Abstract

Long-term estivation (45 days) in the apple snail Pomacea canaliculata induces an increase of non-enzymatic antioxidants, such as uric acid and reduced glutathione (GSH), which constitutes an alternative to the adaptive physiological strategy of preparation for oxidative stress (POS). Here, we studied markers of oxidative stress damage, uric acid levels, and non-enzymatic antioxidant capacity, enzymatic antioxidant defenses, such as superoxide dismutase (SOD), catalase (CAT), and glutathione S-transferase (GST), and transcription factors expression [forkhead box protein O (FOXO), hypoxia-inducible factor-1 alpha (HIF1α), and nuclear factor erythroid 2-related factor 2 (Nrf2)] in control active animals, 7-day estivating and aroused snails, in digestive gland, gill, and lung tissue samples. In the digestive gland, SOD and CAT activities significantly increased after estivation and decreased during arousal. Meanwhile, GST activity decreased significantly during the activity–estivation–arousal cycle. Gill CAT activity increased significantly at 7 days of estivation, and it decreased during arousal. In the lung, the CAT activity level increased significantly during the cycle. FOXO upregulation was observed in the studied tissues, decreasing its expression only in the gill of aroused animals during the cycle. HIF1α and Nrf2 transcription factors decreased their expression during estivation in the gill, while in the lung and the digestive gland, both transcription factors did not show significant changes. Our results showed that the short-term estivation induced oxidative stress in different tissues of P. canaliculata thereby increasing overall antioxidant enzymes activity and highlighting the role of FOXO regulation as a possible underlying mechanism of the POS strategy.

Highlights

  • Several organisms live under harsh environmental conditions and have evolved different strategies to cope with them

  • Attempting to answer this question, we evaluated the physiological response at the tissue level, including the expression of REDOX-sensitive transcription factors, in a model of a short-term (7 days) activity–estivation–arousal cycle in P. canaliculata

  • Mollusks have been proposed as model organisms to study the preparation for oxidative stress (POS) strategy after estivation; freshwater gastropods have not received attention comparable to terrestrial gastropods (Hermes-Lima and Storey, 1995; Hermes-Lima et al, 1998; Ramos-Vasconcelos and Hermes-Lima, 2003; Nowakowska et al, 2009; Giraud-Billoud et al, 2011, 2013; Nowakowska et al, 2011)

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Summary

INTRODUCTION

Several organisms live under harsh environmental conditions and have evolved different strategies to cope with them. Proteomic studies in this species have shown that CAT expression increases after a 30-day-period of estivation (Sun et al, 2013) These findings suggest that, in the initial stages of the activity–estivation– arousal cycle, P. canaliculata prepares for oxidative stress through activating enzymatic antioxidant defense mechanisms, as is shown for other animal species (Hermes-Lima et al, 2015). A plausible hypothesis to test is that, once antioxidant enzymatic defenses are diminished by molecular or cellular alterations induced by stress, non-enzymatic defense mechanisms would play a leading role in tissue protection Attempting to answer this question, we evaluated the physiological response at the tissue level, including the expression of REDOX-sensitive transcription factors, in a model of a short-term (7 days) activity–estivation–arousal cycle in P. canaliculata. We (c) assessed for changes in the expression of REDOX-sensitive transcription factors (FOXO, HIF1α, and Nrf2) as potential molecular mechanisms that lead to the development of the POS strategy during the activity– estivation–arousal cycle

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