",
"author": "Pruijssers",
"doi-asserted-by": "crossref",
"first-page": "107940",
"journal-title": "Cell Rep.",
"key": "10.1016/j.stemcr.2023.05.007_bib36",
"volume": "32",
"year": "2020"
},
{
"DOI": "10.1001/jamacardio.2020.3557",
"article-title": "Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19)",
"author": "Puntmann",
"doi-asserted-by": "crossref",
"first-page": "1265",
"journal-title": "JAMA Cardiol.",
"key": "10.1016/j.stemcr.2023.05.007_bib37",
"volume": "5",
"year": "2020"
},
{
"DOI": "10.1016/j.bbrc.2020.03.044",
"article-title": "Single cell RNA sequencing of 13 human tissues identify cell types and receptors of human coronaviruses",
"author": "Qi",
"doi-asserted-by": "crossref",
"first-page": "135",
"journal-title": "Biochem. Biophys. Res. Commun.",
"key": "10.1016/j.stemcr.2023.05.007_bib38",
"volume": "526",
"year": "2020"
},
{
"DOI": "10.1016/j.yjmcc.2020.08.009",
"article-title": "Genes encoding ACE2, TMPRSS2 and related proteins mediating SARS-CoV-2 viral entry are upregulated with age in human cardiomyocytes",
"author": "Robinson",
"doi-asserted-by": "crossref",
"first-page": "88",
"journal-title": "J. Mol. Cell. Cardiol.",
"key": "10.1016/j.stemcr.2023.05.007_bib39",
"volume": "147",
"year": "2020"
},
{
"DOI": "10.1093/bioinformatics/btp616",
"article-title": "edgeR: a Bioconductor package for differential expression analysis of digital gene expression data",
"author": "Robinson",
"doi-asserted-by": "crossref",
"first-page": "139",
"journal-title": "Bioinformatics",
"key": "10.1016/j.stemcr.2023.05.007_bib40",
"volume": "26",
"year": "2010"
},
{
"DOI": "10.1038/s41598-021-92940-3",
"article-title": "The RNA sensor MDA5 detects SARS-CoV-2 infection",
"author": "Sampaio",
"doi-asserted-by": "crossref",
"first-page": "13638",
"journal-title": "Sci. Rep.",
"key": "10.1016/j.stemcr.2023.05.007_bib41",
"volume": "11",
"year": "2021"
},
{
"article-title": "SARS-CoV-2 direct cardiac damage through spike-mediated cardiomyocyte fusion",
"author": "Schneider",
"journal-title": "Research Square",
"key": "10.1016/j.stemcr.2023.05.007_bib42",
"year": "2020"
},
{
"DOI": "10.1073/pnas.2003138117",
"article-title": "Cell entry mechanisms of SARS-CoV-2",
"author": "Shang",
"doi-asserted-by": "crossref",
"first-page": "11727",
"journal-title": "Proc. Natl. Acad. Sci. USA",
"key": "10.1016/j.stemcr.2023.05.007_bib43",
"volume": "117",
"year": "2020"
},
{
"article-title": "Myocardial injury is associated with higher mortality in patients with coronavirus disease 2019: a meta-analysis",
"author": "Shao",
"first-page": "224",
"journal-title": "J. Geriatr. Cardiol.",
"key": "10.1016/j.stemcr.2023.05.007_bib44",
"volume": "17",
"year": "2020"
},
{
"DOI": "10.1016/j.xcrm.2020.100052",
"article-title": "Human iPSC-derived cardiomyocytes are susceptible to SARS-CoV-2 infection",
"author": "Sharma",
"doi-asserted-by": "crossref",
"first-page": "100052",
"journal-title": "Cell Rep. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib45",
"volume": "1",
"year": "2020"
},
{
"DOI": "10.1371/journal.ppat.1009800",
"article-title": "SARS-CoV-2 suppresses IFNbeta production mediated by NSP1, 5, 6, 15, ORF6 and ORF7b but does not suppress the effects of added interferon",
"author": "Shemesh",
"doi-asserted-by": "crossref",
"first-page": "e1009800",
"journal-title": "PLoS Pathog.",
"key": "10.1016/j.stemcr.2023.05.007_bib46",
"volume": "17",
"year": "2021"
},
{
"DOI": "10.1001/jamacardio.2020.0950",
"article-title": "Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China",
"author": "Shi",
"doi-asserted-by": "crossref",
"first-page": "802",
"journal-title": "JAMA Cardiol.",
"key": "10.1016/j.stemcr.2023.05.007_bib47",
"volume": "5",
"year": "2020"
},
{
"DOI": "10.1038/s41591-020-0868-6",
"article-title": "SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes",
"author": "Sungnak",
"doi-asserted-by": "crossref",
"first-page": "681",
"journal-title": "Nat. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib48",
"volume": "26",
"year": "2020"
},
{
"DOI": "10.1016/j.stemcr.2021.02.005",
"article-title": "Revealing tissue-specific SARS-CoV-2 infection and host responses using human stem cell-derived lung and cerebral organoids",
"author": "Tiwari",
"doi-asserted-by": "crossref",
"first-page": "437",
"journal-title": "Stem Cell Rep.",
