The OsmC-like protein MG1142 resides on the cell surface and binds heparin Free

Abstract

is an avian pathogen that causes a chronic respiratory disease of chickens and results in significant economic losses to the poultry industry worldwide. Colonization of the host and the establishment of chronic disease are initiated by the cytadherence of to the host respiratory epithelium. While several proteins involved in cytadhesion have been characterized, molecules that interact with components of the host extracellular matrix, a process that is central to pathogenesis, are only now being identified. In this study, whole cells were shown to bind heparin in a specific and saturable manner. Heparin also significantly inhibited the binding of to the human lung fibroblast cell line MRC-5, suggesting a potential role for glycosaminoglycans (GAGs) in cytadherence. protein MG1142 (encoded by ), which displays homology to the osmotically induced (OsmC) family of proteins, binds strongly to heparin, is highly expressed during culture, and is surface accessible. Recombinant MG1142 bound heparin in a dose-dependent and saturable manner with a dissociation constant ( ) of 10±1.8 nM, which is within a physiologically significant range, compared to that of other heparin-binding proteins. Binding to heparin was inhibited by the heavily sulfated polysaccharide fucoidan, but not by mucin or chondroitin sulfate A or B, suggesting that electrostatic interactions between the sulfate groups of heparin and the positively charged basic residues of the MG1142 protein are important in binding. The ability of to bind GAGs may contribute to host adherence and colonization.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/004937-0
2007-05-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/5/1455.html?itemId=/content/journal/micro/10.1099/mic.0.2006/004937-0&mimeType=html&fmt=ahah

References

  1. Alvarez R. A., Blaylock M. W., Baseman J. B. 2003; Surface localized glyceraldehyde-3-phosphate dehydrogenase of Mycoplasma genitalium binds mucin. Mol Microbiol 48:1417–1425 [CrossRef]
    [Google Scholar]
  2. Burnett T. A., Dinkla K., Rohde M., Chhatwal G. S., Uphoff C., Srivastava M., Cordwell S. J., Geary S., Liao X. other authors 2006; P159 is a proteolytically processed, surface adhesin of Mycoplasma hyopneumoniae : defined domains of P159 bind heparin and promote adherence to eukaryote cells. Mol Microbiol 60:669–686 [CrossRef]
    [Google Scholar]
  3. Cardin A. D., Weintraub H. J. 1989; Molecular modeling of protein–glycosaminoglycan interactions. Arteriosclerosis 9:21–32 [CrossRef]
    [Google Scholar]
  4. Chen T., Swanson J., Wilson J., Belland R. J. 1995; Heparin protects Opa+ Neisseria gonorrhoeae from the bactericidal action of normal human serum. Infect Immun 63:1790–1795
    [Google Scholar]
  5. Chin R. P., Daft B. M., Meteyer C. U., Yamamoto R. 1991; Meningoencephalitis in commercial meat turkeys associated with Mycoplasma gallisepticum. Avian Dis 35:986–993 [CrossRef]
    [Google Scholar]
  6. Cussiol J. R., Alves S. V., Netto L. E., de Oliveira M. A. 2003; Organic hydroperoxide resistance gene encodes a thiol-dependent peroxidase. J Biol Chem 278:11570–11578 [CrossRef]
    [Google Scholar]
  7. Dallo S. F., Kannan T. R., Blaylock M. W., Baseman J. B. 2002; Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol Microbiol 46:1041–1051 [CrossRef]
    [Google Scholar]
  8. Davalos-Garcia M., Conter A., Toesca I., Gutierrez C., Cam K. 2001; Regulation of osm C gene expression by the two-component system rcs B– rcs C in Escherichia coli. J Bacteriol 183:5870–5876 [CrossRef]
    [Google Scholar]
  9. Djordjevic S. P., Cordwell S. J., Djordjevic M. A., Wilton J., Minion F. C. 2004; Proteolytic processing of the Mycoplasma hyopneumoniae cilium adhesin. Infect Immun 72:2791–2802 [CrossRef]
    [Google Scholar]
  10. Domermuth C. H., Gross W. B., DuBose R. T. 1967; Mycoplasmal salpingitis of chickens and turkeys. Avian Dis 11:393–398 [CrossRef]
    [Google Scholar]
