Redirecting the humoral immune response against Streptococcus mutans antigen P1 with monoclonal antibodies

Infection and Immunity

Volumn 72, Issue 12, 2004, Pages 6951-6960

  Oli, Monika W ^a   Rhodin, Nikki ^a   McArthur, William P ^a   Brady, L Jeannine ^a,b  

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

^b UNIVERSITY OF FLORIDA HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ADHESIN P1; ADHESIN P1 MONOCLONAL ANTIBODY; AGGLUTININ; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; MONOCLONAL ANTIBODY; STREPTOCOCCUS ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY COMPLEX; ARTICLE; BACTERIUM ADHERENCE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION COEFFICIENT; DENTAL CARIES; DRUG ADMINISTRATION ROUTE; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOMODULATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; STREPTOCOCCUS MUTANS;

ADHESINS, BACTERIAL; AGGLUTININS; ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; BACTERIAL ADHESION; EPITOPES, T-LYMPHOCYTE; FEMALE; HUMANS; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; SALIVA; STREPTOCOCCUS MUTANS;

EID: 9244227615     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.12.6951-6960.2004     Document Type: Article

References (83)

1. Akdis, C. A., T. Blesken, D. Wymann, M. Akdis, and K. Blaser. 1998. Differential regulation of human T cell cytokine patterns and IgE and IgG4 responses by conformational antigen variants. Eur. J. Immunol. 28:914-925.
2. Anderson, C. F., J. S. Gerber, and D. M. Mosser. 2002. Modulating macrophage function with IgG immune complexes. J. Endotoxin Res. 8:477-481.
3. Anderson, C. F., and D. M. Mosser. 2002. Cutting edge: biasing immune responses by directing antigen to macrophage Fc gamma receptors. J. Immunol. 168:3697-3701.
4. Anderson, C. F., and D. M. Mosser. 2002. A novel phenotype for an activated macrophage: the type 2 activated macrophage. J. Leukoc. Biol. 72:101-106.
5. 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.
6. 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 FyRII. Eur. J. Immunol. 32:530-540.
7. Ayakawa, G. Y., A. S. Bleiweis, P. J. Crowley, and M. W. Cunningham. 1988. Heart cross-reactive antigens of mutans streptococci share epitopes with group A streptococci and myosin. J. Immunol. 140:253-257.
8. 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.
9. Banas, J. A. 2004. Virulence properties of Streptococcus mutans. Front. Biosci. 9:1267-1277.
10. 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.
11. 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 prolinc-rich repeat domain results in altered antigenicity and lack of surface expression of the Streptococcus mutans P1 adhesin molecule. Infect. Immun. 66:4274-4282.
12. Brady, L. J., D. A. Piacentini, P. J. Crowley, and A. S. Bleiweis. 1991. 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.
13. 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.
14. 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.
15. 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.
16. Carmicle, S., G. Dai, N. K. Steede, and S. J. Landry. 2002. Proteolytic sensitivity and helper T-cell epitope immunodominance associated with the mobile loop in Hsp10s. J. Biol. Chem. 277:155-160.
17. Casadevall, A., and L. A. Pirofski. 2003. Microbial virulence results from the interaction between host and microorganism. Trends Microbiol. 11:157-158.
18. Chia, J. S., H. T. Lien, P. R. Hsueh, P. M. Chen, A. Sun, and J. Y. Chen. 2002. Induction of cytokines by glucosyltransferases of Streptococcus mutans. Clin. Diagn. Lab. Immunol. 9:892-897.
