Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: Key events in microbial pathogenicity

Journal of Medical Microbiology

Volumn 48, Issue 3, 1999, Pages 223-233

  Wadström, Torkel ^a   Ljungh, Åsa ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; BACTERIAL PROTEIN; BINDING PROTEIN; CYTOKINE; DERMATAN SULFATE; GLYCOSAMINOGLYCAN; GLYPICAN; GROWTH FACTOR; HEPARAN SULFATE; HEPARIN; HEPARIN BINDING PROTEIN; PERLECAN; SYNDECAN; VIRUS PROTEIN;

ARTHRITIS; BACTERIUM ADHERENCE; BORDETELLA PERTUSSIS; BRAIN MALARIA; CHLAMYDIA TRACHOMATIS; DENGUE VIRUS; EUKARYOTIC CELL; EXTRACELLULAR MATRIX; HELICOBACTER PYLORI; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; LEISHMANIA; NONHUMAN; PARASITE DEVELOPMENT; PATHOGENICITY; PLASMODIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTOZOON; REVIEW; SYNOVIUM;

EID: 0032788960     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/00222615-48-3-223     Document Type: Review

References (90)

1. Rostand KS, Esko JD. Microbial adherence to and invasion through proteoglycans. Infect Immun 1997; 65: 1-8.
2. Norkin L.C. Virus receptors: implications for pathogenesis and the design of antiviral agents. Clin Microbiol Rev 1995; 8: 293-315.
3. Ljungh Å, Wadstöm T. Binding of extracellular matrix proteins by microbes. In: Doyle RJ, Ofek (eds) Adhesion of microbial pathogens. Methods in enzymology, vol 253. New York, Academic Press. 1995: 501-514.
4. Ljungh Å, Moran AP, Wadström T. Interactions of bacterial adhesins with extracellular matrix and plasma proteins: pathogenic implications and therapeutic possibilities. FEMS Immunol Med Microbiol 1996; 16: 117-126.
5. Conrad HE. Heparin-binding proteins. San Diego, Academic Press. 1998.
6. Vlodavsky I, Bar-Shavit R, Korner G, Fuks Z. Extracellular matrix-bound growth factors, enzymes and plasma proteins. In: Rohrbach DH, Timpl R (eds) Basement membranes: cellular and molecular aspects. Orlando, Academic Press. 1993: 327-342.
7. Wadström T, Trust TJ. Bacterial lectins. In: Easmon CSF, Jeljaszewicz J (eds) Medical microbiology IV. London, Academic Press. 1984: 287-334.
8. WuDunn D, Spear PG. Initial interaction of Herpes simplex virus with cells is binding to heparan sulfate. J Virol 1989; 63: 52-58.
9. Utt M, Wadström T. Identification of heparan sulphate binding surface proteins of Helicobacter pylori: inhibition of heparan sulphate binding with sulphated carbohydrate polymers. J Med Microbiol 1997; 46: 541-546.
10. Liang OD, Ascencio F, Fransson L-Å, Wadström T. Binding of heparan sulfate to Staphylococcus aureus. Infect Immun 1992; 60: 899-906.
11. Bergey EJ, Stinson MW. Heparin-inhibitable basement membrane-binding protein of Streptococcus pyogenes. Infect Immun 1988; 56: 1715-1721.
12. Ortega-Barria E, Pereira MEA. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 1991; 67: 411-421.
13. Ouaissi MA, Dutoit E, Vernes A, Guerret-Stocker S, Capron A. In vitro inhibition of Plasmodium falciparum merozoite invasion by human plasma fibronectin. Parasitology 1985; 90: 227-236.
14. Lahav J. The functions of thrombospondin and its involvement in physiology and pathophysiology. Biochim Biophys Acta 1993; 1182: 1-14.
15. Pancake SJ, Holt GD, Mellouk S, Hoffman SL, Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J Cell Biol 1992; 117: 1351-1357.
16. Kulane A, Ekre H-P, Perlmann P, Rombo L, Wahlgren M, Wahlin B. Effect of different fractions of heparin on Plasmodium falciparum merozoite invasion of red blood cells in vitro. Am J Trop Med Hyg 1992; 46: 589-594.
17. Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV. Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J Exp Med 1995; 182: 15-20.
18. Menozzi FD, Rouse JH, Alavi M. et al. Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med 1996; 184: 993-1001.
19. Alvarez-Domínguez C, Vázquez-Boland J-A, Carrasco-Marín E, López-Mato P, Leyva-Cobián F. Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect Immun 1997; 65: 78-88.
20. Chen T, Swanson J, Wilson J, Belland RJ. Heparin protects Opa ' Neisseria gonorrhoeae from the bactericidal action of normal human serum. Infect Immun 1995; 63: 1790-1795.
