Annals of Biomedical Engineering

, Volume 40, Issue 4, pp 777–789 | Cite as

The Role of Sugars in Dendritic Cell Trafficking

  • Zélia Silva
  • Konstantinos Konstantopoulos
  • Paula A. Videira


Dendritic cells (DCs) are crucial components of the immune response, strategically positioned as immune sentinels. Complex trafficking and accurate positioning of DCs are indispensable for both immunity and tolerance. This is particularly evident for their therapeutic application where an unmet clinical need exists for DCs with improved migratory capacity upon adoptive transfer into patients. One critical step that directs the trafficking of DCs throughout the body is their egress from the vasculature, starting with their adhesive interactions with vascular endothelium under shear flow. Both tethering and rolling rely on interactions mediated by specific glycans attached to glycoproteins and glycolipids present on the DC surface. In DCs, surface glycosylation, including the expression of selectin ligands, changes significantly depending on the local microenvironment and the functional state of the cells. These changes have been documented and have potential implications in important cell functions such as migration. In this article, we review the glycobiological aspects in the context of DC interaction with endothelium, and offer insights on how it can be applied to modulate DC applicability in therapy.


Dendritic cells Migration Selectin Sialyl Lewisx Adhesion Shear flow 



C–C-chemokine ligand


C–C-chemokine receptor


Dendritic cell


Dendritic cell-specific intracellular adhesion molecule-3 grabbing non-integrin








Lymph nodes


Major histocompatibility complex


Monocyte-derived dendritic cell


Prostaglandin E2


P-Selectin glycoprotein ligand-1


Sialic acid-binding immunoglobulin-like lectin


Sialyl Lewis X antigen



This study was supported in part by the Fundação para a Ciência e Tecnologia, Portugal—PTDC/SAU-MII/67561/2006 and SFRH/BPD/41168/2007 (Z.S.), and the NIH/NCI R01 CA101135 and U54 CA143868 (K.K.). We thank Mariana Silva for the help on text revision of the manuscript.


