Endoglycan, a member of the CD34 family of sialomucins, is a ligand for the vascular selectins

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 1480-1490

  Kerr, Sheena C ^a   Fieger, Claudia B ^a,c   Snapp, Karen R ^b   Rosen, Steven D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c Raven Biotechnologies Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; ENDOGLYCAN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FUCOSE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY HECA 452; P SELECTIN GLYCOPROTEIN LIGAND 1; PADGEM PROTEIN; SIALIC ACID; SIALOMUCIN; SIALYL LEWIS X ANTIGEN; UNCLASSIFIED DRUG; L SELECTIN; LIGAND; MEMBRANE PROTEIN; MUCIN; P SELECTIN LIGAND PROTEIN; P-SELECTIN LIGAND PROTEIN; SELECTIN;

ANTIGEN EXPRESSION; ANTIGEN PURIFICATION; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CELL LINE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKOCYTE; MONOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; SIALYLATION; T LYMPHOCYTE; TONSIL; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM;

ANTIGENS, CD34; B-LYMPHOCYTES; CELL LINE; E-SELECTIN; HUMANS; L-SELECTIN; LIGANDS; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MONOCYTES; MUCINS; P-SELECTIN; SELECTINS; T-LYMPHOCYTES; TONSIL;

EID: 49049119975     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.1480     Document Type: Article

References (74)

1. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689. (Pubitemid 47327397)
2. Marshall, B. T., M. Long, J. W. Piper, T. Yago, R. P. McEver, and C. Zhu. 2003. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423: 190-193.
3. Kansas, G. S. 1996. Selectins and their ligands: current concepts and controversies. Blood 88: 3259-3287. (Pubitemid 26365560)
4. Butcher, E. C., and L. J. Picker. 1996. Lymphocyte homing and homeostasis. Science 272: 60-66.
5. Lowe, J. B. 2002. Glycosylation in the control of selectin counter-receptor structure and function. Immunol. Rev. 186: 19-36.
6. Vestweber, D., and J. E. Blanks. 1999. Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev. 79: 181-213. (Pubitemid 29056952)
7. Dimitroff, C. J., J. Y. Lee, R. C. Fuhlbrigge, and R. Sackstein. 2000. A distinct glycoform of CD44 is an L-selectin ligand on human hematopoietic cells. Proc. Natl. Acad. Sci. USA 97: 13841-13846.
8. Leppanen, A., T. Yago, V. I. Otto, R. P. McEver, and R. D. Cummings. 2003. 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. (Pubitemid 36876778)
9. Mitoma, J., X. Bao, B. Petryanik, P. Schaerli, J. M. Gauguet, S. Y. Yu, H. Kawashima, H. Saito, K. Ohtsubo, J. D. Marth, et al. 2007. Critical functions of N-glycans in L-selectin-mediated lymphocyte homing and recruitment. Nat. Immunol. 8: 409-418. (Pubitemid 46745416)
10. Rosen, S. D. 2004. Ligands for L-selectin: homing, inflammation, and beyond. Annu. Rev. Immunol. 22: 129-156.
11. Kawashima, H., B. Petryniak, N. Hiraoka, J. Mitoma, V. Huckaby, J. Nakayama, K. Uchimura, K. Kadomatsu, T. Muramatsu, J. B. Lowe, and M. Fukuda. 2005. N-acetylglucosamine-6-O-sulfotransferases 1 and 2 cooperatively control lymphocyte homing through L-selectin ligand biosynthesis in high endothelial venules. Nat. Immunol. 6: 1096-1104. (Pubitemid 41541787)
12. Uchimura, K., J. M. Gauguet, M. S. Singer, D. Tsay, R. Kannagi, T. Muramatsu, U. H. von Andrian, and S. D. Rosen. 2005. A major class of L-selectin ligands is eliminated in mice deficient in two sulfotransferases expressed in high endothelial venules. Nat. Immunol. 6: 1105-1113. (Pubitemid 41541788)
13. Lim, Y. C., K. Snapp, G. S. Kansas, R. Camphausen, H. Ding, and F. W. Luscinskas. 1998. Important contributions of P-selectin glycoprotein ligand- 1-mediated secondary capture to human monocyte adhesion to P-selectin, E-selectin, and TNF-α-activated endothelium under flow in vitro. J. Immunol. 161: 2501-2508.
