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Neutrophil Interaction with Emerging Oral Pathogens: A Novel View of the Disease Paradigm

  • Irina Miralda
  • Aruna Vashishta
  • Silvia M. UriarteEmail author
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1197)

Abstract

Periodontitis is a multifactorial chronic inflammatory infectious disease that compromises the integrity of tooth-supporting tissues. The disease progression depends on the disruption of host–microbe homeostasis in the periodontal tissue. This disruption is marked by a shift in the composition of the polymicrobial oral community from a symbiotic to a dysbiotic, more complex community that is capable of evading killing while promoting inflammation. Neutrophils are the main phagocytic cell in the periodontal pocket, and the outcome of the interaction with the oral microbiota is an important determinant of oral health. Novel culture-independent techniques have facilitated the identification of new bacterial species at periodontal lesions and induced a reappraisal of the microbial etiology of periodontitis. In this chapter, we discuss how neutrophils interact with two emerging oral pathogens, Filifactor alocis and Peptoanaerobacter stomatis, and the different strategies deploy by these organisms to modulate neutrophil effector functions, with the goal to outline a new paradigm in our knowledge about neutrophil responses to putative periodontal pathogens and their contribution to disease progression.

Keywords

Neutrophils Emerging oral pathogens Periodontitis 

References

  1. Aas, J. A., Paster, B. J., Stokes, L. N., Olsen, I., & Dewhirst, F. E. (2005). Defining the normal bacterial flora of the oral cavity. Journal of Clinical Microbiology, 43(11), 5721–5732.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abusleme, L., Dupuy, A. K., Dutzan, N., Silva, N., Burleson, J. A., Strausbaugh, L. D., et al. (2013). The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. The ISME Journal, 7(5), 1016–1025.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amulic, B., Cazalet, C., Hayes, G. L., Metzler, K. D., & Zychlinsky, A. (2012). Neutrophil function: From mechanisms to disease. Annual Review of Immunology, 30, 459–489.CrossRefPubMedGoogle Scholar
  4. Anderson, I. C., & Cairney, J. W. (2004). Diversity and ecology of soil fungal communities: Increased understanding through the application of molecular techniques. Environmental Microbiology, 6(8), 769–779.CrossRefPubMedGoogle Scholar
  5. Armstrong, C. L., Miralda, I., Neff, A. C., Tian, S., Vashishta, A., Perez, L., et al. (2016). Filifactor alocis promotes neutrophil degranulation and chemotactic activity. Infection and Immunity, 84(12), 3423–3433.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Armstrong, C. L., Klaes, C. K., Vashishta, A., Lamont, R. J., & Uriarte, S. M. (2018). Filifactor alocis manipulates human neutrophils affecting their ability to release neutrophil extracellular traps induced by PMA. Innate Immunity, 24(4), 210–220.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Aruni, A. W., Roy, F., & Fletcher, H. M. (2011). Filifactor alocis has virulence attributes that can enhance its persistence under oxidative stress conditions and mediate invasion of epithelial cells by Porphyromonas gingivalis. Infection and Immunity, 79(10), 3872–3886.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Aruni, A. W., Roy, F., Sandberg, L., & Fletcher, H. M. (2012). Proteome variation among Filifactor alocis strains. Proteomics, 12(22), 3343–3364.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Aruni, A. W., Mishra, A., Dou, Y., Chioma, O., Hamilton, B. N., & Fletcher, H. M. (2015). Filifactor alocis—a new emerging periodontal pathogen. Microbes and Infection, 17(7), 517–530.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Babior, B. M., Lambeth, J. D., & Nauseef, W. (2002). The neutrophil NADPH oxidase. Archives of Biochemistry and Biophysics, 397(2), 342–344.CrossRefPubMedGoogle Scholar
