The changing faces of Streptococcus antigen I/II polypeptide family adhesins: MicroReview

Molecular Microbiology

Volumn 77, Issue 2, 2010, Pages 276-286

  Brady, L Jeannine ^a   Maddocks, Sarah E ^b   Larson, Matthew R ^c   Forsgren, Nina ^d   Persson, Karina ^d   Deivanayagam, Champion C ^e   Jenkinson, Howard F ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UMEÅ UNIVERSITY   (Sweden)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; EPITOPE; GLYCOPROTEIN; STREPTOCOCCUS ANTIGEN; BACTERIAL PROTEIN; PROTEIN I-II, STREPTOCOCCUS MUTANS;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; BACTERIAL COLONIZATION; BIOFILM; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DENTAL CARIES; IMMUNOMODULATION; MOUTH FLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROLINE RICH PROTEIN DOMAIN; PROTEIN MOTIF; SEQUENCE HOMOLOGY; SHORT SURVEY; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS GORDONII; STREPTOCOCCUS MUTANS; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SUIS; THROMBOCYTE AGGREGATION; CHEMICAL STRUCTURE; CHEMISTRY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ANALYSIS;

PORPHYROMONAS GINGIVALIS; POSIBACTERIA; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS GORDONII; STREPTOCOCCUS MUTANS; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SUIS;

ADHESINS, BACTERIAL; BACTERIAL PROTEINS; EPITOPES; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, PROTEIN; STREPTOCOCCUS;

EID: 77954357076     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07212.x     Document Type: Short Survey

References (66)

