Skip to main content
SpringerLink
Log in

Endothelial glycocalyx of blood circulation system. I. Detection, components, and structural organization

  • Review Article
  • Published:
Russian Journal of Bioorganic Chemistry Aims and scope Submit manuscript

Abstract

The luminal surface of a blood vessel accommodates a complex multicomponent system of mainly carbohydrates and proteins called glycocalyx. According to the concept of the double protective layer, glycocalyx is the first protection barrier of the vascular wall. The structure of glycocalyx is determined by a group of proteoglycans, glycoproteins, and glycosaminoglycans. Two groups of molecules are distinguished within the glycocalyx constituents, that is, membrane proteoglycans (syndecans and glypicans bound to endothelial cell membranes) and soluble proteoglycans (perlecan, biglycan, versican, decorin, and mimecan). There are five types of glycosaminoglycan chains; these are heperan sulfate, chondroitin sulfate, dermatan sulfate, keratan sulfate, and hyaluronan. There is a dynamic equilibrium between the soluble components of glycocalyx and flowing blood, which allows for separation of the endothelial surface layer. Due to its complexity and location at the interface of blood circulation system, glycocalyx is involved in the maintenance of vascular homeostasis. Here, the molecular composition of glycocalyx, properties of its components, biosynthesis, and common structural features are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CLSM and TPLSM:

scanning and two-photon laser scanning microscopy

FITC:

fluorescein isothiocyanate

GFI:

glycosyl phosphatidylinositol

HAS:

hyaluronan synthases

TNFα:

tumor necrosis factor α

ROS:

reactive oxygen species

GAG:

glycosaminoglycans

LDL:

low density lipoproteins

PG:

proteoglycans

EG:

