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Firefly Squid,'' Watasenia Scintillans View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Biochimica et Biophysica Acta 1564 (2002) 189–197 www.bba-direct.com Bioluminescence reaction catalyzed by membrane-bound luciferase in the ‘‘firefly squid,’’ Watasenia scintillans Frederick I. Tsuji* Marine Biology Research Division 0202, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, CA 92093, USA Received 13 December 2001; received in revised form 11 March 2002; accepted 11 April 2002 Abstract The small Japanese ‘‘firefly squid,’’ Watasenia scintillans, emits a bluish luminescence from dermal photogenic organs distributed along the ventral aspects of the head, mantle, funnel, arms and eyes. The brightest light is emitted by a cluster of three tiny organs located at the tip of each of the fourth pair of arms. Studies of extracts of the arm organs show that the light is due to a luciferin–luciferase reaction in which the luciferase is membrane-bound. The other components of the reaction are coelenterazine disulfate (luciferin), ATP, Mg2+, and molecular oxygen. Based on the results, a reaction scheme is proposed which involves a rapid base/luciferase-catalyzed enolization of the keto group of the C-3 carbon of luciferin, followed by an adenylation of the enol group by ATP. The AMP serves as a recognition moiety for docking the substrate molecule to a luciferase bound to membrane, after which AMP is cleaved and a four-membered dioxetanone intermediate is formed by the addition of molecular oxygen. The intermediate then spontaneously decomposes to yield CO2 and coelenteramide disulfate (oxyluciferin) in the excited state, which serves as the light emitter in the reaction. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Luciferin–luciferase; Coelenterazine disulfate; Base/enzyme-catalyzed enolization; ATP activation 1. Introduction ine’’ and ‘‘luciferase’’ have their origin [2,3]. The migration takes place from the middle of March until the end of May. Each spring, in an out-of-the-way region of northern Virtually all (99.9%) of the squids caught by net during this Japan, where the Japanese Alps run close along the coast of period are females bearing fertilized eggs. The phenomenon the Sea of Japan, females of the small, indigenous, deep-sea of mass migration is most notable near the small maritime squid, Watasenia scintillans (mantle length f 5.7 cm; wet city of Namerikawa situated at the southern end of Toyama weight f 8.9 gm), come inshore to spawn [1,2]. They Bay (deepest depth f 1200 m) where the squids swim into number in the hundreds of millions and even a billion when shallow water, lay their eggs and die, thereupon completing calculated on the basis of the number of tons caught a 1-year life cycle. The life cycle of the male is not known. annually by the local fishery. The squid has served as food Watasenia is famous in Japan from years past, but it is not from early times, as has, in Europe, the luminescent boring known outside the country. The squid has some 800 minute mollusc, Pholas dactylus, from which the terms ‘‘lucifer- dermal light organs scattered over its ventral side, five prominent organs distributed along the lower margin of each eye and a cluster of three tiny ( < 1 mm diameter) Abbreviations: Coelenteramide, 2-( p-hydroxyphenylacetyl)-amino- black pigmented organs located at the tip of each of the 3-benzyl-5-( p-hydroxyphenyl)pyrazin; Coelenterazine, 2-( p-hydroxy- fourth pair of ventral arms. The arm organs, which discharge benzyl)-6-( p-hydroxyphenyl)-3,7-dihydroimidazo-[1,2-a]pyrazin-one; Coelenterazine disulfate, 8-benzyl-3,7-dihydro-2-(4-hydroxysulfonyloxy- brilliant flashes of bluish light when the animal is mechan- benzyl)-6-(4-hydroxysulfonyloxyphenyl)-imidazo [1,2-a]pyrazin-3-one; ically or electrically stimulated, produce the brightest light. ATP, adenosine 5V-triphosphate; AMP, adenosine 5V-monophosphate; Except for a difference in color, the flashing of the arm Na4P2O7, tetrasodium pyrophosphate; PAPS, adenosine 3V-phosphate 5V- organs resembles the flashing of a firefly, and thus the squid phosphosulfate; APS, adenosine 5V-phosphosulfate; DTT, dithiothreitol; is commonly called ‘‘hotaru-ika’’ or the ‘‘firefly squid.’’ TTP, thymidine 5V-triphosphate; GTP, guanosine 5V-triphosphate; CTP, cytidine 5V-triphosphate; UTP, uridine 5V-triphosphate Watasenia luminescence has been studied for nearly 100 * Tel.: +1-858-534-3197; fax: +1-858-534-7313. years by various workers [2,3], including Watase´ [4], after E-mail address: [email protected] (F.I. Tsuji). whom the squid is named, and Harvey [3], but the mechanism 0005-2736/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. PII: S0005-2736(02)00447-9 190 F.I. Tsuji / Biochimica et Biophysica Acta 1564 (2002) 189–197 of the luminescence reaction has remained unresolved. Some jC. About 30–40 specimens were kept in the tank at any of the early workers believed that the light was due to given time in order to keep the mortality rate low and the symbiotic luminous bacteria inhabiting the light organs, but animals were not fed. The squids remained quiescent at the later electron microscopic studies demonstrated that the rod- bottom of the tank without luminescing. When netted, they like bodies in the light organs were proteinaceous crystals and flailed their arms and tentacles in the air and their arm organs not bacteria [5]. Chemical studies conducted by Goto et al. emitted brilliant flashes of light that trailed off into long [6–9] have provided evidence that the light may be due to a glows. luciferin–luciferase reaction, with the luciferin having an imidazopyrazine ring structure. The workers isolated from 2.2. Chemicals the arm organs of 10,000 Watasenia specimens a compound which they showed to be a sulfated form of coelenteramide ATP (sodium salt), Na4P2O7, a,h-methyleneadenosine and assumed it to be the oxidation product of the biolumi- 5V-triphosphate (lithium salt), h,g-methyleneadenosine 5V- nescence reaction. They then isolated a second compound triphosphate (sodium salt), PAPS (lithium salt) and APS and determined its structure to be coelenterazine disulfate, (sodium salt) were obtained from Sigma Chemical Co. The which they called Watasenia luciferin. They synthesized the other chemicals were of analytical grade and were pur- compound but it was not tested for activity because an active chased from Wako Pure Chemicals, Osaka, Japan. Synthetic luciferase extract could not be prepared from the arm organs. coelenterazine disulfate was a gift of Dr. Shoji Inoue; Tsuji [10] subsequently showed that Watasenia luminescence coelenterazine was chemically synthesized [7]. is due to an ATP-dependent reaction whose essential compo- nents are luciferin, a membrane-bound luciferase, ATP and 2.3. Measurement of light intensity Mg2+, and whose optimum pH is 8.80. More recently, improved methods for the syntheses of coelenterazine disul- A Mitchell–Hastings photomultiplier photometer [12], fate and monosulfates of coelenterazine have been reported calibrated with a carbon-14 light standard [13], was used to [11]. measure light intensity. The detector was a Hamamatsu Biochemical study of the mechanism of the Watasenia 1P21 photomultiplier, selected for low noise, with an S-4 luminescence reaction has proved difficult because: (a) the spectral response. The output from the amplifier was fed squid is available only for a short time during spring, (b) the into a Panasonic VP-6712A chart recorder. Because Japa- animal cannot be kept alive for more than 3–5 days in nese law stipulates that all radioisotopes must be kept and captivity, (c) the squid dies in about 10–20 min when taken used in a government approved radiological facility, the out of the water with the photophores becoming irreversibly photometer was calibrated at the Osaka Bioscience Institute dark, (d) the physical vitality of the squid, including its in Osaka and transported by rail to the Toyama Prefectural ability to produce light, wanes as the temperature of the Fisheries Research Institute as required. When measurement seawater rises with the oncoming summer, and (e) the of light intensity in absolute light units was not deemed luminescence system is highly unstable even when the light essential, the photometer was used without calibration and organ and extracts of the organ are kept in an ice-bath or the light intensity was recorded in relative light units (RLU). frozen in dry-ice. The present paper reports the results of work carried out 3–4 weeks each spring over a period of 20 2.4. Standard reaction mixture years. Fifteen live specimens were used to prepare a homoge- nate. The cluster of three small black organs at the tip of each 2. Materials and methods of the fourth pair of ventral arms was snipped off with a pair of ophthalmic scissors and homogenized in 5.0 ml of 0.001 All of the experiments were carried out in Namerikawa at M MgCl2 in an all-glass homogenizer immersed in an ice- the Toyama Prefectural Fisheries Research Institute, which bath [10]. The homogenate was kept in the ice-bath through- is largely concerned with the management of fishery stock out the experiment, which usually lasted for about 3.5 h, and the monitoring of the marine environment in the region. during which time the homogenate slowly lost luminescence activity. The standard reaction mixture consisted of 400 Alof 2.1. Materials homogenate + 44 Al of 1.0 M Tris–HCl, pH 8.26. The ATP solution consisted of 200 Al of 0.005 M ATP (dissolved in Specimens of W. scintillans were caught using trap nets set 0.001 M MgCl2 and kept in an ice-bath throughout the offshore in Toyama Bay. The nets were raised in early experiment) + 22 Al of 1.0 M Tris–HCl, pH 8.26.
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