Molecular mechanisms underlying group A streptococcal pathogenesis

Cellular Microbiology

Volumn 11, Issue 1, 2009, Pages 1-12

  Olsen, Randall J ^a   Shelburne, Samuel A ^b   Musser, James M ^a  

^a HOUSTON METHODIST HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ANTIGEN ANTIBODY REACTION; BACTEREMIA; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM COLONY; BACTERIUM ISOLATE; BIOFILM; CELL ACTIVITY; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; CELL PROTECTION; CELL SURFACE; COMORBIDITY; CRYSTAL STRUCTURE; CYTOLYSIS; DISEASE ACTIVITY; DISEASE COURSE; DISEASE PREDISPOSITION; DISEASE SEVERITY; DOWN REGULATION; DRUG RESEARCH; ENZYME ACTIVITY; EPITHELIUM CELL; EUKARYOTE; GENE INTERACTION; GENETIC VARIABILITY; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; INFECTION PREVENTION; INFECTION RISK; INTERNALIZATION; MICROBIAL ACTIVITY; MORBIDITY; MORTALITY; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PHAGOCYTOSIS; PHARYNGITIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; RISK ASSESSMENT; SEQUENCE HOMOLOGY; SHORT SURVEY; STREPTOCOCCUS GROUP A; STREPTOCOCCUS INFECTION; TISSUE INJURY;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; MODELS, ANIMAL; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES;

ANIMALIA; EUKARYOTA; MUS MUSCULUS; STREPTOCOCCUS SP. 'GROUP A';

EID: 58149313653     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01225.x     Document Type: Short Survey

References (80)

1. Akesson, P., Rasmussen, M., Mascini, E., von Pawel-Rammingen, U., Janulczyk, R., Collin, M., et al. (2004) Low antibody levels against cell wall-attached proteins of Streptococcus pyogenes predispose for severe invasive disease. J Infect Dis 189:797-804.
2. Amerongen, A.V., and Veerman, E.C. (2002) Saliva - the defender of the oral cavity. Oral Dis 8: 12-22.
3. Ashbaugh, C.D., Moser, T.J., Shearer, M.H., White, G.L., Kennedy, R.C., and Wessels, M.R. (2000) Bacterial determinants of persistent throat colonization and the associated immune response in a primate model of human group A streptococcal pharyngeal infection. Cell Microbiol 2: 283-292.
4. Basma, H., Norrby-Teglund, A., Guedez, Y., McGeer, A., Low, D.E., El-Ahmedy, O., etal. (1999) Risk factors in the pathogenesis of invasive group A streptococcal infections: Role of protective humoral immunity. Infect Immun 67: 1871-1877.
5. Beres, S.B., Sylva, G.L., Barbian, K.D., Lei, B., Hoff, J.S., Mammarella, N.D., etal. (2002) Genome sequence of a serotype M3 strain of group A Streptococcus: Phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci USA 99: 10078-10083.
6. Bisno, A.L., Brito, M.O., and Collins, C.M. (2003) Molecular basis of group A streptococcal virulence. Lancet Infect Dis 3: 191-200.
7. Brown, C.K., Gu, Z.Y., Matsuka, Y.V., Purushothaman, S.S., Winter, L.A., Cleary, P.P., etal. (2005) Structure of the streptococcal cell wall C5a peptidase. Proc Natl Acad Sci USA 102: 18391-18396.
8. Buchanan, J.T., Simpson, A.J., Aziz, R.K., Liu, G.Y., Kristian, S.A., Kotb, M., etal. (2006) DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 16: 396-400.
9. Carapetis, J.R. (2007) Rheumatic heart disease in developing countries. N Engl J Med 357: 439-441.
10. Carapetis, J.R., Steer, A.C., Mulholland, E.K., and Weber, M. (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5: 685-694.
11. Chaussee, M.S., Watson, R.O., Smoot, J.C., and Musser, J.M. (2001) Identification of Rgg-regulated exoproteins of Streptococcus pyogenes. Infect Immun 69: 822-831.
12. Cole, J.N., McArthur, J.D., McKay, F.C., Sanderson-Smith, M.L., Cork, A.J., Ranson, M., etal. (2006) Trigger for group A streptococcal M1T1 invasive disease. FASEB J 20: 1745-1747.
