Telocytes constitute a widespread interstitial meshwork in the lamina propria and underlying striated muscle of human tongue

Irene Rosa,Mirko Manetti,Cecilia Taverna,Lidia Ibba-Manneschi,Mirca Marini,Luca Novelli

doi:10.1038/s41598-019-42415-3

Irene Rosa, Mirko Manetti + Show 4 more

Open Access

https://doi.org/10.1038/s41598-019-42415-3

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Abstract

Telocytes have recently emerged as unique interstitial cells defined by their extremely long, thin and moniliform prolongations termed telopodes. Despite growing evidence that these cells consistently reside in the stromal compartment of various organs from human beings, studies dealing with telocytes in structures of the oral cavity are scarce. Hence, the present morphologic study was undertaken to explore for the first time the presence and specific localization of telocytes within tissues of the normal human tongue, a complex muscular organ whose main functions include taste, speech, and food manipulation in the oral cavity. Telocytes were initially identified by CD34 immunostaining and confirmed by CD34/PDGFRα double immunofluorescence and transmission electron microscopy. CD34+/PDGFRα+ telocytes were organized in interstitial meshworks either in the tongue lamina propria or in the underlying striated muscle. Lingual telocytes were immunonegative for CD31, c-kit and α-SMA. Telopodes were finely distributed throughout the stromal space and concentrated beneath the lingual epithelium and around CD31+ vessels, skeletal muscle bundles/fibers, and intramuscular nerves and ganglia. They also enveloped salivary gland units outside the α-SMA+ myoepithelial cells and delimited lymphoid aggregates. These findings establish telocytes as a previously overlooked interstitial cell population worth investigating further in the setting of human tongue pathophysiology.

Highlights

During the last decade, there has been substantial progress in our understanding of the morphofunctional characteristics of a variety of organs from different systems thanks to the discovery of a previously neglected cell population residing in the stromal space, namely telocytes (TCs)[1,2,3,4,5,6]
In keeping with a large body of research on TCs published over the last decade[9,10,16,17,18,44], we started by studying TCs within tissues of the human tongue by means of immunoperoxidase-based immunohistochemical detection of the CD34 cell surface antigen (Figs 1 and 2)
We selected archival paraffin-embedded human tongue sections that, according to routine histologic analysis, exhibited a normal microscopic structure consisting of a mass of interlacing skeletal muscle bundles firmly bound to the overlying oral mucosa by a dense connective tissue, with numerous mucous and serous accessory salivary glands scattered throughout the tongue lamina propria and muscle (Figs 1A and 2A)

Summary

Introduction

There has been substantial progress in our understanding of the morphofunctional characteristics of a variety of organs from different systems thanks to the discovery of a previously neglected cell population residing in the stromal space, namely telocytes (TCs)[1,2,3,4,5,6]. As far as the digestive system is concerned, these cells have been uncovered in different portions of the gastrointestinal tract, but, to the best of our knowledge, reports dealing with TCs in structures of the oral cavity are scarce[6,7,16,19,21,43] We undertook this morphologic study to provide a first proof of the existence and microanatomic localization of TCs in tissues of the normal human tongue, a peculiar striated muscular organ covered in oral mucosa with functions as various as taste, speech, food manipulation and swallowing initiation

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