Abstract
Glutamate, the major excitatory neurotransmitter in the central nervous system, activates at least three types of channel-forming receptors defined by the selective agonists N-methyl-D-aspartate (NMDA), kainate, and quisqualate [or more selectively by alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)]. Activation of the NMDA receptor requires glycine as well as NMDA or glutamate. Recent studies have provided evidence that certain polyamines potentiate the binding by NMDA receptors of glycine and the open channel blocker MK-801. To determine whether polyamines alter channel opening, we examined their effects on rat brain glutamate receptors expressed in Xenopus oocytes. Our results demonstrate that spermine potentiates the response of the NMDA receptor but has no effect on responses to kainate and quisqualate. Furthermore, spermine increases the maximum response to NMDA and glycine and acts, at least in part, by increasing the apparent affinity of the NMDA receptor/channel complex for glycine. The present findings and the fact that polyamines are a natural constituent of brain suggest that polyamines may play a role in the regulation of glutamatergic transmission.
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- Benveniste M., Clements J., Vyklický L., Jr, Mayer M. L. A kinetic analysis of the modulation of N-methyl-D-aspartic acid receptors by glycine in mouse cultured hippocampal neurones. J Physiol. 1990 Sep;428:333–357. doi: 10.1113/jphysiol.1990.sp018215. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brackley P., Goodnow R., Jr, Nakanishi K., Sudan H. L., Usherwood P. N. Spermine and philanthotoxin potentiate excitatory amino acid responses of Xenopus oocytes injected with rat and chick brain RNA. Neurosci Lett. 1990 Jun 22;114(1):51–56. doi: 10.1016/0304-3940(90)90427-b. [DOI] [PubMed] [Google Scholar]
- Brewer G. J., Cotman C. W. NMDA receptor regulation of neuronal morphology in cultured hippocampal neurons. Neurosci Lett. 1989 May 8;99(3):268–273. doi: 10.1016/0304-3940(89)90458-8. [DOI] [PubMed] [Google Scholar]
- Christine C. W., Choi D. W. Effect of zinc on NMDA receptor-mediated channel currents in cortical neurons. J Neurosci. 1990 Jan;10(1):108–116. doi: 10.1523/JNEUROSCI.10-01-00108.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cline H. T., Debski E. A., Constantine-Paton M. N-methyl-D-aspartate receptor antagonist desegregates eye-specific stripes. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4342–4345. doi: 10.1073/pnas.84.12.4342. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collingridge G. L., Kehl S. J., McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol. 1983 Jan;334:33–46. doi: 10.1113/jphysiol.1983.sp014478. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dingledine R., Hynes M. A., King G. L. Involvement of N-methyl-D-aspartate receptors in epileptiform bursting in the rat hippocampal slice. J Physiol. 1986 Nov;380:175–189. doi: 10.1113/jphysiol.1986.sp016279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
- Forsythe I. D., Westbrook G. L. Slow excitatory postsynaptic currents mediated by N-methyl-D-aspartate receptors on cultured mouse central neurones. J Physiol. 1988 Feb;396:515–533. doi: 10.1113/jphysiol.1988.sp016975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gustafsson B., Wigström H. Physiological mechanisms underlying long-term potentiation. Trends Neurosci. 1988 Apr;11(4):156–162. doi: 10.1016/0166-2236(88)90142-7. [DOI] [PubMed] [Google Scholar]
- Harris E. W., Ganong A. H., Cotman C. W. Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res. 1984 Dec 3;323(1):132–137. doi: 10.1016/0006-8993(84)90275-0. [DOI] [PubMed] [Google Scholar]
