Alterations in immunodominance of Streptococcus mutans AgI/II: Lessons learned from immunomodulatory antibodies

Vaccine

Volumn 32, Issue 3, 2014, Pages 375-382

  Robinette, Rebekah A ^a   Heim, Kyle P ^a   Oli, Monika W ^a   Crowley, Paula J ^a   McArthur, William P ^a   Brady, L Jeannine ^a  

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

Author keywords

Immune complex; Immunodominance; Monoclonal antibody; Streptococcus; Vaccine design

Indexed keywords

EPITOPE; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; MONOCLONAL ANTIBODY; P1 POLYPEPTIDE; POLYPEPTIDE; STREPTOCOCCUS ANTIGEN; STREPTOCOCCUS ANTIGEN I; STREPTOCOCCUS ANTIGEN II; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENTAL CARIES; FEMALE; FOLLOW UP; HELPER CELL; IMMUNOGENICITY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; STREPTOCOCCUS MUTANS;

IMMUNE COMPLEX; IMMUNODOMINANCE; MONOCLONAL ANTIBODY; STREPTOCOCCUS; VACCINE DESIGN;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; EPITOPES, T-LYMPHOCYTE; FEMALE; IMMUNODOMINANT EPITOPES; MICE; MICE, INBRED BALB C; PROTEIN STRUCTURE, TERTIARY; STREPTOCOCCAL VACCINES; STREPTOCOCCUS MUTANS;

EID: 84890966735     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.11.023     Document Type: Article

References (104)

