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Cephalopod myocardial receptors: Pharmacological studies on the isolated heart ofSepia officinalis (L.)

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This paper presents a synopsis of the information available about the pharmacological action of various substances on the cephalopod heart, with special emphasis on the central heart ofSepia officinalis. Threshold concentrations, EC50 values and maximum effective concentrations have been experimentally determined. Studies with various transmitter substances, analogous compounds and antagonists have led to the following picture: Acetylcholine is the natural inhibitory transmitter substance; it acts via receptors with nicotinic properties which can be blocked by d-tubocurarine and α-bungarotoxin. The probable excitatory transmitter system is represented by a noradrenergic innervation. Noradrenaline has a positive inotropic and a positive chronotropic action on in vitro heart preparations. A positive inotropic response can also be evoked by serotonin (5-HT); this effect is not due to stimulation of the catecholamine receptor, as is shown by cross-over experiments with specific blocking agents. Furthermore, a peptidergic receptor system has been described which reacts with the ‘molluscan cardioactive peptide’ FMRF amide most effectively. It is assumed that cardioactive peptides may reach the central heart in the circulating blood; the sites of synthesis and release are still unknown. Possibly the NSV-layer of the vena cava is involved in hormonal cardiovascular regulation processes.

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References

  1. Agarwal, R.A., Ligon, P.J.B., and Greenberg, M.J., Distribution of cardioactive agents in molluscan tissue. Am. Zool.9 (1969) Abstr. 249.

    Google Scholar 

  2. Agarwal, R.A., Ligon, P.J.B., and Greenberg, M.J., The distribution of cardioactive agents among molluscan species and tissues. Comp. gen. Pharmac.3 (1972) 249–260.

    Article  CAS  Google Scholar 

  3. Ahlquist, R.P., Studies of adrenotropic receptors. Am. J. Physiol.153 (1948) 486–600.

    Article  Google Scholar 

  4. Alexandrowicz, J.S., Innervation of the hearts ofSepia officinalis Acta zool. Stockh.41 (1960) 65–100.

    Article  Google Scholar 

  5. Alexandrowicz, J.S., The neurosecretory system of the vena cava in Cephalopoda I.Eledone cirrhosa. J. mar. biol. Ass. U.K.44 (1964) 111–132.

    Article  Google Scholar 

  6. Alexandrowicz, J.S., The neurosecretory system of the vena cava in Cephalopoda II.Sepia officinalis andOctopus vulgaris. J. mar. biol. Ass. U.K.45 (1965) 209–228.

    Article  Google Scholar 

  7. Atlas, S.A., Kleinert, H.D., Camargo, M.J., Januszewicz, A., Sealey, J.E., Largah, J.H., Schilling, J.W., Lewicki, J.A., Johnson, L.K., and Maack, T., Purification, sequencing and synthesis of natriuretic and vasoactive rat atrial peptide. Nature309 (1984) 717–719.

    Article  CAS  PubMed  Google Scholar 

  8. Axelrod, J., and Saavedra, J.M., Octopamin. Nature265 (1977) 501–504.

    Article  CAS  PubMed  Google Scholar 

  9. Bacq, Z.M., Action d'adrenaline, d'ergotamine et de tyramine sur le ventricule median isolé deLoligo pealii. C.r. Soc. biol.114 (1933) 1358–1360.

    CAS  Google Scholar 

  10. Bacq, Z.M., Réaction du ventricule median isolé deLoligo pealii à l'acetylcholine, à l'atropine et aux ions K, Ca et Mg. C.r. Soc. biol.114 (1933) 1360–1361.

    CAS  Google Scholar 

  11. Bacq, Z.M., Recherches sur la physiologie du système nerveux autonome. Archs int. Physiol.38 (1934) 138–159.

    CAS  Google Scholar 

  12. Bacq, Z.M., Recherches sur la physiologie et la pharmacologie du système nerveux autonome. Archs int. Physiol.42 (1935) 24–42.

