Embryonic development of parakeratinized epithelium of the tongue in the domestic duck (Anas platyrhynchos f. domestica): LM, SEM, and TEM observations

Abstract

The parakeratinized epithelium is a common and widespread type of keratinized epithelium in the oral cavity in adult birds. In contrast to orthokeratinized epithelium, which mostly covers mechanical papillae and the lingual nail, parakeratinized epithelium covers almost the entire dorsal surface of the tongue in birds. The characteristic feature of parakeratinized epithelium is the presence of nuclei in the keratinized layer. The present study aimed to investigate for the first time the micro- and ultrastructural changes of parakeratinized epithelium during embryonic development and to assess the readiness of the epithelium to serve protective functions during food transport to the esophagus. Three developmental stages were distinguished: embryonic, transformation, and pre-hatching stages. The embryonic stage lasts from the 9th to the 14th day of incubation and the epithelium is composed of undifferentiated epithelial cells. The transformation stage lasts from the 15th to the 22nd day of incubation and the epithelium undergoes transformation into stratified epithelium consisting of basal, intermediate, and superficial layers. The characteristic feature of this stage is formation of the periderm with osmophilic granules. The pre-hatching stage starts on the 23rd day, and the epithelium with a fully developed keratinized layer resembles that of the epithelium in adult animals. No periderm was observed on the epithelial surface. It was confirmed that at the time of hatching the parakeratinized epithelium is fully differentiated and ready to fulfill its function during food transport. The presence of periderm is a common feature characteristic for para- and orthokeratinized epithelium in the oral cavity of birds. However, the formation of the keratinized/cornified layer is different for these two types of keratinized epithelia.

Morphology of the Atlantic salmon (Salmo salar)tongue

“…Morphological data, particularly on tongue of different species of fish, are present in literature (Abbate et al., 2006, 2017; Abbate, Guerrera, Montalbano, Ciriaco, & Germanà, 2012; Abbate, Guerrera, Montalbano, De Carlos, et al, 2012; Collar, O'Meara, Wainwright, & Near, 2009; Dos Santos, Arantes, Santiago, & Santos, 2015; El Bakary, 2014; Elgendy, Alsafy, & Tanekhy, 2016; Guerrera et al., 2015; Ikpegbu, Ibe, & Nlebedum, 2019; Levanti et al., 2017; Mahmoud, Essa, & Sayed, 2016; Montalbano et al, 2016; Price et al., 2010; Sadeghinezhad, Rahmati‐Holasoo, Fayyaz, & Zargar, 2015; Yashpal, Kumari, Mittal, & Mittal, 2009). Nevertheless, recent data regarding the tongue anatomy in upper vertebrates are significative and could be very important in comparative anatomy (Abbate et al., 2008, 2009, ; Emura, 2016a, 2016b, 2016c, 2017, 2018a, 2018b, 2018c, 2018d; Emura & Sugiyama, 2016; Erdogan & Alan, 2012; Erdoğan & Iwasaki, 2014; Erdoğan, Lima, & Pérez, 2016; Erdoğan & Sağsöz, 2018; Erdoğan, Villar Arias, & Pérez, 2016; Erdoğan, Villar, König, & Pérez, 2018; Herrel, Redding, Meyers, & Nishikawa, 2014; Jackowiak, Skieresz‐Szewczyk, Godynicki, Iwasaki, & Meyer, 2011; Jackowiak, Skieresz‐Szewczyk, Kwiecińsk, Trzcielińska‐Lorych, & Godynicki, 2010; Sadeghinezhad et al., 2015; Sadeghinezhad, Sheibani, Memarian, & Chiocchetti, 2017; Sadeghinezhad, Tootian, & Javadi, 2018; Skieresz‐Szewczyk, Cornillie, & Jackowiak, 2018; Skieresz‐Szewczyk & Jackowiak, 2016, 2017; Skieresz‐Szewczyk, Jackowiak, & Ratajczak, 2018, 2019). The objective of this study is to investigate, by light, laser confocal and scanning electron microscopy, the morphological characteristics of the tongue, considering the importance of the correlations between feeding habits and...…”

Unique pattern of histogenesis of the parakeratinized epithelium on lingual prominence in the domestic goose embryos (Anser anser f. domestica)

“…The next developmental stage, the transformation stage, in the epithelium of the lingual prominence in the domestic goose lasted from 16th to 23rd day of incubation. This stage in the parakeratinized epithelium of the lingual body lasts from 15th to 22nd day of incubation, and in the orthokeratinized epithelium from 14 to 20th day 24,26 .…”

“…Previous histological and ultrastructural studies on the development of the parakeratinized epithelium of the flat lingual body and the orthokeratinized epithelium of the ventral surface of the lingual apex in domestic duck have shown that differentiation of the cornified epithelia occurs at three developmental stages: embryonic stage, transformation stage and pre-hatching stage 24,26 .…”

“…The only studies concerning the development of the orthokeratinized epithelium on the conical papillae of the tongue were proceeded in chicken by using the scanning electron microscopy 30 and in the domestic goose and duck by using light microscopy and scanning electron microscopy 23,25,31 . Later histological and ultrastructural studies in the scanning and transmission electron microscopy were conducted by the Skieresz-Szewczyk et al 24,26 and describe the development of the orthokeratinized epithelium on the ventral surface of the lingual apex and parakeratinized epithelium of the flat lingual body in the domestic duck. Those studies give detailed information about the histodifferentiation of these epithelia during embryonic period.…”

“…The embryonic stage, characterized by undifferentiated epithelial cells convex over the surface of the epithelium, on the lingual prominence in domestic goose, lasted until day 15 of incubation. While in the parakeratinized epithelium of the lingual body and the orthokeratinized epithelium, the embryonic stage lasts shorter until 13th/14th day of incubation 24,26 .…”