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J. Biol. Chem., Vol. 275, Issue 22, 16885-16890, June 2, 2000

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N-Methyl-D-aspartate Receptor Stimulation Activates Tyrosinase and Promotes Melanin Synthesis in the Ink Gland of the Cuttlefish Sepia officinalis through the Nitric Oxide/cGMP Signal Transduction Pathway
A NOVEL POSSIBLE ROLE FOR GLUTAMATE AS PHYSIOLOGIC ACTIVATOR OF MELANOGENESIS^*

Anna Palumbo^§, Annarita Poli, Anna Di Cosmo^¶, and Marco d'Ischia^**

From the  Zoological Station "Anton Dohrn," Villa Communale, 80121 Naples and the Departments of ^¶ Zoology and  Organic and Biological Chemistry, University of Naples Federico II, 80134 Naples, Italy

The tyrosinase-catalyzed conversion of L-tyrosine to melanin represents the most distinctive biochemical pathway in the ink gland of the cuttlefish Sepia officinalis; however, the molecular mechanisms underlying its activation have remained so far largely uncharted. In this paper we demonstrate for the first time that L-glutamate can stimulate tyrosinase activity and promote melanin synthesis in Sepia ink gland via the N-methyl-D-aspartate (NMDA) receptor/NO/cGMP signal transduction pathway. Incubation of intact ink glands with either L-glutamate or NMDA resulted in an up to 18-fold increase of tyrosinase activity and a more than 6-fold elevation of cGMP levels. Comparable stimulation of tyrosinase was induced by an NO donor and by 8-bromo-cGMP. An NMDA receptor antagonist, NO synthase (NOS) inhibitors, and a guanylate cyclase blocker suppressed NMDA-induced effects. Immunohistochemical evidence indicated that enhanced cGMP production was localized largely in the mature part of the ink gland. Increased de novo synthesis of melanin was demonstrated in NMDA- and NO-stimulated ink glands by a combined microanalytical approach based on spectrophotometric determination of pigment levels and high performance liquid chromatography quantitation of pyrrole-2,3,5-tricarboxylic acid, a specific melanin marker, in melanosome-containing fractions. These results fill a longstanding gap in the understanding of the complex biochemical mechanisms underlying activation of melanogenesis in the mature ink gland cells of S. officinalis and disclose a novel physiologic role of the excitatory neurotransmitter glutamate mediated by the NMDA receptor/NO/cGMP signaling pathway.

This paper is dedicated to the memory of Prof. Giovanna Misuraca, an esteemed colleague and friend who is dearly missed by all those who had the fortune to share her interest in the field of melanogenesis.

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