Interaction of platelet endothelial cell adhesion molecule (PECAM) with α2,6-sialylated glycan regulates its cell surface residency and anti-apoptotic role

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27604-27613

  Kitazume, Shinobu ^a   Imamaki, Rie ^a   Kurimoto, Ayako ^a   Ogawa, Kazuko ^a   Kato, Masaki ^a   Yamaguchi, Yoshiki ^a   Tanaka, Katsunori ^a   Ishida, Hideharu ^b   Ando, Hiromune ^b,c   Kiso, Makoto ^b,c   Hashii, Noritaka ^d   Kawasaki, Nana ^d   Taniguchi, Naoyuki ^a  

^a RIKEN   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOMOLECULES; CELL ADHESION; CELL DEATH; CELL MEMBRANES; MOLECULES; OLIGOSACCHARIDES; PLATELETS; POLYSACCHARIDES; PROTEINS;

APOPTOTIC STIMULI; BINDING LECTIN; BINDING PROPERTIES; CELL SURFACES; INHIBITORY ACTIVITY; INHIBITORY EFFECT; PLATELET ENDOTHELIAL CELL ADHESION MOLECULES; VASCULAR ENDOTHELIAL CELLS;

ENDOTHELIAL CELLS;

ALPHA2,6 SIALYLATED GLYCAN; CELL ADHESION MOLECULE; GLYCAN; PENTASACCHARIDE; PLATELET ENDOTHELIAL CELL ADHESION MOLECULE; UNCLASSIFIED DRUG; CD31 ANTIGEN; LECTIN; N ACETYLNEURAMINIC ACID; OLIGOSACCHARIDE; POLYSACCHARIDE; PROTEIN BINDING;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; PROTEIN INTERACTION; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; CHEMISTRY; CYTOLOGY; GENETICS; GLYCOCALYX; METABOLISM; MOUSE;

ANIMALS; ANTIGENS, CD31; APOPTOSIS; CELL SURVIVAL; GLYCOCALYX; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LECTINS; MICE; N-ACETYLNEURAMINIC ACID; OLIGOSACCHARIDES; POLYSACCHARIDES; PROTEIN BINDING;

EID: 84907525094     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.563585     Document Type: Article

References (48)