19. Crowley, P. J., L. J. Brady, S. M. Michalek, and A. S. Bleiweis. 1999. Virulence of a spaP mutant of Streptococcus mutans in a gnotobiotic rat model. Infect. Immun. 67:1201-1206.
20. Crowley, P. J., L. J. Brady, D. A. Piacentini, and A. S. Bleiweis. 1993. Identification of a salivary agglutinin-binding domain within cell surface adhesin P1 of Streptococcus mutans. Infect. Immun. 61:1547-1552.
21. Dai, G., S. Carmicle, N. K. Steede, and S. J. Landry. 2002. Structural basis for helper T-cell and antibody epitope immunodominance in bacteriophage T4 Hsp10. Role of disordered loops. J. Biol. Chem. 277:161-168.
22. Demuth, D. R., C. A. Davis, A. M. Corner, R. J. Lamont, P. S. Leboy, and D. Malamud. 1988. Cloning and expression of a Streptococcus sanguis surface antigen that interacts with a human salivary agglutinin. Infect. Immun. 56:2484-2490.
23. Demuth, D. R., and D. C. Irvine. 2002. Structural and functional variation within the alanine-rich repetitive domain of streptococcal antigen I/II. Infect. Immun. 70:6389-6398.
24. Ebersole, J. L. 2003. Humoral immune responses in gingival crevice fluid: local and systemic implications. Periodontol. 2000 31:135-166.
25. Fan, M. W., Z. Bian, Z. X. Peng, Y. Zhong, Z. Chen, B. Peng, and R. Jia. 2002. A DNA vaccine encoding a cell-surface protein antigen of Streptococcus mutans protects gnotobiotic rats from caries. J. Dent. Res. 81:784-787.
26. Gong, K., T. Ouyang, and M. C. Herzberg. 1998. A streptococcal adhesion system for salivary pellicle and platelets. Infect. Immun. 66:5388-5392.
27. Guo, J., M. Fan, Z. Bian, R. Jia, and B. Peng. 2002. Intranasal immunization against dental caries with plasmid DNA encoding pac gene of Streptococcus mutans in gnotobiotic rats. Zhonghua Kou Qiang Yixue Zazhi 37:452-455.
28. 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.
29. Hamada, S., and H. D. Slade. 1980. Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol. Rev. 44:331-384.
30. Harder, E. J., C. J. Wilkowske, J. A. Washington II, and J. E. Geraci. 1974. Streptococcus mutans endocarditis. Ann. Intern. Med. 80:364-368.
31. Heyman, B. 1990. The immune complex: possible ways of regulating the antibody response. Immunol. Today 11:310-313.
32. 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.
33. Huang, Y., G. Hajishengallis, and S. M. Michalek. 2001. Induction of protective immunity against Streptococcus mutans colonization after mucosal immunization with attenuated Salmonella enterica serovar Typhimurium expressing an S. mutans adhesin under the control of in vivo-inducible nirB promoter. Infect. Immun. 69:2154-2161.
34. Hubbard, S. J., R. J. Beynon, and J. M. Thornton. 1998. Assessment of conformational parameters as predictors of limited proteolytic sites in native protein structures. Protein Eng. 11:349-359.
35. Jenkinson, H. F., and D. R. Demuth. 1997. Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol. Microbiol. 23:183-190.
36. Katona, L. I., S. Ayalew, J. L. Coleman, and J. L. Benach. 2000. A bactericidal monoclonal antibody elicits a change in its antigen, OspB of Borrelia burgdorferi, that can be detected by limited proteolysis. J. Immunol. 164:1425-1431.
37. Kelly, C. G., S. Todryk, H. L. Kendal, G. H. Munro, and T. Lehner. 1995. T-cell, adhesion, and B-cell epitopcs of the cell surface Streptococcus mutans protein antigen I/II. Infect. Immun. 63:3649-3658.
38. Kelly, C. G., J. S. Younson, B. Y. Hikmat, S. M. Todryk, M. Czisch, P. I. Haris, I. R. Flindall, C. Newby, A. I. Mallet, J. K. Ma, and T. Lehner. 1999. A synthetic peptide adhesion epitope as a novel antimicrobial agent. Nat. Biotechnol. 17:42-47.
39. Koga, T., T. Oho, Y. Shimazaki, and Y. Nakano. 2002. Immunization against dental caries. Vaccine 20:2027-2044.