  11. Barrientos, L., Marin-Esteban, V., de Chaisemartin, L., Le-Moal, V. L., Sandre, C., Bianchini, E., et al. (2013). An improved strategy to recover large fragments of functional human neutrophil extracellular traps. Frontiers in Immunology, 4, 166.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Beiter, K., Wartha, F., Albiger, B., Normark, S., Zychlinsky, A., & Henriques-Normark, B. (2006). An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Current Biology, 16(4), 401–407.CrossRefPubMedGoogle Scholar
  13. Belambri, S. A., Rolas, L., Raad, H., Hurtado-Nedelec, M., Dang, P. M.-C., & El-Benna, J. (2018). NADPH oxidase activation in neutrophils: Role of the phosphorylation of its subunits. European Journal of Clinical Investigation, 48(S2), e12951.CrossRefPubMedGoogle Scholar
  14. Berezow, A. B., & Darveau, R. P. (2011). Microbial shift and periodontitis. Periodontology 2000, 55(1), 36–47.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bingham, C. O. I., & Moni, M. (2013). Periodontal disease and rheumatoid arthritis: The evidence accumulates for complex pathobiologic interactions. Current Opinion in Rheumatology, 25(3), 345–353.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Borregaard, N. (2010). Neutrophils, from marrow to microbes. Immunity, 33(5), 657–670.CrossRefPubMedGoogle Scholar
  17. Borregaard, N., & Cowland, J. B. (1997). Granules of the human neutrophilic polymorphonuclear leukocyte. Blood, 89(10), 3503–3521.CrossRefPubMedGoogle Scholar
  18. Borregaard, N., Sørensen, O. E., & Theilgaard-Mönch, K. (2007). Neutrophil granules: A library of innate immunity proteins. Trends in Immunology, 28(8), 340–345.CrossRefPubMedGoogle Scholar
  19. Bostanci, N., Ozturk, V. O., Emingil, G., & Belibasakis, G. N. (2013a). Elevated oral and systemic levels of soluble triggering receptor expressed on myeloid cells-1 (sTREM-1) in periodontitis. Journal of Dental Research, 92, 161–165.CrossRefPubMedGoogle Scholar
  20. Bostanci, N., Thurnheer, T., Aduse-Opoku, J., Curtis, M. A., Zinkernagel, A. S., & Belibasakis, G. N. (2013b). Porphyromonas gingivalis regulates TREM-1 in human polymorphonuclear neutrophils via its gingipains. PLoS One, 8(10), e75784.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Brinkmann, V., & Zychlinsky, A. (2012). Neutrophil extracellular traps: Is immunity the second function of chromatin? The Journal of Cell Biology, 198(5), 773–783.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., et al. (2004). Neutrophil extracellular traps kill bacteria. Science, 303(5663), 1532–1535.CrossRefGoogle Scholar
  23. Buchanan, J. T., Simpson, A. J., Aziz, R. K., Liu, G. Y., Kristian, S. A., Kotb, M., et al. (2006). DNase expression allows the pathogen group a Streptococcus to escape killing in neutrophil extracellular traps. Current Biology, 16(4), 396–400.CrossRefPubMedGoogle Scholar
  24. Cassatella, M. A. (1999). Neutrophil-derived proteins: Selling cytokines by the pound. Advances in Immunology, 73, 369–509.CrossRefPubMedGoogle Scholar
  25. Cato, E. P., Moore, L. V. H., & Moore, W. E. C. (1985). Fusobacterium alocis sp. nov. and Fusobacterium sulci sp. nov. from the human gingival sulcus. International Journal of Systematic Bacteriology, 35(4), 475–477.CrossRefGoogle Scholar
  26. Chen, H., Liu, Y., Zhang, M., Wang, G., Qi, Z., Bridgewater, L., et al. (2015). A Filifactor alocis-centered co-occurrence group associates with periodontitis across different oral habitats. Scientific Reports, 5, 9053.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Cheng, O. Z., & Palaniyar, N. (2013). NET balancing: A problem in inflammatory lung diseases. Frontiers in Immunology, 4, 1.PubMedPubMedCentralGoogle Scholar
  28. Chertov, O., Yang, D., Howard, O. M. Z., & Oppenheim, J. J. (2000). Leukocyte granule proteins mobilize innate host defenses and adaptive immune responses. Immunological Reviews, 177(1), 68–78.CrossRefPubMedGoogle Scholar
  29. Cooper, P. R., Palmer, L. J., & Chapple, I. L. (2013). Neutrophil extracellular traps as a new paradigm in innate immunity: Friend or foe? Periodontology 2000, 63(1), 165–197.CrossRefPubMedGoogle Scholar
