Molecular and Cellular Mechanisms of Syndecans in Tissue Injury and Inflammation

  • Bartlett, Allison H. ;
  • Hayashida, Kazutaka ;
  • Park, Pyong Woo
  • Received : 2007.09.22
  • Accepted : 2007.09.24
  • Published : 2007.10.31

Abstract

The syndecan family of heparan sulfate proteoglycans is expressed on the surface of all adherent cells. Syndecans interact with a wide variety of molecules, including growth factors, cytokines, proteinases, adhesion receptors and extracellular matrix components, through their heparan sulfate chains. Recent studies indicate that these interactions not only regulate key events in development and homeostasis, but also key mechanisms of the host inflammatory response. This review will focus on the molecular and cellular aspects of how syndecans modulate tissue injury and inflammation, and how syndecans affect the outcome of inflammatory diseases in vivo.

Keywords

Chemokine;Heparan Sulfate;Host Defense;Infection;Microbial Pathogenesis;Pneumonia;Proteoglycan;Tissue Repair

References

  1. Alexander, C. M., Reichsman, F., Hinkes, M. T., Lincecum, J., Becker, K. A., et al. (2000) Syndecan-1 is required for Wnt- 1-induced mammary tumorigenesis in mice. Nat. Genet. 25, 329−332
  2. Arribas, J. and Borroto, A. (2002) Protein ectodomain shedding. Chem. Rev. 102, 4627−4638
  3. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., et al. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729−777
  4. Bobardt, M. D., Chatterji, U., Selvarajah, S., Van der Schueren, B., David, G., et al. (2007) Cell-free human immunodeficiency virus type 1 transcytosis though primary genital epithelial cells. J. Virol. 81, 395−405
  5. Bode, L., Eklund, E. A., Murch, S., and Freeze, H. H. (2005) Heparan sulfate depletion amplifies TNF-alpha-induced protein leakage in an in vitro model of protein-losing enteropathy. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G1015− 1023
  6. Bode, L., Murch, S., and Freeze, H. H. (2006) Heparan sulfate plays a central role in a dynamic in vitro model of proteinlosing enteropathy. J. Biol. Chem. 281, 7809−7815
  7. Chen, L., Klass, C., and Woods, A. (2004b) Syndecan-2 regulates transforming growth factor-beta signaling. J. Biol. Chem. 279, 15715−15718
  8. Colgan, S. P., Parkos, C. A., McGuirk, D., Brady, H. R., Papayianni, A. A., et al. (1995) Receptors involved in carbohydrate binding modulate intestinal epithelial-neutrophil interactions. J. Biol. Chem. 270, 10531−10539
  9. Davidson, B. L., Geerts, W. H., and Lensing, A. W. (2002) Lowdose heparin for severe sepsis. N. Engl. J. Med. 347, 1036− 1037 https://doi.org/10.1056/NEJM200209263471317
  10. Day, R. M., Mitchell, T. J., Knight, S. C., and Forbes, A. (2003) Regulation of epithelial syndecan-1 expression by inflammatory cytokines. Cytokine 21, 224−233
  11. Ding, K., Lopez-Burks, M., Sánchez-Duran, J. A., Korc, M., and Lander, M. D. (2005) Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells. J. Cell Biol. 171, 729−738
  12. Finsen, A. V., Woldbaek, P. R., Li, J., Wu, J., Lyberg, T., et al. (2004) Increased syndecan expression following myocardial infarction indicates a role in cardiac remodeling. Physiol. Genomics 16, 301−308
