Streptococcal co-infection augments candida pathogenicity by amplifying the mucosal inflammatory response

Cellular Microbiology

Volumn 16, Issue 2, 2014, Pages 214-231

  Xu, H ^a   Sobue, T ^a   Thompson, A ^a   Xie, Z ^a   Poon, K ^b   Ricker, A ^a   Cervantes, J ^a   Diaz, P I ^a   Dongari Bagtzoglou, A ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b Phalanx Biotech   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TOLL LIKE RECEPTOR 2; TLR2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; CANDIDA ALBICANS; CONTROLLED STUDY; FEMALE; FUNGAL VIRULENCE; GASTROINTESTINAL TRACT; GENOME; IN VITRO STUDY; INFLAMMATION; MICROARRAY ANALYSIS; MIXED INFECTION; MOUSE; MOUTH LESION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS GORDONII; STREPTOCOCCUS INFECTION; STREPTOCOCCUS ORALIS; THRUSH; TONGUE; ANIMAL; COMPLICATION; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION PROFILING; IMMUNOLOGY; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; MICROBIOLOGY; MUCOSA; NEUTROPHIL; OROPHARYNX; PATHOLOGY;

ANIMALIA; CANDIDA; MURINAE; STREPTOCOCCUS ORALIS;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS, ORAL; COINFECTION; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; INFLAMMATION; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MUCOUS MEMBRANE; NEUTROPHILS; OROPHARYNX; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS ORALIS; TOLL-LIKE RECEPTOR 2; TONGUE;

EID: 84892478656     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12216     Document Type: Article

References (72)

