Exposure to the Neurotoxic Dinoflagellate, Alexandrium catenella, Induces Apoptosis of the Hemocytes of the Oyster, Crassostrea gigas

Abstract

This study assessed the apoptotic process occurring in the hemocytes of the Pacific oyster, Crassostrea gigas, exposed to Alexandrium catenella, a paralytic shellfish toxins (PSTs) producer. Oysters were experimentally exposed during 48 h to the toxic algae. PSTs accumulation, the expression of 12 key apoptotic-related genes, as well as the variation of the number of hemocytes in apoptosis was measured at time intervals during the experiment. Results show a significant increase of the number of hemocytes in apoptosis after 29 h of exposure. Two pro-apoptotic genes (Bax and Bax-like) implicated in the mitochondrial pathway were significantly upregulated at 21 h followed by the overexpression of two caspase executor genes (caspase-3 and caspase-7) at 29 h, suggesting that the intrinsic pathway was activated. No modulation of the expression of genes implicated in the cell signaling Fas-Associated protein with Death Domain (FADD) and initiation-phase (caspase-2) was observed, suggesting that only the extrinsic pathway was not activated. Moreover, the clear time-dependent upregulation of five (Bcl2, BI-1, IAP1, IAP7B and Hsp70) inhibitors of apoptosis-related genes associated with the return to the initial number of hemocytes in apoptosis at 48 h of exposure suggests the involvement of strong regulatory mechanisms of apoptosis occurring in the hemocytes of the Pacific oyster.

The paralytic shellfish toxin, saxitoxin, enters the cytoplasm and induces apoptosis of oyster immune cells through a caspase-dependent pathway

“…gigas (Medhioub et al 2013). Altogether, these data support a mechanism for PST-induced apoptosis in bivalve hemocytes that is independent of ROS production.…”

“…Previous studies have shown that PSTproducing algae increase the mortality of C. gigas hemocytes both in vitro (Hegaret et al 2011;Lassudrie et al 2016) and in vivo (Medhioub et al 2013). However, fundamental features of this process, including key mechanistic details of how specific PSTs cause toxicity, remained poorly characterized.…”

“…More recently and in contrast to the non-toxic Alexandrium tamarens, the neurotoxic Alexandrium catenella has been found to induce apoptosis (Medhioub et al 2013) and mortality (Hegaret et al 2007b;Lassudrie et al 2016) in hemocyte immune cells of Crassostrea gigas.…”

“…Although filtration of toxic algae by oysters was shown to alter hemocyte functions (Medhioub et al 2013), it remains unclear whether PSTs directly cause these deleterious effects. Studies were therefore conducted to determine if PSTs, produced by Alexandrium catenella, are responsible for apoptosis of hemocytes in Crassostrea gigas exposed to toxic algae.…”

Adult somatic progenitor cells and hematopoiesis in oyster

“…Both in vivo and in vitro infections were shown to result in hemocyte phagocytosis, respiratory burst and finally in apoptosis (Goedken et al, 2005). In addition, detoxification of environmental pollutants, including of toxic substances produced by harmful algal blooms, has been shown to induce massive apoptotic death among the hemocyte population in bivalves (Medhioub et al, 2013;Ray et al, 2013;Yao et al, 2013;Prado-Alvarez et al, 2013). Finally, a physiological process not related to immune defense, shell mineralization, also leads to an important loss of hemocytes because it requires the migration of numerous hemocytes to the surface of the shell-facing outer mantle epithelium (Mount et al, 2004).…”