  13. Freissler, E., Meyer auf der Heyde, A., David, G., Meyer, T. F., and Dehio, C. (2000) Syndecan-1 and syndecan-4 can mediate the invasion of $Opa_{HSPG}$-expressing Neisseria gonorrhoeae into epithelial cells. Cell. Microbiol. 2, 69−82
  14. Gaffney, P. R., Doyle, C. T., Gaffney, A., Hogan, J., Hayes, D. P., et al. (1995) Paradoxical response to heparin in 10 patients with ulcerative colitis. Am. J. Gastroenterol. 90, 220−223
  15. Gallay, P. (2004) Syndecans and HIV-1 pathogenesis. Microbes. Infect. 6, 617−622
  16. Garton, K. J., Gough, P. J., and Raines, E. W. (2006) Emerging roles for ectodomain shedding in the regulation of inflammatory responses. J. Leukoc. Biol. 79, 1105−1116
  17. Giuffre, L., Cordey, A. S., Monai, N., Tardy, Y., Schapira, M., et al. (1997) Monocyte adhesion to activated aortic endothelium: role of L-selectin and heparan sulfate proteoglycans. J. Cell Biol. 136, 945−956
  18. Gotte, M. (2003) Syndecans in inflammation. Faseb J. 17, 575− 591
  19. Grassme, H., Gulbins, E., Brenner, B., Ferlinz, K., Sandhoff, K., et al. (1997) Acidic sphingomyelinase mediates entry of N. gonorrhoeae into nonphagocytic cells. Cell 91, 605−615
  20. Halden, Y., Rek, A., Atzenhofer, W., Szilak, L., Wabnig, A., et al. (2004) Interleukin-8 binds to syndecan-2 on human endothelial cells. Biochem. J. 377, 533−538
  21. Ishiguro, K., Kadomatsu, K., Kojima, T., Muramatsu, H., Iwase, M., et al. (2001a) Syndecan-4 deficiency leads to high mortality of lipopolysaccharide-injected mice. J. Biol. Chem. 276, 47483−47488
  22. Ishiguro, K., Kadomatsu, K., Kojima, T., Muramatsu, H., Matsuo, S., et al. (2001b) Syndecan-4 deficiency increases susceptibility to kappa-carrageenan-induced renal damage. Lab. Invest. 81, 509−516
  23. Ishiguro, K., Kadomatsu, K., Kojima, T., Muramatsu, H., Nakamura, E., et al. (2000a) Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth. Dev. Dyn. 219, 539−544
  24. Kuschert, G. S. V., Coulin, F., Power, C. A., Proudfoot, A. E. I., Hubbard, R. E., et al. (1999) Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry 38, 12959−12968
  25. Langford, J. K., Yang, Y., Kieber-Emmons, T., and Sanderson, R. D. (2005) Identification of an invasion regulatory domain within the core protein of syndecan-1. J. Biol. Chem. 280, 3467−3473
  26. Lindahl, U., Kusche-Gullberg, M., and Kjellén, L. (1998) Regulated diversity of heparan sulfate. J. Biol. Chem. 273, 24979− 24982
  27. Middleton, J., Patterson, A. M., Gardner, L., Schmutz, C., and Ashton, B. A. (2002) Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 100, 3853−3860
  28. Midwood, K. S., Valenick, L. V., Hsia, H. C., and Schwarzbauer, J. E. (2004) Coregulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol. Biol. Cell. 15, 5670−5677
  29. Munesue, S., Yoshitomi, Y., Kusano, Y., Koyama, Y., Nishiyama, A., et al. (2007) A novel function of syndecan-2, suppression of MMP-2 activation, which causes suppression of metastasis. J. Biol. Chem. 282, 28167−28174
  30. Pancake, S. J., Holt, G. D., Mellouk, S., and Hoffman, S. L. (1992) Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J. Cell Biol. 117, 1351−1357
  31. Parish, C. R. (2006) The role of heparan sulphate in inflammation. Nat. Rev. Immunol. 6, 633−643