    CAS  Google Scholar 

  13. Bacq, Z.M., Physiologie comparé de la transmission chimique des excitations nerveuses. Annls Soc. r. zool. Belg.72 (1941) 181–203.

    Google Scholar 

  14. Bacq, Z.M., Fischer, P., and Ghiretti, F., Action de la 5-hydroxitryptamine chez les cephalopodes. Archs int. Physiol.59 (1952) 165–171.

    Google Scholar 

  15. Berry, C.F., and Cottrell, G.A., Neurosecretion in the vena cava of the cephalopodEledone cirrosa. Z. Zellforsch.104 (1970) 107–115.

    Article  CAS  PubMed  Google Scholar 

  16. Blanchi, D., Esperimenti sulla funzione del sistema neurosecretori della vena cava nei cefalopodi. Nota I. Boll. Soc. Ital. Biol. Sper.45 (1969) 1615–1617.

    CAS  PubMed  Google Scholar 

  17. Blanchi, D., Esperimenti sulla funzione del sistema neurosecretori della vena cava nei cefalopodi. Nota II. Boll. Soc. Ital. Biol. Sper.45 (1969) 1616–1619.

    Google Scholar 

  18. Blanchi, D., Noviello, L., and Libonati, M., A neurohormone of cephalopods with cardioexcitatory activity. Gen. comp. Endocr.21 (1973) 267–277.

    Article  CAS  PubMed  Google Scholar 

  19. Bold, A.J. de, Borenstein, H.B., Veress, A.T., and Sonnenberg, H., A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci.28 (1981) 89–94.

    Article  PubMed  Google Scholar 

  20. Boyd, P.J., Gardner, C.R., and Walker, R.J., Actions of some 5-hydroxytryptamine analogues on the isolated heart of the snailHelix aspersa. Comp. Biochem. Physiol.81 (1985) 233–239.

    Google Scholar 

  21. Carlson, A.J., A note on the action of curare, atropine and nicotine on the invertebrate heart. J. gen. Physiol.4 (1922) 559–568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Cottrell, G.A., Occurrence of dopamine and noradrenaline in the nervous tissue of some invertebrate animal. Br. J. Pharmac.29 (1967) 63–69.

    CAS  Google Scholar 

  23. Cottrell, G.A., and Osborne, N., A neurosecretory system in theHelix heart. Comp. Biochem. Physiol.28 (1969) 1455–1459.

    Article  Google Scholar 

  24. Erspamer, V., and Boretti, G., Identification and characterisation by paper chromatography of enteramine, octopamine, tyramine, histamine and allied substances in extracts of posterior salivary glands of Octopoda and other tissue extracts of vertebrates and invertebrates. Archs int. Pharmacodyn.88 (1951) 296–332.

    CAS  Google Scholar 

  25. Erspamer, V., and Ghiretti, F., The action of enteramine on the heart of molluscs. J. Physiol.115 (1951) 470–481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fänge, R., and Östlund, E., The effects of adrenaline, noradrenaline, tyramine and other drugs on the isolated heart from marine vertebrates and a cephalopod. Acta zool.35 (1954) 289–305.

    Article  Google Scholar 

  27. Fiedler, A., and Schipp, R., Die monoaminerge Komponente der Innervation des Kiemenherzens vonSepia officinalis (L.)-eine vergleichend pharmakologisch-histochemische Untersuchung. Verh. dt. zool. Ges.79 (1986) 348.

    Google Scholar 

  28. Fischer, H., Vergleichende Pharmakologie von Überträgersubstanzen in tiersystematischer Darstellung, in: Handbuch der Experimentellen Pharmakologie, Bd. 26. Eds O. Eichler, A. Farah, H. Herken and A.D. Welch. Springer, Berlin 1971.

    Google Scholar 

  29. Florey, E., and Florey, E., Über die mögliche Bedeutung von Enteramin als nervöse Aktionssubstanz bei Cephalopoden und decapoden Crustaceen. Z. Naturforsch.9 (1954) 58–68.

    Article  Google Scholar 

  30. Forssmann, W.G., Hock, D., Lottspeich, F., Henschen, A., Kreye, V., Christmann, M., Reinecke, M., Metz, J., and Mutt, V., The right auricle of the heart is an endocrine organ. Cardiodilatin as a peptide hormone candidate. Anat. Embryol.168 (1983) 307–313.

    Article  CAS  Google Scholar 

  31. Forssmann, W.G., Birr, C., Carlquist, M., Christmann, M., Flinke, R., Henschen, A., Hock, D., Kirchheim, H., Kreye, V., Lottspeich, F., Metz, J., Mutt, V., and Reinecke, M., The auricular myocardiocytes of the heart constitute an endocrine organ. Characterisation of a porcine cardiac peptide hormone, cardiodilatin-126. Cell Tissue Res.238 (1984) 425–430.

    Article  CAS  PubMed  Google Scholar 

  32. Forssmann, W.G., Hock, D., Kirchheim, F., Metz, J., Mutt, V., and Reinecke, M., Cardiac hormones: morphological and functional aspects. Clin. Exp. Theor. Pract.A 6 (1984) 1873–1878.

    CAS  Google Scholar 

  33. Foti, L., Trara Genoino, J., and Agnisola, C., In vitro cardiac performance inOctopus vulgaris (LAM.). Comp. Biochem. Physiol.82c (1985) 484–488.

    Google Scholar 

  34. Frederique, H., Action cardioinhibitrice du nerf viscerale des cephalopodes: stimuli isolés et sommation de deux stimuli. Bull. Acad. r. Belg.25 (1939) 611–624.

    Google Scholar 

  35. Ghiretti, F., Studio comparativo dell'azzione della colina e dell'acetilcolina sul cuore isolato dei mollusci gasteropodi e cephalopodi. Archo Sci. biol.32 (1948) 239–251.

    CAS  Google Scholar 

  36. Goldberg, A.M., and Hanin, J., Biology of cholinergic function. Raven press, New York 1976.

    Google Scholar 

  37. Greenberg, M.J., A compendium of responses of Bivalve hearts to acetylcholine. Comp. Biochem. Physiol.14 (1965) 513–539.

    Article  CAS  PubMed  Google Scholar 

  38. Greenberg, M.J., and Price, D.A., FMRFamide, a cardioexcitatory neuropeptide of molluscs: an agent in search of a mission. Am. Zool.19 (1979) 163–174.

    Article  CAS  Google Scholar 

  39. Greenberg, M.J., and Price, D.A., Cardioregulatory peptides in molluscs, in: Peptides-Integrators of Cell and Tissue Function. pp. 107–126. Ed. F.E. Bloom. Raven press, New York 1980.

    Google Scholar 

  40. Greenberg, M.J., and Price, D.A., Invertebrate neuropeptides: native and naturalized. A. Rev. Physiol.45 (1983) 271–288.

    Article  CAS  Google Scholar 

  41. Greenberg, M.J., Roop, T., and Painter, S.D., The relative contributions of the receptors and cholinesterases to the effects of acetylcholine on the heart of bivalve molluscs. Gen. Pharmac.11 (1980) 65–74.

    Article  CAS  Google Scholar 

  42. Grigoreva, G.M., Rosengart, E.V., and Turpayev, T.M., The specificity of cholinesterase from the heart muscle and haemolymph in molluscs. J. evol. Biochem. Physiol, Suppl.: Physiology and Biochemistry of Invertebrates. Nauka, Leningrad 1968.

    Google Scholar 

  43. Higgens, W.J., Intracellular actions of 5-hydroxytryptamine on the bivalve myocardium. I. Adenylate and guanylate cylcases. J. exp. Zool.190 (1974) 99–110.

    Article  Google Scholar 

  44. Higgens, W.J., 5-hydroxytryptamine-induced tachyphylaxis of the molluscan heart and concomitant desensitization of adenylate cyclase. J. cycl. Nucleot. Res.3 (1977) 293–302.

