Metabolomic/lipidomic profiling of COVID-19 and individual response to tocilizumab
The current pandemic emergence of novel coronavirus disease (COVID-19) poses a relevant threat to global health. SARS-CoV-2 infection is characterized by a wide range of clinical manifestations, ranging from absence of symptoms to severe forms that need intensive care treatment. Here, plasma-EDTA sa...
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| Veröffentlicht in: | PLoS pathogens 2021-02, Vol.17 (2), p.e1009243-e1009243, Article 1009243 |
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| creator | Meoni, Gaia Ghini, Veronica Maggi, Laura Vignoli, Alessia Mazzoni, Alessio Salvati, Lorenzo Capone, Manuela Vanni, Anna Tenori, Leonardo Fontanari, Paolo Lavorini, Federico Peris, Adriano Bartoloni, Alessandro Liotta, Francesco Cosmi, Lorenzo Luchinat, Claudio Annunziato, Francesco Turano, Paola |
| description | The current pandemic emergence of novel coronavirus disease (COVID-19) poses a relevant threat to global health. SARS-CoV-2 infection is characterized by a wide range of clinical manifestations, ranging from absence of symptoms to severe forms that need intensive care treatment. Here, plasma-EDTA samples of 30 patients compared with age- and sex-matched controls were analyzed via untargeted nuclear magnetic resonance (NMR)-based metabolomics and lipidomics. With the same approach, the effect of tocilizumab administration was evaluated in a subset of patients. Despite the heterogeneity of the clinical symptoms, COVID-19 patients are characterized by common plasma metabolomic and lipidomic signatures (91.7% and 87.5% accuracy, respectively, when compared to controls). Tocilizumab treatment resulted in at least partial reversion of the metabolic alterations due to SARS-CoV-2 infection. In conclusion, NMR-based metabolomic and lipidomic profiling provides novel insights into the pathophysiological mechanism of human response to SARS-CoV-2 infection and to monitor treatment outcomes.
Author summary
The current COVID-19 pandemic caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) is markedly affecting the world population. Here we report about the small-molecule profile of patients hospitalized during the first wave of the COVID-19 pandemic in Florence (Italy). Using magnetic resonance spectroscopy, we showed that the infection induces profound changes in the metabolome. The analysis of the specific metabolite changes and correlations with clinical data enabled the identification of potential biochemical determinants of the disease fingerprint. We also followed how metabolic alterations revert towards those of the control group upon treatment with tocilizumab, a recombinant humanized monoclonal antibody against the interleukin-6 receptor. These results open up possibilities for the monitoring of novel patients and their individual response to treatment. |
| doi_str_mv | 10.1371/journal.ppat.1009243 |
| format | Article |
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Author summary
The current COVID-19 pandemic caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) is markedly affecting the world population. Here we report about the small-molecule profile of patients hospitalized during the first wave of the COVID-19 pandemic in Florence (Italy). Using magnetic resonance spectroscopy, we showed that the infection induces profound changes in the metabolome. The analysis of the specific metabolite changes and correlations with clinical data enabled the identification of potential biochemical determinants of the disease fingerprint. We also followed how metabolic alterations revert towards those of the control group upon treatment with tocilizumab, a recombinant humanized monoclonal antibody against the interleukin-6 receptor. These results open up possibilities for the monitoring of novel patients and their individual response to treatment.</description><identifier>ISSN: 1553-7366</identifier><identifier>ISSN: 1553-7374</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1009243</identifier><identifier>PMID: 33524041</identifier><language>eng</language><publisher>SAN FRANCISCO: Public Library Science</publisher><subject>Accuracy ; Antibodies, Monoclonal, Humanized - administration & dosage ; Biology and Life Sciences ; Blood cells ; Carboxylates ; Cardiovascular disease ; Cholesterol ; Citric acid ; Coronary artery ; Coronary artery disease ; Coronaviruses ; COVID-19 ; COVID-19 - blood ; COVID-19 - drug therapy ; COVID-19 - epidemiology ; Cytokines ; Erythrocytes ; Ethylenediaminetetraacetic acids ; Female ; Heart diseases ; High density lipoprotein ; Humans ; Hypoxia ; Immunosuppressive agents ; Infections ; Intensive care ; Life Sciences & Biomedicine ; Lipidomics ; Lipids ; Lipids - blood ; Low density lipoprotein ; Male ; Medicine and Health Sciences ; Metabolites ; Metabolomics ; Microbiology ; Monoclonal antibodies ; Neutrophils ; NMR ; NMR spectroscopy ; Nuclear magnetic resonance ; Nuclear Magnetic Resonance, Biomolecular ; Pandemics ; Parasitology ; Patients ; Phenylalanine ; Plasma ; Pneumonia ; Principal components analysis ; Research and analysis methods ; SARS-CoV-2 - metabolism ; Science & Technology ; Sepsis ; Severe acute respiratory syndrome coronavirus 2 ; Spectroscopy ; Spectrum analysis ; Tyrosine ; Ventilators ; Virology</subject><ispartof>PLoS pathogens, 2021-02, Vol.17 (2), p.e1009243-e1009243, Article 1009243</ispartof><rights>2021 Meoni et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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SARS-CoV-2 infection is characterized by a wide range of clinical manifestations, ranging from absence of symptoms to severe forms that need intensive care treatment. Here, plasma-EDTA samples of 30 patients compared with age- and sex-matched controls were analyzed via untargeted nuclear magnetic resonance (NMR)-based metabolomics and lipidomics. With the same approach, the effect of tocilizumab administration was evaluated in a subset of patients. Despite the heterogeneity of the clinical symptoms, COVID-19 patients are characterized by common plasma metabolomic and lipidomic signatures (91.7% and 87.5% accuracy, respectively, when compared to controls). Tocilizumab treatment resulted in at least partial reversion of the metabolic alterations due to SARS-CoV-2 infection. In conclusion, NMR-based metabolomic and lipidomic profiling provides novel insights into the pathophysiological mechanism of human response to SARS-CoV-2 infection and to monitor treatment outcomes.
