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Review
. 2024 Jan 6;25(2):737.
doi: 10.3390/ijms25020737.

Mitochondria: An Emerging Unavoidable Link in the Pathogenesis of Periodontitis Caused by Porphyromonas gingivalis

Shiyin Luo  1 , Tong Xu  1 , Qifan Zheng  1 , Aijia Jiang  1 , Jiahui Zhao  1 , Yue Ying  1 , Nan Liu  1 , Yaping Pan  2 , Dongmei Zhang  2
Affiliations
Review

Mitochondria: An Emerging Unavoidable Link in the Pathogenesis of Periodontitis Caused by Porphyromonas gingivalis

Shiyin Luo et al. Int J Mol Sci. .

Abstract

Porphyromonas gingivalis (P. gingivalis) is a key pathogen of periodontitis. Increasing evidence shows that P. gingivalis signals to mitochondria in periodontal cells, including gingival epithelial cells, gingival fibroblast cells, immune cells, etc. Mitochondrial dysfunction affects the cellular state and participates in periodontal inflammatory response through the aberrant release of mitochondrial contents. In the current review, it was summarized that P. gingivalis induced mitochondrial dysfunction by altering the mitochondrial metabolic state, unbalancing mitochondrial quality control, prompting mitochondrial reactive oxygen species (ROS) production, and regulating mitochondria-mediated apoptosis. This review outlines the impacts of P. gingivalis and its virulence factors on the mitochondrial function of periodontal cells and their role in periodontitis.

Keywords: Porphyromonas gingivalis; energy metabolism; mitochondria; mitochondrial dysfunction; mitochondrial quality control; periodontitis.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Diagram of how Porphyromonas gingivalis (P. gingivalis) participates in periodontal inflammation by interfering with mitochondria. P. gingivalis has multiple virulence factors that can launch an attack at the host cells. When macrophages are infected, the center of the cellular energy metabolism transfers from oxidative phosphorylation (OXPHOS) into glycolysis, and macrophages differentiate toward the pro-inflammatory M1 phenotypes. Under defective OXPHOS, abnormal electrons released from the electron transport chain (ETC) drive reactive oxygen species (ROS) formation and oxidize mitochondrial DNA (mtDNA) into fragmentation. ROS propel the release of pro-inflammatory factors by activating the P38/JNK and NF-κB signaling pathways and forming a feedback loop with p53. Additionally sustained mtDNA efflux through the ROS/mitochondrial permeability transition pore (mPTP) pathway was found under P. gingivalis infection, which also contributes to inflammation. In addition, plenty of studies have confirmed that by modulating mitochondria-associated apoptotic molecules, P. gingivalis and its virulence factors inhibited periodontal cell apoptosis, thereby prolonging periodontal inflammation, such as in human gingival fibroblasts (HGFs), gingival epithelial cells (GECs), dendritic cell (DCs), peripheral blood mononuclear cells (PBMCs), epithelial cells (ECs), etc. Nonetheless, P. gingivalis promoting apoptosis in a mitochondrial manner has also been documented in some host cells, such as in macrophages and ECs, as a way to indicate its toxicity. Together, these cytopathic alterations illustrate the inflammatory damage in infected periodontal tissues.
Figure 2
Figure 2
P. gingivalis induces mitochondrial quality control imbalance in HGFs and macrophages. Upon P. gingivalis infection, the life cycle of mitochondria turns into chaos. P. gingivalis down-regulates mitochondrial biogenesis by inhibiting the expression of PGC1-α and TFAM. It also stimulates mitochondrial fission by inducing DRP1 expression, leading to mitochondrial fragments. Additionally, P. gingivalis blocks mitophagy by suppressing PINK1/Parkin expression and intracellular lysosome quantity, and results in the failure of dysfunctional mitochondria elimination. The dysregulation of mitochondrial homeostasis culminates in a decrease in overall mitochondrial mass and disruption of energy metabolism, therefore deranging normal cellular behavior.
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