1. Andre, I., Persson, J., Blom, A.M., Nilsson, H., Drakenberg, T., Lindahl, G., et al. (2006) Streptococcal M protein: structural studies of the hypervariable region, free and bound to human C4BP. Biochemistry 45 : 4559 4568.
2. Brady, L.J., Crowley, P.J., Ma, J.K.-C., Kelly, C., Lee, S.F., Lehner, T. Bleiweis, A.S. (1991a) Restriction fragment length polymorphisms and sequence variation within the spaP gene of Streptococcus mutans serotype c isolates. Infect Immun 59 : 1803 1810.
3. Brady, L.J., Piacentini, D.A., Crowley, P.J. Bleiweis, A.S. (1991b) Identification of monoclonal antibody-binding domains within antigen P1 of Streptococcus mutans and cross-reactivity with related surface antigens of oral streptococci. Infect Immun 59 : 4425 4435.
4. Brady, L.J., Piacentini, D.A., Crowley, P.J., Oyston, P.C.F. Bleiweis, A.S. (1992) Differentiation of salivary agglutinin-mediated adherence and aggregation of mutans streptococci by use of monoclonal antibodies against the major surface adhesin P1. Infect Immun 60 : 1008 1017.
5. Brady, L.J., Cvitkovitch, D.G., Geric, C.M., Addison, M.N., Joyce, J.C., Crowley, P.J., et al. (1998) Deletion of the central proline-rich repeat domain results in altered antigenicity and lack of surface expression of the Streptococcus mutans P1 adhesin molecule. Infect Immun 66 : 4274 4282.
6. Crowley, P.J., Brady, L.J., Piacentini, D.A. Bleiweis, A.S. (1993) Identification of a salivary agglutinin-binding domain within cell surface adhesin P1 of Streptococcus mutans. Infect Immun 61 : 1537 1552.
7. Crowley, P.J., Seifert, T.B., Isoda, R., van Tilburg, M., Oli, M.W., Robinette, R.A., et al. (2008) Requirements for surface expression and function of adhesin P1 from Streptococcus mutans. Infect Immun 76 : 2456 2468.
8. Daep, C.A., James, D.M., Lamont, R.J. Demuth, D.R. (2006) Structural characterization of peptide-mediated inhibition of Porphyromonas gingivalis biofilm formation. Infect Immun 74 : 5756 5762.
9. Dalbey, R.E. Chen, M. (2004) Sec-translocase mediated membrane biogenesis. Biochim Biophys Acta 1694 : 37 53.
10. Deivanayagam, C.C., Rich, R.L., Carson, M., Owens, R.T., Danthuluri, S., Bice, T., et al. (2000) Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Struct Fold Des 8 : 67 78.
11. Deivanayagam, C.C., Wann, E.R., Chen, W., Carson, M., Rajashankar, K.R., Höök, M., et al. (2002) A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J 21 : 6660 6672.
12. van Dolleweerd, C.J., Kelly, C.G., Chargelegue, D. Ma, J.K. (2004) Peptide mapping of a discontinuous epitope of the major surface adhesin from Streptococcus mutans. J Biol Chem 279 : 22198 22203.
13. Eriksson, C., Frängsmyr, L., Danielsson Niemi, L., Holmskov, U., Bergman, T., Leffler, H., et al. (2007) Variant size- and glycoforms of the scavenger receptor cysteine-rich protein gp-340 with differential bacterial aggregation. Glyconj J 24 : 131 142.
14. Forsgren, N., Lamont, R.J. Persson, K. (2009) Crystal structure of the variable domain of the Streptococcus gordonii surface protein SspB. Protein Sci 18 : 1896 1905.
15. Forsgren, N., Lamont, R.J. Persson, K. (2010) Two intramolecular isopeptide bonds are identified in the crystal structure of the Streptococcus gordonii SspB C-terminal domain. J Mol Biol 397 : 740 751.
16. Foster, T.J. Höök, M. (1998) Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6 : 484 488.
17. Funes, S., Hasona, A., Bauerschmitt, H., Grubbauer, C., Kauff, F., Collins, R., et al. (2009) Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function. Proc Natl Acad Sci USA 106 : 6656 6661.
18. Hasona, A., Crowley, P.J., Levesque, C.M., Mair, R.W., Cvitkovitch, D.G., Bleiweis, A.S., et al. (2005) Streptococcal viability and diminished stress tolerance in mutants lacking the signal recognition particle pathway or YidC2. Proc Natl Acad Sci USA 102 : 17466 17471.
19. Heddle, C., Nobbs, A.H., Jakubovics, N.S., Gal, M., Mansell, J.P., Dymock, D., et al. (2003) Host collagen signal induces antigen I/II adhesin and invasion gene expression in oral Streptococcus gordonii. Mol Microbiol 50 : 597 607.
20. Jakubovics, N.S., Strömberg, N., van Dolleweerd, C.J., Kelly, C.G. Jenkinson, H.F. (2005) Differential binding specificities of oral streptococcal antigen I/II family adhesins for human or bacterial ligands. Mol Microbiol 55 : 1591 1605.
21. Jenkinson, H.F. Demuth, D.R. (1997) Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol Microbiol 23 : 183 190.
22. Jonasson, A., Eriksson, C., Jenkinson, H.F., Källestål, C., Johansson, I. Strömberg, N. (2007) Innate immunity glycoprotein gp-340 variants may modulate human susceptibility to dental caries. BMC Infect Dis 7 : 57.