40. Kolenbrander, P. E., R. N. Andersen, D. S. Blehert, P. G. Egland, J. S. Foster, and R. J. Palmer, Jr. 2002. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66:486-505.
41. 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.
42. Lanzavecchia, A. 1985. Antigen-specific interaction between T and B cells. Nature 314:537-539.
43. 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.
44. Love, R. M., M. D. McMillan, and H. F. Jenkinson. 1997. Invasion of dentinal tubules by oral streptococci is associated with collagen recognition mediated by the antigen I/II family of polypeptides. Infect. Immun. 65:5157-5164.
45. 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.
46. Manca, F. 1991. Interference of monoclonal antibodies with proteolysis of antigens in cellular and in acellular systems. Ann. Ist. Super. Sanita 27:15-19.
47. Manca, F., D. Fenoglio, A. Kunkl, C. Cambiaggi, M. Sasso, and F. Celada. 1988. Differential activation of T cell clones stimulated by macrophages exposed to antigen complexed with monoclonal antibodies. A possible influence of paratope specificity on the mode of antigen processing. J. Immunol. 140:2893-2898.
48. 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.
49. Manca, F., A. Kunkl, D. Fenoglio, A. Fowler, E. Sercarz, and F. Celada. 1985. Constraints in T-B cooperation related to epitope topology on E. coli beta-galactosidase. I. The fine specificity of T cells dictates the fine specificity of antibodies directed to conformation-dependent determinants. Eur. J. Immunol. 15:345-350.
50. McLean, G. R., M. Torres, N. Elguezabal, A. Nakouzi, and A. Casadevall. 2002. Isotype can affect the fine specificity of an antibody for a polysaccharide antigen. J. Immunol. 169:1379-1386.
51. Michalek, S. M., J. Katz, and N. K. Childers. 2001. A vaccine against dental caries: an overview. BioDrugs 15:501-508.
52. Milich, D. R., F. Schodel, J. L. Hughes, J. E. Jones, and D. L. Peterson. 1997. The hepatitis B virus core and e antigens elicit different Th cell subsets: antigen structure can affect Th cell phenotype. J. Virol. 71:2192-2201.
53. Moisset, A., N. Schatz, Y. Lepoivre, S. Amadio, D. Wachsmann, M. Scholler, and J. P. Klein. 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.
54. Nakai, M., N. Okahashi, H. Ohta, and T. Koga. 1993. Saliva-binding region of Streptococcus mutans surface protein antigen. Infect. Immun. 61:4344-4349.
55. Nemoto, T., N. Sato, H. Iwanari, H. Yamashita, and T. Takagi. 1997. Domain structures and immunogenic regions of the 90-kDa heat-shock protein (HSP90). Probing with a library of anti-HSP90 monoclonal antibodies and limited proteolysis. J. Biol. Chem. 272:26179-26187.
56. Nie, X., S. Basu, and J. Cerny. 1997. Immunization with immune complex alters the repertoire of antigen-reactive B cells in the germinal centers. Eur. J. Immunol. 27:3517-3525.
57. Okahashi, N., C. Sasakawa, M. Yoshikawa, S. Hamada, and T. Koga. 1989. Cloning of a surface protein antigen gene from serotype c Streptococcus mutans. Mol. Microbiol. 3:221-228.
58. Pokric, B., D. Sladic, S. Juros, and S. Cajavec. 1993. Application of the immune complex for immune protection against viral disease. Vaccine 11:655-659.
59. Prakobphol, A., F. Xu, V. M. Hoang, T. Larsson, J. Bergstrom, I. Johansson, L. Frangsmyr, U. Holmskov, H. Leffler, C. Nilsson, T. Boren, J. R. Wright, N. Stromberg, and S. J. Fisher. 2000. Salivary agglutinin, which binds Streptococcus mutans and Helicobacter pylori, is the lung scavenger receptor cysteine-rich protein gp-340. J. Biol. Chem. 275:39860-39865.
