Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice

Blood

Volumn 120, Issue 8, 2012, Pages 1742-1751

  Axelsson, Jakob ^a   Xu, Ding ^a   Kang, Bit Na ^b   Nussbacher, Julia K ^a   Handel, Tracy M ^c   Ley, Klaus ^d   Sriramarao, P ^b   Esko, Jeffrey D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARAN SULFATE; HEPARAN SULFATE 2 O SULFOTRANSFERASE; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 2; N ACETYLGLUCOSAMINE; SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; ENDOTHELIUM CELL; ENZYME INACTIVATION; ENZYME STRUCTURE; EXPERIMENTAL ANIMAL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SULFATION;

EID: 84865440249     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-03-417139     Document Type: Article

References (49)

1. Ley K, Cerrito M, Arfors KE. Sulfated polysaccharides inhibit leukocyte rolling in rabbit mesentery venules. Am J Physiol. 1991;260:1667-1673.
2. Wang LC, Brown JR, Varki A, Esko JD. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L-and P-selectins. J Clin Invest. 2002;110(1):127-136. (Pubitemid 34743473)
3. Young E. The anti-inflammatory effects of heparin and related compounds. Thromb Res. 2008;122(6):743-752.
4. Wang L, Fuster M, Sriramarao P, Esko JD. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol. 2005;6(9):902-910. (Pubitemid 43090445)
5. Zuberi RI, Ge XN, Jiang S, et al. Deficiency of endothelial heparan sulfates attenuates allergic airway inflammation. J Immunol. 2009;183(6):3971-3979.
6. Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest. 2001;108(2):169-173. (Pubitemid 32656238)
7. Esko JD, Selleck SB. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 2002;71:435-471. (Pubitemid 34800227)
8. Stanford KI, Wang L, Castagnola J, et al. Heparan sulfate 2-O-sulfotransferase is required for triglyceride-rich lipoprotein clearance. J Biol Chem. 2010;285(1):286-294.
9. Constien R, Forde A, Liliensiek B, et al. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line. Genesis. 2001;30(1):36-44.
10. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999;8(4):265-277. (Pubitemid 29523965)
11. Bame KJ, Esko JD. Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. J Biol Chem. 1989;264:8059-8065. (Pubitemid 19137289)
12. Skidmore MA, Guimond SE, Dumax-Vorzet AF, Yates EA, Turnbull JE. Disaccharide compositional analysis of heparan sulfate and heparin polysaccharides using UV or high-sensitivity fluorescence (BODIPY) detection. Nat Protoc. 2010;5(12):1983-1992.
13. Jung U, Bullard DC, Tedder TF, Ley K. Velocity differences between L- and P-selectin-dependent neutrophil rolling in venules of mouse cremaster muscle in vivo. Am J Physiol. 1996;271(6):H2740-H2747.
14. Siemsen DW, Schepetkin IA, Kirpotina LN, Lei B, Quinn MT. Neutrophil isolation from nonhuman species. Methods Mol Biol. 2007;412:21-34.
15. Allen SJ, Hamel DJ, Handel TM. A rapid and efficient way to obtain modified chemokines for functional and biophysical studies. Cytokine. 2011;55(2):168-173.
16. Rong J, Habuchi H, Kimata K, Lindahl U, Kusche-Gullberg M. Substrate specificity of the heparan sulfate hexuronic acid 2-O-sulfotransferase. Biochemistry. 2001;40(18):5548-5555. (Pubitemid 32458257)
17. Maccarana M, Sakura Y, Tawada A, Yoshida K, Lindahl U. Domain structure of heparan sulfates from bovine organs. J Biol Chem. 1996;271:17804-17810. (Pubitemid 26250756)
18. Bullock SL, Fletcher JM, Beddington RS, Wilson VA. Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 1998;12(12):1894-1906. (Pubitemid 28304341)
19. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol. 2001;230(2):230-242. (Pubitemid 32171420)
20. Linhardt RJ. Analysis of glycosaminoglycans with polysaccharide lyases. Curr Protoc Mol Biol. 2001;Chapter 17:Unit17 13B.
21. Bai XM, Esko JD. An animal cell mutant defective in heparan sulfate hexuronic acid 2-O-sulfation. J Biol Chem. 1996;271:17711-17717. (Pubitemid 26250742)
22. Merry CLR, Bullock SL, Swan DC, et al. The molecular phenotype of heparan sulfate in the Hs2st-/- mutant mouse. J Biol Chem. 2001;276(38):35429-35434.
23. Ledin J, Staatz W, Li JP, et al. Heparan sulfate structure in mice with genetically modified heparan sulfate production. J Biol Chem. 2004;279(41):42732-42741. (Pubitemid 39372160)
24. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 2003;19(1):71-82. (Pubitemid 36859902)
25. Sunderkotter C, Nikolic T, Dillon MJ, et al. Sub-populations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol. 2004;172(7):4410-4417. (Pubitemid 38375256)
26. Jemth P, Kreuger J, Kusche-Gullberg M, Sturiale L, Giménez-Gallego G, Lindahl U. Biosynthetic oligosaccharide libraries for identification of protein-binding heparan sulfate motifs: exploring the structural diversity by screening for fibroblast growth factor (FGF) 1 and FGF2 binding. J Biol Chem. 2002;277(34):30567-30573. (Pubitemid 34970750)
