Innocent until proven guilty: Mechanisms and roles of Streptococcus-Candida interactions in oral health and disease

Molecular Oral Microbiology

Volumn 29, Issue 3, 2014, Pages 99-116

  Xu, H ^a   Jenkinson, H F ^b   Dongari Bagtzoglou, A ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Fungal bacterial interactions; Microbial synergy; Mucosal infection; Polymicrobial biofilms

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL PROTEIN; COMPETENCE STIMULATING PEPTIDE; FUNGAL PROTEIN; GLUCAN; LACTIC ACID; PATTERN RECOGNITION RECEPTOR; POLYSACCHARIDE; PROBIOTIC AGENT; PROTEIN CSHA; PROTEIN SSPA; PROTEIN SSPB; SALIVA PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ALPHA HEMOLYTIC STREPTOCOCCUS; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BIOFILM; CANDIDA; CANDIDA ALBICANS; CELL ADHESION; CELL INTERACTION; COMMENSAL; DENTAL CARIES; DENTURE; ENTEROCOCCUS FAECALIS; FUNGAL CELL; FUNGAL COLONIZATION; FUNGAL METABOLISM; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; MEDICAL LITERATURE; MIXED INFECTION; MOLECULAR INTERACTION; MOUTH FLORA; MOUTH INFECTION; MUCOCUTANEOUS CANDIDIASIS; NONHUMAN; OPPORTUNISTIC INFECTION; ORAL MUCOSAL DISEASE; OROPHARYNX CANDIDIASIS; PATHOGENESIS; PERMEABILITY BARRIER; PROTEIN PROTEIN INTERACTION; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STOMATITIS; STREPTOCOCCUS; STREPTOCOCCUS GORDONII; STREPTOCOCCUS INFECTION; STREPTOCOCCUS MUTANS; STREPTOCOCCUS ORALIS; STREPTOCOCCUS PARASANGUINIS; STREPTOCOCCUS SANGUINIS; THRUSH; TOOTH PLAQUE; BACTERIUM ADHERENCE; HEALTH; MICROBIOLOGY; MOUTH DISEASE; ORGANISMAL INTERACTION; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

BACTERIAL ADHESION; CANDIDA ALBICANS; COINFECTION; HUMANS; MICROBIAL INTERACTIONS; MOUTH DISEASES; ORAL HEALTH; STREPTOCOCCUS; VIRULENCE;

EID: 84899480651     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/omi.12049     Document Type: Review

References (136)

1. Aderem, A. and Ulevitch, R.J. (2000) Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
2. Alam, S., Brailsford, S.R., Adams, S. et al. (2000) Genotypic heterogeneity of Streptococcus oralis and distinct aciduric subpopulations in human dental plaque. Appl Environ Microbiol 66: 3330-3336.
3. Alarco, A.M., Marcil, A., Chen, J., Suter, B., Thomas, D. and Whiteway, M. (2004) Immune-deficient Drosophila melanogaster: a model for the innate immune response to human fungal pathogens. J Immunol 172: 5622-5628.
4. Al-Fattani, M.A. and Douglas, L.J. (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55: 999-1008.
5. Andrutis, K.A., Riggle, P.J., Kumamoto, C.A. and Tzipori, S. (2000) Intestinal lesions associated with disseminated candidiasis in an experimental animal model. J Clin Microbiol 38: 2317-2323.
6. Bamford, C.V., d'Mello, A., Nobbs, A.H., Dutton, L.C., Vickerman, M.M. and Jenkinson, H.F. (2009) Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect Immun 77: 3696-3704.
7. Barber, C.E., Tang, J.L., Feng, J.X. et al. (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24: 555-566.
8. Barnard, J.P. and Stinson, M.W. (1996) The alpha-hemolysin of Streptococcus gordonii is hydrogen peroxide. Infect Immun 64: 3853-3857.
9. Biswas, S., Van Dijck, P. and Datta, A. (2007) Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol Mol Biol Rev 71: 348-376.
10. Bowen, W.H., Pearson, S.K. and Young, D.A. (1988) The effect of desalivation on coronal and root surface caries in rats. J Dent Res 67: 21-23.
