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Regulation of Arylalkylamine N-Acetyltransferase-2 (AANAT2, EC 2.3.1.87) in the Fish Pineal Organ: Evidence for a Role of Proteasomal Proteolysis

Section on Neuroendocrinology (J.F., K.M.G., J.L.W., S.L.C., D.C.K.), Laboratory of Developmental Neurobiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892-4480; Laboratoire de Neurobiologie Cellulaire (J.F.), Département des Neurosciences, CNRS-UMR 6558, F-86022 Poitiers Cédex, France; and Fish Physiology Department (B.R., G.C.), National Center for Mariculture, Oceanographic & Limnological Research Institute, Eilat 88112, Israel

Address all correspondence and requests for reprints to: David C. Klein, NIH 49–6A82, Bethesda, Maryland 20892-4480. E-mail: klein{at}helix.nih.gov

In fish, individual photoreceptor cells in the pineal organ and retina contain complete melatonin rhythm generating systems. In the pike and seabream, this includes a photodetector, circadian clock, and melatonin synthesis machinery; the trout lacks a functional clock. The melatonin rhythm is due in part to a nocturnal increase in the activity of the arylalkylamine N-acetyltransferase (AANAT) which is inhibited by light. Two AANATs have been identified in fish: AANAT1, more closely related to AANATs found in higher vertebrates, is specifically expressed in the retina; AANAT2 is specifically expressed in the pineal organ. We show that there is a physiological day/night rhythm in pineal AANAT2 protein in the pike, and that light exposure at midnight decreases the abundance of AANAT2 protein and activity. In culture, this decrease is blocked by inhibitors of the proteasomal degradation pathway. If glands are maintained under light at night, treatment with these inhibitors increases AANAT2 activity and protein. Organ culture studies with the trout and seabream also indicate that the light-induced decrease of AANAT2 activity is prevented when proteasomal proteolysis is blocked. A cAMP-dependent pathway protects AANAT2 protein from degradation. These results provide a clue to understanding how light regulates the daily rhythm in melatonin secretion in fish photoreceptor cells and provides evidence that proteasomal proteolysis is a conserved element in the regulation of AANAT in vertebrates.

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