Beneficial immunomodulation by Streptococcus mutans anti-P1 monoclonal antibodies is Fc independent and correlates with increased exposure of a relevant target epitope

Journal of Immunology

Volumn 183, Issue 7, 2009, Pages 4628-4638

  Robinette, Rebekah A ^a   Oli, Monika W ^a   McArthur, William P ^a   Brady, L Jeannine ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; EPITOPE; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; PEPSIN A; AGGLUTININ; IMMUNOGLOBULIN FC FRAGMENT; SALIVA PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN ANTIBODY COMPLEX; ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; CELL SURFACE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOMODULATION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; STREPTOCOCCUS MUTANS; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; ANTIBODY COMBINING SITE; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; COMPARATIVE STUDY; FEMALE; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNOLOGY; MALE; METABOLISM; PHYSIOLOGY;

ADHESINS, BACTERIAL; AGGLUTININS; ANIMALS; ANTIBODIES, MONOCLONAL; BACTERIAL ADHESION; BINDING SITES, ANTIBODY; EPITOPES; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; SALIVARY PROTEINS AND PEPTIDES; STREPTOCOCCUS MUTANS;

EID: 70449704669     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803300     Document Type: Article

References (64)

1. Hamada, S., and H. D. Slade. 1980. Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol. Rev. 44: 331-384.
2. Michalek, S. M., J. Katz, and N. K. Childers. 2001. A vaccine against dental caries: an overview. BioDrugs 15: 501-508. (Pubitemid 33771733)
3. Smith, D. J., B. Shoushtari, R. L. Heschel, W. F. King, and M. A. Taubman. 1997. Immunogenicity and protective immunity induced by synthetic peptides associated with a catalytic subdomain of mutans group streptococcal glucosyl-transferase. Infect. Immun. 65: 4424-4430.
4. Smith, D. J., and M. A. Taubman. 1996. Experimental immunization of rats with a Streptococcus mutans 59-kilodalton glucan-binding protein protects against dental caries. Infect. Immun. 64: 3069-3073.
5. Zhang, P., C. Jespersgaard, L. Lamberty-Mallory, J. Katz, Y. Huang, G. Hajishengallis, and S. M. Michalek. 2002. Enhanced immunogenicity of a genetic chimeric protein consisting of two virulence antigens of Streptococcus mutans and protection against infection. Infect. Immun. 70: 6779-6787. (Pubitemid 35387909)
6. Russell, M. W., and T. Lehner. 1978. Characterization of antigens extracted from cells and culture fluids of Streptococcus mutans serotype c. Arch. Oral Biol. 23: 7-15.
7. Okahashi, N., C. Sasakawa, M. Yoshikawa, S. Hamada, and T. Koga. 1989. Molecular characterization of a surface protein antigen gene from serotype c Streptococcus mutans, implicated in dental caries. Mol. Microbiol. 3: 673-678.
8. Jenkinson, H. F., and D. R. Demuth. 1997. Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol. Microbiol. 23: 183-190.
9. Brady, L. J., D. A. Piacentini, P. J. Crowley, P. C. Oyston, and A. S. Bleiweis. 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.
10. Koga, T., Y. Yamashita, Y. Nakano, M. Kawasaki, T. Oho, H. Yu, M. Nakai, and N. Okahashi. 1995. Surface proteins of Streptococcus mutans. Dev. Biol. Stand. 85: 363-369.
11. Lee, S. F., A. Progulske-Fox, G. W. Erdos, D. A. Piacentini, G. Y. Ayakawa, P. J. Crowley, and A. S. Bleiweis. 1989. Construction and characterization of isogenic mutants of Streptococcus mutans deficient in major surface protein antigen P1 (I/II). Infect. Immun. 57: 3306-3313.
12. Munro, G. H., P. Evans, S. Todryk, P. Buckett, C. G. Kelly, and T. Lehner. 1993. A protein fragment of streptococcal cell surface antigen I/II which prevents adhesion of Streptococcus mutans. Infect. Immun. 61: 4590-4598.