Author summary
The current COVID-19 pandemic caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) is markedly affecting the world population. Here we report about the small-molecule profile of patients hospitalized during the first wave of the COVID-19 pandemic in Florence (Italy). Using magnetic resonance spectroscopy, we showed that the infection induces profound changes in the metabolome. The analysis of the specific metabolite changes and correlations with clinical data enabled the identification of potential biochemical determinants of the disease fingerprint. We also followed how metabolic alterations revert towards those of the control group upon treatment with tocilizumab, a recombinant humanized monoclonal antibody against the interleukin-6 receptor. These results open up possibilities for the monitoring of novel patients and their individual response to treatment.</description><subject>Accuracy</subject><subject>Antibodies, Monoclonal, Humanized - administration & dosage</subject><subject>Biology and Life Sciences</subject><subject>Blood cells</subject><subject>Carboxylates</subject><subject>Cardiovascular disease</subject><subject>Cholesterol</subject><subject>Citric acid</subject><subject>Coronary artery</subject><subject>Coronary artery disease</subject><subject>Coronaviruses</subject><subject>COVID-19</subject><subject>COVID-19 - blood</subject><subject>COVID-19 - drug therapy</subject><subject>COVID-19 - epidemiology</subject><subject>Cytokines</subject><subject>Erythrocytes</subject><subject>Ethylenediaminetetraacetic acids</subject><subject>Female</subject><subject>Heart diseases</subject><subject>High density lipoprotein</subject><subject>Humans</subject><subject>Hypoxia</subject><subject>Immunosuppressive agents</subject><subject>Infections</subject><subject>Intensive care</subject><subject>Life Sciences & Biomedicine</subject><subject>Lipidomics</subject><subject>Lipids</subject><subject>Lipids - blood</subject><subject>Low density lipoprotein</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Metabolites</subject><subject>Metabolomics</subject><subject>Microbiology</subject><subject>Monoclonal antibodies</subject><subject>Neutrophils</subject><subject>NMR</subject><subject>NMR spectroscopy</subject><subject>Nuclear magnetic resonance</subject><subject>Nuclear Magnetic Resonance, Biomolecular</subject><subject>Pandemics</subject><subject>Parasitology</subject><subject>Patients</subject><subject>Phenylalanine</subject><subject>Plasma</subject><subject>Pneumonia</subject><subject>Principal components analysis</subject><subject>Research and analysis methods</subject><subject>SARS-CoV-2 - metabolism</subject><subject>Science & Technology</subject><subject>Sepsis</subject><subject>Severe acute respiratory syndrome coronavirus 2</subject><subject>Spectroscopy</subject><subject>Spectrum 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Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Meoni, Gaia</au><au>Ghini, Veronica</au><au>Maggi, Laura</au><au>Vignoli, Alessia</au><au>Mazzoni, Alessio</au><au>Salvati, Lorenzo</au><au>Capone, Manuela</au><au>Vanni, Anna</au><au>Tenori, Leonardo</au><au>Fontanari, Paolo</au><au>Lavorini, Federico</au><au>Peris, Adriano</au><au>Bartoloni, Alessandro</au><au>Liotta, Francesco</au><au>Cosmi, Lorenzo</au><au>Luchinat, Claudio</au><au>Annunziato, Francesco</au><au>Turano, Paola</au><au>Subbarao, Kanta</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metabolomic/lipidomic profiling of COVID-19 and individual response to tocilizumab</atitle><jtitle>PLoS pathogens</jtitle><stitle>PLOS PATHOG</stitle><addtitle>PLoS Pathog</addtitle><date>2021-02-01</date><risdate>2021</risdate><volume>17</volume><issue>2</issue><spage>e1009243</spage><epage>e1009243</epage><pages>e1009243-e1009243</pages><artnum>1009243</artnum><issn>1553-7366</issn><issn>1553-7374</issn><eissn>1553-7374</eissn><abstract>The current pandemic emergence of novel coronavirus disease (COVID-19) poses a relevant threat to global health. SARS-CoV-2 infection is characterized by a wide range of clinical manifestations, ranging from absence of symptoms to severe forms that need intensive care