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Combined Astaxanthin and Fish Oil Supplementation Improves View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Repositório Institucional UNIFESP Chemico-Biological Interactions 197 (2012) 58–67 Contents lists available at SciVerse ScienceDirect Chemico-Biological Interactions journal homepage: www.elsevier.com/locate/chembioint Combined astaxanthin and fish oil supplementation improves glutathione-based redox balance in rat plasma and neutrophils Marcelo Paes Barros a, Douglas Popp Marin b, Anaysa Paola Bolin b, Rita de Cássia Santos Macedo b, Thais Regina Campoio b, Claudio Fineto Jr. b, Beatriz Alves Guerra b, Tatiana Geraldo Polotow a, ⇑ Cristina Vardaris a, Rita Mattei c, Rosemari Otton b, a Postgraduate Program, Human Movement Sciences, Institute of Physical Activity and Sport Sciences (ICAFE), Universidade Cruzeiro do Sul, 01506000 São Paulo, SP, Brazil b Postgraduate Program, Health Sciences, CBS, Universidade Cruzeiro do Sul, 03342000 São Paulo, SP, Brazil c Department of Psychobiology, Universidade Federal de São Paulo (UNIFESP), 04023062 São Paulo, SP, Brazil article info abstract Article history: The present study aimed to investigate the effects of daily (45 days) intake of fish oil (FO; 10 mg EPA/kg Received 3 November 2011 body weight (BW) and 7 mg DHA/kg BW) and/or natural ASTA (1 mg ASTA/kg BW) on oxidative stress and Received in revised form 9 March 2012 ÅÀ functional indexes of neutrophils isolated from Wistar rats by monitoring superoxide (O2 ), hydrogen Accepted 10 March 2012 Å peroxide (H O ), and nitric oxide (NO ) production compared to the progression of auto-induced lipid Available online 21 March 2012 2 2 peroxidation and Ca2+ release in activated neutrophils. Furthermore, phagocytic capacity, antioxidant enzyme activities, glutathione-recycling system, and biomarkers of lipid and protein oxidation in neutro- Keywords: phils were compared to the redox status. Our results show evidence of the beneficial effects of FO + ASTA DHA supplementation for immune competence based on the redox balance in plasma (significant increase in EPA Omega-3 GSH-dependent reducing power), non-activated neutrophils (increased activity of the glutathione-recy- ÅÀ Å Carotenoid cling enzymes GPx and GR) and PMA-activated neutrophils (lower O2 ,H2O2, and NO generation, reduced Anti-inflammatory membrane oxidation, but higher phagocytic activity). Combined application of ASTA and FO promoted Leukocyte hypolipidemic/hypocholesterolemic effects in plasma and resulted in increased phagocytic activity of activated neutrophils when compared with ASTA or FO applied alone. In PMA-activated neutrophils, ASTA was superior to FO in exerting antioxidant effects. The bulk of data reinforces the hypothesis that habitual consumption of marine fish (e.g. salmon, which is a natural source of both astaxanthin and fish oil) is beneficial to human health, in particular by improving immune response and lowering the risk of vascular and infectious diseases. Ó 2012 Elsevier Ireland Ltd. Open access under the Elsevier OA license. 1. Introduction effects on immune function due to the influence of PUFAs on mem- brane fluidity, which could result in higher sensitivity to oxidation Habitual intake of marine fish and seafood has been strongly [6,7]. Depending on the concentration, DHA and EPA can also affect associated with human health. It is particularly considered to the microstructure and composition of lipid rafts in the neutrophil enhance immune competence and prevent infectious diseases membrane, resulting in severe changes of cell–cell molecular com- [1]. Fish oil (FO) components eicosapentaenoic acid (EPA) and munication [8]. docosahexaenoic acid (DHA) – well-known as n-3 polyunsaturated Although anti-inflammatory mechanisms in humans have been fatty acids (n-3/PUFA) – have been studied in immune cells and well discussed, there are still unanswered questions with respect to proved to increase anti-inflammatory responses by stimulating redox imbalances provoked in neutrophils during the pathogen- interleukin production [2]. As central players in inflammatory pro- activation process. As a consensus, a wide range of reactive oxy- ÅÀ Å cesses, neutrophils are main protagonists of innate immune re- gen/nitrogen species ROS/RNS (including O2 ,H2O2, and NO ) are sponses necessary for early host defense [3]. Regarding continuously produced by neutrophil oxidative burst, and pathogen nutraceuticals, dietary long-chain (>C20) n-3/PUFAs are considered cells are undoubtedly not the only targets at the inflammatory site. antioxidant compounds, which significantly diminish superoxide In fact, ROS/RNS can also (auto)-oxidize neutrophil membrane, trig- ÅÀ (O2 ) and hydrogen peroxide (H2O2) production in activated gering lipid peroxidation and producing