14. McEver, R. P., and R. D. Cummings. 1997. Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest. 100: S97-S103. (Pubitemid 28009555)
15. Laszik, Z., P. J. Jansen, R. D. Cummings, T. F. Tedder, R. P. McEver, and K. L. Moore. 1996. P-selectin glycoprotein ligand-1 is broadly expressed in cells of myeloid, lymphoid, and dendritic lineage and in some nonhematopoietic cells. Blood 88: 3010-3021. (Pubitemid 26357383)
16. + hematopoietic progenitor cells. J. Cell Biol. 135: 523-531.
17. Snapp, K. R., H. Ding, K. Atkins, R. Warnke, F. W. Luscinskas, and G. S. Kansas. 1998. A novel P-selectin glycoprotein ligand-1 monoclonal antibody recognizes an epitope within the tyrosine sulfate motif of human PSGL-1 and blocks recognition of both P- and L-selectin. Blood 91: 154-164.
18. da Costa Martins, P., J. J. Garcia-Vallejo, J. V. van Thienen, M. Fernandez-Borja, J. M. van Gils, C. Beckers, A. J. Horrevoets, P. L. Hordijk, and J. J. Zwaginga. 2007. P-selectin glycoprotein ligand-1 is expressed on endothelial cells and mediates monocyte adhesion to activated endothelium. Arterioscler. Thromb. Vasc. Biol. 27: 1023-1029.
19. Rivera-Nieves, J., T. L. Burcin, T. S. Olson, M. A. Morris, M. McDuffie, F. Cominelli, and K. Ley. 2006. Critical role of endothelial P-selectin glycoprotein ligand 1 in chronic murine ileitis. J. Exp. Med. 203: 907-917.
20. Asa, D., L. Raycroft, L. Ma, P. A. Aeed, P. S. Kaytes, A. P. Elhammer, and J. G. Geng. 1995. The P-selectin glycoprotein ligand functions as a common human leukocyte ligand for P- and E-selectins. J. Biol. Chem. 270: 11662-11670.
21. Borges, E., G. Pendl, R. Eytner, M. Steegmaier, O. Zollner, and D. Vestweber. 1997. The binding of T cell-expressed P-selectin glycoprotein ligand-1 to E- and P-selectin is differentially regulated. J. Biol. Chem. 272: 28786-28792. (Pubitemid 27517838)
22. Hirata, T., G. Merrill-Skoloff, M. Aab, J. Yang, B. C. Furie, and B. Furie. 2000. P-Selectin glycoprotein ligand 1 (PSGL-1) is a physiological ligand for E-selectin in mediating T helper 1 lymphocyte migration. J. Exp. Med. 192: 1669-1676.
23. Moore, K. L., K. D. Patel, R. E. Bruehl, F. Li, D. A. Johnson, H. S. Lichenstein, R. D. Cummings, D. F. Bainton, and R. P. McEver. 1995. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J. Cell Biol. 128: 661-671.
24. Yang, J., T. Hirata, K. Croce, G. Merrill-Skoloff, B. Tchernychev, E. Williams, R. Flaumenhaft, B. C. Furie, and B. Furie. 1999. Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin- mediated but not E-selectin-mediated neutrophil rolling and migration. J. Exp. Med. 190: 1769-1782. (Pubitemid 30013843)
25. Xia, L., M. Sperandio, T. Yago, J. M. McDaniel, R. D. Cummings, S. Pearson-White, K. Ley, and R. P. McEver. 2002. P-selectin glycoprotein ligand- 1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest. 109: 939-950. (Pubitemid 34275115)
26. Alcaide, P., S. L. King, C. J. Dimitroff, Y. C. Lim, R. C. Fuhlbrigge, and F. W. Luscinskas. 2007. The 130-kDa glycoform of CD43 functions as an Eselectin ligand for activated Th1 cells in vitro and in delayed-type hypersensitivity reactions in vivo. J. Invest. Dermatol. 127: 1964-1972. (Pubitemid 47075363)
27. + human T cells. Blood 107: 1421-1426.