  30. Costalonga, M., & Herzberg, M. C. (2014). The oral microbiome and the immunobiology of periodontal disease and caries. Immunology Letters, 162(2 Pt A), 22–38.CrossRefPubMedPubMedCentralGoogle Scholar
  31. da Silva, E. S., Feres, M., Figueiredo, L. C., Shibli, J. A., Ramiro, F. S., & Faveri, M. (2014). Microbiological diversity of peri-implantitis biofilm by Sanger sequencing. Clinical Oral Implants Research, 25(10), 1192–1199.CrossRefPubMedGoogle Scholar
  32. Dabdoub, S. M., Ganesan, S. M., & Kumar, P. S. (2016). Comparative metagenomics reveals taxonomically idiosyncratic yet functionally congruent communities in periodontitis. Scientific Reports, 6, 38993.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Dahlen, G., & Leonhardt, A. (2006). A new checkerboard panel for testing bacterial markers in periodontal disease. Oral Microbiology and Immunology, 21(1), 6–11.CrossRefPubMedGoogle Scholar
  34. Dahlen, G., Wikstrom, M., & Moller, A. (1983). Production of histolytic enzymes by a combination of oral bacteria with known pathogenicity. Journal of Dental Research, 62(10), 1041–1044.CrossRefPubMedGoogle Scholar
  35. Darveau, R. P. (2009). The oral microbial consortium’s interaction with the periodontal innate defense system. DNA and Cell Biology, 28(8), 389–395.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Darveau, R. P. (2010). Periodontitis: A polymicrobial disruption of host homeostasis. Nature Reviews. Microbiology, 8(7), 481–490.CrossRefPubMedGoogle Scholar
  37. Deng, W., Xi, D., Mao, H., & Wanapat, M. (2008). The use of molecular techniques based on ribosomal RNA and DNA for rumen microbial ecosystem studies: A review. Molecular Biology Reports, 35(2), 265–274.CrossRefPubMedGoogle Scholar
  38. Dewhirst, F. E., Chen, T., Izard, J., Paster, B. J., Tanner, A. C., Yu, W. H., et al. (2010). The human oral microbiome. Journal of Bacteriology, 192(19), 5002–5017.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Douglass, C. W. (2006). Risk assessment and management of periodontal disease. Journal of the American Dental Association (1939), 137, S27–S32.CrossRefGoogle Scholar
  40. Downes, J., & Wade, W. G. (2006). Peptostreptococcus stomatis sp. nov., isolated from the human oral cavity. International Journal of Systematic and Evolutionary Microbiology, 56(Pt 4), 751–754.CrossRefPubMedGoogle Scholar
  41. Duran-Pinedo, A. E., Yost, S., & Frias-Lopez, J. (2015). Small RNA transcriptome of the oral microbiome during periodontitis progression. Applied and Environmental Microbiology, 81(19), 6688–6699.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Edmisson, J. S., Tian, S., Armstrong, C. L., Vashishta, A., Klaes, C. K., Miralda, I., et al. (2018). Filifactor alocis modulates human neutrophil antimicrobial functional responses. Cellular Microbiology, 20(6), e12829.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Eke, P. I., Thornton-Evans, G. O., Wei, L., Borgnakke, W. S., Dye, B. A., & Genco, R. J. (2018). Periodontitis in US adults: national health and nutrition examination survey 2009–2014. Journal of the American Dental Association (1939), 149(7), 576–88.e6.CrossRefGoogle Scholar
  44. Feres, M., Cortelli, S. C., Figueiredo, L. C., Haffajee, A. D., & Socransky, S. S. (2004). Microbiological basis for periodontal therapy. Journal of Applied Oral Science, 12(4), 256–266.CrossRefPubMedGoogle Scholar
  45. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., et al. (2007). Novel cell death program leads to neutrophil extracellular traps. The Journal of Cell Biology, 176(2), 231–241.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Gray, R. M., & Vidwans, M. (2019). Mixed anaerobic thoracic empyema: The first report of Filifactor alocis causing extra-oral disease. New Microbes and New Infections, 29, 100528.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Griffen, A. L., Beall, C. J., Campbell, J. H., Firestone, N. D., Kumar, P. S., Yang, Z. K., et al. (2012). Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME Journal, 6(6), 1176–1185.CrossRefPubMedGoogle Scholar