21. Guo BP, Norris SJ, Rosenberg LC, Höök M. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect Immun 1995; 63: 3467-3472.
22. Alderete JF, Baseman JB. Serum lipoprotein binding by Treponema pallidum: possible role for proteoglycans. Genitourin Med 1989; 65: 177-182.
23. Chen Y, Maguire T, Hileman RE et al. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 1997; 3: 866-871.
24. Hart CA. Prion disease. Br J Hosp Med 1996; 56: 64-65.
25. Lane DA, Lindahl U. Heparin. London, Edward-Arnold, 1989.
26. Limper AH, Standing JE. Vitronectin interacts with Candida albicans and augments organism attachment to the NR8383 macrophage cell line. Immunol Lett 1995; 42 139-144.
27. Avila JL, Rojas M, Velazquez-Avila G, von der Mark H, Timpl R. Antibodies to basement protein nidogen in Chagas' disease and American cutaneous leishmaniasis. J Clin Microbiol 1986; 24: 775-778.
28. Frevert, U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 1993; 177: 1287-1298.
29. Carlson J, Ekre H-P, Helmby H, Gysin J, Greenwood BM, Wahlgren M. Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. Am J Trop Med Hyg 1992; 46: 595-602.
30. Vaheri A. Heparin and related polyionic substances as virus inhibitors, Acta Pathol Microbiol Scand 1964; Suppl 171: 1-98.
31. Howell AL, Taylor TH, Miller JD, Groveman DS, Eccles EH, Zacharski LR. Inhibition of HIV-1 infectivity by low molecular weight heparin. Results of in vitro studies and a pilot clinical trial in patients with advanced AIDS. Int J Clin Lab Res 1996; 26: 124-131.
32. Tyrrell DJ, Kilfeather S, Page CP. Therapeutic uses of heparin beyond its traditional role as an anticoagulant. Trends Polysacch Sci 1996; 16: 198-204.
33. Prioli RP, Roenberg I, Pereira MEA. Specific inhibition of Trypanosoma cruzi neuraminidase by the human plasma glycoprotein 'cruzin'. Proc Natl Acad Sci USA 1987; 84: 3097-3101.
34. Yamaguchi H, Osaki T, Kurihara N et al. Heat-shock protein 60 homologue of Helicobacter pylori is associated with adhesion of H. pylori to human gastric epithelial cells. J Med Microbiol 1997; 46: 825-831.
35. Stephens RS. Molecular mimicry and Chlamydia-host cell interactions. In: Mårdh PA, La Placa M, Ward M (eds) Proceedings of the European Society for Chlamydia research. Uppsala, Uppsala University Centre for STD Research. 1992: 5-9.
36. Yi Y, Yang X, Brunbam RC. Autoimmunity to heat shock protein 60 and antigen-specific production of interleukin-10. Infect Immun 1997; 65: 1669-1674.
37. Klotz SA, Smith RL. Glycosaminoglycans inhibit Candida albicans adherence lo extracellular matrix proteins. FEMS Microbiol Lett 1992; 99: 205-208.
38. Swoboda RK, Bertram G, Budge S, Gooday GW, Gow NAR, Brown AJP. Structure and regulation of the HSP90 gene from the pathogenic fungus Candida albicans. Infect Immun 1995; 63: 4506-4514.
39. Geuijen CAW, Willems RJL, Hoogerhout P, Puijk WC, Meloen RH, Mooi FR. Identification and characterization of heparin binding regions of the Fim2 subunit of Bordetella pertussis. Infect Immun 1998; 66: 2256-2263.
40. Stearns NA, Prigent-Richard S, Letourneur D, Castellot JJ. Synthesis and characterization of highly sensitive heparin probes for detection of heparin-binding proteins. Anal Biochem 1997; 247: 348-356.
41. Keller JM. Specificity in heparin/heparan sulphate-protein interactions. Glycobiology 1994; 4: 1-2.
42. Ascencio F, Liang OD, Schmidt KH, Fransson L-Å, Wadström T. Comparative studies on heparin- and heparan sulfate-binding bacterial lectins. In: van Driessche E, Franz H, Beeckmans S, Pfüller U, Kallikorm A, Bög-Hansen TC (eds) Lectins. Hellerup, Textop. 1993: 235-242.
43. Covacci A, Rappuoli R. Helicobacter pylori: molecular evaluation of a bacterial quasi-species. Curr Opin Microbiol 1998; 1: 96-102.
44. Hannah JH, Menozzi FD, Renauld G, Locht C, Brennan MJ. Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain of FHA. Infect Immun 1994; 62: 5010-5019.
