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Effect of kainic acid injections and other brain lesions on vasoactive intestinal peptide (VIP)-stimulated formation of cAMP in rat brain

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Summary

In rat striatal slices, both intrastriatal kainic acid injection, which destroys striatal neurones, and intranigral injection of 6-hydroxydopamine (6-OHDA), which leads to a degeneration of dopamine nerve terminals in the striatum, reduced vasoactive intestinal peptide (VIP)-induced cAMP accumulation by approximately 60%. Cortical ablation, which leads to degeneration of cortico-striatal fibres, had no effect on striatal VIP-induced cAMP formation, Knife cut lesions transecting the stria terminalis, which destroy afferent fibres to the amygdala, decreased the VIP-induced increase in cAMP in amygdala slices by 40%, while kainic acid injection into the amygdala had no effect. Kainic acid injection into several other brain regions, including hippocampus, cortex and hypothalamus also failed to affect the VIP-elicited increase in cAMP in slices, despite reductions in choline acetyltransferase, glutamate decarboxylase, cyclic nucleotide phosphodiesterase and basal levels of cAMP. The results of a study of the effects of various VIP fragments on cAMP stimulation in striatal and cortical slices suggests that the entire sequence of VIP is necessary for full activity. The results suggest that VIP may be involved in neuromodulation or neurotransmission in the striatum and/or nigrostriatal pathway and also in the stria terminalis from the bed nucleus to the amygdala.

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References

  • Albers, R. W., Brady, R. O.: The distribution of glutamate decarboxylase in the nervous system of the Rhesus monkey. J. Biol. Chem. 234, 926–928 (1959)

    Google Scholar 

  • Bataille, D., Freychet, P., Rosselin, C.: Interaction of glucagon, gut glucagon, vasoactive intestinal polypeptide and secretin with liver and fat cell plasma membranes: binding to specific sites and stimulation of adenylate cyclase. Endocrinology 95, 713–721 (1974)

    Google Scholar 

  • Bodanszky, M., Klausner, Y. S., Said, S. I.: Biological activities of synthetic peptides corresponding to fragments of and to the entire sequence of the vasoactive intestinal peptide. Proc. Natl. Acad. Sci. U.S.A. 70, 383–384 (1973)

    Google Scholar 

  • Brown, B. L., Albano, J. D. M., Ekins, R. P., Sgherzi, A. M.: A simple and sensitive saturation assay for the measurement of adenosine-3′ 5′-cyclic monophosphate. Biochem. J. 121, 561–562 (1971)

    Google Scholar 

  • Bryant, M. G., Polak, J. M., Modlin, I., Bloom, S. R., Albuquerque, R. H., Pearse, A. G. E.: Possible dual role for vasoactive intestinal peptide as a gastrointestinal hormone and neurotransmitter substance. Lancet 1976I, 991–993

  • Coyle, J. T., Schwarcz, R.: Lesions of striatal neurons with kainic acid provides a model for Huntington's chorea. Nature 263, 244–246 (1976)

    Google Scholar 

  • de Olmos, J. S.: The amygdaloid projection field in the rat as studied with the cupric-silver method. In: Neurobiology of the amygdala (B. Eleftheriou, ed.), pp. 145–204. New York: Plenum Press 1972

    Google Scholar 

  • Desbuquois, B., Laudat, M. H., Laudat, P.: Vasoactive intestinal polypeptide and glucagon: stimulation of adenylate cyclase activity via distinct receptors in liver and fat cell membranes. Biochim. Biophys. Res. Commun. 53, 1187–1194 (1973)

    Google Scholar 

  • Deschodt-Lanckman, M., Robberecht, P., Christophe, J.: Characterization of VIP sensitive adenylate cyclase in guinea pig brain. FEBS Letters 83, 76–80 (1977)

    Google Scholar 

  • Emson, P. C., Fahrenkrug, J., Schaffalitzky de Muckadell, O. B., Jessell, T. M., Iversen, L. L.: Vasoactive intestinal polypeptide (VIP): vesicular localization and potassium evoked release from rat hypothalamus. Brain Res. 143, 174–178 (1978a)

    Google Scholar 

  • Emson, P. C., Jessell, T., Paxinos, G., Cuello, A. C.: Substance P in the amygdaloid complex, bed nucleus and stria terminalis of the rat. Brain Res. 149, 97–105 (1978b)