  11. Dubreuil J. D., Giudice G. D., Rappuoli R. 2002; Helicobacter pylori interactions with host serum and extracellular matrix proteins: potential role in the infectious process. Microbiol Mol Biol Rev 66:617–629 [CrossRef]
    [Google Scholar]
  12. Duensing T. D., Putten J. P. 1998; Vitronectin binds to the gonococcal adhesin OpaA through a glycosaminoglycan molecular bridge. Biochem J 334:133–139
    [Google Scholar]
  13. Duensing T. D., van Putten J. P. 1997; Vitronectin mediates internalization of Neisseria gonorrhoeae by Chinese hamster ovary cells. Infect Immun 65:964–970
    [Google Scholar]
  14. Duensing T. D., Wing J. S., van Putten J. P. 1999; Sulfated polysaccharide-directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenesis. Infect Immun 67:4463–4468
    [Google Scholar]
  15. Gautier-Bouchardon A. V., Reinhardt A. K., Kobisch M., Kempf I. 2002; In vitro development of resistance to enrofloxacin, erythromycin, tylosin, tiamulin and oxytetracycline in Mycoplasma gallisepticum, Mycoplasma iowae and Mycoplasma synoviae. Vet Microbiol 88:47–58 [CrossRef]
    [Google Scholar]
  16. Geary S. J., Gabridge M. G., Intres R., Draper D. L., Gladd M. F. 1989; Identification of Mycoplasma binding proteins utilizing a 100 kilodalton lung fibroblast receptor. J Recept Res 9:465–478
    [Google Scholar]
  17. Giron J. A., Lange M., Baseman J. B. 1996; Adherence, fibronectin binding, and induction of cytoskeleton reorganization in cultured human cells by Mycoplasma penetrans. Infect Immun 64:197–208
    [Google Scholar]
  18. Goh M. S., Gorton T. S., Forsyth M. H., Troy K. E., Geary S. J. 1998; Molecular and biochemical analysis of a 105 kDa Mycoplasma gallisepticum cytadhesin (GapA). Microbiology 144:2971–2978 [CrossRef]
    [Google Scholar]
  19. Hileman R. E., Fromm J. R., Weiler J. M., Linhardt R. J. 1998; Glycosaminoglycan–protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 20:156–167 [CrossRef]
    [Google Scholar]
  20. Hytonen J., Haataja S., Gerlach D., Podbielski A., Finne J. 2001; The SpeB virulence factor of Streptococcus pyogenes , a multifunctional secreted and cell surface molecule with strepadhesin, laminin-binding and cysteine protease activity. Mol Microbiol 39:512–519 [CrossRef]
    [Google Scholar]
  21. Jenkins C., Wilton J. L., Minion F. C., Falconer L., Walker M. J., Djordjevic S. P. 2006; Two domains within the Mycoplasma hyopneumoniae cilium adhesin bind heparin. Infect Immun 74:481–487 [CrossRef]
    [Google Scholar]
  22. Joh D., Wann E. R., Kreikemeyer B., Speziale P., Hook M. 1999; Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol 18:211–223 [CrossRef]
    [Google Scholar]
  23. Jordan F. T. W. 1979; Avian mycoplasmas. In The Mycoplasmas pp 9–16 Edited by Tully J. G., Whitcomb R. F. New York: Academic Press;
    [Google Scholar]
  24. Kannan T. R., Provenzano D., Wright J. R., Baseman J. B. 2005; Identification and characterization of human surfactant protein A binding protein of Mycoplasma pneumoniae. Infect Immun 73:2828–2834 [CrossRef]
    [Google Scholar]
  25. Lamas da Silva J. M., Adler H. E. 1969; Pathogenesis of arthritis induced in chickens by Mycoplasma gallisepticum. Pathol Vet 6:385–395
    [Google Scholar]
  26. Lesniak J., Barton W. A., Nikolov D. B. 2003; Structural and functional features of the Escherichia coli hydroperoxide resistance protein OsmC. Protein Sci 12:2838–2843 [CrossRef]
    [Google Scholar]
  27. Levisohn S., Kleven S. H. 2000; Avian mycoplasmosis ( Mycoplasma gallisepticum ). Rev Sci Tech 19:425–442
    [Google Scholar]
  28. Ley D. H., Yoder H. W. Jr 1997; Mycoplasma gallisepticum infection. In Diseases of Poultry Edited by Calnek B. W., Barnes H. J., Beard C., McDougald L. R., Saif Y. M. Ames, IA: Iowa State University Press;
    [Google Scholar]
  29. Margalit H., Fischer N., Ben-Sasson S. A. 1993; Comparative analysis of structurally defined heparin binding sequences reveals a distinct spatial distribution of basic residues. J Biol Chem 268:19228–19231
    [Google Scholar]
  30. May M., Papazisi L., Gorton T. S., Geary S. J. 2006; Identification of fibronectin-binding proteins in Mycoplasma gallisepticum strain R. Infect Immun 74:1777–1785 [CrossRef]
    [Google Scholar]