endothelial glycocalyx

References

  1. Pries, A.R., Secomb, T.W., and Gaehtgens, P., Pflugers Arch., 2000, vol. 440, pp. 653–666.

    Article  PubMed  CAS  Google Scholar 

  2. Weinbaum, S., Tarbell, J.M., and Damiano, E.R., Annu. Rev. Biomed. Eng., 2007, vol. 9, pp. 121–167.

    Article  PubMed  CAS  Google Scholar 

  3. Dvorak, H.F., Curr. Opin. Hematol., 2010, vol. 17, pp. 225–229.

    PubMed Central  PubMed  CAS  Google Scholar 

  4. Starling, E.H., J. Physiol., 1896, vol. 19, pp. 312–326.

    PubMed Central  PubMed  CAS  Google Scholar 

  5. Weinbaum, S., Ann. Biomed. Eng., 1998, vol. 26, pp. 627–643.

    Article  PubMed  CAS  Google Scholar 

  6. Michel, C.C., Exp. Physiol., 1997, vol. 82, pp. 1–30.

    PubMed  CAS  Google Scholar 

  7. Danielli, J.F., J. Physiol., 1940, vol. 98, pp. 109–129.

    PubMed Central  PubMed  CAS  Google Scholar 

  8. Chambers, R. and Zweifach, B.W., Physiol. Rev., 1947, vol. 27, pp. 436–463.

    PubMed  CAS  Google Scholar 

  9. Luft, J.H., Fed. Proc., 1966, vol. 25, pp. 1773–1783.

    PubMed  CAS  Google Scholar 

  10. Baldwin, A.L. and Winlove, C.P., J. Histochem. Cytochem., 1984, vol. 32, pp. 259–266.

    Article  PubMed  CAS  Google Scholar 

  11. Clough, G. and Moffitt, H., Int. J. Microcirc. Clin. Exp., 1992, vol. 11, pp. 345–358.

    PubMed  CAS  Google Scholar 

  12. Adamson, R.H. and Clough, G., J. Physiol., 1992, vol. 445, pp. 473–486.

    PubMed Central  PubMed  CAS  Google Scholar 

  13. Damiano, E.R., Microvasc. Res., 1998, vol. 55, pp. 77–91.

    Article  PubMed  CAS  Google Scholar 

  14. Secomb, T.W., Hsu, R., and Pries, A.R., Am. J. Physiol. Heart Circ. Physiol., 2001, vol. 281, pp. H629–H636.

    PubMed  CAS  Google Scholar 

  15. Berg, B.M., Vink, H., and Spaan, J.A., Circ. Res., 2003, vol. 92, pp. 592–594.

    Article  PubMed  CAS  Google Scholar 

  16. Sims, D.E. and Horne, M.M., Eur. J. Morphol., 1993, vol. 31, pp. 251–255.

    PubMed  CAS  Google Scholar 

  17. Hjalmarsson, C., Johansson, B.R., and Haraldsson, B., Microvasc. Res., 2004, vol. 67, pp. 9–17.

    Article  PubMed  Google Scholar 

  18. Rostgaard, J. and Qvortrup, K., Microvasc. Res., 1997, vol. 53, pp. 1–13.

    Article  PubMed  CAS  Google Scholar 

  19. Rostgaard, J. and Qvortrup, K., Cells Tissues Organs, 2002, vol. 170, pp. 132–138.

    Article  PubMed  Google Scholar 

  20. Vink, H. and Duling, B.R., Circ. Res., 1996, vol. 79, pp. 581–589.

    Article  PubMed  CAS  Google Scholar 

  21. Constantinescu, A.A., Vink, H., and Spaan, J.A., Arterioscler. Thromb. Vasc. Biol., 2003, vol. 23, pp. 1541–1547.

    Article  PubMed  CAS  Google Scholar 

  22. Vink, H., Constantinescu, A.A., and Spaan, J.A., Circulation, 2000, vol. 101, pp. 1500–1502.

    Article  PubMed  CAS  Google Scholar 

  23. Smith, M.L., Long, D.S., Damiano, E.R., and Ley, K., Biophys. J., 2003, vol. 85, pp. 637–645.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  24. Damiano, E.R., Long, D.S., and Smith, M.L., J. Fluid Mech., 2004, vol. 512, pp. 1–19.

    Article  Google Scholar 

  25. Florian, J.A., Kosky, J.R., Ainslie, K., Pang, Z., Dull, R.O., and Tarbell, J.M., Circ. Res., 2003, vol. 93, pp. e136–e142.

    Article  PubMed  CAS  Google Scholar 

  26. Mulivor, A.W. and Lipowsky, H.H., Am. J. Physiol. Heart Circ. Physiol., 2004, vol. 286, pp. H1672–H1680.

    Article  PubMed  CAS  Google Scholar 

  27. Barker, A.L., Konopatskaya, O., Neal, C.R., Macpherson, J.V., Whatmore, J.L., Winlove, C.P., Unwin, P.R., and Shore, A.C., Phys. Chem. Chem. Phys., 2004, vol. 6, pp. 1006–1011.

    Article  CAS  Google Scholar 

  28. Megens, R.T., Reitsma, S., Schiffers, P.H., Hilgers, R.H., De Mey, J.G., Slaaf, D.W., de Egbrink, M.G., and van Zandvoort, M.A., J. Vasc. Res., 2007, vol. 44, pp. 87–98.

    Article  PubMed  CAS  Google Scholar 

  29. Nieuwdorp, M., Meuwese, M.C., Mooij, H.L., Ince, C., Broekhuizen, L.N., Kastelein, J.J., Stroes, E.S., and Vink, H., J. Appl. Physiol., 2008, vol. 104, pp. 845–852.

    Article  PubMed  Google Scholar 

  30. den Uil, C.A., Klijn, E., Lagrand, W.K., Brugts, J.J., Ince, C., Spronk, P.E., and Simoons, M.L., Prog. Cardiovasc. Dis., 2008, vol. 51, pp. 161–170.

    Article  Google Scholar 

  31. Raman, R., Sasisekharan, V., and Sasisekharan, R., Chem. Biol., 2005, vol. 12, pp. 267–277.

    Article  PubMed  CAS  Google Scholar 

  32. Lawrenson, J.G., Cassella, J.P., Hayes, A.J., Firth, J.A., and Allt, G., J. Anat., 2000, vol. 196, pp. 55–60.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  33. Bernfield, M., Gotte, M., Park, P.W., Reizes, O., Fitzgerald, M.L., Lincecum, J., and Zako, M., Annu. Rev. Biochem., 1999, vol. 68, pp. 729–777.

    Article  PubMed  CAS  Google Scholar 

  34. Osterloh, K., Ewert, U., and Pries, A.R., Am. J. Physiol. Heart Circ. Physiol., 2002, vol. 283, pp. H398–H405.

    PubMed  CAS  Google Scholar 

  35. McGee, M.P. and Liang, J., J. Biol. Chem., 2001, vol. 276, pp. 49275–49282.

    Article  PubMed  CAS  Google Scholar 

  36. Coombe, D.R. and Kett, W.C., Cell Mol. Life Sci., 2005, vol. 62, pp. 410–424.

    Article  PubMed  CAS  Google Scholar 

  37. Lipowsky, H.H., Microcirculation, 2005, vol. 12, pp. 5–15.

    Article  PubMed  Google Scholar 

  38. Obunike, J.C., Pillarisetti, S., Paka, L., Kako, Y., Butteri, M.J., Ho, Y.Y., Wagner, W.D., Yamada, N., Mazzone, T., Deckelbaum, R.J., and Goldberg, I.J., Arterioscler. Thromb. Vasc. Biol., 2000, vol. 20, pp. 111–118.