  48. Hajishengallis, G. (2013). Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends in Immunology, 35(1), 3–11.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Hajishengallis, G. (2014). The inflammophilic character of the periodontitis-associated microbiota. Molecular Oral Microbiology, 29(6), 248–257.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Hajishengallis, G. (2015). Periodontitis: From microbial immune subversion to systemic inflammation. Nature Reviews. Immunology, 15(1), 30–44.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hajishengallis, G., & Lambris, J. D. (2012). Complement and dysbiosis in periodontal disease. Immunobiology, 217(11), 1111–1116.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hajishengallis, G., & Lambris, J. D. (2016). More than complementing tolls: Complement–toll-like receptor synergy and crosstalk in innate immunity and inflammation. Immunological Reviews, 274(1), 233–244.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Hajishengallis, G., & Lamont, R. J. (2012). Beyond the red complex and into more complexity: The polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Molecular Oral Microbiology, 27(6), 409–419.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Hajishengallis, G., & Lamont, R. J. (2016). Dancing with the stars: How choreographed bacterial interactions dictate nososymbiocity and give rise to keystone pathogens, accessory pathogens, and pathobionts. Trends in Microbiology, 24(6), 477–489.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Hajishengallis, G., Moutsopoulos, N. M., Hajishengallis, E., & Chavakis, T. (2016). Immune and regulatory functions of neutrophils in inflammatory bone loss. Seminars in Immunology, 28(2), 146–158.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Hajishengallis, G., Kajikawa, T., Hajishengallis, E., Maekawa, T., Reis, E. S., Mastellos, D. C., et al. (2019). Complement-dependent mechanisms and interventions in periodontal disease. Frontiers in Immunology, 10, 406.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Jalava, J., & Eerola, E. (1999). Phylogenetic analysis of Fusobacterium alocis and Fusobacterium sulci based on 16S rRNA gene sequences: Proposal of Filifactor alocis (Cato, Moore and Moore) comb. nov. and Eubacterium sulci (Cato, Moore and Moore) comb. nov. International Journal of Systematic Bacteriology, 49(Pt 4), 1375–1379.CrossRefPubMedGoogle Scholar
  58. Jimenez Flores, E., Tian, S., Sizova, M., Epstein, S. S., Lamont, R. J., & Uriarte, S. M. (2017). Peptoanaerobacter stomatis primes human neutrophils and induces granule exocytosis. Infection and Immunity, 85(7), e01043–e01016.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Jorth, P., Turner, K. H., Gumus, P., Nizam, N., Buduneli, N., & Whiteley, M. (2014). Metatranscriptomics of the human oral microbiome during health and disease. MBio, 5(2), e01012–e01014.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Jusko, M., Miedziak, B., Ermert, D., Magda, M., King, B. C., Bielecka, E., et al. (2016). FACIN, a double-edged sword of the emerging periodontal pathogen Filifactor alocis: A metabolic enzyme moonlighting as a complement inhibitor. Journal of Immunology, 197(8), 3245–3259.CrossRefGoogle Scholar
  61. Kebschull, M., Demmer, R. T., & Papapanou, P. N. (2010). “Gum Bug, Leave My Heart Alone!”—Epidemiologic and mechanistic evidence linking periodontal infections and atherosclerosis. Journal of Dental Research, 89(9), 879–902.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kolaczkowska, E., & Kubes, P. (2013). Neutrophil recruitment and function in health and inflammation. Nature Reviews. Immunology, 13(3), 159–175.CrossRefPubMedGoogle Scholar
  63. Krishnan, K., Chen, T., & Paster, B. J. (2017). A practical guide to the oral microbiome and its relation to health and disease. Oral Diseases, 23(3), 276–286.CrossRefPubMedGoogle Scholar