  32. Park, P. W., Pier, G. B., Hinkes, M. T., and Bernfield, M. (2001) Exploitation of syndecan-1 shedding by Pseudomonas aeruginosa enhances virulence. Nature 411, 98−102
  33. Peiris, M. (2006) Pathogenesis of avian flu H5N1 and SARS. Novartis Found .Symp. 279, 56−60
  34. Rapraeger, A. and Ott, V. L. (1998) Molecular interactions of the syndecan core proteins. Curr. Opin. Cell Biol. 10, 620−628
  35. Shukla, D., Liu, J., Blaiklock, P., Shworak, N. W., Bai, Z., et al. (1999) A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99, 13−22
  36. Slimani, H., Charnaux, N., Mbemba, E., Saffar, L., Vassy, R., et al. (2003) Binding of the CC-chemokine RANTES to syndecan- 1 and syndecan-4 expressed on HeLa cells. Glycobiology 13, 623−634
  37. Stepp, M. A., Gibson, H. E., Gala, P. H., Iglesia, D. D., Pajoohesh- Ganji, A., et al. (2002) Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci. 115, 4517−4531
  38. Sutton, A., Friand, V., Brule-Donneger, S., Chaigneau, T., Ziol, M., et al. (2007) Stromal cell-derived factor-1/chemokine (CX- C motif) ligand 12 stimulates human hepatoma cell growth, migration, and invasion. Mol. Cancer Res. 5, 21−33
  39. Tyrrell, D. J., Horne, A. P., Holme, K. R., Preuss, J. M., and Page, C. P. (1999) Heparin in inflammation: potential therapeutic applications beyond anticoagulation. Adv. Pharmacol. 46, 151−208
  40. Utt, M. and Wadstrom. T. (1997) Identification of heparan sulphate binding surface proteins of Helicobacter pylori: inhibition of heparan sulphate binding with sulphated carbohydrate polymers. J. Med. Microbiol. 46, 541−546
  41. van Putten, J. P. and Paul, S. M. (1995) Binding of syndecanlike cell surface proteoglycan receptors is required for Neisseria gonorrheae entry into human mucosal cells. EMBO J. 14, 2144−2154
  42. Watt, S. M., Williamson, J., Genevier, H., Fawcett, J., Simmons, D. L., et al. (1993) The heparin binding PECAM-1 adhesion molecule is expressed by CD34+ hematopoietic precursor cells with early myeloid and B-lymphoid cell phenotypes. Blood 82, 2649−2663
  43. Wells, T. N. and Proudfoot, A. E. (1999) Chemokine receptors and their antagonists in allergic lung disease. Inflamm. Res. 48, 353−362
  44. Xu, J., Park, P. W., Kheradmand, F., and Corry, D. B. (2005) Endogenous attenuation of allergic lung inflammation by syndecan-1. J. Immunol. 174, 5758−5765
  45. Yu, W. H. and Woessner, J. F. Jr. (2001) Heparin-enhanced zymographic detection of matrilysin and collagenases. Anal. Biochem. 293, 38−42
  46. de Parseval, A., Bobardt, M. D., Chatterji, A., Chatterji, U., Elder, J. H., et al. (2005) A highly conserved arginine in gp120 governs HIV-1 binding to both syndecans and CCR5 via sulfated motifs. J. Biol. Chem. 280, 39493−39504
  47. Evans, R. C., Wong, V. S, Morris, A. I., and Rhodes, J. M. (1997) Treatment of corticosteroid-resistant ulcerative colitis with heparin-a report of 16 cases. Aliment. Pharmacol. Ther. 11, 1037−1040
  48. HajMohammadi, S., Enjyoji, K., Princivalle, M., Christi, P., Lech, M., et al. (2003) Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis. J. Clin. Invest. 111, 989−999
  49. Lowe, J. B. (2002) Glycosylation in the control of selectin counter-receptor structure and function. Immunol. Rev. 186, 19−36
