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The Relationship of Candida albicans with the Oral Bacterial Microbiome in Health and Disease

  • Martinna Bertolini
  • Anna Dongari-BagtzoglouEmail author
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1197)

Abstract

Candida albicans is an opportunistic pathogen colonizing the oropharyngeal, esophageal, and gastrointestinal mucosa in most healthy humans. In immunocompromised hosts, this fungal organism can cause mucosal candidiasis in these sites. C. albicans also causes fungemia, a serious consequence of cancer cytotoxic chemotherapy, which is thought to develop from fungal translocation through compromised mucosal barriers. Changes in endogenous bacterial population size or composition as well as changes in the host environment can transform fungal commensals into opportunistic pathogens in the upper and lower GI tract. Pioneering studies from our group have shown that a ubiquitous oral commensal of the mitis streptococcal group (Streptococcus oralis) has a mutualistic relationship with C. albicans, with C. albicans enabling streptococcal biofilm growth at mucosal sites, and S. oralis facilitating invasion of the oral and esophageal mucosa by C. albicans. In these studies, we used a cortisone-induced immunosuppression mouse model. More recently, the development of a novel mouse chemotherapy model has allowed us to examine the interactions of C. albicans with the endogenous bacterial microbiota in the oral and small intestinal mucosa, two sites adversely affected by cytotoxic chemotherapy. In this model, oral inoculation with C. albicans causes severe dysbiosis in the mucosal bacterial composition in both sites. We also found that antibiotic treatment ameliorates invasion of the oral mucosa but aggravates dissemination through the intestinal mucosa. In this chapter, we discuss work from our laboratory and others examining the relationships of C. albicans with oral bacteria and their role in mucosal homeostasis or disease.

References

  1. Abusleme, L., Diaz, P. I., Freeman, A. F., Greenwell-Wild, T., Brenchley, L., Desai, J. V., Ng, W. I., Holland, S. M., Lionakis, M. S., Segre, J. A., Kong, H. H., & Moutsopoulos, N. M. (2018). Human defects in STAT3 promote oral mucosal fungal and bacterial dysbiosis. JCI Insight, 3(17), 122061.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bertolini, M., Sobue, T., Thompson, A., & Dongari-Bagtzoglou, A. (2017). Chemotherapy induces oral mucositis in mice without additional noxious stimuli. Translational Oncology, 10(4), 612–620.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bertolini, M., Ranjan, A., Thompson, A., Diaz, P., Sobue, T., Maas, K., & Dongari-Bagtzoglou, A. (2019). Candida albicans induces mucosal bacterial dysbiosis that promotes invasive infection. PLoS Pathogens, 15(4), e1007717.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bohm, L., Torsin, S., Tint, S. H., Eckstein, M. T., Ludwig, T., & Perez, J. C. (2017). The yeast form of the fungus Candida albicans promotes persistence in the gut of gnotobiotic mice. PLoS Pathogens, 13(10), e1006699.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Boktour, M. R., Kontoyiannis, D. P., Hanna, H. A., Hachem, R. Y., Girgawy, E., Bodey, G. P., & Raad, I. I. (2004). Multiple-species candidemia in patients with cancer. Cancer, 101, 1860–1865.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brent, N. B. (2001). Thrush in the breastfeeding dyad: Results of a survey on diagnosis and treatment. Clinical Pediatrics, 40(9), 503–506.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cho, I., & Blaser, M. J. (2012). The human microbiome: At the interface of health and disease. Nature Reviews Genetics, 13(4), 260–270.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Clancy, C. J., Cheng, S., & Nguyen, M. H. (2009). Animal models of candidiasis. Methods in Molecular Biology, 499, 65–76.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Clemons, K. V., Gonzalez, G. M., Singh, G., Imai, J., Espiritu, M., Parmar, R., & Stevens, D. A. (2006). Development of an orogastrointestinal mucosal model of candidiasis with dissemination to visceral organs. Antimicrobial Agents and Chemotherapy, 50(8), 2650–2657.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cole, G. T., Halawa, A. A., & Anaissie, E. J. (1996). The role of the gastrointestinal tract in hematogenous candidiasis: From the laboratory to the bedside. Clinical Infectious Diseases, 22(Suppl. 2), S73–S88.