  64. Kumar, P. S., Griffen, A. L., Barton, J. A., Paster, B. J., Moeschberger, M. L., & Leys, E. J. (2003). New bacterial species associated with chronic periodontitis. Journal of Dental Research, 82(5), 338–344.CrossRefPubMedGoogle Scholar
  65. Kumar, P. S., Griffen, A. L., Moeschberger, M. L., & Leys, E. J. (2005). Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. Journal of Clinical Microbiology, 43(8), 3944–3955.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Kumar, P. S., Leys, E. J., Bryk, J. M., Martinez, F. J., Moeschberger, M. L., & Griffen, A. L. (2006). Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. Journal of Clinical Microbiology, 44(10), 3665–3673.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Lamont, R. J., & Hajishengallis, G. (2015). Polymicrobial synergy and dysbiosis in inflammatory disease. Trends in Molecular Medicine, 21(3), 172–183.CrossRefPubMedGoogle Scholar
  68. Ley, K., Hoffman, H. M., Kubes, P., Cassatella, M. A., Zychlinsky, A., Hedrick, C. C., et al. (2018). Neutrophils: new insights and open questions. Science Immunology, 3(30), eaat4579.CrossRefPubMedGoogle Scholar
  69. Listgarten, M. A. (1976). Structure of the microbial flora associated with periodontal health and disease in man. A light and electron microscopic study. Journal of Periodontology, 47(1), 1–18.CrossRefPubMedGoogle Scholar
  70. Listgarten, M. A., & Hellden, L. (1978). Relative distribution of bacteria at clinically healthy and periodontally diseased sites in humans. Journal of Clinical Periodontology, 5(2), 115–132.CrossRefPubMedGoogle Scholar
  71. Lominadze, G., Powell, D. W., Luerman, G. C., Link, A. J., Ward, R. A., & McLeish, K. R. (2005). Proteomic analysis of human neutrophil granules. Molecular & Cellular Proteomics, 4(10), 1503–1521.CrossRefGoogle Scholar
  72. Maekawa, T., Krauss Jennifer, L., Abe, T., Jotwani, R., Triantafilou, M., Triantafilou, K., et al. (2014). Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host & Microbe, 15(6), 768–778.CrossRefGoogle Scholar
  73. Marsh, P. D. (1994). Microbial ecology of dental plaque and its significance in health and disease. Advances in Dental Research, 8(2), 263–271.CrossRefPubMedGoogle Scholar
  74. Moffatt, C. E., Whitmore, S. E., Griffen, A. L., Leys, E. J., & Lamont, R. J. (2011). Filifactor alocis interactions with gingival epithelial cells. Molecular Oral Microbiology, 26(6), 365–373.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Murphy, E. C., & Frick, I. M. (2013). Gram-positive anaerobic cocci--commensals and opportunistic pathogens. FEMS Microbiology Reviews, 37(4), 520–553.CrossRefPubMedGoogle Scholar
  76. Nauseef, W. M. (2007). How human neutrophils kill and degrade microbes: An integrated view. Immunological Reviews, 219, 88–102.CrossRefPubMedGoogle Scholar
  77. Nauseef, W. M. (2014). Detection of superoxide anion and hydrogen peroxide production by cellular NADPH oxidases. Biochimica et Biophysica Acta, 1840(2), 757–767.CrossRefPubMedGoogle Scholar
  78. Nauseef, W. M., & Borregaard, N. (2014). Neutrophils at work. Nature Immunology, 15(7), 602–611.CrossRefPubMedGoogle Scholar
  79. Parker, H., Dragunow, M., Hampton, M. B., Kettle, A. J., & Winterbourn, C. C. (2012). Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. Journal of Leukocyte Biology, 92(4), 841–849.CrossRefPubMedGoogle Scholar
  80. Paster, B. J., Boches, S. K., Galvin, J. L., Ericson, R. E., Lau, C. N., Levanos, V. A., et al. (2001). Bacterial diversity in human subgingival plaque. Journal of Bacteriology, 183(12), 3770–3783.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Paster, B. J., Olsen, I., Aas, J. A., & Dewhirst, F. E. (2006). The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontology 2000, 42, 80–87.CrossRefPubMedGoogle Scholar
  82. Pelletier, M., Maggi, L., Micheletti, A., Lazzeri, E., Tamassia, N., Costantini, C., et al. (2010). Evidence for a cross-talk between human neutrophils and Th17 cells. Blood, 115(2), 335–343.CrossRefPubMedGoogle Scholar