    Google Scholar 

  • Emson, P. C., Paxinos, G., LeGal La Salle, G., Ben-Ari, Y., Silver, A.: Choline acetyltransferase and acetylcholinesterase containing projections from the basal forebrain of the rat to the amygdaloid complex. Brain Res. (in press, 1979)

  • Fahrenkrug, J., Schaffalitzky de Muckadell, O. B.: Distribution of vasoactive intestinal polypeptide in the porcine central nervous system. J. Neurochem. 31, 1445–1452 (1978)

    Google Scholar 

  • Fonnum, F.: Radiochemical microassays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem. J. 115, 465–472 (1969)

    Google Scholar 

  • Fonnum, F., Storm-Mathisen, J., Walberg, F.: Glutamate decarboxylase in inhibitory neurons. A study of the enzyme in Purkinje cell axons and boutons in the cat. Brain Res. 20, 275–279 (1970)

    Google Scholar 

  • Forn, J., Krueger, B. K., Greengard, P.: Adenosine-3′5′-monophosphate content in rat caudate nucleus: demonstration of dopaminergic and adrenergic receptors. Science 186, 1118–1120 (1974)

    Google Scholar 

  • Frandsen, E. K., Krishna, G. A., Said, S. I.: Vasoactive intestinal polypeptide promotes cyclic adenosine 3′,5′-monophosphate accumulation in guinea pig trachea. Br. J. Pharmacol. 62, 367–369 (1978)

    Google Scholar 

  • Fuxe, K., Hökfelt, T., Said, S. I., Mutt, V.: Vasoactive intestinal polypeptide and the nervous system: immunohistochemical evidence for localization in central and peripheral neurons, particularly intracortical neurons of the cerebral cortex. Neurosci. Lett. 5, 241–246 (1977)

    Google Scholar 

  • Giachetti, A., Rosenberg, R. N., Said, S. I.: Vasoactive intestinal polypeptide in brain synaptosomes. Lancet 1976II, 741–742

  • Giachetti, A., Said, S. I., Reynolds, R. C., Koniges, F. C.: Vasoactive intestinal polypeptide in brain: localization in and release from isolated nerve terminals. Proc. Natl. Acad. Sci. U.S.A. 74, 3424–3428 (1977)

    Google Scholar 

  • Hattori, T., McGeer, E. C.: Fine structural changes in the rat striatum after local injection of kainic acid. Brain Res. 129, 174–180 (1977)

    Google Scholar 

  • Hendry, I. A., Iversen, L. L.: Effect of nerve growth factor and its antiserum on tyrosine hydroxylase activity in mouse superior cervical ganglion. Brain Res. 29, 159–162 (1971)

    Google Scholar 

  • Herndon, R. M., Coyle, J. T.: Selective destruction of neurons by a transmitter agonist. Science 198, 71–72 (1977)

    Google Scholar 

  • König, J. F. R., Klippel, R. A.: The rat brain: A stereotaxic atlas of the forebrain and lower parts of the brain stem. Baltimor, Md.: Williams and Wilkins 1963

    Google Scholar 

  • Krueger, B. K., Forn, J., Walters, J. R., Roth, R. H., Greengard, P.: Stimulation by dopamine of adenosine cyclic 3′,5′-monophosphate formation in rat caudate nucleus: effect of lesions of the nigrostriatal pathway. Mol. Pharmacol. 12, 639–648 (1976)

    Google Scholar 

  • Larsson, L.-I., Fahrenkrug, J., Schaffalitzky de Muckadell, O., Sundler, F., Hakånson, R., Rehfeld, J. F.: Localization of vasoactive intestinal polypeptide (VIP) to central and peripheral neurons. Proc. Natl. Acad. Sci. U.S.A. 73, 3197–3200 (1976a)

    Google Scholar 

  • Larsson, L.-I., Edvinsson, L., Fahrenkrug, J., Hakånson, R., Owman, Ch., Schaffalitzky de Muckadell, O., Sundler, F.: Immunohistochemical localization of a vasodilatory polypeptide (VIP) in cerebrovascular nerves. Brain Res. 113, 400–404 (1976b)

    Google Scholar 

  • Lehmann, J., Fibiger, H. C.: Acetylcholinesterase in the substantia nigra and caudate putamen of the rat: properties and localization in dopaminergic neurons. J. Neurochem. 30, 615–624 (1978)