  1. 1.
    Ali, O. A., and D. J. Mooney. Immunologically active biomaterials for cancer therapy. Curr. Top. Microbiol. Immunol. 344:279–297, 2011.PubMedCrossRefGoogle Scholar
  2. 2.
    Alvarez, D., E. H. Vollmann, and U. H. von Andrian. Mechanisms and consequences of dendritic cell migration. Immunity 29:325–342, 2008.PubMedCrossRefGoogle Scholar
  3. 3.
    Ando, J., and K. Yamamoto. Vascular mechanobiology: endothelial cell responses to fluid shear stress. Circ. J. 73:1983–1992, 2009.PubMedCrossRefGoogle Scholar
  4. 4.
    Bachleitner-Hofmann, T., J. Friedl, M. Hassler, H. Hayden, P. Dubsky, M. Sachet, E. Rieder, R. Pfragner, C. Brostjan, S. Riss, B. Niederle, M. Gnant, and A. Stift. Pilot trial of autologous dendritic cells loaded with tumor lysate(s) from allogeneic tumor cell lines in patients with metastatic medullary thyroid carcinoma. Oncol. Rep. 21:1585–1592, 2009.PubMedCrossRefGoogle Scholar
  5. 5.
    Banchereau, J., and A. K. Palucka. Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 5:296–306, 2005.PubMedCrossRefGoogle Scholar
  6. 6.
    Bao, X., E. A. Moseman, H. Saito, B. Petryniak, A. Thiriot, S. Hatakeyama, Y. Ito, H. Kawashima, Y. Yamaguchi, J. B. Lowe, U. H. von Andrian, and M. Fukuda. Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes. Immunity 33:817–829, 2010.PubMedCrossRefGoogle Scholar
  7. 7.
    Bippes, C. C., A. Feldmann, S. Stamova, M. Cartellieri, A. Schwarzer, R. Wehner, M. Schmitz, E. P. Rieber, S. Zhao, K. Schakel, A. Temme, R. H. Scofield, B. T. Kurien, H. Bartsch, and M. Bachmann. A novel modular antigen delivery system for immuno targeting of human 6-sulfo LacNAc-positive blood dendritic cells (SlanDCs). PLoS One 6:e16315, 2011.PubMedCrossRefGoogle Scholar
  8. 8.
    Bonasio, R., M. L. Scimone, P. Schaerli, N. Grabie, A. H. Lichtman, and U. H. von Andrian. Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat. Immunol. 7:1092–1100, 2006.PubMedCrossRefGoogle Scholar
  9. 9.
    Boog, C. J., J. J. Neefjes, J. Boes, H. L. Ploegh, and C. J. Melief. Specific immune responses restored by alteration in carbohydrate chains of surface molecules on antigen-presenting cells. Eur. J. Immunol. 19:537–542, 1989.PubMedCrossRefGoogle Scholar
  10. 10.
    Burdick, M. M., B. S. Bochner, B. E. Collins, R. L. Schnaar, and K. Konstantopoulos. Glycolipids support E-selectin-specific strong cell tethering under flow. Biochem. Biophys. Res. Commun. 284:42–49, 2001.PubMedCrossRefGoogle Scholar
  11. 11.
    Cabral, M. G., A. R. Piteira, Z. Silva, D. Ligeiro, R. Brossmer, and P. A. Videira. Human dendritic cells contain cell surface sialyltransferase activity. Immunol. Lett. 131:89–96, 2010.PubMedCrossRefGoogle Scholar
  12. 12.
    Carlow, D. A., K. Gossens, S. Naus, K. M. Veerman, W. Seo, and H. J. Ziltener. PSGL-1 function in immunity and steady state homeostasis. Immunol. Rev. 230:75–96, 2009.PubMedCrossRefGoogle Scholar
  13. 13.
    Caux, C., S. Ait-Yahia, K. Chemin, O. de Bouteiller, M. C. Dieu-Nosjean, B. Homey, C. Massacrier, B. Vanbervliet, A. Zlotnik, and A. Vicari. Dendritic cell biology and regulation of dendritic cell trafficking by chemokines. Springer Semin. Immunopathol. 22:345–369, 2000.PubMedCrossRefGoogle Scholar
  14. 14.
    Chapuis, F., M. Rosenzwajg, M. Yagello, M. Ekman, P. Biberfeld, and J. C. Gluckman. Differentiation of human dendritic cells from monocytes in vitro. Eur. J. Immunol. 27:431–441, 1997.PubMedCrossRefGoogle Scholar
