Reduction in glutamate uptake is associated with extrasynaptic NMDA and metabotropic glutamate receptor activation at the hippocampal CA1 synapse of aged rats

Aging Cell

Volumn 9, Issue 5, 2010, Pages 722-735

  Potier, Brigitte ^a   Billard, Jean Marie ^a   Rivière, Sylvain ^a   Sinet, Pierre Marie ^a   Denis, Isabelle ^b   Champeil Potokar, Gaelle ^b   Grintal, Barbara ^b   Jouvenceau, Anne ^a   Kollen, Melanie ^a   Dutar, Patrick ^a  

^a CENTRE DE PSYCHIATRIE ET NEUROSCIENCES   (France)

^b INRA   (France)

Author keywords

Aging; Extrasynaptic receptors; GLAST; GLT 1; Glutamate transporters; Hippocampus; MGluRs; Synaptic plasticity; Synaptic transmission

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; GLUTAMATE AMMONIA LIGASE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID;

AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; LONG TERM DEPRESSION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

AGING; ANIMALS; ASPARTIC ACID; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; OXIDATION-REDUCTION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPSES; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION;

ANIMALIA; RATTUS;

EID: 78349291932     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00593.x     Document Type: Article

References (73)

1. Anderson WW, Collingridge GL (2007) Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions. J. Neurosci. Methods 162, 346-356.
2. Banay-Schwartz M, Lajtha A, Palkovits M (1989) Changes with aging in the levels of amino acids in rat CNS structural elements. I. Glutamate and related amino acids. Neurochem. Res. 14, 555-562.
3. Banke TG, Traynelis SF (2003) Activation of NR1/NR2B NMDA receptors. Nat. Neurosci. 6, 144-152.
4. Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93, 74-104.
5. Barnes CA, McNaughton BL (1985) An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses. Behav. Neurosci. 99, 1040-1048.
6. Barnes CA, Rao G, Shen J (1997) Age-related decrease in the N-methyl-D-aspartateR-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol. Aging 18, 445-452.
7. Baude A, Nusser Z, Roberts JDB, Mulvihill E, Jeffrey Mcllhinney RA, Somogyi P (1993) The metabotropic glutamate receptor (mGluRl[alpha]) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771-787.
8. Billard J-M (2010) Long-term depression in the hippocampal CA1 area of aged rats, revisited: contribution of temporal constraints related to slice preparation. PLoS ONE 5, e9843.
9. Billard J-M, Jouvenceau A, Lamour Y, Dutar P (1997) NMDA receptor activation in the aged rat: electrophysiological investigations in the CA1 area of the hippocampal slice ex vivo. Neurobiol. Aging 18, 535-542.
10. Boric K, Munoz P, Gallagher M, Kirkwood A (2008) Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus. J. Neurosci. 28, 8034-8039.
11. Bridges RJ, Kavanaugh MP, Chamberlin AR (1999) A pharmacological review of competitive inhibitors and substrates of high-affinity, sodium-dependent glutamate transport in the central nervous system. Curr. Pharm. Des. 5, 363-379.
12. Burke JP, Hablitz JJ (1994) Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. J. Neurosci. 14, 5120-5130.
13. Cavelier P, Attwell D (2005) Tonic release of glutamate by a DIDS-sensitive mechanism in rat hippocampal slices. J. Physiol. 564, 397-410.
14. Cavelier P, Hamann M, Rossi D, Mobbs P, Attwell D (2005) Tonic excitation and inhibition of neurons: ambient transmitter sources and computational consequences. Prog. Biophys. Mol. Biol. 87, 3-16.
15. Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
16. Clayton DA, Browning MD (2001) Deficits in the expression of the NR2B subunit in the hippocampus of aged Fisher 344 rats. Neurobiol. Aging 22, 165-168.
17. Cotrina ML, Nedergaard M (2002) Astrocytes in the aging brain. J. Neurosci. Res. 67, 1-10.
18. Van Dam EJ, Kamal A, Artola A, De Graan PN, Gispen WH, Ramakers GM (2004) Group I metabotropic glutamate receptors regulate the frequency-response function of hippocampal CA1 synapses for the induction of LTP and LTD. Eur. J. Neurosci. 19, 112-118.
19. Danbolt NC (2001) Glutamate uptake. Prog. Neurobiol. 65, 1-105.
20. Debanne D, Guérineau NC, Gähwiler BH, Thompson SM (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J. Physiol. 491, 163-176.
21. Fonnum F (1984) Glutamate: a neurotransmitter in mammalian brain. J. Neurochem. 42, 1-11.