treatment. Here, plasma-EDTA samples of 30 patients compared with age- and sex-matched controls were analyzed via untargeted nuclear magnetic resonance (NMR)-based metabolomics and lipidomics. With the same approach, the effect of tocilizumab administration was evaluated in a subset of patients. Despite the heterogeneity of the clinical symptoms, COVID-19 patients are characterized by common plasma metabolomic and lipidomic signatures (91.7% and 87.5% accuracy, respectively, when compared to controls). Tocilizumab treatment resulted in at least partial reversion of the metabolic alterations due to SARS-CoV-2 infection. In conclusion, NMR-based metabolomic and lipidomic profiling provides novel insights into the pathophysiological mechanism of human response to SARS-CoV-2 infection and to monitor treatment outcomes.
Author summary
The current COVID-19 pandemic caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) is markedly affecting the world population. Here we report about the small-molecule profile of patients hospitalized during the first wave of the COVID-19 pandemic in Florence (Italy). Using magnetic resonance spectroscopy, we showed that the infection induces profound changes in the metabolome. The analysis of the specific metabolite changes and correlations with clinical data enabled the identification of potential biochemical determinants of the disease fingerprint. We also followed how metabolic alterations revert towards those of the control group upon treatment with tocilizumab, a recombinant humanized monoclonal antibody against the interleukin-6 receptor. These results open up possibilities for the monitoring of novel patients and their individual response to treatment.</abstract><cop>SAN FRANCISCO</cop><pub>Public Library Science</pub><pmid>33524041</pmid><doi>10.1371/journal.ppat.1009243</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-4690-9960</orcidid><orcidid>https://orcid.org/0000-0002-0463-2799</orcidid><orcidid>https://orcid.org/0000-0003-4038-6596</orcidid><orcidid>https://orcid.org/0000-0002-3293-2123</orcidid><orcidid>https://orcid.org/0000-0001-9758-1523</orcidid><orcidid>https://orcid.org/0000-0002-8150-8177</orcidid><orcidid>https://orcid.org/0000-0002-7683-8614</orcidid><orcidid>https://orcid.org/0000-0002-8608-4641</orcidid><orcidid>https://orcid.org/0000-0003-2862-9591</orcidid><orcidid>https://orcid.org/0000-0001-6438-059X</orcidid><orcidid>https://orcid.org/0000-0001-7768-3805</orcidid><orcidid>https://orcid.org/0000-0001-5831-0392</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1553-7366 |
| ispartof | PLoS pathogens, 2021-02, Vol.17 (2), p.e1009243-e1009243, Article 1009243 |
| issn | 1553-7366 1553-7374 1553-7374 |
| language | eng |
| recordid | cdi_plos_journals_2501881104 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Public Library of Science (PLoS) Journals Open Access; Web of Science - Science Citation Index Expanded - 2021<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" />; PubMed Central |
| subjects | Accuracy Antibodies, Monoclonal, Humanized - administration & dosage Biology and Life Sciences Blood cells Carboxylates Cardiovascular disease Cholesterol Citric acid Coronary artery Coronary artery disease Coronaviruses COVID-19 COVID-19 - blood COVID-19 - drug therapy COVID-19 - epidemiology Cytokines Erythrocytes Ethylenediaminetetraacetic acids Female Heart diseases High density lipoprotein Humans Hypoxia Immunosuppressive agents Infections Intensive care Life Sciences & Biomedicine Lipidomics Lipids Lipids - blood Low density lipoprotein Male Medicine and Health Sciences Metabolites Metabolomics Microbiology Monoclonal antibodies Neutrophils NMR NMR spectroscopy Nuclear magnetic resonance Nuclear Magnetic Resonance, Biomolecular Pandemics Parasitology Patients Phenylalanine Plasma Pneumonia Principal components analysis Research and analysis methods SARS-CoV-2 - metabolism Science & Technology Sepsis Severe acute respiratory syndrome coronavirus 2 Spectroscopy Spectrum analysis Tyrosine Ventilators Virology |
| title | Metabolomic/lipidomic profiling of COVID-19 and individual response to tocilizumab |
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