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Regulation of adenylyl cyclase signaling system by insulin, biogenic amines and glucagon at their separate and combined action in muscle membranes of mollusc Anodonta cygnea

  • Comparative and Ontogenic Biochemistry
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Abstract

In the smooth muscles of mollusc Anodonta cygnea the regulatory action of hormones on adenylyl cyclase signaling system (ACSS) are realized through the receptors of serpentine type (biogenic amines, isoproterenol, glucagon) and receptor tyrosine kinase (insulin) type. Intracellular mechanisms of their interaction are interconnected. Application of hormones, their antagonists and pertussis toxin in combination with insulin and biogenic amines or glucagon on adenylyl cyclase (AC) activity allows revealing the possible sites of cross-linking in the mechanisms of their action. Combined influence of insulin and serotonin or glucagon leads to decreased stimulation of adenylyl cyclase (AC) by these hormones, whereas combined application of insulin and isoproterenol suppresses AC-stimulating effect of insulin, but AC-inhibiting effect of isoproterenol is maintained in the presence and absence of non-hydrolysable analog of GTP—guanylyl imido diphosphate (GIDP). The specific blockage of AC-stimulating effect of serotonin by cyproheptadine—antagonist of serotonin receptors, did not change AC stimulation by insulin. Beta-adrenoblockers (propranolol and alprenolol) prevent inhibition of AC activity by isoproterenol, but did not change AC stimulation by insulin. Pertussis toxin blocked AC-inhibiting effect of isoproterenol and weakened AC-stimulating action of insulin. Thus, in the muscles of Anodonta cygnea negative interaction between ACS have been revealed, which are realized under combined influence of insulin and serotonin or glucagon, most probably, at the level of receptor of serpentine type (serotonin, glucagon), whereas under action of insulin and isoproterenol at the level of Gi protein and AC interaction.

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References

  1. Fabbri, E. and Capuzzo, A., Cyclic AMP Signaling in Bivalve Molluscs: an Overview, J. Exp. Zool. Ecol. Genet. Physiol., 2010, vol. 313, pp. 179–200.

    Google Scholar 

  2. Feldman, R.D., Insulin-Mediated Sensitization of Adenylyl Cyclase Activation, Br. J. Pharmacol., 1993, vol. 110, pp. 1640–1647.

    Article  PubMed  CAS  Google Scholar 

  3. Hurley, J.H., Zhang, S., Bye, L.S., Marshall, M.S., De Paoli-Roach, A.A., Guan, K., Fox, A.P., and Yu, L., Insulin Inhibits the 5-HT2c Receptor in Choroids Plexus via MAP Kinase, BMC Neurosci., 2003, vol. 4, pp. 2202–2210.

    Article  Google Scholar 

  4. Rodriguez-Perez, C.E., Calvo-Ochoa, E., Kalashnikova, E.V., Reyes-Cruz, G., Romero-Avila, M.T., and Garcia-Sainz, J.A., Receptor Tyrosine Kinases Regulate Alpha1 D-Adrenoceptor Signaling Properties: Phosphorylation and Desensitization, Int. J. Biochem. Cell Biol., 2009, vol. 41, pp. 1276–1283.

    Article  PubMed  CAS  Google Scholar 

  5. Chesik, D., Wilczak, N., and De Keyser, J., IGF-1 Regulates cAMP Levels in Astrocytes through a Beta2-Adrenergic Receptor-Dependant Mechanism, Int. J. Med. Sci., 2008, vol. 5, pp. 240–243.

    Article  PubMed  CAS  Google Scholar 

  6. Bennun, A., Characterization of the Norepinephrine-Activation of Adenylate Cyclase Suggests a Role in Memory Affirmation Pathways. Overexposure to Epinephrine Inactivates Adenylate Cyclase, a Causal Pathway for Stress-Pathologies, Biosystems, 2010, vol. 100, pp. 87–93.

    Article  PubMed  CAS  Google Scholar 

  7. Sunabara, R.K. and Taussig, R., Isoforms of Mammalian Adenylyl Cyclase: Multiplicities of Signaling, Mol. Intervol., 2002, vol. 2, pp. 168–184.