22. Forsythe ID, Clements JD (1990) Presynaptic glutamate receptors depress excitatory monosynaptic transmission between mouse hippocampal neurones. J. Physiol. 429, 1-16.
23. Greene JG, Greenamyre JT (1996) Bioenergetics and glutamate excitotoxicity. Prog. Neurobiol. 48, 613-634.
24. Grintal B, Champeil-Potokar G, Lavialle M, Vancassel S, Breton S, Denis I (2009) Inhibition of astroglial glutamate transport by polyunsaturated fatty acids: evidence for a signalling role of docosahexaenoic acid. Neurochem. Int. 54, 535-543.
25. Gundersen V, Danbolt NC, Ottersen OP, Storm-Mathisen J (1993) Demonstration of glutamate/aspartate uptake activity in nerve endings by use of antibodies recognizing exogenous d-aspartate. Neuroscience 57, 97-111.
26. Hardingham GE, Bading H, Fukunaga Y, Arnold FJ (2003) The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 26, 81-89.
27. Herman MA, Jahr CE (2007) Extracellular glutamate concentration in hippocampal slice. J. Neurosci. 27, 9736-9741.
28. Jabaudon D, Shimamoto K, Yasuda-Kamatani Y, Scanziani M, Gahwiler BH, Gerber U (1999) Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc. Natl. Acad. Sci. U S A 96, 8733-8738.
29. Jouvenceau A, Dutar P, Billard JM (1998) Alteration of NMDA receptor-mediated synaptic responses in CA1 area of the aged rat hippocampus: contribution of GABAergic and cholinergic deficits. Hippocampus 8, 627-637.
30. Junjaud G, Rouaud E, Turpin F, Mothet JP, Billard JM (2006) Age-related effects of the neuromodulator D-serine on neurotransmission and synaptic potentiation in the CA1 hippocampal area of the rat. J. Neurochem. 98, 1159-1166.
31. Kamal A, Biessels GJ, Gispen WH, Urban IJA (1998) Increasing age reduces expression of long-term depression and dynamic range of transmission plasticity in CA1 field of the rat hippocampus. Neuroscience 83, 707-715.
32. Kollen M, Dutar P, Jouvenceau A (2008) The magnitude of hippocampal long term depression depends on the synaptic location of activated NR2-containing N-methyl-d-aspartate receptors. Neuroscience 154, 1308-1317.
33. Kollen M, Stephan A, Faivre-Bauman A, Loudes C, Sinet PM, Alliot J, Billard JM, Epelbaum J, Dutar P, Jouvenceau A (2010) Preserved memory capacities in aged Lou/C/Jall rats. Neurobiol. Aging 31, 129-142.
34. Kumar A, Foster TC (2005) Intracellular calcium stores contribute to increased susceptibility to LTD induction during aging. Brain Res. 1031, 125-128.
35. Kumar A, Foster TC (2007) Shift in induction mechanisms underlies an age-dependent increase in DHPG-induced synaptic depression at CA3-CA1 synapses. J. Neurophysiol. 98, 2729-2736.
36. Le Meur K, Galante M, Angulo MC, Audinat E (2007) Tonic activation of NMDA receptors by ambient glutamate of non-synaptic origin in the rat hippocampus. J. Physiol. 580, 373-383.
37. Lee HK, Min SS, Gallagher M, Kirkwood A (2005) NMDA receptor-independent long-term depression correlates with successful aging in rats. Nat. Neurosci. 8, 1657-1659.
38. Lujan R, Nusser Z, Roberts JD, Shigemoto R, Somogyi P (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci. 8, 1488-1500.
39. Magnusson KR, Scruggs B, Zhao X, Hammersmark R (2007) Age-related declines in a two-day reference memory task are associated with changes in NMDA receptor subunits in mice. BMC Neurosci. 8, 43.
40. Mothet JP, Rouaud E, Sinet PM, Potier B, Jouvenceau A, Dutar P, Videau C, Epelbaum J, Billard JM (2006) A critical role for the glial-derived neuromodulator D-serine in the age-related deficits of cellular mechanisms of learning and memory. Aging Cell 5, 267-274.
41. Najlerahim A, Francis PT, Bowen DM (1990) Age-related alteration in excitatory amino acid neurotransmission in rat brain. Neurobiol. Aging 11, 155-158.
42. Nickell J, Salvatore MF, Pomerleau F, Apparsundaram S, Gerhardt GA (2007) Reduced plasma membrane surface expression of GLAST mediates decreased glutamate regulation in the aged striatum. Neurobiol. Aging 28, 1737-1748.
43. Norris CM, Korol DL, Foster TC (1996) Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J. Neurosci. 16, 5382-5392.
44. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083-1086.
45. Potier B, Poindessous-Jazat F, Dutar P, Billard JM (2000) NMDA receptor activation in the aged rat hippocampus. Exp. Gerontol. 35, 1185-1199.
46. Price MT, Olney JW, Haft R (1981) Age-related changes in glutamate concentration and synaptosomal glutamate uptake in adult rat striatum. Life Sci. 28, 1365-1370.