  15. 15.
    Cobb, A., L. K. Roberts, A. K. Palucka, H. Mead, M. Montes, R. Ranganathan, S. Burkeholder, J. P. Finholt, D. Blankenship, B. King, L. Sloan, A. C. Harrod, Y. Levy, and J. Banchereau. Development of a HIV-1 lipopeptide antigen pulsed therapeutic dendritic cell vaccine. J. Immunol. Methods 365:27–37, 2011.PubMedCrossRefGoogle Scholar
  16. 16.
    Crespo, H. J., M. G. Cabral, A. V. Teixeira, J. T. Lau, H. Trindade, and P. A. Videira. Effect of sialic acid loss on dendritic cell maturation. Immunology 128:e621–e631, 2009.PubMedCrossRefGoogle Scholar
  17. 17.
    Crocker, P. R., J. C. Paulson, and A. Varki. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7:255–266, 2007.PubMedCrossRefGoogle Scholar
  18. 18.
    Crocker, P. R., and P. Redelinghuys. Siglecs as positive and negative regulators of the immune system. Biochem. Soc. Trans. 36:1467–1471, 2008.PubMedCrossRefGoogle Scholar
  19. 19.
    Curti, A., P. Tosi, P. Comoli, C. Terragna, E. Ferri, C. Cellini, M. Massaia, A. D’Addio, V. Giudice, C. Di Bello, M. Cavo, R. Conte, G. Gugliotta, M. Baccarani, and R. M. Lemoli. Phase I/II clinical trial of sequential subcutaneous and intravenous delivery of dendritic cell vaccination for refractory multiple myeloma using patient-specific tumour idiotype protein or idiotype (VDJ)-derived class I-restricted peptides. Br. J. Haematol. 139:415–424, 2007.PubMedCrossRefGoogle Scholar
  20. 20.
    Dawson, N. Immunotherapeutic approaches in prostate cancer: PROVENGE. Clin. Adv. Hematol. Oncol. 8:419–421, 2010.PubMedGoogle Scholar
  21. 21.
    Dimitroff, C. J., J. Y. Lee, R. C. Fuhlbrigge, and R. Sackstein. A distinct glycoform of CD44 is an l-selectin ligand on human hematopoietic cells. Proc. Natl. Acad. Sci. USA 97:13841–13846, 2000.PubMedCrossRefGoogle Scholar
  22. 22.
    Dorrie, J., N. Schaft, I. Muller, V. Wellner, T. Schunder, J. Hanig, G. J. Oostingh, M. P. Schon, C. Robert, E. Kampgen, and G. Schuler. Introduction of functional chimeric E/L-selectin by RNA electroporation to target dendritic cells from blood to lymph nodes. Cancer Immunol. Immunother. 57:467–477, 2008.PubMedCrossRefGoogle Scholar
  23. 23.
    Eggert, A. A., M. W. Schreurs, O. C. Boerman, W. J. Oyen, A. J. de Boer, C. J. Punt, C. G. Figdor, and G. J. Adema. Biodistribution and vaccine efficiency of murine dendritic cells are dependent on the route of administration. Cancer Res. 59:3340–3345, 1999.PubMedGoogle Scholar
  24. 24.
    Erdmann, I., E. P. Scheidegger, F. K. Koch, L. Heinzerling, B. Odermatt, G. Burg, J. B. Lowe, and T. M. Kundig. Fucosyltransferase VII-deficient mice with defective E-, P-, and L-selectin ligands show impaired CD4+ and CD8+ T cell migration into the skin, but normal extravasation into visceral organs. J. Immunol. 168:2139–2146, 2002.PubMedGoogle Scholar
  25. 25.
    Fadul, C. E., J. L. Fisher, T. H. Hampton, E. C. Lallana, Z. Li, J. Gui, Z. M. Szczepiorkowski, T. D. Tosteson, C. H. Rhodes, H. A. Wishart, L. D. Lewis, and M. S. Ernstoff. Immune response in patients with newly diagnosed glioblastoma multiforme treated with intranodal autologous tumor lysate-dendritic cell vaccination after radiation chemotherapy. J. Immunother. 34:382–389, 2011.PubMedCrossRefGoogle Scholar
  26. 26.
    Fishman, M. A changing world for DCvax: a PSMA loaded autologous dendritic cell vaccine for prostate cancer. Expert Opin. Biol. Ther. 9:1565–1575, 2009.PubMedCrossRefGoogle Scholar
