Skip to main content
Log in

How peptidergic neurons cope with variation in physiological stimulation

  • Original Articles
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

A general scheme for neuropeptide metabolism is outlined and the potential sites of regulation are discussed. Two major sites of regulation are distinguished: transcription which ultimately limits the rate of translation to form the prepropeptide, and post-translational processing steps. The consequences of up-regulation of these steps in response to increased metabolic demand are discussed. An alternative strategy for peptidergic neurons, reliance on a large pool of neuropeptide, is proposed. Data on the response of enkephalin-containing cell to increased levels of stimulation are reviewed. It is concluded that there is good evidence for genomic up-regulation, perhaps in association with regulation of processing. Evidence based on studies on enkephalin-containing amacrine cells in the chicken retina is also reviewed. It is suggested that these cells rely on a large pool of neuropeptide to cope with changes in demand.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Hökfelt, T., Johansson, O., Ljungdahl, Å., Lundberg, J. M. and Schultzberg, M. 1990. Peptidergic neurones. Nature 285:514–521.

    Google Scholar 

  2. McKelvy, J. F., and Blumberg, S. 1986. Inactivation and metabolism of neuropeptides. Ann. Rev. Neurosci. 9:415–434.

    Google Scholar 

  3. Bartfai, T., Iverfeldt, K., Fisone, G., and Serfözö, P. 1988. Regulation of the release of coexisting transmitters. Ann. Rev. Pharmacol. Toxicol. 28:285–310.

    Google Scholar 

  4. Kow, L.-M., and Pfaff, D. W. 1988. Modulatory actions of peptides. Ann. Rev. Pharmacol. Toxicol. 28:163–188.

    Google Scholar 

  5. Turner, A. J. 1986. Processing and metabolism of neuropeptides. Essays in Biochemistry 22:69–121.

    Google Scholar 

  6. Zigmond, R. E., Schwarzschild, M. A., and Rittenhouse, A. R. 1989. Acute regulation of tyrosine hydroxylase by nerve activity and by neurotransmitters via phosphorylation. Ann. Rev. Neurosci. 12:415–461.

    Google Scholar 

  7. Abraham, D., Pisan, J. J., and Udenfriend, S. J. 1964. Uptake of carnosine and homocamosine by rat brain slices. Arch. Biochem. Biophys. 104:160–165.

    Google Scholar 

  8. Nakata, Y., Kusaka, Y., Yajima, H., and Segawa, T. 1981. Active uptake of substance P carboxyterminal heptapeptide (5–11) into rat brain and rabbit spinal cord slices. J. Neurochem. 37:1529–1534.

    Google Scholar 

  9. Pachero, M. F., Woodward, D. J., McKelvy, J. F., and Griffin, W. S. T. 1981. TRH in the rat cerebellum: II. Uptake by cerebellar slices. Peptides 2:283–288.

    Google Scholar 

  10. Roy, B. P., Jamal, I., and Go, J. 1982. Synaptic mechanism of methionine-enkephalin uptake. Life Sci. 31:2307–2310.

    Google Scholar 

  11. Takeda, M., Takeda, F., Matsumoto, F., Tanaka, R., and Konno, K. 1982. Divalent cation, ATP-dependent [3H] Leu-enkephalin uptake by synaptic vesicle fraction isolated from bovine caudate nucleus. Brain Res. 234:319–329.

    Google Scholar 

  12. Day, N. C., Wien, D., and Michaelson, D. M. 1985. Saturable [D-Ala2, D-Leu5]enkephalin transport into cholinergic synaptic vesicles. FEBS Lett. 166:183–188.

    Google Scholar 

  13. Takeda, F., Takeda, M., Shimada, A., and Konno, K. 1985. ATP-dependent [3H] Met-enkephalin uptake by bovine adrenal chomaffin granule membranes. Brain Res. 344:220–226.

    Google Scholar 

  14. Michaelson, D. M., and Wien-Naor, D. 1987. Enkephalin uptake into cholinergic synaptic vesicles and nerve terminals. Ann. N. Y. Acad. Sci. 493:234–251.

    Google Scholar 

  15. Lundberg, J. M., Anggård, Ä., Fahrenkrug, J., Lundgren, G., and Holmstedt, B. 1982. Corelease of VIP and acetylcholine in relation to blood flow and salivary secretion in cat submandibular salivary gland. Acta Physiol. Scand. 115:525–528.

    Google Scholar 

  16. Lundberg, J. M., Rudehill, A., Sollevi, A., Theordorsson-Norheim, E., and Hamberger, B. 1986. Frequency- and reserpinedependent chemical coding of sympathetic transmission: differential release of noradrenaline and neuropeptide Y from pig spleen. Neurosci. Letters 63:96–100.

    Google Scholar 

  17. Goodman, R. H. 1990. Regulation of neuropeptide gene expression. Ann. Rev. Neurosci. 13:111–127.

    Google Scholar 

  18. Mains, R. E., Cullen, E. I., May, V., and Eipper B. A. 1987. The role of secretory granules in peptide biosynthesis. Ann. N.Y. Acad. Sci. 493:278–291.

    Google Scholar 

  19. Eiden, L. E. 1987. The enkephalin-containing cell: Strategies for polypeptide synthesis and secretion throughout the neuroendocrine system. Cell Mol. Neurobiol. 7:339–352.

    Google Scholar 

  20. Viveros, O. H., Diliberto, E. J., Hong, J.-H., Kizer, J. S., Unsworth, C. D., and Kanamatsu, T. 1987. The regulation of enkephalin levels in adrenomedullary cells and its relation to chromaffin vesicle biogenesis and functional plasticity. Ann. N.Y. Acad. Sci. 493:324–341.