47. Renden R, Taschenberger H, Puente N, Rusakov DA, Duvoisin R, Wang L-Y, Lehre KP, Von Gersdorff H (2005) Glutamate transporter studies reveal the pruning of metabotropic glutamate receptors and absence of AMPA receptor desensitization at mature calyx of held synapses. J. Neurosci. 25, 8482-8497.
48. Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol. 69, 143-179.
49. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675-686.
50. Rozovsky I, Finch CE, Morgan TE (1998) Age-related activation of microglia and astrocytes: in vitro studies show persistent phenotypes of aging, increased proliferation, and resistance to down-regulation. Neurobiol. Aging 19, 97-103.
51. Rusakov DA (2001) The role of perisynaptic glial sheaths in glutamate spillover and extracellular Ca(2 +) depletion. Biophys. J. 81, 1947-1959.
52. Rusakov DA, Kullmann DM (1998) Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J. Neurosci. 18, 3158-3170.
53. Saransaari P, Oja SS (1995) Age-related changes in the uptake and release of glutamate and aspartate in the mouse brain. Mech. Ageing Dev. 81, 61-71.
54. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385, 630-634.
55. Schipper HM (1996) Astrocytes, brain aging, and neurodegeneration. Neurobiol. Aging 17, 467-480.
56. Segovia G, Porras A, Del Arco A, Mora F (2001) Glutamatergic neurotransmission in aging: a critical perspective. Mech. Ageing Dev. 122, 1-29.
57. Sheldon AL, Robinson MB (2007) The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem. Int. 51, 333-355.
58. Shi L, Adams MM, Linville MC, Newton IG, Forbes ME, Long AB, Riddle DR, Brunso-Bechtold JK (2007) Caloric restriction eliminates the aging-related decline in NMDA and AMPA receptor subunits in the rat hippocampus and induces homeostasis. Exp. Neurol. 206, 70-79.
59. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, Nakajima T (1998) DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol. Pharmacol. 53, 195-201.
60. Sonntag WE, Bennett SA, Khan AS, Thornton PL, Xu X, Ingram RL, Brunso-Bechtold JK (2000) Age and insulin-like growth factor-1 modulate N-methyl-d-aspartate receptor subtype expression in rats. Brain Res. Bull. 51, 331-338.
61. Strolin Benedetti M, Cini M, Fusi R, Marrari P, Dostert P (1990) The effects of aging on MAO activity and amino acid levels in rat brain. J. Neural Transm. Suppl. 29, 259-268.
62. Syková E, Vargová L (2008) Extrasynaptic transmission and the diffusion parameters of the extracellular space. Neurochem. Int. 52, 5-13.
63. Sykova E, Mazel T, Hasenohrl RU, Harvey AR, Simonova Z, Mulders WH, Huston JP (2002) Learning deficits in aged rats related to decrease in extracellular volume and loss of diffusion anisotropy in hippocampus. Hippocampus 12, 269-279.
64. Turpin FR, Potier B, Dulong JR, Sinet PM, Alliot J, Oliet SHR, Dutar P, Epelbaum J, Mothet JP, Billard JM (2009). Reduced serine racemase expression contributes to age-related deficits in hippocampal cognitive function. Neurobiol. Aging. doi:.
65. Tzingounis AV, Wadiche JI (2007) Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 8, 935-947.
66. Vatassery GT, Lai JC, Smith WE, Quach HT (1998) Aging is associated with a decrease in synaptosomal glutamate uptake and an increase in the susceptibility of synaptosomal vitamin E to oxidative stress. Neurochem. Res. 23, 121-125.
67. Ventura R, Harris KM (1999) Three-Dimensional Relationships between Hippocampal Synapses and Astrocytes. J. Neurosci. 19, 6897-6906.
68. Vignes M, Clarke VRJ, Davies CH, Chambers A, Jane DE, Watkins JC, Collingridge GL (1995) Pharmacological evidence for an involvement of group II and group III mGluRs in the presynaptic regulation of excitatory synaptic responses in the CA1 region of rat hippocampal slices. Neuropharmacology 34, 973-982.
69. Wadiche JI, Jahr CE (2005) Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat. Neurosci. 8, 1329-1334.
70. Wenk GL, Barnes CA (2000) Regional changes in the hippocampal density of AMPA and NMDA receptors across the lifespan of the rat. Brain Res. 885, 1-5.
71. Wheeler DD, Ondo JG (1986) Time course of the aging of the high affinity L-glutamate transporter in rat cortical synaptosomes. Exp. Gerontol. 21, 159-168.
72. Zhang X, Liu H, Wu J, Zhang X, Liu M, Wang Y (2009) Metabonomic alterations in hippocampus, temporal and prefrontal cortex with age in rats. Neurochem. Int. 54, 481-487.
73. Zucker RS (1989) Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13-31.