    Article  Google Scholar 

  8. Sadana, R. and Dessauer, C.W., Physiological Roles for G Protein-Regulated Adenylyl Cyclase Isoforms: Insights from Knockout and Overexpression Studies, Neurosignals, 2009, vol. 17, pp. 5–22.

    Article  PubMed  CAS  Google Scholar 

  9. Pertseva, M.N., Kuznetzova, L.A., Plesneva, S.A., Grishin, A.V., and Panchenko, M.P., Beta-Agonist-Induced Inhibitory-Guanine-Nucleotide-Binding Regulatory Protein Coupling to Adenylate Cyclase in Mollusc Anodonta cygnea Foot Muscle Sarcolemma, Eur. J. Biochem., 1992, vol. 210, pp. 279–286.

    Article  PubMed  CAS  Google Scholar 

  10. Shpakov, A.O., Shipilov, V.N., Bondareva, V.M., Kuznetsova, L.A., Plesneva, S.A., Rusakov, Yu.I., and Pertseva, M.N., Regulatory Effect of Insulin-Related Neuropeptides of Mollusc Anodonta cygnea on the Functional Activity of Adenylyl Cyclase Signaling System, Neirokhimiya, 2005, vol. 22, pp. 28–37.

    Google Scholar 

  11. Pertseva, M.N., Shpakov, A.O., Plesneva, S.A., and Kuznetsova, L.A., A Novel View on the Mechanisms of Action of Insulin and Other Insulin Superfamily Peptides: Involvement of Adenylyl Cyclase Signaling System, Comp. Biochem. Physiol., 2003, vol. 134, pp. 11–36.

    CAS  Google Scholar 

  12. Kuznetsova, L.A., Plesneva, S.A., Derkach, K.V., and Pertseva, M.N., Effects of Biogenic Amines and Glucagon on the Adenylate Cyclase System in Molluscan, Holothurian and Ascidian Muscle Membranes, Comp. Biochem. Physiol., 1995, vol. 111, pp. 293–301.

    Article  Google Scholar 

  13. Klein, M., Differential Cyclic AMP Dependence of Facilitation at Aplysia Sensorimotor Synapses as a Function of Prior Stimulation: Augmentation versus Restoration of Transmitter Release, J. Neurosci., 1993, vol. 13, pp. 3793–3801.

    PubMed  CAS  Google Scholar 

  14. Brennesvik, E.O., Ktori, C., Ruzzin, J., Jebens, E., Shepherd, P.R., and Jensen, J., Adrenaline Potentiates Insulin-Stimulated PKB Activation via cAMP and Epac: Implications for Cross Talk between Insulin and Adrenaline, Cell. Signal., 2005, vol. 17, pp. 1551–1559.

    Article  PubMed  CAS  Google Scholar 

  15. Hadcock, J.R., Port, J.D., Gelman, M.S., and Malbon, C.C., Cross-Talk between Tyrosine Kinase and G-Protein-Linked Receptors. Phosphorylation of Beta 2-Adrenergic Receptors in Response to Insulin, J. Biol. Chem., 1992, vol. 267, pp. 26 017–26 022.

    CAS  Google Scholar 

  16. Kidwai, A.M., Radcliffe, M.A., Lee, E.Y., and Daniel, E.E., Isolation and Properties of Skeletal Muscle Membranes, Biochem. Biophys. Acta, 1973, vol. 298, pp. 593–607.

    Article  PubMed  CAS  Google Scholar 

  17. Salomon, Y., Londos, C., and Rodbell, M., A Highly Sensitive Adenylate Cyclase Assay, Anal. Biochem., 1974, vol. 58, pp. 541–548.

    Article  PubMed  CAS  Google Scholar 

  18. Pertseva, M.N., Plesneva, S.A., Shpakov, A.O., Rusakov, Yu.I., and Kuznetsova, L.A., Involvement of Adenylyl Cyclase Signalling System in the Action of Insulin and Mollusc Insulin-Like Peptide, Comp. Biochem. Physiol., 1995, vol. 112, pp. 689–695.

