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RECEPTOR DIFFERENTIATION and MECHANISMS of SIGNAL TRANSDUCTION in the CIRCULATORY SYSTEM of SEPIA OFFICINALIS R Schipp, T Lehr

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RECEPTOR DIFFERENTIATION and MECHANISMS of SIGNAL TRANSDUCTION in the CIRCULATORY SYSTEM of SEPIA OFFICINALIS R Schipp, T Lehr RECEPTOR DIFFERENTIATION AND MECHANISMS OF SIGNAL TRANSDUCTION IN THE CIRCULATORY SYSTEM OF SEPIA OFFICINALIS R Schipp, T Lehr To cite this version: R Schipp, T Lehr. RECEPTOR DIFFERENTIATION AND MECHANISMS OF SIGNAL TRANS- DUCTION IN THE CIRCULATORY SYSTEM OF SEPIA OFFICINALIS. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2006, pp.157-165. hal-03228738 HAL Id: hal-03228738 https://hal.sorbonne-universite.fr/hal-03228738 Submitted on 18 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. VIE ET MILIEU – LIFE & ENVIRONMENT, 2006, 56 (2) : 157-165 The cuttlefish Sepia officinalis (N. Koueta, J.P. Andrade, S. v. Boletzky, eds) RECEPTOR DIFFERENTIATION AND MECHANISMS OF SIGNAL TRANSDUCTION IN THE CIRCULATORY SYSTEM OF SEPIA OFFICINALIS R. SCHIPP*, T. LEHR Institut für Allgemeine und Spezielle Zoologie, Justus-Liebig-Universität Giessen, Stephanstrasse 24, 35390 Giessen, Germany * corresponding author: [email protected] SEPIA OFFICINALIS ABSTRACT. – Considering most recent pharmacological as well as histo- and bio- RECEPTORS chemical findings, receptor differentiations and mechanisms of signal transduction SIGNAL TRANSDUCTION in central organs of the circulatory system of Sepia officinalis are demonstrated. In CIRCULATORY SYSTEM this easily available species the systemic and branchial heart, the cephalic aorta and vein as well as the branchial vein are well accessible to experimental studies; these studies suggest: 1. The neurotransmitters: acetylcholine (ACh), noradrenaline (NA), adrenaline (A), dopamine (DA), 5-hydroxytryptamine (5-HT), FMRFamide and nitric oxide (NO) are involved in the neuroregulation showing very different action profiles in the organs mentioned. 2. As in vertebrates there is a general but differing excitatory-inhibitory antagonism between monoamines and ACh. 3. The ACh-receptor seems to be of a nicotinic type, mediating inhibitory actions in the heart organs and arteries but a peristalsis activation in the cephalic vein. 4. Cate- cholamines act by an α1-like receptor coupled with the PI-cycle, that is ascertained for the cephalic aorta, the systemic and branchial heart; for the auricle and branchial vein additionally a β-like cAMP coupled receptor seems probable. 5. 5- HT is an essential neurotransmitter in all the organs studied; in the densely- innervated, autonomously contractile auricle, the central motor of the blood circula- tion, four different receptors seem to be established: a 5HT1– and 5-HT4-like recep- tor, cAMP coupled and a 5-HT2-like receptor, PI-response-coupled as well as a 5- HT3-like receptor that is probably an ion channel. 6. NO is demonstrated for the cephalic aorta and the rhythmically contractile bulbus of the branchial heart, mediating inhibitory and dilatatory actions by the cGMP mechanism. INTRODUCTION and biochemical investigations, especially results of physio-pharmacological bioassays applying neuro- transmitters and their mimetics as well as antago- The highly evolved central nervous system, nists and inhibitors of enzymes to characterise the sense organs and behaviour of the coleoid cephalo- receptors; an undertaking that is faced with the fun- pods are supported by the efficient and sophisti- damental problem that the immense potential of cated performance of the nearly closed circulatory pharmacological tools available has been primarily system (Wells & Smith 1987, Schipp 1987a). For designed for the receptor classification of verte- experimental studies of this system Sepia brates. But for lack of other, invertebrate neurosci- officinalis is a well suited model, because the ence had to use these, and the results more and more animals are available in great number, readily yielded the insight that in cephalopods the standardised in age and size, easily cultured and neuroreceptors are as complex as those of verte- their central circulatory system clears up like an brates and that there are remarkable similarities, open book after some quick surgical cuts per- which is surprising given the fact that both groups formed on the anaesthetized animal (Fig. 1A). – have evolved separately for some hundred millions Our contribution intends to give an overview and of years. outlook on the most recent studies concerning the neurotransmitters, the receptor differentiation and putative mechanisms of signal transduction of Thesystemicheart