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cruz, M. R., Graham, C. E., Gagliano, B. C., Lorenz, M. C., & Garsin, D. A. (2013). Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infection and Immunity, 81(1), 189–200.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dutzan, N., Abusleme, L., Bridgeman, H., Greenwell-Wild, T., Zangerle-Murray, T., Fife, M. E., Bouladoux, N., Linley, H., Brenchley, L., Wemyss, K., Calderon, G., Hong, B. Y., Break, T. J., Bowdish, D. M. E., Lionakis, M. S., Jones, S. A., Trinchieri, G., Diaz, P. I., Belkaid, Y., Konkel, J. E., & Moutsopoulos, N. M. (2017). On-going mechanical damage from mastication drives homeostatic Th17 cell responses at the oral barrier. Immunity, 46(1), 133–147.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fan, D., Coughlin, L. A., Neubauer, M. M., Kim, J., Kim, M. S., Zhan, X., Simms-Waldrip, T. R., Xie, Y., Hooper, L. V., & Koh, A. Y. (2015). Activation of HIF-1α and LL-37 by commensal bacteria inhibits Candida albicans colonization. Nature Medicine, 21(7), 808–814.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Ghannoum, M. A., Jurevic, R. J., Mukherjee, P. K., Cui, F., Sikaroodi, M., Naqvi, A., & Gillevet, P. M. (2010). Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathogens, 6(1), e1000713.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gligorov, J., Bastit, L., Gervais, H., Henni, M., Kahila, W., Lepille, D., Luporsi, E., Sasso, G., Varette, C., Azria, D., & Candidoscope Study, G. (2011). Prevalence and treatment management of oropharyngeal candidiasis in cancer patients: Results of the French CANDIDOSCOPE study. International Journal of Radiation Oncology, Biology, Physics, 80(2), 532–539.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gonçalves, L. S., Soares Ferreira, S. M., Souza, C. O., Souto, R., & Colombo, A. P. (2007). Clinical and microbiological profiles of human immunodeficiency virus (HIV)-seropositive Brazilians undergoing highly active antiretroviral therapy and HIV-seronegative Brazilians with chronic periodontitis. Journal of Periodontology, 78, 87.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gonçalves, L. S., Souto, R., & Colombo, A. P. (2009). Detection of Helicobacter pylori, Enterococcus faecalis, and Pseudomonas aeruginosa in the subgingival biofilm of HIV-infected subjects undergoing HAART with chronic periodontitis. European Journal of Clinical Microbiology & Infectious Diseases, 28(11), 1335–1342.CrossRefGoogle Scholar
  18. Gow, N. A., van de Veerdonk, F. L., Brown, A. J., & Netea, M. G. (2011). Candida albicans morphogenesis and host defence: Discriminating invasion from colonization. Nature Reviews Microbiology, 10(2), 112–122.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Graham, C. E., Cruz, M. R., Garsin, D. A., & Lorenz, M. C. (2017). Enterococcus faecalis bacteriocin EntV inhibits hyphal morphogenesis, biofilm formation, and virulence of Candida albicans. Proceedings of the National Academy of Sciences of the United States of America, 114(17), 4507–4512.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hata, K., Horii, T., Miyazaki, M., Watanabe, N. A., Okubo, M., Sonoda, J., Nakamoto, K., Tanaka, K., Shirotori, S., Murai, N., Inoue, S., Matsukura, M., Abe, S., Yoshimatsu, K., & Asada, M. (2011). Efficacy of oral E1210, a new broad-spectrum antifungal with a novel mechanism of action, in murine models of candidiasis, aspergillosis, and fusariosis. Antimicrobial Agents and Chemotherapy, 55(10), 4543–4551.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Holler, E., Butzhammer, P., Schmid, K., Hundsrucker, C., Koestler, J., Peter, K., Zhu, W., Sporrer, D., Hehlgans, T., Kreutz, M., et al. (2014). Metagenomic analysis of the stool microbiome in patients receiving allogeneic stem cell transplantation: Loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal graft-versus-host disease. Biology of Blood and Marrow Transplantation, 20, 640–645.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Iliev, I. D., Funari, V. A., Taylor, K. D., Nguyen, Q., Reyes, C. N., Strom, S. P., Brown, J., Becker, C. A., Fleshner, P. R., Dubinsky, M., Rotter, J. I., Wang, H. L., McGovern, D. P., Brown, G. D., & Underhill, D. M. (2012). Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science, 336(6086), 1314–1317.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jarvis, W. R. (1995). Epidemiology of nosocomial fungal infections, with emphasis on Candida species. Clinical Infectious Diseases, 20(6), 1526–1530.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kim, Y., & Mylonakis, E. (2011). Killing of Candida albicans filaments by Salmonella enterica serovar Typhimurium is mediated by sopB effectors, parts of a type III secretion system. Eukaryotic Cell, 10(6), 782–790.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kleinegger, C. L., Lockhart, S. R., Vargas, K., & Soll, D. R. (1996). Frequency, intensity, species, and strains of oral Candida vary as a function of host age. Journal of Clinical Microbiology, 34(9), 2246–2254.PubMedPubMedCentralGoogle Scholar