- Hayashi Y., Hattori Y., Moriwaki A., Saeki K., Hori Y. Changes in polyamine concentrations in amygdaloid-kindled rats. J Neurochem. 1989 Sep;53(3):986–988. doi: 10.1111/j.1471-4159.1989.tb11805.x. [DOI] [PubMed] [Google Scholar]
- Heby O., Persson L. Molecular genetics of polyamine synthesis in eukaryotic cells. Trends Biochem Sci. 1990 Apr;15(4):153–158. doi: 10.1016/0968-0004(90)90216-x. [DOI] [PubMed] [Google Scholar]
- Hestrin S., Nicoll R. A., Perkel D. J., Sah P. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol. 1990 Mar;422:203–225. doi: 10.1113/jphysiol.1990.sp017980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson J. W., Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature. 1987 Feb 5;325(6104):529–531. doi: 10.1038/325529a0. [DOI] [PubMed] [Google Scholar]
- Kleckner N. W., Dingledine R. Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science. 1988 Aug 12;241(4867):835–837. doi: 10.1126/science.2841759. [DOI] [PubMed] [Google Scholar]
- Kleinschmidt A., Bear M. F., Singer W. Blockade of "NMDA" receptors disrupts experience-dependent plasticity of kitten striate cortex. Science. 1987 Oct 16;238(4825):355–358. doi: 10.1126/science.2443978. [DOI] [PubMed] [Google Scholar]
- Kremzner L. T. Metabolism of polyamines in the nervous system. Fed Proc. 1970 Jul-Aug;29(4):1583–1588. [PubMed] [Google Scholar]
- Kushner L., Lerma J., Zukin R. S., Bennett M. V. Coexpression of N-methyl-D-aspartate and phencyclidine receptors in Xenopus oocytes injected with rat brain mRNA. Proc Natl Acad Sci U S A. 1988 May;85(9):3250–3254. doi: 10.1073/pnas.85.9.3250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lerma J., Kushner L., Spray D. C., Bennett M. V., Zukin R. S. mRNA from NCB-20 cells encodes the N-methyl-D-aspartate/phencyclidine receptor: a Xenopus oocyte expression study. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1708–1711. doi: 10.1073/pnas.86.5.1708. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lerma J., Kushner L., Zukin R. S., Bennett M. V. N-methyl-D-aspartate activates different channels than do kainate and quisqualate. Proc Natl Acad Sci U S A. 1989 Mar;86(6):2083–2087. doi: 10.1073/pnas.86.6.2083. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lerma J., Zukin R. S., Bennett M. V. Glycine decreases desensitization of N-methyl-D-aspartate (NMDA) receptors expressed in Xenopus oocytes and is required for NMDA responses. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2354–2358. doi: 10.1073/pnas.87.6.2354. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lester R. A., Clements J. D., Westbrook G. L., Jahr C. E. Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature. 1990 Aug 9;346(6284):565–567. doi: 10.1038/346565a0. [DOI] [PubMed] [Google Scholar]
- Mayer M. L., Westbrook G. L., Guthrie P. B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature. 1984 May 17;309(5965):261–263. doi: 10.1038/309261a0. [DOI] [PubMed] [Google Scholar]
- Morris R. G., Anderson E., Lynch G. S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. 1986 Feb 27-Mar 5Nature. 319(6056):774–776. doi: 10.1038/319774a0. [DOI] [PubMed] [Google Scholar]
- Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 1984 Feb 2;307(5950):462–465. doi: 10.1038/307462a0. [DOI] [PubMed] [Google Scholar]
- Pegg A. E. Polyamine metabolism and its importance in neoplastic growth and a target for chemotherapy. Cancer Res. 1988 Feb 15;48(4):759–774. [PubMed] [Google Scholar]
- Peters S., Koh J., Choi D. W. Zinc selectively blocks the action of N-methyl-D-aspartate on cortical neurons. Science. 1987 May 1;236(4801):589–593. doi: 10.1126/science.2883728. [DOI] [PubMed] [Google Scholar]
- Ransom R. W., Deschenes N. L. Polyamines regulate glycine interaction with the N-methyl-D-aspartate receptor. Synapse. 1990;5(4):294–298. doi: 10.1002/syn.890050406. [DOI] [PubMed] [Google Scholar]