"key": "10.1016/j.stemcr.2023.05.007_bib49",
"volume": "16",
"year": "2021"
},
{
"DOI": "10.1016/j.stem.2012.09.013",
"article-title": "Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes",
"author": "Tohyama",
"doi-asserted-by": "crossref",
"first-page": "127",
"journal-title": "Cell Stem Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib50",
"volume": "12",
"year": "2013"
},
{
"DOI": "10.1126/science.1260419",
"article-title": "Proteomics. Tissue-based map of the human proteome",
"author": "Uhlén",
"doi-asserted-by": "crossref",
"first-page": "1260419",
"journal-title": "Science",
"key": "10.1016/j.stemcr.2023.05.007_bib51",
"volume": "347",
"year": "2015"
},
{
"DOI": "10.1038/s43856-021-00025-z",
"article-title": "Characterization of SARS-CoV-2 and host entry factors distribution in a COVID-19 autopsy series",
"author": "Wang",
"doi-asserted-by": "crossref",
"first-page": "24",
"journal-title": "Commun. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib52",
"volume": "1",
"year": "2021"
},
{
"DOI": "10.1038/s42003-021-02453-y",
"article-title": "Human embryonic stem cell-derived cardiomyocyte platform screens inhibitors of SARS-CoV-2 infection",
"author": "Williams",
"doi-asserted-by": "crossref",
"first-page": "926",
"journal-title": "Commun. Biol.",
"key": "10.1016/j.stemcr.2023.05.007_bib53",
"volume": "4",
"year": "2021"
},
{
"DOI": "10.1016/j.celrep.2020.108234",
"article-title": "Evasion of type I interferon by SARS-CoV-2",
"author": "Xia",
"doi-asserted-by": "crossref",
"first-page": "108234",
"journal-title": "Cell Rep.",
"key": "10.1016/j.stemcr.2023.05.007_bib54",
"volume": "33",
"year": "2020"
},
{
"DOI": "10.1186/s41065-020-00168-4",
"article-title": "Mediators of SARS-CoV-2 entry are preferentially enriched in cardiomyocytes",
"author": "Yang",
"doi-asserted-by": "crossref",
"first-page": "4",
"journal-title": "Hereditas",
"key": "10.1016/j.stemcr.2023.05.007_bib55",
"volume": "158",
"year": "2021"
},
{
"article-title": "The FDA-approved drug Alectinib compromises SARS-CoV-2 nucleocapsid phosphorylation and inhibits viral infection in vitro",
"author": "Yaron",
"journal-title": "bioRxiv",
"key": "10.1016/j.stemcr.2023.05.007_bib56",
"year": "2020"
},
{
"DOI": "10.1016/j.stem.2020.10.004",
"article-title": "Three-dimensional human alveolar stem cell culture models reveal infection response to SARS-CoV-2",
"author": "Youk",
"doi-asserted-by": "crossref",
"first-page": "905",
"journal-title": "Cell Stem Cell",
"key": "10.1016/j.stemcr.2023.05.007_bib57",
"volume": "27",
"year": "2020"
},
{
"DOI": "10.1126/science.abd4570",
"article-title": "Inborn errors of type I IFN immunity in patients with life-threatening COVID-19",
"author": "Zhang",
"doi-asserted-by": "crossref",
"first-page": "eabd4570",
"journal-title": "Science",
"key": "10.1016/j.stemcr.2023.05.007_bib58",
"volume": "370",
"year": "2020"
},
{
"DOI": "10.1038/s41586-020-2951-z",
"article-title": "Addendum: a pneumonia outbreak associated with a new coronavirus of probable bat origin",
"author": "Zhou",
"doi-asserted-by": "crossref",
"first-page": "E6",
"journal-title": "Nature",
"key": "10.1016/j.stemcr.2023.05.007_bib59",
"volume": "588",
"year": "2020"
},
{
"DOI": "10.1038/s41467-019-09234-6",
"article-title": "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets",
"author": "Zhou",
"doi-asserted-by": "crossref",
"first-page": "1523",
"journal-title": "Nat. Commun.",
"key": "10.1016/j.stemcr.2023.05.007_bib60",
"volume": "10",
"year": "2019"
},
{
"DOI": "10.1007/s11684-020-0754-0",
"article-title": "Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection",
"author": "Zou",
"doi-asserted-by": "crossref",
"first-page": "185",
"journal-title": "Front. Med.",
"key": "10.1016/j.stemcr.2023.05.007_bib61",
"volume": "14",
"year": "2020"
}
],
"reference-count": 61,
"references-count": 61,
"relation": {},
"resource": {
"primary": {
"URL": "https://linkinghub.elsevier.com/retrieve/pii/S2213671123001856"
}
},
"score": 1,
"short-title": [],
"source": "Crossref",
"subject": [
"Cell Biology",
"Developmental Biology",
"Genetics",
"Biochemistry"
],
"subtitle": [],
"title": "Parallel use of human stem cell lung and heart models provide insights for SARS-CoV-2 treatment",
"type": "journal-article",
"update-policy": "http://dx.doi.org/10.1016/elsevier_cm_policy",
"volume": "18"
}