28. Matsumoto, M., K. Atarashi, E. Umemoto, Y. Furukawa, A. Shigeta, M. Miyasaka, and T. Hirata. 2005. CD43 functions as a ligand for E-Selectin on activated T cells. J. Immunol. 175: 8042-8050. (Pubitemid 41798366)
29. Matsumoto, M., A. Shigeta, Y. Furukawa, T. Tanaka, M. Miyasaka, and T. Hirata. 2007. CD43 collaborates with P-selectin glycoprotein ligand-1 to mediate E-selectin-dependent T cell migration into inflamed skin. J. Immunol. 178: 2499-2506. (Pubitemid 46233451)
30. Katayama, Y., A. Hidalgo, J. Chang, A. Peired, and P. S. Frenette. 2005. CD44 is a physiological E-selectin ligand on neutrophils. J. Exp. Med. 201: 1183-1189. (Pubitemid 40637228)
31. Hidalgo, A., A. J. Peired, M. K. Wild, D. Vestweber, and P. S. Frenette. 2007. Complete identification of E-selectin ligands on neutrophils reveals distinct functions of PSGL-1, ESL-1, and CD44. Immunity 26: 477-489. (Pubitemid 46603003)
32. Bernimoulin, M. P., X. L. Zeng, C. Abbal, S. Giraud, M. Martinez, O. Michielin, M. Schapira, and O. Spertini. 2003. Molecular basis of leukocyte rolling on PSGL-1. Predominant role of core-2 O-glycans and of tyrosine sulfate residue 51. J. Biol. Chem. 278: 37-47.
33. Rodgers, S. D., R. T. Camphausen, and D. A. Hammer. 2001. Tyrosine sulfation enhances but is not required for PSGL-1 rolling adhesion on P-selectin. Biophys. J. 81: 2001-2009.
34. Wilkins, P. P., K. L. Moore, R. P. McEver, and R. D. Cummings. 1995. Tyrosine sulfation of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-selectin. J. Biol. Chem. 270: 22677-22680.
35. Li, F., P. P. Wilkins, S. Crawley, J. Weinstein, R. D. Cummings, and R. P. McEver. 1996. Post-translational modifications of recombinant P-selectin glycoprotein ligand-1 required for binding to P- and E-selectin. J. Biol. Chem. 271: 3255-3264. (Pubitemid 26055629)
36. Martinez, M., M. Joffraud, S. Giraud, B. Baisse, M. P. Bernimoulin, M. Schapira, and O. Spertini. 2005. Regulation of PSGL-1 interactions with L-selectin, Pselectin, and E-selectin: role of human fucosyltransferase-IV and -VII. J. Biol. Chem. 280: 5378-5390. (Pubitemid 40280012)
37. Fuhlbrigge, R. C., J. D. Kieffer, D. Armerding, and T. S. Kupper. 1997. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skinhoming T cells. Nature 389: 978-981.
38. Picker, L. J., T. K. Kishimoto, C. W. Smith, R. A. Warnock, and E. C. Butcher. 1991. ELAM-1 is an adhesion molecule for skin-homing T cells. Nature 349: 796-799.
39. Postigo, A. A., M. Marazuela, F. Sanchez-Madrid, and M. O. de Landazuri. 1994. B lymphocyte binding to E- and P-selectins is mediated through the de novo expression of carbohydrates on in vitro and in vivo activated human B cells. J. Clin. Invest. 94: 1585-1596.
40. Rott, L. S., M. J. Briskin, and E. C. Butcher. 2000. Expression of α4β7 and E-selectin ligand by circulating memory B cells: implications for targeted traf- ficking to mucosal and systemic sites. J. Leukocyte Biol. 68: 807-814.
41. Wagers, A. J., J. B. Lowe, and G. S. Kansas. 1996. An important role for the α 1,3 fucosyltransferase, FucT-VII, in leukocyte adhesion to E-selectin. Blood 88: 2125-2132.
42. Montoya, M. C., K. Holtmann, K. R. Snapp, E. Borges, F. Sanchez-Madrid, F. W. Luscinskas, G. Kansas, D. Vestweber, and M. O. de Landazuri. 1999. Memory B lymphocytes from secondary lymphoid organs interact with E-selectin through a novel glycoprotein ligand. J. Clin. Invest. 103: 1317-1327.
43. Armerding, D., R. C. Fuhlbrigge, J. D. Kieffer, and T. S. Kupper. 2001. Tonsillar B cells do not express PSGL-1, but a significant fraction displays the cutaneous lymphocyte antigen and exhibits effective E- and P-selectin ligand activity. Int. Arch. Allergy Immunol. 126: 78-90. (Pubitemid 32973975)
44. Sassetti, C., K. Tangemann, M. S. Singer, D. B. Kershaw, and S. D. Rosen. 1998. Identification of podocalyxin-like protein as a high endothelial venule ligand for L-selectin: parallels to CD34. J. Exp. Med. 187: 1965-1975. (Pubitemid 28285566)
45. Doyonnas, R., D. B. Kershaw, C. Duhme, H. Merkens, S. Chelliah, T. Graf, and K. M. McNagny. 2001. Anuria, omphalocele, and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J. Exp. Med. 194: 13-27. (Pubitemid 32660434)
46. Furness, S. G., and K. McNagny. 2006. Beyond mere markers: functions for CD34 family of sialomucins in hematopoiesis. Immunol. Res. 34: 13-32.