13. Prakobphol, A., F. Xu, V. M. Hoang, T. Larsson, J. Bergstrom, I. Johansson, L. Frangsmyr, U. Holmskov, H. Leffler, C. Nilsson, et al. 2000. Salivary agglutinin, which binds Streptococcus mutans and Helicobacter pylori, is the lung scavenger receptor cysteine-rich protein gp-340. J. Biol. Chem. 275: 39860-39866.
14. Hajishengallis, G., T. Koga, and M. W. Russell. 1994. Affinity and specificity of the interactions between Streptococcus mutans antigen I/II and salivary components. J. Dent. Res. 73: 1493-1502.
15. Smith, D. J., and R. O. Mattos-Graner. 2008. Secretory immunity following mutans streptococcal infection or immunization. Curr. Top. Microbiol. Immunol. 319: 131-156.
16. Bratthall, D., R. Serinirach, K. Hamberg, and L. Widerstrom. 1997. Immunoglobulin A reaction to oral streptococci in saliva of subjects with different combinations of caries and levels of mutans streptococci. Oral Microbiol. Immunol. 12: 212-218. (Pubitemid 27335708)
17. Challacombe, S. J., L. A. Bergmeier, and A. S. Rees. 1984. Natural antibodies in man to a protein antigen from the bacterium Streptococcus mutans related to dental caries experience. Arch. Oral Biol. 29: 179-184.
18. Hocini, H., S. Iscaki, J. P. Bouvet, and J. Pillot. 1993. Unexpectedly high levels of some presumably protective secretory immunoglobulin A antibodies to dental plaque bacteria in salivas of both caries-resistant and caries-susceptible subjects. Infect. Immun. 61: 3597-3604. (Pubitemid 23260026)
19. Kelly, C. G., S. Todryk, H. L. Kendal, G. H. Munro, and T. Lehner. 1995. T-cell, adhesion, and B-cell epitopes of the cell surface Streptococcus mutans protein antigen I/II. Infect. Immun. 63: 3649-3658.
20. Lehtonen, O. P., E. M. Grahn, T. H. Stahlberg, and L. A. Laitinen. 1984. Amount and avidity of salivary and serum antibodies against Streptococcus mutans in two groups of human subjects with different dental caries susceptibility. Infect. Immun. 43: 308-313.
21. Rose, P. T., R. L. Gregory, L. E. Gfell, and C. V. Hughes. 1994. IgA antibodies to Streptococcus mutans in caries-resistant and -susceptible children. Pediatr. Dent. 16: 272-275.
22. Tenovuo, J., O. P. Lehtonen, and A. S. Aaltonen. 1990. Caries development in children in relation to the presence of mutans streptococci in dental plaque and of serum antibodies against whole cells and protein antigen I/II of Streptococcus mutans. Caries Res. 24: 59-64.
23. Brady, L. J., M. L. van Tilburg, C. E. Alford, and W. P. McArthur. 2000. Monoclonal antibody-mediated modulation of the humoral immune response against mucosally applied Streptococcus mutans. Infect. Immun. 68: 1796-1805.
24. Heyman, B., E. J. Wiersma, and T. Kinoshita. 1990. In vivo inhibition of the antibody response by a complement receptor-specific monoclonal antibody. J. Exp. Med. 172: 665-668. (Pubitemid 20248411)
25. Laissue, J., H. Cottier, M. W. Hess, and R. D. Stoner. 1971. Early and enhanced germinal center formation and antibody responses in mice after primary stimulation with antigen-isologous antibody complexes as compared with antigen alone. J. Immunol. 107: 822-831.
26. Pincus, C. S., and V. Nussenzweig. 1969. Passive antibody may simultaneously suppress and stimulate antibody formation against different portions of a protein molecule. Nature 222: 594-596.
27. Yuan, R., A. Casadevall, G. Spira, and M. D. Scharff. 1995. Isotype switching from IgG3 to IgG1 converts a nonprotective murine antibody to Cryptococcus neoformans into a protective antibody. J. Immunol. 154: 1810-1816.
