Heparin prevents in vitro glycocalyx shedding induced by plasma from COVID-19 patients

The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial cells express Angiotensin-Converting Enzyme 2 (ACE2), which is the entrance door for the severe acute respiratory syndrome coronavirus 2 (SARS-...

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Published inLife sciences (1973) Vol. 276; p. 119376
Main Authors Potje, Simone R., Costa, Tiago J., Fraga-Silva, Thais F.C., Martins, Ronaldo B., Benatti, Maira N., Almado, Carlos E.L., de Sá, Keyla S.G., Bonato, Vânia L.D., Arruda, Eurico, Louzada-Junior, Paulo, Oliveira, Rene D.R., Zamboni, Dario S., Becari, Christiane, Auxiliadora-Martins, Maria, Tostes, Rita C.
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier Inc 01.07.2021
Elsevier BV
Subjects
ACE2
adhesion
Aged
Alveoli
Angiotensin
Angiotensin-converting enzyme 2
Blood Coagulation Disorders - blood
Blood Coagulation Disorders - virology
C-reactive protein
Capillaries
Cardiovascular diseases
Case-Control Studies
Cell Adhesion - physiology
Coronaviridae
Coronaviruses
COVID-19
COVID-19 - blood
COVID-19 - metabolism
COVID-19 - pathology
COVID-19 infection
COVID-19 Testing
Cytokines
Degradation
Dimers
disease severity
Endothelial cells
Endothelium, Vascular - metabolism
Female
Ferritin
Glycocalyx
Glycocalyx - metabolism
Glycocalyx - pathology
Glycocalyx - virology
Glycoproteins
Health services
Heparan sulfate proteoglycans
Heparin
Heparin - pharmacology
Homeostasis
Human Umbilical Vein Endothelial Cells
Humans
Hypertension
Inflammation
Inflammatory response
Interleukin 1
Interleukin 6
Interleukin-1beta - blood
Interleukin-6 - blood
Leukocytes
Lipid peroxidation
Lipids
Low molecular weight heparin
Low molecular weights
Lymphopenia
Male
Middle Aged
Molecular weight
Neutrophilia
Oxidation-Reduction
Peptidyl-dipeptidase A
Permeability
Peroxidation
Perturbation
Plasma
Proteoglycans
Reactive oxygen species
Respiratory diseases
SARS-CoV-2
Severe acute respiratory syndrome coronavirus 2
Shedding
Thromboembolism
Thrombosis
Thrombosis - metabolism
Umbilical vein
Vascular dysfunction
Viral diseases
COVID-19
Heparan sulfate proteoglycans
Low molecular weight heparin
Glycocalyx
Vascular dysfunction
Endothelial cells
Online AccessGet full text
ISSN0024-3205
1879-0631
1879-0631
DOI10.1016/j.lfs.2021.119376

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Abstract The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial cells express Angiotensin-Converting Enzyme 2 (ACE2), which is the entrance door for the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The hallmarks of severe illness caused by SARS-CoV-2 infection are increased levels of IL-6, C-reactive protein, D-dimer, ferritin, neutrophilia and lymphopenia, pulmonary intravascular coagulopathy and microthrombi of alveolar capillaries. The endothelial glycocalyx, a proteoglycan- and glycoprotein-rich layer covering the luminal side of endothelial cells, contributes to vascular homeostasis. It regulates vascular tonus and permeability, prevents thrombosis, and modulates leukocyte adhesion and inflammatory response. We hypothesized that cytokine production and reactive oxygen species (ROS) generation associated with COVID-19 leads to glycocalyx degradation. A cohort of 20 hospitalized patients with a confirmed COVID-19 diagnosis and healthy subjects were enrolled in this study. Mechanisms associated with glycocalyx degradation in COVID-19 were investigated. Increased plasma concentrations of IL-6 and IL1-β, as well as increased lipid peroxidation and glycocalyx components were detected in plasma from COVID-19 patients compared to plasma from healthy subjects. Plasma from COVID-19 patients induced glycocalyx shedding in cultured human umbilical vein endothelial cells (HUVECs) and disrupted redox balance. Treatment of HUVECs with low molecular weight heparin inhibited the glycocalyx perturbation. In conclusion, plasma from COVID-19 patients promotes glycocalyx shedding and redox imbalance in endothelial cells, and heparin treatment potentially inhibits glycocalyx disruption. [Display omitted] •Endothelial cells are a crucial interface between blood and tissues, maintaining vascular homeostasis•SARS-CoV-2 infection threatens endothelial function by increasing cytokines and ROS, thus shedding the endothelial glycocalyx•Plasma from COVID-19 patients disrupts the glycocalyx, which is prevented by heparin/LMWH
