Hyaluronic acid capsule modulates M protein-mediated adherence and acts as a ligand for attachment of group A streptococcus to CD44 on human keratinocytes

Journal of Clinical Investigation

Volumn 101, Issue 8, 1998, Pages 1708-1716

  Schrager, Harry M ^a   Albertí, Sebastián ^a,e   Cywes, Colette ^a   Dougherty, Graeme J ^c   Wessels, Michael R ^a,b,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

^d CHANNING LABORATORY   (United States)

^e UNIVERSITAT DE LES ILLES BALEARS   (Spain)

Author keywords

Adherence; CD44; Group A Streptococcus; Hyaluronic acid; Keratinocyte

Indexed keywords

HERMES ANTIGEN; HYALURONIC ACID; M PROTEIN;

ARTICLE; BACTERIAL MEMBRANE; BACTERIUM ADHERENCE; CELL STRAIN K 562; CONTROLLED STUDY; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; STREPTOCOCCUS GROUP A;

STREPTOCOCCUS;

EID: 0032523209     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI2121     Document Type: Article

References (41)

1. Hasty, D.L., I. Ofek, H.S. Courtney, and R.J. Doyle. 1992. Multiple adhesins of streptococci. Infect. Immun. 60:2147-2152.
2. Hanski, E., and M. Caparon. 1992. Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus, Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA. 89:6172-6176.
3. Okada, N., A.P. Pentland, P. Falk, and M.G. Caparon. 1994. M protein and protein F act as important determinants of cell-specific tropism of Streptococcus pyogenes in skin tissue. J. Clin. Invest. 94:965-977.
4. Talay, S.R., P. Valentin-Weigand, P.O. Jerlstrom, K.N. Timmis, and G.S. Chhatwal. 1992. Fibronectin-binding protein of Streptococcus pyogenes: sequence of the binding domain involved in adherence of streptococci to epithelial cells. Infect. Immun. 60:3837-3844.
5. Courtney, H.S., Y. Li, J.B. Dale, and D.L. Hasty. 1994. Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci. Infect. Immun. 62:3937-3946.
6. Natanson, S., S. Sela, A. Moses, J.M. Musser, M.G. Caparon, and E. Hanski. 1995. Distribution of fibronectin-binding proteins among group A streptococci of different M types. J. Infect. Dis. 171:871-878.
7. Okada, N., M.K. Liszewski, J.P. Atkinson, and M. Caparon. 1995. Membrane cofactor protein (CD46) is a keratinocyte receptor for the M protein of group A streptococcus. Proc. Natl. Acad. Sci. USA. 92:2489-2493.
8. Caparon, M.G., D.S. Stephens, A. Olsen, and J.R. Scott. 1991. Role of M protein in adherence of group A streptococci. Infect. Immun. 59:1811-1817.
9. Courtney, H.S., M.S. Bronze, J.B. Dale, and D.L. Hasty. 1994. Analysis of the role of M24 protein in group A streptococcal adhesion and colonization by use of Ω-interposon mutagenesis. Infect. Immun. 62:4868-4873.
10. Wessels, M.R., A.E. Moses, J.B. Goldberg, and T.J. DiCesare. 1991. Hyaluronic acid capsule is a virulence factor for mucoid group A streptococci. Proc. Natl. Acad. Sci. USA. 88:8317-8321.
11. Dale, J.B., R.G. Washburn, M.B. Marques, and M.R. Wessels. 1996. Hyaluronate capsule and surface M protein in resistance to opsonization of group A streptococci. Infect. Immun. 64:1495-1501.
12. Wessels, M.R., and M.S. Bronze. 1994. Critical role of the group A streptococcal capsule in pharyngeal colonization and infection in mice. Proc. Natl. Acad. Sci. USA. 91:12238-12242.
13. Schrager, H.M., J.G. Rheinwald, and M.R. Wessels. 1996. Hyaluronic acid capsule and the role of streptococcal entry into keratinocytes in invasive skin infection. J. Clin. Invest. 98:1954-1958.
14. Husman, L.K., D.-L. Yung, S.K. Hollingshead, and J.R. Scott. 1997. Role of putative virulence factors of Streptococcus pyocenes in mouse models of long-term throat colonization and pneumonia. Infect. Immun. 65:1422-1430.
15. Bartelt, M.A., and J.L. Duncan. 1978. Adherence of group A streptococci to human epithelial cells. Infect. Immun. 20:200-208.
16. Wessels, M.R., J.B. Goldberg, A.E. Moses, and T.J. DiCesare. 1994. Effects on virulence of mutations in a locus essential for hyaluronic acid capsule expression in group A streptococci. Infect. Immun. 62:433-441.
17. 16a. Wang, R.F., and S.R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene. 100:195-199.
18. Perez-Casal, J., J.A. Price, E. Maguin, and J.R. Scott. 1993. An M protein with a single C repeat prevents phagocytosis of Streptococcus pvogenes: use of a temperature-sensitive shuttle vector to deliver homologous sequences to the chromosome of S. pyogenes. Mol. Microbiol. 8:809-819.