  50. Utt, M., Danielsson, B., and Wadstrom, T. (2001) Helicobacter pylori vacuolating cytotoxin binding to a putative cell surface receptor, heparan sulfate, studied by surface plasmon resonance. FEMS Immunol. Med. Microbiol. 30, 109−113
  51. Chen, Y., Hayashida, A., Bennett, A. E., Hollingshead, S. K., and Park, P. W. (2007) Streptococcus pneumoniae sheds syndecan- 1 ectodomains through ZmpC, a metalloproteinase virulence factor. J. Biol. Chem. 282, 159−167
  52. Kim, H. R., Choi, M. S., and Kim, I. S. (2004) Role of syndecan- 4 in the cellular invasion of Orientia tsutsugamushi. Microb. Pathog. 36, 219−225
  53. Muller, W. A. (2003) Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24, 327−334
  54. Park, P. W., Reizes, O., and Bernfield, M. (2000b) Cell surface heparan sulfate proteoglycans: selective regulators of ligandreceptor encounters. J. Biol. Chem. 275, 29923−29926
  55. Rauch, B. H., Millette, E., Kenagy, R. D., Daum, G., Fischer, J. W., et al. (2005) Syndecan-4 is required for thrombin-induced migration and proliferation in human vascular smooth muscle cells. J. Biol. Chem. 280, 17507−17511
  56. Westphal, V., Murch, S., Kim, S., Srikrishna, G., Winchester, B., et al. (2000) Reduced heparan sulfate accumulation in enterocytes contributes to protein-losing enteropathy in a congenital disorder of glycosylation. Am. J. Pathol. 157, 1917−1925
  57. Ojeh, N., Hiilesvuo, K., Warri, A., Salmivirta, M., Henttinen, T., et al. (2007) Ectopic expression of syndecan-1 in basal epidermis affects keratinocyte proliferation and wound reepithelialization. J. Invest. Dermatol. (in press)
  58. Chen, E., Hermanson, S., and Ekker, S. C. (2004a) Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood 103, 1710−1719
  59. Gengrinovitch, S., Berman, B., David, G., Witte, L., Neufeld, G., et al. (1999) Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165. J. Biol. Chem. 274, 10816−10822
  60. Kerr, A. R., Irvine, J. J., Search, J. J., Gingles, N. A., Kadioglu, A., et al. (2002) Role of inflammatory mediators in resistance and susceptibility to pneumococcal infection. Infect. Immun. 70, 1547−1557
  61. Alexopoulou, A. N., Multhaupt, H. A., and Couchman, J. R. (2007) Syndecans in wound healing, inflammation and vascular biology. Int. J. Biochem. Cell Biol. 39, 505−528
  62. Charnaux, N., Brule, S., Chaigneau, T., Saffar, L., Sutton, A., et al. (2005) RANTES (CCL5) induces a CCR5-dependent accelerated shedding of syndecan-1 (CD138) and syndecan-4 from HeLa cells and forms complexes with the shed ectodomains of these proteoglycans as well as with those of CD44. Glycobiology 15, 119−130
  63. Dias-Baruffi, M., Pereira-da-Silva, G., Jamur, M. C., and Roque- Barreira, M. C. (1998) Heparin potentiates in vivo neutrophil migration induced by IL-8. Glycoconj. J. 15, 523−526
  64. Elenius, K., Maatta, A., Salmivirta, M., and Jalkanen, M. (1992) Growth factors induce 3T3 cells to express bFGF-binding syndecan. J. Biol. Chem. 267, 6435−6441
  65. Yang, Y., Yaccoby, S., Liu, W., Langford, J. K., Pumphrey, C. Y., et al. (2002) Soluble syndecan-1 promotes growth of myeloma tumors in vivo. Blood 100, 610−617
  66. Zen, K. and Parkos, C. A. (2003) Leukocyte-epithelial interactions. Curr. Opin. Cell Biol. 15, 557−564
