The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.
Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses
Abstract
Here we have studied the involvement of endothelial heparan sulfate in inflammation by inactivating the enzyme N-acetyl glucosamine N-deacetylase-N-sulfotransferase-1 in endothelial cells and leukocytes, which is required for the addition of sulfate to the heparin sulfate chains. Mutant mice developed normally but showed impaired neutrophil infiltration in various inflammation models. These effects were due to changes in heparan sulfate specifically in endothelial cells. Decreased neutrophil infiltration was partially due to altered rolling velocity correlated with weaker binding of L-selectin to endothelial cells. Chemokine transcytosis across endothelial cells and presentation on the cell surface were also reduced, resulting in decreased neutrophil firm adhesion and migration. Thus, endothelial heparan sulfate has three functions in inflammation: by acting as a ligand for L-selectin during neutrophil rolling; in chemokine transcytosis; and by binding and presenting chemokines at the lumenal surface of the endothelium.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Crossbreeding Ndst1 f/f mice with TekCre mice resulted in greater than 95% inactivation of the gene in endothelial cells derived from the liver or lung microvasculature.
“Crossbreeding Ndst1 f/f mice with TekCre mice resulted in greater than 95% inactivation of the gene in endothelial cells derived from the liver or lung microvasculature (47).”
From Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members (2007) · cites this paper as [47]
These changes in HS led to reduced leukocyte extravasation due to altered binding of L-selectin and chemokines to the endothelium.
“These changes in HS led to reduced leukocyte extravasation due to altered binding of L-selectin and chemokines to the endothelium (47).”
From Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members (2007) · cites this paper as [47]
Altering Ndst1 in these cells led to changes in HS composition similar to those observed in hepatocytes, except that 2-O-sulfation was not reduced as dramatically.
“Altering Ndst1 in these cells also led to changes in HS composition similar to those observed in hepatocytes, except that 2-O-sulfation was not reduced as dramatically (47).”
From Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members (2007) · cites this paper as [47]
Citations
Cites
Order Out of Chaos: Assembly of Ligand Binding Sites in Heparan Sulfate
Esko, J. D., & Selleck, S. B. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135458 · Cited by 1,495
Self-citationWang, L., Brown, J. R., Varki, A., & Esko, J. D. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0214996 · Cited by 288
Self-citationGiuffrè, L., Cordey, A.-S., Monai, N., Tardy, Y., Schapira, M., & Spertini, O. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.4.945 · Cited by 122
Flagged first, then by citations
Research works printed but not linked: 52
- Springer, T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76, 301–314 (1994). · DOI
- Lowe, J.B. Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr. Opin. Cell Biol. 15, 531–538 (2003). · DOI
- Ley, K. Arrest chemokines. Microcirculation 10, 289–295 (2003). · DOI
- Varki, A. Selectin ligands: Will the real ones please stand up? J. Clin. Invest. 99, 158–162 (1997). · DOI
- Rosen, S.D. Ligands for L-selectin: homing, inflammation, and beyond. Annu. Rev. Immunol. 22, 129–156 (2004). · DOI
- Leppanen, A., Yago, T., Otto, V.I., McEver, R.P. & Cummings, R.D. Model glycosulfopeptides from P-selectin glycoprotein ligand-1 require tyrosine sulfation and a core 2-branched O-glycan to bind to L-selectin. J. Biol. Chem. 278, 26391–26400 (2003). · DOI
- Jung, U. & Ley, K. Mice lacking two or all three selectins demonstrate overlapping and distinct functions for each selectin. J. Immunol. 162, 6755–6762 (1999). · DOI
- Robinson, S.D. et al. Multiple, targeted deficiencies in selectins reveal a predominant role for P-selectin in leukocyte recruitment. Proc. Natl. Acad. Sci. USA 96, 11452–11457 (1999). · DOI
- Norgard-Sumnicht, K.E., Varki, N.M. & Varki, A. Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endothelial cells. Science 261, 480–483 (1993). · DOI · Paper page
- Nelson, R.M. et al. Heparin oligosaccharides bind L- and P-Selectin and inhibit acute inflammation. Blood 82, 3253–3258 (1993). · DOI
- Yoshie, O., Imai, T. & Nomiyama, H. Chemokines in immunity. Adv. Immunol. 78, 57–110 (2001). · DOI
- Middleton, J., Patterson, A.M., Gardner, L., Schmutz, C. & Ashton, B.A. Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 100, 3853–3860 (2002). · DOI