45. van't Wout J, Burnette WN, Mar VL, Rozdzinski E, Wright SD, Tuomanen EI. Role of carbohydrate recognition domains of pertussis toxin in adherence of Bordetella pertussis to human macrophages. Infect Immun 1992; 60: 3303-3308.
46. Sandros J, Tuomanen E. Attachment factors of Bordetella pertussis: mimicry of cukaryotic cell recognition molecules. Trends Microbiol 1993; 1: 192-195.
47. Noel GJ, Love DC, Mosser DM. High-molecular-weight proteins of nontypeable Haemophilus influenzae mediate bacterial adhesion to cellular proteoglycans. Infect Immun 1994; 62: 4028-4033.
48. Tomb J-F, White O, Kerlavage AR et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997; 388: 539-547.
49. Krivan HC, Olson LD, Barile MF, Ginsburg V, Roberts DD. Adhesion of Mycoplasma pneumoniae to sulfated glycolipids and inhibition by dextran sulfate. J Biol Chem 1989; 264: 9283-9288.
50. Guruge JL, Falk PG, Lorenz RG et al. Epithelial attachment alters the outcome of Helicobacter pylori infection. Proc Natl Acad Sci USA 1998; 95: 3925-3930.
51. Ilver D, Arnqvist A, Ögren J et al. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998; 279: 373-377.
52. van Putten JPM, Hayes SF, Duensing TD. Natural proteoglycan receptor analogs determine the dynamics of Opa adhesin-mediated gonococcal infection of Chang epithelial cells. Infect Immun 1997; 65: 5028-5034.
53. Burillo CA, Fontenot JD, Phillips DM. Sulfated polysaccharides block chlamydia infection in vitro, but do not protect mice from vaginal inoculation. Microb Pathog 1998; 24: 253-256.
54. Chen JC-R, Zhang JP, Stephens RS. Structural requirements of heparin binding to Chlamydia trachomatis. J Biol Chem 1996; 271: 11134-11140.
55. Chen JC-R, Stephens RS. Chlamydia trachomatis glycosamino-glycan-dependent and independent attachment to cukaryotic cells. Microb Pathog 1997; 22: 23-30.
56. Kuo C-C, Jackson LA, Campbell LA, Grayston JT. Chlamydia pneumoniae (TWAR). Clin Microbiol Rev 1995; 8: 451-461.
57. Stephens RS. Molecular mimicry and Chlamydia trachomatis infection of eukaryotic cells. Trends Microbiol 1994; 2: 99-101.
58. Baird A, Klagsbrun M. The fibroblast growth factor family. Ann NY Acad Sci 1991; 638.
59. Chmiela M, Czkwianianc E, Wadström T, Rudnicka W. Role of Helicobacter pylori surface structures in bacterial interaction with macrophages. Gut 1997; 40: 20-24.
60. Ernst JD. Macrophage receptors for Mycobacterium tuberculosis. Infect Immun 1998; 66: 1277-1281.
61. Love DC, Esko JD, Moser DM. A heparin-binding activity on leishmania amastigotes which mediates adhesion to cellular proteoglycans. J Cell Biol 1993; 123: 759-766.
62. Boyd AP, Sory M-P, Iriarte M, Cornelis GR. Heparin interferes with translocation of Yop proteins into HeLa cells and binds to LcrG, a regulatory component of the Yersinia Yop apparatus. Mol Microbiol 1998; 27: 425-436.
63. Coles KA, Plant AJ, Riley TV, Smith DW. Cardiovascular disease: an infectious aetiology? Rev Med Microbiol 1998; 9: 17-27.
64. Yang Y, Isberg RR. Cellular internalization in the absence of invasin expression is promoted by the Yersinia pseudotuberculosis yadA product. Infect Immun 1993; 61: 3907-3913.
65. Cornelis GR, Wolf-Watz H. The Yersinia Yop virulon: a bacterial system for subverting cukaryotic cells. Mol Microbiol 1997; 23: 861-867.
66. Limper AH, Standing JE, Hoffman OA, Castro M, Neese LW. Vitronectin binds to Pneumocystis carinii and mediates organism attachment to cultured lung epithelial cells. Infect Immun 1993; 61: 4302-4309.
67. Lundberg F, Lea T, Ljungh Å. Vitronectin-binding staphylococci enhance surface-associated complement activation. Infect Immun 1997; 65: 897-902.
68. Spear PG, Shieh MT, Herold BC, WuDunn D. Cell surface receptors required for Herpes simplex virus infection include heparan sulfate glucoseaminoglycans. In: Höök M (ed) Molecular mechanisms of microbial adhesion II. New York: Springer Verlag. 1992: 43-58.
69. Temm-Grove C, Jockusch BM, Rohde M, Niebuhr K, Chakraborty T, Wehland J. Exploitation of microfilament proteins by Listeria monocytogenes: microvillus-like composition of the comet tails and vectorial spreading in polarized epithelial sheets. J Cell Sci 1994; 107: 2951-2960.