  31. Menozzi F. D., Rouse J. H., Alavi M., Laude-Sharp M., Muller J., Bischoff R., Brennan M. J., Locht C. 1996; Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med 184:993–1001 [CrossRef]
    [Google Scholar]
  32. Menozzi F. D., Pethe K., Bifani P., Soncin F., Brennan M. J., Locht C. 2002; Enhanced bacterial virulence through exploitation of host glycosaminoglycans. Mol Microbiol 43:1379–1386 [CrossRef]
    [Google Scholar]
  33. Mitchell J., Tristan A., Foster T. J. 2004; Characterization of the fibrinogen-binding surface protein Fbl of Staphylococcus lugdunensis. Microbiology 150:3831–3841 [CrossRef]
    [Google Scholar]
  34. Much P., Winner F., Stipkovits L., Rosengarten R., Citti C. 2002; Mycoplasma gallisepticum : influence of cell invasiveness on the outcome of experimental infection in chickens. FEMS Immunol Med Microbiol 34:181–186 [CrossRef]
    [Google Scholar]
  35. Nunoya T., Kanai K., Yagihashi T., Hoshi S., Shibuya K., Tajima M. 1997; Natural case of salpingitis apparently caused by Mycoplasma gallisepticum in chickens. Avian Pathol 26:391–398 [CrossRef]
    [Google Scholar]
  36. Pankhurst G. J., Bennett C. A., Easterbrook-Smith S. B. 1998; Characterization of the heparin-binding properties of human clusterin. Biochemistry 37:4823–4830 [CrossRef]
    [Google Scholar]
  37. Papazisi L., Troy K. E., Gorton T. S., Liao X., Geary S. J. 2000; Analysis of cytadherence-deficient, GapA-negative Mycoplasma gallisepticum strain R. Infect Immun 68:6643–6649 [CrossRef]
    [Google Scholar]
  38. Papazisi L., Gladd M., Liao X., Yogev D., Geary S. J., Frasca S. Jr 2002; GapA and CrmA coexpression is essential for Mycoplasma gallisepticum cytadherence and virulence. Infect Immun 70:6839–6845 [CrossRef]
    [Google Scholar]
  39. Papazisi L., Gorton T. S., Kutish G., Markham P. F., Browning G. F., Nguyen D. K., Swartzell S., Madan A., Mahairas G., Geary S. J. 2003; The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain R(low). Microbiology 149:2307–2316 [CrossRef]
    [Google Scholar]
  40. Patankar M. S., Oehninger S., Barnett T., Williams R. L., Clark G. F. 1993; A revised structure for fucoidan may explain some of its biological activities. J Biol Chem 268:21770–21776
    [Google Scholar]
  41. Patti J. M., Hook M. 1994; Microbial adhesins recognizing extracellular matrix macromolecules. Curr Opin Cell Biol 6:752–758 [CrossRef]
    [Google Scholar]
  42. Pethe K., Aumercier M., Fort E., Gatot C., Locht C., Menozzi F. D. 2000; Characterization of the heparin-binding site of the mycobacterial heparin-binding hemagglutinin adhesin. J Biol Chem 275:14273–14280 [CrossRef]
    [Google Scholar]
  43. Pethe K., Alonso S., Biet F., Delogu G., Brennan M. J., Locht C., Menozzi F. D. 2001; The heparin-binding haemagglutinin of Mycobacterium tuberculosis is required for extrapulmonary dissemination. Nature 412:190–194 [CrossRef]
    [Google Scholar]
  44. Rehse P. H., Ohshima N., Nodake Y., Tahirov T. H. 2004; Crystallographic structure and biochemical analysis of the Thermus thermophilus osmotically inducible protein C. J Mol Biol 338:959–968 [CrossRef]
    [Google Scholar]
  45. Sturny R., Cam K., Gutierrez C., Conter A. 2003; NhaR and RcsB independently regulate the osm Cp1 promoter of Escherichia coli at overlapping regulatory sites. J Bacteriol 185:4298–4304 [CrossRef]
    [Google Scholar]
  46. Thorns C. J., Boughton E. 1980; Effect of serial passages through liquid medium on the virulence of Mycoplasma bovis for the mouse mammary gland. Res Vet Sci 29:328–332
    [Google Scholar]
  47. Toesca I., Perard C., Bouvier J., Gutierrez C., Conter A. 2001; The transcriptional activator NhaR is responsible for the osmotic induction of osm C(p1), a promoter of the stress-inducible gene osm C in Escherichia coli. Microbiology 147:2795–2803
    [Google Scholar]
  48. Winner F., Rosengarten R., Citti C. 2000; In vitro cell invasion of Mycoplasma gallisepticum. Infect Immun 68:4238–4244 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/004937-0
Loading
/content/journal/micro/10.1099/mic.0.2006/004937-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed