Skip to main content

Advertisement

Log in

Protein-glycosaminoglycan interactions: infectiological aspects

  • Review
  • Published:
Medical Microbiology and Immunology Aims and scope Submit manuscript

Abstract

Glycosaminoglycans (GAGs) are linear heteropolysaccharides consisting of repeated disaccharide units that are variablyN- andO-sulfated. Due to this heterogeneity, GAGs possess a high amount of structural information. Linked to a protein core to form a proteoglycan, GAGs are present on the surface of probably all mammalian tissues. During the recent years, a number of pathogens ranging from viruses to protozoans were found to interact specifically with cell surface GAGs to recognize and bind to their target cells. This review is intended to give a short overview over protein-GAG interaction under the aspects of infection.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Baba M, Pauwels R, Balzarini J, Arnout J, Desmyter J, De Clerq E (1988) Mechanism of inhibitory effect of dextran sulfate and heparin on replication of human immunodeficiency virus in vitro. Proc Natl Acad Sci USA 85:6132–6136

    Article  PubMed  CAS  Google Scholar 

  2. Batinic D, Robey FA (1992) The V3 region of the envelope glycoprotein of human immunodeficiency virus type 1 binds sulfated polysaccharides and CD4-derived synthetic peptides. J Biol Chem 267:6664–6671

    PubMed  CAS  Google Scholar 

  3. Bendheim PE, Barry RA, DeArmond SJ, Stites DP, Pruisiner SB (1984) Antibodies to scrapie prion protein. Nature 310:418–421

    Article  PubMed  CAS  Google Scholar 

  4. Bergey EJ, Stinson MW (1988) Heparin-inhibitable basement membrane-binding protein ofStreptococcus pyogenes. Infect Immun 56:1715–1721

    PubMed  CAS  Google Scholar 

  5. Brener Z (1973) The biology ofTrypanosoma cruzi. Annu Rev Microbiol 27:347–381

    Article  PubMed  CAS  Google Scholar 

  6. Callahan LN, Phelan M, Mallinson M, Norcross MA (1991) Dextran sulfate blocks antibody binding to the principal neutralizing domain of human immunodeficiency virus type I without interfering with gp120-CD4 interactions. J Virol 65:1543–1550

    PubMed  CAS  Google Scholar 

  7. Cardin AD, Taylor DL, Krstenansky JL, Tyms AS, Jackson RL (1989) A heparin which binds to the envelope glycoprotein gp120 inhibits human immunodeficiency virus replication. Trans Assoc Am Physicians CII:101–109

    Google Scholar 

  8. Cardin AD, Weintraub HJR (1989) Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9:21–32

    PubMed  CAS  Google Scholar 

  9. Caughey B (1994) Protease-resistant PrP accumulation and scrapie agent replication: a role for sulphated glycosaminoglycans? Biochem Soc Trans 22:163–167

    PubMed  CAS  Google Scholar 

  10. Caughey B, Race RE (1992) Potent inhibition of scrapie-associated PrP accumulation by Congo red. J Neurochem 59:768–771

    PubMed  CAS  Google Scholar 

  11. Caughey B, Raymond GJ (1993) Sulfated polyanion inhibition of scrapie-associated PrP accumulation in cultured cells. J Virol 67:634–650

    Google Scholar 

  12. Caughey B, Ernst D, Race RE (1993) Conge red inhibition of scrapie agent replication. J Virol 67:6270–6272

    PubMed  CAS  Google Scholar 

  13. Caughey B, Brown K, Raymond GJ, Katzenstein GE, Thresher W (1994) Binding of the protease-sensitive form of prion protein PrP to sulfated glycosaminoglycan and congo red. J Virol 68:2135–2141

    PubMed  CAS  Google Scholar 

  14. Cerami C, Frevert U, Sinnis P, Takacs B, Clavijo P, Santos MJ, Nussenzweig V (1992) The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein ofPlasmodium falciparum sporozoites. Cell 70:1021–1033

    Article  PubMed  CAS  Google Scholar 

  15. Cohen JI, Seidel KE (1994) Absence of varicella-zoster virus (VZV) glycoprotein v does not alter growth of VZV in vitro or sensitivity to heparin. J Gen Virol 75:3087–3093

    PubMed  CAS  Google Scholar 

  16. Compton T, Nowlin DM, Cooper NL (1993) Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834–841

    Article  PubMed  CAS  Google Scholar 

  17. Dalgleish AG, Beverley PCL, Clapham PR, Crawford DH, Greaves MF, Weiss RA (1984) CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312:763–767

    Article  PubMed  CAS  Google Scholar 

  18. Flynn SJ, Ryan P (1995) A heterologous heparin-binding domain can promote functional attachment of a Pseudorabies virus gC mutant to cell surfaces. J Virol 69:834–839

    PubMed  CAS  Google Scholar 

  19. Flynn SJ, Burgett BL, Stein DS, Wilkinson KS, Ryan P (1993) The amino-terminal one-third of pseudorabies virus glycoprotein gIII contains a functional attachment domain, but this domain is not required for the efficient penetration of Vero cells. J Virol 67:2646–2654

    PubMed  CAS  Google Scholar 

  20. Fraser PE, Nguyen JT, Chin DT, Kirschner DA (1992) Effects of sulfate ions on Alzheimer β/A4 peptide assemblies: implications for amyloid fibril-proteoglycan interactions. J Neurochem 59:1531–1540

    PubMed  CAS  Google Scholar 

  21. Gerok W, Kottgen E, Reutter W (1982) Glycoproteins on hepatocytic surfaces. Proc Liver Dis 7:87–107

    CAS  Google Scholar 

  22. Glenner GG, Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885–890

    Article  PubMed  CAS  Google Scholar 

  23. Glenner GG, Wong CW (1984) Alzheimer's disease and Down's syndrome: sharing a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 120:1131–1135

    Article  Google Scholar 

  24. Hannah JH, Menozzi FD, Renauld G, Locht C, Brennan MJ (1994) Sulfated glycoconjugate receptors for theBordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA. Infect Immun 62:5010–5019

    PubMed  CAS  Google Scholar 

  25. Haywood AM (1994) Virus receptors: binding, adhesion strengthening, and changes in viral structure. Minireview. J Virol 68:1–5

    PubMed  CAS  Google Scholar 

  26. Herold BC, WuDunn D, Soltys N, Spear PG (1991) Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J Virol 65: 1090–1098

    PubMed  CAS  Google Scholar 

  27. Herold BC, Visalli RJ, Susmarski N, Brandt CR, Spear PC (1994) Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surface heparan sulphate and glycoprotein B J Gen Virol 75:1211–1222

    PubMed  CAS  Google Scholar 

  28. Hinkes MT, Bernfield M (1993) Syndecan. In: Kreis T, Vale R (eds) Guidebook to the extracellular matrix and adhesion proteins. Oxford University Press, New York, pp 91–93

    Google Scholar 

  29. Holt GD, Pangburn MK, Ginsburg V (1989) Properdin binds to sulfatide [Gal(3-SO4)β1-1Cer] and has a sequence homology with other proteins that bind sulfated glycoconjugates. J Biol Chem 265:2852–2855

    Google Scholar 

  30. Ida H, Kurata A, Eguchi K, Yamashita I, Nakashima M, Sakai M, Kawabe Y, Nakamura T, Nagataki S (1994) Mechanism of inhibitory effect of dextran sulfate and heparin on human T-cell lymphotrophic virus type I (HTLV-I)-induced syncytium formation in vitro: role of cell-to-cell contact. Antiviral Res 23: 143–159

    Article  PubMed  CAS  Google Scholar 

  31. Jackson RL, Busch SJ, Cardin AD (1991) Glycosaminoglycans molecular properties, protein interactions, and role in physiological processes. Physiol Rev 71:481–539

    PubMed  CAS  Google Scholar 

  32. Johnson DC, Ligas MW (1988) Herpes simplex viruses lacking glycoprotein D are unable to inhibit virus penetration: quantitative evidence for virus-specific cell surface receptors. J Virol 62:4605–4612

    PubMed  CAS  Google Scholar 

  33. Karger A, Mettenleiter TC (1993) Glycoproteins gIII and gp50 play dominant roles in the biphasic attachment of pseudorabies virus. Virology 194:654–664

    Article  PubMed  CAS  Google Scholar 

  34. Kiyokawa T, Yoshikura H, Hattori S, Seiki M, Yoshida M (1984) Envelope proteins in human T-cell leukemia virus: expression inEscherichia coli and its application to studies of env gene functions. Proc Natl Acad Sci USA 81:6202–6206

    Article  PubMed  CAS  Google Scholar 

  35. Klatzmann D, Champagne E, Chamaret S, Grust J, Guetard D, Hercend T, Gluckman J-C, Montagnier L (1984) T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312:767–768

    Article  PubMed  CAS  Google Scholar 

  36. Kocisko DA, Come JH, Priola SA, Chesebro B, Raymond GJ, Lansbury PT, Caughey B (1994) Cell-free formation of protease-resistant prion protein. Nature 370:471–474

    Article  PubMed  CAS  Google Scholar 

  37. Kosik KS, Joachim CL, Selkoe DJ (1986) Microtubule-associated protein tau (τ) is a major antigenic component of paired filaments in Alzheimer's disease. Proc Natl Acad Sci USA 83: 4044–4048

