Bacterial invasion of epithelial cells and spreading in periodontal tissue

Abstract

The composition of the subgingival bacterial microbiota is a critical determinant in the health status of periodontal tissues. Gram-negative anaerobes such as Porphyromonas gingivalis are well-established periodontal pathogens, and high numbers of these bacteria are found in the subgingival sulcus of patients with chronic periodontitis (43). However, a burgeoning pool of evidence indicates that these organisms have a far more complex relationship with the host than merely as pathogens. Gram-negative anaerobes are frequently present in the oral cavity of periodontally healthy individuals (23, 44, 92, 121, 127, 128, 170), and indeed health is the most common status of the human gingiva despite years of exposure to a large microbial burden. Periodontal organisms thus appear to have co-evolved with their host to maintain an ecologically balanced association whereby minimal harm is inflicted on, or by, either party. Disease will only ensue when this interaction becomes unbalanced, an event that has been termed an ecological catastrophe (83). Organisms such as P. gingivalis may thus be more accurately characterized as accidental, or host-adapted, pathogens. In the subgingival compartment, epithelial cells represent a major host interface for colonizing organisms; hence, the interaction between gingival epithelial cells and periodontal bacteria will contribute to the success or failure of colonization, and to the maintenance of health or disease in the host. Undeniably, in the case of P. gingivalis, an intricate and multithreaded relationship exists between the organism and gingival epithelial cells, which, under optimal conditions, results in stable cohabitation, with both bacteria and host cells responding and adapting to the presence of their partner to maintain a state of health. In the event that this relationship becomes perturbed, for example because of an increase in bacterial burden or an inappropriate immune response, the periodontal disease process can be initiated (13). The ability to adapt in response to the host environment is reflected in the genetic diversity found within many species of periodontal bacteria. Bacteria are masters of adaptation, and at the genetic level are able to rapidly modify and share DNA. For example, there are significant levels of genetic variation among P. gingivalis strains, and many studies have linked this genetic variability to virulence potential (7, 14, 18, 38, 67, 85, 108). Genetic variability among strains is common in bacteria with long-term carrier states, possibly arising from the co-evolutionary dynamic of host–pathogen interactions (62, 123). Genetic variation can produce lineages of bacteria with `good or evil' personalities, in that some are more virulent and associated with disease, whereas other strains of the same species behave in a more commensal manner. In this review, we will discuss the current understanding of pathogenic and commensal aspects of bacterial interactions with periodontal tissues, with a specific focus on P. gingivalis intracellular invasion and molecular modulation of host cells.