lipid-derived cytotoxic neutrophils [4,5]. On the other hand, fish oil also showed adverse aldehydes, e.g. malondialdehyde and 4-hydroxynonenal [9]. Thus, long-living/persistent neutrophils as part of an efficient immune system have to cope with huge oxidative challenges imposed by ⇑ Corresponding author. Tel./fax: +55 11 26726200. E-mail address: [email protected] (R. Otton). pathogen activation. Several authors have, therefore, proposed that 0009-2797 Ó 2012 Elsevier Ireland Ltd. Open access under the Elsevier OA license. http://dx.doi.org/10.1016/j.cbi.2012.03.005 M.P. Barros et al. / Chemico-Biological Interactions 197 (2012) 58–67 59 dietary programs based on antioxidant supplementation could of- (mostly palmitoleic and oleic acids), and 50% with polyunsaturated fer enhancement of immune functions, especially in terms of life- fatty acids (180 mg EPA and 120 mg DHA). Natural ASTA supple- span and slower turnover of damaged immune cells [10,11]. ments (AstaREAL A1010) were obtained as a donation from the Accordingly, many antioxidants present in human diet have also Swedish company BioReal AB (Gustavsberg, Sweden), a subsidiary positively affected immune functions in patients of ROS-related dis- of BioReal Inc., (Hawaii, USA) and part of the pharmaceutical Group eases, such as diabetes [12,13]. Fuji Chemical Industry CO. AstaREAL A1010 is an astaxanthin-rich The marine carotenoid astaxanthin (ASTA; Fig. 1) is naturally natural microalgal product, consisting of crushed and spray-dried found in a wide variety of aquatic organisms, such as microalgae, aplanospores of the green microalgae Haematococcus pluvialis. crustaceans (crabs, lobsters, and shrimp), and fishes (salmon and AstaREAL A1010 contains 42% of crude fat, 10% of crude protein, trout). ASTA is renowned as a powerful antioxidant [14,15], and 40% of carbohydrates, and 4% of ashes. Regarding carotenoid com- also reported to afford benefits to human health, including photo- position, AstaREAL A1010 contains 5.2–5.8% of total carotenoids, protection against UV radiation (skin and eyes) [16], prophylaxis/ 5.0–5.6% of which are being pure astaxanthin (3.9% as monoesters, remediation of gastric ulcer induced by Helicobacter pylori [17], 0.9% as diesters, and 0.1% in free form) among others. and ROS-mediated neurodegenerative processes, as in Parkinson’s disease [18]. Thus, it is reasonable to assume that combined FO 2.3. Animals and supplementation protocols and ASTA supplementation could better balance pro- and antioxi- dative events in activated neutrophils to enhance anti-inflamma- Adult Wistar male rats, weighing 191 ± 35 g at the beginning of tory responses and, thus, provide substantial health benefits to the study, were provided by the Department of Psychobiology, Uni- humans. versidade Federal de São Paulo (UNIFESP), São Paulo, Brazil. All ani- The present study aimed to investigate the effects of daily in- mals were housed in plexiglas cage (four rats/cage), under take of natural sources of n-3/PUFAs (here provided as fish oil) standard laboratory conditions: 12 h light/dark cycle; lights on at and/or natural ASTA (obtained from the biomass of the green mic- 7:00 a.m.; 22 ± 1 °C; water and Purina rat chow ad libitum. The ani- roalgae Haematococcus pluvialis) [19] on oxidative stress and func- mals used in this study were handled in accordance with the tional indexes of neutrophils isolated from Wistar rats. This study guidelines of the committee on care and use of laboratory animal ÅÀ was performed by monitoring superoxide (O2 ), hydrogen peroxide resources of the Ethics Committee on Care and Use of Laboratory Å (H2O2), and nitric oxide (NO ) production compared to the progres- Animal Resources from Universidade Federal de Sao Paulo, which sion of auto-induced lipid peroxidation and Ca2+ release in acti- approved the study protocol (CEP/UNIFESP n° 1938/09). The ani- vated neutrophils. Furthermore, our study evaluated antioxidant mals were treated with ASTA and/or FO by gavage, 5 days a week, enzyme activities, the glutathione-recycling system and biomark- for 45 days. A maximum volume of 400 lL was established for the ers of lipid and protein oxidation as related to the FO and/or ASTA gavage treatment in order to prevent regurgitation or stomach dis- diet, and examined the redox status in plasma as well as in isolated comfort of the animals. Fish oil (FO) content of capsules was di- resting and stimulated neutrophils from experimental animals. luted in 10% Tween 80 aqueous solution (v/v) to reach final n-3/ PUFAs concentrations of 10 mg EPA/kg body weight (BW) and 2. Materials and methods 7 mg DHA/kg BW. An identical procedure was conducted for ani- mal supplementation with 1 mg ASTA/kg BW using AstaREAL 2.1. Chemicals A1010 as the carotenoid source (5.3% of which is
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