70. Hoepelman AIM, Tuomanen EI. Consequences of microbial attachment: directing host cell functions with adhesins. Infect Immun 1992; 60: 1729-1733.
71. Pascu C, Ljungh Å, Wadstro̊m T. Staphlococci bind heparin-binding host growth factors. Curr Microbiol 1996; 32: 201-207.
72. Ascencio F, Hansson H-A, Larm O, Wadström T. Helicobacter pylori interacts with heparin and heparin-dependent growth factors. FEMS Immunol Med Microbiol 1995; 12: 272.
73. Mesri EA, Ono M, Kreitman RJ, Klagsbrun M, Pastan I. The heparin-binding domain of heparin-binding EGF-like growth factor can target Pseudomonas exotoxin to kill cells exclusively through heparin sulfate proteoglycans. J Cell Sci 1994; 107: 2599-2608.
74. Ofek I, Goldhar J, Keisari Y, Sharon N. Nonopsonic phagocytosis of microorganisms. Annu Rev Microbiol 1995; 49: 239-276.
75. Bagasra O, Whittle P, Heins B, Pomerantz RJ. Anti-human immunodeficiency virus type 1 activity of sulfated monosaccharides: comparison with sulfated polysaccharides and other polyions. J Infect Dis 1991; 164: 1082-1090.
76. Maubert B, Guilbert U, Deloron P. Cytoadherence of Plasmodium falciparum to intercellular adhesion molecule 1 and chondroitin-4-sulfate expressed by the syncytiotrophoblast in the human placenta. Infect Immun 1997; 65: 1251-1257.
77. Zugmaier G, Lippman ME, Wellstein A. Inhibition by pentosan polysulfate (PPS) of heparin-binding growth factors released from tumor cells and blockage by PPS of tumor growth in animals. J Natl Cancer Inst 1992; 84: 1716-1724.
78. Lasky LA. Selecting: interpreters of cell-specific carbohydrate information during inflammation. Science 1992; 258: 964-969.
79. Kuusela P, Ullberg M, Saksela O, Kronvall G. Tissue-type plasminogen activator-mediated activation of plasminogen on the surface of group A, C, and G streptococci. Infect Immun 1992; 60: 196-201.
80. Kuusela P, Kaukoranta-Tolvanen S-F, Ullberg M, Kronvall G, Saksela O. Surface associated activation of plasminogen on staphylococci and streptococci, and novel mechanisms for bacteriemia to use the activator system of the host. In: Wadström T, Holder IA, Kronvall G (eds) Molecular pathogenesis of surgical infections. Stuttgart, Gustav Fischer Verlag. 1994: 97-102.
81. Parkkinen J, Korhonen TK. Binding of plasminogen to Escherichia coli adhesion proteins FEBS Lett 1989; 250: 437-440.
82. Hu LT, Pratt SD, Perides G, Katz L, Rogers RA, Klempner MS. Isolation, cloning, and expression of a 70-kilodalton plasminogen binding protein of Borrelia burgdorferi. Infect Immun 1997; 65: 4989-4995.
83. Ringnér M, Valkonen KH, Wadström T. Binding of vitronectin and plasminogen to Helicobacter pylori. FEMS Microbiol Immunol 1994; 9: 29-34.
84. Andriessen MP, van den Born J, Latijnhouwers MA, Bergers M, van de Kerkhof PC, Schalkwijk J. Basal membrane heparan sulphate proteoglycan expression during wound healing in human skin. J Pathol 1997; 183: 264-271.
85. Gaffney PR, Doyle CT, Gaffney A, Hogan J, Hayes DP, Annis P. Paradoxical response to heparin in 10 patients with ulcerative colitis. Am J Gastroenterol 1995; 90: 220-223.
86. Kontani M, Kimura S, Nakagawa I, Hamada S. Adherence of Porphyromonas gingivalis to matrix proteins via a fimbrial cryptic receptor exposed by its own arginine-specific protease. Mol Microbiol 1997; 24; 1179-1187.
87. Oksala O, Haapasalmi K, Hakkinen L, Uitto VJ, Larjava H. Expression of heparan sulphate and small dermatan/chondroitin sulphate proteoglycans in chronically inflamed human periodontium. J Dent Res 1997; 76: 1250-1259.
88. Moxon ER. Applications of molecular microbiology to vaccinology. Lancet 1997; 350: 1240-1244.
89. Leininger E, Bowen S, Renauld-Mongénie G et al. Immuno-dominant domains present on the Bordetella pertussis vaccine component filamentous hemagglutinin. J Infect Dis 1997; 175: 1423-1431.
90. Greinacher A, Zinn S, Wizemann, Birk UW. Heparin-induced antibodies as a risk factor for thromboembolism and haemorrhage in patients undergoing chronic haemodialysis. Lancet 1996; 348: 764.