11. Bowen, W.H., Schilling, K., Giertsen, E. et al. (1991) Role of a cell surface-associated protein in adherence and dental caries. Infect Immun 59: 4606-4609.
12. Burns, E., Bachrach, G., Shapira, L. and Nussbaum, G. (2006) Cutting Edge: TLR2 is required for the innate response to Porphyromonas gingivalis: activation leads to bacterial persistence and TLR2 deficiency attenuates induced alveolar bone resorption. J Immunol 177: 8296-8300.
13. Byers, H.L., Tarelli, E., Homer, K.A. and Beighton, D. (2000) Isolation and characterisation of sialidase from a strain of Streptococcus oralis. J Med Microbiol 49: 235-244.
14. Calderone, R.A. (2002) Candida and Candidiasis. Washington, D.C.: ASM Press.
15. Campos, M.S., Marchini, L., Bernardes, L.A., Paulino, L.C. and Nobrega, F.G. (2008) Biofilm microbial communities of denture stomatitis. Oral Microbiol Immunol 23: 419-424.
16. Chiavolini, D., Pozzi, G. and Ricci, S. (2008) Animal models of Streptococcus pneumoniae disease. Clin Microbiol Rev 21: 666-685.
17. Clarke, T.B., Francella, N., Huegel, A. and Weiser, J.N. (2011) Invasive bacterial pathogens exploit TLR-mediated downregulation of tight junction components to facilitate translocation across the epithelium. Cell Host Microbe 9: 404-414.
18. Clemons, K.V., Gonzalez, G.M., Singh, G. et al. (2006) Development of an orogastrointestinal mucosal model of candidiasis with dissemination to visceral organs. Antimicrob Agents Chemother 50: 2650-2657.
19. Cosseau, C., Devine, D.A., Dullaghan, E. et al. (2008) The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun 76: 4163-4175.
20. Cotter, G., Doyle, S. and Kavanagh, K. (2000) Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol Med Microbiol 27: 163-169.
21. Daep, C.A., Novak, E.A., Lamont, R.J. and Demuth, D.R. (2011) Structural dissection and in vivo effectiveness of a peptide inhibitor of Porphyromonas gingivalis adherence to Streptococcus gordonii. Infect Immun 79: 67-74.
22. Diaz, P.I., Dupuy, A.K., Abusleme, L. et al. (2012a) Using high throughput sequencing to explore the biodiversity in oral bacterial communities. Mol Oral Microbiol 27: 182-201.
23. Diaz, P.I., Xie, Z., Sobue, T. et al. (2012b) Synergistic interaction between Candida albicans and commensal oral streptococci in a novel in vitro mucosal model. Infect Immun 80: 620-632.
24. Dongari-Bagtzoglou, A., Kashleva, H., Dwivedi, P., Diaz, P. and Vasilakos, J. (2009) Characterization of mucosal Candida albicans biofilms. PLoS ONE 4: e7967.
25. Dow, J.M., Crossman, L., Findlay, K., He, Y.Q., Feng, J.X. and Tang, J.L. (2003) Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A 100: 10995-11000.
26. Duan, K., Dammel, C., Stein, J., Rabin, H. and Surette, M.G. (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50: 1477-1491.
27. Dwivedi, P., Thompson, A., Xie, Z. et al. (2011) Role of Bcr1-activated genes Hwp1 and Hyr1 in Candida albicans oral mucosal biofilms and neutrophil evasion. PLoS ONE 6: e16218.
28. Ebanks, R.O., Chisholm, K., McKinnon, S., Whiteway, M. and Pinto, D.M. (2006) Proteomic analysis of Candida albicans yeast and hyphal cell wall and associated proteins. Proteomics 6: 2147-2156.
29. Elliott, D., Harrison, E., Handley, P.S. et al. (2003) Prevalence of Csh-like fibrillar surface proteins among mitis group oral streptococci. Oral Microbiol Immunol 18: 114-120.
30. Falk, P.G., Hooper, L.V., Midtvedt, T. and Gordon, J.I. (1998) Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev 62: 1157-1170.
31. Filler, S.G., Crislip, M.A., Mayer, C.L. and Edwards, J.E. Jr (1991) Comparison of fluconazole and amphotericin B for treatment of disseminated candidiasis and endophthalmitis in rabbits. Antimicrob Agents Chemother 35: 288-292.
