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Cited by 2,838SARS-CoV-2 and COVID-19 ResearchDental Research and COVID-19Dermatological and COVID-19 studies

High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa

Open access
Xu, Hao, Zhong, Liang, Deng, Jiaxin, Peng, Jiakuan, Dan, Hongxia, Zeng, Xin, Li, Taiwen, Chen, Qianming·2020·International Journal of Oral Science
DOI 10.1038/s41368-020-0074-xPMC PMC7039956
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Abstract

It has been reported that ACE2 is the main host cell receptor of 2019-nCoV and plays a crucial role in the entry of virus into the cell to cause the final infection. To investigate the potential route of 2019-nCov infection on the mucosa of oral cavity, bulk RNA-seq profiles from two public databases including The Cancer Genome Atlas (TCGA) and Functional Annotation of The Mammalian Genome Cap Analysis of Gene Expression (FANTOM5 CAGE) dataset were collected. RNA-seq profiling data of 13 organ types with para-carcinoma normal tissues from TCGA and 14 organ types with normal tissues from FANTOM5 CAGE were analyzed in order to explore and validate the expression of ACE2 on the mucosa of oral cavity. Further, single-cell transcriptomes from an independent data generated in-house were used to identify and confirm the ACE2-expressing cell composition and proportion in oral cavity. The results demonstrated that the ACE2 expressed on the mucosa of oral cavity. Interestingly, this receptor was highly enriched in epithelial cells of tongue. Preliminarily, those findings have explained the basic mechanism that the oral cavity is a potentially high risk for 2019-nCoV infectious susceptibility and provided a piece of evidence for the future prevention strategy in dental clinical practice as well as daily life.

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  3. Reference list26 references found
  4. Reference check27 of 27 references checked
  5. StatisticsRecomputed
  6. Claims33 claims anchored to a quote
  7. Cited sourcesChecked
  8. Self-checkDidn’t finish — the rest of the report still applies.
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Crossref · 10.1038/s41368-020-0074-x

Cites

27 of 27 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 23 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The mucosa of the oral cavity expresses ACE2.

    “The results demonstrated that the ACE2 expressed on the mucosa of oral cavity.”
    • Also stated in: § Public bulk RNA-seq dataset analysis · hedged
      “According to the mean expression of ACE2, the mucosa of oral cavity could express ACE2, and the results were validated by the data of normal tissues from the FANTOM5 CAGE dataset (Fig. 1b).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Public TCGA para-carcinoma normal tissues and FANTOM5 normal tissues are adequate proxies for normal oral mucosa.
    • Rests on an assumption: The FANTOM5 CAGE dataset with only two tongue samples can validate ACE2 expression in the oral cavity.
  • Findingown data

    ACE2 can be expressed in various organs according to TCGA bulk RNA-seq.

    “Fig. 1a showed that ACE2 could be expressed in various organs, the mean expression of different organs could be found in Table 1.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Public TCGA para-carcinoma normal tissues and FANTOM5 normal tissues are adequate proxies for normal oral mucosa.
  • Interpretationown data

    The oral cavity is a potentially high-risk site for 2019-nCoV infectious susceptibility.

    “These findings indicated that oral cavity could be regarded as potentially high risk for 2019-nCov infectious susceptibility.”
    • Also stated in: § Abstract · hedged
      “Preliminarily, those findings have explained the basic mechanism that the oral cavity is a potentially high risk for 2019-nCoV infectious susceptibility”
    Quote in the paperSubstantial claim
    • Rests on an assumption: ACE2 RNA expression levels in tissues indicate the presence of functional ACE2 receptor protein and susceptibility to 2019-nCoV infection.
  • Study design and conductcitation

    The in-house tissues came from a previous project that found no significant expression difference among common epithelial markers in past and other studies.

    “which from our previous project found no significant expression difference among the common epithelial markers in our past study and other previous study22–24.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [22] Dionne, K. R., Warnakulasuriya, S., Zain, R. B. & Cheong, S. C. Potentially malignant disorders of the oral cavity: current practice and future directions in the clinic and laboratory. Int. J. Cancer 136, 503–515 (2015). source

      Not checked in the free run.