    Article  CAS  Google Scholar 

  19. Cohen, J.E., Onyike, C.U., McElroy, V.L., Lin, A.H., and Abrams, T.W., Pharmacological Characterization of an Adenylyl Cyclase-Coupled 5-HT Receptor in Aplysia: Comparison with Mammalian 5-HT Receptors, J. Neurophysiol., 2003, vol. 89, pp. 1440–1455.

    Article  PubMed  CAS  Google Scholar 

  20. Jarrard, H.E., Goldsmith, B.A., and Abrams, T.W., In Aplysia Sensory Neurons, the Neuropeptide SCPB and Serotonin Differ in Efficacy Both in Modulating Cellular Properties and in Activating Adenylyl Cyclase: Implications for Mechanisms Underlying Presynaptic Facilitation, Brain Res., 1993, vol. 616, pp. 188–199.

    Article  PubMed  CAS  Google Scholar 

  21. Gilles, M., Wilke, A., Kopf, D., Nonell, A., Lehnert, H., and Deuschle, M., Antagonism of the Serotonin (5-HT)2 Receptor and Insulin Sensitivity: Implication for Atypical Antipsychotics, Psychosomat. Medic., 2005, vol. 67, pp. 748–751.

    Article  CAS  Google Scholar 

  22. Lee, Y.S., Choi, S.L., Lee, S.H., Kim, H., Park, H., Lee, N., Lee, S.H., Chae, Y.S., Jang, D.J., Kandel, E.R., and Kaang, B.K., Identification of a Serotonin Receptor Coupled to Adenylyl Cyclase Involved in Learning-Related Heterosynaptic Facilitation in Aplysia, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 14 634–14 639.

    CAS  Google Scholar 

  23. Lin, A.H., Cohen, J.E., Wan, Q., Niu, K., Shrestha, P., Bernstein, S.L., and Abrams, T.W., Serotonin Stimulation of cAMP-Dependent Plasticity in Aplysia Sensory Neurons is Mediated by Calmodulin-Sensitive Adenylyl Cyclase, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 15 607–15 612.

    CAS  Google Scholar 

  24. Bahouth, S.W. and Lopez, S., Insulin Desensitized Beta 1-Adrenergic Receptor-Mediated Stimulation of Adenylyl Cyclase in SK-N-MC Cells, Life Sci., 1992, vol. 51, pp. PL271–276.

    Article  PubMed  CAS  Google Scholar 

  25. Morisco, C., Condorelli, G., Trimarco, V., Bellis, A., Marrone, C., Condorelli, G., Sadoshima, J., and Trimarco, B., Akt Mediates the Cross-Talk Between Beta-Adrenergic and Insulin Receptors in Neonatal Cardiomyocytes, Circ. Res., 2005, vol. 96, pp. 180–188.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Sechenov Institute of Evolutionary Physiology and Biochemistry Russian Academy of Sciences, St. Petersburg, Russia

    L. A. Kuznetsova, S. A. Plesneva, T. S. Sharova, M. N. Pertseva & A. O. Shpakov

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  1. L. A. Kuznetsova
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  2. S. A. Plesneva
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  3. T. S. Sharova
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  4. M. N. Pertseva
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  5. A. O. Shpakov
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Correspondence to S. A. Plesneva.

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Original Russian Text © L.A. Kuznetsova, S.A. Plesneva, T.S. Sharova, M.N. Pertseva, A.O. Shpakov, 2013, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2013, Vol. 49, No. 2, pp. 111–117.

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Kuznetsova, L.A., Plesneva, S.A., Sharova, T.S. et al. Regulation of adenylyl cyclase signaling system by insulin, biogenic amines and glucagon at their separate and combined action in muscle membranes of mollusc Anodonta cygnea . J Evol Biochem Phys 49, 145–152 (2013). https://doi.org/10.1134/S0022093013020035

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  • DOI: https://doi.org/10.1134/S0022093013020035

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