Periodontitis-resistant and -susceptible matriline regulation of gingival transcriptome in nonhuman primates

J Periodontal Res. 2023 Dec;58(6):1171-1187. doi: 10.1111/jre.13162. Epub 2023 Aug 28.

Abstract

Objective: This report identified if gingival gene expression transcriptomes demonstrated unique profiles that discriminated periodontitis-susceptible (PDS) and periodontitis-resistant (PDR) animals in health and disease.

Background: Nonhuman primates generally organize their social groups based upon matriline origin. We have used a multi-generational colony of rhesus macaques to identify matrilines presenting with significant differences in periodontitis (e.g., earlier age onset, greater prevalence, and severity).

Methods: Animals from 12 to 23 years of age (n = 17; 8 - PDR, 9 - PDS) were entered into a ligature-induced periodontitis trial. Gingival biopsies were taken at baseline and 0.5, 1, 3, and 5 months post-ligation, and microarray analysis was used to quantify gene expression in samples at each time point.

Results: Over 1000 genes showed significant (p < .01) differences in the PDR versus PDS animals at baseline. The frequency of differences generally decreased during the disease process, and increased with resolution (i.e., 5 months). A nearly 2:1 ratio of elevated gene levels was noted in baseline PDR samples that included up-regulated MMPs, Fc receptors, chemokines, interleukins, and innate immune receptors, and down-regulated genes particularly related to epithelial biology. Most dramatically, there was a skewed differential expression of adaptive immune response genes in the PDR and epithelial cell structure/function genes in PDS samples.

Conclusions: The results demonstrate substantive differences in gingival tissue response capacity/programming in PDR and PDS samples that may contribute to the differences in clinical outcomes related to the heritability of disease risk through matrilines.

Keywords: gingiva; nonhuman primates; periodontitis; transcriptome.

MeSH terms

  • Animals
  • Disease Susceptibility
  • Gingiva / pathology
  • Macaca mulatta / genetics
  • Periodontitis* / pathology
  • Transcriptome* / genetics