32. Fonzi, W.A. (1999) PHR1 and PHR2 of Candida albicans encode putative glycosidases required for proper cross-linking of β-1, 3- and β-1, 6-glucans. J Bacteriol 181: 7070-7079.
33. Fransen, J., Van Cutsem, J., Vandesteene, R. and Janssen, P.A. (1984) Histopathology of experimental systemic candidosis in guinea-pigs. Sabouraudia 22: 455-469.
34. Frandsen, E.V., Pedrazzoli, V. and Kilian, M. (1991) Ecology of viridans streptococci in the oral cavity and pharynx. Oral Microbiol Immunol 6: 129-133.
35. Gale, D. and Sandoval, B. (1957) Response of mice to the inoculations of both Candida albicans and Escherichia coli I. The enhancement phenomenon. J Bacteriol 73: 616-624.
36. Gibbons, R.J. (1989) Bacterial adhesion to oral tissues: a model for infectious diseases. J Dent Res 68: 750-760.
37. Gopal, P.K., Shepherd, M.G. and Sullivan, P.A. (1984) Analysis of wall glucans from yeast, hyphal and germ-tube forming cells of Candida albicans. J Gen Microbiol 130: 3295-3301.
38. Gow, N.A. and Hube, B. (2012) Importance of the Candida albicans cell wall during commensalism and infection. Curr Opin Microbiol 15: 406-412.
39. Gregoire, S., Xiao, J., Silva, B.B. et al. (2011) Role of glucosyltransferase B in interactions of Candida albicans with Streptococcus mutans and with an experimental pellicle on hydroxyapatite surfaces. Appl Environ Microbiol 77: 6357-6367.
40. de Groot, P.W., Bader, O., de Boer, A.D., Weig, M. and Chauhan, N. (2013) Adhesins in human fungal pathogens: glue with plenty of stick. Eukaryot Cell 12: 470-481.
41. Hajishengallis, G., Liang, S., Payne, M.A. et al. (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10: 497-506.
42. Hamamoto, H., Kurokawa, K., Kaito, C. et al. (2004) Quantitative evaluation of the therapeutic effects of antibiotics using silkworms infected with human pathogenic microorganisms. Antimicrob Agents Chemother 48: 774-779.
43. Hanaoka, N., Takano, Y., Shibuya, K., Fugo, H., Uehara, Y. and Niimi, M. (2008) Identification of the putative protein phosphatase gene PTC1 as a virulence-related gene using a silkworm model of Candida albicans infection. Eukaryot Cell 7: 1640-1648.
44. Heo, S.M., Sung, R.S., Scannapieco, F.A. and Haase, E.M. (2011) Genetic relationships between Candida albicans strains isolated from dental plaque, trachea, and bronchoalveolar lavage fluid from mechanically ventilated intensive care unit patients. J Oral Microbiol 3: 6332. DOI: 10.3402/jom.v3i0.6362.
45. Holmes, A.R., McNab, R. and Jenkinson, H.F. (1996) Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect Immun 64: 4680-4685.
46. Hornby, J.M., Jensen, E.C., Lisec, A.D. et al. (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67: 2982-2992.
47. Hoshino, T., Fujiwara, T. and Kilian, M. (2005) Use of phylogenetic and phenotypic analyses to identify nonhemolytic streptococci isolated from bacteremic patients. J Clin Microbiol 43: 6073-6085.
48. Hsu, L.Y., Minah, G.E., Peterson, D.E. et al. (1990) Coaggregation of oral Candida isolates with bacteria from bone marrow transplant recipients. J Clin Microbiol 28: 2621-2626.
49. Ishijima, S.A., Hayama, K., Burton, J.P. et al. (2012) Effect of Streptococcus salivarius K12 on the in vitro growth of Candida albicans and its protective effect in an oral candidiasis model. Appl Environ Microbiol 78: 2190-2199.
50. Jakubovics, N.S. and Kolenbrander, P.E. (2010) The road to ruin: the formation of disease-associated oral biofilms. Oral Dis 16: 729-739.
51. Jamieson, A.M., Yu, S., Annicelli, C.H. and Medzhitov, R. (2010) Influenza virus-induced glucocorticoids compromise innate host defense against a secondary bacterial infection. Cell Host Microbe 7: 103-114.