  83. Perez-Chaparro, P. J., Goncalves, C., Figueiredo, L. C., Faveri, M., Lobao, E., Tamashiro, N., et al. (2014). Newly identified pathogens associated with periodontitis: A systematic review. Journal of Dental Research, 93(9), 846–858.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Pilsczek, F. H., Salina, D., Poon, K. K., Fahey, C., Yipp, B. G., Sibley, C. D., et al. (2010). A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. Journal of Immunology, 185(12), 7413–7425.CrossRefGoogle Scholar
  85. Porschen, R. K., & Sonntag, S. (1974). Extracellular deoxyribonuclease production by anaerobic bacteria. Applied Microbiology, 27(6), 1031–1033.PubMedPubMedCentralGoogle Scholar
  86. Remijsen, Q., Kuijpers, T. W., Wirawan, E., Lippens, S., Vandenabeele, P., & Vanden Berghe, T. (2011). Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death and Differentiation, 18(4), 581–588.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Rørvig, S., Østergaard, O., Heegaard, N. H. H., & Borregaard, N. (2013). Proteome profiling of human neutrophil granule subsets, secretory vesicles, and cell membrane: Correlation with transcriptome profiling of neutrophil precursors. Journal of Leukocyte Biology, 94(4), 711–721.CrossRefPubMedGoogle Scholar
  88. Rudek, W., & Haque, R. U. (1976). Extracellular enzymes of the genus Bacteroides. Journal of Clinical Microbiology, 4(5), 458–460.PubMedPubMedCentralGoogle Scholar
  89. Ryder, M. I. (2010). Comparison of neutrophil functions in aggressive and chronic periodontitis. Periodontology 2000, 53(1), 124–137.CrossRefPubMedGoogle Scholar
  90. Scapini, P., & Cassatella, M. A. (2014). Social networking of human neutrophils within the immune system. Blood, 124(5), 710–719.CrossRefPubMedGoogle Scholar
  91. Schlafer, S., Riep, B., Griffen, A. L., Petrich, A., Hubner, J., Berning, M., et al. (2010). Filifactor alocis—involvement in periodontal biofilms. BMC Microbiology, 10, 66.CrossRefPubMedPubMedCentralGoogle Scholar
  92. Scott, D. A., & Krauss, J. (2012). Neutrophils in periodontal inflammation. Frontiers of Oral Biology, 15, 56–83.CrossRefPubMedGoogle Scholar
  93. Simon, D., Simon, H. U., & Yousefi, S. (2013). Extracellular DNA traps in allergic, infectious, and autoimmune diseases. Allergy, 68(4), 409–416.CrossRefPubMedGoogle Scholar
  94. Siqueira, J. F., Jr., & Rocas, I. N. (2003). Detection of Filifactor alocis in endodontic infections associated with different forms of periradicular diseases. Oral Microbiology and Immunology, 18(4), 263–265.CrossRefPubMedGoogle Scholar
  95. Siqueira, J. F., Jr., Rocas, I. N., Alves, F. R., & Silva, M. G. (2009). Bacteria in the apical root canal of teeth with primary apical periodontitis. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics, 107(5), 721–726.CrossRefPubMedGoogle Scholar
  96. Sizova, M. V., Hohmann, T., Hazen, A., Paster, B. J., Halem, S. R., Murphy, C. M., et al. (2012). New approaches for isolation of previously uncultivated oral bacteria. Applied and Environmental Microbiology, 78(1), 194–203.CrossRefPubMedPubMedCentralGoogle Scholar
  97. Sizova, M. V., Chilaka, A., Earl, A. M., Doerfert, S. N., Muller, P. A., Torralba, M., et al. (2015). High-quality draft genome sequences of five anaerobic oral bacteria and description of Peptoanaerobacter stomatis gen. Nov., sp. nov., a new member of the family Peptostreptococcaceae. Standards in Genomic Sciences, 10, 37.CrossRefPubMedPubMedCentralGoogle Scholar
  98. Socransky, S. S., & Haffajee, A. D. (1994). Evidence of bacterial etiology: A historical perspective. Periodontology 2000, 5, 7–25.CrossRefPubMedGoogle Scholar
  99. Socransky, S. S., & Haffajee, A. D. (2005). Periodontal microbial ecology. Periodontology 2000, 38, 135–187.CrossRefPubMedGoogle Scholar
  100. Socransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C., & Kent, R. L., Jr. (1998). Microbial complexes in subgingival plaque. Journal of Clinical Periodontology, 25(2), 134–144.CrossRefPubMedGoogle Scholar