    Google Scholar 

  45. Higgens, W.J., and Greenberg, M.J., Intracellular actions of 5-hydroxytryptamine on the bivalve myocardium. II. Cyclic nucleotide-dependent protein kinases and microsomal calcium uptake. J. exp. Zool.190 (1974) 305–316.

    Article  Google Scholar 

  46. Higgens, W.J., Price, D.A., and Greenberg, M.J., FMRFamide increases the adenylate cyclase activity and cyclic AMPlevel of molluscan heart. Eur. J. Pharmac.48 (1978) 425–430.

    Article  Google Scholar 

  47. Johansen, K., and Huston, M.J., Effects of some drugs on the circulatory system of the intact non-anesthetized cephalopod,Octopus dofleini. Comp. Biochem. Physiol.5 (1962) 177–184.

    Article  CAS  PubMed  Google Scholar 

  48. Jullien, A., Vincent, D., Bouchet, M., and Vuillet, M., Observations sur l'acétylcholine et la cholinesterase du cœur des mollusques. Annls Physiol. Physicochim. biol.14 (1938) 567–574.

    CAS  Google Scholar 

  49. Juorio, A.V., Catecholamines and 5-hydroxytryptamine in nervous tissue of cephalopods. J. Physiol.216 (1971) 213–226.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Juorio, A.V., and Barlow, J.J., Catecholamine levels in the vertical lobes ofOctopus vulgaris and other cephalopodes and the effect of experimental degeneration. Comp. gen. Pharmac.5 (1974) 281–284.

    Article  Google Scholar 

  51. Juorio, A.V., and Killick, S.W., The distribution of monoamines and some of their acid metabolites in the posterior salivary glands and viscera of some cephalopods. Comp. Biochem. Physiol.44A (1973) 1059–1067.

    Article  Google Scholar 

  52. Kehoe, J., Sealock, R., and Bou, C., Effects of α-toxins fromBungarus multicinctus andBungarus caerulcus on cholinergic responses inAplysia neurons. Brain Res.107 (1976) 527–540.

    Article  CAS  PubMed  Google Scholar 

  53. Kling, G., Innervation und Pharmakologie des Zentralherzens vonSepia officinalis (cholinerges System). Verh. dt. zool. Ges.76 (1983) 298.

    Google Scholar 

  54. Kling, G., Die Darstellung biogener Amine und der Acetylcholinesterase im Octopodenherz. Verh. dt. zool. Ges.77 (1984) 300.

    Google Scholar 

  55. Kling, G., Vergleich der Axon-Glia Beziehung im Nervus cardiacus der Cephalopoden. Verh. dt. zool. Ges.78 (1985) 289.

    Google Scholar 

  56. Kling, G., Histochemical localisation of cholinesterases and monoamines in the central heart ofSepia officinalis L. (Cephalopoda). Histochemistry85 (1986) 241–250.

    Article  CAS  PubMed  Google Scholar 

  57. Kling, G., Die Wirkung von Acetylcholin, Cholinomimetika und cholinerger Rezeptorenblocker auf das isolierte Zentralherz vonSepia officinalis. Zool. Jb. Physiol.91 (1987) 13–25.

    CAS  Google Scholar 

  58. Kling, G., and Schipp, R., The peripheral innervation of the heart ofEledone moschata demonstrated by histofluorescence microscopy. Experientia40 (1984) 1266–1268.

    Article  Google Scholar 

  59. Kling, G., and Schipp, R., Effects of biogenic amines and related agonists and antagonists on the isolated heart of the common cuttlefishSepia officinalis. Comp. Biochem. Physiol. (1987) in press.

  60. Kling, G., Wendt, C., and Hevert, F., Histochemische und pharmakologische Untersuchungen zur aminergen Innervation des Herzens vonCrassostrea gigas. Verh. dt. zool. Ges.79 (1986) 351.

    Google Scholar 

  61. Krijgsman, B.J., and Divaris, G.A., Contractile and pacemaker mechanisms of the heart of mollusca. Biol. Rev.30 (1955) 1–39.