    Google Scholar 

  21. Waschek, J. A., Pruss, R. M., Siegel, R. E., Eiden, L. E., Bader, M.-F., and Aunis, D. 1987. Regulation of enkephalin, VIP, and chromogranin biosynthesis in actively secreting chromaffin cells. Ann. N.Y. Acad. Sci. 493:308–323.

    Google Scholar 

  22. Hook, V. Y. H., Eiden, L. E., and Pruss, R. M. 1985. Selective regulation of carboxypeptidase peptide hormone-processing enzyme during enkephalin biosynthesis in cultured bovine adrenomedullary chromaffin cells. J. Biol. Chem. 260:5991–5997.

    Google Scholar 

  23. Udenfriend, S., and Kilpatrick, D. L. 1983. Biochemistry of the enkephalins and enkephalin-containing peptides. Arch. Biochem. Biophys. 221:309–323.

    Google Scholar 

  24. Liston, D., Patey, G., Rossier, J., Verbanck, P., and Vanderhaeghan, J.-J. 1984. Processing of proenkephalin is tissue-specific. Science 225:734–737.

    Google Scholar 

  25. Hong, J.-S., Wood, P. L., Gillin, J. C., Yang, H. Y. T., and Costa, E. 1980. Changes of hippocampal met-enkephalin content after recurrent motor seizures. Nature 285:231–232.

    Google Scholar 

  26. Kanamatsu, T., Obie, J., Grimes, L., McGinty, J. F., Yoshikawa, K., Sabol, S., and Hong, J.-S. 1986. Kainic acid alters the metabolism of 5-methionine enkephalin and the level of dynorphin A in the rat hippocampus. J. Neurosci. 6:3094–3102.

    Google Scholar 

  27. Sabol, S. L., Yoshikawa, K., and Hong, J.-S. 1985. Regulation of methionine-enkephalin precursor messenger RNA in rat striatum by haloperidol and lithium. Biochem. Biophys. Res. Commun. 113:391–399.

    Google Scholar 

  28. Sivam, S. P., and Hong, J.-S. 1986. GABAergic regulation of enkephalin in rat striatum: alterations in Met5-enkephalin level, precursor content and preproenkephalin messenger RNA abundance. J. Pharmacol. Exp. Ther. 237:326–331.

    Google Scholar 

  29. Tang, F., Costa, E., and Schwartz, J. P. 1983. Increase of proenkephalin mRNA and enkephalin content of rat striatum after daily injection of haloperidol for 2 to 3 weeks. Proc. Natl. Acad. Sci. USA 80:3841–3844.

    Google Scholar 

  30. White, J. D., Gall, C. M., and McKelvy, J. F. 1987. Enkephalin biosynthesis and enkephalin gene expression are increased in hoppocampal mossy fibers following a unilateral lesion of the hilus. J. Neurosci. 7:753–759.

    Google Scholar 

  31. Yoshikawa, K., Hong, J.-S., and Sabol, S. L. 1985. Electrocovulsive shock increases preproenkephalin messenger RNA abundance in rat hypothalamus. Proc. Natl. Acad. Sci. USA 82:589–593.

    Google Scholar 

  32. Millar, T. J., Salipan, N., Oliver, J. O., Morgan, I. G., and Chubb, I. W. 1984. The concentration of enkephalin-like material in the check is light dependent. Neurosci 13:221–226.

    Google Scholar 

  33. Ishimoto, I., Millar, T., Chubb, I. W., and Morgan, I. G. 1986. Somatostatin-immunoreactive amacrine cells of chicken retina: Retinal mosaic, ultrastructural features and light-driven variations in peptide metabolism. Neurosci. 17:1217–1233.

    Google Scholar 

  34. Kamano, K., Katayama-Kumoi, Y., Kiyama, H., Ishimoto, I., Manabe, R., and Tohyama, H. 1989. Coexistence of enkephalin and somatostatin in the chicken retina. Brain. Res. 489:254–260.

    Google Scholar 

  35. Li, H.-B., Watt, C. B., and Lam, D. M.-K. 1990. Double-label analysis of somatostatin's coexistence with enkephalin and gamma-amino-butyric acid in amacrine cells of the chicken retina. Brain Res. 525:304–309.

    Google Scholar 

  36. Millar, T. J., and Chubb, I. W. 1984. Substance P in the chick retina: Effects of light and dark. Brain Res. 307:303–309.

    Google Scholar 

  37. Boelen, M. K., Dowton, M., and Chubb, I. W. 1989. The release of Leu5-enkephalin-like immunoreactivity from the chicken retina is reduced by light in vitro. Brain Res. 488:43–48.

    Google Scholar 

  38. Dowton, M., Boelen, M. K., Morgan, I. G., and Chubb, I. W. 1990. Light drives the release of both Met5-enkephalin and Met5-enkephalin containing peptides in chicken retina, but not their syntheses. Neurosci. 38:187–193.

    Google Scholar 

  39. Miller, R. F., and Bloomfield, S. A. 1983. Electroanatomy of a unique amacrine cell in the rabbit retina. Proc. Natl. Acad. Sci. USA 80:3069–3073.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Special issue dedicated to Dr. Lawrence Austin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morgan, I.G., Chubb, I.W. How peptidergic neurons cope with variation in physiological stimulation. Neurochem Res 16, 705–714 (1991). https://doi.org/10.1007/BF00965559

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00965559

Key Words

Navigation