β-Naphthoflavone and benzo(a)pyrene treatment affect liver intermediary metabolism and plasma cortisol levels in rainbow trout Oncorhynchus mykiss
Introduction
Polycyclic aromatic hydrocarbons (PAHs) have been demonstrated to be mutagenic and carcinogenic precursors as well as to impair growth, reproduction, and osmoregulation in fish (Nicolas, 1999). PAHs interfere with endocrine function by mimicking or blocking the effects of naturally occurring hormones (Johnson et al., 1998). At least some of those alterations appear to occur through changes in the hypothalamus–pituitary–interrenal (HPI) and hypothalamus–pituitary–gonad (HPG) axis (Zhou et al., 2000; Monteiro et al., 2000b; Gesto et al., 2006). Those interactions can lead to a disturbance of hormone metabolism or hormone-regulated cellular and physiological processes (Navas et al., 2004). One of those physiological processes is energy metabolism since hormones that can be affected by PAHs exposure like 17β-estradiol and cortisol are also known to regulate energy metabolism in fish (Mommsen et al., 1999; Laiz-Carrión et al., 2003; Sangiao-Alvarellos et al., 2005b). Moreover, several studies have shown that changes in fish energy metabolism may occur to overcome toxic stress (Frasco and Guilhermino, 2002). Thus, changes in plasma metabolites after PAHs exposure have been described in several studies such as for glucose and lactate (Teles et al., 2004, Teles et al., 2005), and lipids (Monteiro et al., 2000a).
The liver is the primary organ receiving PAHs (Deb et al., 2000). However, the studies carried out to assess the impact of PAHs exposure on liver energy metabolism are scarce (Vijayan et al., 1997; Roche et al., 2002; Stephensen et al., 2003). In a previous study, we have assessed the impact of naphthalene, the simplest PAHs, on intermediary metabolism in liver of rainbow trout (Tintos et al., 2006b, Tintos et al., 2007). Since naphthalene is probably one of the less powerful inducers of detoxification processes, we aimed to assess the effects of more powerful PAHs in energy metabolism of liver in rainbow trout. Accordingly we have assessed in the present study the effects of β-naphthoflavone (β-NF) and benzo(a)pyrene (BaP). β-NF, a synthetic analog of a large series of naturally occurring flavoned compounds, is an aromatic hydrocarbon (Ah) receptor agonist (Pacheco and Santos, 2002) that has been considered the most potent P450 mixed-function oxidase (MFO) inducer among a number of synthetic flavonoid compounds. BaP is a ubiquitous PAH, and has been also shown to be carcinogenic and MFO inducer in fish (Lemaire-Gony and Lemaire, 1992). The information regarding effects of both PAHs in liver energy metabolism is limited to several studies with β-NF (Vijayan et al., 1997; Morrow et al., 2004; Teles et al., 2005) and very few with BaP (Lemaire-Gony and Lemaire, 1992). Therefore, the specific objectives of the present study were to examine whether or not β-NF or BaP treatment induced in fish hepatic intermediary metabolism as well as levels of plasma steroid hormones more important changes than those observed after treatment with other PAHs like naphthalene.
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Fish
Sexually immature female rainbow trout (Oncorhynchus mykiss, 50±6 g body weight) were provided by a hatchery in Soutorredondo (Noia, Spain) and transferred to the laboratory in the Faculty of Biology (Vigo, Spain). Fish were acclimated for 4 weeks in flow-through tanks providing a constant supply of freshwater before the experiments. Fish were kept under natural photoperiod (December 2005) and constant temperature (15 °C). Fish were fed once daily to satiation with commercial dry pellets
Results
No mortality, health disturbances or any alterations in behavior were observed in any group of fish throughout the experiments. No differences were observed between uninjected fish (data not shown) and those fish implanted with vehicle alone (control) for any parameter assessed.
Plasma cortisol levels increased after 24 or 72 h in fish treated with β-NF or BaP with the increase being higher in fish treated with β-NF (Fig. 1A) while no changes were noticed in plasma 17β-estradiol levels (Fig. 1B).
Discussion
Since PAHs were administered intraperitoneally at a single dose instead of dietary or water exposure routes, the present study is limited relative to environmental extrapolations. To better understand the effects of the PAHs assessed, more studies are needed including dietary or water exposure, dose–responses, sampling additional time points, and assessing different life stages or body sizes.
The administration procedure used in the present study was similar to others described in literature for
Conclusions
In summary, the results obtained in the present study support an increase in plasma levels of cortisol after β-NF or BaP exposure. Moreover, several changes were observed in several pathways of liver energy metabolism including increased mobilization of glycogen stores as well as in increased glucose production through gluconeogenesis whereas β-NF also stimulated amino acid catabolism. The activation of those pathways can be attributed to cortisol action and result in increased glucose export
Acknowledgments
This study was supported by Grants VEM2003-20062 (Ministerio de Ciencia y Tecnología and FEDER, Spain) and PGIDT04PXIC31208PN (Xunta de Galicia, Spain). M.G. was recipient of a predoctoral fellowship from the Xunta de Galicia.
The experiments described comply with the guidelines of the European Union Council (86/609/EU) and the Spanish Government (RD 1201/2005) for the use of animals in research.
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