AbstractList The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial cells express Angiotensin-Converting Enzyme 2 (ACE2), which is the entrance door for the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The hallmarks of severe illness caused by SARS-CoV-2 infection are increased levels of IL-6, C-reactive protein, D-dimer, ferritin, neutrophilia and lymphopenia, pulmonary intravascular coagulopathy and microthrombi of alveolar capillaries. The endothelial glycocalyx, a proteoglycan- and glycoprotein-rich layer covering the luminal side of endothelial cells, contributes to vascular homeostasis. It regulates vascular tonus and permeability, prevents thrombosis, and modulates leukocyte adhesion and inflammatory response. We hypothesized that cytokine production and reactive oxygen species (ROS) generation associated with COVID-19 leads to glycocalyx degradation. A cohort of 20 hospitalized patients with a confirmed COVID-19 diagnosis and healthy subjects were enrolled in this study. Mechanisms associated with glycocalyx degradation in COVID-19 were investigated. Increased plasma concentrations of IL-6 and IL1-β, as well as increased lipid peroxidation and glycocalyx components were detected in plasma from COVID-19 patients compared to plasma from healthy subjects. Plasma from COVID-19 patients induced glycocalyx shedding in cultured human umbilical vein endothelial cells (HUVECs) and disrupted redox balance. Treatment of HUVECs with low molecular weight heparin inhibited the glycocalyx perturbation. In conclusion, plasma from COVID-19 patients promotes glycocalyx shedding and redox imbalance in endothelial cells, and heparin treatment potentially inhibits glycocalyx disruption.
The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial cells express Angiotensin-Converting Enzyme 2 (ACE2), which is the entrance door for the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The hallmarks of severe illness caused by SARS-CoV-2 infection are increased levels of IL-6, C-reactive protein, D-dimer, ferritin, neutrophilia and lymphopenia, pulmonary intravascular coagulopathy and microthrombi of alveolar capillaries. The endothelial glycocalyx, a proteoglycan- and glycoprotein-rich layer covering the luminal side of endothelial cells, contributes to vascular homeostasis. It regulates vascular tonus and permeability, prevents thrombosis, and modulates leukocyte adhesion and inflammatory response. We hypothesized that cytokine production and reactive oxygen species (ROS) generation associated with COVID-19 leads to glycocalyx degradation. A cohort of 20 hospitalized patients with a confirmed COVID-19 diagnosis and healthy subjects were enrolled in this study. Mechanisms associated with glycocalyx degradation in COVID-19 were investigated. Increased plasma concentrations of IL-6 and IL1-β, as well as increased lipid peroxidation and glycocalyx components were detected in plasma from COVID-19 patients compared to plasma from healthy subjects. Plasma from COVID-19 patients induced glycocalyx shedding in cultured human umbilical vein endothelial cells (HUVECs) and disrupted redox balance. Treatment of HUVECs with low molecular weight heparin inhibited the glycocalyx perturbation. In conclusion, plasma from COVID-19 patients promotes glycocalyx shedding and redox imbalance in endothelial cells, and heparin treatment potentially inhibits glycocalyx disruption.The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial cells express Angiotensin-Converting Enzyme 2 (ACE2), which is the entrance door for the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The hallmarks of severe illness caused by SARS-CoV-2 infection are increased levels of IL-6, C-reactive protein, D-dimer, ferritin, neutrophilia and lymphopenia, pulmonary intravascular coagulopathy and microthrombi of alveolar capillaries. The endothelial glycocalyx, a proteoglycan- and glycoprotein-rich layer covering the luminal side of endothelial cells, contributes to vascular homeostasis. It regulates vascular tonus and permeability, prevents thrombosis, and modulates leukocyte adhesion and inflammatory response. We hypothesized that cytokine production and reactive oxygen species (ROS) generation associated with COVID-19 leads to glycocalyx degradation. A cohort of 20 hospitalized patients with a confirmed COVID-19 diagnosis and healthy subjects were enrolled in this study. Mechanisms associated with glycocalyx degradation in COVID-19 were investigated. Increased plasma concentrations of IL-6 and IL1-β, as well as increased lipid peroxidation and glycocalyx components were detected in plasma from COVID-19 patients compared to plasma from healthy subjects. Plasma from COVID-19 patients induced glycocalyx shedding in cultured human umbilical vein endothelial cells (HUVECs) and disrupted redox balance. Treatment of HUVECs with low molecular weight heparin inhibited the glycocalyx perturbation. In conclusion, plasma from COVID-19 patients promotes glycocalyx shedding and redox imbalance in endothelial cells, and heparin treatment potentially inhibits glycocalyx disruption.