1. Gitay-Goren, H., Soker, S., Vlodavsky, I, and Neufeld, G. (1992) The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. J. Biol. Chem. 267, 6093-6098
2. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M. (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848
3. Rolny, C., Spillmann, D., Lindahl, U., and Claesson-Welsh, L. (2002) Heparin amplifies platelet-derived growth factor (PDGF)- BB-induced PDGFα receptor but not PDGFβ receptor tyrosine phosphorylation in heparan sulfate-deficient cells. Effects on signal transduction and biological responses.J. Biol. Chem. 277,19315-19321
4. Fuster, M. M., and Esko, J. D. (2005) The sweet and sour of cancer: glycans as novel therapeutic targets. Nat. Rev. Cancer 5, 526 -542
5. Presta, M., Leali, D., Stabile, H., Ronca, R., Camozzi, M., Coco, L., Moroni, E., Lielcens, S., and Rusnati, M. (2003) Heparin derivatives as angiogenesis inhibitors. Curr. Pharm. Des. 9, 553-566
6. Lapierre, F., Holme, K., Lam, L., Tressler, R. J., Storm, N., Wee, J., Stack, R. J., Castellot, J., and Tyrrell, D. J. (1996) Chemical modifications of heparin that diminish its anticoagulant but preserve its heparanase-inhibitory, angiostatic, anti-tumor and anti-metastatic properties. Glycobiology 6, 355 -366
7. Iozzo, R. V., and San Antonio, J. D. (2001) Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena.J. Clin. Invest. 108, 349-355
8. Fu, J., Gerhardt, H., McDaniel, J. M., Xia, B., Liu, X., Ivanciu, L., Ny, A.,Hermans, K., Silasi-Mansat, R., McGee, S., Nye, E., Ju, T., Ramirez, M. I, Carmeliet, P., Cummings, R. D., Lupu, F., and Xia, L. (2008) Endothelial cell O-glycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice.J. Clin. Invest. 118, 3725-3737
9. Wang, Y., Ju, T., Ding, X., Xia, B., Wang, W., Xia, L, He, M., and Cummings, R. D. (2010) Cosme is an essential chaperone for correct protein O-glycosylation. Proc. Natl. Acad. Sci. U.S.A. 107, 9228 -9233
10. Croci, D. O., Cerliani, J. P., Dalotto-Moreno, T., Méndez-Huergo, S. P., Mascanfroni, I. D., Dergan-Dylon, S., Toscano, M. A., Caramelo, J. J., García-Vallejo, J. J., Ouyang, J., Mesri, E. A., Junttila, M. R., Bais, C., Shipp, M. A., Salatino, M., and Rabinovich, G. A. (2014) Glycosylati on-dependent lectin-receptor interactions preserve angiogenesis in anti-VEGF refractory tumors. Cell 156, 744-758
11. Grewal, P. K., Uchiyama, S., Ditto, D., Varki, N., Le, D. T., Nizet, V., and Marth, J. D. (2008) The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat. Med. 14, 648-655
12. SØrensen, A. L., Rumjantseva, V., Nayeb-Hashemi, S., Clausen, H., Hartwig, J. H., Wandall, H. H., and Hoffmeister, K. M. (2009) Role of sialic acid for platelet life span: exposure of β-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptorexpressing liver macrophages and hepatocytes. Blood 114, 1645-1654
13. Hanasaki, K., Varki, A., and Powell, L. D. (1995) CD22-mediated cell adhesion to cytokine-activated human endothelial cells. Positive and negative regulation by α2- 6-sialylation of cellular glycoproteins.J. Biol. Chem. 270, 7533-7542
14. Hanasaki, K., Varki, A., Stamenkovic, I, and Bevilacqua, M. P. (1994) Cytokine-induced β-galactoside α-2,6-sialyltransferase in human endothelial cells mediates α2,6-sialylation of adhesion molecules and CD22 ligands.J. Biol. Chem. 269,10637-10643
15. Nitschke, L., Floyd, H., Ferguson, D. J., and Crocker, P. R. (1999) Identification of CD22 ligands on bone marrow sinusoidal endothelium implicated in CD22-dependent homing of recirculating B cells. J. Exp. Med. 189,1513-1518
16. Kitazume, S., Imamaid, R., Ogawa, K., Komi, Y., Futakawa, S., Kojima, S., Hashimoto, Y., Marth, J. D., Paulson, J. C., and Taniguchi, N. (2010) α2,6-Sialic acid on platelet endothelial cell adhesion molecule (PECAM) regulates its homophilic interactions and downstream antiapoptotic signaling. J. Biol. Chem. 285, 6515-6521
17. Woodfin, A., Voisin, M. B., and Nourshargh, S. (2007) PECAM-1: a multi-functional molecule in inflammation and vascular biology. Arterioscler. Thromb. Vase. Biol. 27, 2514-2523
18. Newman, P. J., and Newman, D. K. (2003) Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler. Thromb. Vase. Biol. 23, 953-964
19. Cao, G., Fehrenbach, M.L., Williams, J. T., Finklestein, J. M., Zhu, J. X., and Delisser, H. M. (2009) Angiogenesis in platelet endothelial cell adhesion molecule-1-null mice. Am. J. Pathol. 175, 903-915
20. Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., Cao, G., DeLisser, H., and Schwartz, M. A. (2005) Amechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426 - 431
21. Gao, C., Sun, W., Christofidou-Solomidou, M., Sawada, M., Newman, D. K., Bergom, C., Albelda, S. M., Matsuyama, S., and Newman, P. J. (2003) PECAM-1 functions as a specific and potent inhibitor of mitochondrial-dependent apoptosis. Blood 102, 169-179
22. Osawa, M., Masuda, M., Kusano, K., and Fujiwara, K. (2002) Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J. Cell Biol. 158, 773-785
23. Park, S., DiMaio, T. A., Scheef, E. A., Sorenson, C. M., and Sheibani, N. (2010) PECAM-1 regulates proangiogenic properties of endothelial cells through modulation of cell-cell and cell-matrix interactions. Am. J. Physiol. Cell Physiol. 299, C1468-C1484
24. Mamdouh, Z., Chen, X., Pierini, L. M., Maxfleld, F. R., and Muller, W. A. (2003) Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature 421, 748-753