23. Kelly, C., Evans, P., Bergmeier, L., Lee, S.F., Progulske-Fox, A., Harris, A.C., et al. (1989) Sequence analysis of the cloned streptococcal cell surface antigen I/II. FEBS Lett 258 : 127 132.
24. Kelly, C.G., Todryk, S., Kendal, H.L., Munro, G.H. Lehner, T. (1995) T-cell, adhesion, and B-cell epitopes of the cell surface Streptococcus mutans protein antigen I/II. Infect Immun 63 : 3649 3658.
25. Kelly, C.G., Younson, J.S., Hikmat, B.Y., Todryk, S.M., Czisch, M., Haris, P.I., et al. (1999) A synthetic peptide adhesion epitope as a novel antimicrobial agent. Nat Biotechnol 17 : 42 47.
26. Kilian, M., Poulsen, K., Blomqvist, T., Håvarstein, L.S., Bek-Thomsen, M., Tettelin, H., et al. (2008) Evolution of Streptococcus pneumoniae and its close commensal relatives. PLoS ONE 3 : e2683.
27. Koga, T., Okahashi, N., Takahashi, I., Kanamoto, T., Asakawa, H. Iwaki, M. (1990) Surface hydrophobicity, adherence, and aggregation of cell surface protein antigen mutants of Streptococcus mutans serotype c. Infect Immun 58 : 289 296.
28. Larson, M., Rajashankar, K., Patel, M., Robinette, R.A., Crowley, P.J., Michalek, S., et al. (2010) Elongated fimbrial structure of a streptococcal adhesin assembled by the high affinity association of α and PPII-helices. Proc Natl Acad Sci USA 107 : 5983 5988.
29. Lehner, T., Challacombe, S.J. Caldwell, J. (1975) Immunological and bacteriological basis for vaccination against dental caries in rhesus monkeys. Nature 254 : 517 520.
30. Lehner, T., Russell, M.W. Caldwell, J. (1980) Immunisation with a purified protein from Streptococcus mutans against dental caries in rhesus monkeys. Lancet 315 : 995 996.
31. Leito, J.T., Ligtenberg, A.J., Nazmi, K., de Blieck-Hogervorst, J.M., Veerman, E.C. Nieuw Amerongen, A.V. (2008) A common binding motif for various bacteria of the bacteria-binding peptide SRCRP2 of DMBT1/gp-340/salivary agglutinin. Biol Chem 389 : 1193 1200.
32. Loimaranta, V., Jakubovics, N.S., Hytönen, F., Finne, J.M., Jenkinson, H.F. Strömberg, N. (2005) Fluid- or surface-phase human salivary scavenger protein gp340 exposes different bacterial recognition properties. Infect Immun 73 : 2245 2252.
33. Ma, J.K., Hunjan, M., Smith, R., Kelly, C. Lehner, T. (1990) An investigation into the mechanism of protection by local passive immunization with monoclonal antibodies against Streptococcus mutans. Infect Immun 58 : 3407 3414.
34. Ma, J.K., Hikmat, B.Y., Wycoif, K., Vine, N.D., Chargelegue, D., Yu, L., et al. (1998) Characterization of a recombinant plant monoclonal secretory antibody and preventive immunotherapy in humans. Nat Med 4 : 601 606.
35. McArthur, W.P., Rhodin, N.R., Seifert, T.B., Oli, M.W., Robinett, R.A., Demuth, D.R., et al. (2007) Characterization of epitopes recognized by anti-Streptococcus mutans P1 monoclonal antibodies. FEMS Immunol Med Microbiol 50 : 342 353.
36. Matsushita, K., Nisizawa, T., Nagaoka, S., Kawagoe, M. Koga, T. (1994) Identification of antigen epitopes in a surface protein antigen of Streptococcus mutans in humans. Infect Immun 62 : 4034 4042.
37. Moisset, A., Schatz, N., Lepoivre, Y., Amadio, S., Wachsmann, D., Scholler, M., et al. (1994) Conservation of salivary glycoprotein-interacting and human immunoglobulin G-cross-reactive domains of antigen I/II in oral streptococci. Infect Immun 62 : 184 193.
38. Munro, G.H., Evans, P., Todryk, S., Buckett, P., Kelly, C.G. Lehner, T. (1993) A protein fragment of streptococcal cell surface antigen I/II which prevents adhesion of Streptococcus mutans. Infect Immun 61 : 4590 4598.
39. Nakai, M., Okahashi, N., Ohta, H. Koga, T. (1993) Saliva-binding region of Streptococcus mutans surface protein antigen. Infect Immun 61 : 4344 4349.
40. Nobbs, A.H., Shearer, B.H., Drobni, M., Jepson, M.A. Jenkinson, H.F. (2007) Adherence and internalization of Streptococcus gordonii by epithelial cells involves β1 integrin recognition by SspA and SspB (antigen I/II family) polypeptides. Cell Microbiol 9 : 65 83.
41. Nobbs, A.H., Lamont, R.J. Jenkinson, H.F. (2009) Streptococcus adherence and colonization. Microbiol Mol Biol Rev 73 : 407 450.
42. Nouwen, N., Berrelkamp, G. Driessen, A.J. (2007) Bacterial sec-translocase unfolds and translocates a class of folded protein domains. J Mol Biol 372 : 422 433.
43. Okahashi, N., Takahashi, I., Nakai, M., Senpuku, H., Nisizawa, T. Koga, T. (1993) Identification of antigenic epitopes in an alanine-rich repeating region of a surface protein antigen of Streptococcus mutans. Infect Immun 61 : 1301 1306.
44. Oli, M.W., Rhodin, N., McArthur, W.P. Brady, L.J. (2004) Redirecting the humoral immune response against Streptococcus mutans antigen P1 with monoclonal antibodies. Infect Immun 72 : 6951 6960.
