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Dopamine System Components in Neuroendocrine Complexes in Snail Atrium

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Abstract

Catecholamine dopamine (DA) is an important neurotransmitter and hormone involved in many physiological processes and stress reactions in vertebrates and invertebrates. The aim of the work was to clarify the presence and localization of dopamine system elements (tyrosine hydrokinase (TH), dopamine beta-hydrokinase (DAbetaHK), and dopamine type 1 receptors (DA-R1)) in the Achatina achatina gastropod atrial neuroendocrine complex (NEC) cells. The snail atrial NEC cells are generated by large granular cells (GCs) and nerve fibers that are in close contact with them. The methods of histochemistry, immunofluorescence staining, and immunoelectron microscopy were used. Glyoxylic acid-induced fluorescence demonstrated the presence of catecholamines in the nerve fibers and GC. TH-like and DAbetaH-like immunoreactive material was found both in nerve fibers and in GC granules. DA-R1-positive material was detected only in nerve fibers. In addition, it was demonstrated that exogenous DA induces an enhanced degranulation of GC in vivo. Data obtained indicate the involvement of dopamine system in the functioning of snail NEC.

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REFERENCES

  1. Barron, A.B., Søvik, E., and Cornish, J.L., The roles of dopamine and related compounds in reward-seeking behavior across animal phyla, Front. Behav. Neurosci., 2010, vol. 4, p. 163. doi https://doi.org/10.3389/fnbeh.2010.00163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Basu, S. and Dasgupta, P.S., Dopamine, a neurotransmitter, influences the immune system, J. Neuroimmunol., 2000, vol. 102, pp. 113–124.

    Article  CAS  PubMed  Google Scholar 

  3. Bédécarrats, A., Cornet, C., Simmers, J., and Nargeot, R., Implication of dopaminergic modulation in operant reward learning and the induction of compulsive-like feeding behavior in Aplysia, Learn. Mem., 2013, vol. 20, pp. 318–327.

    Article  CAS  PubMed  Google Scholar 

  4. Beiras, R. and Widdows, J., Effect of the neurotransmitters dopamine, serotonin and norepinephrine on the ciliary activity of mussel (Mytilus edulis) larvae, Mar. Biol., 1995, vol. 122, pp. 597–603.

    Article  CAS  Google Scholar 

  5. Blom, J.M.C. and Ottaviani, E., Immune–neuroendocrine interactions: evolution, ecology, and susceptibility to illness, Med. Sci. Monit. Basic Res., 2017, vol. 23, pp. 362–367.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bystrova, O.A., Shabelnikov, S.V., and Martynova, M.G., The process of granule exocytosis in non-stimulated atrial granular cells of the snail, Achatina achatina: an ultrastructural, histochemical and immunocytochemical study, Acta Histochem., 2014, vol. 116, pp. 14–19.

    Article  CAS  PubMed  Google Scholar 

  7. Casagrande, C., Dopamine and the kidney in heart failure, Herz, 1991, vol. 16, pp. 102–115.

    CAS  PubMed  Google Scholar 

  8. Chen, M., Yang, H., Xu, B., Wang, F., and Liu, B., Catecholaminergic responses to environmental stress in the hemolymph of Zhikong scallop Chlamys farreri, J. Exp. Zool. Ecol. Genet. Physiol., 2008, vol. 309, pp. 289–296.

    Article  CAS  Google Scholar 

  9. Cheng, W., Ka, Y.W., and Chang, C.C., Dopamine beta-hydroxylase participate in the immunoendocrine responses of hypothermal stressed white shrimp, Litopenaeus vannamei, Fish Shellfish Immunol., 2016, vol. 59, pp. 166–178.

    Article  CAS  PubMed  Google Scholar 

  10. Cheng, W., Ka, Y.W., and Chang, C.C., Involvement of dopamine beta-hydroxylase in the neuroendocrine-immune regulatory network of white shrimp, Litopenaeus vannamei, Fish Shellfish Immunol., 2017, vol. 68, pp. 92–101.