47. Sassetti, C., A. Van Zante, and S. D. Rosen 2000. Identification of endoglycan, a member of the CD34/ podocalyxin family of sialomucins. J. Biol. Chem. 275: 9001-9010. (Pubitemid 30180259)
48. Fieger, C. B., C. M. Sassetti, and S. D. Rosen. 2003. Endoglycan, a member of the CD34 family, functions as an L-selectin ligand through modification with tyrosine sulfation and sialyl lewis X. J. Biol. Chem. 278: 27390-27396.
49. Sarangapani, K. K., T. Yago, A. G. Klopocki, M. B. Lawrence, C. B. Fieger, S. D. Rosen, R. P. McEver, and C. Zhu. 2004. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279: 2291-2298.
50. Harlow, E., and D. Lane. 1999. Using Antibodies. Cold Spring Harbor Laboratory Press, NY.
51. Snapp, K. R., C. E. Heitzig, and G. S. Kansas. 2002. Attachment of the PSGL-1 cytoplasmic domain to the actin cytoskeleton is essential for leukocyte rolling on P-selectin. Blood 99: 4494-4502.
52. Ley, K., T. F. Tedder, and G. S. Kansas. 1993. L-selectin can mediate leukocyte rolling in untreated mesenteric venules in vivo independent of E- or P-selectin. Blood 82: 1632-1638. (Pubitemid 23263983)
53. Davenpeck, K. L., M. E. Brummet, S. A. Hudson, R. J. Mayer, and B. S. Bochner. 2000. Activation of human leukocytes reduces surface P-selectin glycoprotein ligand-1 (PSGL-1, CD162) and adhesion to P-selectin in vitro. J. Immunol. 165: 2764-2772.
54. Liu, Y. J., C. Barthelemy, O. de Bouteiller, C. Arpin, I. Durand, and J. Banchereau. 1995. Memory B cells from human tonsils colonize mucosal epithelium and directly present antigen to T cells by rapid up-regulation of B7-1 and B7-2. Immunity 2: 239-248.
55. Mitsuoka, C., N. Kawakami-Kimura, M. Kasugai-Sawada, N. Hiraiwa, K. Toda, H. Ishida, M. Kiso, A. Hasegawa, and R. Kannagi. 1997. Sulfated sialyl Lewis X, the putative L-selectin ligand, detected on endothelial cells of high endothelial venules by a distinct set of anti-sialyl Lewis X antibodies. Biochem. Biophys. Res. Commun. 230: 546-551. (Pubitemid 27225572)
56. Tu, L., P. G. Murphy, X. Li, and T. F. Tedder. 1999. L-selectin ligands expressed by human leukocytes are HECA-452 antibody-defined carbohydrate epitopes 1489 The Journal of Immunology preferentially displayed by P-selectin glycoprotein ligand-1. J. Immunol. 163: 5070-5078. (Pubitemid 29501276)
57. Dimitroff, C. J., R. J. Bernacki, and R. Sackstein. 2003. Glycosylation-dependent inhibition of cutaneous lymphocyte-associated antigen expression: implications in modulating lymphocyte migration to skin. Blood 101: 602-610.
58. Ohmori, K., F. Fukui, M. Kiso, T. Imai, O. Yoshie, H. Hasegawa, K. Matsushima, and R. Kannagi. 2006. Identification of cutaneous lymphocyteassociated antigen as sialyl 6-sulfo Lewis X, a selectin ligand expressed on a subset of skin-homing helper memory T cells. Blood 107: 3197-3204.
59. Renkonen, J., O. Tynninen, P. Hayry, T. Paavonen, and R. Renkonen. 2002. Glycosylation might provide endothelial zip codes for organ-specific leukocyte traffic into inflammatory sites. Am. J. Pathol. 161: 543-550. (Pubitemid 36142163)
60. Blanchet, M. R., S. Maltby, D. J. Haddon, H. Merkens, L. Zbytnuik, and K. M. McNagny. 2007. CD34 facilitates the development of allergic asthma. Blood 110: 2005-2012.
