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Oxidative Stress and Fish Immune System: Phagocytosis and Leukocyte Respiratory Burst Activity Anais da Academia Brasileira de Ciências (2018) 90(4): 3403-3414 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201820170730 www.scielo.br/aabc | www.fb.com/aabcjournal Oxidative stress and fish immune system: phagocytosis and leukocyte respiratory burst activity JAQUELINE D. BILLER and LEONARDO S. TAKAHASHI Universidade Estadual Paulista/UNESP, Faculdade de Ciências Agrárias e Tecnológicas/FCAT, Campus de Dracena, Rodovia Comandante João Ribeiro de Barros, Km 651, Bairro das Antas, 17900-000 Dracena, SP, Brazil Manuscript received on September 18, 2017; accepted for publication on February 19, 2018 ABSTRACT Molecular oxygen is a necessary compound for all aerobic organisms, although oxygen is a potent oxidant, which can cause oxidative stress (OS). OS occurs when there is an imbalance between the production of oxidant and antioxidants components, are result of normal cell metabolism, and many of these compounds play a fundamental role in several metabolic pathways. The organism produces several reactive oxygen species (ROS), but they are balanced by an antioxidant defense system that maintains the levels of these oxidizing compounds at an acceptable level. Many of these components are essential in the organism defense and their byproducts are considered potent bactericides that actively act in the destruction of invading pathogens. Fish immune system is composed of innate and acquired mechanisms of defense. Phagocytosis is an innate process of defense, which interconnects these two systems, since the pathogens processing by professional phagocytes is a fundamental stage for antibodies production. During phagocytosis there is production of ROS and consequent production of free radicals (FR), these compounds lead to the formation of potent bactericides to combat microorganisms. However, it is known that OS limits the immune response, with an impairment in defense compounds in an attempt to decrease the ROS production. Studies of fish FR production are preliminary and should be executed to evaluate the effects of ROS on fish, including their beneficial action against pathogens and its deleterious action on the oxidation of cellular components. Key words: reactive oxygen species, innate immunity, antioxidant system, free radical. INTRODUCTION metabolism, and many of these compounds play a key role in various metabolic pathways. Many Molecular oxygen is a necessary compound for all of these components are essential in the organism aerobic organisms, since this element is critical for energy production; however, is a potent oxidant, defense and their byproducts are considered potent which can lead to oxidative stress (OS). The bactericides that act actively in the destruction of reactive oxygen species (ROS) produced and the invasive pathogens (Cross et al. 1987, Dong et al. resulting free radicals (FR) are results of normal cell 2017, Biller-Takahashi et al. 2015). Correspondence to: Jaqueline Dalbello Biller OS occurs when there is an imbalance E-mail: [email protected] between the production of oxidant and antioxidant An Acad Bras Cienc (2018) 90 (4) 3404 JAQUELINE D. BILLER and LEONARDO S. TAKAHASHI components. The organism during its normal OXIDATIVE STRESS metabolism produces several ROSs, however, it has Oxidative stress is a condition that refers to an antioxidant defense system that keeps the levels the imbalance between levels of ROS and their of these oxidizing compounds at an acceptable antioxidants. ROS may be increased and damage level. In some situations the oxidants production is lipids, proteins and DNA. OS has been linked to a very high and the cells can suffer serious damage wide variety of diseases; however, ROS molecules and die (Dong et al. 2017, Finkel 2011, Kiley and Storz 2004, Li et al. 2016). also act on immune defense, as well as signaling The fish immune system is composed of innate molecules and on the maintenance of physiological and acquired mechanisms of defense. Phagocytosis processes (Figure 1) (Wood et al. 2003, Schieber is an innate process, which interconnects these and Chandel 2014). two systems, since the pathogens processing by ROS are involved in energy production, professional phagocytes is a fundamental stage for phagocytosis, regulation of cell growth, intercellular the antibodies production. During phagocytosis signaling and synthesis of important biological there is the production of ROS and consequent FR, substances. They may also be classified as FR, these compounds lead to the formation of potent since chemical properties give them reactivity to bactericides compounds to combat microorganisms different biological targets, and when in excess (Biller-Takahashi et al. 