Evidence map›Paper›PMID 23354168›Full record

ArticleNature cell biology2013

Spatial regulation of VEGF receptor endocytosis in angiogenesis.

Masanori Nakayama, Akiko Nakayama, Max van Lessen, Hiroyuki Yamamoto, Sarah Hoffmann, Hannes C A Drexler, Norimichi Itoh, Tomonori Hirose, Georg Breier, Dietmar Vestweber and 4 more

Erratum issuedAbstract read
In one paragraph

Article in Nature cell biology, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 149 papers.

0numbers the graph read from it
0cells of the map it votes in
149citing papers in PubMed
15.5field-weighted citation impact, top 1% 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

149 citing papers in PubMed, 270 citations in OpenAlex.

  1. Trial
  2. VEGFAngiogenesis · 2026
    Article
  3. Angiogenic Doping: Plausible Yet Difficult to Detect.Sports medicine (Auckland, N.Z.) · 2026
    Review
  4. Article
  5. Review
  6. Article
  7. Article
  8. Article
  9. Article
  10. Neuropilin-1: A Multifaceted Target for Cancer Therapy.Current oncology (Toronto, Ont.) · 2025
    Review
  11. The dual role of VEGF-A in a complex in vitro model of oxaliplatin-induced neurotoxicity: Pain-related and neuroprotective effects.Neurotherapeutics : the journal of the American Society for Experimental NeuroTherapeutics · 2025
    Article
  12. Article
  13. Article
  14. Article
  15. Review
  16. Review
  17. Review
  18. Review
  19. Article
  20. Review

89 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

14 authors at 5 institutions in 3 countries.

Masanori NakayamaMax Planck Institute for Molecular Biomedicine, Department of Tissue Morphogenesis, and University of Muenster, Faculty of Medicine, D-48149 Muenster, Germany. mnakaya@gwdg.de
Akiko Nakayama
Max van Lessen
Hiroyuki Yamamoto
Sarah Hoffmann
Hannes C A Drexler
Norimichi Itoh
Tomonori Hirose
Georg Breier
Dietmar Vestweber
Jonathan A Cooper
Shigeo Ohno
Kozo Kaibuchi
Ralf H Adams
Max Planck Institute for Molecular Biomedicine · DENagoya University · JPYokohama City University · JPFred Hutch Cancer Center · USUniversity Hospital Carl Gustav Carus · DE

Funding

Epsin in Angiogenesis and Vascular RemodelingR01HL093242 · NHLBI · OKLAHOMA MEDICAL RESEARCH FOUNDATION · PI CHEN, HONG, WANG, DA-ZHI · 2009 to 2021
$7.3M
NHLBI NIH HHS R01 HL093242
6 · The paper itself

Abstract

Activities as diverse as migration, proliferation and patterning occur simultaneously and in a coordinated fashion during tissue morphogenesis. In the growing vasculature, the formation of motile, invasive and filopodia-carrying endothelial sprouts is balanced with the stabilization of blood-transporting vessels. Here, we show that sprouting endothelial cells in the retina have high rates of VEGF uptake, VEGF receptor endocytosis and turnover. These internalization processes are opposed by atypical protein kinase C activity in more stable and mature vessels. aPKC phosphorylates Dab2, a clathrin-associated sorting protein that, together with the transmembrane protein ephrin-B2 and the cell polarity regulator PAR-3, enables VEGF receptor endocytosis and downstream signal transduction. Accordingly, VEGF receptor internalization and the angiogenic growth of vascular beds are defective in loss-of-function mice lacking key components of this regulatory pathway. Our work uncovers how vessel growth is dynamically controlled by local VEGF receptor endocytosis and the activity of cell polarity proteins.

Indexed as

Neovascularization, PhysiologicAdaptor Proteins, Signal TransducingAdaptor Proteins, Vesicular TransportAnimalsApoptosis Regulatory ProteinsBlotting, WesternCell Adhesion MoleculesCell Cycle ProteinsCell MovementCell ProliferationCells, CulturedChromatography, High Pressure LiquidEndocytosisEndothelium, VascularEphrin-B2FemaleAdaptor Proteins, Signal TransducingAdaptor Proteins, Vesicular TransportApoptosis Regulatory ProteinsCell Adhesion MoleculesCell Cycle ProteinsDab2 protein, mouseEphrin-B2Pard3 protein, mousePKC-3 proteinProtein Kinase CReceptors, Vascular Endothelial Growth FactorRNA, MessengerRNA, Small Interfering

Identifiers

PMID23354168
PMCPMC3901019
OpenAlexW1970338125

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.