28. Heyman, B. 1990. The immune complex: possible ways of regulating the antibody response. Immunol. Today 11: 310-313. (Pubitemid 20251351)
29. Heyman, B. 2000. Regulation of antibody responses via antibodies, complement, and Fc receptors. Annu. Rev. Immunol. 18: 709-737. (Pubitemid 30365395)
30. Heyman, B. 2001. Functions of antibodies in the regulation of B cell responses in vivo. Springer Semin. Immunopathol. 23: 421-432. (Pubitemid 34045279)
31. Heyman, B. 2003. Feedback regulation by IgG antibodies. Immunol. Lett. 88: 157-161.
32. Isoda, R., R. A. Robinette, T. L. Pinder, W. P. McArthur, and L. J. Brady. 2007. Basis of beneficial immunomodulation by monoclonal antibodies against Streptococcus mutans adhesin P1. FEMS Immunol. Med. Microbiol. 51: 102-111. (Pubitemid 47387480)
33. Oli, M. W., W. P. McArthur, and L. J. Brady. 2005. A whole cell BIAcore assay to evaluate P1-mediated adherence of Streptococcus mutans to human salivary agglutinin and inhibition by specific antibodies. J. Microbiol. Methods 65: 503-511.
34. Oli, M. W., N. Rhodin, W. P. McArthur, and L. J. Brady. 2004. Redirecting the humoral immune response against Streptococcus mutans antigen P1 with monoclonal antibodies. Infect. Immun. 72: 6951-6960.
35. Crowley, P. J., T. B. Seifert, R. Isoda, M. van Tilburg, M. W. Oli, R. A. Robinette, W. P. McArthur, A. S. Bleiweis, and L. J. Brady. 2008. Requirements for surface expression and function of adhesin P1 from Streptococcus mutans. Infect. Immun. 76: 2456-2468.
36. Rhodin, N. R., J. M. Cutalo, K. B. Tomer, W. P. McArthur, and L. J. Brady. 2004. Characterization of the Streptococcus mutans P1 epitope recognized by immunomodulatory monoclonal antibody 6-11A. Infect. Immun. 72: 4680-4688. (Pubitemid 38989328)
37. Seifert, T. B., A. S. Bleiweis, and L. J. Brady. 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.
38. McArthur, W. P., N. R. Rhodin, T. B. Seifert, M. W. Oli, R. A. Robinette, D. R. Demuth, and L. J. Brady. 2007. Characterization of epitopes recognized by anti-Streptococcus mutans P1 monoclonal antibodies. FEMS Immunol. Med. Microbiol. 50: 342-353. (Pubitemid 47041460)
39. Brady, L. J., D. G. Cvitkovitch, C. M. Geric, M. N. Addison, J. C. Joyce, P. J. Crowley, and A. S. Bleiweis. 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.
40. Ayakawa, G. Y., L. W. Boushell, P. J. Crowley, G. W. Erdos, W. P. McArthur, and A. S. Bleiweis. 1987. Isolation and characterization of monoclonal antibodies specific for antigen P1, a major surface protein of mutans streptococci. Infect. Immun. 55: 2759-2767.
41. Rundegren, J., and R. R. Arnold. 1987. Differentiation and interaction of secretory immunoglobulin A and a calcium-dependent parotid agglutinin for several bacterial strains. Infect. Immun. 55: 288-292. (Pubitemid 17004101)
42. Petrushina, I., M. Tran, N. Sadzikava, A. Ghochikyan, V. Vasilevko, M. G. Agadjanyan, and D. H. Cribbs. 2003. Importance of IgG2c isotype in the immune response to β-amyloid in amyloid precursor protein/transgenic mice. Neurosci. Lett. 338: 5-8. (Pubitemid 36136024)
43. Rivera, J., and A. Casadevall. 2005. Mouse genetic background is a major determinant of isotype-related differences for antibody-mediated protective efficacy against Cryptococcus neoformans. J. Immunol. 174: 8017-8026. (Pubitemid 40806313)
44. Nimmerjahn, F., and J. V. Ravetch. 2005. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 310: 1510-1512. (Pubitemid 41746349)
45. 2 and Fab]. Klin. Wochenschr. 61: 723-736.
46. Taborda, C. P., J. Rivera, O. Zaragoza, and A. Casadevall. 2003. More is not necessarily better: prozone-like effects in passive immunization with IgG. J. Immunol. 170: 3621-3630.