  27. 27.
    Foxall, C., S. R. Watson, D. Dowbenko, C. Fennie, L. A. Lasky, M. Kiso, A. Hasegawa, D. Asa, and B. K. Brandley. The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J. Cell Biol. 117:895–902, 1992.PubMedCrossRefGoogle Scholar
  28. 28.
    Frommhold, D., A. Ludwig, M. G. Bixel, A. Zarbock, I. Babushkina, M. Weissinger, S. Cauwenberghs, L. G. Ellies, J. D. Marth, A. G. Beck-Sickinger, M. Sixt, B. Lange-Sperandio, A. Zernecke, E. Brandt, C. Weber, D. Vestweber, K. Ley, and M. Sperandio. Sialyltransferase ST3Gal-IV controls CXCR2-mediated firm leukocyte arrest during inflammation. J. Exp. Med. 205:1435–1446, 2008.PubMedCrossRefGoogle Scholar
  29. 29.
    Fuhlbrigge, R. C., S. L. King, R. Sackstein, and T. S. Kupper. CD43 is a ligand for E-selectin on CLA+ human T cells. Blood 107:1421–1426, 2006.PubMedCrossRefGoogle Scholar
  30. 30.
    Garcia-Vallejo, J. J., and Y. van Kooyk. Endogenous ligands for C-type lectin receptors: the true regulators of immune homeostasis. Immunol. Rev. 230:22–37, 2009.PubMedCrossRefGoogle Scholar
  31. 31.
    Garcia-Vallejo, J. J., E. van Liempt, P. da Costa Martins, C. Beckers, B. van het Hof, S. I. Gringhuis, J. J. Zwaginga, W. van Dijk, T. B. Geijtenbeek, Y. van Kooyk, and I. van Die. DC-SIGN mediates adhesion and rolling of dendritic cells on primary human umbilical vein endothelial cells through LewisY antigen expressed on ICAM-2. Mol. Immunol. 45:2359–2369, 2008.PubMedCrossRefGoogle Scholar
  32. 32.
    Grassi, F., C. Dezutter-Dambuyant, D. McIlroy, C. Jacquet, K. Yoneda, S. Imamura, L. Boumsell, D. Schmitt, B. Autran, P. Debre, and A. Hosmalin. Monocyte-derived dendritic cells have a phenotype comparable to that of dermal dendritic cells and display ultrastructural granules distinct from Birbeck granules. J. Leukoc. Biol. 64:484–493, 1998.PubMedGoogle Scholar
  33. 33.
    Hartge, M. M., T. Unger, and U. Kintscher. The endothelium and vascular inflammation in diabetes. Diabetes Vasc. Dis. Res. 4:84–88, 2007.CrossRefGoogle Scholar
  34. 34.
    Hsu, D. K., A. I. Chernyavsky, H. Y. Chen, L. Yu, S. A. Grando, and F. T. Liu. Endogenous galectin-3 is localized in membrane lipid rafts and regulates migration of dendritic cells. J. Invest. Dermatol. 129:573–583, 2009.PubMedCrossRefGoogle Scholar
  35. 35.
    Jacobs, P. P., and R. Sackstein. CD44 and HCELL: preventing hematogenous metastasis at step 1. FEBS Lett., 2011 [Epub ahead of print].Google Scholar
  36. 36.
    Jenner, J., G. Kerst, R. Handgretinger, and I. Muller. Increased alpha2,6-sialylation of surface proteins on tolerogenic, immature dendritic cells and regulatory T cells. Exp. Hematol. 34:1212–1218, 2006.PubMedCrossRefGoogle Scholar
  37. 37.
    Johnson, L. A., S. Clasper, A. P. Holt, P. F. Lalor, D. Baban, and D. G. Jackson. An inflammation-induced mechanism for leukocyte transmigration across lymphatic vessel endothelium. J. Exp. Med. 203:2763–2777, 2006.PubMedCrossRefGoogle Scholar
  38. 38.
    Johnson, L. A., and D. G. Jackson. Cell traffic and the lymphatic endothelium. Ann. N. Y. Acad. Sci. 1131:119–133, 2008.PubMedCrossRefGoogle Scholar
  39. 39.
    Johnson, L. A., and D. G. Jackson. Inflammation-induced secretion of CCL21 in lymphatic endothelium is a key regulator of integrin-mediated dendritic cell transmigration. Int. Immunol. 22:839–849, 2010.PubMedCrossRefGoogle Scholar
  40. 40.
