Alteration of L-Dopa decarboxylase expression in SARS-CoV-2 infection and its association with the interferon-inducible ACE2 isoform

PLoS One. 2021 Jun 29;16(6):e0253458. doi: 10.1371/journal.pone.0253458. eCollection 2021.

Abstract

L-Dopa decarboxylase (DDC) is the most significantly co-expressed gene with ACE2, which encodes for the SARS-CoV-2 receptor angiotensin-converting enzyme 2 and the interferon-inducible truncated isoform dACE2. Our group previously showed the importance of DDC in viral infections. We hereby aimed to investigate DDC expression in COVID-19 patients and cultured SARS-CoV-2-infected cells, also in association with ACE2 and dACE2. We concurrently evaluated the expression of the viral infection- and interferon-stimulated gene ISG56 and the immune-modulatory, hypoxia-regulated gene EPO. Viral load and mRNA levels of DDC, ACE2, dACE2, ISG56 and EPO were quantified by RT-qPCR in nasopharyngeal swab samples from COVID-19 patients, showing no or mild symptoms, and from non-infected individuals. Samples from influenza-infected patients were analyzed in comparison. SARS-CoV-2-mediated effects in host gene expression were validated in cultured virus-permissive epithelial cells. We found substantially higher gene expression of DDC in COVID-19 patients (7.6-fold; p = 1.2e-13) but not in influenza-infected ones, compared to non-infected subjects. dACE2 was more elevated (2.9-fold; p = 1.02e-16) than ACE2 (1.7-fold; p = 0.0005) in SARS-CoV-2-infected individuals. ISG56 (2.5-fold; p = 3.01e-6) and EPO (2.6-fold; p = 2.1e-13) were also increased. Detected differences were not attributed to enrichment of specific cell populations in nasopharyngeal tissue. While SARS-CoV-2 virus load was positively associated with ACE2 expression (r≥0.8, p<0.001), it negatively correlated with DDC, dACE2 (r≤-0.7, p<0.001) and EPO (r≤-0.5, p<0.05). Moreover, a statistically significant correlation between DDC and dACE2 expression was observed in nasopharyngeal swab and whole blood samples of both COVID-19 and non-infected individuals (r≥0.7). In VeroE6 cells, SARS-CoV-2 negatively affected DDC, ACE2, dACE2 and EPO mRNA levels, and induced cell death, while ISG56 was enhanced at early hours post-infection. Thus, the regulation of DDC, dACE2 and EPO expression in the SARS-CoV-2-infected nasopharyngeal tissue is possibly related with an orchestrated antiviral response of the infected host as the virus suppresses these genes to favor its propagation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Adult
  • Aged
  • Angiotensin-Converting Enzyme 2 / genetics
  • Angiotensin-Converting Enzyme 2 / metabolism*
  • Area Under Curve
  • Aromatic-L-Amino-Acid Decarboxylases
  • COVID-19 / pathology*
  • COVID-19 / virology
  • Dopa Decarboxylase / genetics
  • Dopa Decarboxylase / metabolism*
  • Down-Regulation
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Erythropoietin / genetics
  • Erythropoietin / metabolism
  • Female
  • Humans
  • Male
  • Middle Aged
  • Nasopharynx / metabolism
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • ROC Curve
  • SARS-CoV-2 / genetics
  • SARS-CoV-2 / isolation & purification
  • Up-Regulation
  • Viral Load

Substances

  • Adaptor Proteins, Signal Transducing
  • EPO protein, human
  • IFIT1 protein, human
  • Protein Isoforms
  • RNA-Binding Proteins
  • Erythropoietin
  • ACE2 protein, human
  • Angiotensin-Converting Enzyme 2
  • Dopa Decarboxylase
  • Aromatic-L-Amino-Acid Decarboxylases
  • DDC protein, human

Grants and funding

This work was supported by the « URGENCE COVID-19 » fundraising campaign of Institut Pasteur. G.M. was supported by an excellence PhD fellowship from Hellenic Pasteur Institute. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.