The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial cells express Angiotensin-Converting Enzyme 2 (ACE2), which is the entrance door for the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The hallmarks of severe illness caused by SARS-CoV-2 infection are increased levels of IL-6, C-reactive protein, D-dimer, ferritin, neutrophilia and lymphopenia, pulmonary intravascular coagulopathy and microthrombi of alveolar capillaries. The endothelial glycocalyx, a proteoglycan- and glycoprotein-rich layer covering the luminal side of endothelial cells, contributes to vascular homeostasis. It regulates vascular tonus and permeability, prevents thrombosis, and modulates leukocyte adhesion and inflammatory response. We hypothesized that cytokine production and reactive oxygen species (ROS) generation associated with COVID-19 leads to glycocalyx degradation. A cohort of 20 hospitalized patients with a confirmed COVID-19 diagnosis and healthy subjects were enrolled in this study. Mechanisms associated with glycocalyx degradation in COVID-19 were investigated. Increased plasma concentrations of IL-6 and IL1-β, as well as increased lipid peroxidation and glycocalyx components were detected in plasma from COVID-19 patients compared to plasma from healthy subjects. Plasma from COVID-19 patients induced glycocalyx shedding in cultured human umbilical vein endothelial cells (HUVECs) and disrupted redox balance. Treatment of HUVECs with low molecular weight heparin inhibited the glycocalyx perturbation. In conclusion, plasma from COVID-19 patients promotes glycocalyx shedding and redox imbalance in endothelial cells, and heparin treatment potentially inhibits glycocalyx disruption. Unlabelled Image
The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial cells express Angiotensin-Converting Enzyme 2 (ACE2), which is the entrance door for the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The hallmarks of severe illness caused by SARS-CoV-2 infection are increased levels of IL-6, C-reactive protein, D-dimer, ferritin, neutrophilia and lymphopenia, pulmonary intravascular coagulopathy and microthrombi of alveolar capillaries. The endothelial glycocalyx, a proteoglycan- and glycoprotein-rich layer covering the luminal side of endothelial cells, contributes to vascular homeostasis. It regulates vascular tonus and permeability, prevents thrombosis, and modulates leukocyte adhesion and inflammatory response. We hypothesized that cytokine production and reactive oxygen species (ROS) generation associated with COVID-19 leads to glycocalyx degradation. A cohort of 20 hospitalized patients with a confirmed COVID-19 diagnosis and healthy subjects were enrolled in this study. Mechanisms associated with glycocalyx degradation in COVID-19 were investigated. Increased plasma concentrations of IL-6 and IL1-β, as well as increased lipid peroxidation and glycocalyx components were detected in plasma from COVID-19 patients compared to plasma from healthy subjects. Plasma from COVID-19 patients induced glycocalyx shedding in cultured human umbilical vein endothelial cells (HUVECs) and disrupted redox balance. Treatment of HUVECs with low molecular weight heparin inhibited the glycocalyx perturbation. In conclusion, plasma from COVID-19 patients promotes glycocalyx shedding and redox imbalance in endothelial cells, and heparin treatment potentially inhibits glycocalyx disruption. [Display omitted] •Endothelial cells are a crucial interface between blood and tissues, maintaining vascular homeostasis•SARS-CoV-2 infection threatens endothelial function by increasing cytokines and ROS, thus shedding the endothelial glycocalyx•Plasma from COVID-19 patients disrupts the glycocalyx, which is prevented by heparin/LMWH
ArticleNumber 119376
Author Becari, Christiane
Costa, Tiago J.
Martins, Ronaldo B.
Auxiliadora-Martins, Maria
de Sá, Keyla S.G.
Louzada-Junior, Paulo
Tostes, Rita C.
Almado, Carlos E.L.
Oliveira, Rene D.R.
Potje, Simone R.
Arruda, Eurico
Fraga-Silva, Thais F.C.
Bonato, Vânia L.D.
Benatti, Maira N.
Zamboni, Dario S.
Author_xml – sequence: 1
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  surname: Potje
  fullname: Potje, Simone R.
  organization: Department of Chemistry and Physics, Faculty of Pharmaceutical Sciences of Ribeirao Preto, University of São Paulo – USP, Brazil
– sequence: 2
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  surname: Costa
  fullname: Costa, Tiago J.
  organization: Department of Pharmacology, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Thais F.C.
  surname: Fraga-Silva
  fullname: Fraga-Silva, Thais F.C.
  organization: Department of Biochemistry and Immunology, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
– sequence: 4
  givenname: Ronaldo B.
  surname: Martins
  fullname: Martins, Ronaldo B.
  organization: Department of Cell and Molecular Biology, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Maira N.
  surname: Benatti
  fullname: Benatti, Maira N.
  organization: Department of Clinical Medicine, Division of Internal Medicine, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Carlos E.L.
  surname: Almado
  fullname: Almado, Carlos E.L.
  organization: Department of Surgery and Anatomy, Division of Intensive Care, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Keyla S.G.