27. Kreuger J, Salmivirta M, Sturiale L, Giménez-Gallego G, Lindahl U. Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2. J Biol Chem. 2001;276(33):30744-30752.
28. Spillmann D, Witt D, Lindahl U. Defining the interleukin-8-binding domain of heparan sulfate. J Biol Chem. 1998;273:15487-15493. (Pubitemid 28298157)
29. Rosen SD. Ligands for L-selectin: homing, inflammation, and beyond. Annu Rev Immunol. 2004;22:129-156. (Pubitemid 38680420)
30. Norgard-Sumnicht KE, Varki A. Endothelial heparan sulfate proteoglycans that bind to L-selectin have glucosamine residues with unsubstituted amino groups. J Biol Chem. 1995;270:12012-12024.
31. Norgard-Sumnicht KE, Varki NM, Varki A. Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endothelial cells. Science. 1993;261:480-483. (Pubitemid 23276559)
32. Giuffre L, Cordey AS, Monai N, Tardy Y, Schapira M, Spertini O. Monocyte adhesion to activated aortic endothelium: role of L-selectin and heparan sulfate proteoglycans. J Cell Biol. 1997;136(4):945-956. (Pubitemid 27098749)
33. Zakrzewicz A, Gräfe M, Terbeek D, et al. L-selectin-dependent leukocyte adhesion to microvascular but not to macrovascular endothelial cells of the human coronary system. Blood. 1997;89:3228-3235. (Pubitemid 27229807)
34. Tu LL, Chen AJ, Delahunty MD, et al. L-selectin binds to P-selectin glycoprotein ligand-1 on leukocytes: interactions between the lectin, epidermal growth factor, and consensus repeat domains of the selectins determine ligand binding specificity. J Immunol. 1996;157:3995-4004. (Pubitemid 126449310)
35. Rivera-Nieves J, Burcin TL, Olson TS, et al. Critical role of endothelial P-selectin glycoprotein ligand 1 in chronic murine ileitis. J Exp Med. 2006;203(4):907-917.
36. Leppanen A, Parviainen V, Ahola-Iivarinen E, Kalkkinen N, Cummings RD. Human L-selectin preferentially binds synthetic glycosulfopeptides modeled after endoglycan and containing tyrosine sulfate residues and sialyl Lewis x in core 2 O-glycans. Glycobiology. 2010;20(9):1170-1185.
37. Alon R, Fuhlbrigge RC, Finger EB, Springer TA. Interactions through L-selectin between leukocytes and adherent leukocytes nucleate rolling adhesions on selectins and VCAM-1 in shear flow. J Cell Biol. 1996;135:849-865. (Pubitemid 26372938)
38. Fuhlbrigge RC, Alon R, Puri KD, Lowe JB, Springer TA. Sialylated, fucosylated ligands for L-selectin expressed on leukocytes mediate tethering and rolling adhesions in physiologic flow conditions. J Cell Biol. 1996;135:837-848. (Pubitemid 26372937)
39. Bao X, Moseman EA, Saito H, et al. Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes. Immunity. 2010;33(5):817-829.
40. 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. 1998;101(4):877-889. (Pubitemid 28096085)
41. Stringer SE, Forster MJ, Mulloy B, Bishop CR, Graham GJ, Gallagher JT. Characterization of the binding site on heparan sulfate for macrophage inflammatory protein 1alpha. Blood. 2002;100(5):1543-1550. (Pubitemid 34925125)
42. Lau EK, Paavola CD, Johnson Z, et al. Identification of the glycosaminoglycan binding site of the CC chemokine, MCP-1: implications for structure and function in vivo. J Biol Chem. 2004;279(21):22294-22305. (Pubitemid 38679426)
43. Sarrazin S, Bonnaffe D, Lubineau A, Lortat-Jacob H. Heparan sulfate mimicry: a synthetic glycoconjugate that recognizes the heparin binding domain of interferon-gamma inhibits the cytokine activity. J Biol Chem. 2005;280(45):37558-37564. (Pubitemid 41642364)
44. Lortat-Jacob H, Turnbull JE, Grimaud JA. Molecular organization of the interferon gamma-binding domain in heparan sulphate. Biochem J. 1995;310:497-505.
45. Li X, Steeber DA, Tang MLK, Farrar MA, Perlmutter RM, Tedder TF. Regulation of L-selectin-mediated rolling through receptor dimerization. J Exp Med. 1998;188:1385-1390. (Pubitemid 28478028)
46. Krenn EC, Wille I, Gesslbauer B, Poteser M, van Kuppevelt TH, Kungl AJ. Glycanogenomics: a qPCR-approach to investigate biological glycan function. Biochem Biophys Res Commun. 2008;375(3):297-302.
47. Celie JW, Rutjes NW, Keuning ED, et al. Subendothelial heparan sulfate proteoglycans become major L-selectin and monocyte chemoattractant protein-1 ligands upon renal ischemia/reperfusion. Am J Pathol. 2007;170(6):1865-1878. (Pubitemid 47339261)
48. Celie JW, Beelen RH, van den Born J. Heparan sulfate proteoglycans in extravasation: assisting leukocyte guidance. Front Biosci. 2009;14:4932-4949.
49. Lawrence R, Lu H, Rosenberg RD, Esko JD, Zhang L. Disaccharide structure code for the easy representation of constituent oligosaccharides from glycosaminoglycans. Nat Methods. 2008;5(4):291-292. (Pubitemid 351455150)