some central organs of this system. The results concern: the systemic heart and its auricles, the ThesystemicheartofS. officinalis consists of branchial heart complex, the cephalic aorta, the ce- the ventricle – which is innervated by the nervus phalic vein and the branchial vein. This account is cardiacus – and two auricles with a remarkably considering histochemical, immunohistochemical dense nerve supply by fibres of the ganglion cardi- 158 R. SCHIPP, T. LEHR acum (Alexandrowicz 1960) (Fig. 1B). The auri- well as by transmitters released by the neurohemal cles show a myogenic automatism, in contrast to organ (NSV-system) in the cephalic vein (Martin & the ventricle, which is under control of the pace- Voigt 1987, Schipp 1987b, Marschinke & Schipp maker function of them. In vivo the beating rhythm 1993). of both auricles is neuronally synchronized by cen- Many earlier histochemical and pharmacologi- ters within the visceral ganglion (Schipp et al. cal studies suggest that, besides catecholamines, 1997, Versen et al. 1997, Versen & Schipp 1997) as serotonin (5-HT) and acetylcholine (ACh), numer- ous further putative neurotransmitters (particularly peptides) are involved in the neurocontrol of the systemic heart of coleoids, and it seems probable that they have also corresponding receptors situ- ated in the sarcolemma of the cardiomyocytes (Kling & Jakobs 1987, Jakobs 1991, Messenger 1996) (Table I). More recent pharmacological and biochemical findings gave first evidence concern- ing a further subclassification and the pathways of signal transduction of the putative catechola- minergic and serotoninergic receptors, especially for the auricle; these will be referred to here. Phar- macological bioassays of Versen et al. (1999) using different agonists together with blocking drugs and enzyme inhibitors suggest that there are two catecholaminergic receptors established in the auri- cle myocytes: an α-like adrenoreceptor mediating mainly positive chronotropic effects, which accord- ing to biochemical findings seem to be generated by the G-protein coupled PI-cycle (phosphati- dylinositol response) (Berridge 1987) (Fig. 2A, B) and a β-like receptor, mediating positive inotropic effects by activating the cAMP second messenger pathway that is also G-protein coupled and that could be blocked by the adenylate cyclase inhibitors MDL-12,330A and SQ-22,536. Pharmacological findings of Pflänzel (1994) concerning the cholinergic neuroregulation of the auricle of S. officinalis revealed a nicotinergic receptor, because arecoline, carbachol and nicotine mimicked the negative inotropic ACh-action but not the m-ligands muscarine, pilocarpine or oxotremorine. However, the fact that the ACh-action could be blocked by α-bungarotoxine (α-BTX) but Fig. 1. – A, Diagram of the circulatory system of Sepia officinalis in ventral view. V=ventricle, AU=auricles, BH=branchial hearts, BHA=branchial heart appendages; arteries: CA/PAO= cephalic and posterior aorta, AFUA=anterior funnel artery, AMA=anterior mantle a., BRA=branchial a., GA=genital a., OA=ophtalmic a., PFUA=posterior funnel a., SA=siphuncle a., TA=ten- tacle a.; veins: AV=arm v., ABV/EBV=afferent and ef- ferent branchial vessels, ACV=anterior cephalic vein., AFV=anterior funnel v., AFIV=anterior fin v., AMV=anterior mantle v., CV=cephalic v., ISV=inksac v., OV=ophthalmic v., PFV=posterior funnel v., PMV=posterior mantle v., RVH=ring vein of head, VC=vena cava, OS/PBS=optic and peribuccal blood si- nus (from Schipp 1987a). B, Innervation of the systemic heart and branchial heart complex of Sepia officinalis by the paired visceral nerve; nervus cardiacus (arrow heads) (after Alexandrowicz 1960). RECEPTOR DIFFERENTIATION IN THE CIRCULATORY SYSTEM OF S. OFFICINALIS 159 Table I. – Effects of intrinsic neurotransmitters of the central organs of the circulatory system of Sepia officinalis L.* also by the m2-antagonist 4-DAMP and that the classic n-antagonist d-tubocurarine blocked the action of nicotine but not that of ACh has been in- terpreted as an indication that a G-protein coupled m-receptor could also be present (Hannan & Hall 1993, Pflänzel 1994). In accordance with fluores- cence- and immunohistochemical findings on the occurrence of 5-HT in the auricle nerve endings of S. officinalis recent pharmacological studies re- vealed a sophisticated system of probably four dif- ferent 5-HT receptor-subtypes mediating excit- atory or inhibitory effects (Lehr & Schipp 2004a, Lehr & Schipp 2004b, Lehr & Schipp 2005) (Fig.3A).A5-HT1-like subtype generating posi- tive chronotropic, inotropic and tonotropic effects is counteracted by a 5-HT4-like subtype mediating negative
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