    Julien, S., M. J. Grimshaw, M. Sutton-Smith, J. Coleman, H. R. Morris, A. Dell, J. Taylor-Papadimitriou, and J. M. Burchell. Sialyl-Lewis(x) on P-selectin glycoprotein ligand-1 is regulated during differentiation and maturation of dendritic cells: a mechanism involving the glycosyltransferases C2GnT1 and ST3Gal I. J. Immunol. 179:5701–5710, 2007.PubMedGoogle Scholar
  41. 41.
    Kannagi, R. Regulatory roles of carbohydrate ligands for selectins in the homing of lymphocytes. Curr. Opin. Struct. Biol. 12:599–608, 2002.PubMedCrossRefGoogle Scholar
  42. 42.
    Katayama, Y., A. Hidalgo, J. Chang, A. Peired, and P. S. Frenette. CD44 is a physiological E-selectin ligand on neutrophils. J. Exp. Med. 201:1183–1189, 2005.PubMedCrossRefGoogle Scholar
  43. 43.
    Kieffer, J. D., R. C. Fuhlbrigge, D. Armerding, C. Robert, K. Ferenczi, R. T. Camphausen, and T. S. Kupper. 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, 2001.PubMedCrossRefGoogle Scholar
  44. 44.
    Kobzdej, M. M., A. Leppanen, V. Ramachandran, R. D. Cummings, and R. P. McEver. Discordant expression of selectin ligands and sialyl Lewis x-related epitopes on murine myeloid cells. Blood 100:4485–4494, 2002.PubMedCrossRefGoogle Scholar
  45. 45.
    Konstantopoulos, K., and L. V. McIntire. Effects of fluid dynamic forces on vascular cell adhesion. J. Clin. Invest. 100:S19–S23, 1997.PubMedGoogle Scholar
  46. 46.
    Konstantopoulos, K., and S. N. Thomas. Cancer cells in transit: the vascular interactions of tumor cells. Annu. Rev. Biomed. Eng. 11:177–202, 2009.PubMedCrossRefGoogle Scholar
  47. 47.
    Koszik, F., D. Strunk, I. Simonitsch, L. J. Picker, G. Stingl, and E. Payer. Expression of monoclonal antibody HECA-452-defined E-selectin ligands on Langerhans cells in normal and diseased skin. J. Invest. Dermatol. 102:773–780, 1994.PubMedCrossRefGoogle Scholar
  48. 48.
    Lammermann, T., B. L. Bader, S. J. Monkley, T. Worbs, R. Wedlich-Soldner, K. Hirsch, M. Keller, R. Forster, D. R. Critchley, R. Fassler, and M. Sixt. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453:51–55, 2008.PubMedCrossRefGoogle Scholar
  49. 49.
    Lappin, M. B., J. M. Weiss, V. Delattre, B. Mai, H. Dittmar, C. Maier, K. Manke, S. Grabbe, S. Martin, and J. C. Simon. Analysis of mouse dendritic cell migration in vivo upon subcutaneous and intravenous injection. Immunology 98:181–188, 1999.PubMedCrossRefGoogle Scholar
  50. 50.
    Lee, A. W., T. Truong, K. Bickham, J. F. Fonteneau, M. Larsson, I. Da Silva, S. Somersan, E. K. Thomas, and N. Bhardwaj. A clinical grade cocktail of cytokines and PGE2 results in uniform maturation of human monocyte-derived dendritic cells: implications for immunotherapy. Vaccine 20(Suppl 4):A8–A22, 2002.PubMedCrossRefGoogle Scholar
  51. 51.
    Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7:678–689, 2007.PubMedCrossRefGoogle Scholar
  52. 52.
    Ludwig, A., J. E. Ehlert, H. D. Flad, and E. Brandt. Identification of distinct surface-expressed and intracellular CXC-chemokine receptor 2 glycoforms in neutrophils: N-glycosylation is essential for maintenance of receptor surface expression. J. Immunol. 165:1044–1052, 2000.PubMedGoogle Scholar
  53. 53.
    Matsumoto, M., A. Shigeta, M. Miyasaka, and T. Hirata. CD43 plays both antiadhesive and proadhesive roles in neutrophil rolling in a context-dependent manner. J. Immunol. 181:3628–3635, 2008.PubMedGoogle Scholar
  54. 54.
