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Cited by 133Proteoglycans and glycosaminoglycans researchLymphatic System and DiseasesSphingolipid Metabolism and Signaling

Binding of hyaluronan to the native lymphatic vessel endothelial receptor LYVE-1 is critically dependent on receptor clustering and hyaluronan organization

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Lawrance, William, Banerji, Suneale, Day, Anthony J., Bhattacharjee, Shaumick, Jackson, David G.·2016·Journal of Biological Chemistry
DOI 10.1074/jbc.m115.708305PMC PMC4825007
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Abstract

The lymphatic endothelial receptor LYVE-1 has been implicated in both uptake of hyaluronan (HA) from tissue matrix and in facilitating transit of leukocytes and tumor cells through lymphatic vessels based largely onin vitrostudies with recombinant receptor in transfected fibroblasts. Curiously, however, LYVE-1 in lymphatic endothelium displays little if any binding to HAin vitro, and this has led to the conclusion that the native receptor is functionally silenced, a feature that is difficult to reconcile with its proposedin vivofunctions. Nonetheless, as we reported recently, LYVE-1 can function as a receptor for HA-encapsulated Group A streptococci and mediate lymphatic dissemination in mice. Here we resolve these paradoxical findings and show that the capacity of LYVE-1 to bind HA is strictly dependent on avidity, demanding appropriate receptor self-association and/or HA multimerization. In particular, we demonstrate the prerequisite of a critical LYVE-1 threshold density and show that HA binding may be elicited in lymphatic endothelium by surface clustering with divalent LYVE-1 mAbs. In addition, we show that cross-linking of biotinylated HA in streptavidin multimers or supramolecular complexes with the inflammation-induced protein TSG-6 enables binding even in the absence of LYVE-1 cross-linking. Finally, we show that endogenous HA on the surface of macrophages can engage LYVE-1, facilitating their adhesion and transit across lymphatic endothelium. These results reveal LYVE-1 as a low affinity receptor tuned to discriminate between different HA configurations through avidity and establish a new mechanistic basis for the functions ascribed to LYVE-1 in matrix HA binding and leukocyte traffickingin vivo.

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  • LYVE-1 is necessary for macrophage entry into initial LVs.

    “LYVE-1 is also necessary for macrophage entry into initial LVs (117).”

    From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [117]

    The Results report that blocking LYVE-1 reduced macrophage transit across lymphatic endothelial cell monolayers in vitro. They do not establish that LYVE-1 is necessary for macrophage entry into initial lymphatic vessels: transit still occurred with blocking, and the Discussion says studies of LYVE-1 deletion and leukocyte migration in lymphatics were ongoing. No page numbers are available in our copy. (LLM, conf=0.90)

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Authors
Lawrance, W., Banerji, S., Day, A. J., Bhattacharjee, S., & Jackson, D. G.
Affiliations
  • John Radcliffe Hospital (GB)
  • Wellcome Centre for Cell-Matrix Research (GB)
Corresponding author
Jackson, David G.
ORCID
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2016-04
Volume
291
Issue
15
Pages
8014-8030
ISSN
0021-9258 (ISSN-L)
DOI
10.1074/jbc.m115.708305
PMC
PMC4825007
OpenAlex
W2290737450
Cited by
133
References
3
Citations by year
2026: 11 · 2025: 13 · 2024: 13 · 2023: 11 · 2022: 12 · 2021: 12 · 2020: 18 · 2019: 12 · 2018: 11 · 2017: 12 · 2016: 8
FWCI
9.87
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Biological Chemistry (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research Explorer (The University of Manchester) (publishedVersion, cc-by)
Funders
Medical Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
  • Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sphingolipid Metabolism and Signaling
Keywords
LYVE-1, hyaluronic acid, lymphatic endothelium, receptor clustering, receptor avidity, TSG-6, macrophage adhesion, leukocyte migration, lymphatic dissemination, Streptococcus pyogenes, low-affinity receptor
MeSH terms
Adult, Animals, Cell Adhesion, Cell Movement, Cells, Cultured, Endothelium, Lymphatic, Humans, Hyaluronic Acid, Macrophages, Models, Molecular, Hyaluronan Receptors, Jurkat Cells, Vesicular Transport Proteins, Mice, Protein Multimerization, HEK293 Cells

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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