FOOD INTAKE TAEES FACILIATES BRAIN PLASTICITY

Open Access Open Access
Restricted Access Subscription Access

Abstract


To define how extracellular glucose levels affect synaptic efficacy and long-term potentiation (LTP), we evaluated electrophysiological and neurochemical properties in hippocampal CA1 region following alterations in glucose levels in the ACSF with 3,5 mM glucose, fEPSPsgenerated by Schaffer collateral/commissural stimulation markedlyincreased when ACSF glucose levels were increased from 3,5 to 7,0 mM. The paired-pulse facilitation reflecting presynaptic transmitter release efficacy was significantly suppressed by elevation of 7,0 mM glucose indicating the increase of the presynaptic transmitter release. Single pulse stimulation of presynaptic terminals also shows the increase of fEPSP amplitudes. Prolonged potentiation of fEPSPs by elevation of 7 mM glucose coincided with increased autophosphorylation both Ca ions / calmodulin dependent protein kinase II(CaMKII) and protein kinase C (PKC a). The increased I/O relationship of fEPSPs was also associated with markedly increased synapsin Iphosphorylation by CaMKII. Transmitter-evoked postsynaptic currents were also measured in CA1 neurons by electrophoretic application of NMDA anAMPA by elevation to 7,0 mM. Notably high frequency stimulation of the Schaffer collateral/commissural pathway failed to induce LTP in the CA1region at 3,5 mM glucose but LTP was restored dose dependently by increasing glucose levels to 7,0 mM and l0mM. LTP induction in the presence of 7,0 mM glucose was closely associated with further increase in CaMKII autophosphorylation without changes in PKC a autophsphorylation. Taken together, CaMKII and PKC activation likely mediate potentiation of fEPSPsby elevated glucose levels, and CaMKII activity is also associated with LTP Induction in the hippocampal CAl region.

Yutaka Oomura

Kyushu University Fukuoka

Email: y_oomura25@hotmail.com
Fukuoka, Japan professor, Department of Integrated Physiology Faculty of Medicine