    Article  PubMed  CAS  Google Scholar 

  39. Reitsma, S., Slaaf, D.W., Vink, H., van Zandvoort, M.A., and de Egbrink, M.G., Pflugers Arch., 2007, vol. 454, pp. 345–359.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  40. Zeng, Y., Ebong, E.E., Fu, B.M., and Tarbell, J.M., PLos ONE, 2012, vol. 7, p. e43168. doi: 10.1371/journal.pone0043168 (www.plosone.org).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  41. Landsverk, S.A., Tsai, A.G., Cabrales, P., and Intaglietta, M., Crit. Care Res. Pract., 2012, vol. 2012, Article ID 842545. doi: 10.1155/2012/842545

  42. Taylor, K.R. and Gallo, R.L., FASEB J., 2006, vol. 20, pp. 9–22.

    Article  PubMed  CAS  Google Scholar 

  43. Gandhi, N.S. and Mancera, R.L., Chem. Biol. Drug Des., 2008, vol. 72, pp. 455–482.

    Article  PubMed  CAS  Google Scholar 

  44. Jackson, R.L., Busch, S.J., and Cardin, A.D., Physiol. Rev., 1991, vol. 71, pp. 481–539.

    PubMed  CAS  Google Scholar 

  45. Oohira, A., Wight, T.N., and Bornstein, P., J. Biol. Chem., 1983, vol. 258, pp. 2014–2021.

    PubMed  CAS  Google Scholar 

  46. Sasisekharan, R. and Venkataraman, G., Curr. Opin. Chem. Biol., 2000, vol. 4, pp. 626–631.

    Article  PubMed  CAS  Google Scholar 

  47. Sugahara, K. and Kitagawa, H., IUBMB Life, 2002, vol. 54, pp. 163–175.

    Article  PubMed  CAS  Google Scholar 

  48. Silbert, J.E. and Sugumaran, G., IUBMB Life, 2002, vol. 54, pp. 177–186.

    Article  PubMed  CAS  Google Scholar 

  49. Solursh, M., Hardingham, T.E., Hascall, V.C., and Kimura, J.H., Dev. Biol., 1980, vol. 75, pp. 121–129.

    Article  PubMed  CAS  Google Scholar 

  50. Almond, A. and Sheehan, J.K., Glycobiology, 2000, vol. 10, pp. 329–338.

    Article  PubMed  CAS  Google Scholar 

  51. Seog, J., Dean, D., Rolauffs, B., Wu, T., Genzer, J., Plaas, A.H., Grodzinsky, A.J., and Ortiz, C., J. Biomech., 2005, vol. 38, pp. 1789–1797.

    Article  PubMed  Google Scholar 

  52. Maksimenko, A.V., Shchechilina, Yu.V., and Tishchenko, E.G., Biochemistry (Moscow), 2003, vol. 68, pp. 862–868.

    Article  CAS  Google Scholar 

  53. Iozzo, R.V. and San, Antonio, J.D., J. Clin. Invest., 2001, vol. 108, pp. 349–355.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  54. Liu, D., Shriver, Z., Qi, Y., Venkataraman, G., and Sasisekharan, R., Semin. Thromb. Hemost., 2002, vol. 28, pp. 67–78.

    Article  PubMed  CAS  Google Scholar 

  55. Timar, J., Lapis, K., Dudis, J., Sebestyen, A., Kopper, L., and Kovalszky, I., Semin. Cancer, 2002, vol. 12, pp. 173–186.

    Article  CAS  Google Scholar 

  56. Sanderson, R.D., Cell Dev. Biol., 2001, vol. 12, pp. 89–98.

    Article  CAS  Google Scholar 

  57. Liu, J. and Pedersen, L.C., Appl. Microbiol. Biotechnol., 2007, vol. 74, pp. 263–272.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  58. Filmus, J., Glycobiology, 2001, vol. 11, pp. 19R–23R.