- Lortat-Jacob, H., Grosdidier, A. & Imberty, A. Structural diversity of heparan sulfate binding domains in chemokines. Proc. Natl. Acad. Sci. USA 99, 1229–1234 (2002). · DOI
- Lau, E.K., Allen, S., Hsu, A.R. & Handel, T.M. Chemokine-receptor interactions: GPCRs, glycosaminoglycans and viral chemokine binding proteins. Adv. Protein Chem. 68, 351–391 (2004). · DOI
- Lander, A.D., Nie, Q. & Wan, F.Y. Do morphogen gradients arise by diffusion? Dev. Cell 2, 785–796 (2002). · DOI
- Rot, A. Neutrophil attractant/activation protein-1 (interleukin-8) induces in vitro neutrophil migration by haptotactic mechanism. Eur. J. Immunol. 23, 303–306 (1993). · DOI
- Wiedermann, C.J. et al. Monocyte haptotaxis induced by the RANTES chemokine. Curr. Biol. 3, 735–739 (1993). · DOI
- Orban, P.C., Chui, D. & Marth, J.D. Tissue- and site-specific DNA recombination in transgenic mice. Proc. Natl. Acad. Sci. USA 89, 6861–6865 (1992). · DOI
- Grobe, K. et al. Heparan sulfate and development: Differential roles of the N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes. Biochim. Biophys. Acta Gen. Subj. 1573, 209–215 (2002). · DOI
- Holmborn, K. et al. Heparan sulfate synthesized by mouse embryonic stem cells deficient in NDST1 and NDST2 is 6-O-sulfated but contains no N-sulfate groups. J. Biol. Chem. 279, 42355–42358 (2004). · DOI
- Ringvall, M. et al. Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking N-deacetylase/N-sulfotransferase-1. J. Biol. Chem. 275, 25926–25930 (2000). · DOI · Paper page
- Grobe, K. et al. Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function. Development, advance online publication, 14 July 2005 10.1242/dev.01935. · DOI · Paper page
- Fan, G. et al. Targeted disruption of NDST-1 gene leads to pulmonary hypoplasia and neonatal respiratory distress in mice. FEBS Lett. 467, 7–11 (2000). · DOI
- Forsberg, E. et al. Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400, 773–776 (1999). · DOI
- Humphries, D.E. et al. Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400, 769–772 (1999). · DOI
- Ledin, J. et al. Heparan sulfate structure in mice with genetically modified heparan sulfate production. J. Biol. Chem. 279, 42732–42741 (2004). · DOI · Paper page
- Kisanuki, Y.Y. et al. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230–242 (2001). · DOI · Paper page
- Bame, K.J. & Esko, J.D. Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. J. Biol. Chem. 264, 8059–8065 (1989). · DOI
- Toyoda, H., Nagashima, T., Hirata, R., Toida, T. & Imanari, T. Sensitive high-performance liquid chromatographic method with detection for the determination of heparin and heparan sulfate in biological samples: application to human urinary heparan sulfate. J. Chromatogr. B Biomed. Sci. Appl. 704, 19–24 (1997). · DOI
- Kanegae, Y. et al. Efficient gene activation in mammalian cells by using recombinant adenovirus expressing site-specific Cre recombinase. Nucleic Acids Res. 23, 3816–3821 (1995). · DOI
- Ishihara, M., Kiefer, M.C., Barr, P.J., Guo, Y. & Swiedler, S.J. Selection of COS cell mutants defective in the biosynthesis of heparan sulfate proteoglycan. Anal. Biochem. 206, 400–407 (1992). · DOI
- Norgard-Sumnicht, K. & Varki, A. Endothelial heparan sulfate proteoglycans that bind to L-selectin have glucosamine residues with unsubstituted amino groups. J. Biol. Chem. 270, 12012–12024 (1995). · DOI · Paper page
- Koenig, A., Norgard-Sumnicht, K., Linhardt, R. & Varki, A. Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins. Implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J. Clin. Invest. 101, 877–889 (1998). · DOI
- Tedder, T.F., Steeber, D.A. & Pizcueta, P. L-selectin-deficient mice have impaired leukocyte recruitment into inflammatory sites. J. Exp. Med. 181, 2259–2264 (1995). · DOI
- Middleton, J. et al. Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91, 385–395 (1997). · DOI
- Schnitzer, J.E. & Oh, P. Albondin-mediated capillary permeability to albumin. Differential role of receptors in endothelial transcytosis and endocytosis of native and modified albumins. J. Biol. Chem. 269, 6072–6082 (1994). · DOI
- McEver, R.P. & Cummings, R.D. Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest. 100, 485–492 (1997). · DOI
- Sperandio, M. et al. P-selectin glycoprotein ligand-1 mediates L-selectin-dependent leukocyte rolling in venules. J. Exp. Med. 197, 1355–1363 (2003). · DOI
- Hayward, R., Nossuli, T.O. & Lefer, A.M. Heparinase III exerts endothelial and cardioprotective effects in feline myocardial ischemia-reperfusion injury. J. Pharmacol. Exp. Ther. 283, 1032–1038 (1997).