1. Hamada S., Slade H.D. Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiological Reviews 1980, 44:331-384.
2. Taubman M.A., Nash D.A. The scientific and public-health imperative for a vaccine against dental caries. Nature Reviews Immunology 2006, 6:555-563.
3. Michalek S.M., Katz J., Childers N.K. A vaccine against dental caries: an overview. BioDrugs 2001, 15:501-508.
4. Smith D.J., Shoushtari B., Heschel R.L., King W.F., Taubman M.A. Immunogenicity and protective immunity induced by synthetic peptides associated with a catalytic subdomain of mutans group streptococcal glucosyltransferase. Infection and Immunity 1997, 65:4424-4430.
5. Smith D.J., Taubman M.A. Experimental immunization of rats with a Streptococcus mutans 59-kilodalton glucan-binding protein protects against dental caries. Infection and Immunity 1996, 64:3069-3073.
6. Zhang P., Jespersgaard C., Lamberty-Mallory L., Katz J., Huang Y., Hajishengallis G., et al. Enhanced immunogenicity of a genetic chimeric protein consisting of two virulence antigens of Streptococcus mutans and protection against infection. Infection and Immunity 2002, 70:6779-6787.
7. Russell M.W., Lehner T. Characterisation of antigens extracted from cells and culture fluids of Streptococcus mutans serotype c. Archives of Oral Biology 1978, 23:7-15.
8. Forester H., Hunter N., Knox K.W. Characteristics of a high molecular weight extracellular protein of Streptococcus mutans. Journal of General Microbiology 1983, 129(Pt 9):2779-2788.
9. Russell R.R. Wall-associated protein antigens of Streptococcus mutans. Journal of General Microbiology 1979, 114:109-115.
10. Okahashi N., Sasakawa C., Yoshikawa M., Hamada S., Koga T. Molecular characterization of a surface protein antigen gene from serotype c Streptococcus mutans, implicated in dental caries. Molecular Microbiology 1989, 3:673-678.
11. Brady L.J., Maddocks S.E., Larson M.R., Forsgren N., Persson K., Deivanayagam C.C., et al. The changing faces of Streptococcus antigen I/II polypeptide family adhesins. Molecular Microbiology 2010, 77:276-286.
12. Brady L.J., Crowley P.J., Ma J.K., Kelly C., Lee S.F., Lehner T., et al. Restriction fragment length polymorphisms and sequence variation within the spaP gene of Streptococcus mutans serotype c isolates. Infection and Immunity 1991, 59:1803-1810.
13. Kelly C., Evans P., Bergmeier L., Lee S.F., Progulske-Fox A., Harris A.C., et al. Sequence analysis of the cloned streptococcal cell surface antigen I/II. FEBS Letters 1989, 258:127-132.
14. Larson M.R., Rajashankar K.R., Patel M.H., Robinette R.A., Crowley P.J., Michalek S., et al. Elongated fibrillar structure of a streptococcal adhesin assembled by the high-affinity association of {alpha}- and PPII-helices. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(13):5983-5988.
15. Troffer-Charlier N., Ogier J., Moras D., Cavarelli J. Crystal structure of the V-region of Streptococcus mutans antigen I/II at 2,4A resolution suggests a sugar preformed binding site. Journal of Molecular Biology 2002, 318:179-188.
16. Larson M.R., Rajashankar K.R., Crowley P.J., Kelly C., Mitchell T.J., Brady L.J., et al. Crystal structure of the C-terminal region of Streptococcus mutans antigen I/II and characterization of salivary agglutinin adherence domains. Journal of Biological Chemistry 2011, 286:21657-21666.
17. Heim K.P., Crowley P.J., Brady L.J. An intramolecular interaction involving the N terminus of a streptococcal adhesin affects its conformation and adhesive function. Journal of Biological Chemistry 2013, 288:13762-13774.
18. Hajishengallis G., Koga T., Russell M.W. Affinity and specificity of the interactions between Streptococcus mutans antigen I/II and salivary components. Journal of Dental Research 1994, 73:1493-1502.
19. Brady L.J., Piacentini D.A., Crowley P.J., Oyston P.C., Bleiweis A.S. Differentiation of salivary agglutinin-mediated adherence and aggregation of mutans streptococci by use of monoclonal antibodies against the major surface adhesin P1. Infection and Immunity 1992, 60:1008-1017.
20. Oho T., Yu H., Yamashita Y., Koga T. Binding of salivary glycoprotein-secretory immunoglobulin A complex to the surface protein antigen of Streptococcus mutans. Infection and Immunity 1998, 66:115-121.