  67. Henry-Stanley, M. J., Hess, D. J., Erlandsen, S. L., and Wells, C. L. (2005) Ability of the heparan sulfate proteoglycan syndecan- 1 to participate in bacterial translocation across the intestinal epithelial barrier. Shock 24, 571−576
  68. Li, Q., Park, P. W., Wilson, C. L., and Parks, W. C. (2002) Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111, 635−646
  69. Ma, P., Beck, S. L., Raab, R. W., McKown, R. L., Coffman, G. L., et al. (2006) Heparanase deglycanation of syndecan-1 is required for binding of the epithelial-restricted prosecretory mitogen lacritin. J. Cell Biol. 174, 1097−1106
  70. Proudfoot, A. E., Handel, T. M., Johnson, Z., Lau, E. K., Li- Wang, P., et al. (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl. Acad. Sci. USA 100, 1885−1890
  71. Hess, D. J., Henry-Stanley, M., J., Erlandsen, S. L., and Wells, C. J. (2006) Heparan sulfate proteoglycans mediate Staphylococcus aureus interactions with intestinal epithelium. Med. Microbiol. Immunol. 195, 133−141
  72. Kaksonen, M., Pavlov, I., Voikar, V., Lauri, S. E., Hienola, A., et al. (2002) Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol. Cell Neurosci. 21, 158−172
  73. Kojima, T., Takagi, A., Maeda, M., Segawa, T., Shimizu, A., et al. (2001) Plasma levels of syndecan-4 (ryudocan) are elevated in patients with acute myocardial infarction. Thromb. Haemost. 85, 793−799
  74. Middleton, J., Neil, S., Wintle, J., Clark-Lewis, I., Moore, H., et al. (1997) Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91, 385−395
  75. Rot, A. and von Andrian, U. H. (2004) Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22, 891−928
  76. Yang, Y., Macleod, V., Miao, H. Q., Theus, A., Zhan, F., et al. (2007) Heparanase enhances syndecan-1 shedding: a novel mechanism for stimulation of tumor growth and metastasis. J. Biol. Chem. 282, 13326−13333
  77. Fitzgerald, M. L., Wang, Z., Park, P. W., Murphy, G., and Bernfield, M. (2000) Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3 sensitive metalloproteinase. J. Cell Biol. 148, 811− 824
  78. Henry-Stanley, M. J., Zhang, B., Erlandsen, S. L., and Wells, C. L. (2006) Synergistic effect of tumor necrosis factor-alpha and interferon- gamma on enterocyte shedding of syndecan-1 and associated decreases in internalization of Listeria monocytogenes and Staphylococcus aureus. Cytokine 34, 252−259
  79. Shieh, M. T., WuDunn, D., Montgomery, R. I., Esko, J. D., and Spear, P. G. (1992) Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J. Cell Biol. 116, 1273−1281
  80. Bergeron, Y., Ouellet, N., Deslauriers, A. M., Simard, M., Olivier, M., et al. (1998) Cytokine kinetics and other host factors in response to pneumococcal pulmonary infection in mice. Infect. Immun. 66, 912−922
  81. Bernfield, M., Kokenyesi, R., Kato, M., Hinkes, M. T., Spring, J., et al. (1992) Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8, 365−393
  82. Esko, J. D. and Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169−173
  83. Handel, T. M., Johnson, Z., Crown, S. E, Lau, E. K., and Proudfoot, A. E. (2005) Regulation of protein function by glycosaminoglycans - as exemplified by chemokines. Annu. Rev. Biochem. 74, 385−410.
