Defense Date

2025

Document Type

Dissertation

Degree Name

Doctor of Philosophy

Department

Microbiology & Immunology

First Advisor

Daniel Miller, Ph.D.

Second Advisor

Kimberly Jefferson, Ph.D.

Third Advisor

Jennifer Koblinski, Ph.D.

Fourth Advisor

Jason Carlyon, Ph.D.

Fifth Advisor

Michael McVoy, Ph.D.

Abstract

Periodontitis is a chronic inflammatory disease driven by dysbiotic microbial communities and maladaptive host responses. Treponema denticola, a spirochete pathobiont, is strongly associated with disease severity. However, the molecular mechanisms underlying its interaction with host tissues and regulation of virulence remain incompletely understood. This work examines both the epithelial immune responses and bacterial transduction systems that shape T. denticola pathogenesis. Transcriptomic analysis of gingival keratinocytes revealed IL-36γ as the most highly induced cytokine following infection with T. denticola. Functional studies demonstrated that IL-36γ induction occurs in a dose- and time-dependent manner through TLR2/6 signaling, requiring the NF-κB, PI3K/Akt, and MAPK pathways. MSK1 was identified as a novel regulator of IL-36γ. Interestingly, mutants lacking dentilisin or Msp elicited increased IL-36γ expression, suggesting additional surface components also contribute to epithelial signaling. These findings position IL-36γ as a key cytokine in the epithelial response to T. denticola infection, highlighting the complexity of host–pathogen interactions at the gingival barrier. The AtcS/AtcR two-component system was also investigated as a regulator of T. denticola virulence. Transcriptomic profiling of the ΔatcS strain showed that AtcS is involved in the expression of genes related to transport, chemotaxis, and proteolysis. Loss of AtcS impaired motility, dentilisin activity, and epithelial adherence, while also reducing alveolar bone loss in vivo. These findings establish AtcS/R as a central signaling hub in spirochetal physiology and pathogenesis. Overall, these studies define IL-36γ as a major epithelial immune effector and AtcS as an essential bacterial regulator, advancing our understanding of T. denticola biology. Future research should focus on clarifying the mechanisms of IL-36γ secretion, the downstream targets of AtcR, and the potential of these pathways as therapeutic options in periodontal disease.

Rights

© Annie Nicole Hinson

Is Part Of

VCU University Archives

Is Part Of

VCU Theses and Dissertations

Date of Submission

9-15-2025

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