    McEver, R. P. Selectins: lectins that initiate cell adhesion under flow. Curr. Opin. Cell Biol. 14:581–586, 2002.PubMedCrossRefGoogle Scholar
  55. 55.
    Miteva, D. O., J. M. Rutkowski, J. B. Dixon, W. Kilarski, J. D. Shields, and M. A. Swartz. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ. Res. 106:920–931, 2010.PubMedCrossRefGoogle Scholar
  56. 56.
    Moingeon, P., V. Lombardi, N. Saint-Lu, S. Tourdot, V. Bodo, and L. Mascarell. Adjuvants and vector systems for allergy vaccines. Immunol. Allergy Clin. N. Am. 31:407–419, xii, 2011.Google Scholar
  57. 57.
    Napier, S. L., Z. R. Healy, R. L. Schnaar, and K. Konstantopoulos. Selectin ligand expression regulates the initial vascular interactions of colon carcinoma cells: the roles of CD44v and alternative sialofucosylated selectin ligands. J. Biol. Chem. 282:3433–3441, 2007.PubMedCrossRefGoogle Scholar
  58. 58.
    Nimrichter, L., M. M. Burdick, K. Aoki, W. Laroy, M. A. Fierro, S. A. Hudson, C. E. Von Seggern, R. J. Cotter, B. S. Bochner, M. Tiemeyer, K. Konstantopoulos, and R. L. Schnaar. E-selectin receptors on human leukocytes. Blood 112:3744–3752, 2008.PubMedCrossRefGoogle Scholar
  59. 59.
    Oosterhoff, D., B. J. Sluijter, B. N. Hangalapura, and T. D. de Gruijl. The dermis as a portal for dendritic cell-targeted immunotherapy of cutaneous melanoma. Curr. Top. Microbiol. Immunol. 351:181–220, 2012.PubMedCrossRefGoogle Scholar
  60. 60.
    Patel, K. D., K. L. Moore, M. U. Nollert, and R. P. McEver. Neutrophils use both shared and distinct mechanisms to adhere to selectins under static and flow conditions. J. Clin. Invest. 96:1887–1896, 1995.PubMedCrossRefGoogle Scholar
  61. 61.
    Quillien, V., A. Moisan, A. Carsin, T. Lesimple, C. Lefeuvre, H. Adamski, N. Bertho, A. Devillers, C. Leberre, and L. Toujas. Biodistribution of radiolabelled human dendritic cells injected by various routes. Eur. J. Nucl. Med. Mol. Imaging 32:731–741, 2005.PubMedCrossRefGoogle Scholar
  62. 62.
    Randolph, G. J., V. Angeli, and M. A. Swartz. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5:617–628, 2005.PubMedCrossRefGoogle Scholar
  63. 63.
    Rey-Gallardo, A., C. Delgado-Martin, R. Gerardy-Schahn, J. L. Rodriguez-Fernandez, and M. A. Vega. Polysialic acid is required for Neuropilin-2a/b-mediated control of CCL21-driven chemotaxis of mature dendritic cells, and for their migration in vivo. Glycobiology 21:655–662, 2011.PubMedCrossRefGoogle Scholar
  64. 64.
    Ridolfi, R., A. Riccobon, R. Galassi, G. Giorgetti, M. Petrini, L. Fiammenghi, M. Stefanelli, L. Ridolfi, A. Moretti, G. Migliori, and G. Fiorentini. Evaluation of in vivo labelled dendritic cell migration in cancer patients. J. Transl. Med. 2:27, 2004.PubMedCrossRefGoogle Scholar
  65. 65.
    Robert, C., R. C. Fuhlbrigge, J. D. Kieffer, S. Ayehunie, R. O. Hynes, G. Cheng, S. Grabbe, U. H. von Andrian, and T. S. Kupper. Interaction of dendritic cells with skin endothelium: a new perspective on immunosurveillance. J. Exp. Med. 189:627–636, 1999.PubMedCrossRefGoogle Scholar
  66. 66.
    Sackstein, R. The lymphocyte homing receptors: gatekeepers of the multistep paradigm. Curr. Opin. Hematol. 12:444–450, 2005.PubMedCrossRefGoogle Scholar
  67. 67.
    Sackstein, R., and C. J. Dimitroff. A hematopoietic cell L-selectin ligand that is distinct from PSGL-1 and displays N-glycan-dependent binding activity. Blood 96:2765–2774, 2000.PubMedGoogle Scholar