19. Perez-Casal, J., M.G. Caparon, and J.R. Scott. 1991. Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two component regulatory systems. J. Bactcriol. 173:2617-2624.
20. Caparon, M.G., and J.R. Scott. 1991. Genetic manipulation of pathogenic streptococci. Methods Enzymol. 204:556-586.
21. Droll, A., S.T. Dougherty, R.K. Chiu, J.F. Dirks, W.H. McBride, D.L. Cooper, and G.J. Dougherty. 1995. Adhesive interactions between alternatively spliced CD44 isoforms. J. Biol. Chem. 270:11567-11573.
22. Haynes, B.F., H.-X. Liao, and K.L. Patton. 1991. The transmembrane hyaluronate receptor (CD44): multiple functions, multiple forms. Cancer Cells. 3:347-350.
23. Isacke, C.M., C.A. Sauvage, R. Hyman, J. Lesley, R. Schulte, and I.S. Trowbridge. 1986. Identification and characterization of the human Pgp-1 glycoprotein. Immunogenetics. 23:326-332.
24. Zheng, Z., S. Katoh, Q. He, K. Oritani, K. Miyake, J. Lesley, R. Hyman, A. Hamik, R.M.E. Parkhouse, A.G. Farr, and P.W. Kincade. 1995. Monoclonal antibodies to CD44 and their influence on hyaluronan recognition. J. Cell Biol. 130:485-495.
25. St. Jacques, S., H.K. Dadi, and M. Letarte. 1993. CD44 in human placenta: localization and binding to hyaluronic acid. Placenta. 14:25-39.
26. Rheinwald, J.G., and M.A. Beckett. 1981. Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultured from human squamous cell carcinomas. Cancer Res. 41:1657-1663.
27. 25a. Dougherty, G.J., P.M. Lansdorp. D.L. Cooper, and R.K. Humphries. 1991. Molecular cloning of CD44R1 and CD44R2, two novel isoforms of the human CD44 lymphocyte "homing" receptor expresed by hematopoietic cells. J. Exp. Med. 174:1-5.
28. Crater, D.L., and I. van de Rijn. 1995. Hyaluronic acid synthesis operon (has) expression in group A streptococci. J. Biol. Chem. 270:18452-18458.
29. Courtney, H.S., C. von Hunolstein, J.B. Dale, M.S. Bronze, E.H. Beachey, and D.L. Hasty. 1992. Lipoteichoic acid and M protein: dual adhesins of group A streptococci. Microb. Pathog. 12:199-208.
30. Tylewska, S.K., V.A Fischetti, and R.J. Gibbons. 1988. Binding selectivity of Streptococcus pyogenes and M-protein to epithelial cells differs from that of lipoteichoic acid. Curr. Microbiol. 16:209-216.
31. Pancholi, V., and V. Fischelti. 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 176:415-426.
32. Courtncy, H.S., I. Ofek, and D.L. Hasty. 1997. M protein mediated adhesion of M type 24 Streptococcus pyogenes stimulates release of interleukin-6 by HEp-2 tissue culture cells. FEMS Microbiol Lett. 151:65-70.
33. Brown, T.A., T. Bouchard, T. St. John, E. Wayner, and W.G. Carter. 1991. Human keratinocytes express a new CD44 core protein (CD44E) as a heparan-sulfate intrinsic membrane proteoglycan with additional exons. J. Cell Biol. 113:207-220.
34. Haggerty, J.G., R.H. Bretton, and L.M. Milstone. 1992. Identification and characterization of a cell surface proteoglycan on keratinocytes. J. Investig. Dermatol. 99:374-380.
35. Hale, L.P., D.D. Patel, R.E. Clark, and B.F. Haynes. 1995. Distribution of CD44 variant isoforms in human skin: differential expression in components of benign and malignant epithelia. J. Cutaneous Pathol. 22:536-545.
36. Yasaka, N., M. Furue, and K. Taniaki. 1995. CD44 expression in normal human skin and skin tumors. J. Dermatol. (Tokyo). 22:88-94.
37. Penneys, N.S. 1993. CD44 expression in normal and inflamed skin. J. Cutaneous Pathol. 20:250-253.
38. Oksala, O., T. Salo, R. Tammi, L. Hakkinen, M. Jalkanen, P. Inki, and H. Larjava. 1995. Expression of proteoglycans and hyaluronan during wound healing. J. Histochem. Cytochem. 43:125-135.
39. + by transfer of a plasmid con-taining an M6 gene. J. Exp. Med. 164:1641-1651.
40. Caparon, M.G., R.T. Geist, J. Perez-Casal, and J.R. Scott. 1992. Environmental regulation of virulence in group A streptococci: transcription of the gene encoding M protein is stimulated by carbon dioxide. J. Bacteriol. 174: 5693-5701.
41. Moses, A.E., M.R. Wessels, K. Zalcman, S. Alberti, S. Natanson-Yaron, T. Menes, and E. Hanski. 1997. Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of group A Streptococcus. Infect. Immun. 65:64-71.