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  fullname: de Sá, Keyla S.G.
  organization: Department of Cell and Molecular Biology, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Vânia L.D.
  surname: Bonato
  fullname: Bonato, Vânia L.D.
  organization: Department of Biochemistry and Immunology, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Paulo
  surname: Louzada-Junior
  fullname: Louzada-Junior, Paulo
  organization: Department of Clinical Medicine, Division of Internal Medicine, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
– sequence: 11
  givenname: Rene D.R.
  surname: Oliveira
  fullname: Oliveira, Rene D.R.
  organization: Department of Clinical Medicine, Division of Internal Medicine, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Dario S.
  surname: Zamboni
  fullname: Zamboni, Dario S.
  organization: Department of Cell and Molecular Biology, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
– sequence: 13
  givenname: Christiane
  surname: Becari
  fullname: Becari, Christiane
  organization: Department of Surgery and Anatomy, Division of Intensive Care, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
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  givenname: Maria
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  organization: Department of Surgery and Anatomy, Division of Intensive Care, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
– sequence: 15
  givenname: Rita C.
  surname: Tostes
  fullname: Tostes, Rita C.
  email: rtostes@usp.br
  organization: Department of Pharmacology, Ribeirao Preto Medical School, University of São Paulo – USP, Brazil
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33781826$$D View this record in MEDLINE/PubMed
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ISSN 0024-3205
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IngestDate Thu Aug 21 13:32:25 EDT 2025
Sat Sep 27 22:06:40 EDT 2025
Sat Sep 27 21:49:13 EDT 2025
Wed Aug 13 07:20:41 EDT 2025
Wed Feb 19 02:26:14 EST 2025
Tue Jul 01 04:30:11 EDT 2025
Thu Apr 24 23:09:20 EDT 2025
Sat Jul 06 15:30:44 EDT 2024
IsDoiOpenAccess true
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Keywords COVID-19
Heparan sulfate proteoglycans
Low molecular weight heparin
Glycocalyx
Vascular dysfunction
Endothelial cells
Language English
License Copyright © 2021 Elsevier Inc. All rights reserved.
Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.
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These authors equally contributed to the manuscript.
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Snippet The severe forms and worsened outcomes of COVID-19 (coronavirus disease 19) are closely associated with hypertension and cardiovascular disease. Endothelial...
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SubjectTerms ACE2
adhesion
Aged
Alveoli
Angiotensin
Angiotensin-converting enzyme 2
Blood Coagulation Disorders - blood
Blood Coagulation Disorders - virology
C-reactive protein
Capillaries
Cardiovascular diseases
Case-Control Studies
Cell Adhesion - physiology
Coronaviridae
Coronaviruses
COVID-19
COVID-19 - blood
COVID-19 - metabolism
COVID-19 - pathology
COVID-19 infection
COVID-19 Testing
Cytokines
Degradation
Dimers
disease severity
Endothelial cells
Endothelium, Vascular - metabolism
Female
Ferritin
Glycocalyx
Glycocalyx - metabolism
Glycocalyx - pathology
Glycocalyx - virology
Glycoproteins
Health services
Heparan sulfate proteoglycans
Heparin
Heparin - pharmacology
Homeostasis
Human Umbilical Vein Endothelial Cells
Humans
Hypertension
Inflammation
Inflammatory response
Interleukin 1
Interleukin 6
Interleukin-1beta - blood
Interleukin-6 - blood
Leukocytes
Lipid peroxidation
Lipids
Low molecular weight heparin
Low molecular weights
Lymphopenia
Male
Middle Aged
Molecular weight
Neutrophilia
Oxidation-Reduction
Peptidyl-dipeptidase A
Permeability
Peroxidation
Perturbation
Plasma
Proteoglycans
Reactive oxygen species
Respiratory diseases
SARS-CoV-2
Severe acute respiratory syndrome coronavirus 2
Shedding
Thromboembolism
Thrombosis
Thrombosis - metabolism
Umbilical vein
Vascular dysfunction
Viral diseases
Title Heparin prevents in vitro glycocalyx shedding induced by plasma from COVID-19 patients
URI https://dx.doi.org/10.1016/j.lfs.2021.119376
https://www.ncbi.nlm.nih.gov/pubmed/33781826
https://www.proquest.com/docview/2528502191
https://www.proquest.com/docview/2507146138
https://www.proquest.com/docview/2540479307
https://pubmed.ncbi.nlm.nih.gov/PMC7997864
Volume 276
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