    • cites [23] Li, J. et al. Associations between proteasomal activator PA28γ and outcome of oral squamous cell carcinoma: evidence from cohort studies and functional analyses. EBioMedicine 2, 851–858 (2015). source

      Not checked in the free run.

    • cites [24] Wang, Z. et al. RACK1, an excellent predictor for poor clinical outcome in oral squamous carcinoma, similar to Ki67. Eur. J. Cancer 45, 490–496 (2009). source

      Not checked in the free run.

  • Interpretationcitation

    The relatively low ACE2 expression of lung in bulk RNA-seq datasets may be because ACE2 expression in lung is concentrated in a small population of type II alveolar cells.

    “According to the study of Zhao et al.11, the ACE2 expression in lung is concentrated in a small population of type II alveolar cells (AT2), that may cause the relatively low ACE2 expression of lung in bulk-seq RNA datasets analysis.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Zhao et al.11 Zhao, Y. et al. Single-cell RNA expression profiling of ACE2, the putative receptor of Wuhan 2019-nCov. Preprint at https://www.biorxiv.org/content/10.1101/2020.01.26.919985v1 (2020).

      Not checked in the free run.

  • May combine two claims. 18
  • The quote only partly states this claim. 2
  • Classified as probably not a substantial claim. 10

  • May combine two claims.

    Findingown data

    ACE2 expression is higher in oral tongue than in buccal and gingival tissues, with 95.86% of ACE2-positive cells located in oral tongue.

    “and higher in oral tongue than buccal and gingival tissues (95.86% ACE2-positive cells located in oral tongue).”
    • Also stated in: § Discussion · boosted
      “The results of our single cell RNA-seq profiles validated the ACE2 expression in oral cavity, and the level of ACE2 expression in oral tissues was higher in tongue than buccal or gingival tissues.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The four in-house oral tissue samples are representative of normal oral mucosa and of the oral cavity generally.

  • May combine two claims. The quote only partly states this claim.

    Findingown data

    ACE2 is highly enriched in epithelial cells, with 93.38% of ACE2-positive cells belonging to epithelial cells.

    “and the ACE2 was highly enriched in epithelial cells, of which 93.38% ACE2-positive cells belong to epithelial cells (Fig. 2f).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The four in-house oral tissue samples are representative of normal oral mucosa and of the oral cavity generally.

  • May combine two claims.

    Findingown data

    ACE2-positive cells in oral tissues include epithelial cells (1.19%), T cells (<0.5%), B cells (<0.5%), and fibroblasts (<0.5%).

    “Figure 2e shows that the ACE2-positive cells could be found in oral tissues including epithelial cells (1.19% ACE2-positive cells), T cells (<0.5%), B cells (<0.5%), and fibroblast (<0.5%)”
    • Also stated in: § Discussion · plain
      “Interestingly, we found that the ACE2 also expressed in lymphocytes within oral mucosa, and similar results were found in various organs of the digestive system and in lungs11,12.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The four in-house oral tissue samples are representative of normal oral mucosa and of the oral cavity generally.

  • May combine two claims. The quote only partly states this claim.

    Findingown data

    Single-cell RNA-seq of four oral tissues yielded 22,969 cells and identified seven cell types: epithelial cells, fibroblasts, T cells, macrophages, mast cells, B cells, and endothelial cells.

    “After the data preprocessing (shown in section “Materials and methods”), 22 969 cells were acquired and 7 cell types were identified (Fig. 2a), including epithelial cells”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The four in-house oral tissue samples are representative of normal oral mucosa and of the oral cavity generally.

  • May combine two claims.

    Findingown data

    In TCGA adjacent normal oral tissues, mean ACE2 expression was higher in oral tongue than in other oral sites combined, but the difference was not statistically significant (P = 0.062).

    “When we combined the base of tongue, floor of mouth and oral cavity as other sites, and compared them with oral tongue, we found the obvious tendency that the mean expression of ACE2 was higher in oral tongue (13 tissues) than others (19 tissues) (Fig. 1d), while may due to the limitation of the sample size, the p value was not significant (P = 0.062).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The TCGA site annotations for oral cavity samples are accurate.