  68. 68.
    Schlickeiser, S., S. Stanojlovic, C. Appelt, K. Vogt, S. Vogel, S. Haase, T. Ritter, H. D. Volk, U. Pleyer, and B. Sawitzki. Control of TNF-induced dendritic cell maturation by hybrid-type N-glycans. J. Immunol. 186:5201–5211, 2011.PubMedCrossRefGoogle Scholar
  69. 69.
    Schon, M. P., and M. Schon. TLR7 and TLR8 as targets in cancer therapy. Oncogene 27:190–199, 2008.PubMedCrossRefGoogle Scholar
  70. 70.
    Silva, Z., Z. Tong, M. Guadalupe Cabral, C. Martins, R. Castro, C. Reis, H. Trindade, K. Konstantopoulos, and P. A. Videira. Sialyl Lewis(x)-dependent binding of human monocyte-derived dendritic cells to selectins. Biochem. Biophys. Res. Commun. 409:459–464, 2011.PubMedCrossRefGoogle Scholar
  71. 71.
    Sperandio, M., C. A. Gleissner, and K. Ley. Glycosylation in immune cell trafficking. Immunol. Rev. 230:97–113, 2009.PubMedCrossRefGoogle Scholar
  72. 72.
    Stamatos, N. M., I. Carubelli, D. van de Vlekkert, E. J. Bonten, N. Papini, C. Feng, B. Venerando, A. d’Azzo, A. S. Cross, L. X. Wang, and P. J. Gomatos. LPS-induced cytokine production in human dendritic cells is regulated by sialidase activity. J. Leukoc. Biol. 88:1227–1239, 2010.PubMedCrossRefGoogle Scholar
  73. 73.
    Steinman, R. M. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271–296, 1991.PubMedCrossRefGoogle Scholar
  74. 74.
    Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685–711, 2003.PubMedCrossRefGoogle Scholar
  75. 75.
    Sundd, P., M. K. Pospieszalska, L. S. Cheung, K. Konstantopoulos, and K. Ley. Biomechanics of leukocyte rolling. Biorheology 48:1–35, 2011.PubMedGoogle Scholar
  76. 76.
    Thomas, S. N., F. Zhu, R. L. Schnaar, C. S. Alves, and K. Konstantopoulos. Carcinoembryonic antigen and CD44 variant isoforms cooperate to mediate colon carcinoma cell adhesion to E- and L-selectin in shear flow. J. Biol. Chem. 283:15647–15655, 2008.PubMedCrossRefGoogle Scholar
  77. 77.
    Triozzi, P. L., W. Aldrich, and S. Ponnazhagan. Inhibition and promotion of tumor growth with adeno-associated virus carcinoembryonic antigen vaccine and Toll-like receptor agonists. Cancer Gene Ther., 2011 [Epub ahead of print].Google Scholar
  78. 78.
    Trottein, F., L. Schaffer, S. Ivanov, C. Paget, C. Vendeville, A. Cazet, S. Groux-Degroote, S. Lee, M. A. Krzewinski-Recchi, C. Faveeuw, S. R. Head, P. Gosset, and P. Delannoy. Glycosyltransferase and sulfotransferase gene expression profiles in human monocytes, dendritic cells and macrophages. Glycoconj. J. 26:1259–1274, 2009.Google Scholar
  79. 79.
    Tuettenberg, A., C. Becker, A. Correll, K. Steinbrink, and H. Jonuleit. Immune regulation by dendritic cells and T cells—basic science, diagnostic, and clinical application. Clin. Lab. 57:1–12, 2011.PubMedGoogle Scholar
  80. 80.
    Ueno, H., N. Schmitt, E. Klechevsky, A. Pedroza-Gonzalez, T. Matsui, G. Zurawski, S. Oh, J. Fay, V. Pascual, J. Banchereau, and K. Palucka. Harnessing human dendritic cell subsets for medicine. Immunol. Rev. 234(1):199–200, 211, 212, 2010.Google Scholar
  81. 81.
    van Kooyk, Y. C-type lectins on dendritic cells: key modulators for the induction of immune responses. Biochem. Soc. Trans. 36:1478–1481, 2008.PubMedCrossRefGoogle Scholar
  82. 82.
    van Kooyk, Y., and G. A. Rabinovich. Protein–glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 9:593–601, 2008.PubMedCrossRefGoogle Scholar
  83. 83.
