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Transcripts Encoding Two Melatonin Synthesis Enzymes in the Teleost Pineal Organ: Circadian Regulation in Pike and Zebrafish, But Not in Trout¹

Laboratoire de Neurobiologie Cellulaire, Département des Neurosciences, CNRS-UMR 6558, Faculté des Sciences (V.B., J.F.), F-86022 Poitiers, France; the Department of Biology, University of Houston (G.M.C.), Houston, Texas 77204-5513; and the Section on Neuroendocrinology, Laboratory of Developmental Neurobiology, National Institute of Child Health and Human Development, National Institutes of Health (D.C.K., S.L.C.), Bethesda, Maryland 20892

Address all correspondence and requests for reprints to: Dr. Steven L. Coon, National Institutes of Health, Building 49, Room 5A38, Bethesda, Maryland 20892-4480. E-mail: coon{at}codon.nih.gov

In this report the photosensitive teleost pineal organ was studied in three teleosts, in which melatonin production is known to exhibit a daily rhythm with higher levels at night; in pike and zebrafish this increase is driven by a pineal clock, whereas in trout it occurs exclusively in response to darkness. Here we investigated the regulation of messenger RNA (mRNA) encoding serotonin N-acetyltransferase (AA-NAT), the penultimate enzyme in melatonin synthesis, which is thought to be primarily responsible for changes in melatonin production. AA-NAT mRNA was found in the pineal organ of all three species and in the zebrafish retina. A rhythm in AA-NAT mRNA occurs in vivo in the pike pineal organ in a light/dark (L/D) lighting environment, in constant lighting (L/L), or in constant darkness (D/D) and in vitro in the zebrafish pineal organ in L/D and L/L, indicating that these transcripts are regulated by a circadian clock. In contrast, trout pineal AA-NAT mRNA levels are stable in vivo and in vitro in L/D, L/L, and D/D. Analysis of mRNA encoding the first enzyme in melatonin synthesis, tryptophan hydroxylase, reveals that the in vivo abundance of this transcript changes on a circadian basis in pike, but not in trout. A parsimonious hypothesis to explain the absence of circadian rhythms in both AA-NAT and tryptophan hydroxylase mRNAs in the trout pineal is that one circadian system regulates the expression of both genes and that this system has been disrupted by a single mutation in this species.

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