61. Drew, E., H. Merkens, S. Chelliah, R. Doyonnas, and K. M. McNagny. 2002. CD34 is a specific marker of mature murine mast cells. Exp. Hematol. 30: 1211.
62. Drew, E., J. S. Merzaban, W. Seo, H. J. Ziltener, and K. M. McNagny. 2005. CD34 and CD43 inhibit mast cell adhesion and are required for optimal mast cell reconstitution. Immunity 22: 43-57. (Pubitemid 40143450)
63. Somasiri, A., J. S. Nielsen, N. Makretsov, M. L. McCoy, L. Prentice, C. B. Gilks, S. K. Chia, K. A. Gelmon, D. B. Kershaw, D. G. Huntsman, et al. 2004. Overexpression of the anti-adhesin podocalyxin is an independent predictor of breast cancer progression. Cancer Res. 64: 5068-5073. (Pubitemid 39006520)
64. Baumheter, S., M. S. Singer, W. Henzel, S. Hemmerich, M. Renz, S. D. Rosen, and L. A. Lasky. 1993. Binding of L-selectin to the vascular sialomucin CD34. Science 262: 436-438. (Pubitemid 23353389)
65. Puri, K. D., E. B. Finger, G. Gaudernack, and T. A. Springer. 1995. Sialomucin CD34 is the major L-selectin ligand in human tonsil high endothelial venules. J. Cell Biol. 131: 261-270.
66. Picker, L. J., L. W. Terstappen, L. S. Rott, P. R. Streeter, H. Stein, and E. C. Butcher. 1990. Differential expression of homing-associated adhesion molecules by T cell subsets in man. J. Immunol. 145: 3247-3255.
67. Kieffer, J. D., R. C. Fuhlbrigge, D. Armerding, C. Robert, K. Ferenczi, R. T. Camphausen, and T. S. Kupper. 2001. Neutrophils, monocytes, and dendritic cells express the same specialized form of PSGL-1 as do skin-homing memory T cells: cutaneous lymphocyte antigen. Biochem. Biophys. Res. Commun. 285: 577-587.
68. Cyster, J. G. 2005. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu. Rev. Immunol. 23: 127-159.
69. Underhill, G. H., H. A. Minges Wols, J. L. Fornek, P. L. Witte, and G. S. Kansas. 2002. IgG plasma cells display a unique spectrum of leukocyte adhesion and homing molecules. Blood 99: 2905-2912.
70. Sperandio, M., M. L. Smith, S. B. Forlow, T. S. Olson, L. Xia, R. P. McEver, and K. Ley. 2003. P-selectin glycoprotein ligand-1 mediates L-selectin-dependent leukocyte rolling in venules. J. Exp. Med. 197: 1355-1363. (Pubitemid 36617782)
71. Veerman, K. M., M. J. Williams, K. Uchimura, M. S. Singer, J. S. Merzaban, S. Naus, D. A. Carlow, P. Owen, J. Rivera-Nieves, S. D. Rosen, and H. J. Ziltener. 2007. Interaction of the selectin ligand PSGL-1 with chemokines CCL21 and CCL19 facilitates efficient homing of T cells to secondary lymphoid organs. Nat. Immunol. 8: 532-539.
72. Hirata, T., Y. Furukawa, B. G. Yang, K. Hieshima, M. Fukuda, R. Kannagi, O. Yoshie, and M. Miyasaka. 2004. Human P-selectin glycoprotein ligand-1 (PSGL-1) interacts with the skin-associated chemokine CCL27 via sulfated tyrosines at the PSGL-1 amino terminus. J. Biol. Chem. 279: 51775-51782. (Pubitemid 39656544)
73. Hirose, J., H. Kawashima, O. Yoshie, K. Tashiro, and M. Miyasaka. 2001. Versican interacts with chemokines and modulates cellular responses. J. Biol. Chem. 276: 5228-5234. (Pubitemid 37371420)
74. Kawashima, H., K. Atarashi, M. Hirose, J. Hirose, S. Yamada, K. Sugahara, and M. Miyasaka. 2002. Oversulfated chondriotin/ dermatin sulfates containing GlcAβ1/Ido 1-3αGalNAc (4-6-O-disulfate) interact with L- and P-Selectin and chemokines. J. Biol. Chem. 277: 12921-12930. (Pubitemid 34952659)