    Vanbervliet, B., B. Homey, I. Durand, C. Massacrier, S. Ait-Yahia, O. de Bouteiller, A. Vicari, and C. Caux. Sequential involvement of CCR2 and CCR6 ligands for immature dendritic cell recruitment: possible role at inflamed epithelial surfaces. Eur. J. Immunol. 32:231–242, 2002.PubMedCrossRefGoogle Scholar
  84. 84.
    Vara, D. S., G. Punshon, K. M. Sales, G. Hamilton, and A. M. Seifalian. Haemodynamic regulation of gene expression in vascular tissue engineering. Curr. Vasc. Pharmacol. 9:167–187, 2011.PubMedCrossRefGoogle Scholar
  85. 85.
    Varki, A. Selectin ligands: will the real ones please stand up? J. Clin. Invest. 99:158–162, 1997.PubMedCrossRefGoogle Scholar
  86. 86.
    Vassileva, G., H. Soto, A. Zlotnik, H. Nakano, T. Kakiuchi, J. A. Hedrick, and S. A. Lira. The reduced expression of 6Ckine in the plt mouse results from the deletion of one of two 6Ckine genes. J. Exp. Med. 190:1183–1188, 1999.PubMedCrossRefGoogle Scholar
  87. 87.
    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. 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, 2007.PubMedCrossRefGoogle Scholar
  88. 88.
    Vermi, W., R. Bonecchi, F. Facchetti, D. Bianchi, S. Sozzani, S. Festa, A. Berenzi, M. Cella, and M. Colonna. Recruitment of immature plasmacytoid dendritic cells (plasmacytoid monocytes) and myeloid dendritic cells in primary cutaneous melanomas. J. Pathol. 200:255–268, 2003.PubMedCrossRefGoogle Scholar
  89. 89.
    Vestweber, D., and J. E. Blanks. Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev. 79:181–213, 1999.PubMedGoogle Scholar
  90. 90.
    Videira, P. A., I. F. Amado, H. J. Crespo, M. C. Alguero, F. Dall’Olio, M. G. Cabral, and H. Trindade. Surface alpha 2–3- and alpha 2–6-sialylation of human monocytes and derived dendritic cells and its influence on endocytosis. Glycoconj. J. 25:259–268, 2008.PubMedCrossRefGoogle Scholar
  91. 91.
    Weiss, J. M., J. Sleeman, A. C. Renkl, H. Dittmar, C. C. Termeer, S. Taxis, N. Howells, M. Hofmann, G. Kohler, E. Schopf, H. Ponta, P. Herrlich, and J. C. Simon. An essential role for CD44 variant isoforms in epidermal Langerhans cell and blood dendritic cell function. J. Cell Biol. 137:1137–1147, 1997.PubMedCrossRefGoogle Scholar
  92. 92.
    Woodard-Grice, A. V., A. C. McBrayer, J. K. Wakefield, Y. Zhuo, and S. L. Bellis. Proteolytic shedding of ST6Gal-I by BACE1 regulates the glycosylation and function of alpha4beta1 integrins. J. Biol. Chem. 283:26364–26373, 2008.PubMedCrossRefGoogle Scholar
  93. 93.
    Xia, L., M. Sperandio, T. Yago, J. M. McDaniel, R. D. Cummings, S. Pearson-White, K. Ley, and R. P. McEver. P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest. 109:939–950, 2002.PubMedGoogle Scholar
  94. 94.
    Yago, T., J. Fu, J. M. McDaniel, J. J. Miner, R. P. McEver, and L. Xia. Core 1-derived O-glycans are essential E-selectin ligands on neutrophils. Proc. Natl. Acad. Sci. USA 107:9204–9209, 2010.PubMedCrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2011

Authors and Affiliations

  • Zélia Silva
    • 1
  • Konstantinos Konstantopoulos
    • 2
    • 3
  • Paula A. Videira
    • 1
  1. 1.CEDOC, Departamento de Imunologia, Faculdade de Ciências MédicasUniversidade Nova de LisboaLisboaPortugal
  2. 2.Department of Chemical and Biomolecular EngineeringThe Johns Hopkins UniversityBaltimoreUSA
  3. 3.Institute for NanoBioTechnologyThe Johns Hopkins UniversityBaltimoreUSA

Personalised recommendations