45. Palmer, T., Sargent, F. Berks, B.C. (2005) Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol 13 : 175 180.
46. Pecharki, D., Petersen, F.C., Assev, S. Scheie, A.A. (2005) Involvement of antigen I/II surface proteins in Streptococcus mutans and Streptococcus intermedius biofilm formation. Oral Microbiol Immunol 20 : 366 371.
47. Petersen, F.C., Assev, S., van der Mei, H.C., Busscher, H.J. Scheie, A.A. (2002) Functional variation of the antigen I/II surface protein in Streptococcus mutans and Streptococcus intermedius. Infect Immun 70 : 249 256.
48. Petersen, H.J., Keane, C., Jenkinson, H.F., Vickerman, M.M., Jesionowski, A., Waterhouse, J.C., et al. (2010) Human platelets recognize a novel surface protein, PadA, on Streptococcus gordonii through a unique interaction involving fibrinogen receptor GPIIbIIIa. Infect Immun 78 : 413 422.
49. Phillips, G.N., Jr., Flicker, P.F., Cohen, C., Manjula, B.N. Fischetti, V.A. (1981) Streptococcal M protein: alpha-helical coiled-coil structure and arrangement on the cell surface. Proc Natl Acad Sci USA 78 : 4689 4693.
50. Robinette, R.A., Oli, M.W., McARthur, W.P. Brady, L.J. (2009) Beneficial immunomodulation by Streptococcus mutans anti-P1 monoclonal antibodies is Fc independent and correlates with increased exposure of a relevant target epitope. J Immunol 183 : 4628 4638.
51. Russell, M.W., Bergmeier, L.A., Zanders, E.D. Lehner, T. (1980) Protein antigens of Streptococcus mutans: purification and properties of a double antigen and its protease-resistant component. Infect Immun 28 : 486 493.
52. Sciotti, M.A., Yamodo, I., Klein, J.P. Ogier, J.A. (1997) The N-terminal half part of the oral streptococcal antigen I/IIf contains two distinct binding domains. FEMS Microbiol Lett 153 : 439 445.
53. Scott, J.R. Barnett, T.C. (2006) Surface proteins of gram-positive bacteria and how they get there. Annu Rev Microbiol 60 : 397 423.
54. Seifert, T.B., Bleiweis, S.S. Brady, L.J. (2004) Contribution of the alanine-rich region of Streptococcus mutans P1 to antigenicity, surface expression, and interaction with the proline-rich repeat domain. Infect Immun 72 : 4699 4706.
55. Senpuku, H., Miyauchi, T., Hanada, N. Nisizawa, T. (1995) An antigenic peptide inducing cross-reacting antibodies inhibiting the interactions of Streptococcus mutans Pac with human salivary components. Infect Immun 63 : 4695 4703.
56. Senpuku, H., Kato, H., Takeuchi, H. Noda, A. (1997) Identification of core B cell epitope in the synthetic peptide inducing cross-inhibiting antibodies to a surface protein antigen of Streptococcus mutans. Immunol Invest 26 : 531 548.
57. Senpuku, H., Yanagi, K. Nisizawa, T. (1998) Identification of Streptococcus mutans Pac peptide binding with human MHC class II molecules (DRB1*0802, *1101, *1041 and *1405). Immunology 95 : 322 330.
58. Takahashi, I., Okahashi, N., Matsushita, K., Tokuda, M., Kanamoto, T., Munehata, E., et al. (1991) Immunogenicity and protective effect against oral colonization by Streptococcus mutans of synthetic peptides of a streptococcal surface protein antigen. J Immunol 146 : 332 336.
59. Taubman, M.A. Nash, D.A. (2006) The scientific and public-health imperative for a vaccine against dental caries. Nat Rev Immunol 6 : 555 563.
60. Tettelin, H., Masignani, V., Cieslewicz, M.J., Donati, C., Medini, D., Ward, N.L., et al. (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial 'pan-genome'. Proc Natl Acad Sci USA 102 : 13950 13955.
61. Todryk, S.M., Kelly, C.G., Munro, G.H. Lehner, T. (1996) Induction of immune responses to functional determinants of a cell surface streptococcal antigen. Immunology 87 : 55 63.
62. Troffer-Charlier, N., Ogier, J., Moras, D. Cavarelli, J. (2002) Crystal structure of the V-region of Streptococcus mutans antigen I/II at 2.4 A resolution suggests a sugar preformed binding site. J Mol Biol 318 : 179 188.
63. Waters, C.M., Hirt, H., McCormick, J.K., Schlievert, P.M., Wells, C.L. Dunny, G.M. (2004) An amino-terminal domain of Enterococcus faecalis aggregation substance is required for aggregation, bacterial internalization by epithelial cells and binding to lipoteichoic acid. Mol Microbiol 52 : 1159 1171.
64. Xu, P., Alves, J.M., Kitten, T., Brown, A., Chen, Z., Ozaki, L.S., et al. (2007) Genome of the opportunistic pathogen Streptococcus sanguinis. J Bacteriol 189 : 3166 3175.
65. Zhang, S., Green, N.M., Sitkiewicz, I., Lefebrve, R.B. Musser, J.M. (2006) Identification and characterization of an antigen I/II family protein produced by group A Streptococcus. Infect Immun 74 : 4200 4213.
66. Zong, Y., Xu, Y., Liang, X., Keene, D.R., Höök, A., Gurusiddappa, S., et al. (2005) A 'collagen hug' model for Staphylococcus aureus CNA binding to collagen. EMBO J 24 : 4224 4236.