  26. Koh, A. Y. (2013). Murine models of Candida gastrointestinal colonization and dissemination. Eukaryotic Cell, 12(11), 1416–1422.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Komiyama, E. Y., Lepesqueur, L. S., Yassuda, C. G., Samaranayake, L. P., Parahitiyawa, N. B., Balducci, I., & Koga-Ito, C. Y. (2016). Enterococcus species in the oral cavity: Prevalence, virulence factors and antimicrobial susceptibility. PLoS One, 11(9), e0163001.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kong, E. F., Kucharíková, S., Van Dijck, P., Peters, B. M., Shirtliff, M. E., & Jabra-Rizk, M. A. (2015). Clinical implications of oral candidiasis: Host tissue damage and disseminated bacterial disease. Infection and Immunity, 83(2), 604–613.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kraneveld, E. A., Buijs, M. J., Bonder, M. J., Visser, M., Keijser, B. J., Crielaard, W., & Zaura, E. (2012). The relation between oral Candida load and bacterial microbiome profiles in Dutch older adults. PLoS One, 7(8), e42770.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Krause, R., Schwab, E., Bachhiesl, D., Daxbock, F., Wenisch, C., Krejs, G. J., & Reisinger, E. C. (2001). Role of Candida in antibiotic-associated diarrhea. The Journal of Infectious Diseases, 184(8), 1065–1069.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lagkouvardos, I., Joseph, D., Kapfhammer, M., Giritli, S., Horn, M., Haller, D., & Clavel, T. (2016). IMNGS: A comprehensive open resource of processed 16S rRNA microbial profiles for ecology and diversity studies. Scientific Reports, 6, 33721.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lalla, R. V., Latortue, M. C., Hong, C. H., Ariyawardana, A., D’Amato-Palumbo, S., Fischer, D. J., Martof, A., Nicolatou-Galitis, O., Patton, L. L., Elting, L. S., Spijkervet, F. K., Brennan, M. T., & Fungal Infections Section, Oral Care Study Group, Multinational Association of Supportive Care in Cancer (MASCC)/International Society of Oral Oncology (ISOO). (2010). A systematic review of oral fungal infections in patients receiving cancer therapy. Supportive Care in Cancer, 18(8), 985–992.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Leendertse, M., Willems, R. J., Giebelen, I. A., Roelofs, J. J., Bonten, M. J., & van der Poll, T. (2009). Neutrophils are essential for rapid clearance of Enterococcus faecium in mice. Infection and Immunity, 77(1), 485–491.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lucatorto, F. M., Franker, C., Hardy, W. D., & Chafey, S. (1991). Treatment of refractory oral candidiasis with fluconazole. A case report. Oral Surgery, Oral Medicine, and Oral Pathology, 71(1), 42–44.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Maeda, Y., Elborn, J. S., Parkins, M. D., Reihill, J., Goldsmith, C. E., Coulter, W. A., Mason, C., Millar, B. C., Dooley, J. S., Lowery, C. J., Ennis, M., Rendall, J. C., & Moore, J. E. (2011). Population structure and characterization of viridans group streptococci (VGS) including Streptococcus pneumoniae isolated from adult patients with cystic fibrosis (CF). Journal of Cystic Fibrosis, 10(2), 133–139.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mason, K. L., Erb Downward, J. R., Falkowski, N. R., Young, V. B., Kao, J. Y., & Huffnagle, G. B. (2012a). Interplay between the gastric bacterial microbiota and Candida albicans during postantibiotic recolonization and gastritis. Infection and Immunity, 80(1), 150–158.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mason, K. L., Erb Downward, J. R., Mason, K. D., Falkowski, N. R., Eaton, K. A., Kao, J. Y., Young, V. B., & Huffnagle, G. B. (2012b). Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infection and Immunity, 80(10), 3371–3380.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Meunier, F., Gerard, M., Richard, V., Debusscher, L., Bleiberg, H., & Malengrau, A. (1989). Hepatic candidosis in a patient with acute leukemia. Mycoses, 32(8), 421–426.