    Article  CAS  PubMed  Google Scholar 

  11. Croll, R.P., Boudko, D.Y., Pires, A., and Hadfield, M.G., Transmitter contents of cells and fibres in the cephalic sensory organs of the gastropod mollusc Phestilla sibogae, Cell Tiss. Res., 2003, vol. 314, pp. 437–448.

    Article  CAS  Google Scholar 

  12. De la Torre, J.C. and Surgeon, J.W., A methodological approach to rapid and sensitive monoamine histofluorescence using a modified glyoxylic acid technique: the SPG method, Histochemistry, 1976, vol. 49, pp. 81–93.

    Article  CAS  Google Scholar 

  13. Faller, S., Stauback, S., and Klussman-Kolb, A., Comparative immunohistochemistry of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda), Zoomorphology, 2008, vol. 127, pp. 227–239.

    Article  Google Scholar 

  14. Fong, P.P., Noordhuis, R., and Ram, J.L., Dopamine reduces intensity of serotonin-induced sprowning in the zebra mussel Dreissena polymorpha (Pallas), J. Exp. Zool., 1993, vol. 266, pp. 79–83.

    Article  CAS  Google Scholar 

  15. Hernádi, L., Vehovszky, Á., and Serfőző, Z., Immunological and pharmacological identification of the dopamine D1 receptor in the CNS of the pond snail, Lymnaea stagnalis, Acta Biol. Hung., 2012, vol. 63, suppl. 2, pp. 151–159.

    Article  CAS  PubMed  Google Scholar 

  16. Kiehn, L., Saleuddin, S., and Lange, A., Dopaminergic neurons in the brain and dopaminergic innervation of the albumen gland in mated and virgin Helisoma duryi (Mollusca: Pulmonata), BMC Physiol., 2001, vol. 1, p. 9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lacoste, A., Malham, S.K., Cueff, A., and Poulet, S.A., Stress-induced catecholamine changes in the hemolymph of the oyster Crassostrea gigas, Gen. Comp. Endocrinol., 2001, vol. 122, pp. 181–188.

    Article  CAS  PubMed  Google Scholar 

  18. Liu, H., Mishima, Y., Fujiwara, T., Nagai, H., Kitazawa, A., Mine, Y., Kobayashi, H., Yao, X., Yamada, J., Oda, T., and Namikoshi, M., Isolation of araguspongine M, a new stereoisomer of an araguspongine/xestospongin alkaloid, and dopamine from the marine sponge Neopetrosia exigua collected in Palau, Mar. Drugs, 2004, vol. 2, pp. 154–163.

    Article  PubMed Central  Google Scholar 

  19. Malagoli, D. and Ottaviani, E., Cross-talk among immune and neuroendocrine systems in molluscs and other invertebrate models, Horm. Behav., 2017, vol. 88, pp. 41–44.

    Article  CAS  PubMed  Google Scholar 

  20. Marsden, C.A., Dopamine: the rewarding years, Br. J. Pharmacol., 2006, vol. 147, suppl. 1, pp. 136–144.

    Article  CAS  Google Scholar 

  21. Martynova, M.G., Krylova, M.I., and Bystrova, O.A., Immunocytochemical localization of atrial natriuretic peptide in endothelial and granular cells of the heart of Lophotrochozoa, Tsitologiia, 2004, vol. 46, no. 5, pp. 448–455.

    CAS  PubMed  Google Scholar 

  22. Martynova, M.G., Bystrova, O.A., Shabelnikov, S.V., Margulis, B.A., and Prokofjeva, D.S., Hsp70 in the atrial neuroendocrine units of the snail, Achatina fulica, Cell Biol. Int., 2007, vol. 31, pp. 413–419.

    Article  CAS  PubMed  Google Scholar 

  23. Martynova, M.G., Shabelnikov, S.V., and Bystrova, O.A., Long-term consequences of a short-term hypergravity load in a snail model, Int. J. Astrobiol., 2015, vol. 14, pp. 489–495.