13. Cole, J.N., Aquilina, J.A., Hains, P.G., Henningham, A., Sriprakash, K.S., Caparon, M.G., etal. (2007) Role of group A Streptococcus HtrA in the maturation of SpeB protease. Proteomics 7: 4488-4498.
14. Courtney, H.S., Hasty, D.L., and Dale, J.B. (2002) Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci. Ann Med 34: 77-87.
15. Cunningham, M.W. (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13: 470-511.
16. Daneman, N., Green, K.A., Low, D.E., Simor, A.E., Willey, B., Schwartz, B., et al. (2007) Surveillance for hospital outbreaks of invasive group A streptococcal infections in Ontario, Canada, 1992-2000. Ann Intern Med 147: 234-241.
17. Darenberg, J., Luca-Harari, B., Jasir, A., Sandgren, A., Pettersson, H., Schalen, C., et al. (2007) Molecular and clinical characteristics of invasive group A streptococcal infection in Sweden. Clin Infect Dis 45: 450-458.
18. Datta, V., Myskowski, S.M., Kwinn, L.A., Chiem, D.N., Varki, N., Kansal, R.G., et al. (2005). Mutational analysis of the group A streptococcal operon encoding streptolysin S and its virulence role in invasive infection. Mol Microbiol 56: 681-695.
19. Edwards, A.M., Manetti, A.G., Falugi, F., Zingaretti, C., Capo, S., Buccato, S., et al. (2008) Scavenger receptor gp340 aggregates group A streptococci by binding pili. Mol Microbiol 68: 1378-1394.
20. Factor, S.H., Levine, O.S., Harrison, L.H., Farley, M.M., McGeer, A., Skoff, T., et al. (2005) Risk factors for pediatric invasive group A streptococcal disease. Emerg Infect Dis 11: 1062-1066.
21. Gough, H., Luke, G.A., Beeley, J.A., and Geddes, D.A. (1996) Human salivary glucose analysis by high-performance ion-exchange chromatography and pulsed amperometric detection. Arch Oral Biol 41: 141-145.
22. Graham, M.R., Smoot, L.M., Migliaccio, C.A., Virtaneva, K., Sturdevant, D.E., Porcella, S.F., et al. (2002) Virulence control in group A Streptococcus by a two-component gene regulatory system: Global expression profiling and in vivo infection modeling. Proc Natl Acad Sci USA 99: 13855-13860.
23. Hanski, E., and Caparon, M. (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.
24. Herwald, H., Cramer, H., Morgelin, M., Russell, W., Sollenberg, U., Norrby-Teglund, A., et al. (2004) M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116: 367-379.
25. Hoe, N.P., Ireland, R.M., DeLeo, F.R., Gowen, B.B., Dorward, D.W., Voyich, J.M., et al. (2002) Insight into the molecular basis of pathogen abundance: Group A Streptococcus inhibitor of complement inhibits bacterial adherence and internalization into human cells. Proc Natl Acad Sci USA 99: 7646-7651.
26. Iafrate, A.J., Feuk, L., Rivera, M.N., Listewnik, M.L., Donahoe, P.K., Qi, Y., et al. (2004) Detection of large-scale variation in the human genome. Nat Genet 36: 949-951.
27. Johansson, L., Thulin, P., Sendi, P., Hertzen, E., Linder, A., Akesson, P., et al. (2008) LL-37 in severe Streptococcus pyogenes soft tissue infections. Infect Immun 76: 3399-3404.
28. Kang, H.J., Coulibaly, F., Clow, F., Proft, T., and Baker, E.N. (2007) Stabilizing isopeptide bonds revealed in gram-positive bacterial pilus structure. Science 318: 1625-1628.
29. Kazmi, S.U., Kansal, R., Aziz, R.K., Hooshdaran, M., Norrby-Teglund, A., Low, D.E., et al. (2001) Reciprocal, temporal expression of SpeA and SpeB by invasive M1T1 group A streptococcal isolates in vivo. Infect Immun 69: 4988-4995.
30. Kotb, M., Norrby-Teglund, A., McGeer, A., El-Sherbini, H., Dorak, M.T., Khurshid, A., et al. (2002) An immunogenetic and molecular basis for differences in outcomes of invasive group A streptococcal infections. Nat Med 8: 1398-1404.
