Stress inhibition of melatonin synthesis in the pineal organ of rainbow trout (Oncorhynchus mykiss) is mediated by cortisol

Marcos A. López-Patiño, Manuel Gesto, Marta Conde-Sieira, José L. Soengas, Jesús M. Míguez

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Cortisol has been suggested to mediate the effect of stress on pineal melatonin synthesis in fish. Therefore, we aimed to determine how pineal melatonin synthesis is affected by exposing rainbow trout to different stressors, such as hypoxia, chasing and high stocking density. In addition, to test the hypothesis that cortisol is a mediator of such stress-induced effects, a set of animals were intraperitoneally implanted with coconut oil alone or containing cortisol (50 mg kg-1 body mass) and sampled 5 or 48 h post-injection at midday and midnight. The specificity of such effect was also assessed in cultured pineal organs exposed to cortisol alone or with the general glucocorticoid receptor antagonist, mifepristone (RU486). Stress (in particular chasing and high stocking density) affected the patterns of plasma and pineal organ melatonin content during both day and night, with the greatest reduction occurring at night. The decrease in nocturnal melatonin levels in the pineal organ of stressed fish was accompanied by increased serotonin content and decreased AANAT2 enzymatic activity and mRNA abundance. Similar effects on pineal melatonin synthesis to those elicited by stress were observed in trout implanted with cortisol for either 5 or 48 h. These data indicate that stress negatively influences the synthesis of melatonin in the pineal organ, thus attenuating the day-night variations of circulating melatonin. The effect might be mediated by increased cortisol, which binds to trout pineal organ-specific glucocorticoid receptors to modulate melatonin rhythms. Our results in cultured pineal organs support this. Considering the role of melatonin in the synchronization of daily and annual rhythms, the results suggest that stress-induced alterations in melatonin synthesis could affect the availability of fish to integrate rhythmic environmental information.
Original languageEnglish
JournalJournal of Experimental Biology
Volume217
Issue number8
Pages (from-to)1407-1416
ISSN0022-0949
DOIs
Publication statusPublished - 2014
Externally publishedYes

Keywords

  • Animal Science and Zoology
  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Physiology
  • Insect Science
  • Aquatic Science
  • Medicine (all)
  • AANAT2
  • Cortisol
  • Melatonin
  • Pineal organ
  • Rainbow trout
  • Stress
  • 5 hydroxyindoleacetic acid
  • aralkylamine acetyltransferase
  • fish protein
  • hydrocortisone
  • melatonin
  • messenger RNA
  • serotonin
  • animal
  • blood
  • genetics
  • metabolism
  • physiological stress
  • physiology
  • pineal body
  • rainbow trout
  • real time polymerase chain reaction
  • reverse transcription polymerase chain reaction
  • Animals
  • Arylalkylamine N-Acetyltransferase
  • Fish Proteins
  • Hydrocortisone
  • Hydroxyindoleacetic Acid
  • Oncorhynchus mykiss
  • Pineal Gland
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • RNA, Messenger
  • Serotonin
  • Stress, Physiological
  • HYDROCORTISONE
  • annual rhythm
  • body mass
  • chasing
  • enzymatic activity
  • hypoxia
  • rhythmic environmental information
  • stocking density
  • stress inhibition
  • Pisces Vertebrata Chordata Animalia (Animals, Chordates, Fish, Nonhuman Vertebrates, Vertebrates) - Osteichthyes [85206] Oncorhynchus mykiss species rainbow trout common
  • 5-hydroxyindoleacetic acid 5-HIAA 54-16-0
  • coconut oil
  • cortisol 50-23-7
  • melatonin 73-31-4
  • mifepristone RU486 84371-65-3 glucocorticoid receptor antagonist
  • mRNA
  • serotonin 5-HT 50-67-9
  • 10060, Biochemistry studies - General
  • 10062, Biochemistry studies - Nucleic acids, purines and pyrimidines
  • 10064, Biochemistry studies - Proteins, peptides and amino acids
  • 10067, Biochemistry studies - Sterols and steroids
  • 15002, Blood - Blood and lymph studies
  • 15004, Blood - Blood cell studies
  • 17002, Endocrine - General
  • 17012, Endocrine - Pineal
  • 17020, Endocrine - Neuroendocrinology
  • 20504, Nervous system - Physiology and biochemistry
  • Chemical Coordination and Homeostasis
  • Neural Coordination
  • pineal organ endocrine system, nervous system
  • plasma blood and lymphatics
  • Biochemistry and Molecular Biophysics
  • Endocrine System
  • Nervous System

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