21. Prakobphol A., Xu F., Hoang V.M., Larsson T., Bergstrom J., Johansson I., et al. Salivary agglutinin, which binds Streptococcus mutans and Helicobacter pylori, is the lung scavenger receptor cysteine-rich protein gp-340. Journal of Biological Chemistry 2000, 275:39860-39866.
22. Loimaranta V., Jakubovics N.S., Hytonen J., Finne J., Jenkinson H.F., Stromberg N. Fluid- or surface-phase human salivary scavenger protein gp340 exposes different bacterial recognition properties. Infection and Immunity 2005, 73:2245-2252.
23. Esberg A., Lofgren-Burstrom A., Ohman U., Stromberg N. Host and bacterial phenotype variation in adhesion of Streptococcus mutans to matched human hosts. Infection and Immunity 2012, 80:3869-3879.
24. Madsen J., Mollenhauer J., Holmskov U. Review: Gp-340/DMBT1 in mucosal innate immunity. Innate Immunity 2010, 16:160-167.
25. Edwards A.M., Manetti A.G., Falugi F., Zingaretti C., Capo S., Buccato S., et al. Scavenger receptor gp340 aggregates group A streptococci by binding pili. Molecular Microbiology 2008, 68:1378-1394.
26. Brady L.J. Antibody-mediated immunomodulation: a strategy to improve host responses against microbial antigens. Infection and Immunity 2005, 73:671-678.
27. Michalek S.M., Childers N.K. Development and outlook for a caries vaccine. Critical Reviews in Oral Biology and Medicine 1990, 1:37-54.
28. Challacombe S.J., Bergmeier L.A., Rees A.S. Natural antibodies in man to a protein antigen from the bacterium Streptococcus mutans related to dental caries experience. Archives of Oral Biology 1984, 29:179-184.
29. Lehtonen O.P., Grahn E.M., Stahlberg T.H., Laitinen L.A. Amount and avidity of salivary and serum antibodies against Streptococcus mutans in two groups of human subjects with different dental caries susceptibility. Infection and Immunity 1984, 43:308-313.
30. Tenovuo J., Lehtonen O.P., Aaltonen A.S. 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 Research 1990, 24:59-64.
31. Ebersole J.L. Humoral immune responses in gingival crevice fluid: local and systemic implications. Periodontology 2000 2003, 31:135-166.
32. Huang Y., Hajishengallis G., Michalek S.M. 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. Infection and Immunity 2001, 69:2154-2161.
33. Lehner T., Russell M.W., Caldwell J., Smith R. Immunization with purified protein antigens from Streptococcus mutans against dental caries in rhesus monkeys. Infection and Immunity 1981, 34:407-415.
34. Gregory R.L., Hobbs L.C., Kindle J.C., VanTo T., Malmstrom H.S. Immunodominant antigens of Streptococcus mutans in dental caries-resistant subjects. Human Antibodies and Hybridomas 1990, 1:132-136.
35. Kelly C.G., Todryk S., Kendal H.L., Munro G.H., Lehner T. T-cell, adhesion, and B-cell epitopes of the cell surface Streptococcus mutans protein antigen I/II. Infection and Immunity 1995, 63:3649-3658.
36. Hocini H., Iscaki S., Bouvet J.P., Pillot J. 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. Infection and Immunity 1993, 61:3597-3604.
37. Casadevall A., Pirofski L.A. Exploiting the redundancy in the immune system: vaccines can mediate protection by eliciting 'unnatural' immunity. Journal of Experimental Medicine 2003, 197:1401-1404.
38. Brady L.J., van Tilburg M.L., Alford C.E., McArthur W.P. Monoclonal antibody-mediated modulation of the humoral immune response against mucosally applied Streptococcus mutans. Infection and Immunity 2000, 68:1796-1805.
39. Isoda R., Robinette R.A., Pinder T.L., McArthur W.P., Brady L.J. Basis of beneficial immunomodulation by monoclonal antibodies against Streptococcus mutans adhesin P1. FEMS Immunology and Medical Microbiology 2007, 51:102-111.
40. Oli M.W., McArthur W.P., Brady L.J. A whole cell BIAcore assay to evaluate P1-mediated adherence of Streptococcus mutans to human salivary agglutinin and inhibition by specific antibodies. Journal of Microbiological Methods 2005, 65(3):503-511.
41. Oli M.W., Rhodin N., McArthur W.P., Brady L.J. Redirecting the humoral immune response against Streptococcus mutans antigen P1 with monoclonal antibodies. Infection and Immunity 2004, 72:6951-6960.
42. Rhodin N.R. Immunomodulation by an anti-Streptococcus mutans monoclonal antibody 2003, (Ph.D.) University of Florida, Gainesville, FL.
43. Robinette R.A., Oli M.W., McArthur W.P., Brady L.J. 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 2009, 183:4628-4638.