    Article  PubMed  CAS  Google Scholar 

  38. Kühn JE, Kramer MD, Willenbacher W, Wieland U, Lorentzen EU, Braun RW (1990) Identification of herpes simplex virus type 1 glycoproteins interacting with the cell surface. J Virol 64:2491–2497

    PubMed  Google Scholar 

  39. Lander AD (1993) Proteoglycans. In: Kreis T, Vale R (eds) Guidebook to the extracellular matrix and adhesion proteins. Oxford University Press, New York, pp 12–16

    Google Scholar 

  40. Lee MV-Y, Balin BJ, Otvos L Jr, Trojanowski JQ (1991) A68: a major subunit of paired helical filaments and derived forms of normal tau. Science 251:675–678

    PubMed  CAS  Google Scholar 

  41. Liang OD, Ascencio F, Fransson LA, Wadstrom T (1992) Binding of heparan sulfate toStaphylococcus aureus. Infect Immun 60:899–906

    PubMed  CAS  Google Scholar 

  42. Liang X, Babiuk LA, Zamb TJ (1993) Mapping of heparin-binding structures on bovine herpesvirus 1 and pseudorabies virus glycoprotein gIII glycoproteins. Virology 194:233–243

    Article  PubMed  CAS  Google Scholar 

  43. Love DC, Esko JD, Mosser DM (1993) A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans. J Cell Biol 123:759–766

    Article  PubMed  CAS  Google Scholar 

  44. Lüscher-Mattli M, Glück R, Kempf C, Zanoni-Grassi M (1993) A comparative study of the effect of dextran sulfate on the fusion and the in vitro replication of influenza A and B, Semliki Forest, vesicular stomatitis, rabies, Sendai, and mumps virus. Arch Virol 130:317–326

    Article  PubMed  Google Scholar 

  45. Menozzi FD, Gantiez C, Locht C (1991) Interaction of theBordetella pertussis filamentous hemagglutin with heparin. FEMS Microbiol Lett 78:59–64

    Article  CAS  Google Scholar 

  46. Mettenleiter TC, Zsak L, Zuckermann F, Sugg N, Kern H, Ben-Porat T (1990) Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J Virol 64:278–286

    PubMed  CAS  Google Scholar 

  47. Mitsuya H, Looney DJ, Kuno S, Ueno R, Wong-Staal F, Broder S (1988) Dextran sulfate suppression of viruses in the HIV family: inhibition of virion binding to CD4+ cells. Science 240:646–649

    PubMed  CAS  Google Scholar 

  48. Moulder JW (1991) Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55:143–190

    PubMed  CAS  Google Scholar 

  49. Nahmias AJ, Kibrick S (1964) Inhibitory effect of heparin on herpes simplex virus. J Bacteriol 87:1060–1066

    PubMed  CAS  Google Scholar 

  50. Narindrasorasak S, Lowery D, Gonzalez-DeWitt P, Poorman RA, Greenberg B, Kililevsky R (1991) High affinity interactions between the Alzheimer's beta-amyooid precursor proteins and the basement membrane form of heparan sulfate proteoglycan. J Biol Chem 266:12878–12883

    PubMed  CAS  Google Scholar 

  51. Neyts J, Snoeck R, Schols D, Balzarini J, Esko JD, Schepdael A van De Clerq E (1992) Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparan sulfate. Virology 189:48–58

    Article  PubMed  CAS  Google Scholar 

  52. Okada T, Patterson BK, Otto PA, Gurney ME (1994) HIV type 1 infection of CD4+ T cells depends critically on basic amino acid residues in the V3 domain of envelope glycoprotein 120. AIDS Res Hum Retroviruses 10:803–811

    Article  PubMed  CAS  Google Scholar 

  53. Okazaki K, Matsuzaki T, Sugahara Y, Okada J, Hasebe M, Iwamura Y, Ohnishi M, Kanno T, Shimizu M, Honda E, Kono Y (1991) BHV-1 adsorption is mediated by the interaction of glycoprotein III with heparinlike moiety on the cell surface. Virology 181:666–670

    Article  PubMed  CAS  Google Scholar 

  54. Oohira A, Katoh-Semba R, Watanabe E, Matsui F (1994) Brain development and multiple molecular species of proteoglycan. Neurosci Res 20:195–207

    Article  PubMed  CAS  Google Scholar 

  55. Ortega-Barria E, Pereira MEA (1991) A novelT. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67:411–421

    Article  PubMed  CAS  Google Scholar 

  56. Osame M, Usuku K, Izumo S, Ijichi N, Amitani H, Igata A, Matsumoto M, Tara M (1986) HTLV-I associated myelopathy, a new clinical entity. Lancet I:1031–1032

    Article  Google Scholar 

  57. Pancake SJ, Holt GD, Mellouk S, Hoffman SL (1992) Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J Cell Biol 117:1351–1357

    Article  PubMed  CAS  Google Scholar 

  58. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC (1980) Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci USA 77:7415–7419