    Article  CAS  Google Scholar 

  24. Martynova, M.G., Petukhova, O.A., Sharlaimova, N.S., Shabelnikov, S.V., and Bystrova, O.A., Components of corticotropin-releasing factor (CRF) signaling system in snail atria, Cell Tissue Biol., 2018, vol. 12, no. 4, pp. 342–349.

    Article  Google Scholar 

  25. McDonald, P.W., Jessen, T., Field, J.R., and Blakely, R.D., Dopamine signaling architecture in Caenorhabditis elegans, Cell Mol. Neurobiol., 2006, vol. 26, pp. 593–618.

    Article  CAS  PubMed  Google Scholar 

  26. Moroz, L.I. and Winlow, W., Respiratory behaviour in Lymnaea stagnalis: pharmacological and cellular analyses, Acta Biol. Hung., 1992, vol. 43, pp. 421–429.

    CAS  PubMed  Google Scholar 

  27. Mukai, S.T., Kiehn, L., and Saleuddin, A.S., Dopamine stimulates snail albumen gland glycoprotein secretion through the activation of a D1-like receptor, J. Exp. Biol., 2004, vol. 207, pp. 2507–2518.

    Article  CAS  PubMed  Google Scholar 

  28. Mustard, J.A., Beggs, K.T., and Mercer, A.R., Molecular biology of the invertebrate dopamine receptors, Arch. Insect Biochem. Physiol., 2005, vol. 59, pp. 103–117.

    Article  CAS  PubMed  Google Scholar 

  29. Ottaviani, E., Caselgrandi, E., Franchini, A., and Franceschi, C., CRF provokes the release of norepinephrine by hemocytes of Viviparus ater (Gastropoda, Prosobranchia): further evidence in favour of the evolutionary hypothesis of the mobile immune-brain, Biochem. Biophys. Res. Commun., 1993, vol. 193, pp. 446–452.

    Article  CAS  PubMed  Google Scholar 

  30. Pavlova, G.A., Effect of serotonin, dopamine and ergometrine on locomotion in the pulmonate mollusk Helix lucorum, J. Exp. Biol., 2001, vol. 204, pp. 1625–1633.

    CAS  PubMed  Google Scholar 

  31. Polakowski, J.S., Segreti, J.A., Cox, B.F., Hsieh, G.C., Kolasa, T., Moreland, R.B., and Brioni, J.D., Effects of selective dopamine receptor subtype agonists on cardiac contractility and regional haemodynamics in rats, Clin. Exp. Pharmacol. Physiol., 2004, vol. 31, pp. 837–841.

    Article  CAS  PubMed  Google Scholar 

  32. Quinlan, E.M., Arnett, B.C., and Murphy, A.D., Feeding stimulants activate an identified dopaminergic interneuron that induces the feeding motor program in Helisoma, J. Neurophysiol., 1997, vol. 78, pp. 812–824.

    Article  CAS  PubMed  Google Scholar 

  33. Rönnberg, E. and Pejler, G., Serglycin: the master of the mast cell, Methods Mol. Biol., 2012, vol. 836, pp. 201–217.

    Article  CAS  PubMed  Google Scholar 

  34. Rönnberg, E., Calounova, G., and Pejler, G., Mast cells express tyrosine hydroxylase and store dopamine in a serglycin-dependent manner, Biol. Chem., 2012, vol. 393, pp. 107–112.

    Article  CAS  PubMed  Google Scholar 

  35. Roshchin, M. and Balaban, P.M., Neural control of olfaction and tentacle movements by serotonin and dopamine in terrestrial snail, J. Comp Physiol. Neuroethol. Sens. Neural. Behav. Physiol., 2012, vol. 198, pp. 145–158.