60. Rhodin, N. R., J. Cuttalo, K. B. Tomer, W. P. McArthur, and L. J. Brady. 2004. Characterization of Streptococcus mutans P1 epitope recognized by immunomodulatory monoclonal antibody 6-11A. Infect. Immun. 72:4680-4688.
61. Rhodin, N. R., M. L. Van Tilburg, M. W. Oli, W. P. McArthur, and L. J. Brady. 2004. Further characterization of immunomodulation by a monoclonal antibody against Streptococcus mutans antigen P1. Infect. Immun. 72:13-21.
62. Ria, F., A. Gallard, C. R. Gabaglia, J. C. Guery, E. E. Sercarz, and L. Adorini. 2004. Selection of similar naive T cell repertoires but induction of distinct T cell responses by native and modified antigen. J. Immunol. 172:3447-3453.
63. 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.
64. Seifert, T. B., A. S. Bleiweis, and L. J. Brady. 2004. Contribution of the alanine-rich region of Streptococcus mutans P1 epitope expression, and interaction with the proline-rich repeat domain. Infect. Immun. 72:4699-4706.
65. Sewell, W. A., and S. Jolles. 2002. Immunomodulatory action of intravenous immunoglobulin. Immunology 107:387-393.
66. Siegrist, C. A. 2003. Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 21:3406-3412.
67. 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.
68. Smith, D. J. 2003. Caries vaccines for the twenty-first century. J. Dent. Educ. 67:1130-1139.
69. So, T., H. Ito, M. Hirata, T. Ueda, and T. Imoto. 2001. Contribution of conformational stability of hen lysozyme to induction of type 2 T-helper immune responses. Immunology 104:259-268.
70. So, T., H. O. Ito, T. Koga, S. Watanabe, T. Ueda, and T. Imoto. 1997. Depression of T-cell epitope generation by stabilizing hen lysozyme. J. Biol. Chem. 272:32136-32140.
71. + T-cell responses. Nat. Med. 9:1287-1292.
72. Stevens, T. L., A. Bossie, V. M. Sanders, R. Fernandez-Botran, R. L. Coffman, T. R. Mosmann, and E. S. Vitetta. 1988. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334:255-258.
73. Uhr, J. W., and J. B. Baumann. 1961. Antibody formation: the suppression of antibody formation by passively administered antibody. J. Exp. Med. 113:935-957.
74. 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.
75. 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.
76. Van Tilburg, M. L., E. V. Kozarov, A. Progulske-Fox, and L. J. Brady. 2001. The effect of monoclonal antibody and route of immunization on the humoral immune response against Porphyromonas gingivalis. Oral Microbiol. Immunol. 16:153-162.
77. Wang, J., N. S. Tan, B. Ho, and J. L. Ding. 2002. Modular arrangement and secretion of a multidomain serine protease. Evidence for involvement of proline-rich region and N-glycans in the secretion pathway. J. Biol. Chem. 277:36363-36372.
78. 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.
79. Wu, H. Y., E. B. Nikolova, K. W. Beagley, and M. W. Russell. 1996. Induction of antibody-secreting cells and T-helper and memory cells in murine nasal lymphoid tissue. Immunology 88:493-500.
80. Yang, F., Y. Cheng, J. Peng, J. Zhou, and G. Jing. 2001. Probing the conformational state of a truncated staphylococcal nuclease R using time of flight mass spectrometry with limited proteolysis. Eur. J. Biochem. 268:4227-4232.
81. Yoneto, T., S. Waki, T. Takai, Y. Tagawa, Y. Iwakura, J. Mizuguchi, H. Nariuchi, and T. Yoshimoto. 2001. A critical role of Fc receptor-mediated antibody-dependent phagocytosis in the host resistance to blood-stage Plasmodium berghei XAT infection. J. Immunol. 166:6236-6241.
82. 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.
83. Zheng, B. J., M. H. Ng, L. F. He, X. Yao, K. W. Chan, K. Y. Yuen, and Y. M. Wen. 2001. Therapeutic efficacy of hepatitis B surface antigen-antibodies- recombinant DNA composite in HBsAg transgenic mice. Vaccine 19:4219-4225.