44. Robinette R.A., Oli M.W., McArthur W.P., Brady L.J. A therapeutic anti-Streptococcus mutans monoclonal antibody used in human passive protection trials influences the adaptive immune response. Vaccine 2011, 29:6292-6300.
45. McArthur W.P., Rhodin N.R., Seifert T.B., Oli M.W., Robinette R.A., Demuth D.R., et al. Characterization of epitopes recognized by anti-Streptococcus mutans P1 monoclonal antibodies. FEMS Immunology and Medical Microbiology 2007, 50:342-353.
46. van Dolleweerd C.J., Chargelegue D., Ma J.K. Characterization of the conformational epitope of Guy's 13, a monoclonal antibody that prevents Streptococcus mutans colonization in humans. Infection and Immunity 2003, 71:754-765.
47. van Dolleweerd C.J., Kelly C.G., Chargelegue D., Ma J.K. Peptide mapping of a novel discontinuous epitope of the major surface adhesin from Streptococcus mutans. Journal of Biological Chemistry 2004, 279:22198-22203.
48. Brady L.J., Cvitkovitch D.G., Geric C.M., Addison M.N., Joyce J.C., Crowley P.J., et al. Deletion of the central proline-rich repeat domain results in altered antigenicity and lack of surface expression of the Streptococcus mutans P1 adhesin molecule. Infection and Immunity 1998, 66:4274-4282.
49. Ayakawa G.Y., Boushell L.W., Crowley P.J., Erdos G.W., McArthur W.P., Bleiweis A.S. Isolation and characterization of monoclonal antibodies specific for antigen P1, a major surface protein of mutans streptococci. Infection and Immunity 1987, 55:2759-2767.
50. Rundegren J., Arnold R.R. Differentiation and interaction of secretory immunoglobulin A and a calcium-dependent parotid agglutinin for several bacterial strains. Infection and Immunity 1987, 55:288-292.
51. Inagaki H., Katoh M., Kurosawa-Ohsawa K., Tanaka S. A new sandwich enzyme-linked immunosorbent assay (ELISA) for transforming growth factor alpha (TGF alpha) based upon conformational modification by antibody binding. Journal of Immunological Methods 1990, 128:27-37.
52. Valenzuela C.F., Dowding A.J., Arias H.R., Johnson D.A. Antibody-induced conformational changes in the Torpedo nicotinic acetylcholine receptor: a fluorescence study. Biochemistry 1994, 33:6586-6594.
53. Mazza M.M., Retegui L.A. Monoclonal antibodies to human growth hormone induce an allosteric conformational change in the antigen. Immunology 1989, 67:148-153.
54. Cao L., Yoshino T., Nishiuchi R., Yamadori I., Akagi T. Homotypic cell aggregation via conformational change of CD44 molecule induced by anti-CD44 monoclonal antibodies. Immunobiology 1995, 193:1-14.
55. Davies D.R., Cohen G.H. Interactions of protein antigens with antibodies. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:7-12.
56. Towbin H., Erard F., van Oostrum J., Schmitz A., Rordorf C. Neoepitope immunoassay: an assay for human interleukin 1 beta based on an antibody induced conformational change. Journal of Immunoassay 1996, 17:353-369.
57. Frillingos S., Wu J., Venkatesan P., Kaback H.R. Binding of ligand or monoclonal antibody 4B1 induces discrete structural changes in the lactose permease of Escherichia coli. Biochemistry 1997, 36:6408-6414.
58. Monaco-Malbet S., Berthet-Colominas C., Novelli A., Battai N., Piga N., Cheynet V., et al. Mutual conformational adaptations in antigen and antibody upon complex formation between an Fab and HIV-1 capsid protein p24. Structure 2000, 8:1069-1077.
59. Ulrichts H., Harsfalvi J., Bene L., Matko J., Vermylen J., Ajzenberg N., et al. A monoclonal antibody directed against human von Willebrand factor induces type 2B-like alterations. Journal of Thrombosis and Haemostasis 2004, 2:1622-1628.
60. Ganesan R., Eigenbrot C., Kirchhofer D. Structural and mechanistic insight into how antibodies inhibit serine proteases. Biochemical Journal 2010, 430:179-189.
61. Kitamura H., Shindo K., Sasabe M., Matsuura E., Sakairi N., Nishi N. Conformational change of DNA on the formation of DNA-anti-DNA antibody immune complex. Nucleic Acids Symposium Series 1997, 14:5-6.
62. Lazear E., Whitbeck J.C., Ponce-de-Leon M., Cairns T.M., Willis S.H., Zuo Y., et al. Antibody-induced conformational changes in herpes simplex virus glycoprotein gD reveal new targets for virus neutralization. Journal of Virology 2012, 86:1563-1576.
63. Cha K., Reeves P.J., Khorana H.G. Structure and function in rhodopsin: destabilization of rhodopsin by the binding of an antibody at the N-terminal segment provides support for involvement of the latter in an intradiscal tertiary structure. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:3016-3021.