  1. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiationin the hippocampus // Nature. - 1993. - Vol. 361. - P. 31-39.
  2. Danysz W., Zajaczkowski W., Parsons C.G. Modulation of learning processes by ionotropic glutamate receptor ligands // Behav. Pharmacol. - 1995. - Vol. 6. - P. 455-474.
  3. Malenka R.C. Synaptic plasticity in the hippocampus: LTP and LTD // Cell. - 1994. - Vol. 78. - P. 535-538.
  4. 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. - Vol. 323. - P. 132-137.
  5. Fukunaga K., Goto S., Miyamoto E. Immnohistochemical localization of Ca+/calmodulin-dependent protein kinase II in rat brain and various tissues // J. Neurochem. - 1988. - Vol. 51. - P. 1070-1078.
  6. Fukunaga K., Sodering T.R., Miyamoto E. Activation of Ca+/calmodulin-dependent protein kinase If and protein kinase C by glutamate in cultured rathippocampal neurons // J. Biol. Chem. - 1992. - Vol. 267. - P. 22527-22533.
  7. Fukunaga K., Stoppini L., Miyamoto E., Muller D. Long-term potentiation isassociated with a increased activity of Cacalmodulin-dependent protein kinase II // J. Biol. Chem. - 1993. - Vol. 268. - P. 7863-7867.
  8. Fukunaga K., Muller D., Miyamoto E. Increased phosphorylation of Ca / calmodulin-dependent protein kinase II and its endogeneous substrates in the induction of long term potentiation // J. Biol. Chem. - 1995. - Vol. 270. - P. 6119-6124.
  9. Hudman A., Schulman H. Neuronal Ca2+ / calmodulin-dependent protein kinaseII: the role of structure and autoregulation in cellular function // Ann. Rev. Biochem. - 2002. - Vol. 71. - P. 473-510.
  10. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function insynaptic and behavioral memory // Nat. Rev. Neurosci. - 2002. - Vol. 3. - P. 175-190.
  11. Lledo P. M., Hjelmstad G.O., Mukhherji S., Sodering T.R., Malenka R.C., Nicoll R.A. Calcium / calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism // Proc. Natl Acad. Sci. USA. - 1995. - Vol. 92. - P. 11176-11179.
  12. Wing J.H., Kelly P.T. Postsynaptic injection of Ca2+/CaM induces synapticpotentiation requiring CaMKII and PKC activitv // Neuron. - 1995. - Vol. 15. - P. 443-452.
  13. Bariа A., Muller D., Derkach V., Griffith L.C., Sodring T.R. Regulatory phosphorylation of AMPA-type glutamate receptor by CaM-KII during long-term potentiation // Science. - 1997. - Vol. 276. - P. 2042-2045.
  14. Giese R.V., Fedorov N.B., Filipkowski R.K., Silva A.J. Autophosphoiylation atThr286 o the alpha calcium/calmodulin kinase II in LTP and learning // Science. - 1998. - Vol. 279. - P. 370-873.
  15. McGlade-McCullon E., Yamamoto H., Tan S.E., Brickey D.A., Sodering T.R. Phosphorulation and regulation of glutamate receptors by calcium/calmodulin dependent protein kinase II // Nature. - 1993. - Vol. 362. - P. 640-642.
  16. Shi S.H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation // Science. - 1999. - Vol. 284. - P. 1811-1826.
  17. Poncer J. C., Esteban J. A., Malinow R. Multiple mechanism for the potentiation of AMPA receptor-mediated transmission by alpha-Ca2+/calmod-ulin dependent protein kinase II // J. Neurosci. - Vol. 22. - P. 4406-4411.
  18. Song I., Huganir R.L. Regulation of AMPA receptor during synaptic plasticity // Trends Neurosci. - 2002. - Vol. 25. - P. 578-588.
  19. Collingridge G.L., Isaac J.T., Wang Y.T. Receptor trafficking and synaptic plasticity // Nat. Rev. Neurosci. - 2004. - Vol. 5. - P. 952-962.
  20. Tingley W.G., Rocke K.W., Thompson A.K., Huganir R.L. Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain // Nature. - 1993. - Vol. 364. - P. - 70-73.
  21. Tingley W.G., Ehlers M.D., Kameyama K., Doherty C., Ptak J.B., Riley C. T., Huganir R.L. Characterization of protein kinase A and protein kinase Сphosphorylation of the N-methyl-D aspartate receptor NR1 subunit using phosphorylation site-SDecific antibodies // J. Biol. Chem. - 1997. - Vol. 272. - P. 5157-5166.
  22. Manabe T., Wyllie D.J., Perlcel D.J., Nicoll R.A. Modulation of synaptic transmissionand long-term potentiation: effects on paired-pulse facilitation and EPSC variance in the CA1 region of the hippocampus // J. Neurophysiol. - 1993. - Vol. 70. - P. 1451-1459.
  23. Manabe T., Noda Y., Mamiya T., Katagiri H., Houtani T., Nishi М., Noda T., Takahashi T., Sugimoto T., Nabeshima T., Takeshima H. Facilitation of long-term potentiation and memory in mice lacking nociceptin receptors // Nature. - 1998. - Vol. 394. - P. 577-581.
  24. Sieber F.E., Traystman R.J., Brown P.R., Martin L.J. Protein kinase Сexpressionand activity after global incomplete cerebral ischemia in dogs // Stroke. - 1998. - Vol. 29. - P. 1445-1452.
  25. Frey U., Huang Y.Y., Kandel E.R. Effects of camp stimulate a late stage of LTP in hippocampal CA1 neurons. Science. - 1993. - Vol. 260. - P. 1661-1664.
  26. Gold P.E. Glucose modulation of memory storage processing // Behav. Neural. Biol. - 1986. - Vol. 45. - P. 342-349.
  27. Messier C., Write N.M. Memory impairment by glucose, fructose, and two glucose analogs: a possible effect on peripheral glucose transport // Behav. Neural. Biol. - 1987. - Vol. 48. - P. 104-127.
  28. Hall J.L., Gonder-Frederick L.A., Chewning W.W., Silveira J., Gold P.E. Glucose enhancement of performance on memory tests: youn and aged humans // Neuropsychologia. - 1989. - Vol. 27. - P. 1129-1138.
  29. Manning C.A., Ragozzino M.E., Gold P. E. Glucose enhancement of memory in patients with Alzheimer’s disease // Neurobiol. Aging. - 1993. - Vol. 14. - P. 523-528.
  30. Abi-saab W.M., Maggs D.G., Jones T., Jacob R., Srihara V., Thompson J., Kerr D., Leone P., Krystal J.H., Spencer D.D., During M.J., Sherwin R.S. Striking differences in glucose and lactate levels between brain extracellular fluid and plasma in conscious human subjects: effects of hyperglycemia and hypoglycemia // J. Cereb. Blood Flow Metab. - 2002. - Vol. 22. - P. 271-279.
  31. Jacob R.J., Fan X., Evans M.L., Dziura J., Shewin R.S. Brain glucose levels are elevated in chronically hyperglycemic diabetic rats: no evidence for protective adaptation by the blood brain barrier // Metabolism. - 2002. - Vol. 51. - P. 1522-1524.
  32. McNay E.C., Fries T.M., Gold P.E. Decreases in rat extracellular hippocampalglucose concentration associated with cognitive demand during spatial task // Proc. Natl Acad. Sci. USA. - 2000. - Vol. 97. - P. 2881-2885.
  33. Yamagata Y. New aspects of neurotransmitter release and exocytosis: dynamic and differential regulation of synapsin I phosphorylation by acute neuronal excitation in vivo // J. Pharmacol. Sci. - 2003. - Vol. 93. - P. 22-29.
  34. Kamal A., Spoelstra K., Biessels G.J., Urban I.J., Gispen W.H. Effects of changes inglucose concentration on synaptic plasticity in hippocampal slices // Brain Res. - 1999. - Vol.84. - P. 238-242.
  35. Derkach V., Barria A., Sodering T.R. Ca2+/calmodulin-kinase II enhanceschannel conductance of alpha-amino-3-hydroxy-5-methyI-4-isoxa-zolepropionate type glutamate receptors // Proc. Natl Acad. Sci. USA. - 1999. - Vol. 96. - P. 3269-3274.
  36. Mulkey R.M., Malenka R.C. Mechanisms underlying induction of homosynapticlong-term depression in are CA1 ofthe hippocampus // Neuron. - 1992. - Vol. 9. - P. 967-975.
  37. Edwards S., Simmons D.L., Galmdo D.G., Doherty J.M., Scott A.M., Hugnes P.H., Wilcox R.E. Antagonistic effects of dopaminergic signaling and hanol on protein kinase A-mediated phosphorylation of DARPP-32 and the NR1 subunit of the NMDA receptors // Alcohol. Clin. Exp. Res. - 2002. - Vol. 26. - P. 173-180.

Views

Abstract - 17

PDF (Russian) - 0

PlumX

Refbacks

  • There are currently no refbacks.

Copyright (c) 2015 Oomura Y.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.