31. Kotb, M., Norrby-Teglund, A., McGeer, A., Green, K., and Low, D.E. (2003) Association of human leukocyte antigen with outcomes of infectious diseases: The streptococcal experience. Scand J Infect Dis 35: 665-669.
32. Kwinn, L.A., Khosravi, A., Aziz, R.K., Timmer, A.M., Doran, K.S., Kotb, M., and Nizet, V. (2007) Genetic characterization and virulence role of the RALP3/LSA locus upstream of the streptolysin s operon in invasive M1T1 group A Streptococcus. J Bacteriol 189: 1322-1329.
33. Lamagni, T.L., Neal, S., Keshishian, C., Alhaddad, N., George, R., Duckworth, G., et al. (2008) Severe Streptococcus pyogenes infections, United Kingdom, 2003-2004. Emerg Infect Dis 14: 202-209.
34. Laupland, K.B., Davies, H.D., Low, D.E., Schwartz, B., Green, K., and McGeer, A. (2000) Invasive group A streptococcal disease in children and association with varicella-zoster virus infection. Ontario Group A Streptococcal Study Group. Pediatrics 105: E60.
35. Lei, B., DeLeo, F.R., Reid, S.D., Voyich, J.M., Magoun, L., Liu, M., etal. (2002). Opsonophagocytosis-inhibiting mac protein of group A streptococcus: Identification and characteristics of two genetic complexes. Infect Immun 70: 6880-6890.
36. Llewelyn, M. (2005) Human leukocyte antigen class II haplotypes that protect against or predispose to streptococcal toxic shock. Clin Infect Dis 41 (Suppl. 7): S445-S448.
37. Lukomski, S., Hoe, N.P., Abdi, I., Rurangirwa, J., Kordari, P., Liu, M., et al. (2000) Nonpolar inactivation of the hypervariable streptococcal inhibitor of complement gene (sic) in serotype M1 Streptococcus pyogenes significantly decreases mouse mucosal colonization. Infect Immun 68: 535-542.
38. Lyon, W.R., and Caparon, M.G. (2004) Role for serine protease HtrA (DegP) of Streptococcus pyogenes in the biogenesis of virulence factors SpeB and the hemolysin streptolysin S. Infect Immun 72: 1618-1625.
39. Ma, Y., Bryant, A.E., Salmi, D.B., Hayes-Schroer, S.M., McIndoo, E., Aldape, M.J., and Stevens, D.L. (2006) Identification and characterization of bicistronic speB and prsA gene expression in the group A Streptococcus. J Bacteriol 188: 7626-7634.
40. Maripuu, L., Eriksson, A., Eriksson, B., Pauksen, K., Holm, S., and Norgren, M. (2007) Dynamics of the immune response against extracellular products of group A streptococci during infection. Clin Vaccine Immunol 14: 44-51.
41. Mascini, E.M., Jansze, M., Schellekens, J.F., Musser, J.M., Faber, J.A., Verhoef-Verhage, L.A., etal. (2000) Invasive group A streptococcal disease in the Netherlands: Evidence for a protective role of anti-exotoxin A antibodies. J Infect Dis 181: 631-638.
42. Mora, M., Bensi, G., Capo, S., Falugi, F., Zingaretti, C., Manetti, A.G., etal. (2005) Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci USA 102: 15641-15646.
43. Musser, J.M., and DeLeo, F.R. (2005) Toward a genome-wide systems biology analysis of host-pathogen interactions in group A Streptococcus. Am J Pathol 167: 1461-1472.
44. Nandakumar, K.S., Johansson, B.P., Bjorck, L., and Holmdahl, R. (2007) Blocking of experimental arthritis by cleavage of IgG antibodies in vivo. Arthritis Rheum 56: 3253-3260.
45. Norrby-Teglund, A., Nepom, G.T., and Kotb, M. (2002) Differential presentation of group A streptococcal superantigens by HLA class II DQ and DR alleles. Eur J Immunol 32: 2570-2577.
46. Nuwayhid, Z.B., Aronoff, D.M., and Mulla, Z.D. (2007) Blunt trauma as a risk factor for group A streptococcal necrotizing fasciitis. Ann Epidemiol 17: 878-881.