52. Jarosz, L.M., Deng, D.M., van der Mei, H.C., Crielaard, W. and Krom, B.P. (2009) Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. Eukaryot Cell 8: 1658-1664.
53. Jenkinson, H.F. and Demuth, D.R. (1997) Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol Microbiol 23: 183-190.
54. Jenkinson, H.F., Lala, H.C. and Shepherd, M.G. (1990) Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans. Infect Immun 58: 1429-1436.
55. Jergens, A.E., Wilson-Welder, J.H., Dorn, A. et al. (2007) Helicobacter bilis triggers persistent immune reactivity to antigens derived from the commensal bacteria in gnotobiotic C3H/HeN mice. Gut 56: 934-940.
56. Johnson, C.C., Yu, A., Lee, H., Fidel, P.L. Jr and Noverr, M.C. (2012) Development of a contemporary animal model of Candida albicans-associated denture stomatitis using a novel intraoral denture system. Infect Immun 80: 1736-1743.
57. Johnston, C., Hinds, J., Smith, A., van der Linden, M., Van Eldere, J. and Mitchell, T.J. (2010) Detection of large numbers of pneumococcal virulence genes in streptococci of the mitis group. J Clin Microbiol 48: 2762-2769.
58. Kash, J.C., Walters, K.A., Davis, A.S. et al. (2011) Lethal synergism of 2009 pandemic H1N1 influenza virus and Streptococcus pneumoniae coinfection is associated with loss of murine lung repair responses. MBio 2: e00172-11. DOI: 10.1128/mBio.00172-11.
59. Katz, J., Yang, Q.B., Zhang, P. et al. (2002) Hydrolysis of epithelial junctional proteins by Porphyromonas gingivalis gingipains. Infect Immun 70: 2512-2518.
60. Kawamura, Y., Hou, X.G., Sultana, F., Miura, H. and Ezaki, T. (1995) Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int J Syst Bacteriol 45: 406-408.
61. Khan, S.A. and Wingard, J.R. (2001) Infection and mucosal injury in cancer treatment. J Natl Cancer Inst Monogr 3: 1-36.
62. Klotz, S.A., Gaur, N.K., De Armond, R. et al. (2007) Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Med Mycol 45: 363-370.
63. Knapp, S., Wieland, C.W., van 't Veer, C. et al. (2004) Toll-like receptor 2 plays a role in the early inflammatory response to murine pneumococcal pneumonia but does not contribute to antibacterial defense. J Immunol 172: 3132-3138.
64. Koh, A.Y., Kohler, J.R., Coggshall, K.T., Van Rooijen, N. and Pier, G.B. (2008) Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog 4: e35.
65. Kolenbrander, P.E., Andersen, R.N., Blehert, D.S., Egland, P.G., Foster, J.S. and Palmer, R.J. Jr (2002) Communication among oral bacteria. Microbiol Mol Biol Rev 66: 486-505, table of contents.
66. Koo, H., Hayacibara, M.F., Schobel, B.D. et al. (2003) Inhibition of Streptococcus mutans biofilm accumulation and polysaccharide production by apigenin and tt-farnesol. J Antimicrob Chemother 52: 782-789.
67. Kuramitsu, H.K., He, X., Lux, R., Anderson, M.H. and Shi, W. (2007) Interspecies interactions within oral microbial communities. Microbiol Mol Biol Rev 71: 653-670.
68. Leigh, J.E., Shetty, K. and Fidel, P.L. Jr (2004) Oral opportunistic infections in HIV-positive individuals: review and role of mucosal immunity. AIDS patient care STDs 18: 443-456.
69. Liljemark, W.F. and Gibbons, R.J. (1973) Suppression of Candida albicans by human oral streptococci in gnotobiotic mice. Infect Immun 8: 846-849.
70. Lim, J.H., Ha, U., Sakai, A. et al. (2008) Streptococcus pneumoniae synergizes with nontypeable Haemophilus influenzae to induce inflammation via upregulating TLR2. BMC Immunol 9: 40.