- Xie, X. et al. Inhibition of selectin-mediated cell adhesion and prevention of acute inflammation by nonanticoagulant sulfated saccharides - Studies with carboxyl-reduced and sulfated heparin and with trestatin A sulfate. J. Biol. Chem. 275, 34818–34825 (2000). · DOI
- Kawashima, H. et al. Collagen XVIII, a basement membrane heparan sulfate proteoglycan, interacts with L-selectin and monocyte chemoattractant protein-1. J. Biol. Chem. 278, 13069–13076 (2003). · DOI
- Tyrrell, D.J., Horne, A.P., Holme, K.R., Preuss, J.M. & Page, C.P. Heparin in inflammation: potential therapeutic applications beyond anticoagulation. Adv. Pharmacol. 46, 151–208 (1999). · DOI
- Mayadas, T.N., Johnson, R.C., Rayburn, H., Hynes, R.O. & Wagner, D.D. Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell 74, 541–554 (1993). · DOI
- Xia, L. et al. P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest. 109, 939–950 (2002). · DOI
- Humphries, D.E., Lanciotti, J. & Karlinsky, J.B. cDNA cloning, genomic organization and chromosomal localization of human heparan glucosaminyl N-deacetylase/N-sulphotransferase-2. Biochem. J. 332, 303–307 (1998). · DOI
- Marelli-Berg, F.M., Peek, E., Lidington, E.A., Stauss, H.J. & Lechler, R.I. Isolation of endothelial cells from murine tissue. J. Immunol. Methods 244, 205–215 (2000). · DOI
- Heffernan, M. & Dennis, J.W. Polyoma and hamster papovavirus large T antigen-mediated replication of expression shuttle vectors in Chinese hamster ovary cells. Nucleic Acids Res. 19, 85–92 (1991). · DOI
- Aikawa, J., Grobe, K., Tsujimoto, M. & Esko, J.D. Multiple isozymes of heparan sulfate/heparin GlcNAc N-deacetylase/N-sulfotransferase: structure and activity of the fourth member, NDST4. J. Biol. Chem. 276, 5876–5882 (2001). · DOI
- Bai, X. & Esko, J.D. An animal cell mutant defective in heparan sulfate hexuronic acid 2-O-sulfation. J. Biol. Chem. 271, 17711–17717 (1996). · DOI
- Romano, M. et al. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6, 315–325 (1997). · DOI
- Forlow, S.B. & Ley, K. Selectin-independent leukocyte rolling and adhesion in mice deficient in E-, P-, and L-selectin and ICAM-1. Am. J. Physiol. Heart Circ. Physiol. 280, H634–H641 (2001). · DOI
- Allport, J.R. et al. Neutrophils from MMP-9- or neutrophil elastase-deficient mice show no defect in transendothelial migration under flow in vitro. J. Leukoc. Biol. 71, 821–828 (2002). · DOI
Cited by
Sorted by citations
Neutrophil recruitment and function in health and inflammation
Kolaczkowska, E., & Kubes, P. (2013) · Nature Reviews Immunology · doi:10.1038/nri3399 · Cited by 5,472
Heparan sulphate proteoglycans fine-tune mammalian physiology
Bishop, J. R., Schuksz, M., & Esko, J. D. (2007) · Nature · doi:10.1038/nature05817 · Cited by 1,631
Self-citationImmune cell migration in inflammation: present and future therapeutic targets
Luster, A. D., Alon, R., & von Andrian, U. H. (2005) · Nature Immunology · doi:10.1038/ni1275 · Cited by 1,313
The extracellular matrix and the immune system: A mutually dependent relationship
Sutherland, T. E., Dyer, D. P., & Allen, J. E. (2023) · Science · doi:10.1126/science.abp8964 · Cited by 519
Thomas, S. R., Witting, P. K., & Drummond, G. R. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2027 · Cited by 383
The blood-brain barrier, chemokines and multiple sclerosis
Holman, D. W., Klein, R. S., & Ransohoff, R. M. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.07.019 · Cited by 247
MacArthur, J. M., Bishop, J. R., Stanford, K. I., Wang, L., Bensadoun, A., Witztum, J. L., & Esko, J. D. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29154 · Cited by 216
Self-citationBao, X., Moseman, E. A., Saito, H., Petryanik, B., Thiriot, A., Hatakeyama, S., Ito, Y., Kawashima, H., Yamaguchi, Y., Lowe, J. B., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.10.018 · Cited by 167
Habuchi, H., Nagai, N., Sugaya, N., Atsumi, F., Stevens, R. L., & Kimata, K. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m607434200 · Cited by 139
Jhingran, A., Kasahara, S., Shepardson, K. M., Junecko, B. A. F., Heung, L. J., Kumasaka, D. K., Knoblaugh, S. E., Lin, X., Kazmierczak, B. I., Reinhart, T. A., et al. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1004589 · Cited by 108
Human genetic disorders and knockout mice deficient in glycosaminoglycan
Mizumoto, S., Yamada, S., & Sugahara, K. (2014) · BioMed Research International · doi:10.1155/2014/495764 · Cited by 54
Heparan Sulfate Modulates Slit3-Induced Endothelial Cell Migration
Qiu, H., Xiao, W., Yue, J., & Wang, L. (2015) · Methods in Molecular Biology · doi:10.1007/978-1-4939-1714-3_43 · Cited by 12
Self-citation
Metadata
- Authors
- Wang, L., Fuster, M., Sriramarao, P., & Esko, J. D.
- Venue
- Nature Immunology
- Published
- 2005-07-31
- Volume
- 6
- Issue
- 9
- Pages
- 902-910
- ISSN
- 1529-2908
- 1529-2916
- Cited by
- 413
- References
- 3
- Language
- en
- Licence
- www.springer.com/tdm (tdm)
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review