Proteomics of circulating extracellular vesicles reveals diverse clinical presentations of COVID-19 but fails to identify viral peptides

Front Cell Infect Microbiol. 2024 Nov 6:14:1442743. doi: 10.3389/fcimb.2024.1442743. eCollection 2024.

Abstract

Extracellular vesicles (EVs) released by virus-infected cells have the potential to encapsulate viral peptides, a characteristic that could facilitate vaccine development. Furthermore, plasma-derived EVs may elucidate pathological changes occurring in distal tissues during viral infections. We hypothesized that molecular characterization of EVs isolated from COVID-19 patients would reveal peptides suitable for vaccine development. Blood samples were collected from three cohorts: severe COVID-19 patients (G1), mild/asymptomatic cases (G2), and SARS-CoV-2-negative healthcare workers (G3). Samples were obtained at two time points: during the initial phase of the pandemic in early 2020 (m0) and eight months later (m8). Clinical data analysis revealed elevated inflammatory markers in G1. Notably, non-vaccinated individuals in G1 exhibited increased levels of neutralizing antibodies at m8, suggesting prolonged exposure to viral antigens. Proteomic profiling of EVs was performed using three distinct methods: immunocapture (targeting CD9), ganglioside-capture (utilizing Siglec-1) and size-exclusion chromatography (SEC). Contrary to our hypothesis, this analysis failed to identify viral peptides. These findings were subsequently validated through Western blot analysis targeting the RBD of the SARS-CoV-2 Spike protein's and comparative studies using samples from experimentally infected Syrian hamsters. Furthermore, analysis of the EV cargo revealed a diverse molecular profile, including components involved in the regulation of viral replication, systemic inflammation, antigen presentation, and stress responses. These findings underscore the potential significance of EVs in the pathogenesis and progression of COVID-19.

Keywords: COVID-19 patients; SARS-CoV-2; antibody response; extracellular vesicles; ganglioside-capture (CD169/Siglec-1); immunocapture (CD9); proteomics profiling; size-exclusion chromatography (SEC).

MeSH terms

  • Adult
  • Animals
  • Antibodies, Neutralizing / blood
  • Antibodies, Neutralizing / immunology
  • Antibodies, Viral / blood
  • COVID-19* / immunology
  • COVID-19* / virology
  • Cricetinae
  • Extracellular Vesicles* / metabolism
  • Female
  • Humans
  • Male
  • Mesocricetus
  • Middle Aged
  • Peptides / metabolism
  • Proteomics*
  • SARS-CoV-2*
  • Viral Proteins / metabolism

Substances

  • Antibodies, Neutralizing
  • Peptides
  • Antibodies, Viral
  • Viral Proteins

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The proteomics of EVs isolated by CD9 was performed at the proteomics facility of Utrecht (Netherlands) as part of an EPIC-XS grant (0000205) to CT and HP. The proteomics analyses of EVs isolated by SEC were performed in the IJC Proteomic unit, which is part of the of Proteored, PRB3 and is supported by grant PT17/0019, of the PE I+D+i 2013-2016, funded by ISCIII and ERDF”. The CRG/UPF Proteomics Unit is part of the Spanish Infrastructure for Omics Technologies (ICTS OmicsTech), and it is supported by “Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement de la Generalitat de Catalunya” (2017SGR595). We thank Foundation Dormeur for financial support for the acquisition of the QuantStudio-5 real time PCR system. JM-P was supported by the Spanish Ministry of Science,Innovation and Universities (grants PID2022-139271OB-I00 and CB21/13/00063, Spain), and Fundació La Marató de TV3 (grant 202120-30-31-32, Spain). Funded in part by the European Union. The PCR-4-ALL and UNDINE projects have received funding under the Horizon Europe research and innovation programme (grant agreement No 101095606 and No 101057100 respectively). CF-B and HP acknowledge support from the Spanish Ministry of Science and Innovation (MICINN) (PID2022- 142908OB-I00) and support from the grant CEX2023-0001290-S funded by MCIN/AEI/10.13039/501100011033, and support from the Generalitat de Catalunya through the CERCA Program. This research is part of the ISGlobal’s Program on the Molecular Mechanisms of Malaria which is partially supported by the Fundación Ramón Areces. We also acknowledged the internal funding from IrsiCaixa through the crowdfunding initiative YoMeCorono (JM-P) and ISGlobal (HP) to initiate these studies.