- Ransom R. W., Stec N. L. Cooperative modulation of [3H]MK-801 binding to the N-methyl-D-aspartate receptor-ion channel complex by L-glutamate, glycine, and polyamines. J Neurochem. 1988 Sep;51(3):830–836. doi: 10.1111/j.1471-4159.1988.tb01818.x. [DOI] [PubMed] [Google Scholar]
- Rauschecker J. P., Hahn S. Ketamine-xylazine anaesthesia blocks consolidation of ocular dominance changes in kitten visual cortex. Nature. 1987 Mar 12;326(6109):183–185. doi: 10.1038/326183a0. [DOI] [PubMed] [Google Scholar]
- SHIMIZU H., KAKIMOTO Y., SANO I. THE DETERMINATION AND DISTRIBUTION OF POLYAMINES IN MAMMALIAN NERVOUS SYSTEM. J Pharmacol Exp Ther. 1964 Feb;143:199–204. [PubMed] [Google Scholar]
- Sacaan A. I., Johnson K. M. Spermine enhances binding to the glycine site associated with the N-methyl-D-aspartate receptor complex. Mol Pharmacol. 1989 Dec;36(6):836–839. [PubMed] [Google Scholar]
- Schwarcz R., Whetsell W. O., Jr, Mangano R. M. Quinolinic acid: an endogenous metabolite that produces axon-sparing lesions in rat brain. Science. 1983 Jan 21;219(4582):316–318. doi: 10.1126/science.6849138. [DOI] [PubMed] [Google Scholar]
- Shaw G. G., Pateman A. J. The regional distribution of the polyamines spermidine and spermine in brain. J Neurochem. 1973 Apr;20(4):1225–1230. doi: 10.1111/j.1471-4159.1973.tb00091.x. [DOI] [PubMed] [Google Scholar]
- Shaw G. G. The polyamines in the central nervous system. Biochem Pharmacol. 1979;28(1):1–6. doi: 10.1016/0006-2952(79)90261-2. [DOI] [PubMed] [Google Scholar]
- Simon R. P., Swan J. H., Griffiths T., Meldrum B. S. Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain. Science. 1984 Nov 16;226(4676):850–852. doi: 10.1126/science.6093256. [DOI] [PubMed] [Google Scholar]
- Snutch T. P. The use of Xenopus oocytes to probe synaptic communication. Trends Neurosci. 1988 Jun;11(6):250–256. doi: 10.1016/0166-2236(88)90102-6. [DOI] [PubMed] [Google Scholar]
- Ullrich A., Shine J., Chirgwin J., Pictet R., Tischer E., Rutter W. J., Goodman H. M. Rat insulin genes: construction of plasmids containing the coding sequences. Science. 1977 Jun 17;196(4296):1313–1319. doi: 10.1126/science.325648. [DOI] [PubMed] [Google Scholar]
- Westbrook G. L., Mayer M. L. Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature. 1987 Aug 13;328(6131):640–643. doi: 10.1038/328640a0. [DOI] [PubMed] [Google Scholar]
- Wieloch T. Hypoglycemia-induced neuronal damage prevented by an N-methyl-D-aspartate antagonist. Science. 1985 Nov 8;230(4726):681–683. doi: 10.1126/science.2996146. [DOI] [PubMed] [Google Scholar]
- Williams K., Dawson V. L., Romano C., Dichter M. A., Molinoff P. B. Characterization of polyamines having agonist, antagonist, and inverse agonist effects at the polyamine recognition site of the NMDA receptor. Neuron. 1990 Aug;5(2):199–208. doi: 10.1016/0896-6273(90)90309-4. [DOI] [PubMed] [Google Scholar]
- Williams K., Romano C., Molinoff P. B. Effects of polyamines on the binding of [3H]MK-801 to the N-methyl-D-aspartate receptor: pharmacological evidence for the existence of a polyamine recognition site. Mol Pharmacol. 1989 Oct;36(4):575–581. [PubMed] [Google Scholar]
- Young A. B., Greenamyre J. T., Hollingsworth Z., Albin R., D'Amato C., Shoulson I., Penney J. B. NMDA receptor losses in putamen from patients with Huntington's disease. Science. 1988 Aug 19;241(4868):981–983. doi: 10.1126/science.2841762. [DOI] [PubMed] [Google Scholar]
- Zawia N. H., Bondy S. C. Electrically stimulated rapid gene expression in the brain: ornithine decarboxylase and c-fos. Brain Res Mol Brain Res. 1990 Apr;7(3):243–247. doi: 10.1016/0169-328x(90)90034-b. [DOI] [PubMed] [Google Scholar]