  101. Solbiati, J., & Frias-Lopez, J. (2018). Metatranscriptome of the oral microbiome in health and disease. Journal of Dental Research, 97(5), 492–500.CrossRefPubMedPubMedCentralGoogle Scholar
  102. Sumby, P., Barbian, K. D., Gardner, D. J., Whitney, A. R., Welty, D. M., Long, R. D., et al. (2005). Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proceedings of the National Academy of Sciences of the United States of America, 102(5), 1679–1684.CrossRefPubMedPubMedCentralGoogle Scholar
  103. Tamassia, N., Bianchetto-Aguilera, F., Arruda-Silva, F., Gardiman, E., Gasperini, S., Calzetti, F., et al. (2018). Cytokine production by human neutrophils: Revisiting the “dark side of the moon”. European Journal of Clinical Investigation, 48(S2), e12952.CrossRefPubMedGoogle Scholar
  104. Tecchio, C., & Cassatella, M. A. (2016). Neutrophil-derived chemokines on the road to immunity. Seminars in Immunology, 28(2), 119–128.CrossRefPubMedGoogle Scholar
  105. Tsai, C. Y., Wolff, L. F., Germaine, G., & Hodges, J. (2003). A rapid DNA probe test compared to culture methods for identification of subgingival plaque bacteria. Journal of Clinical Periodontology, 30(1), 57–62.CrossRefPubMedGoogle Scholar
  106. Uriarte, S. M., Powell, D. W., Luerman, G. C., Merchant, M. L., Cummins, T. D., Jog, N. R., et al. (2008). Comparison of proteins expressed on secretory vesicle membranes and plasma membranes of human neutrophils. Journal of Immunology, 180(8), 5575–5581.CrossRefGoogle Scholar
  107. Uriarte, S. M., Edmisson, J. S., & Jimenez-Flores, E. (2016). Human neutrophils and oral microbiota: A constant tug-of-war between a harmonious and a discordant coexistence. Immunological Reviews, 273(1), 282–298.CrossRefPubMedPubMedCentralGoogle Scholar
  108. Vashishta, A., Jimenez Flores, E., Klaes, C. K., Tian, S., Miralda, I., Lamont, R. J., & Uriarte, S. M. (2019). Putative periodontal pathogens, Filifactor alocis and Peptoanaerobacter stomatis, induce differential cytokine and chemokine production by human neutrophils. Pathogens, 8(2), 59.CrossRefPubMedCentralGoogle Scholar
  109. Vitkov, L., Klappacher, M., Hannig, M., & Krautgartner, W. D. (2009). Extracellular neutrophil traps in periodontitis. Journal of Periodontal Research, 44(5), 664–672.CrossRefPubMedGoogle Scholar
  110. Wang, Q., Wright, C. J., Dingming, H., Uriarte, S. M., & Lamont, R. J. (2013). Oral community interactions of Filifactor alocis in vitro. PLoS One, 8(10), e76271.CrossRefPubMedPubMedCentralGoogle Scholar
  111. Wang, Q., Jotwani, R., Le, J., Krauss, J. L., Potempa, J., Coventry, S. C., et al. (2014). Filifactor alocis infection and inflammatory responses in the mouse subcutaneous chamber model. Infection and Immunity, 82(3), 1205–1212.CrossRefPubMedPubMedCentralGoogle Scholar
  112. White, P. C., Chicca, I. J., Cooper, P. R., Milward, M. R., & Chapple, I. L. (2016). Neutrophil extracellular traps in periodontitis: A web of intrigue. Journal of Dental Research, 95(1), 26–34.CrossRefPubMedGoogle Scholar
  113. Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N., Zbytnuik, L. D., et al. (2012). Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nature Medicine, 18(9), 1386–1393.CrossRefPubMedPubMedCentralGoogle Scholar
  114. Yost, S., Duran-Pinedo, A. E., Teles, R., Krishnan, K., & Frias-Lopez, J. (2015). Functional signatures of oral dysbiosis during periodontitis progression revealed by microbial metatranscriptome analysis. Genome Medicine, 7(1), 27.CrossRefPubMedPubMedCentralGoogle Scholar
  115. Zhang, C., Hou, B. X., Zhao, H. Y., & Sun, Z. (2012). Microbial diversity in failed endodontic root-filled teeth. Chinese Medical Journal, 125(6), 1163–1168.PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Irina Miralda
    • 1
    • 2
  • Aruna Vashishta
    • 1
  • Silvia M. Uriarte
    • 1
    • 2
    Email author
  1. 1.Department of MedicineSchool of Medicine, University of LouisvilleLouisvilleUSA
  2. 2.Department of Microbiology and ImmunologySchool of Medicine, University of LouisvilleLouisvilleUSA

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