47. Nyberg, P., Rasmussen, M., Von Pawel-Rammingen, U., and Bjorck, L. (2004). SpeB modulates fibronectin-dependent internalization of Streptococcus pyogenes by efficient proteolysis of cell-wall-anchored protein F1. Microbiol 150: 1559-1569.
48. O'Loughlin, R.E., Roberson, A., Cieslak, P.R., Lynfield, R., Gershman, K., Craig, A., et al. (2007) The epidemiology of invasive group A streptococcal infection and potential vaccine implications: United States, 2000-2004. Clin Infect Dis 45: 853-862.
49. Osterlund, A., Popa, R., Nikkila, T., Scheynius, A., and Engstrand, L. (1997) Intracellular reservoir of Streptococcus pyogenes in vivo: A possible explanation for recurrent pharyngotonsillitis. Laryngoscope 107: 640-647.
50. Parry, M.A., Zhang, X.C., and Bode, I. (2000) Molecular mechanisms of plasminogen activation: Bacterial cofactors provide clues. Trends Biochem Sci 25: 53-59.
51. Purushothaman, S.S., Wang, B., and Cleary, P.P. (2003) M1 protein triggers a phosphoinositide cascade for group A Streptococcus invasion of epithelial cells. Infect Immun 71: 5823-5830.
52. Purushothaman, S.S., Park, H.S., and Cleary, P.P. (2004) Promotion of fibronectin independent invasion by C5a peptidase into epithelial cells in group A Streptococcus. Indian J Med Res 119 (Suppl.): 44-47.
53. Reid, S.D., Chaussee, M.S., Doern, C.D., Chaussee, M.A., Montgomery, A.G., Sturdevant, D.E., and Musser, J.M. (2006) Inactivation of the group A Streptococcus regulator srv results in chromosome wide reduction of transcript levels, and changes in extracellular levels of Sic and SpeB. FEMS Immunol Med Microbiol 48: 283-292.
54. Rodriguez-Ortega, M.J., Norais, N., Bensi, G., Liberatori, S., Capo, S., Mora, M., et al. (2006) Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol 24: 191-197.
55. Seki, M., Saito, M., Iida, K., Taniai, H., Soejima, T., Nakayama, H., and Yoshida, S. (2008) Onset of streptococcal toxic shock syndrome is accelerated by bruising in a mouse model. Microb Pathog 44: 339-343.
56. Shelburne, S.A., Sumby, P., Sitkiewicz, I., Granville, C.N., DeLeo, F.R., and Musser, J.M. (2005a) Central role of a two-component gene regulatory system of previously unknown function in pathogen persistence in human saliva. Proc Natl Acad Sci USA 102: 16037-16042.
57. Shelburne, S.A., 3rd, Granville, C., Tokuyama, M., Sitkiewicz, I., Patel, P., and Musser, J.M. (2005b) Growth characteristics of and virulence factor production by group A Streptococcus during cultivation in human saliva. Infect Immun 73: 4723-4731.
58. Shelburne, S.A., 3rd, Keith, D.B., Davenport, M.T., Horstmann, N., Brennan, R.G., and Musser, J.M. (2008) Molecular characterization of group A Streptococcus maltodextrin catabolism and its role in pharyngitis. Mol Microbiol 69: 436-452.
59. Sitkiewicz, I., Nagiec, M.J., Sumby, P., Butler, S.D., Cywes-Bentley, C., and Musser, J.M. (2006) Emergence of a bacterial clone with enhanced virulence by acquisition of a phage encoding a secreted phospholipase A2. Proc Natl Acad Sci USA 103: 16009-16014.
60. Soderberg, J.J., Engstrom, P., and von Pawel-Rammingen, U. (2008) The intrinsic immunoglobulin G endopeptidase activity of streptococcal Mac-2 proteins implies a unique role for the enzymatically impaired Mac-2 protein of M28 serotype strains. Infect Immun 76: 2183-2188.
61. Sumby, P., Barbian, K.D., Gardner, D.J., Whitney, A.R., Welty, D.M., Long, R.D., et al. (2005) Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci USA 102: 1679-1684.
62. Sumby, P., Whitney, A.R., Graviss, E.A., DeLeo, F.R., and Musser, J.M. (2006) Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog 2, e5.
63. Sumby, P., Tart, A.H., and Musser, J.M. (2008) A non-human primate model of acute group a Streptococcus pharyngitis. Methods Mol Biol 431: 255-267.
