Degeneration of the midgut epithelium in Epilachna cf. nylanderi (Insecta, Coccinellidae): apoptosis, autophagy, and necrosis

Abstract

This study investigates mechanisms of adaptation to metal toxicity peculiar to the midgut epithelium of Epilachna cf. nylanderi (Mulsant, 1850) (Coccinellidae). This species of beetle has currently been identified in only one locality in South Africa and is known to feed on the nickel hyperaccumulator Berkheya coddii Roessl. (Asteraceae), an endemic plant species of the South African ultramafic ecosystem. Our focus involves an analysis of the morphological features of cells forming the midgut epithelium, which is the first organ exposed to toxic levels of metals ingested by the insect. Through the three key processes of apoptosis, necrosis, and autophagy, excess metals are eliminated from the organism and homeostatic conditions are maintained. Apoptosis and necrosis are both known to be involved in the degradation of midgut epithelial cells, while the role of autophagy is mainly implicated in the disintegration of the organelles of cells. This study reports on the participation of these three key degenerative processes in the removal of excess metals based on targeted observations of the insect midgut epithelium by light and electron microscopies. Additionally, the TUNEL reaction was specifically used to detect apoptosis.

Apoptosis and necrosis during the circadian cycle in the centipede midgut

“…Thus, apoptosis represents a mechanism that protects against infection and inflammation in the different organs and tissues of the organism. Similar results have been described in the digestive epithelium of many arthropods (Baton and Ranford-Cartwright 2007;Rost-Roszkowska et al 2008, 2015b. S. cingulata did not have any rickettsia-like microorganisms in the cytoplasm of the digestive cells.…”

“…Many stress factors that originate from the external environment can disrupt and damage cell organelles, causing the activation of the cell death pathways (Okuda et al 2007;Menze et al 2010;Maghsoudi et al 2012;Jain et al 2013;Teixeira et al 2013;Lipovšek and Novak 2015). Among all of the processes of cell death that are known, only apoptosis, necrosis, and autophagy have been clearly described in the digestive epithelium of invertebrates (Parthasarathy and Palli 2007;Park and Takeda 2008;Park et al 2009;Tettamanti et al 2011;Franzetti et al 2012;Rost-Roszkowska et al 2008, 2015bLipovšek and Novak 2015). Additionally, functions of the digestive cells (e.g., enzymes synthesis, transport of ions and nutrients, storage of the reserve material and toxic substances) can cause the accumulation of reactive oxygen species (ROS), which trigger apoptosis and necrosis.…”

“…Inflammation is activated when apoptotic cells do not release their organelles and content into the extracellular space that surrounds neighboring tissues and where they are phagocytosed by the surrounding cells, e.g., macrophages and/or parenchymal cells (Kurosaka et al 2003;Elmore 2007). In the midgut epithelium of invertebrates, cells that have phagocytic abilities do not appear and therefore, another mechanism is created-apoptotic cells or apoptotic bodies are discharged into the gut lumen where they are digested (Rost-Roszkowska et al 2008, 2015b. To date, the dependence between apoptosis and circadian rhythms has been described in vertebrates Potten 1988, 1990;Granda et al 2005;Sankar 2011a, 2011b), while no information can be found in the literature about these processes in the gut epithelium of invertebrates.…”

Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae)

“…These changes together with changes in level of cytoplasmic membrane and cytoskeleton, such as cell swelling, loss of microvilli, formation of cytoplasmic protrusions, intercellular spaces and disruption of the cytoplasmic membrane are very diverse evidence of the process of cell degeneration by necrosis (Nasiruddin and Mordue (Luntz), 1993;Cheville, 1994Cheville, , 2009Proskuryakov et al, 2003;Gregorc et al, 2004;Ziegler and Groscurth, 2004;Rello et al, 2005;Rost-Roszkowska et al, 2008).…”

Morpho-functional characterization and esterase patterns of the midgut of Tribolium castaneum Herbst, 1797 (Coleoptera: Tenebrionidae) parasitized by Gregarina cuneata (Apicomplexa: Eugregarinidae)

“…The majority of proteins synthesised by endocrine cells are polypeptide hormones that are involved in the proliferation and differentiation of regenerative cells (Parthasarathy and Palli, 2008), peristaltic movements (Nässel et al, 1995), synthesis and secretion of digestive enzymes (Brown et al, 1985), diuresis (Patel et al, 1995), development and reproduction (Woodhead et al, 1989), and the activity of the central nervous system and the fat body of insects (Billingsley and Lehane, 1996;Rost-Roszkowska et al, 2008b;Sehnal and Zitnan, 1996).…”