Cell Death in the Epithelia of the Intestine and Hepatopancreas in Neocaridina heteropoda (Crustacea, Malacostraca)

Abstract

The endodermal region of the digestive system in the freshwater shrimp Neocaridina heteropoda (Crustacea, Malacostraca) consists of a tube-shaped intestine and large hepatopancreas, which is formed by numerous blind-ended tubules. The precise structure and ultrastructure of these regions were presented in our previous studies, while here we focused on the cell death processes and their effect on the functioning of the midgut. We used transmission electron microscopy, light and confocal microscopes to describe and detect cell death, while a quantitative assessment of cells with depolarized mitochondria helped us to establish whether there is the relationship between cell death and the inactivation of mitochondria. Three types of the cell death were observed in the intestine and hepatopancreas–apoptosis, necrosis and autophagy. No differences were observed in the course of these processes in males and females and or in the intestine and hepatopancreas of the shrimp that were examined. Our studies revealed that apoptosis, necrosis and autophagy only involves the fully developed cells of the midgut epithelium that have contact with the midgut lumen–D-cells in the intestine and B- and F-cells in hepatopancreas, while E-cells (midgut stem cells) did not die. A distinct correlation between the accumulation of E-cells and the activation of apoptosis was detected in the anterior region of the intestine, while necrosis was an accidental process. Degenerating organelles, mainly mitochondria were neutralized and eventually, the activation of cell death was prevented in the entire epithelium due to autophagy. Therefore, we state that autophagy plays a role of the survival factor.

Functional cytology of the hepatopancreas of decapod crustaceans

“…Sonakowska et al () observed three modes of cell death in the midgut proper and hepatopancreas of Neocaridina davidi , namely necrosis, apoptosis, and autophagy. They found apoptosis mainly in the anterior part of the intestine, and autophagy mainly in the proximal region of the hepatopancreas tubules, that is, in the oldest cells.…”

“…The hepatopancreas of the Decapoda may serve as a comparative model for biologists studying the digestive systems of other animals, particularly invertebrates. It may also be of some value for investigating more general topics such as stem cell activity (Vogt, ), cell aging (Vogt, ), and cell death (Sonakowska et al, ). The polar architecture of the heptopancreas tubules with terminal stem cells and the distinct age gradient along the tubules offer particularly good conditions for such investigations.…”

“…This cell type has the same ultrastructure as the M‐cells of the hepatopancreas depicted in Figure . Rost‐Roszkowska and colleagues named the large cells in the intestine of shrimp Neocaridina davidi (Bouvier, 1904) D‐cells (digestive cells) and the small cells first E‐cells (embryonic cells; Sonakowska et al, ) and later R‐cells (regenerative cells; Sonakowska et al, ) and interpreted them as secretory cells and their progenitor cells, respectively.…”

The role of autophagy in the midgut epithelium of Parachela (Tardigrada)

“…However, three types are best known: apoptosis, necrosis and autophagy. They are common processes that occur in the digestive epithelia of invertebrates (Malagoli et al 2010; Franzetti et al 2012; Romanelli et al 2014, 2016; Wilczek et al 2014; Lipovšek and Novak 2015; Rost-Roszkowska et al 2015, 2016; Sonakowska et al 2016). When the cytoplasm is rich in autophagic structures, apoptosis and/or necrosis is activated (Levine and Yuan 2005; Giusti et al 2007; Tettamanti et al 2007; Rost-Roszkowska et al 2013b).…”

“…It is digested due to autophagy so numerous autophagic structures have been detected in the cytoplasm of the digestive cells during the later stages of oogenesis, which suggests the participation of this accumulated material in vitellogenesis and choriogenesis (Rost-Roszkowska et al 2011). The reserve material is commonly accumulated in the cytoplasm of the digestive cells in insects (Lipovšek et al 2011; Amiri and Bandani 2013; Lipovšek and Novak 2015), myriapods (Chajec et al 2012, 2014; Sosinka et al 2014), crustaceans (Sousa and Petriella 2000; Sonakowska et al 2016) and tardigrades (Rost-Roszkowska et al 2011; Hyra et al 2016). It can be exploited due to digestion that involves autophagy during the natural periods of starvation such as the hibernation (Lipovšek et al 2011; Kamińska et al 2016), molting (Franzetti et al 2012; Romanelli et al 2014, 2016) or during starvation that is caused by a lack of food in the environment in which the animal lives (Zaffagnini and Martens 2016).…”