    Article  PubMed  CAS  Google Scholar 

  59. Casu, B., Vlodavsky, I., and Sanderson, R.D., Pathophysiol. Haemost. Thromb., 2008, vol. 36, pp. 195–203.

    Article  PubMed  CAS  Google Scholar 

  60. Kisilevsky, R., Ancsin, J.B., Szarek, W.A., and Petanceska, S., Amyloid, 2007, vol. 14, pp. 21–32.

    Article  PubMed  CAS  Google Scholar 

  61. Ley, K., Laudanna, C., Cybulsky, M.I., and Nourshargh, S., Nat. Rev. Immunol., 2007, vol. 7, pp. 678–689.

    Article  PubMed  CAS  Google Scholar 

  62. Rostand, K.S. and Esko, J.D., Infect. Immun., 1997, vol. 65, pp. 1–8.

    PubMed Central  PubMed  CAS  Google Scholar 

  63. Broekhuizen, L.N., Mooij, H.L., Kastelein, J.J., Stroes, E.S., Vink, H., and Nieuwdorp, M., Curr. Opin. Lipidol., 2009, vol. 20, pp. 57–62.

    Article  PubMed  CAS  Google Scholar 

  64. Lopez-Quintero, S.V., Amaya, R., Pahakis, M., and Tarbell, J.M., Am/ J. Physiol. Heart Circ. Physiol., 2009, vol. 296, pp. H1451–H1456.

    Article  CAS  Google Scholar 

  65. Esko, J.F., Kimata, K., and Lindahl, U., Essentials of Glycobiology, 2nd ed., New York: Cold Spring Harbor Laboratory Press, 2009.

    Google Scholar 

  66. Rapraeger, A., Jalkanen, M., Endo, E., Koda, J., and Bernfield, M., J. Biol. Chem., 1985, vol. 260, pp. 11046–11052.

    PubMed  CAS  Google Scholar 

  67. Tkachenko, E., Rhodes, J.M., and Simons, M., Circ. Res., 2005, vol. 96, pp. 488–500.

    Article  PubMed  CAS  Google Scholar 

  68. Rosenberg, R.D., Shworak, N.W., Liu, J., Schwartz, J.J., and Zhang, L., J. Clin. Invest., 1997, vol. 99, pp. 2062–2070.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  69. Halden, Y., Rek, A., Atzenhofer, W., Szilak, L., Wabnig, A., and Kungl, A.J., Biochem. J., 2004, vol. 377, pp. 533–538.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  70. Kokenyesi, R. and Bernfield, M., J. Biol. Chem., 1994, vol. 269, pp. 12304–12309.

    PubMed  CAS  Google Scholar 

  71. Fransson, L.A., Belting, M., Cheng, F., Jonsson, M., Mani, K., and Sandgren, S., Cell Mol., Life Sci., 2004, vol. 61, pp. 1016–1024.

    Article  CAS  Google Scholar 

  72. Belting, M., Trends Biochem. Sci., 2003, vol. 28, pp. 145–151.

    Article  PubMed  CAS  Google Scholar 

  73. van Deurs, B., Roepstorff, K., Hommelgaard, A.M., and Sandvig, K., Trends Cell Biol., 2003, vol. 13, pp. 92–100.

    Article  PubMed  Google Scholar 

  74. Jackson, D.G., Immunol. Rev., 2009, vol. 230, pp. 216–231.

    Article  PubMed  CAS  Google Scholar 

  75. Evanko, S.P., Tammi, M.I., Tammi, R.H., and Wight, T.N., Adv. Drug Deliv. Rev., 2007, vol. 59, pp. 1351–1365.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  76. Segev, A., Nili, N., and Strauss, B.H., Cardiovasc. Res., 2004, vol. 63, pp. 603–610.

    Article  PubMed  CAS  Google Scholar 

  77. Wight, T.N., Front. Biosci., 2008, vol. 13, pp. 4933–4937.

    Article  PubMed  CAS  Google Scholar 

  78. Lawrenson, J.G., Cassella, J.P., Hayes, A.J., Firth, J.A., and Allt, G., J. Anat., 2000, vol. 196, pp. 55–60.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  79. Levi, M., van der Poll, T., and Buller, H.R., Circulation, 2004, vol. 109, pp. 2698–2704.

    Article  PubMed  Google Scholar 

  80. Levi, M., Keller, T.T., van Gorp, E., and Cate, H., Cardiovasc. Res., 2003, vol. 60, pp. 26–39.

    Article  PubMed  CAS  Google Scholar 

  81. Ruegg, C. and Mariotti, A., Cell Mol. Life Sci., 2003, vol. 60, pp. 1135–1157.

    PubMed  CAS  Google Scholar 

  82. Galkina, E. and Ley, K., Arterioscler. Thromb. Vasc. Biol., 2007, vol. 27, pp. 2292–2301.

    Article  PubMed  CAS  Google Scholar 

  83. Xiong, J.P., Stehle, T., Goodman, S.L., and Arnaout, M.A., J. Thromb. Haemost., 2003, vol. 1, pp. 1642–1654.

    Article  PubMed  CAS  Google Scholar 

  84. Kansas, G.S., Saunders, K.B., Ley, K., Zakrzewicz, A., Gibson, R.M., Furie, B.C., Furie, B., and Tedder, T.F., J. Cell Biol., 1994, vol. 124, pp. 609–618.