    Article  Google Scholar 

  62. Kruta, V., Sur l'action de l'adrenaline, de l'ergotamine et du piperidinemethylbenzodioxane sur le cœur de la seiche. S.r. Soc. biol. Paris119 (1935) 397–399.

    CAS  Google Scholar 

  63. Kruta, V., Sur l'action de l'acétylcholine et de l'atropine sur le cœur deSepia officinalis. C.r. Soc. biol. Paris119 (1935) 608–610.

    CAS  Google Scholar 

  64. Kruta, V., Action de quelques alcaloides sur les nerfs cardiaques chez les céphalopodes. C.r. Soc. Biol. Paris122 (1936) 585–586.

    CAS  Google Scholar 

  65. Kruta, V., Action des poisons du système nerveux autonome sur le cœur isolé de la seiche. J. Physiol. Path. gén.34 (1936) 65–76.

    CAS  Google Scholar 

  66. Leake, L., and Walker, R.J., Invertebrate neuropharmacology. Blackie, Glasgow/London 1980.

    Google Scholar 

  67. Loe, P.R., and Florey, E., The distribution of acetylcholine and choline esterase in the nervous system and in innervated organs ofOctopus dofleini. Comp. Biochem. Physiol.17 (1966) 509–522.

    Article  CAS  PubMed  Google Scholar 

  68. Loewi, O., Über humorale Übertragbarkeit der Herznervenwirkung. Pflügers Arch. ges. Physiol.189 (1921) 239–242.

    Article  Google Scholar 

  69. Mandelbaum, D.E., Koester, J., Schonberg, M., and Weiss, K.R., Cyclic AMP mediation of the excitatory effect of serotonin in the heart ofAplysia. Brain Res.177 (1979) 388–394.

    Article  CAS  PubMed  Google Scholar 

  70. Martin, R., Fine structure of the neurosecretory system of the vena cava. Brain Res.8 (1968) 201–205.

    Article  CAS  PubMed  Google Scholar 

  71. Martin, R., Frösch, D., Weber, E., and Voigt, K.H., Met-enkephalin-like immunreactivity in a cephalopod neurohemal organ. Neurosci. Lett.15 (1979) 253–257.

    Article  CAS  PubMed  Google Scholar 

  72. Martin, R., Frösch, D., and Voigt, K.H., Immunocytochemical evidence for melanotropin- and vasopressin-like material in a cephalopod neurohemal organ. Gen. comp. Endocr.42 (1980) 235–243.

    Article  CAS  PubMed  Google Scholar 

  73. Martin, R., Frösch, D., Kiahling, C., and Voigt, K.H., Molluscan neurophysin-like and enkephalin-like materials coexist inOctopus nerves. Neuropeptides2 (1981) 141–150.

    Article  CAS  Google Scholar 

  74. Östlund, E., The distribution of catecholamines in lower animals and their effect on the heart. Acta physiol. scand.31, Suppl. 112 (1954) 1–67.

    Google Scholar 

  75. Painter, S.D., and Greenberg, M.J., A survey of responses of Bivalve hearts to the molluscan neuropeptide FMRFamide and to 5-hydroxytryptamine. Biol. Bull.162 (1982) 311–332.

    Article  CAS  Google Scholar 

  76. Price, D.A., and Greenberg, M.J., Purification and characterisation of a cardioexcitatory neuropeptide from the central ganglia of a bivalve mollusc. Prep. Biochem.7 (1977) 261–281.

    CAS  PubMed  Google Scholar 

  77. Price, D.A., and Greenberg, M.J., Structure of a molluscan cardioexcitatory neuropeptide. Science197 (1977) 670–671.

    Article  CAS  PubMed  Google Scholar 

  78. Ransom, W.B., On the cardiac rhythm of Invertebrata. J. Physiol.5 (1884) 261–341.

    Article  Google Scholar 

  79. Richter, K., Struktur und Funktion der Herzen wirbelloser Tiere. Zool. Jb. Physiol.77 (1973) 477–668.

    Google Scholar 

  80. Reinecke, M., Nehls, M., and Forssmann, W.G., Phylogenetic aspects of cardiac hormones as revealed by immunocytochemistry, electronmicroscopy, and bioassay. Peptides6 (1986) 321–331.