64. Sun, H., Ringdahl, U., Homeister, J.W., Fay, W.P., Engleberg, N.C., Yang, A.Y., etal. (2004) Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305: 1283-1286.
65. Svensson, M.D., Scaramuzzino, D.A., Sjobring, U., Olsen, A., Frank, C., and Bessen, D.E. (2000) Role for a secreted cysteine proteinase in the establishment of host tissue tropism by group A streptococci. Mol Microbiol 38: 242-253.
66. Tamura, F., Nakagawa, R., Akuta, T., Okamoto, S., Hamada, S., Maeda, H., et al. (2004). Proapoptotic effect of proteolytic activation of matrix metalloproteinases by Streptococcus pyogenes thiol proteinase (Streptococcus pyrogenic exotoxin B). Infect Immun 72: 4836-4847.
67. Tart, A.H., Walker, M.J., and Musser, J.M. (2007) New understanding of the group A Streptococcus pathogenesis cycle. Trends Microbiol 15: 318-325.
68. Taylor, F.B., Jr, Bryant, A.E., Blick, K.E., Hack, E., Jansen, P.M., Kosanke, S.D., and Stevens, D.L. (1999) Staging of the baboon response to group A streptococci administered intramuscularly: A descriptive study of the clinical symptoms and clinical chemical response patterns. Clin Infect Dis 29: 167-177.
69. Thulin, P., Johansson, L., Low, D.E., Gan, B.S., Kotb, M., McGeer, A., and Norrby-Teglund, A. (2006) Viable group A streptococci in macrophages during acute soft tissue infection. PLoS Med 3, e53.
70. Valiquette, L., Low, D.E., Chow, R., and McGeer, A.J. (2006) A survey of physician's attitudes regarding management of severe group A streptococcal infections. Scand J Infect Dis 38: 977-982.
71. Virtaneva, K., Porcella, S.F., Graham, M.R., Ireland, R.M., Johnson, C.A., Ricklefs, S.M., et al. (2005) Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci USA 102: 9014-9019.
72. Walker, M.J., Hollands, A., Sanderson-Smith, M.L., Cole, J.N., Kirk, J.K., Henningham, A., et al. (2007) DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 13: 981-985.
73. Wang, B., Cue, D., and Cleary, P. (2006a) Intracelluar invasion by Streptococcus pyogenes: Invasins, host receptors, and relevance to human disease. In Gram-Positive Pathogens. Fischetti, V., Novick, R.P., Ferretti, J.J., Portnoy, D.A., and Rodd, J.I. (eds). Washington, DC: American Society for Microbiology Press, pp. 29-36.
74. Wang, B., Li, S., Southern, P.J., and Cleary, P.P. (2006b) Streptococcal modulation of cellular invasion via TGF-beta1 signaling. Proc Natl Acad Sci USA 103: 2380-2385.
75. Wang, B., Yurecko, R.S., Dedhar, S., and Cleary, P.P. (2006c) Integrin-linked kinase is an essential link between integrins and uptake of bacterial pathogens by epithelial cells. Cell Microbiol 8: 257-266.
76. Wang, B., Li, S., Dedhar, S., and Cleary, P.P. (2007) Paxillin phosphorylation: Bifurcation point downstream of integrin-linked kinase (ILK) in streptococcal invasion. Cell Microbiol 9: 1519-1528.
77. Wang, S.M., Lu, I.H., Lin, Y.L., Lin, Y.S., Wu, J.J., Chuang, W.J., et al. (2008) The severity of Streptococcus pyogenes infections in children is significantly associated with plasma levels of inflammatory cytokines. Diagn Microbiol Infect Dis 61: 165-169.
78. Woodbury, R., and Haldenwang, W.G. (2003) HrcA is a negative regulator of the dnaK and groESL operons of Streptococcus pyogenes. Biochem Biophys Res Commun 302: 722-727.
79. Yang, L.P., Eriksson, B.K., Harrington, Z., Curtis, N., Lang, S., Currie, B.J., et al. (2006) Variations in the protective immune response against streptococcal superantigens in populations of different ethnicity. Med Microbiol Immunol 195: 37-43.
80. Zahner, D., and Scott, J.R. (2007) SipA is required for pilus formation in Streptococcus pyogenes serotype M3. J Bacteriol 190: 527-535.