  84. Johnson, Z., Kosco-Vilbois, M., H., Herren, S., Cirillo, R., Muzio, V., et al. (2004) Interference with heparin binding and oligomerization creates a novel anti-inflammatory strategy targeting the chemokine system. J. Immunol. 173, 5776−5785
  85. Kato, M., Saunders, S., Nguyen, H., and Bernfield, M. (1995) Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells. Mol. Biol. Cell. 6, 559−576
  86. Popova, T. G., Millis, B., Bradburne, C., Nazarenko, S., Bailey, C., et al. (2006) Acceleration of epithelial cell syndecan-1 shedding by anthrax hemolytic virulence factors. BMC Microbiol. 6, 8−24
  87. Stepp, M. A., Liu, Y., Pal-Ghosh, S., Jurjus, R. A., Tadvalkar, G., et al. (2007) Reduced migration, altered matrix and enhanced TGFbeta1 signaling are signatures of mouse keratinocytes lacking Sdc1. J. Cell Sci. 120, 2851−2863
  88. Subramanian, S. V., Fitzgerald, M. L., and Bernfield, M. (1997) Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor activation. J. Biol. Chem. 272, 14713−14720
  89. Elenius, V., Götte, M., Reizes, O., Elenius, K., and Bernfield, M. (2004) Inhibition by the soluble syndecan-1 ectodomains delays wound repair in mice overexpressing syndecan-1. J. Biol. Chem. 279, 41928−41935
  90. Yao, Y., Rabodzey, A., and Forbes Dewey, C. Jr. (2007) Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. Am. J. Physiol. Heart Circ. Physiol. 293, H1023−1030
  91. Zhang, L. and Esko, J. D. (1994) Amino acid determinants that drive heparan sulfate assembly in a proteoglycan. J. Biol. Chem. 269, 19295−19299
  92. Chen, Y., Maguire, T., Hileman, R. E., Fromm, J. R., Esko, J. D., et al. (1997) Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3, 866−871
  93. Endo, K., Takino, T., Miyamori, H., Kinsen, H., Yoshizaki, R., et al. (2003) Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278, 40764−40770
  94. Fears, C. Y. and Woods, A. (2006) The role of syndecans in disease and wound healing. Matrix Biol. 25, 443−456
  95. Ishiguro, K., Kadomatsu, K., Kojima, T., Muramatsu, H., Tsuzuki, S., et al. (2000b) Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J. Biol. Chem. 275, 5249−5252
  96. Yu, W. H. and Woessner, J. F. (2000) Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7). J. Biol. Chem. 275, 4183−4191
  97. Brule, S., Charnaux, N., Sutton, A., Ledoux, D., Chaigneau, T., et al. (2006) The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the matrix metalloproteinase- 9. Glycobiology 16, 488−501
  98. Echtermeyer, F., Streit, M., Wilcox-Adelman, S., Saoncella, S., Denhez, F., et al. (2001) Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J. Clin. Invest. 107, R9−R14
  99. Labandeira-Rey, M., Couzon, F., Boisset, S., Brown, E. L., Bes, M., et al. (2007) Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315, 1130− 1133
  100. Patel, K. D., Cuvelier, S. L., and Wiehler, S. (2002) Selectins: critical mediators of leukocyte recruitment. Semin. Immunol. 14, 73−81
  101. Principi, M., Day, R., Marangi, S., Burattini, O., De Francesco, V., et al. (2006) Differential immunohistochemical expression of syndecan-1 and tumor necrosis factor alpha in colonic mucosa of patients with Crohn's disease. Immunopharmacol. Immunotoxicol. 28, 185−195
  102. Sadir, R., Imberty, A., Baleux, F., and Lortat-Jacob, H. (2004) Heparan sulfate/heparin oligosaccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV. J. Biol. Chem. 279, 43854−43860
  103. Schmidt, A., Echtermeyer, F., Alozie, A., Brands, K., and Buddecke, E. (2005) Plasmin- and thrombin-accelerated shedding of syndecan-4 ectodomain generates cleavage sites at Lys(114)-Arg(115) and Lys(129)-Val(130) bonds. J. Biol. Chem. 280, 34441−34446
