Evidence map›Paper›PMID 27386939›Full record

ArticleArteriosclerosis, thrombosis, and vascular biology2016

New Functional Tools for Antithrombogenic Activity Assessment of Live Surface Glycocalyx.

Sashka Dimitrievska, Liqiong Gui, Amanda Weyers, Tylee Lin, Chao Cai, Wei Wu, Charles T Tuggle, Sumati Sundaram, Jenna L Balestrini, David Slattery and 5 more

Open access · bronzeAbstract readComparative Study
PubMed Full text at PMC Publisher
In one paragraph

Article in Arteriosclerosis, thrombosis, and vascular biology, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 11 papers.

0numbers the graph read from it
0cells of the map it votes in
11citing papers in PubMed
2.1field-weighted citation impact, top 13% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

11 citing papers in PubMed, 22 citations in OpenAlex.

  1. Review
  2. Mechanisms of lung crosstalk with end organs: scientific session V-ReSPIRE 2025.American journal of physiology. Lung cellular and molecular physiology · 2025
    Review
  3. Review
  4. Novel Insights into the Molecular Mechanisms of Atherosclerosis.International journal of molecular sciences · 2023
    Review
  5. Article
  6. Review
  7. Reporting Sex and Sex Differences in Preclinical Studies.Arteriosclerosis, thrombosis, and vascular biology · 2018
    Article
  8. Thrombotic Regulation From the Endothelial Cell Perspectives.Arteriosclerosis, thrombosis, and vascular biology · 2018
    Review
  9. Review
  10. Review
  11. Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

15 authors at 3 institutions in 1 country.

Sashka DimitrievskaFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Liqiong GuiFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Amanda WeyersFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Tylee LinFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Chao CaiFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Wei WuFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Charles T TuggleFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Sumati SundaramFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Jenna L BalestriniFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
David SlatteryFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Lise TchoutaFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Themis R KyriakidesFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
John M TarbellFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Robert J LinhardtFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.).
Laura E NiklasonFrom the Department of Biomedical Engineering (S.D., T.L., W.W., T.R.K., L.E.N.), Department of Anesthesiology (L.G., S.S., J.L.B., L.E.N.), Department of Surgery (W.W., C.T.T.), Department of Medicine (L.T.), and Department of Pharmacology (T.R.K.), Yale University, New Haven, CT; Howard Hughes Medical Institute, Chevy Chase, MD (S.D., R.J.L.); Department of Chemical and Biological Engineering, Rensselaer Polytechnic Institute, Troy, NY (A.W., C.C., R.J.L.); Department of Biomedical Engineering, University of Connecticut, Storrs (D.S.); and Department of Biomedical Engineering, The City College of New York (J.M.T.). laura.niklason@yale.edu.
Howard Hughes Medical Institute · USUniversity of Connecticut · USRensselaer Polytechnic Institute · US

Funding

Yale Clinical and Translational Science Award (U Component)UL1TR001863 · NCATS · YALE UNIVERSITY · PI John H. Krystal, LUCILA OHNO-MACHADO · 2016 to 2026
$102.9M
NRSA Training CoreTL1TR001864 · NCATS · YALE UNIVERSITY · PI CANTLEY, LLOYD G, EDELMAN, E. JENNIFER · 2016 to 2025
$9.9M
Biological Vascular GraftsR01HL083895 · NHLBI · YALE UNIVERSITY · PI NIKLASON, LAURA E · 2006 to 2015
$5.7M
Hyaluronan Coatings for Engineered VesselsR01HL127386 · NHLBI · YALE UNIVERSITY · PI NIKLASON, LAURA E · 2016 to 2019
$2.5M
Howard Hughes Medical InstituteNCATS NIH HHS TL1 TR001864NCATS NIH HHS UL1 TR001863NHLBI NIH HHS R01 HL083895NHLBI NIH HHS R01 HL127386
6 · The paper itself

Abstract

objectiveIt is widely accepted that the presence of a glycosaminoglycan-rich glycocalyx is essential for endothelialized vasculature health; in fact, a damaged or impaired glycocalyx has been demonstrated in many vascular diseases. Currently, there are no methods that characterize glycocalyx functionality, thus limiting investigators' ability to assess the role of the glycocalyx in vascular health. APPROACH AND

resultsWe have developed novel, easy-to-use, in vitro assays that directly quantify live endothelialized surface's functional heparin weights and their anticoagulant capacity to inactivate Factor Xa and thrombin. Using our assays, we characterized 2 commonly used vascular models: native rat aorta and cultured human umbilical vein endothelial cell monolayer. We determined heparin contents to be ≈10 000 ng/cm(2) on the native aorta and ≈10-fold lower on cultured human umbilical vein endothelial cells. Interestingly, human umbilical vein endothelial cells demonstrated a 5-fold lower anticoagulation capacity in inactivating both Factor Xa and thrombin relative to native aortas. We verified the validity and accuracy of the novel assays developed in this work using liquid chromatography-mass spectrometry analysis.

conclusionsOur assays are of high relevance in the vascular community because they can be used to establish the antithrombogenic capacity of many different types of surfaces such as vascular grafts and transplants. This work will also advance the capacity for glycocalyx-targeting therapeutics development to treat damaged vasculatures.

Indexed as

Blood CoagulationAnimalsAntithrombinsAorta, ThoracicBiological AssayCells, CulturedChromatography, LiquidFactor XaGlycocalyxHeparan SulfateHeparinHuman Umbilical Vein Endothelial CellsMaleMass SpectrometryMicroscopy, Electron, TransmissionRats, Sprague-DawleyAntithrombinsFactor XaHeparan SulfateHeparinThrombinanesthesiaendothelial cellsglycocalyxheparinthrombosis

Identifiers

PMID27386939
PMCPMC5283952
OpenAlexW2467093793

What OpenQuestion holds

Textmetadata
LicenceTDM
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.