Streptococcus pyogenes expressing M and M-like surface proteins are phagocytosed but survive inside human neutrophils

Cellular Microbiology

Volumn 5, Issue 4, 2003, Pages 253-265

  Staali, Leïla ^a,b   Mörgelin, Matthias ^a   Björck, Lars ^a   Tapper, Hans ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

M PROTEIN; MEMBRANE PROTEIN;

ACTIN POLYMERIZATION; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BIOASSAY; BLOOD SAMPLING; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HOST CELL; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; INTERNALIZATION; INTRACELLULAR KILLING; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PYOGENES; WILD TYPE;

ACTINS; ANTIGENS, BACTERIAL; ANTIGENS, SURFACE; BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER PROTEINS; CYTOSKELETON; FLOW CYTOMETRY; HUMANS; MICROSCOPY, FLUORESCENCE; NEUTROPHILS; OPSONIN PROTEINS; PHAGOCYTOSIS; STREPTOCOCCUS PYOGENES;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SP. 'GROUP A';

EID: 0037397627     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2003.00272.x     Document Type: Review

References (49)

1. Åkesson, P., Cooney, J., Kishimito, F., and Björck, L. (1990) Protein H - a novel lgG binding bacterial protein. Mol Immunol 27: 523-531.
2. Åkesson, P., Sjöholm, A.G., and Björck, L. (1996) Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J Biol Chem 271: 1081-1088.
3. Alouf, J. E. (1980) Streptococcal toxins (streptolysin O, streptolysin S, erythrogenic toxin). Pharmacol Ther 11: 661-717.
4. Beachey, E.H., and Cunningham, M. (1973) Type-specific inhibition of preopsonization versus immunoprecipitation by streptococcal M proteins. Infect Immun 8: 19-24.
5. Berge, A., Kihlberg, B.-M., Sjöholm, A.G., and Björck, L. (1997) Streptococcal protein H forms soluble complement-activating complexes with lgG, but inhibits complement activation by lgG-coated targets. J Biol Chem 272: 20774-20781.
6. Bisno, A.L. (1991) Group A streptococcal infections and acute rheumatic fever. N Engl J Med 325: 783-793.
7. Bisno, A.L., and Stevens, D.L. (1996) Streptococcal infections of skin and soft tissues. N Engl J Med 334: 240-245.
8. de Chastellier, C., and Thilo, L. (1999) Mycobacteria and the endocytic pathway. In Microbial Invasion. Advances in Cell and Molecular Biology of Membranes and Organelles, Vol. 6. Gordon, S. (ed). Stanford, CT: JAI Press, pp. 107-135.
9. Collin, M., and Olsén, A. (2000) Generation of a mature streptococcal cysteine proteinase is dependent on cell wall-anchored M1 protein. Mol Microbiol 36: 1306-1318.
10. Collin, M., and Olsén, A. (2001) EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human lgG. EMBO J 20: 3046-3055.
11. Courtney, H.S., von Hunolstein, C., Dale, J.B., Bronze, S., Beachey, E.H., and Hasty, D.L. (1992) Lipoteichoic acid and M protein: dual adhesins of group A streptococci. Microbial Pathogenesis 12: 199-208.
12. Cunningham, M.W. (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13: 470-511.
13. Dale, J.B., Washburn, R.G., Marques, M.B., and Wessels, M.R. (1996) Hyaluronate capsule and surface M protein in resistance to opsonization of group A streptococci. Infect Immun 64: 1495-1501.
14. Dale, J.B., Chiang, E.Y., Liu, S., Courtney, H.S., and Hasty, D.L. (1999) New protective antigen of group A streptococci. J Clin Invest 103: 1261-1268.
15. Ernst, J.D. (2000) Bacterial inhibition of phagocytosis. Cell Microbiol 2: 379-386.
16. Finlay, B.B., and Cossart, P. (1997) Exploitation of mammalian host cell functions by bacterial pathogens. Science 276: 718-725.
17. Fischetti, V.A. (1989) Streptococcal M protein: Molecular design and biological behavior. Clin Microbiol Rev 2: 285-314.
18. Fluckiger, U., Jones, K.F., and Fischetti, V.A. (1998) Immunoglobulins to group A streptococcal surface molecules decrease adherence to and invasion of human pharyngeal cells. Infect Immun 66: 974-979.
19. Frick, I.-M., Mörgelin, M., and Björck, L. (2000) Virulent aggregates of Streptococcus pyogenes are generated by homophilic protein-protein interactions. Mol Microbiol 37: 1232-1247.
20. Goldberg, M.B. (2001) Actin-based motility of intracellular microbial pathogens. Microbiol Mol Biol Rev 65: 595-626.
21. Hampton, M.B., Kettle, A.J., and Winterbourn, C.C. (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase and bacterial killing. Blood 92: 3007-3017.
22. Heath, D.G., and Cleary, P.P. (1989) Fc-receptors and M-protein genes of group A streptococci are products of gene duplication. Proc Natl Acad Sci USA 86: 4741-4745.
23. Horstmann, R.D., Sievertsen, H.J., Knobloch, J., and Fischetti, V.A. (1988) Antiphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H. Proc Natl Acad Sci USA 85: 1657-1661.