1. Aas, J.A., Paster, B.J., Stokes, L.N., Olsen, I., and Dewhirst, F.E. (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43: 5721-5732.
2. Aderem, A., and Ulevitch, R.J. (2000) Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
3. Alam, S., Brailsford, S.R., Adams, S., Allison, C., Sheehy, E., Zoitopoulos, L., etal. (2000) Genotypic heterogeneity of Streptococcus oralis and distinct aciduric subpopulations in human dental plaque. Appl Environ Microbiol 66: 3330-3336.
4. 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.
5. Barrett, A.P. (1989) Recognition and management of invasive pharyngeal candidiasis in acute leukemia. Oral Surg Oral Med Oral Pathol 67: 275-278.
6. Beisswenger, C., Lysenko, E.S., and Weiser, J.N. (2009) Early bacterial colonization induces toll-like receptor-dependent transforming growth factor beta signaling in the epithelium. Infect Immun 77: 2212-2220.
7. Bradley, P.P., Priebat, D.A., Christensen, R.D., and Rothstein, G. (1982) Measurement of cutaneaous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78: 206-209.
8. 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.
9. 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.
10. Conti, H.R., Shen, F., Nayyar, N., Stocum, E., Sun, J.N., Lindemann, M.J., etal. (2009) Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 206: 299-311.
11. Daley, J.M., Thomay, A.A., Connolly, M.D., Reichner, J.S., and Albina, J.E. (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64-70.
12. Dessing, M.C., Florquin, S., Paton, J.C., and van der Poll, T. (2008) Toll-like receptor 2 contributes to antibacterial defence against pneumolysin-deficient pneumococci. Cell Microbiol 10: 237-246.
13. Dewhirst, F.E., Chen, T., Izard, J., Paster, B.J., Tanner, A.C., Yu, W.H., etal. (2010) The human oral microbiome. J Bacteriol 192: 5002-5017.
14. Diaz, P.I., Xie, Z., Sobue, T., Thompson, A., Biyikoglu, B., Ricker, A., etal. (2012a) Synergistic interaction between Candida albicans and commensal oral streptococci in a novel in vitro mucosal model. Infect Immun 80: 620-632.
15. Diaz, P.I., Dupuy, A.K., Abusleme, L., Reese, B., Obergfell, C., Choquette, L., etal. (2012b) Using high throughput sequencing to explore the biodiversity in oral bacterial communities. Mol Oral Microbiol 27: 182-201.
16. Dongari-Bagtzoglou, A., Villar, C.C., and Kashleva, H. (2005) Candida albicans-infected oral epithelial cells augment the anti-fungal activity of human neutrophils in vitro. Med Mycol 43: 545-549.
17. Dongari-Bagtzoglou, A., Kashleva, H., Dwivedi, P., Diaz, P., and Vasilakos, J. (2009) Characterization of mucosal Candida albicans biofilms. PLoS ONE 4: e7967.
18. Dwivedi, P., Thompson, A., Xie, Z., Kashleva, H., Ganguly, S., Mitchell, A.P., and Dongari-Bagtzoglou, A. (2011) Role of Bcr1-activated genes Hwp1 and Hyr1 in Candida albicans oral mucosal biofilms and neutrophil evasion. PLoS ONE 6: e16218.
19. Fujiwara, T., Hoshino, T., Ooshima, T., Sobue, S., and Hamada, S. (2000) Purification, characterization, and molecular analysis of the gene encoding glucosyltransferase from Streptococcus oralis. Infect Immun 68: 2475-2483.
20. Geiss, G.K., Bumgarner, R.E., Birditt, B., Dahl, T., Dowidar, N., Dunaway, D.L., etal. (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26: 317-325.
21. Gillum, A.M., Tsay, E.Y., and Kirsch, D.R. (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179-182.
22. Gligorov, J., Bastit, L., Gervais, H., Henni, M., Kahila, W., Lepille, D., etal. (2011) Prevalence and treatment management of oropharyngeal candidiasis in cancer patients: results of the French CANDIDOSCOPE study. Int J Radiat Oncol Biol Phys 80: 532-539.
23. Grunwald, J.E., Daniel, E., Ying, G.S., Pistilli, M., Maguire, M.G., Alexander, J., etal. (2012) Photographic assessment of baseline fundus morphologic features in the comparison of age-related macular degeneration treatments trials. Ophthalmology 119: 1634-1641.
24. Hajishengallis, G., Liang, S., Payne, M.A., Hashim, A., Jotwani, R., Eskan, M.A., etal. (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10: 497-506.
25. Hillegas, L.M., Griswold, D.E., Brickson, B., and Albrightson-Winslow, C. (1990) Assessment of myeloperoxidase activity in whole rat kidney. J Pharmacol Methods 24: 285-295.
26. 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.
27. Jergens, A.E., Wilson-Welder, J.H., Dorn, A., Henderson, A., Liu, Z., Evans, R.B., etal. (2007) Helicobacter bilis triggers persistent immune reactivity to antigens derived from the commensal bacteria in gnotobiotic C3H/HeN mice. Gut 56: 934-940.
28. 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.
29. Khan, S.A., and Wingard, J.R. (2001) Infection and mucosal injury in cancer treatment. J Natl Cancer Inst Monogr 29: 31-36.
30. Knapp, S., Wieland, C.W., van 't Veer, C., Takeuchi, O., Akira, S., Florquin, S., and van der Poll, T. (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.
31. Krause, R., Schwab, E., Bachhiesl, D., Daxbock, F., Wenisch, C., Krejs, G.J., and Reisinger, E.C. (2001) Role of Candida in antibiotic-associated diarrhea. J Infect Dis 184: 1065-1069.
32. Kulkarni, S., Sitaru, C., Jakus, Z., Anderson, K.E., Damoulakis, G., Davidson, K., etal. (2011) PI3Kbeta plays a critical role in neutrophil activation by immune complexes. Sci Signal 4: ra23.
33. Liljemark, W.F., and Gibbons, R.J. (1973) Suppression of Candida albicans by human oral streptococci in gnotobiotic mice. Infect Immun 8: 846-849.
34. Maeda, Y., Elborn, J.S., Parkins, M.D., Reihill, J., Goldsmith, C.E., Coulter, W.A., etal. (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.
35. Moore, W.E., Holdeman, L.V., Smibert, R.M., Hash, D.E., Burmeister, J.A., and Ranney, R.R. (1982) Bacteriology of severe periodontitis in young adult humans. Infect Immun 38: 1137-1148.