    Article  PubMed  CAS  Google Scholar 

  59. Prusiner SB (1994) Biology and genetics of prion diseases. Annu Rev Microbiol 48:655–686

    Article  PubMed  CAS  Google Scholar 

  60. Sattenau QJ, Weiss RA (1988) The CD4 antigen: physiological ligand and HIV receptor. Cell 52:631–633

    Article  Google Scholar 

  61. Sawitzky D, Hampl H, Habermehl K-O (1990) Comparison of heparin-sensitive attachment of pseudorabies virus and herpes simplex virus type 1 and identification of heparin-binding PrV-glycoproteins. J Gen Virol 71:1221–1225

    PubMed  CAS  Google Scholar 

  62. Sawitzky D, Hampl H, Habermehl K-O (1990) Entry of pseudorabies virus into CHO cells is blocked at the level of penetration. Arch Virol 115:309–316

    Article  PubMed  CAS  Google Scholar 

  63. Sawitzky D, Voigt A, Habermehl K-O (1993) A peptide-model for the heparin-binding property of pseudorabies virus glycoprotein III. Med Microbiol Immunol 182:285–292

    Article  PubMed  CAS  Google Scholar 

  64. Schachter J (1988) Overview of human diseases. In Barron AL (ed) Microbiology of Chlamydia. CRC Press, Boca Raton, pp 153–165

    Google Scholar 

  65. Schols D, Pauwels R, Desmyter J, De Clerq E (1990) Dextran sulfate and other polyanionic anti-HIV compounds specifically interact with the viral gp120 glycoprotein expressed by T-cells persistently infected with HIV. Virology 175:556–561

    Article  PubMed  CAS  Google Scholar 

  66. Snow AD, Wight TN (1989) Proteoglycans in the pathogenesis of Alzheimer's disease and other amyloidoses. Neurobiol Aging 10:481–497

    Article  PubMed  CAS  Google Scholar 

  67. Snow AD, Sekiguchi R, Nochlin D, Fraser P, Kimata K, Mizutani A, Arai M, Schreier WA, Morgan DG (1994) An important role of heparin sulfate proteoglycan (Perlecan) in a model system for the deposition and persistence of fibrillar A beta-amyloid in rat brain. Neuron 12:219–234

    Article  PubMed  CAS  Google Scholar 

  68. Taylor HP, Cooper NR (1990) The human cytomegalovirus receptor on fibroblasts is a 30-kilodalton membrane protein. J Virol 64:2484–2490

    PubMed  CAS  Google Scholar 

  69. Trybala E, Bergström T, Svennerholm B, Jeansson S, Glorioso JC, Olofsson S (1994) Localization of a functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulfate. J Gen Virol 75:743–752

    Article  PubMed  CAS  Google Scholar 

  70. Ueno R, Kuno S (1987) Dextran sulphate, a potent anti-HIV agent in vitro having synergism with zidovudine. Lancet I:1379

    Article  Google Scholar 

  71. Vaheri A (1964) heparin and related polyionic substances as virus inhibitors. Acta Pathol Microbiol Scand [Suppl] 171:7–97

    Google Scholar 

  72. Vaheri A, Cantell K (1963) The effect of heparin on herpes simplex virus. Virology 21:661–662

    Article  PubMed  CAS  Google Scholar 

  73. Weiss RA, Clapham P, Nagy K, Hoshino H (1985) Envelope properties of human T-cell leukemia viruses. Curr Top Microbiol Immunol 115:235–246

    PubMed  CAS  Google Scholar 

  74. Witvrouw M, Desmyter J, De Clercq (1995) Antiviral portrait series. 4. Polysulfates as inhibitors of HIV and other enveloped viruses. Antiviral Chem Chemother 5:345–359

    Google Scholar 

  75. WuDunn D, Spear PG (1989) Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol 63:52–58

    PubMed  CAS  Google Scholar 

  76. Wyler DJ (1992) Plasmodium and Babesia. In: Gorbach SL, Bartlett JG, Blacklow NR (eds) Infectious diseases. Saunders, Philadelphia, pp 1967–1978

    Google Scholar 

  77. Wyrick PB, Choong J, Davis CH, Knight ST, Royal MO, Maslow AS, Bagnell CR (1989) Entry of genital Chlamydia trachomatis into polarized human epithelial cells. Infect Immun 57:2378–2389

    PubMed  CAS  Google Scholar 

  78. Zhang JP, Stephens RS (1992) Mechanism ofC. trachomatis attachment to eukaryotic host cells. Cell 69:861–869

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sawitzky, D. Protein-glycosaminoglycan interactions: infectiological aspects. Med Microbiol Immunol 184, 155–161 (1996). https://doi.org/10.1007/BF02456129

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02456129

Key words

Navigation