Linking the Mechanics of Chewing to Biology of the Junctional Epithelium

Abstract

The capacity of a tissue to continuously alter its phenotype lies at the heart of how an animal is able to quickly adapt to changes in environmental stimuli. Within tissues, differentiated cells are rigid and play a limited role in adapting to new environments; however, differentiated cells are replenished by stem cells that are defined by their phenotypic plasticity. Here we demonstrate that a Wnt-responsive stem cell niche in the junctional epithelium is responsible for the capability of this tissue to quickly adapt to changes in the physical consistency of a diet. Mechanical input from chewing is required to both establish and maintain this niche. Since the junctional epithelium directly attaches to the tooth surface via hemidesmosomes, a soft diet requires minimal mastication, and consequently, lower distortional strains are produced in the tissue. This reduced strain state is accompanied by reduced mitotic activity in both stem cells and their progeny, leading to tissue atrophy. The atrophied junctional epithelium exhibits suboptimal barrier functions, allowing the ingression of bacteria into the underlying connective tissues, which in turn trigger inflammation and mild alveolar bone loss. These data link the mechanics of chewing to the biology of tooth-supporting tissues, revealing how a stem cell niche is responsible for the remarkable adaptability of the junctional epithelium to different diets.

Dynamic analyses of a soft tissue–implant interface: Biological responses to immediate versus delayed dental implants

“…Using a variety of injury repair models, we demonstrated that oral epithelial repair is generally made possible by tissue-resident stem cell niches (Byrd et al, 2019;Yuan et al, 2019;Yuan, Chen, Gauer, et al, 2020;. Under homeostatic conditions, these epithelial niches produce daughter cells that contribute to the continuous turnover of the epithelia (Byrd et al, 2019;Tanaka et al, 2021;Yuan et al, 2019Yuan et al, , 2023Yuan, Chen, Gauer, et al, 2020;. In response to injury, for example, extraction of a tooth, gingivectomy and placement of an implant, these same epithelial niches dramatically increase production of mitotically active daughter cells, which then migrate widely to occupy and heal the damaged areas (Yuan et al, 2021;Yuan, Chen, Gauer, et al, 2020;.…”

“…And if so, from where does this second cell population originate? We know something about the mechanisms, both physical and/or biological, that contribute to establishment of a JE stem cell niche (Yuan et al, 2023); could these same factors be reactivated to create a stem cell niche around implants? These questions form the basis of ongoing investigations by our group into methods to accelerate and rejuvenate barrier functions to the PIE.…”

“…Wnt signalling from the JE is required for stabilization of the hemidesmosomal proteins that directly mediate this soft-tissue attachment (Yuan et al, 2023), and Wnt and other biological signals require physical input in the form of distortional strains to maintain the stem cell niche and the attachment of JE to the tooth surface (Yuan et al, 2023).…”

“…For example, the JE is known to originate from the reduced enamel epithelium (REE) (Shimono et al, 2003) but the PIE develops from the oral epithelium (OE) (Yuan et al, 2021). The rate of cell proliferation in the PIE also varies dramatically, depending on the stage of healing (Yuan et al, 2021); in contrast, a consistently high mitotic index is a hallmark of an intact JE (Yuan et al, 2021(Yuan et al, , 2023Yuan, Chen, Gauer, et al, 2020). From that study, we concluded that the attachment of the PIE to the implant surface was sub-optimal compared to the attachment of an intact JE to a tooth surface (Yuan et al, 2021).…”

Enamel Matrix Derivative Suppresses Chemokine Expression in Oral Epithelial Cells

“…Periodontal health is difficult to maintain as the periodontium must steadily defend against the microbial and other burdens inherent to the oral cavity [ 1 , 2 , 3 ]. There is also mechanical damage to the gingiva coming from exaturated mastication that the periodontium has to deal with [ 4 ], however, physiological masticatory loaging is required for periodontal homeostasis [ 5 ]. Thus, the gingiva and the junctional epithelium with the periodontal ligament underneath build a vital barrier toward the oral cavity equipped with a defense system driven by inflammation [ 6 , 7 , 8 , 9 ].…”