64. Hernandez R., Paredes A., Brown D.T. Sindbis virus conformational changes induced by a neutralizing anti-E1 monoclonal antibody. Journal of Virology 2008, 82:5750-5760.
65. Hato T., Watanabe A., Nakatani S., Minamoto Y., Fujita S. A novel mechanism for exposure of fibrinogen binding sites on GPIIb-IIIa by a monoclonal antibody. Thrombosis and Haemostasis 1995, 73:138-143.
66. Verhamme I., Kvassman J.O., Day D., Debrock S., Vleugels N., Declerck P.J., et al. Accelerated conversion of human plasminogen activator inhibitor-1 to its latent form by antibody binding. Journal of Biological Chemistry 1999, 274:17511-17517.
67. Flynn D.C., Olmsted R.A., Mackenzie J.M., Johnston R.E. Antibody-mediated activation of Sindbis virus. Virology 1988, 166:82-90.
68. Ros C., Gerber M., Kempf C. Conformational changes in the VP1-unique region of native human parvovirus B19 lead to exposure of internal sequences that play a role in virus neutralization and infectivity. Journal of Virology 2006, 80:12017-12024.
69. Paredes A.M., Ferreira D., Horton M., Saad A., Tsuruta H., Johnston R., et al. Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virology 2004, 324:373-386.
70. Lu C., Shimaoka M., Zang Q., Takagi J., Springer T.A. Locking in alternate conformations of the integrin alphaLbeta2 I domain with disulfide bonds reveals functional relationships among integrin domains. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:2393-2398.
71. Gilmore A.P., Metcalfe A.D., Romer L.H., Streuli C.H. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. Journal of Cell Biology 2000, 149:431-446.
72. Takagi J., Isobe T., Takada Y., Saito Y. Structural interlock between ligand-binding site and stalk-like region of beta1 integrin revealed by a monoclonal antibody recognizing conformation-dependent epitope. Journal of Biochemistry 1997, 121:914-921.
73. Ugarova T.P., Ljubimov A.V., Deng L., Plow E.F. Proteolysis regulates exposure of the IIICS-1 adhesive sequence in plasma fibronectin. Biochemistry 1996, 35:10913-10921.
74. Higazi A.A., Upson R.H., Cohen R.L., Manuppello J., Bognacki J., Henkin J., et al. Interaction of single-chain urokinase with its receptor induces the appearance and disappearance of binding epitopes within the resultant complex for other cell surface proteins. Blood 1996, 88:542-551.
75. Honda S., Tomiyama Y., Pelletier A.J., Annis D., Honda Y., Orchekowski R., et al. Topography of ligand-induced binding sites, including a novel cation-sensitive epitope (AP5) at the amino terminus, of the human integrin beta 3 subunit. Journal of Biological Chemistry 1995, 270:11947-11954.
76. Ugarova T.P., Zamarron C., Veklich Y., Bowditch R.D., Ginsberg M.H., Weisel J.W., et al. Conformational transitions in the cell binding domain of fibronectin. Biochemistry 1995, 34:4457-4466.
77. Niewiarowska J., Cierniewski C.S. GPIIIa(90-102) and GPIIIa(631-653) epitopes as markers of conformational changes occurring during the activation of the glycoprotein IIb/IIIa complex. European Journal of Biochemistry/FEBS 1994, 224:803-809.
78. Di Simone C., Buchmeier M.J. Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 1995, 209:3-9.
79. Meyer W.J., Gidwitz S., Ayers V.K., Schoepp R.J., Johnston R.E. Conformational alteration of Sindbis virion glycoproteins induced by heat, reducing agents, or low pH. Journal of Virology 1992, 66:3504-3513.
80. Geng J.G., Moore K.L., Johnson A.E., McEver R.P. Neutrophil recognition requires a Ca(2+)-induced conformational change in the lectin domain of GMP-140. Journal of Biological Chemistry 1991, 266:22313-22318.
81. Flynn D.C., Meyer W.J., Mackenzie J.M., Johnston R.E. A conformational change in Sindbis virus glycoproteins E1 and E2 is detected at the plasma membrane as a consequence of early virus-cell interaction. Journal of Virology 1990, 64:3643-3653.
82. Nilsson B., Nilsson Ekdahl K., Avila D., Nilsson U.R., Lambris J.D. Neoantigens in complement component C3 as detected by monoclonal antibodies. Mapping of the recognized epitopes by synthetic peptides. Biochemical Journal 1990, 268:55-61.