  104. Wang, L., Fuster, M., Sriramarao, P., and Esko, J. D. (2005) Endothelial heparan sulfate deficiency impairs L-selectinand chemokine-mediated neutrophil trafficking during inflammatory responses. Nat. Immunol. 6, 902−910
  105. Asundi, V. K., Erdman, R., Stahl, R. C., and Carey, D. J. (2003) Matrix metalloproteinase-dependent shedding of syndecan-3, a transmembrane heparan sulfate proteoglycan, in Schwann cells. J. Neurosci. Res. 73, 593−602
  106. Endo, C., Kusachi, S., Yamamoto, K., Murakami, M., Murakami, T., et al. (1997) Time-dependent increases in syndecan-1 and fibroglycan messenger RNA expression in the infarct zone after experimentally induced myocardial infarction in rats. Coron. Artery Dis. 8, 155−161
  107. Hoogewerf, A. J., Kuschert, G. S. V., Proudfoot, A. E., I., Borlat, F., Clark-Lewis, I., et al. (1997) Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 36, 13570−13578
  108. Norgard-Sumnicht, K. E., Varki, N. M., and Varki, A. (1993) Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endothelial cells. Science 261, 480−483
  109. Rostand, K. S. and Esko, J. D. (1997) Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65, 1−8
  110. Beauvais, D. M., Burbach, B. J., and Rapraeger, A. C. (2004) The syndecan-1 ectodomain regulates alphavbeta3 integrin activity in human mammary carcinoma cells. J. Cell Biol. 167, 171−181
  111. Blobel, C. P. (2002) Functional and biochemical characterization of ADAMs and their predicted role in protein ectodomain shedding. Inflamm. Res. 51, 83−84
  112. Haynes, A., Rumbaugh, 3rd, K. P., Park, P. W., Hamood, A. N., and Griswold, J. A. (2005b) Protamine sulfate reduces the susceptibility of thermally injured mice to Pseudomonas aeruginosa infection. J. Surg. Res. 123, 109−117
  113. Lind, T., Tufaro, F., McCormick, C., Lindahl, U., and Lidholt, K. (1998) The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis of heparan sulfate. J. Biol. Chem. 273, 26265−26268
  114. McCormick, C., Duncan, G., Goutsos, K. T., and Tufaro, F. (2000) The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. Proc. Natl. Acad. Sci. USA 97, 668−673
  115. Andrian, E., Grenier, D., and Rouabhia, M. (2005) Porphyromonas gingivalis lipopolysaccharide induces shedding of syndecan-1 expressed by gingival epithelial cells. J. Cell. Physiol. 204, 178−183
  116. Chung, M. C., Popova, T. G., Millis, B. A., Mukherjee, D. W., Zhou, W., et al. (2006) Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J. Biol. Chem. 281, 31408−31418
  117. Esko, J. D. and Selleck, S. B. (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435−471
  118. Vestweber, D. and Blanks, J. E. (1999) Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev. 79, 181−213
  119. Day, R. and Forbes, A. (1999) Heparin, cell adhesion, and pathogenesis of inflammatory bowel disease. Lancet 354, 62−65 https://doi.org/10.1016/S0140-6736(99)90128-9
  120. Diamond, M. S., Alon, R., Parkos, C. A., Quinn, M. T., and Springer, T. A. (1995) Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD18). J. Cell Biol. 130, 1473−1482
  121. Parks, W. C., Wilson, C. L., and López-Boado, Y. S. (2004) Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 4, 617−629
  122. Carey, D. J. (1997) Syndecans: multifunctional cell-surface coreceptors. Biochem. J. 327, 1−16
  123. Essner, J. J., Chen, E., and Ekker, S. C. (2006) Syndecan-2. Int. J. Biochem. Cell Biol. 38, 152−156
  124. Menozzi, F. D., Rouse, J. H., Alavi, M., Laude-Sharp, M., Muller, J., et al. (1996) Identification of a heparin-binding hemagglutinin present in mycobacteria. J. Exp. Med. 184, 993−1001
  125. Fears, C. Y., Gladson, C. L., and Woods, A. (2006) Syndecan-2 is expressed in the microvasculature of gliomas and regulates angiogenic processes in microvascular endothelial cells. J. Biol. Chem. 281, 14533−14536