47. Getahun, A., J. Dahlstrom, S. Wernersson, and B. Heyman. 2004. IgG2a-mediated enhancement of antibody and T cell responses and its relation to inhibitory and activating Fcγ receptors. J. Immunol. 172: 5269-5276. (Pubitemid 38542024)
48. Lanzavecchia, A. 1990. Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. Annu. Rev. Immunol. 8: 773-793.
49. Manca, F., D. Fenoglio, G. Li Pira, A. Kunkl, and F. Celada. 1991. Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies. J. Exp. Med. 173: 37-48.
50. Wernersson, S., M. C. Karlsson, J. Dahlstrom, R. Mattsson, J. S. Verbeek, and B. Heyman. 1999. IgG-mediated enhancement of antibody responses is low in Fc receptor γ chain-deficient mice and increased in FcγRII-deficient mice. J. Immunol. 163: 618-622.
51. Manca, F. 1991. Interference of monoclonal antibodies with proteolysis of antigens in cellular and in acellular systems. Ann. Ist. Super. Sanita. 27: 15-19.
52. Antoniou, A. N., S. L. Blackwood, D. Mazzeo, and C. Watts. 2000. Control of antigen presentation by a single protease cleavage site. Immunity 12: 391-398.
53. Antoniou, A. N., and C. Watts. 2002. Antibody modulation of antigen presentation: positive and negative effects on presentation of the tetanus toxin antigen via the murine B cell isoform of FcγRII. Eur. J. Immunol. 32: 530-540.
54. Berzofsky, J. A. 1983. T-B reciprocity: an Ia-restricted epitope-specific circuit regulating T cell-B cell interaction and antibody specificity. Surv. Immunol. Res. 2: 223-229.
55. Kunkl, A., and G. G. Klaus. 1981. The generation of memory cells. IV. Immunization with antigen-antibody complexes accelerates the development of B-memory cells, the formation of germinal centres and the maturation of antibody affinity in the secondary response. Immunology 43: 371-378.
56. Liu, C., E. J. Gosselin, and P. M. Guyre. 1996. FcγRII on human B cells can mediate enhanced antigen presentation. Cell. Immunol. 167: 188-194.
57. Simitsek, P. D., D. G. Campbell, A. Lanzavecchia, N. Fairweather, and C. Watts. 1995. Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. J. Exp. Med. 181: 1957-1963.
58. Watts, C., A. Antoniou, B. Manoury, E. W. Hewitt, L. M. McKay, L. Grayson, N. F. Fairweather, P. Emsley, N. Isaacs, and P. D. Simitsek. 1998. Modulation by epitope-specific antibodies of class II MHC-restricted presentation of the tetanus toxin antigen. Immunol. Rev. 164: 11-16.
59. Takahashi, I., K. Matsushita, T. Nisizawa, N. Okahashi, M. W. Russell, Y. Suzuki, E. Munekata, and T. Koga. 1992. Genetic control of immune responses in mice to synthetic peptides of a Streptococcus mutans surface protein antigen. Infect. Immun. 60: 623-629.
60. Ma, J. K., M. Hunjan, R. Smith, C. Kelly, and T. Lehner. 1990. An investigation into the mechanism of protection by local passive immunization with monoclonal antibodies against Streptococcus mutans. Infect. Immun. 58: 3407-3414.
61. Ma, J. K., M. Hunjan, R. Smith, and T. Lehner. 1989. Specificity of monoclonal antibodies in local passive immunization against Streptococcus mutans. Clin. Exp. Immunol. 77: 331-337.
62. Van Dolleweerd, C. J., D. Chargelegue, and J. K. Ma. 2003. Characterization of the conformational epitope of Guy's 13, a monoclonal antibody that prevents Streptococcus mutans colonization in humans. Infect. Immun. 71: 754-765.
63. Ma, J. K., T. Lehner, P. Stabila, C. I. Fux, and A. Hiatt. 1994. Assembly of monoclonal antibodies with IgG1 and IgA heavy chain domains in transgenic tobacco plants. Eur. J. Immunol. 24: 131-138.
64. Van Dolleweerd, C. J., C. G. Kelly, D. Chargelegue, and J. K. Ma. 2004. Peptide mapping of a novel discontinuous epitope of the major surface adhesin from Streptococcus mutans. J. Biol. Chem. 279: 22198-22203.