    Google Scholar 

  • Loren, I., Emson, P. C., Fahrenkrug, J., Björklund, A., Sundler, F., Hakånson, R., Schaffalitzky de Muckadell, O. B.: Regional distribution of VIP in the rat brain: A histochemical and radioimmunoassay study. Neurosci., submitted

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J.: Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951)

    Google Scholar 

  • McGeer, E. G., Innanen, V. T., McGeer, P. L.: Evidence on the cellular localization of adenyl cyclase in the neostriatum. Brain Res. 118, 356–358 (1976)

    Google Scholar 

  • Minneman, K. P., Quik, M., Emson, P. C.: Receptor-linked cyclic AMP systems in rat neostriatum: differential localization revealed by kainic acid injection. Brain Res. 151, 507–521 (1978)

    Google Scholar 

  • Nadler, J. V., Perry, B. W., Cotman, C. W.: Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 271, 676–677 (1978)

    Google Scholar 

  • Paxinos, G., Bindra, D.: Hypothalamic mid brain neural pathways involved in eating, drinking, irritability, aggression and copulation in rats. J. Comp. Physiol. Psychol. 82, 1–14 (1973)

    Google Scholar 

  • Pellegrino, L. J., Cushman, A. J.: A stereotaxic atlas of the brain. New York: Appleton Century Crofts 1967

    Google Scholar 

  • Phillis, J. W., Kirkpatrick, J. R., Said, S. I.: Vasoactive intestinal polypeptide excitation of central neurons. Can. J. Physiol. Pharmacol. 56, 337–340 (1978)

    Google Scholar 

  • Quik, M., Iversen, L. L., Bloom, S. R.: Effect of vasoactive intestinal peptide (VIP) and other peptides on cAMP accumulation in rat brain. Biochem. Pharmacol. 27, 2209–2213

  • Robberecht, P., Conlon, T. P., Gardner, J. D.: Interaction of porcine vasoactive intestinal peptide with dispersed pancreatic acinan cells from the guinea pig. J. Biol. Chem. 251, 4635–4639 (1976)

    Google Scholar 

  • Said, S. I., Mutt, V.: Polypeptide with broad biological activity: isolation from small intestine. Science 169, 1217–1218 (1970)

    Google Scholar 

  • Said, S. I., Mutt, V.: Isolation from porcine intestinal wall of a vasoactive octacosapeptide related to secretin and to glucagon. Eur. J. Biochem. 28, 199–204 (1972)

    Google Scholar 

  • Said, S. I., Rosenberg, R. N.: Vasoactive intestinal polypeptide: Abundant immunoreactivity in neural cell lines and normal nervous tissue. Science 192, 907–908 (1976)

    Google Scholar 

  • Schwarcz, R., Coyle, J. T.: Striatal lesions with kainic acid: neurochemical characteristics. Brain Res. 127, 235–249 (1977)

    Google Scholar 

  • Schwarcz, R., Creese, I., Coyle, J. T., Snyder, S. H.: Dopamine receptors localised on cerebral cortical afferents to rat corpus striatum. Nature 271, 766–768 (1978)

    Google Scholar 

  • Storm-Mathisen, J.: Localization of transmitter candidates in the brain: the hippocampal formation as a model. Progr. Neurobiol. 8, 119–181 (1977)

    Google Scholar 

  • Thompson, W. J., Appleman, M. M.: Multiple cyclic nucleotide phosphodiesterase activities from rat brain. Biochemistry 10, 311–316 (1971)

    Google Scholar 

  • Tranzer, J. P., Thoenen, H.: An electron microscopic study of selective acute degeneration of sympathetic nerve terminals after administration of 6-hydroxydopamine. Experientia 24, 155–156 (1968)

    Google Scholar 

  • Walaas, I., Fonnum, F.: The effect of parenteral glutamate treatment on the localization of neurotransmitters in the mediobasal hypothalamus. Brain Res. 153, 549–562 (1978)

    Google Scholar 

  • Wuerthele, S. M., Lovell, K. L., Jones, M. Z., Moore, K. E.: A histological study of kainic acid induced lesions in the rat brain. Brain Res. 149, 489–497 (1978)

    Google Scholar 

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Quik, M., Emson, P.C., Fahrenkrug, J. et al. Effect of kainic acid injections and other brain lesions on vasoactive intestinal peptide (VIP)-stimulated formation of cAMP in rat brain. Naunyn-Schmiedeberg's Arch. Pharmacol. 306, 281–286 (1979). https://doi.org/10.1007/BF00507115

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