Effects of naphthalene, beta-naphthoflavone and benzo(a)pyrene on the diurnal and nocturnal indoleamine metabolism and melatonin content in the pineal organ of rainbow trout, Oncorhynchus mykiss

Manuel Gesto, Adrian Tintos, Arnau Rodriguez-Illamola, Jose L. Soengas, Jesus M. Miguez

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Polycyclic aromatic hydrocarbons (PAHs) have deleterious effects on neuroendocrine systems in teleost fish affecting, among other processes, reproductive function or stress responses. The hormone melatonin, mainly produced in the pineal organ of vertebrates, is involved in the regulation of biological rhythms as well as other important functions, and may also act as an antioxidant molecule. The effects of environmental pollutants on the endocrine and metabolic activity of the pineal organ have been studied only in mammals. We here evaluate the effects of the PAHs naphthalene (NAP) and benzo(a)pyrene (BaP) and the flavonoid beta-naphthoflavone (BNF) on the pineal organ of rainbow trout by quantifying the diurnal and nocturnal pineal content of some indoles and methoxyindoles, including melatonin. NAP mainly induced diurnal increases in the pineal content of melatonin and other methoxyindoles like 5-methoxytryptamine (5-MT), 5-methoxyi ndole-3-acetic acid (5-MIAA) or 5-methoxytryptophol (5-MTOL). Those increases did not occur at night, when even occasional decreases were observed compared with controls. NAP also induced some diurnal and nocturnal decreases in the levels of indolic compounds like serotonin (5-HT) and 5-hydroxyindole-3-acetic acid (5-HIAA), while pineal content of 5-hydroxytryptophan (5-HTP) was first decreased (few hours after injection) and then increased (few days after injection) during the day. BaP and BNF induced strong increases in diurnal levels of melatonin, whereas other pineal compounds were unaffected. it seems that an increase of the methylation capacity of the pineal organ takes place during the day, and a decrease occurs at night. Those effects could be mediated by changes in the activity of key enzymes involved in pineal melatonin biosynthesis, maybe as a result of the alteration of the cellular phototransduction mechanisms involved in the light-induced inhibition of melatonin synthesis in the pineal photoreceptor cells. These results demonstrate for the first time that environmental pollutants can disrupt the activity of the pineal organ of teleost fish. This disruption could be a threat for the survival of the animals in their natural environment, although the increases observed in melatonin levels could play a relevant role as a toxicity-protection factor. (c) 2008 Elsevier B.V. All rights reserved.
Original languageEnglish
JournalAquatic Toxicology
Volume92
Issue number1
Pages (from-to)1-8
ISSN0166-445X
DOIs
Publication statusPublished - 2009
Externally publishedYes

Keywords

  • Animals
  • Benzo(a)pyrene
  • Circadian Rhythm
  • Indoles
  • Melatonin
  • Naphthalenes
  • Oncorhynchus mykiss
  • Pineal Gland
  • Time Factors
  • Water Pollutants, Chemical
  • beta-Naphthoflavone
  • naphthalene
  • Polycyclic aromatic hydrocarbons
  • Naphthalene
  • Pineal organ
  • Daily rhythms
  • Trout
  • Aquatic Science
  • Health, Toxicology and Mutagenesis
  • 5 hydroxyindoleacetic acid
  • 5 hydroxytryptophan
  • 5 methoxyindoleacetic acid
  • 5 methoxytryptamine
  • 5 methoxytryptophol
  • benzo[a]pyrene
  • beta naphthoflavone
  • indole derivative
  • indoleamine
  • melatonin
  • serotonin
  • benzene
  • diurnal activity
  • endocrine disruptor
  • hormone
  • metabolism
  • nocturnal activity
  • pollution effect
  • pyrene
  • salmonid
  • animal experiment
  • animal tissue
  • article
  • circadian rhythm
  • controlled study
  • enzyme activity
  • hormone synthesis
  • nonhuman
  • photoreceptor cell
  • pineal body
  • pollutant
  • priority journal
  • rainbow trout
  • survival
  • teleost
  • Animalia
  • Mammalia
  • Salmonidae
  • Teleostei
  • Vertebrata
  • MARINE
  • TOXICOLOGY
  • POLYCYCLIC AROMATIC-HYDROCARBONS
  • LIVER INTERMEDIARY METABOLISM
  • OXIDATIVE STRESS
  • AQUATIC ORGANISMS
  • DIETARY EXPOSURE
  • IN-VIVO
  • RECEPTOR
  • BRAIN
  • TOXICITY
  • FISH
  • daily rhythm
  • Pisces Vertebrata Chordata Animalia (Animals, Chordates, Fish, Nonhuman Vertebrates, Vertebrates) - Osteichthyes [85206] Oncorhynchus mykiss species rainbow trout common
  • 5-hydroxyindole-3-acetic acid 54-16-0
  • 5-methoxyindole-3-acetic acid 3471-31-6
  • 5-methoxytryptamine 608-07-1
  • 5-methoxytryptophol 712-09-4
  • benzo(a)pyrene 50-32-8 toxin
  • beta-naphthoflavone 6051-87-2 toxin
  • melatonin 73-31-4
  • naphthalene 91-20-3 toxin
  • nocturnal indoleamine metabolism
  • polycyclic aromatic hydrocarbons toxin
  • 10060, Biochemistry studies - General
  • 10064, Biochemistry studies - Proteins, peptides and amino acids
  • 13002, Metabolism - General metabolism and metabolic pathways
  • 17002, Endocrine - General
  • 17012, Endocrine - Pineal
  • 17020, Endocrine - Neuroendocrinology
  • 20504, Nervous system - Physiology and biochemistry
  • 22501, Toxicology - General and methods
  • Chemical Coordination and Homeostasis
  • Neural Coordination
  • pineal gland endocrine system, nervous system
  • Endocrine System
  • Metabolism
  • Nervous System
  • Toxicology

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