Oxidative stress and antioxidative defense in cephalopods: a function of metabolic rate or age?

Abstract

Activities of the antioxidative enzymes superoxide dismutase (SOD), catalase, glutathione peroxidase (GPX) and glutathione reductase (GR) were measured in the cephalopods Sepia officinalis and Lolliguncula bre6is. Maximal enzyme activities were higher in gill tissue than in the mantle musculature of both species. Activities were generally lower in tissues of L. bre6is than in S. officinalis. Comparison with other ectothermic animals showed both cephalopod species to have a low enzymatic antioxidative status despite their high metabolic rate. Furthermore, changes in antioxidative enzyme activities were measured in the cuttlefish S. officinalis with increasing age. The concentrations of malondialdehyde (MDA) and lipofuscin were determined as indicators of lipid peroxidation. Investigated animals were between 1.5 months and over 12 months old. Changes of antioxidative enzyme activities with age were not uniform. SOD and GPX activities increased with age, while catalase activity declined. In contrast, GR activity remained almost unchanged in all age groups. The low level of antioxidative defense might allow for the significant age-induced rise in MDA levels in gills and mantle musculature and for the increase in lipofuscin levels in mantle and brain tissue. It might thereby contribute to increased oxidative damage and a short life span in these cephalopods.

Growth, metabolism and lipid peroxidation in Mytilus edulis: age and size effects

“…Regardless of body size, FAP concentrations increased exponentially with age between 2 and 10 yr. In some other species the FAP-age relationship is also reported to be exponential (Ju et al 1999, Zielinski & Pörtner 2000. However, there are publications where either no agerelated changes in FAP weight-specific content in molluscs are recorded (Clarke et al 1990, Hole et al 1993 or they are even negative depending on the tissue studied (Clarke et al 1990).…”

“…By contrast, M. edulis from the British Isles displayed higher MDA concentrations in older specimens (>10 yr old) compared to younger ones (2-4 yr old) (Viarengo et al 1989(Viarengo et al , 1991. In the cephalopod Sepia officinalis reared in the laboratory, low levels of MDA were observed until the specimens reached an age of 10 mo, when a significant increase in MDA was recorded (Zielinski & Pörtner 2000). Since MDA is a precursor of FAP (e.g.…”

“…Most authors observed different patterns in SOD and CAT activities with respect to age. A minor increase in or constant levels of SOD and a decrease in CAT activities with age have been reported for Mytilus edulis (Viarengo et al 1991), the marine shrimp Aristeus antennatus (Mourente & Diaz-Salvago 1999) and the cephalopod Sepia officinalis (Zielinski & Pörtner 2000). For some other species -the frog Rana perezi (López-Torres et al 1991), the polychaete Arenicola marina (Buchner et al 1996), laboratory rats (Cand & Verdetti 1989) -contrasting age-related changes in these enzymes (a decrease in SOD and an increase or no change in CAT) have been recorded.…”

Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress

“…This implies higher ROS-formation rates per cell with increasing mitochondrial density. Thus, antioxidant enzyme (AOX) activities tend to be higher in metabolically active tissues like liver and gills as compared to muscle tissue in fish (Lemaire et al, 1993;Ansaldo et al, 2000), digestive gland vs. body wall in polychaetes (Buchner et al, 1996), or gills vs. mantle tissue in cephalopods (Zielinski and Portner, 2000). In ä between species comparison this implies higher AOX activities in warm blooded mammals and birds as compared to cold blooded marine invertebrates.…”

Cell turnover in tissues of the long-lived ocean quahog Arctica islandica and the short-lived scallop Aequipecten opercularis

“…Since the pioneer work of Pearl (1928) and Harman (1956), proposing the 'Free Radical-Rate of Living theory', which predicts a negative correlation between mass specific respiration (MSR) and MLSP of a species, studies of ageing focus on the link between mitochondrial production of reactive oxygen species (ROS) and MSR. Applying this theory to the molluscs, a variety of physiological parameters such as growth, metabolism, antioxidant defence and accumulation of oxidative damage products have been studied in different tissues of several bivalves and squids in an age-dependent manner (Philipp et al 2005a(Philipp et al , b, 2006Strahl et al 2007;Abele et al 2008;Zielinski and Pörtner 2000). The long-lived Icelandic A. islandica has stable antioxidant capacities in mantle and gill over an age range of 30-200 years and the fluorescent age pigment lipofuscin, an oxidative stress and ageing marker, accumulates in several tissues as they age (Strahl et al 2007).…”