  • May combine two claims.

    Findingown data

    ACE2 is expressed in oral tissues, with 0.52% ACE2-positive cells.

    “According to Fig. 2c, d, we confirmed the ACE2 was expressed in oral tissues (0.52% ACE2-positive cells)”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The four in-house oral tissue samples are representative of normal oral mucosa and of the oral cavity generally.

  • May combine two claims.

    Interpretationown data

    ACE2 is expressed on epithelial cells of the oral mucosa and is highly enriched in tongue epithelial cells.

    “The above results indicated that the ACE2 could be expressed on the epithelial cells of the oral mucosa and highly enriched in tongue epithelial cells.”
    • Also stated in: § Abstract · plain
      “Interestingly, this receptor was highly enriched in epithelial cells of tongue.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The four in-house oral tissue samples are representative of normal oral mucosa and of the oral cavity generally.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The respiratory tract should also be considered a vulnerable target to 2019-nCoV infection.

    “Even though, the result of Zou et al. indicated that the respiratory tract should also be considered as a vulnerable target to 2019-nCoV infection10.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [10] Zou, X. et al. The single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to Wuhan 2019-nCoV infection. Front. Med. http://journal.hep.com.cn/fmd/EN/10.1007/s11684-020-0754-0 (2020). source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Cells that express ACE2 can act as target cells and are susceptible to 2019-nCoV infection.

    “These findings suggest that the ACE2 plays an important role in cellular entry, thus ACE2-expressing cells may act as target cells and are susceptible to 2019-nCoV infection10.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] Zou, X. et al. The single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to Wuhan 2019-nCoV infection. Front. Med. http://journal.hep.com.cn/fmd/EN/10.1007/s11684-020-0754-0 (2020). source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    ACE2-expressing cells in oral tissues, especially tongue epithelial cells, might provide possible routes of entry for 2019-nCoV, indicating the oral cavity might be a potential risk route of infection.

    “The ACE2-expressing cells in oral tissues, especially in epithelial cells of tongue, might provide possible routes of entry for the 2019-nCov, which indicate oral cavity might be a potential risk route of 2019-nCov infection.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: ACE2 RNA expression levels in tissues indicate the presence of functional ACE2 receptor protein and susceptibility to 2019-nCoV infection.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given

    RNA-seq data were batch effects normalized and log2-transformed.

    “The RNA-seq data were batch effects normalized and log2-transformed for the subsequent analysis.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    Single-cell data were normalized and confounding variation was removed using the sctransform function in Seurat.

    “The “sctransform” wrapper in Seurat was applied to normalize the data and remove confounding sources of variation”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    ACE2 also serves as the receptor for SARS-CoV and HCoV-NL63.

    “Study of Zhou et al.4 indicated that the angiotensin-converting enzyme II (ACE2) is likely the cell receptor of 2019-nCoV, which were also the receptor for SARS-CoV and HCoV-NL637,8.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [7] Li, W. et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426, 450–454 (2003). source

      Not checked in the free run.

    • cites [8] Hofmann, H. et al. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl Acad. Sci. USA 102, 7988–7993 (2005). source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductcitation

    The in-house oral tissues were diagnosed as hyperkeratosis without dysplasia and their genetic profiles are closer to normal tissue than malignant tissue.

    “The four were taken from three patients with an average age of 50, which were all diagnosed as hyperkeratosis without dysplasia by pathologists, just showing an increase in cell number in the spinous layer and/or in the basal/parabasal cell layers without cellular atypia, and its genetic profiles would be much more closed to normal tissue than malignant tissue22–24.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [22] Dionne, K. R., Warnakulasuriya, S., Zain, R. B. & Cheong, S. C. Potentially malignant disorders of the oral cavity: current practice and future directions in the clinic and laboratory. Int. J. Cancer 136, 503–515 (2015). source

      Not checked in the free run.