2015, Biller-Takahashi and they can cause peroxidation of membrane lipids, Urbinati 2014). impairment of proteins in tissues, membranes, Currently, several studies have evaluated enzymes, carbohydrates and DNA. Even though the effects of FR on the immune system and new ROS are evolutionarily selected to modulate areas of knowledge are being explored, such as immunological and physiological processes (Cross immunosenescence, which studies the aging of et al. 1987, Dong et al. 2017, Kiley and Storz 2004, cells of the immune system caused by FR, as well as Finkel 2011). inflammasomes, which are biochemical pathways FR are highly reactive atoms or molecules initiated by the activation of receptors that provoke that have an unpaired electron in their last electron chronic inflammation (genesis of many diseases) layer, so, have an unpaired number of electrons in (Paiva-Oliveira et al. 2010, Tschopp and Schroder their atomic or molecular orbital. Instability makes 2010, Angosto and Mulero 2014). atoms or molecules very reactive and therefore Studies of the fish FR production are can non-specifically bind with other biological preliminary, but there are two factors that positively molecules. FR can be formed by absorption of influence the OS studies in this species; one of them ultraviolet radiation or visible light, by redox is that fish are considered biological indicators reactions or by enzymatic catalysis (Ferreira and of pollution, which is a factor that promotes the Matsubara 1997). generation of FR by the aquatic organism. Second ROS are produced mainly in the mitochondria, is that many fish are considered biological models peroxisomes, cytoplasm and plasma membrane. for metabolic pathways evaluation, so, due to the Oxygen is a birradical that has two radicals in the importance of the theme, other studies should be orbitals, which makes it little reactive, however, carried out to evaluate the ROS effects on fish, the electron transfer or energy absorption processes including their beneficial effect against pathogens can promote the ROS formation from molecular and deleterious impact on the oxidation of cellular oxygen. ROS include oxygen FR, such as the • •- components (Ahmad et al. 2000, Oruc et al. 2004). hydroxyl radical (HO ), superoxide anion (O2 ), An Acad Bras Cienc (2018) 90 (4) OXIDATIVE STRESS AND FISH IMMUNE SYSTEM 3405 peroxyl (ROO•) and alkoxyl (RO•), nitric oxide or repair the damage caused by it (Halliwell et al. (NO), but also non-radical compounds, such as 1992, Barreiros et al. 2006). •– oxygen, hydrogen peroxide (H2O2), hypochlorous The superoxide anion radical (O2 ) is usually acid (HClO), and transition metals (Cu and Fe) inactive, and in aqueous media produces a hydrogen (Sorg 2004, Barreiros et al. 2006). peroxide molecule and an oxygen molecule by The FR have a different degree of reactivity dismutation. This FR is part of several chemical and half-life, but most of them are very unstable reactions with important biological functions, such and can promote the non-enzymatic oxidation of as HO• radical production, by reducing Fe chelates, biomolecules (proteins, carbohydrates, lipids and as well as Fe2+ released from storage proteins nucleic acids) (Halliwell 2009, Buonocore et al. (ferritin and aconitase) and iron-sulfoproteins, in 2010, Hamanaka and Chandel 2010). Within the addition to reacting with the HO• radical producing 1 cells, there are three main sources of FR formation: singlet oxygen ( O2) and reacting with nitric oxide I. Oxidative metabolism in the mitochondria: (NO•) producing peroxynitrite (ONOO−) (Babior In the mitochondrial respiratory chain, electron 1997, Halliwell 2000, Barreiros et al. 2006). transport is responsible for the ROS formation The superoxide radical, in spite of its (Barreiros et al. 2006). deleterious effects, has important function for II. Leukocyte respiratory burst activity: immune defense, because in phagocytic cells, •– neutrophils, monocytes, macrophages, dendritic lymphocytes and fibroblasts, the O2 has the •– cells and B-lymphocyte produce ROS, being capacity to destroy pathogens. The O2 produced a strategy of the immune system for several in the cells can be eliminated by the superoxide pathogens destruction. The “oxidative burst” is a dismutase enzyme, which catalyzes the dismutation •– resting metabolic pathway in the cells, however, it is of two molecules of O2 in oxygen and hydrogen activated after microbial agent detection. It has the peroxide, however, when there is no enzymatic function of producing strong oxidizing compounds elimination (peroxidases and catalase), this FR (burst activity) that act for microorganisms can lead to formation of hydroxyl radicals (Babior destruction (Park 2003, Cathcart 2004, Klebanoff 1997, Halliwell 2000,
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