    Article  Google Scholar 

  81. Schipp, R., and Schäfer, A., Vergleichende elektronenmikroskopische Untersuchungen an den zentralen Herzorganen von Cephalopoden (Sepia officinalis). Feinstruktur des Herzens. Z. Zellforsch.98 (1969) 576–598.

    Article  CAS  PubMed  Google Scholar 

  82. Tansey, E.M., Neurotransmitters in the cephalopod brain. Comp. Biochem. Physiol. C64 (1979) 173–182.

    Article  Google Scholar 

  83. Tansey, E.M., Aminergic fluorescence in the cephalopod brain. Phil. Trans. R. Soc. B291 (1980) 127–146.

    Google Scholar 

  84. Vincent, D., and Jullien, A., L'activité cholinestérasique des extraits myocardique chez les mollusques. C.r. Soc. biol.127 (1938) 631–632.

    CAS  Google Scholar 

  85. Voigt, K.H., Kiehling, C., Frösch, D., and Martin, R., Enkephalin-related peptides: direct action on the octopus heart. Neurosci. Lett.27 (1981) 25–30.

    Article  CAS  PubMed  Google Scholar 

  86. Voigt, K.H., Kiehling, C., Frösch, D., Bickel, U., Geis, R., and Martin, R., Identify and function of neuropeptides in the vena cava neuropil ofOctopus, in: Molluscan Neuroendocrinology, pp. 228–234. Eds J. Lever and H.H. Boer. North Holland Publishing Company, Amsterdam-Oxford-New York 1983.

    Google Scholar 

  87. Walker, R.J., and Kerkut, G.A., The first family. Comp. Biochem. Physiol.61C (1978) 261–266.

    CAS  Google Scholar 

  88. Waser, P.G., Cholinergic mechanisms. Raven Press, New York 1976.

    Google Scholar 

  89. Wells, M.J., Circulation in cephalopods, in: The Mollusca, vol. 5, pp. 239–290. Ed. K.M. Wilbur. Academic Press, New York 1983.

    Chapter  Google Scholar 

  90. Wells, M.J., Hormones and the circulation inOctopus, in: Molluscan Endocrinology, pp. 221–228. Eds J. Lever and H.H. Boer. Amsterdam-Oxford-New York 1983.

  91. Wells, M.J., and Mangold, K., The effects of extracts from neurosecretory cells in the anterior vena cava and pharyngoopthalmic vein upon the heart of the intact freemovingOctopuses. J. exp. Biol.84 (1980) 319–334.

    Article  CAS  PubMed  Google Scholar 

  92. Wright, A.C., Moorhead, M., and Welsh, J.H., The actions of derivatives of lysergid acid on the heart ofVenus mercenaria. Br. J. Pharmac.18 (1962) 440–450.

    CAS  Google Scholar 

  93. Zeimal, E.V., and Vulvius, E.A., Pharmacology of cholinergic systems in molluscs, in: Comparative Pharmacology, vol. 1, pp. 111–168. Ed. M.J. Michelson. Pergamon Press, Oxford 1983.

    Google Scholar 

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  1. Institut für Allgemeine und Spezielle Zoologie, Justus-Liebig-Universität, Stephanstr. 24, D-6300, Giessen, Germany

    G. Kling & P. M. Jakobs

  2. Station de Biologie Marine d'Arcachon, F-33120, Arcachon, France

    G. Kling & P. M. Jakobs

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Kling, G., Jakobs, P.M. Cephalopod myocardial receptors: Pharmacological studies on the isolated heart ofSepia officinalis (L.). Experientia 43, 511–525 (1987). https://doi.org/10.1007/BF02143580

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