    • cites [23] Li, J. et al. Associations between proteasomal activator PA28γ and outcome of oral squamous cell carcinoma: evidence from cohort studies and functional analyses. EBioMedicine 2, 851–858 (2015). source

      Not checked in the free run.

    • cites [24] Wang, Z. et al. RACK1, an excellent predictor for poor clinical outcome in oral squamous carcinoma, similar to Ki67. Eur. J. Cancer 45, 490–496 (2009). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Single-cell RNA-sequencing technology enables generation of transcriptomic data at cellular resolution.

    “Recently developed single-cell RNA-sequencing technology enabled the generation of vast amounts of the transcriptomic data at cellular resolution19.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [19] Rostom, R., Svensson, V., Teichmann, S. A. & Kar, G. Computational approaches for interpreting scRNA-seq data. FEBS Lett. 591, 2213–2225 (2017). source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    ACE2 is likely the cell receptor for 2019-nCoV and is important for viral entry into cells.

    “Study of Zhou et al.4 indicated that the angiotensin-converting enzyme II (ACE2) is likely the cell receptor of 2019-nCoV, which were also the receptor for SARS-CoV and HCoV-NL637,8.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Zhou et al.4 Zhou, P. et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. https://doi.org/10.1038/s41586-020-2012-7 (2020). source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    High ACE2 expression has been found in several specific cell types across organs, including type II alveolar cells of lung, upper and stratified esophageal epithelial cells, absorptive enterocytes of ileum and colon, cholangiocytes, myocardial cells, kidney proximal tubule cells, and bladder urothelial cells.

    “High ACE2 expression was identified in type II alveolar cells (AT2) of lung10–12, esophagus upper and stratified epithelial cells, absorptive enterocytes from ileum and colon12, cholangiocytes13, myocardial cells, kidney proximal tubule cells, and bladder urothelial cells10.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [10] Zou, X. et al. The single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to Wuhan 2019-nCoV infection. Front. Med. http://journal.hep.com.cn/fmd/EN/10.1007/s11684-020-0754-0 (2020). source

      Not checked in the free run.

    • cites [11] Zhao, Y. et al. Single-cell RNA expression profiling of ACE2, the putative receptor of Wuhan 2019-nCov. Preprint at https://www.biorxiv.org/content/10.1101/2020.01.26.919985v1 (2020).

      Not checked in the free run.

    • cites [12] Zhang, H. et al. The digestive system is a potential route of 2019-nCov infection: a bioinformatics analysis based on single-cell transcriptomes. Preprint at https://www.biorxiv.org/content/10.1101/2020.01.30.927806v1 (2020). source

      Not checked in the free run.

    • cites [13] Chai, X. et al. Specific ACE2 expression in cholangiocytes may cause liver damage after 2019-nCoV infection. Preprint at https://www.biorxiv.org/content/10.1101/2020.02.03.931766v1 (2020). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Cell types were assigned based on canonical markers.

    “The uniform manifold approximation and projection (UMAP) was used for dimensionality reduction and clustering the cells, cell types were assigned based on their canonical markers.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductown data

    The study's results are mainly based on public datasets and single-cell RNA-seq of in-house oral tissues with minimal diseased lesion.

    “Our results are mainly based on public datasets and single cell RNA-sequencing data of in-house oral tissues with minimal diseased lesion”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    The FANTOM5 CAGE dataset had only two tongue samples and was used to validate ACE2 expression in the oral cavity.

    “as only two samples of this dataset which owns 60 samples in total located in the tongue, we just downloaded 14 organ types to validate the ACE2 expression in oral cavity with bar plot”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    The ACE2 expression profile across organs, tissues, and cell types provides bioinformatics evidence for potential infection routes of 2019-nCoV and might be associated with presented symptoms.

    “The ACE2 expression profile in various organs, tissues, and cell types, provides the bioinformatics evidence for the potential infection routes of 2019-nCov, which might also be associated with presented symptoms.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: ACE2 RNA expression levels in tissues indicate the presence of functional ACE2 receptor protein and susceptibility to 2019-nCoV infection.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    Quality control in single-cell RNA-seq removed cells with <200 genes and 500 UMI counts, cells with mitochondrial content >5%, and genes detected in <3 cells.

