Circuit-specific changes in d-serine-dependent activation of the N-methyl-D-aspartate receptor in the aging hippocampus

Age

Volumn 36, Issue 5, 2014, Pages

  Labarriere M ^a   Thomas, F ^a   Dutar, P ^a   Pollegioni, L ^b   Wolosker, H ^c   Billard, J M ^a  

^a CENTRE DE PSYCHIATRIE ET NEUROSCIENCES   (France)

^b UNIVERSITY OF INSUBRIA   (Italy)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Dentate gyrus; Glycine binding site; Learning and memory; LTP; NMDA receptors; Synaptic plasticity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGING; ANIMAL; DENTATE GYRUS; DISEASE MODEL; ELECTROPHYSIOLOGY; FEMALE; HIPPOCAMPUS; MALE; MEMORY; MEMORY DISORDER; METABOLISM; NERVE CELL PLASTICITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; HIPPOCAMPUS; MALE; MEMORY; MEMORY DISORDERS; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84906041078     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-014-9698-0     Document Type: Article

References (63)

1. Anderson WW, Collingridge GL (2001) The LTP Program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events. J Neurosci Methods 108(1):71–83
2. Arima-Yoshida F, Watabe AM, Manabe T (2011) The mechanisms of the strong inhibitory modulation of long-term potentiation in the rat dentate gyrus. Eur J Neurosci 33(9):1637–1646
3. Bai L, Hof PR, Standaret DG, Xing Y, Nelson SE, Young AB, Magnusson KR (2004) Changes in the expression of the NR2B subunit during aging in macaque monkeys. Neurobiol Aging 25(2):201–208
4. Balu DT, Li Y, Puhl MD, Benneyworth MA, Basu AC, Takagi S, Bolshakov VY, Coyle JT (2013) Multiple risk pathways for schizophrenia converge in serine racemase knockout mice, a mouse model of NMDA receptor hypofunction. Proc Natl Acad Sci USA
5. Barnes CA (1994) Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci 17(1):13–18
6. Barnes CA (2003) Long-term potentiation and the ageing brain. Philos Trans R Soc Lond B Biol Sci 358(1432):765–772
7. Barnes CA, McNaughton BL (1980) Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. J Physiol 309:473–485
8. 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(6):1040–1048
9. Barnes CA, Rao G, Foster TC, McNaughton BL (1992) Region-specific age effects on AMPA sensitivity: electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1. Hippocampus 2(4):457–468
10. Barnes CA, Rao G, Houston FP (2000) LTP induction threshold change in old rats at the perforant path—granule cell synapse. Neurobiol Aging 21(5):613–620
11. Barnes CA, Rao G, McNaughton BL (1996) Functional integrity of NMDA-dependent LTP induction mechanisms across the lifespan of F-344 rats. Learn Mem 3(2–3):124–137
12. Barnes CA, Rao G, Shen J (1997) Age-related decrease in the N-methyl-D-aspartate R-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol Aging 18(4):445–452
13. Billard JM (2006) Ageing, hippocampal synaptic activity and magnesium. Magnes Res 19(3):199–215
14. Billard JM (2012) D-amino acids in brain neurotransmission and synaptic plasticity. Amino Acids 43(5):1851–1860
15. Burke SN, Barnes CA (2010) Senescent synapses and hippocampal circuit dynamics. Trends Neurosci 33(3):153–161
16. Burke SN, Ryan L, Barnes CA (2012) Characterizing cognitive aging of recognition memory and related processes in animal models and in humans. Front Aging Neurosci 4:15
17. Clayton DA, Mesches MH, Alvarez E, Bickford PC, Browning MD (2002) A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J Neurosci 22(9):3628–3637
18. Collingridge GL, Bliss TV (1995) Memories of NMDA receptors and LTP. Trends Neurosci 18(2):54–56
19. Diana G, Scotti de Carolis A, Frank C, Domenici MR, Sagratella S (1994) Selective reduction of hippocampal dentate frequency potentiation in aged rats with impaired place learning. Brain Res Bull 35(2):107–111
20. Dieguez D Jr, Barea-Rodriguez EJ (2004) Aging impairs the late phase of long-term potentiation at the medial perforant path-CA3 synapse in awake rats. Synapse 52(1):53–61
21. Fantinato S, Pollegioni L, Pilone MS (2001) Engineering, expression and purification of a His-tagged chimeric D-amino acid oxidase from Rhodotorula gracilis. Enzym Micro Technol 29:407–412
22. Foster TC (2002) Regulation of synaptic plasticity in memory and memory decline with aging. Prog Brain Res 138:283–303