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Moran, C., Grussemeyer, C. A., Spalding, J. R., Benjamin, D. K., Jr., & Reed, S. D. (2010). Comparison of costs, length of stay, and mortality associated with Candida glabrata and Candida albicans bloodstream infections. American Journal of Infection Control, 38(1), 78–80.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Nagy, K. N., Sonkodi, I., Szoke, I., Nagy, E., & Newman, H. N. (1998). The microflora associated with human oral carcinomas. Oral Oncology, 34(4), 304–308.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Nicolatou-Galitis, O., Dardoufas, K., Markoulatos, P., Sotiropoulou-Lontou, A., Kyprianou, K., Kolitsi, G., Pissakas, G., Skarleas, C., Kouloulias, V., Papanicolaou, V., Legakis, N. J., & Velegraki, A. (2001). Oral pseudomembranous candidiasis, herpes simplex virus-1 infection, and oral mucositis in head and neck cancer patients receiving radiotherapy and granulocyte-macrophage colony-stimulating factor (GM-CSF) mouthwash. Journal of Oral Pathology & Medicine, 30(8), 471–480.CrossRefGoogle Scholar
  42. Olczak-Kowalczyk, D., Daszkiewicz, M., Krasuska-Sławińska, Dembowska-Bagińska, B., Gozdowski, D., Daszkiewicz, P., Fronc, B., & Semczuk, K. (2012). Bacteria and Candida yeasts in inflammations of the oral mucosa in children with secondary immunodeficiency. Journal of Oral Pathology & Medicine, 41(7), 568–576.Google Scholar
  43. Passalacqua, G., Albano, M., Canonica, G. W., Bachert, C., Van Cauwenberge, P., Davies, R. J., Durham, S. R., Kontou-Fili, K., Horak, F., & Malling, H. J. (2000). Inhaled and nasal corticosteroids: Safety aspects. Allergy, 55(1), 16–33.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pei, Z., Bini, E. J., Yang, L., Zhou, M., Francois, F., & Blaser, M. J. (2004). Bacterial biota in the human distal esophagus. Proceedings of the National Academy of Sciences of the United States of America, 101(12), 4250–4255.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Perlroth, J., Choi, B., & Spellberg, B. (2007). Nosocomial fungal infections: Epidemiology, diagnosis, and treatment. Medical Mycology, 45(4), 321–346.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Peters, B. M., & Noverr, M. C. (2013). Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infection and Immunity, 81(6), 2178–2189.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Polak-Wyss A. Protective effect of human granulocyte colony stimulating factor (hG-CSF) on Candida infections in normal and immunosuppressed mice. Mycoses. 1991;34(3–4):109–18. PubMed PMID: 1721105.Google Scholar
  48. Ponnuvel, K. M., Rajkumar, R., Menon, T., & Sankaranarayanan, V. S. (1996). Role of Candida in indirect pathogenesis of antibiotic associated diarrhoea in infants. Mycopathologia, 135(3), 145–147.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Puig-Asensio, M., Ruiz-Camps, I., Fernandez-Ruiz, M., Aguado, J. M., Munoz, P., Valerio, M., Delgado-Iribarren, A., Merino, P., Bereciartua, E., Fortun, J., et al. (2015). Epidemiology and outcome of candidaemia in patients with oncological and haematological malignancies: Results from a population-based surveillance in Spain. Clinical Microbiology and Infection, 21, 491–495.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Redding, S. W., Kirkpatrick, W. R., Coco, B. J., Sadkowski, L., Fothergill, A. W., Rinaldi, M. G., Eng, T. Y., & Patterson, T. F. (2002). Candida glabrata oropharyngeal candidiasis in patients receiving radiation treatment for head and neck cancer. Journal of Clinical Microbiology, 40(5), 1879–1881.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Russell, C., & Lay, K. M. (1973). Natural history of Candida species and yeasts in the oral cavities of infants. Archives of Oral Biology, 18(8), 957–962.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sawyer, R. T., & Harmsen, A. G. (1989). The relative contribution of resident pulmonary alveolar macrophage and inflammatory polymorphonuclear neutrophils in host resistance to pulmonary infection by Candida albicans. Mycopathologia, 108(2), 95–105.PubMedPubMedCentralGoogle Scholar
  53. Shankar, J., Solis, N. V., Mounaud, S., Szpakowski, S., Liu, H., Losada, L., Nierman, W. C., & Filler, S. G. (2015). Using Bayesian modelling to investigate factors governing antibiotic-induced Candida albicans colonization of the GI tract. Scientific Reports, 5, 8131.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sjovall, J., Huitfeldt, B., Magni, L., & Nord, C. E. (1986). Effect of beta-lactam prodrugs on human intestinal microflora. Scandinavian Journal of Infectious Diseases Supplementum, 49, 73–84.PubMedPubMedCentralGoogle Scholar