    “To control quality, we removed cells with <200 genes and 500 UMI counts, and as well as the cells with mitochondrial content higher than 5%. Besides, the genes detected in <3 cells were filtered out.”
    Quote in the paperNot a substantial claim
22 of 22

  • The paper relies on this without support.

    ACE2 RNA expression levels in tissues indicate the presence of functional ACE2 receptor protein and susceptibility to 2019-nCoV infection.

    “The expression and distribution of the ACE2 in human body may indicate the potential infection routes of 2019-nCoV.”

  • The paper relies on this without support.

    The four in-house oral tissue samples are representative of normal oral mucosa and of the oral cavity generally.

    “Single cell RNA-seq was utilized for four oral tissues, and the data was analyzed to confirm the above results and assess the cell type-specific expression of ACE2.”

  • The paper relies on this without support.

    Public TCGA para-carcinoma normal tissues and FANTOM5 normal tissues are adequate proxies for normal oral mucosa.

    “Bulk RNA-seq data of para-carcinoma normal tissues which were taken as control tissues in the studies were downloaded from The Cancer Genome Atlas (TCGA; https://www.cancer.gov/tcga), and 695 para-carcinoma normal tissues distributed in different organs were obtained for this study”

  • The paper relies on this without support.

    The FANTOM5 CAGE dataset with only two tongue samples can validate ACE2 expression in the oral cavity.

    “as only two samples of this dataset which owns 60 samples in total located in the tongue, we just downloaded 14 organ types to validate the ACE2 expression in oral cavity with bar plot”

  • The paper relies on this without support.

    The TCGA site annotations for oral cavity samples are accurate.

    “According to the site information provided by the TCGA, among the 32 adjacent normal tissues, 13 tissues located in the oral tongue, 2 tissues located in the base of tongue, 3 tissues located in the floor of mouse, and 14 tissues did not definite the site and were just put into the category of oral cavity.”

  • The paper relies on this without support.

    2019-nCoV infection hardly presents oral symptoms.

    “although 2019-ncov infection hardly presented oral symptoms”
6 of 6

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Authors
Xu, H., Zhong, L., Deng, J., Peng, J., Dan, H., Zeng, X., Li, T., & Chen, Q.
Affiliations
Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
Corresponding author
Li, Taiwen
ORCID
Venue
International Journal of Oral Science
Publisher
Springer Science and Business Media LLC
Published
2020-02-24
Volume
12
Issue
1
Pages
8-8
ISSN
  • 1674-2818 (ISSN-L)
  • 2049-3169
DOI
10.1038/s41368-020-0074-x
PMC
PMC7039956
OpenAlex
W3008295344
Cited by
2,838
References
26
Citations by year
2026: 32 · 2025: 59 · 2024: 136 · 2023: 287 · 2022: 469 · 2021: 846 · 2020: 1003 · 2019: 2 · 2018: 2 · 2015: 1
FWCI
85.00
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Oral Science (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by)
  • PUBLISSO (German National Library of Medicine) (submittedVersion, cc-by)
Funders
  • National Natural Science Foundation of China (111 Project, 81991502, B14038, 81771081, 81520108009, 81991500)
  • Ministry of Education, India
  • Higher Education Discipline Innovation Project (B14038)
Topics
  • Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
  • Health Sciences › Dentistry › General Dentistry › Dental Research and COVID-19
  • Health Sciences › Medicine › Dermatology › Dermatological and COVID-19 studies
Keywords
ACE2 receptor, SARS-CoV-2, oral mucosa, host cell receptors, viral entry, infection susceptibility, single-cell transcriptomics, gene expression profiling, dental disease prevention
MeSH terms
Betacoronavirus, Angiotensin-Converting Enzyme 2, COVID-19, SARS-CoV-2, Epithelial Cells, Humans, Peptidyl-Dipeptidase A, Mouth Mucosa, Pneumonia, Viral, Tongue, Coronavirus Infections, Gene Expression Profiling, Databases, Genetic

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