GABA inhibition of luminescence from lantern shark (Etmopterus spinax) photophores Julien M. Claes a, ⁎, Jenny Krönström b , Susanne Holmgren b , Jérôme Mallefet a a Laboratoire de Biologie Marine, Earth and Life Institute, Université catholique de Louvain, 3 Place Croix du Sud, B-1348 Louvain-la-Neuve, Belgium b Department of Zoophysiology, University of Gothenburg, Box 463, SE 405 30 Göteborg, Sweden abstract article info Article history: Received 15 September 2010 Received in revised form 1 November 2010 Accepted 1 November 2010 Available online 8 November 2010 Keywords: Bioluminescence Chondrichthyes GABA A receptor Melatonin Neurotransmitter Prolactin Photogenic organs (photophores) of the velvet belly lantern shark (Etmopterus spinax) are under hormonal control, since melatonin (MT) and prolactin (PRL) trigger luminescence while α-melanocyte-stimulating hormone (α-MSH) prevents this light to be emitted. A recent study supported, however, the presence of numerous nerve fibres in the photogenic tissue of this shark. Immunohistochemical and pharmacological results collected in this work support these nerve fibres to be inhibitory GABAergic nerves since (i) GABA immunoreactivity was detected inside the photogenic tissue, where previous labelling detected the nerve fibre structures and (ii) GABA was able to inhibit MT and PRL-induced luminescence, which was on the other hand increased by the GABA A antagonist bicuculline (BICU). In addition, we also demonstrated that BICU can induce light per se by provoking pigment retraction in the pigmented cells composing the iris-like structure of the photophore, attaining, however, only about 10% of hormonally induced luminescence intensity at 10 -3 mol L -1 . This strongly supports that a GABA inhibitory tonus controls photophore “aperture” in the photogenic tissue of E. spinax but also that MT and PRL have more than one target cell type in the photophores. © 2010 Elsevier Inc. All rights reserved. 1. Introduction A common feature in deep-sea multicellular organisms are photogenic organs i.e. photophores, which contain either symbiotic luminous bacteria (=extrinsic photophores) or intrinsic photogenic cells i. e. photocytes (= intrinsic photophores) (Herring, 1985). These organs demonstrate an important structural diversity, which not only reflects the numerous independent apparearances of the lumines- cence competence (i.e. the capability to emit a visible light) in this environment but also its important ecological role (Haddock et al., 2010; Widder, 2010). Indeed, luminescence is thought to facilitate or discourage predation (for a predator or a prey, respectively) but also to allow intraspecific visual communication in the darkness of the deep-sea (Buck, 1978; Haddock et al., 2010; Widder, 2010). The functional efficiency of the photophores directly depends on a precise control of their light emission characteristics (wavelength, intensity and angular distribution). Although photophore-associated optical structures (lenses, filters and reflectors) can assume an important part of the control (Denton et al., 1972; 1985), they cannot induce the start of the photogenesis in intrinsic photophores. This light switch was long believed to be exclusively under nervous control since classical neurotransmitters triggered the light in marine organisms endowed with these complex photogenic organs such as the only investigated crustacean, the northern krill Meganyctiphanes norvegica (Kay, 1965; Fregin and Wiese, 2002), and the several investigated teleost fishes (for a review see Claes and Mallefet, 2009). However, a study developed in our laboratory recently demon- strated that photophores of the velvet belly lantern shark, Etmopterus spinax (Linnaeus, 1758) were controlled by hormones rather than by nerves (Claes and Mallefet, 2009): melatonin (MT) and prolactin (PRL) trigger light emission and α-melanocyte-stimulating hormone (α-MSH) whose application prevents the shark's photogenic tissue from glowing, which indicates a putative inhibitory effect of this hormone on the light emission/production. These hormones are also those controlling the skin pigmentation of Elasmobranches (sharks and rays) via movements of chromatophores (Visconti et al., 1999; Gelsleichter, 2004), and two of them (MT and PRL) were recently shown to target chromatophores situated between the photocytes and the photophore's lens, suggesting a common origin of the two phenomena (Claes and Mallefet, 2010a). It was then shown that the actions of these hormones could not explain the important variation in the luminous response to hormones that were found in adult E. spinax specimens, according to the sex and/or to the investigated region of the luminous pattern (=photophore coverage), suggesting the presence of an additional control mechanism (Claes and Mallefet, 2010b). Since nitric oxide (NO) was known to modulate neurally induced luminescence of several marine organisms and especially fishes (Krönström et al., 2005, 2007, Krönström, 2009; Krönström and Mallefet, 2010), the hypothesis of a NO action on the hormonally induced luminescence Comparative Biochemistry and Physiology, Part C 153 (2011) 231–236 ⁎ Corresponding author. Tel.: + 32 10473475; fax: + 32 10473476. E-mail address: julien.m.claes@uclouvain.be (J.M. Claes). 1532-0456/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpc.2010.11.002 Contents lists available at ScienceDirect Comparative Biochemistry and Physiology, Part C journal homepage: www.elsevier.com/locate/cbpc