Telocytes as a Novel Structural Component in the Muscle Layers of the Goat Rumen

Abstract

Telocytes (TCs) have been identified as a distinct type of interstitial cells, but have not yet been reported in the gastrointestinal tract (GIT) of ruminants. In this study, we used transmission electron microscopy (TEM) and double-labelling immunofluorescence (IF) (antibodies: CD34, vimentin and PGP9.5) to seek TCs and investigate their potential functions in the muscle layers of the goat rumen. TCs were distributed widely in the myenteric plexus (TC-MYs) between the circular and longitudinal muscle layers, within circular muscle layers (TC-CMs) as well as in longitudinal muscle layers (TC-LMs). Ultrastructurally, TCs displayed small cell bodies with several long prolongations—telopodes—harboring alternate thin segments (podomers) and dilated segments (podoms). The podoms contained mitochondria, rough endoplasmic reticulum, and caveolae. Telopodes frequently established close physical interactions with near telopodes, collagen fibers (CFs), nerve fibers (NFs), smooth muscle cells (SMCs), nerve tracts, and smooth muscle bundles, as well as with blood vessels (BVs). Furthermore, both homo- and heterotypic connections were observed. In addition, telopodes were capable of releasing extracellular vesicles (EVs). IF analyses proved that TCs were reliably labeled as CD34+/vimentin+ cells, displaying spindle- or triangle-shaped bodies with long prolongations, consistent with TEM results. Specifically, podoms were visible as obvious bright spots. These positive cells covered entire muscular layers, surrounding ganglions, intermuscular BVs as well as entire smooth muscle bundles, forming a network. TC-MYs were distributed as clusters in the external ganglion, encompassing the entire ganglion and spreading to the muscle layers where TC-CMs and TC-LMs seemingly surround whole smooth muscle bundles. TC-MYs were also scattered within the interior of the ganglion, surrounding each ganglionic neuron, following the glial cells layer. We speculate that TCs support the muscle layer structure of the goat rumen and facilitate intercellular signaling directly or indirectly via the TC network.

Identification of Telocytes in the Pancreas of Turtles—A role in Cellular Communication

“…Furthermore, the occurrence of this function in the myocardium has also been proposed [1,60,61]. Previous work shows the extracellular vesicles communicating in TCs mediated by intercellular communications [4,17,61]. In the present study, it was shown that TCs have intercellular communications with nearby cells through shading/extracellular vesicles.…”

“…Consistently, CD34+ TCs are also reported in other mammals, amphibia and reptiles. Previous studies report CD34+ telocytes in human exocrine pancreas [13], in the rumen of goat [4], in the pancreas of Chinese salamander [19], and in the oviduct [5] and testicular parenchyma of Chinese soft-shelled turtle [45]. Using double immunofluorescence analysis in the current study, we were able to exclude the presence of CD34+/α-SMA+ myofibroblast-like telocytes.…”

“…They were named interstitial Cajal-like cells (ICLCs) and interstitial cells of cajal (ICCs) based on their morphology, ultrastructural features, immunophenotype, and site of existence. Later on, ICLCs were renamed TCs [1][2][3][4]. These are moniliform and long structured cells, that sometimes form convoluted trajectories.…”

“…The cell body of TCs varies in shape (fusiform, pyriform, or triangular) depending on the number of Tps arising directly from the cell body; the latter measures between 9 to 15 µm in length. Podoms show caveolae, endoplasmic reticulum, and mitochondria, and are also involved in the uptake and release of calcium [3,4]. TCs frequently establish homo-junctions (telopodes to telopodes), as well as hetero-junctions with other structures of neighboring cells (nerve fibers, collagen fibers), to perform numerous functions and to form three-dimensional (3D) networks [1,[6][7][8][9][10].…”

“…This communication is achieved by releasing the microRNA-filled extracellular vesicles from TCs/Tps to regulate cell functions [22]. Although protein gene product 9•5 (PGP9.5) is a specific tissue marker for the neuroendocrine system and for certain tumors of the lung, colon, and pancreas, a study revealed that CD34, vimentin, tyrosine kinase receptor (c-kit), and PGP 9.5 can be used for TC identification [4]. TCs have been found in the interstitial spaces of the following major organs; namely, intestine [23], lungs [17,24], heart [25], trachea [24,26], parotid glands [27], pulmonary veins [28], pleura [17], skeletal muscle [29], pericardium [25], exocrine pancreas [13,19,30], mesentery [31], gall bladder, placenta [7,32,33], mammary gland, blood vessels [34][35][36][37], uterus, fallopian tube, female reproductive duct [38,39], endometrium [40], and myometrium [41,42].…”