Evidence mapPaperPMID 36459240Full record

ArticleAngiogenesis2023

Proinflammatory activity of VEGF-targeted treatment through reversal of tumor endothelial cell anergy.

Patrycja Nowak-Sliwinska, Judy R van Beijnum, Christian J Griffioen, Zowi R Huinen, Nadine Grima Sopesens, Ralph Schulz, Samir V Jenkins, Ruud P M Dings, Floris H Groenendijk, Elisabeth J M Huijbers and 8 more

Open access · hybridAbstract read
In one paragraph

Article in Angiogenesis, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 36 papers.

0numbers the graph read from it
0cells of the map it votes in
36citing papers in PubMed
3.5field-weighted citation impact, top 6% 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

36 citing papers in PubMed, 48 citations in OpenAlex.

  1. Targeting the Barriers Driving Immune Exclusion.Pharmaceuticals (Basel, Switzerland) · 2026
    Review
  2. Article
  3. Article
  4. Article
  5. Review
  6. Article
  7. Review
  8. LGMNFrontiers in immunology · 2026
    Article
  9. Article
  10. Review
  11. Review
  12. Review
  13. Article
  14. Article
  15. Review
  16. Embryonic reprogramming of the tumor vasculature reveals targets for cancer therapy.Proceedings of the National Academy of Sciences of the United States of America · 2025
    Article
  17. Article
  18. Review
  19. Review
  20. Review
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

18 authors at 10 institutions in 4 countries.

Patrycja Nowak-Sliwinska *Angiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands. Patrycja.Nowak-Sliwinska@unige.ch.ORCID 0000-0002-8299-0444
Judy R van Beijnum *Angiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Christian J GriffioenAngiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Zowi R HuinenAngiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Nadine Grima SopesensAngiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Ralph SchulzAngiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Samir V JenkinsDepartment of Radiation Oncology, University of Arkansas for Medical Sciences, Little Rock, AR, USA.
Ruud P M DingsDepartment of Radiation Oncology, University of Arkansas for Medical Sciences, Little Rock, AR, USA.
Floris H GroenendijkDepartment of Pathology, Erasmus MC Cancer Institute, University Medical Center Rotterdam, Rotterdam, The Netherlands.
Elisabeth J M HuijbersAngiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Victor L J L ThijssenAngiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Eric JonaschDepartment of Genitourinary Oncology, MD Anderson Cancer Center, Houston, TX, USA.
Florry A Vyth-DreeseDivision of Immunology, The Netherlands Cancer Institute, Amsterdam, The Netherlands.
Ekaterina S JordanovaCenter for Gynaecologic Oncology Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.
Axel BexDepartment of Urology, The Netherlands Cancer Institute, Amsterdam, The Netherlands.
René BernardsDivision of Molecular Carcinogenesis, Oncode Institute, Amsterdam, The Netherlands.
Tanja D de GruijlImmunotherapy Laboratory, Department of Medical Oncology, Amsterdam UMC, Cancer Center Amsterdam, Amsterdam, The Netherlands.
Arjan W GriffioenAngiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Cancer Center Amsterdam, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands. a.griffioen@amsterdamumc.nl.ORCID 0000-0002-8508-4754
Amsterdam University Medical Centers · NLUniversity of Arkansas for Medical Sciences · USAmsterdam UMC Location University of Amsterdam · NLCentrum voor Gynaecologische Oncologie Amsterdam · NLErasmus MC Cancer Institute · NLOncode Institute · NLRoyal Free London NHS Foundation Trust · GBThe Netherlands Cancer Institute · NLThe University of Texas MD Anderson Cancer Center · USUniversity of Geneva · CH

Funding

Improvement of cellular immunotherapy during dysbiosis- ResubmissionR01CA245083 · UNIV OF ARKANSAS FOR MED SCIS · 2025 to 2025
$424k
NCI NIH HHS R01 CA245083NIGMS NIH HHS P20 GM103625
6 · The paper itself

Abstract

purposeOngoing angiogenesis renders the tumor endothelium unresponsive to inflammatory cytokines and interferes with adhesion of leukocytes, resulting in escape from immunity. This process is referred to as tumor endothelial cell anergy. We aimed to investigate whether anti-angiogenic agents can overcome endothelial cell anergy and provide pro-inflammatory conditions. EXPERIMENTAL

designTissues of renal cell carcinoma (RCC) patients treated with VEGF pathway-targeted drugs and control tissues were subject to RNAseq and immunohistochemical profiling of the leukocyte infiltrate. Analysis of adhesion molecule regulation in cultured endothelial cells, in a preclinical model and in human tissues was performed and correlated to leukocyte infiltration.

resultsIt is shown that treatment of RCC patients with the drugs sunitinib or bevacizumab overcomes tumor endothelial cell anergy. This treatment resulted in an augmented inflammatory state of the tumor, characterized by enhanced infiltration of all major leukocyte subsets, including T cells, regulatory T cells, macrophages of both M1- and M2-like phenotypes and activated dendritic cells. In vitro, exposure of angiogenic endothelial cells to anti-angiogenic drugs normalized ICAM-1 expression. In addition, a panel of tyrosine kinase inhibitors was shown to increase transendothelial migration of both non-adherent and monocytic leukocytes. In primary tumors of RCC patients, ICAM-1 expression was found to be significantly increased in both the sunitinib and bevacizumab-treated groups. Genomic analysis confirmed the correlation between increased immune cell infiltration and ICAM-1 expression upon VEGF-targeted treatment.

conclusionThe results support the emerging concept that anti-angiogenic therapy can boost immunity and show how immunotherapy approaches can benefit from combination with anti-angiogenic compounds.

Indexed as

Angiogenesis InhibitorsCarcinoma, Renal CellEndothelial CellsKidney NeoplasmsNeovascularization, PathologicBevacizumabEndotheliumHumansImmune ToleranceInflammationIntercellular Adhesion Molecule-1Neoplasm InvasivenessSunitinibVascular Endothelial Growth Factor AAngiogenesis InhibitorsBevacizumabIntercellular Adhesion Molecule-1SunitinibVascular Endothelial Growth Factor AAngiogenesisICAM-1Leukocyte infiltrationSunitinibTumor endothelial cell anergy

Identifiers

PMID36459240
PMCPMC10119234
OpenAlexW4310603919

What Socratic holds

Textmetadata
LicenceCC BY
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 Socratic graph.