O-glycans direct selectin ligands to lipid rafts on leukocytes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 28, 2015, Pages 8661-8666

  Shao, Bojing ^a   Yago, Tadayuki ^a   Setiadi, Hendra ^a   Wang, Ying ^a,b   Mehta D'Souza, Padmaja ^a   Fu, Jianxin ^a   Crocker, Paul R ^c   Rodgers, William ^b   Xia, Lijun ^a,b   McEver, Rodger P ^a,b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Cell adhesion; Cell signaling; Inflammation; Neutrophil; Uropod

Indexed keywords

DETERGENT; GLYCAN; GLYCOSYLATED PROTEIN; HERMES ANTIGEN; IMMUNOGLOBULIN F(AB) FRAGMENT; LEUKOSIALIN; LIGAND; P SELECTIN GLYCOPROTEIN LIGAND 1; PROTEIN TYROSINE KINASE; SIALIC ACID DERIVATIVE; SIALIDASE; SPHINGOLIPID; CD44 PROTEIN, MOUSE; MEMBRANE PROTEIN; P-SELECTIN LIGAND PROTEIN; POLYSACCHARIDE;

ANIMAL CELL; ARTICLE; CELL POLARITY; CONTROLLED STUDY; ENZYME ACTIVATION; INTRACELLULAR SIGNALING; LEUKOCYTE; LEUKOCYTE MICROPARTICLE; LIPID RAFT; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SOLUBILIZATION; WILD TYPE; ANIMAL; CELL MEMBRANE; METABOLISM;

MURINAE; UROPODA;

ANIMALS; ANTIGENS, CD43; ANTIGENS, CD44; LEUKOCYTES; LIGANDS; MEMBRANE GLYCOPROTEINS; MEMBRANE MICRODOMAINS; MICE; POLYSACCHARIDES;

EID: 84937145116     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1507712112     Document Type: Article

References (63)

1. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: New tools and insights. Nat Rev Mol Cell Biol 11(10):688-699.
2. Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68(3):533-544.
3. Harder T, Scheiffele P, Verkade P, Simons K (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141(4):929-942.
4. Horejsi V, Hrdinka M (2014) Membrane microdomains in immunoreceptor signaling. FEBS Lett 588(15):2392-2397.
5. Levental I, Grzybek M, Simons K (2010) Greasing their way: Lipid modifications determine protein association with membrane rafts. Biochemistry 49(30):6305-6316.
6. Potter BA, Hughey RP, Weisz OA (2006) Role of N- and O-glycans in polarized biosynthetic sorting. Am J Physiol Cell Physiol 290(1):C1-C10.
7. Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol 7(9):678-689.
8. McEver RP, Zhu C (2010) Rolling cell adhesion. Annu Rev Cell Dev Biol 26:363-396.
9. Zarbock A, Ley K, McEver RP, Hidalgo A (2011) Leukocyte ligands for endothelial selectins: Specialized glycoconjugates that mediate rolling and signaling under flow. Blood 118(26):6743-6751.
10. Lokeshwar VB, Bourguignon LY (1991) Post-translational protein modification and expression of ankyrin-binding site(s) in GP85 (Pgp-1/CD44) and its biosynthetic precursors during T-lymphoma membrane biosynthesis. J Biol Chem 266(27):17983-17989.
11. Han H, et al. (2012) Comprehensive characterization of the N-glycosylation status of CD44s by use of multiple mass spectrometry-based techniques. Anal Bioanal Chem 404(2):373-388.
12. McEver RP (2002) Selectins: Lectins that initiate cell adhesion under flow. Curr Opin Cell Biol 14(5):581-586.
13. Katayama Y, Hidalgo A, Chang J, Peired A, Frenette PS (2005) CD44 is a physiological E-selectin ligand on neutrophils. J Exp Med 201(8):1183-1189.
14. Yago T, et al. (2010) Core 1-derived O-glycans are essential E-selectin ligands on neutrophils. Proc Natl Acad Sci USA 107(20):9204-9209.
15. Li F, et al. (1996) Visualization of P-selectin glycoprotein ligand-1 as a highly extended molecule and mapping of protein epitopes for monoclonal antibodies. J Biol Chem 271(11):6342-6348.
16. Ellies LG, et al. (1998) Core 2 oligosaccharide biosynthesis distinguishes between selectin ligands essential for leukocyte homing and inflammation. Immunity 9(6):881-890.
17. Ju T, Brewer K, D'Souza A, Cummings RD, CanfieldWM(2002) Cloning and expression of human core 1 β1,3-galactosyltransferase. J Biol Chem 277(1):178-186.
18. Del Conde I, Shrimpton CN, Thiagarajan P, López JA (2005) Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106(5):1604-1611.
19. Miner JJ, et al. (2008) Separable requirements for cytoplasmic domain of PSGL-1 in leukocyte rolling and signaling under flow. Blood 112(5):2035-2045.
20. Neame SJ, Uff CR, Sheikh H, Wheatley SC, Isacke CM (1995) CD44 exhibits a cell type dependent interaction with Triton X-100 insoluble, lipid rich, plasma membrane domains. J Cell Sci 108(Pt 9):3127-3135.
21. Millán J, Montoya MC, Sancho D, Sánchez-Madrid F, Alonso MA (2002) Lipid rafts mediate biosynthetic transport to the T lymphocyte uropod subdomain and are necessary for uropod integrity and function. Blood 99(3):978-984.
22. Thankamony SP, Knudson W (2006) Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J Biol Chem 281(45):34601-34609.
23. Yago T, et al. (2010) E-selectin engages PSGL-1 and CD44 through a common signaling pathway to induce integrin alphaLbeta2-mediated slow leukocyte rolling. Blood 116(3):485-494.
24. 2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 26(6):773-783.
25. Zarbock A, et al. (2008) PSGL-1 engagement by E-selectin signals through Src kinase Fgr and ITAM adapters DAP12 and FcR gamma to induce slow leukocyte rolling. J Exp Med 205(10):2339-2347.
26. Hrachovinová I, et al. (2003) Interaction of P-selectin and PSGL-1 generates microparticles that correct hemostasis in a mouse model of hemophilia A. Nat Med 9(8):1020-1025.
27. Bruehl RE, et al. (1997) Leukocyte activation induces surface redistribution of P-selectin glycoprotein ligand-1. J Leukoc Biol 61(4):489-499.
28. Alonso-Lebrero JL, et al. (2000) Polarization and interaction of adhesion molecules P-selectin glycoprotein ligand 1 and intercellular adhesion molecule 3 with moesin and ezrin in myeloid cells. Blood 95(7):2413-2419.
29. Serrador JM, et al. (1998) CD43 interacts with moesin and ezrin and regulates its redistribution to the uropods of T lymphocytes at the cell-cell contacts. Blood 91(12):4632-4644.
30. Serrador JM, et al. (2002) A juxta-membrane amino acid sequence of P-selectin glycoprotein ligand-1 is involved in moesin binding and ezrin/radixin/moesin-directed targeting at the trailing edge of migrating lymphocytes. Eur J Immunol 32(6):1560-1566.
31. Rossy J, Schlicht D, Engelhardt B, Niggli V (2009) Flotillins interact with PSGL-1 in neutrophils and, upon stimulation, rapidly organize into membrane domains subsequently accumulating in the uropod. PLoS ONE 4(4):e5403.
32. Rodgers W, Rose JK (1996) Exclusion of CD45 inhibits activity of p56lck associated with glycolipid-enriched membrane domains. J Cell Biol 135(6 Pt 1):1515-1523.
33. Lauer S, et al. (2000) Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J 19(14):3556-3564.