71. Liu, Y. and Filler, S.G. (2011) Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot Cell 10: 168-173.
72. Lo, H.J., Kohler, J.R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A. and Fink, G.R. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
73. Loach, D.M., Jenkinson, H.F. and Tannock, G.W. (1994) Colonization of the murine oral cavity by Streptococcus gordonii. Infect Immun 62: 2129-2131.
74. MacCallum, D.M. (2012) Hosting infection: experimental models to assay Candida virulence. Int J Microbiol 2012: 363764.
75. MacCallum, D.M. and Odds, F.C. (2005) Temporal events in the intravenous challenge model for experimental Candida albicans infections in female mice. Mycoses 48: 151-161.
76. Maeda, Y., Elborn, J.S., Parkins, M.D. et al. (2011) Population structure and characterization of viridans group streptococci (VGS) including Streptococcus pneumoniae isolated from adult patients with cystic fibrosis (CF). J Cyst Fibros 10: 133-139.
77. Mason, K.L., Downward, J.R., Mason, K.D. et al. (2012) Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun 80: 3371-3380.
78. McNab, R. and Jenkinson, H.F. (1992) Gene disruption identifies a 290 kDa cell-surface polypeptide conferring hydrophobicity and coaggregation properties in Streptococcus gordonii. Mol Microbiol 6: 2939-2949.
79. McNab, R., Forbes, H., Handley, P.S., Loach, D.M., Tannock, G.W. and Jenkinson, H.F. (1999) Cell wall-anchored CshA polypeptide (259 kilodaltons) in Streptococcus gordonii forms surface fibrils that confer hydrophobic and adhesive properties. J Bacteriol 181: 3087-3095.
80. McNab, R., Ford, S.K., El-Sabaeny, A., Barbieri, B., Cook, G.S. and Lamont, R.J. (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185: 274-284.
81. Meeker, N.D. and Trede, N.S. (2008) Immunology and zebrafish: spawning new models of human disease. Dev Comp Immunol 32: 745-757.
82. Miller, M.B. and Bassler, B.L. (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
83. Monif, G.R. and Carson, H.J. (1998) Female genital tract bacterial coisolates with Candida albicans in patients without clinical vaginitis. Infect Dis Obstet Gynecol 6: 52-56.
84. Moore, W.E., Holdeman, L.V., Smibert, R.M. et al. (1982) Bacteriology of experimental gingivitis in young adult humans. Infect Immun 38: 651-667.
85. Morgan, P.J., Hyman, S.C., Byron, O., Andrew, P.W., Mitchell, T.J. and Rowe, A.J. (1994) Modeling the bacterial protein toxin, pneumolysin, in its monomeric and oligomeric form. J Biol Chem 269: 25315-25320.
86. Muhlschlegel, F.A. and Fonzi, W.A. (1997) PHR2 of Candida albicans encodes a functional homolog of the pH-regulated gene PHR1 with an inverted pattern of pH-dependent expression. Mol Cell Biol 17: 5960-5967.
87. Nasution, O., Srinivasa, K., Kim, M. et al. (2008) Hydrogen peroxide induces hyphal differentiation in Candida albicans. Eukaryot Cell 7: 2008-2011.
88. Nett, J.E., Marchillo, K., Spiegel, C.A. and Andes, D.R. (2010) Development and validation of an in vivo Candida albicans biofilm denture model. Infect Immun 78: 3650-3659.
89. Nobbs, A.H., Lamont, R.J. and Jenkinson, H.F. (2009) Streptococcus adherence and colonization. Microbiol Mol Biol Rev 73: 407-450, Table of Contents.
90. Nobbs, A.H., Vickerman, M.M. and Jenkinson, H.F. (2010) Heterologous expression of Candida albicans cell wall-associated adhesins in Saccharomyces cerevisiae reveals differential specificities in adherence and biofilm formation and in binding oral Streptococcus gordonii. Eukaryot Cell 9: 1622-1634.
91. Nobile, C.J., Fox, E.P., Nett, J.E. et al. (2012) A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126-138.
92. Odds, F.C. (1988) Activity of cilofungin (LY121019) against Candida species in vitro. J Antimicrob Chemother 22: 891-897.
93. Okamoto-Shibayama, K., Sato, Y., Yamamoto, Y., Ohta, K. and Kizaki, H. (2006) Identification of a glucan-binding protein C gene homologue in Streptococcus macacae. Oral Microbiol Immunol 21: 32-41.