  126. Jalkanen, M., Rapraeger, A., Saunders, S., and Bernfield, M. (1987) Cell surface proteoglycan of mouse mammary epithelial cells is shed by cleavage of its matrix-binding ectodomain from its membrane-associated domain. J. Cell Biol. 105, 3087−3096
  127. Lortat-Jacob, H., Grosdidier, A., and Imberty, A. (2002) Structural diversity of heparan sulfate binding domains in chemokines. Proc. Natl. Acad. Sci. USA 99, 1229−1234
  128. Ortega-Barria, E. and Pereira, M. E. (1991) A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67, 411−421
  129. Rops, A. L., Gotte, M., Baselmans, M. H., van den Hoven, M. J., Steenbergen, E. J., et al. (2007) Syndecan-1 deficiency aggravates anti-glomerular basement membrane nephritis. Kidney Int. (in press)
  130. Couchman, J. R. and Woods, A. (1996) Syndecans, signaling, and cell adhesion. J. Cell. Physiol. 61, 578−584
  131. Smith, M. F., Novotony, J., Carl, V. S., and Comeau, L. D. (2006) Helicobacter pylori and toll-like receptor agonists induce syndecan-4 expression in an NF-kB-dependent manner. Glycobiology 16, 221−229
  132. Gaffney, P. R., O'Leary, J. J., Doyle, C. T., Gaffney, A., Hogan, J., et al. (1991) Response to heparin in patients with ulcerative colitis. Lancet 337, 238−239
  133. Park, P. W., Pier, G. B., Preston, M., J., Goldberger, O., Fitzgerald, M. L., et al. (2000a) Syndecan-1 shedding is enhanced by LasA, a secreted virulence factor of Pseudomonas aeruginosa. J. Biol. Chem. 275, 3057−3064
  134. Tuomanen, E. I., Austrian, R., and Masure, H. R. (1995) Pathogenesis of pneumococcal infection. N. Engl. J. Med. 332, 1280−1284
  135. Vanhoutte, D., Schellings, M. W., Gotte, M., Swinnen, M., Herias, V., et al. (2007) Increased expression of syndecan-1 protects against cardiac dilatation and dysfunction after myocardial infarction. Circulation 115, 475−482
  136. Gallagher, J. T. (2001) Heparan sulfate: growth control with a restricted sequence menu. J. Clin. Invest. 108, 357−361
  137. Haynes, A., Ruda, 3rd, F., Oliver, J., Hamood, A. N., Griswold, J. A., et al. (2005a) Syndecan-1 shedding contributes to Pseudomonas aeruginosa sepsis. Infect. Immun. 73, 7914− 7921
  138. Kim, C. W., Goldberger, O. A., Gallo, R. L., and Bernfield, M. (1994) Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development- specific patterns. Mol. Biol. Cell. 5, 797−805
  139. Park, P. W., Foster, T. J., Nishi, E., Duncan, S. J., Klagsbrun, M., et al. (2004) Activation of syndecan-1 ectodomain shedding by Staphylococcus aureus ${alpha}$-toxin and ${\beta}-toxin$. J. Biol. Chem. 279, 251−258
  140. Hayashida, K., Johnston, D. R., Goldberger, O., and Park, P. W. (2006) Syndecan-1 expression in epithelial cells is induced by TGF${\beta}$ through a PKA-dependent pathway. J. Biol. Chem. 281, 24365−24374
  141. Shukla, D. and Spear, P. G. (2001) Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Invest. 108, 503−510
  142. Webb, L. M. C., Ehrengruber, M. U., Clark-Lewis, I., Baggiolini, M., and Rot, A. (1993) Binding of heparan sulfate or heparin enhances neutrophil responses to IL-8. Proc. Natl. Acad. Sci. USA 90, 7158−7162
  143. Contreras, H. R., Fabre, M., Granes, F., Casaroli-Marano, R., Rocamora, N., et al. (2001) Syndecan-2 expression in colorectal cancer-derived HT-29 M6 epithelial cells induces a migratory phenotype. Biochem. Biophys. Res. Commun. 286, 742−751
  144. Gotte, M., Joussen, A., M., Klein, C., Andre, P., Wagner, D. D., et al. (2002) Role of syndecan-1 in leukocyte-endothelial interactions in the ocular vasculature. Invest. Ophthalmol. Vis. Sci. 43, 1135−1141
  145. Reizes, O., Lincecum, J., Wang, Z., Goldberger, O., Huang, L., et al. (2001) Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell 106, 105−116

Acknowledgement

Supported by : GlaxoSmith-Kline, Mizutani Foundation Research, National Institutes of Health