34. Ramachandran V, et al. (1999) Tyrosine replacement in P-selectin glycoprotein ligand-1 affects distinct kinetic and mechanical properties of bonds with P- and L-selectin. Proc Natl Acad Sci USA 96(24):13771-13776.
35. Hassall DG, Graham A (1995) Changes in free cholesterol content, measured by filipin fluorescence and flow cytometry, correlate with changes in cholesterol biosynthesis in THP-1 macrophages. Cytometry 21(4):352-362.
36. Varki A, Gagneux P (2012) Multifarious roles of sialic acids in immunity. Ann N Y Acad Sci 1253:16-36.
37. Lefort CT, Ley K (2012) Neutrophil arrest by LFA-1 activation. Front Immunol 3:157.
38. Sánchez-Madrid F, Serrador JM (2009) Bringing up the rear: Defining the roles of the uropod. Nat Rev Mol Cell Biol 10(5):353-359.
39. Cyster JG, Shotton DM, Williams AF (1991) The dimensions of the T lymphocyte glycoprotein leukosialin and identification of linear protein epitopes that can be modified by glycosylation. EMBO J 10(4):893-902.
40. Clark MC, Baum LG (2012) T cells modulate glycans on CD43 and CD45 during development and activation, signal regulation, and survival. Ann N Y Acad Sci 1253:58-67.
41. Pillai S, Netravali IA, Cariappa A, Mattoo H (2012) Siglecs and immune regulation. Annu Rev Immunol 30:357-392.
42. Lu Q, et al. (2014) PILRα and PILRβ have a siglec fold and provide the basis of binding to sialic acid. Proc Natl Acad Sci USA 111(22):8221-8226.
43. McMillan SJ, et al. (2013) Siglec-E is a negative regulator of acute pulmonary neutrophil inflammation and suppresses CD11b β2-integrin-dependent signaling. Blood 121(11):2084-2094.
44. Wang J, Shiratori I, Uehori J, Ikawa M, Arase H (2013) Neutrophil infiltration during inflammation is regulated by PILRα via modulation of integrin activation. Nat Immunol 14(1):34-40.
45. Brinkman-Van der Linden EC, et al. (2003) CD33/Siglec-3 binding specificity, expression pattern, and consequences of gene deletion in mice. Mol Cell Biol 23(12):4199-4206.
46. Kuroki K, et al. (2014) Structural basis for simultaneous recognition of an O-glycan and its attached peptide of mucin family by immune receptor PILRα. Proc Natl Acad Sci USA 111(24):8877-8882.
47. Shogren R, Gerken TA, Jentoft N (1989) Role of glycosylation on the conformation and chain dimensions of O-linked glycoproteins: Light-scattering studies of ovine submaxillary mucin. Biochemistry 28(13):5525-5536.
48. Rose MC, Voter WA, Sage H, Brown CF, Kaufman B (1984) Effects of deglycosylation on the architecture of ovine submaxillary mucin glycoprotein. J Biol Chem 259(5):3167-3172.
49. Alfalah M, et al. (1999) O-linked glycans mediate apical sorting of human intestinal sucrase-isomaltase through association with lipid rafts. Curr Biol 9(11):593-596.
50. Castillon GA, Michon L, Watanabe R (2013) Apical sorting of lysoGPI-anchored proteins occurs independent of association with detergent-resistant membranes but dependent on their N-glycosylation. Mol Biol Cell 24(12):2021-2033.
51. Matsumoto M, et al. (2005) CD43 functions as a ligand for E-Selectin on activated T cells. J Immunol 175(12):8042-8050.
52. Alcaide P, et al. (2007) The 130-kDa glycoform of CD43 functions as an E-selectin ligand for activated Th1 cells in vitro and in delayed-type hypersensitivity reactions in vivo. J Invest Dermatol 127(8):1964-1972.
53. Angelillo-Scherrer A (2012) Leukocyte-derived microparticles in vascular homeostasis. Circ Res 110(2):356-369.
54. Affentranger S, Martinelli S, Hahn J, Rossy J, Niggli V (2011) Dynamic reorganization of flotillins in chemokine-stimulated human T-lymphocytes. BMC Cell Biol 12:28.
55. Ludwig A, et al. (2010) Flotillin microdomains interact with the cortical cytoskeleton to control uropod formation and neutrophil recruitment. J Cell Biol 191(4):771-781.
56. Martinelli S, et al. (2013) Ezrin/Radixin/Moesin proteins and flotillins cooperate to promote uropod formation in T cells. Front Immunol 4:84.
57. Baumann T, Affentranger S, Niggli V (2013) Analysis of close associations of uropodassociated proteins in human T-cells using the proximity ligation assay. PeerJ 1:e186.
58. Zhang JQ, Biedermann B, Nitschke L, Crocker PR (2004) The murine inhibitory receptor mSiglec-E is expressed broadly on cells of the innate immune system whereas mSiglec-F is restricted to eosinophils. Eur J Immunol 34(4):1175-1184.
59. Fu J, et al. (2008) Endothelial cell O-glycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice. J Clin Invest 118(11):3725-3737.
60. Xia L, et al. (2002) P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J Clin Invest 109(7):939-950.
61. Meng F, Lowell CA (1997) Lipopolysaccharide (LPS)-induced macrophage activation and signal transduction in the absence of Src-family kinases Hck, Fgr, and Lyn. J Exp Med 185(9):1661-1670.
62. Shao B, et al. (2012) Signal-dependent slow leukocyte rolling does not require cytoskeletal anchorage of P-selectin glycoprotein ligand-1 (PSGL-1) or integrin αLβ2. J Biol Chem 287(23):19585-19598.
63. SetiadiH. McEverR.P.2008Clustering endothelial E-selectin in clathrin-coated pits and lipid rafts enhances leukocyte adhesion under flowBlood11141989-1998