94. Parnanen, P., Meurman, J.H., Samaranayake, L. and Virtanen, I. (2010) Human oral keratinocyte E-cadherin degradation by Candida albicans and Candida glabrata. J Oral Pathol Med 39: 275-278.
95. Pestova, E.V., Havarstein, L.S. and Morrison, D.A. (1996) Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a two-component regulatory system. Mol Microbiol 21: 853-862.
96. Peters, B.M. and Noverr, M.C. (2013) Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infect Immun 81: 2178-2189.
97. Peters, B.M., Jabra-Rizk, M.A., Scheper, M.A., Leid, J.G., Costerton, J.W. and Shirtliff, M.E. (2010) Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59: 493-503.
98. Pukkila-Worley, R., Peleg, A.Y., Tampakakis, E. and Mylonakis, E. (2009) Candida albicans hyphal formation and virulence assessed using a Caenorhabditis elegans infection model. Eukaryot Cell 8: 1750-1758.
99. Raja, M., Hannan, A. and Ali, K. (2010) Association of oral candidal carriage with dental caries in children. Caries Res 44: 272-276.
100. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. and Medzhitov, R. (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
101. Ramsey, M.M. and Whiteley, M. (2009) Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc Natl Acad Sci U S A 106: 1578-1583.
102. Ramsey, M.M., Rumbaugh, K.P. and Whiteley, M. (2011) Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog 7: e1002012.
103. Ratner, A.J., Lysenko, E.S., Paul, M.N. and Weiser, J.N. (2005) Synergistic proinflammatory responses induced by polymicrobial colonization of epithelial surfaces. Proc Natl Acad Sci U S A 102: 3429-3434.
104. Reichmann, P., Nuhn, M., Denapaite, D. et al. (2011) Genome of Streptococcus oralis strain Uo5. J Bacteriol 193: 2888-2889.
105. Ricker, A., Vikerman, M.M. and Dongari-Bagtzoglou, A. (2014) S. gordonii glucosyltransferase promoters biofilm interactions with C. albicans. J Oral Microbiol 6. doi: 10.3402/jom.v6.23419. eCollection 2014.
106. Ryan, R.P., Fouhy, Y., Garcia, B.F. et al. (2008) Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68: 75-86.
107. Saporito-Irwin, S.M., Birse, C.E., Sypherd, P.S. and Fonzi, W.A. (1995) PHR1, a pH-regulated gene of Candida albicans, is required for morphogenesis. Mol Cell Biol 15: 601-613.
108. Shah, D.S. and Russell, R.R. (2004) A novel glucan-binding protein with lipase activity from the oral pathogen Streptococcus mutans. Microbiology 150: 1947-1956.
109. Sibley, C.D., Duan, K., Fischer, C. et al. (2008a) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4: e1000184.
110. Sibley, C.D., Parkins, M.D., Rabin, H.R., Duan, K., Norgaard, J.C. and Surette, M.G. (2008b) A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci U S A 105: 15070-15075.
111. Silverman, R.J., Nobbs, A.H., Vickerman, M.M., Barbour, M.E. and Jenkinson, H.F. (2010) Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun 78: 4644-4652.
112. Solis, N.V. and Filler, S.G. (2012) Mouse model of oropharyngeal candidiasis. Nat Protoc 7: 637-642.
113. Steele, C., Ratterree, M. and Fidel, P.L. Jr (1999) Differential susceptibility of two species of macaques to experimental vaginal candidiasis. J Infect Dis 180: 802-810.
114. Sudbery, P.E. (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9: 737-748.
115. Syed, S.A. and Loesche, W.J. (1978) Bacteriology of human experimental gingivitis: effect of plaque age. Infect Immun 21: 821-829.
116. Tanzer, J.M., Baranowski, L.K., Rogers, J.D., Haase, E.M. and Scannapieco, F.A. (2001) Oral colonization and cariogenicity of Streptococcus gordonii in specific pathogen-free TAN:SPFOM(OM)BR rats consuming starch or sucrose diets. Arch Oral Biol 46: 323-333.
117. Uppuluri, P., Mekala, S. and Chaffin, W.L. (2007) Farnesol-mediated inhibition of Candida albicans yeast growth and rescue by a diacylglycerol analogue. Yeast 24: 681-693.