25. Chen, Z., and Tzima, E. (2009) PECAM-1 is necessary for flow-induced vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 29,1067-1073
26. Crocker, P. R., Paulson, J. C., and Varki, A. (2007) Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7, 255-266
27. Walker, J. A., and Smith, K. G. (2008) CD22: an inhibitory enigma. Immunology 123, 314-325
28. Collins, B. E., Blixt, O., DeSieno, A. R., Bovin, N., Marth, J. D., and Paulson, J. C. (2004) Masking of CD22 by cis ligands does not prevent redistribution of CD22 to sites of cell contact. Proc. Natl. Acad. Sci. U.S.A. 101, 6104-6109
29. Fukunaga, K., Toyoda, T., Ishida, H., and Kiso, M. (2003) Synthesis of lacto- and neolacto-series ganglioside analogs containing N-glycolylneuraminic acid: probes for investigation of specific receptor structures recognized by influenza A viruses. J. Carbohydr. Chem. 22, 919-937
30. Tanaka, K., Siwu, E. R., Minami, K., Hasegawa, K., Nozaki, S., Kanayama, Y., Koyama, K., Chen, W. C., Paulson, J. C., Watanabe, Y., and Fukase, K. (2010) Noninvasive imaging of dendrimer-type IV-glycan clusters: in vivo dynamics dependence on oligosaccharide structure.Angew. Chem. Int. Ed. Engl. 49, 8195-8200
31. Takahashi, N., Nakagawa, H., Fujikawa, K., Kawamura, Y., and Tomiya, N. (1995) Three-dimensional elution mapping of pyridylaminated N-linked neutral and sialyl oligosaccharides. Anal. Biochem. 226,139-146
32. Nakagawa, H., Kawamura, Y., Kato, K., Shimada, I., Arata, Y., and Takahashi, N. (1995) Identification of neutral and sialyl IV-linked oligosaccharide structures from human serum glycoproteins using three kinds of high-performance liquid chromatography. Anal. Biochem. 226,130-138
33. Suzuki, T., Hara, I., Nakano, M., Shigeta, M., Nakagawa, T., Kondo, A., Funakoshi, Y., and Taniguchi, N. (2006) Man2Cl, an α-mannosidase, is involved in the trimming of free oligosaccharides in the cytosol. Biochem. J. 400, 33-41
34. Ceroni, A., Maass, K., Geyer, H., Geyer, R., Dell, A., and Haslam, S. M. (2008) GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans.J. Proteome Res. 7, 1650-1659
35. Lee, R. T., and Lee, Y. C. (2000) Affinity enhancement by multivalent lectin-carbohydrate interaction. Glycoconj. J. 17, 543-551
36. Lundquist, J. J., and Toone, E. J. (2002) The cluster glycoside effect. Chem. Rev. 102,555-578
37. Wuhrer, M., Koeleman, C. A., Hokke, C. H., and Deelder, A. M. (2006) Mass spectrometry of proton adducts of fucosylated N-glycans: fucose transfer between antennae gives rise to misleading fragments. Rapid Commun. Mass Spectrom. 20,1747-1754
38. Nakamura, K., Yamaji, T., Crocker, P. R., Suzuki, A., and Hashimoto, Y. (2002) Lymph node macrophages, but not spleen macrophages, express high levels of unmasked sialoadhesin: implication for the adhesive properties of macrophages in vivo. Glycobiology 12, 209-216
39. Stupack, D. G., Puente, X. S., Boutsaboualoy, S., Storgard, C. M., and Cheresh, D. A. (2001) Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins.J. Cell Biol. 155, 459-470
40. Geyer, H., Geyer, R., Odenthal-Schnittler, M., and Schnittler, H. J. (1999) Characterization of human vascular endothelial cadherin glycans. Glycobiology 9, 915-925
41. DeLisser, H., Liu, Y., Desprez, P. Y., Thor, A., Briasouli, P., Handumrongkul, C., Wilfong, J., Yount, G., Nosrati, M., Fong, S., Shtivelman, E., Fehrenbach, M., Cao, G., Moore, D. H., Nayak, S., Nyack, S., Liggitt, D., Kashani-Sabet, M., and Debs, R. (2010) Vascular endothelial platelet endothelial cell adhesion molecule 1 (PECAM-1) regulates advanced metastatic progression. Proc. Natl. Acad. Sci. U.S.A. 107,18616 -18621
42. Rosen, S.D., Chi, S.I., True, D. D., Singer, M. S., and Yednock, T. A. (1989) Intravenously injected sialidase inactivates attachment sites for lymphocytes on high endothelial venules. J. Immunol. 142,1895-1902
43. Kawano, T., Koyama, S., Takematsu, H., Kozutsumi, Y., Kawasaki, H., Kawashima, S., Kawasaki, T., and Suzuki, A. (1995) Molecular cloning of cytidine monophospho-N-acetylneuraminic acid hydroxylase. Regulation of species- and tissue-specific expression of N-glycolylneuraminic acid. J Biol. Chem. 270,16458-16463
44. Hayakawa, T., Satta, Y., Gagneux, P., Varki, A., and Takahata, N. (2001) Alu-mediated inactivation of the human CMP- N-acetylneuraminic acid hydroxylase gene. Proc. Natl. Acad. Sci. U.S.A. 98, 11399 -11404
45. Pham, T., Gregg, C. J., Karp, F., Chow, R., Padler-Karavani, V., Cao, H., Chen, X., Witztum, J. L., Varki, N. M., and Varki, A. (2009) Evidence for a novel human-specific xeno-auto-antibody response against vascular endothelium. Blood 114, 5225-5235
46. Yasukawa, Z., Sato, C., Sano, K., Ogawa, H., and Kitajima, K. (2006) Identification of disialie acid-containing glycoproteins in mouse serum: a novel modification of immunoglobulin light chains, vitronectin, and plasminogen. Glycobiology 16, 651-665
47. Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M. E., Alvarez, R., Bryan, M. C., Fazio, F., Calarese, D., Stevens, J., Razi, N., Stevens, D. J., Skehel, J. J., van Die, I, Burton, D. R., Wilson, I. A., Cummings, R., Bovin, N., Wong, C. H., and Paulson, J. C. (2004) Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. U.S.A. 101,17033-17038
48. Halaby, D. M., Poupon, A., and Mornon, J. (1999) The immunoglobulin fold family: sequence analysis and 3D structure comparisons. Protein Eng. 12, 563-571