    CAS  Google Scholar 

  36. Saleuddin, A.S.M., Mukai, S.T., Almeida, K., and Hatiras, G., Membrane transduction pathway in the neuronal control of protein secretion by the albumen gland in Helisoma (Mollusca), Acta Biol. Hung., 2000, vol. 51, pp. 243–253.

    CAS  PubMed  Google Scholar 

  37. Shabel’nikov, S.V., Bystrova, O.A., and Martynova, M.G., Immunolocalization of the substances P- and FMRFamide in the atrium of the snail Achatina fulica, Cell Tissue Biol., 2008, vol. 2, no. 4, pp. 451–544.

    Article  Google Scholar 

  38. Vallejo, D., Habib, M.R., Delgado, N., Vaasjo, L.O., Croll, R.P., and Miller, M.W., Localization of tyrosine hydroxylase-like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis, J. Comp. Neurol., 2014, vol. 522, pp. 2532–2552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Verlinden, H., Dopamine signalling in locusts and other insects, Insect. Biochem. Mol. Biol., 2018, vol. 97, pp. 40–52.

    Article  CAS  PubMed  Google Scholar 

  40. Werkman, T.R., De, Vlieger, T.A., and Stoof, J.C., Indications for a hormonal function of dopamine in the central nervous system of the snail Lymnaea stagnalis, Neurosci. Lett., 1990, vol. 108, pp. 167–172.

    Article  CAS  PubMed  Google Scholar 

  41. Wieland, S.J. and Gelperin, A., Dopamine elicits feeding motor program in Limax maximus, J. Neurosci., 1983, vol. 3, pp. 1735–1745.

    Article  CAS  PubMed  Google Scholar 

  42. Wilhelm, M., Silver, R., and Silverman, A.J., Central nervous system neurons acquire mast cell products via transgranulation, Eur. J. Neurosci., 2005, vol. 22, pp. 2238–2248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yang, B., Ni, J., Zeng, Z., Shi, B., You, W., and Ke, C., Cloning and characterization of the dopamine like receptor in the oyster Crassostrea angulata: expression during the ovarian cycle, Comp. Biochem. Physiol. Biochem. Mol. Biol., 2013, vol. 164, pp. 168–175.

    Article  CAS  Google Scholar 

  44. Zaitseva, O.V., Shumeev, A.N., Korshunova, T.A., and Martynov, A.V., Heterochronies in the formation of the nervous and digestive systems in early postlarval development of opisthobranch mollusks: organization of major organ systems of the Arctic dorid Cadlina laevis, Biol. Bull., 2015, vol. 42, pp. 186–195.

    Article  CAS  Google Scholar 

  45. Zhou, Z., Wang, L., Shi, X., Zhang, H., Gao, Y., Wang, M., Kong, P., Qiu, L., and Song, L., The modulation of catecholamines to the immune response against bacteria Vibrio anguillarum challenge in scallop Chlamys farreri, Fish Shellfish Immunol., 2011, vol. 31, pp. 1065–1071.

    Article  CAS  PubMed  Google Scholar 

  46. Zhuravlev, V.L., Mechanisms of neurohumoral control of gastropod heart, Zh. Evol. Biochem. Physiol., 1999, vol. 35, no. 2, pp. 65–77.

    Google Scholar 

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ACKNOWLEDGMENTS

This work was supported by the Russian Foundation for Basic Research, project no. 16-04-00069.

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Correspondence to M. G. Martynova.

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Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Translated by A. Barkhash

Abbreviations: GC—granular cell, DA—dopamine, DA-beta-H—dopamine beta hydroxylase, NEC—neuroendocrine complex, TH—tyrosine hydroxylase, DA-R1—dopamine type 1 receptors, EM—electron microscopy.

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Bystrova, O.A., Shumeev, A.N. & Martynova, M.G. Dopamine System Components in Neuroendocrine Complexes in Snail Atrium. Cell Tiss. Biol. 13, 152–159 (2019). https://doi.org/10.1134/S1990519X19020032

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