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Gene Structure of the Goldfish Agouti-Signaling Protein: A Putative Role in the Dorsal-Ventral Pigment Pattern of Fish

Department of Fish Reproductive Physiology (J.M.C.-R.), Instituto de Acuicultura de Torre de la Sal, Consejo Superior de Investigaciones Cientificas, Castellón 12595, Spain; Department of Neuroscience (T.H., H.B.S.), Unit of Pharmacology, Uppsala University, SE 751 24 Uppsala, Sweden; and Department of Biological Sciences (J.M.C.-R., R.E.P.), University of Alberta, Edmonton, Alberta, Canada T6G 2E9

Address all correspondence and requests for reprints to: Dr. J. M. Cerdá-Reverter, Department of Fish Reproductive Physiology, Instituto de Acuicultura de Torre de la Sal, 12595 Torre de la Sal, Ribera de Cabanes, Castellón, Spain. E-mail cerdarev{at}iats.csic.es.

One of the most successful chromatic adaptations in vertebrates is the dorsal-ventral pigment pattern in which the dorsal skin is darkly colored, whereas the ventrum is light. In fish, the latter pattern is achieved because a melanization inhibition factor inhibits melanoblast differentiation and supports iridophore proliferation in the ventrum. In rodents, the patterned pigmentation results from regional production of the agouti-signaling protein (ASP). This peptide controls the switch between production of eumelanin and pheomelanin by antagonizing MSH effects on melanocortin receptor (MCR) 1 in the melanocytes. In addition, ASP inhibits the differentiation and proliferation of melanoblast. Thus, the mammalian ASP may be homologous to the poikilotherm melanization inhibition factor. By screening of a genomic library, we deduced the amino acid sequence of goldfish ASP. The ASP gene is a four-exon gene spanning 3097 bp that encodes a 125-amino acid precursor. Northern blot analysis identified two different ASP mRNAs in ventral skin of red- and black-pigmented and albino fish, but no expression levels were observed in the dorsal skin of the same fish. The dorsal-ventral expression polarity was also detected in both black dorsally pigmented fish and albino fish. Pharmacological studies demonstrate that goldfish ASP acts as a melanocortin antagonist at Fugu MC1R and goldfish MC4R. In addition, goldfish ASP inhibited Nle4, D-Phe7-MSH-stimulated pigment dispersion in medaka melanophores. Our studies support agouti signaling protein as the melanization inhibition factor, a key factor in the development of the dorsal-ventral pigment pattern in fish.

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