Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes

Bao, Xingfeng; Moseman, E. Ashley; Saito, Hideo; Petryanik, Bronislawa; Thiriot, Aude; Hatakeyama, Shingo; Ito, Yuki; Kawashima, Hiroto; Yamaguchi, Yu; Lowe, John B.; von Andrian, Ulrich H.; Fukuda, Minoru

doi:10.1016/j.immuni.2010.10.018

Cited by 168Proteoglycans and glycosaminoglycans researchCell Adhesion Molecules ResearchChemokine receptors and signaling

Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes

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Bao, Xingfeng, Moseman, E. Ashley, Saito, Hideo, Petryanik, Bronislawa, Thiriot, Aude, Hatakeyama, Shingo, Ito, Yuki, Kawashima, Hiroto +4 more·2010·Immunity

DOI 10.1016/j.immuni.2010.10.018PMC PMC2996097

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Abstract

Heparan sulfate can bind several adhesion molecules involved in lymphocyte trafficking. However, the in vivo function of endothelial heparan sulfate in lymphocyte homing and stimulation of the immune response has not been elucidated. Here, we generated mutant mice deficient in the enzyme Ext1, which is required for heparan sulfate synthesis, in a Tek-dependent and inducible manner. Chemokine presentation was diminished in the mutant mice, causing the lack of appropriate integrin-mediated adhesion, and resulted in a marked decrease in lymphocyte sticking to high endothelial venules and in recruitment of resident dendritic cells through lymphatic vessels to the lymph nodes. As a consequence, mutant mice displayed a severe impairment in lymphocyte homing and a compromised contact hypersensitivity response. By contrast, lymphocyte rolling was increased because of loss of electrostatic repulsion by heparan sulfate. These results demonstrate critical roles of endothelial heparan sulfate in immune surveillance and immune response generation.

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CCL21 binds heparan sulfate and collagens in the interstitium via its positively charged C terminus, promoting haptotaxis of DCs and T cells toward initial LVs.
“CCL21 has a positively charged C terminus that binds heparan sulfate and collagens in the interstitium and which, therefore, promotes haptotaxis (migration up a gradient of surface-bound chemoattractant) of DCs and T cells toward initial LVs (101, 102).”
From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [101]
The Introduction (page not available) says CCL21 binds heparan sulfate and that cell-bound CCL21 helps guide dendritic cells toward draining lymph nodes via lymphatic vessels. The Results (page not available) mention possible CCL21 binding to collagen IV, but in lymph-node venules, not the interstitium. Our copy does not attribute these interactions to a positively charged C terminus or show haptotaxis of both dendritic cells and T cells toward initial lymphatic vessels; it describes lymphocyte entry through blood-vessel HEVs instead. (LLM, conf=0.88)
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Authors: Bao, X., Moseman, E. A., Saito, H., Petryanik, B., Thiriot, A., Hatakeyama, S., Ito, Y., Kawashima, H., Yamaguchi, Y., Lowe, J. B., von Andrian, U. H., & Fukuda, M.
Affiliations: Sanford Burnham Prebys Medical Discovery Institute (US)
Harvard University (US)
Case Western Reserve University (US)
Corresponding author: Fukuda, Minoru
ORCID: Bao, Xingfeng
Moseman, E. Ashley
Thiriot, Aude
Hatakeyama, Shingo
Ito, Yuki
Kawashima, Hiroto
Yamaguchi, Yu
Fukuda, Minoru
Venue: Immunity
Publisher: Elsevier BV
Published: 2010-11
Volume: 33
Issue: 5
Pages: 817-829
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2010.10.018
PMC: PMC2996097
OpenAlex: W2037665285
Cited by: 167
References: 49
Citations by year: 2026: 7 · 2025: 10 · 2024: 6 · 2023: 6 · 2022: 9 · 2021: 14 · 2020: 4 · 2019: 14 · 2018: 16 · 2017: 10 · 2016: 10 · 2015: 10 · 2014: 13 · 2013: 13 · 2012: 14
FWCI: 4.97
Type: journal article
Language: en
Update notices: erratum (2011-05-27)
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1020 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Japan Society for the Promotion of Science (22659018, 21390023)
National Cancer Institute (P01CA071932)
National Institute of Allergy and Infectious Diseases (R01AI072252, R01AI069259)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
Keywords: EXT1, lymphocyte homing, dendritic cell recruitment, lymph nodes, high endothelial venules, integrin-mediated adhesion, lymphatic vessels, contact hypersensitivity, immune surveillance, heparan sulfate synthesis
MeSH terms: Exostosin 1, Animals, Cell Adhesion, Dendritic Cells, Endothelium, Vascular, Heparan Sulfate, Lymph Nodes, Lymphocytes, Mice, Inbred C57BL, Venules, Integrins, N-Acetylglucosaminyltransferases, Chemokines, Mice

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Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes

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