118. Vendeville, A., Winzer, K., Heurlier, K., Tang, C.M. and Hardie, K.R. (2005) Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Microbiol 3: 383-396.
119. Vickerman, M.M., Iobst, S., Jesionowski, A.M. and Gill, S.R. (2007) Genome-wide transcriptional changes in Streptococcus gordonii in response to competence signaling peptide. J Bacteriol 189: 7799-7807.
120. Vilchez, R., Lemme, A., Ballhausen, B. et al. (2010) Streptococcus mutans inhibits Candida albicans hyphal formation by the fatty acid signaling molecule trans-2-decenoic acid (SDSF). ChemBioChem 11: 1552-1562.
121. Villar, C.C. and Dongari-Bagtzoglou, A. (2008) Immune defence mechanisms and immunoenhancement strategies in oropharyngeal candidiasis. Expert Rev Mol Med 10: e29.
122. Villar, C.C., Kashleva, H., Nobile, C.J., Mitchell, A.P. and Dongari-Bagtzoglou, A. (2007) Mucosal tissue invasion by Candida albicans is associated with E-cadherin degradation, mediated by transcription factor Rim101p and protease Sap5p. Infect Immun 75: 2126-2135.
123. Vylkova, S., Carman, A.J., Danhof, H.A., Collette, J.R., Zhou, H. and Lorenz, M.C. (2011) The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio 2: e00055-00011.
124. Wade, W.G. (2013) The oral microbiome in health and disease. Pharmacol Res 69: 137-143.
125. Whatmore, A.M., Efstratiou, A., Pickerill, A.P. et al. (2000) Genetic relationships between clinical isolates of Streptococcus pneumoniae, Streptococcus oralis, and Streptococcus mitis: characterization of "Atypical" pneumococci and organisms allied to S. mitis harboring S. pneumoniae virulence factor-encoding genes. Infect Immun 68: 1374-1382.
126. Whitmore, S.E. and Lamont, R.J. (2011) The pathogenic persona of community-associated oral streptococci. Mol Microbiol 81: 305-314.
127. Wilkieson, C., Samaranayake, L.P., MacFarlane, T.W., Lamey, P.J. and MacKenzie, D. (1991) Oral candidosis in the elderly in long term hospital care. J Oral Pathol Med 20: 13-16.
128. Wright, C.J., Burns, L.H., Jack, A.A. et al. (2013) Microbial interactions in building of communities. Mol Oral Microbiol 28: 83-101.
129. Wu, H., Downs, D., Ghosh, K. et al. (2013) Candida albicans secreted aspartic proteases 4-6 induce apoptosis of epithelial cells by a novel Trojan horse mechanism. FASEB 27: 2132-2144.
130. Xu, H., Nobile, C.J. and Dongari-Bagtzoglou, A. (2013a) Glucanase induces filamentation of the fungal pathogen Candida albicans. PLoS ONE 8: e63736.
131. Xu, H., Sobue, T., Thompson, A. et al. (2013b) Streptococcal co-infection augments Candida pathogenicity by amplifying the mucosal inflammatory response. Cell Microbiol 16: 214-231.
132. Yokoyama, T., Sasaki, J., Matsumoto, K. et al. (2011) A necrotic lung ball caused by co-infection with Candida and Streptococcus pneumoniae. Infect Drug Resist 4: 221-224.
133. Yoshida, Y., Palmer, R.J., Yang, J., Kolenbrander, P.E. and Cisar, J.O. (2006) Streptococcal receptor polysaccharides: recognition molecules for oral biofilm formation. BMC Oral Health 6(Suppl 1): S12.
134. Zhang, S., Li, J., Jia, X. and Wu, Y. (2004) The expression of toll-like receptor 2 and 4 mRNA in local tissues of model of oropharyngeal candidiasis in mice. J Huazhong Univ Sci Technolog Med Sci 24: 639-641.
135. Zhu, W. and Filler, S.G. (2010) Interactions of Candida albicans with epithelial cells. Cell Microbiol 12: 273-282.
136. Zijnge, V., van Leeuwen, M.B., Degener, J.E. et al. (2010) Oral biofilm architecture on natural teeth. PLoS ONE 5: e9321.