24. Johnsson, E., Thern, A., Dahlbäck, B., Heden, L.O., Wikström, M., and Lindahl, G. (1996) A highly variable region in members of the streptococcal M protein family binds the human complement regulator C4 BP. J Immunol 157: 3021-3029.
25. Kantor, F.S. (1965) Fibrinogen precipitating by streptococcal M protein. I. Identity of the reactants and stoichiometry of the reaction. J Exp Med 121: 849-859.
26. Kihlberg, B.-M., Cooney, J., Caparon, M.G., Olsén, A., and Björck, L. (1995) Biological properties of a Streptococcus pyogenes mutant generated by Tn916 insertion in mga. Microb Pathog 19: 299-315.
27. Kihlberg, B.-M., Collin, M., Olsén, A., and Björck, L. (1999) Protein H, an antiphagocytic surface protein in Streptococcus pyogenes. Infect Immun 67: 1708-1714.
28. Koroleva, I.V., Sjöholm, A.G., and Schalen, C. (1998) Binding of complement subcomponent C1q to Streptococcus pyogenes: evidence for interactions with the M5 and FcRA76 proteins. FEMS Immunol Med Microbiol 20: 11-20.
29. Krause, K.H. (2000) Professional phagocytes: predators and prey of microorganisms. Schweiz Med Wochenschr 130: 97-100.
30. Lancefield, R.C. (1962) Current knowledge of type-specific M antigens of group A streptococci. J Immunol 89: 307-313.
31. LaPenta, D., Rubens, C., Chi, E., and Cleary, P.P. (1994) Group A streptococci efficiently invade human respiratory epithelial cells. Proc Natl Acad Sci USA 91: 12115-12119.
32. Liu, S., Courtney, S., Bessen, D.E., Hasty, D.L., and Dale, J.B. (1997) M protein expression is not required for resistance to phagocytosis of type 18 group A streptococci. Adv Exp Med Biol 418: 725-727.
33. Manjula, B.B. (1988) Molecular aspects of the phagocytosis resistance of group A streptococci. Eur J Epidemiol 4: 289-300.
34. Meresse, S., Steele-Mortimer, O., Moreno, E., Desjardins, M., Finlay, B.B., and Gorvel, J.-P. (1999) Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nature 1: 183-188.
35. Molinari, G., Rohde, M., Guzmán, C.A., and Chhatwal, G.S. (2000) Two distinct pathways for the invasion of Streptococcus pyogenes in non-phagocytic cells. Cell Microbiol 2: 145-154.
36. Moses, A.E., Wessels, M.R., Zaleman, K., Natanson-Yaron, S., Menes, T., and Hanski, E. (1997) Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of the group A streptococcus. Infect Immun 65: 64-71.
37. Musser, J.M., Hauser, A.R., Kim, M.H., Schlievert, P.M., Nelson, K., and Selander, R.K. (1991) Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases; clonal diversity and pyrogenic exotoxin expression. Proc Natl Acad Sci USA 88: 2668-2672.
38. Navarre, W.W., and Schneewind, O. (1999) Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
39. Podbielski, A., Schnitzler, N., Beyhs, P., and Boyle, M.D.P. (1996) M-related protein (Mrp) contributes to group A streptococcal resistance to phagocytosis by human granulocytes. Mol Microbiol 19: 429-441.
40. Portnoy, D.A., Auerbuch, V., and Glomski, I.J. (2002) The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 158: 409-414.
41. Roy, C.R., and Tilney, L.G. (2002) The road less traveled: transport of Legionella to the endoplasmic reticulum. J Cell Biol 158: 415-419.
42. Schnitzler, N., Haase, G., Büssing, A., Kaufhold, A., Beyhs, P., and Podbielski, A. (1995) Measuring resistance to phagocytosis of group A and G streptococci: comparison of direct bactericidal assay and flow cytometry. Med Microbiol Immunol 184: 17-22.
43. Stevens, D.L. (1992) Invasive group A streptococcus infections. Clin Infect Dis 14: 2-13.
44. Stevens, D.L., Tanner, M.H., Winship, J., Swarts, R., Ries, K. M., Schlievert, P.M., and Kaplan, E. (1989) Severe group A streptococcal infections associated with a toxic shock-like syndrome and scarlet fever toxin. N Engl J Med 321: 1-7.
45. Tang, P., Foubister, V., Pucciarelli, M.G., and Finlay, B.B. (1993) Methods to study bacterial invasion. J Microbiol Meth 18: 227-240.
46. Villaseñor-Sierra, A., McShan, W.M., Salmi, D., Kaplan, E.L., Johnson, D.R., and Stevens, D.L. (1999) Variable susceptibility to opsonophagocytosis of group A streptococcus M1 strains by human immune sera. J Infect Dis 180: 1921-1928.
47. Wessels, M.R., Moses, A.E., Golberg, J.B., and DiCesare, T.J. (1991) Hyaluronic acid capsule is a virulence factor for mucoid group A streptococci. Proc Natl Acad Sci USA 88: 8317-8321.
48. Whitnack, E., Dale, J.B., and Beachey, E. H. (1984) Common protective antigens of group A streptococcal M proteins masked by fibrinogen. J Exp Med 159: 1201-1212.
49. Yan, S.R., and Berton, G. (1998) Antibody-induced engagement of beta2 integrins in human neutrophils causes a rapid redistribution of cytoskeletal proteins Src-family tyrosine kinases, and p72syk that precedes de novo actin polymerization. J Leukocyte Biol 64: 401-408.