83. Strandberg K., Kjellberg M., Erb E.M., Persson U., Mosher D.F., Villoutreix B.O., et al. Activated protein C-protein C inhibitor complex formation: characterization of a neoepitope provides evidence for extensive insertion of the reactive center loop. Biochemistry 2000, 39:15713-15720.
84. Saunders D.N., Buttigieg K.M., Gould A., McPhun V., Baker M.S. Immunological detection of conformational neoepitopes associated with the serpin activity of plasminogen activator inhibitor type-2. Journal of Biological Chemistry 1998, 273:10965-10971.
85. Medved L., Tsurupa G., Yakovlev S. Conformational changes upon conversion of fibrinogen into fibrin. The mechanisms of exposure of cryptic sites. Annals of the New York Academy of Sciences 2001, 936:185-204.
86. Li J., Smolyar A., Sunder-Plassmann R., Reinherz E.L. Ligand-induced conformational change within the CD2 ectodomain accompanies receptor clustering: implication for molecular lattice formation. Journal of Molecular Biology 1996, 263:209-226.
87. de Gasparo M.M., Wood J.M., Heusser C.H. Mechanism of inhibition of human renin by monoclonal antibodies. Hypertension 1988, 11:209-216.
88. Elemer G.S., Edgington T.S. Monoclonal antibody to an activation neoepitope of alpha M beta 2 inhibits multiple alpha M beta 2 functions. Journal of Immunology 1994, 152:5836-5844.
89. Joyner A.S., Willis J.R., Crowe J.E., Aiken C. Maturation-induced cloaking of neutralization epitopes on HIV-1 particles. PLoS Pathogens 2011, 7:e1002234.
90. Gray L., Sterjovski J., Ramsland P.A., Churchill M.J., Gorry P.R. Conformational alterations in the CD4 binding cavity of HIV-1 gp120 influencing gp120-CD4 interactions and fusogenicity of HIV-1 envelopes derived from brain and other tissues. Retrovirology 2011, 8:42.
91. Moscoso C.G., Sun Y., Poon S., Xing L., Kan E., Martin L., et al. Quaternary structures of HIV Env immunogen exhibit conformational vicissitudes and interface diminution elicited by ligand binding. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:6091-6096.
92. Pantophlet R. Antibody epitope exposure and neutralization of HIV-1. Current Pharmaceutical Design 2010, 16:3729-3743.
93. Burastero S.E., Figini M., Frigerio B., Lusso P., Mollica L., Lopalco L. Protective versus pathogenic anti-CD4 immunity: insights from the study of natural resistance to HIV infection. Journal of Translational Medicine 2009, 7:101.
94. Li Q., Yafal A.G., Lee Y.M., Hogle J., Chow M. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. Journal of Virology 1994, 68:3965-3970.
95. Kwong P.D., Doyle M.L., Casper D.J., Cicala C., Leavitt S.A., Majeed S., et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 2002, 420:678-682.
96. Hioe C.E., Visciano M.L., Kumar R., Liu J., Mack E.A., Simon R.E., et al. The use of immune complex vaccines to enhance antibody responses against neutralizing epitopes on HIV-1 envelope gp120. Vaccine 2009, 28:352-360.
97. Kumar R., Visciano M.L., Li H., Hioe C. Targeting a neutralizing epitope of HIV envelope Gp120 by immune complex vaccine. Journal of AIDS & Clinical Research 2012, S8(2):5512.
98. Rhodin N.R., Cutalo J.M., Tomer K.B., McArthur W.P., Brady L.J. Characterization of the Streptococcus mutans P1 epitope recognized by immunomodulatory monoclonal antibody 6-11A. Infection and Immunity 2004, 72:4680-4688.
99. Crowley P.J., Seifert T.B., Isoda R., van Tilburg M., Oli M.W., Robinette R.A., et al. Requirements for surface expression and function of adhesin P1 from Streptococcus mutans. Infection and Immunity 2008, 76:2456-2468.
100. Gross E.L., Beall C.J., Kutsch S.R., Firestone N.D., Leys E.J., Griffen A.L. Beyond Streptococcus mutans: dental caries onset linked to multiple species by 16S rRNA community analysis. PLoS One 2012, 7:e47722.
101. Nyvad B., Crielaard W., Mira A., Takahashi N., Beighton D. Dental caries from a molecular microbiological perspective. Caries Research 2013, 47:89-102.
102. Peterson S.N., Snesrud E., Liu J., Ong A.C., Kilian M., Schork N.J., et al. The dental plaque microbiome in health and disease. PLoS One 2013, 8:e58487.
103. Jakubovics N.S., Stromberg N., van Dolleweerd C.J., Kelly C.G., Jenkinson H.F. Differential binding specificities of oral streptococcal antigen I/II family adhesins for human or bacterial ligands. Molecular Microbiology 2005, 55:1591-1605.
104. Antoniou A.N., Blackwood S.L., Mazzeo D., Watts C. Control of antigen presentation by a single protease cleavage site. Immunity 2000, 12:391-398.