  55. Sobue, T., Diaz, P., Xu, H., Bertolini, M., & Dongari-Bagtzoglou, A. (2016). Experimental models of C. albicans-Streptococcal Co-infection. Methods in Molecular Biology, 1356, 137–152.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sobue, T., Bertolini, M., Thompson, A., Peterson, D. E., Diaz, P. I., & Dongari-Bagtzoglou, A. (2018). Chemotherapy-induced oral mucositis and associated infections in a novel organotypic model. Molecular Oral Microbiology, 33(3), 212–223.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Solis, N. V., & Filler, S. G. (2012). Mouse model of oropharyngeal candidiasis. Nature Protocols, 7(4), 637–642.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sparo, M., Delpech, G., & García Allende, N. (2018). Impact on public health of the spread of high-level resistance to gentamicin and vancomycin in enterococci. Frontiers in Microbiology, 9, 3073.CrossRefPubMedPubMedCentralGoogle Scholar
  59. St Leger, A. J., Desai, J. V., Drummond, R. A., Kugadas, A., Almaghrabi, F., Silver, P., Raychaudhuri, K., Gadjeva, M., Iwakura, Y., Lionakis, M. S., & Caspi, R. R. (2017). An ocular commensal protects against corneal infection by driving an interleukin-17 response from mucosal γδ T cells. Immunity, 47(1), 148–158.e5.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Swidsinski, A., Weber, J., Loening-Baucke, V., Hale, L. P., & Lochs, H. (2005). Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. Journal of Clinical Microbiology, 43(7), 3380–3389.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Tampakakis, E., Peleg, A. Y., & Mylonakis, E. (2009). Interaction of Candida albicans with an intestinal pathogen, Salmonella enterica serovar Typhimurium. Eukaryotic Cell, 8(5), 732–737.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Teoh, F., & Pavelka, N. (2016). How chemotherapy increases the risk of systemic candidiasis in cancer patients: Current paradigm and future directions. Pathogens, 5(1), E6.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Villafuerte, K. R. V., Martinez, C. J. H., Dantas, F. T., Carrara, H. H. A., Dos Reis, F. J. C., & Palioto, D. B. (2018). The impact of chemotherapeutic treatment on the oral microbiota of patients with cancer: A systematic review. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, 125(6), 552–566.CrossRefGoogle Scholar
  64. Wilson, L. S., Reyes, C. M., Stolpman, M., Speckman, J., Allen, K., & Beney, J. (2002). The direct cost and incidence of systemic fungal infections. Value in Health, 5(1), 26–34.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Xu, H., Sobue, T., Thompson, A., Xie, Z., Poon, K., Ricker, A., Cervantes, J., Diaz, P. I., & Dongari-Bagtzoglou, A. (2014). Streptococcal co-infection augments Candida pathogenicity by amplifying the mucosal inflammatory response. Cellular Microbiology, 16(2), 214–231.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Xu, H., Sobue, T., Bertolini, M., Thompson, A., & Dongari-Bagtzoglou, A. (2016). Streptococcus oralis and Candida albicans synergistically activate mu-calpain to degrade E-cadherin from oral epithelial junctions. The Journal of Infectious Diseases, 214(6), 925–934.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Xu, H., Sobue, T., Bertolini, M., Thompson, A., Vickerman, M., Nobile, C. J., & Dongari-Bagtzoglou, A. (2017). S. oralis activates the Efg1 filamentation pathway in C. albicans to promote cross-kingdom interactions and mucosal biofilms. Virulence, 8(8), 1602–1617.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yang, C. H., Chew, K. Y., Solomkin, J. S., Lin, P. Y., Chiang, Y. C., & Kuo, Y. R. (2013). Surgical site infections among high-risk patients in clean-contaminated head and neck reconstructive surgery: Concordance with preoperative oral flora. Annals of Plastic Surgery, 71(Suppl. 1), S55–S60.PubMedPubMedCentralGoogle Scholar
  69. Yano, J., Lilly, E., Barousse, M., & Fidel, P. L., Jr. (2010). Epithelial cell-derived S100 calcium-binding proteins as key mediators in the hallmark acute neutrophil response during Candida vaginitis. Infection and Immunity, 78(12), 5126–5137.CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Oral Health and Diagnostic SciencesUniversity of Connecticut Health CenterFarmingtonUSA

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