36. Morales, D.K., and Hogan, D.A. (2010) Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathog 6: e1000886.
37. Moyes, D.L., and Naglik, J.R. (2011) Mucosal immunity and Candida albicans infection. Clin Dev Immunol 2011: 346307.
38. Netea, M.G., Van der Meer, J.W., and Kullberg, B.J. (2004) Toll-like receptors as an escape mechanism from the host defense. Trends Microbiol 12: 484-488.
39. 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.
40. 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.
41. Nobile, C.J., Fox, E.P., Nett, J.E., Sorrells, T.R., Mitrovich, Q.M., Hernday, A.D., etal. (2012) A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126-138.
42. Otten, M.A., Leusen, J.H.W., Rudolph, E., van der Linden, J.A., Beelen, R.H.J., van de Winkel, J.G.J., etal. (2007) FcR γ-Chain dependent signaling in immature neutrophils is mediated by FcαRI, but not by FcγRI. J Immunol 179: 2918-2924.
43. Pei, Z., Bini, E.J., Yang, L., Zhou, M., Francois, F., and Blaser, M.J. (2004) Bacterial biota in the human distal esophagus. Proc Natl Acad Sci USA 101: 4250-4255.
44. Peters, B.M., and Noverr, M.C. (2013) Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infect Immun 81: 2178-2189.
45. Peyyala, R., Kirakodu, S.S., Ebersole, J.L., and Novak, K.F. (2011) Novel model for multispecies biofilms that uses rigid gas-permeable lenses. Appl Environ Microbiol 77: 3413-3421.
46. Ponnuvel, K.M., Rajkumar, R., Menon, T., and Sankaranarayanan, V.S. (1996) Role of Candida in indirect pathogenesis of antibiotic associated diarrhoea in infants. Mycopathologia 135: 145-147.
47. 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.
48. Ramirez-Carrozzi, V., Sambandam, A., Luis, E., Lin, Z., Jeet, S., Lesch, J., etal. (2011) IL-17C regulates the innate immune function of epithelial cells in an autocrine manner. Nat Immunol 12: 1159-1166.
49. Ramsey, M.M., Rumbaugh, K.P., and Whiteley, M. (2011) Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog 7: e1002012.
50. Rickard, A.H., Palmer, R.J., Blehert, D.S., Campagna, S.R., Semmelhack, M.F., Egland, P.G., etal. (2006) Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol 60: 1446-1456.
51. Sibley, C.D., Duan, K., Fischer, C., Parkins, M.D., Storey, D.G., Rabin, H.R., and Surette, M.G. (2008) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4: e1000184.
52. Sjovall, J., Huitfeldt, B., Magni, L., and Nord, C.E. (1986) Effect of beta-lactam prodrugs on human intestinal microflora. Scand J Infect Dis Suppl 49: 73-84.
53. Solis, N.V., and Filler, S.G. (2012) Mouse model of oropharyngeal candidiasis. Nat Protoc 7: 637-642.
54. Spandidos, A., Wang, X., Wang, H., Dragnev, S., Thurber, T., and Seed, B. (2008) A comprehensive collection of experimentally validated primers for Polymerase Chain Reaction quantitation of murine transcript abundance. BMC Genomics 9: 633.
55. Spandidos, A., Wang, X., Wang, H., and Seed, B. (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38: D792-D799.
56. Stroncek, D.F. (2007) Neutrophil-specific antigen HNA-2a, NB1 glycoprotein, and CD177. Curr Opin Hematol 14: 688-693.
57. Syed, S.A., and Loesche, W.J. (1978) Bacteriology of human experimental gingivitis: effect of plaque age. Infect Immun 21: 821-829.
58. Tessarolli, V., Gasparoto, T.H., Lima, H.R., Figueira, E.A., Garlet, T.P., Torres, S.A., etal. (2010) Absence of TLR2 influences survival of neutrophils after infection with Candida albicans. Med Mycol 48: 129-140.
59. Thom, K., and Forrest, G. (2006) Gastrointestinal infections in immunocompromised hosts. Curr Opin Gastroenterol 22: 18 -23.
60. Thurnheer, T., Gmur, R., Giertsen, E., and Guggenheim, B. (2001) Automated fluorescent in situ hybridization for the specific detection and quantification of oral streptococci in dental plaque. J Microbiol Methods 44: 39-47.
61. Venkatesh, M.P., Pham, D., Fein, M., Kong, L., and Weisman, L.E. (2007) Neonatal coinfection model of coagulase-negative Staphylococcus (Staphylococcus epidermidis) and Candida albicans: fluconazole prophylaxis enhances survival and growth. Antimicrob Agents Chemother 51: 1240-1245.
62. Villar, C.C., and Dongari-Bagtzoglou, A. (2008) Immune defence mechanisms and immunoenhancement strategies in oropharyngeal candidiasis. Expert Rev Mol Med 10: e29.
63. Vonck, R.A., Darville, T., O'Connell, C.M., and Jerse, A.E. (2011) Chlamydial infection increases gonococcal colonization in a novel murine coinfection model. Infect Immun 79: 1566-1577.
64. Wang, X., and Seed, B. (2003) A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 31: e154.
65. Whitmore, S.E., and Lamont, R.J. (2011) The pathogenic persona of community-associated oral streptococci. Mol Microbiol 81: 305-314.
66. Wolpe, S.D., and Cerami, A. (1989) Macrophage inflammatory proteins 1 and 2: members of a novel superfamily of cytokines. FASEB J 3: 2565-2573.
67. Xie, Z., Thompson, A., Kashleva, H., and Dongari-Bagtzoglou, A. (2011) A quantitative real-time RT-PCR assay for mature C.albicans biofilms. BMC Microbiol 11: 93.
68. Xie, Z., Thompson, A., Sobue, T., Kashleva, H., Xu, H., Vasilakos, J., and Dongari-Bagtzoglou, A. (2012) Candida albicans biofilms do not trigger reactive oxygen species and evade neutrophil killing. J Infect Dis 206: 1936-1945.
69. Yano, J., Lilly, E., Barousse, M., and Fidel, P.L. (2010) Epithelial cell-derived S100 calcium-binding proteins as key mediators in the hallmark acute neutrophil response during Candida vaginitis. Infect Immun 78: 5126-5137.
70. Yoshida, Y., Ganguly, S., Bush, C.A., and Cisar, J.O. (2006) Molecular basis of L-rhamnose branch formation in streptococcal coaggregation receptor polysaccharides. J Bacteriol 188: 4125-4130.
71. 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.
72. Zijnge, V., van Leeuwen, M.B., Degener, J.E., Abbas, F., Thurnheer, T., Gmur, R., and Harmsen, H. (2010) Oral biofilm architecture on natural teeth. PLoS ONE 5: e9321.