    Article  PubMed  CAS  Google Scholar 

  85. Zarbock, A. and Ley, K., Microcirculation, 2009, vol. 16, pp. 31–42.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  86. Tanaka, K.A., Key, N.S., and Levy, J.H., Anesth. Analg., 2009, vol. 108, pp. 1433–1446.

    Article  PubMed  CAS  Google Scholar 

  87. Berndt, M.C., Shen, Y., Dopheide, S.M., Gardiner, E.E., and Andrews, R.K., Thromb. Haemost., 2001, vol. 86, pp. 178–188.

    PubMed  CAS  Google Scholar 

  88. Ruggeri, Z.M., J. Thromb. Haemost., 2003, vol. 1, pp. 1335–1342.

    Article  PubMed  CAS  Google Scholar 

  89. Wu, G., Essex, D.W., Meloni, F.J., Takafuta, T., Fujimura, K., Konkle, B.A., and Shapiro, S.S., Blood, 1997, vol. 90, pp. 2660–2669.

    PubMed  CAS  Google Scholar 

  90. Squire, J.M., Chew, M., Nneji, G., Neal, C., Barry, J., and Michel, C., J. Struct. Biol., 2001, vol. 136, pp. 239–255.

    Article  PubMed  CAS  Google Scholar 

  91. Weinbaum, S., Zhang, X., Han, Y., Vink, H., and Cowin, S.C., Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 7988–7995.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  92. Golovanov, M.B. and Bauer, J., Colloids Surf., 2005, vol. 44, pp. 167–171.

    Article  CAS  Google Scholar 

  93. Golovanov, M.V., Vestn. RONTs, 2006, vol. 17, pp. 4–6.

    Google Scholar 

  94. Henry, C.B. and Duling, B.R., Am. J. Physiol., 1999, vol. 277, pp. H508–H514.

    PubMed  CAS  Google Scholar 

  95. Van Teeffelen, J.W., Brands, J., Stroes, E.S., and Vink, H., Trends. Cardiovasc. Med., 2007, vol. 17, pp. 101–105.

    Article  PubMed  CAS  Google Scholar 

  96. Fries, E. and Kaczmarczyk, A., Acta Biochim. Pol., 2003, vol. 50, pp. 735–742.

    PubMed  CAS  Google Scholar 

  97. Platts, S.H. and Duling, B.R., Circ. Res., 2004, vol. 94, pp. 77–82.

    Article  PubMed  CAS  Google Scholar 

  98. Vink, H. and Duling, B.R., Am. J. Physiol. Heart Circ. Physiol., 2000, vol. 278, pp. H285–H289.

    PubMed  CAS  Google Scholar 

  99. Itano, N. and Kimata, K., IUBMB Life, 2002, vol. 54, pp. 195–199.

    Article  PubMed  CAS  Google Scholar 

  100. Weigel, P.H. and DeAngelis, P.L., J. Biol. Chem., 2007, vol. 282, pp. 36777–36781.

    Article  PubMed  CAS  Google Scholar 

  101. Jiang, D., Liang, J., and Noble, P.W., Annu. Rev. Cell Dev. Biol., 2007, vol. 23, pp. 435–461.

    Article  PubMed  CAS  Google Scholar 

  102. Maksimenko, A.V. and Turashev, A.D., Biochem. Res. Intern., 2012, vol. 2012, Article ID 859231. doi: 10.1155/2012/859231/

Download references

Author information

Authors and Affiliations

  1. Institute for Experimental Cardiology, Russian Cardiology Research and Production Complex, Ministry of Healthcare of the Russian Federation, ul. Tretya Cherepkovskaya 15a, Moscow, 121552, Russia

    A. V. Maksimenko & A. D. Turashev

Authors
  1. A. V. Maksimenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. D. Turashev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. V. Maksimenko.

Additional information

Original Russian Text © A.V. Maksimenko, A.D. Turashev, 2014, published in Bioorganicheskaya Khimiya, 2014, Vol. 40, No. 2, pp. 131–141.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maksimenko, A.V., Turashev, A.D. Endothelial glycocalyx of blood circulation system. I. Detection, components, and structural organization. Russ J Bioorg Chem 40, 119–128 (2014). https://doi.org/10.1134/S1068162014020113

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162014020113

Keywords

Search

Navigation