23. Foster TC (2006) Biological markers of age-related memory deficits: treatment of senescent physiology. CNS Drugs 20(2):153–166
24. Foster TC, Barnes CA, Rao G, McNaughton BL (1991) Increase in perforant path quantal size in aged F-344 rats. Neurobiol Aging 12(5):441–448
25. Gazzaley AH, Siegel SJ, Kordower JH, Mufson EJ, Morrison JH (1996) Circuit-specific alterations of N-methyl-D-aspartate receptor subunit 1 in the dentate gyrus of aged monkeys. Proc Natl Acad Sci U S A 93(7):3121–3125
26. Geinisman Y, deToledo-Morrell L, Morrell F, Persina IS, Rossi M (1992) Structural synaptic plasticity associated with the induction of long-term potentiation is preserved in the dentate gyrus of aged rats. Hippocampus 2(4):445–456
27. Griffin R, Nally R, Nolan Y, McCartney Y, Linden J, Lynch MA (2006) The age-related attenuation in long-term potentiation is associated with microglial activation. J Neurochem 99(4):1263–1272
28. Haxaire C, Turpin FR, Potier B, Kervern M, Sinet PM, Barbanel G, Mothet JP, Dutar P, Billard JM (2012) Reversal of age-related oxidative stress prevents hippocampal synaptic plasticity deficits by protecting d-serine-dependent NMDA receptor activation. Aging Cell 11(2):336–344
29. Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463(7278):232–236
30. Izquierdo I (1991) Role of NMDA receptors in memory. Trends Pharmacol Sci 12(4):128–129
31. 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(4):1159–1166
32. Kim SJ, Linden DJ (2007) Ubiquitous plasticity and memory storage. Neuron 56(4):582–592
33. Klann E, Thiels E (1999) Modulation of protein kinases and protein phosphatases by reactive oxygen species: implications for hippocampal synaptic plasticity. Prog Neuropsychopharmacol Biol Psychiatry 23(3):359–376
34. Krause M, Yang Z, Rao G, Houston FP, Barnes CA (2008) Altered dendritic integration in hippocampal granule cells of spatial learning-impaired aged rats. J Neurophysiol 99(6):2769–2778
35. Li Y, Sacchi S, Pollegioni L, Basu AC, Coyle JT, Bolshakov VY (2013) Identity of endogenous NMDAR glycine site agonist in amygdala is determined by synaptic activity level. Nat Commun 4:1760
36. Lisman JE, McIntyre CC (2001) Synaptic plasticity: a molecular memory switch. Curr Biol 11(19):R788–R791
37. Luo L, Craik FI (2008) Aging and memory: a cognitive approach. Can J Psychiatry 53(6):346–353
38. Lynch MA (1998) Analysis of the mechanisms underlying the age-related impairment in long-term potentiation in the rat. Rev Neurosci 9(3):169–201
39. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84(1):87–136
40. Lynch MA (2010) Age-related neuroinflammatory changes negatively impact on neuronal function. Front Aging Neurosci 1:6
41. Magnusson KR, Nelson SE, Young AB (2002) Age-related changes in the protein expression of subunits of the NMDA receptor. Brain Res Mol Brain Res 99(1):40–45
42. Malenka RC, Nicoll RA (1993) NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci 16(12):521–527
43. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711
44. Massaad CA, Washington TM, Pautler RG, Klann E (2009) Overexpression of SOD-2 reduces hippocampal superoxide and prevents memory deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 106(32):13576–13581
45. Matsui T, Sekiguchi M, Hashimoto A, Tomita U, Nishikawa T, Wada K (1995) Functional comparison of D-serine and glycine in rodents: the effects on cloned NMDA receptors and the extracellular concentration. J Neurochem 65(1):454–458
46. Moore CI, Browning MD, Rose GM (1993) Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 344 rats. Hippocampus 3(1):57–66
47. Morrison JH, Gazzaley AH (1996) Age-related alterations of the N-methyl-D-aspartate receptor in the dentate gyrus. Mol Psychiatry 1(5):356–358
48. 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(3):267–274
49. Newton IG, Forbes ME, Linville MC, Pang H, Tucker EW, Riddle DR, Brunso-Bechtold JK (2007) Effects of aging and caloric restriction on dentate gyrus synapses and glutamate receptor subunits. Neurobiol Aging
50. Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y (2004) Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci 24(35):7648–7653
51. Potier B, Poindessous-Jazat F, Dutar P, Billard JM (2000) NMDA receptor activation in the aged rat hippocampus. Exp Gerontol 35(9–10):1185–1199
52. Potier B, Turpin FR, Sinet PM, Rouaud E, Mothet JP, Videau C, Epelbaum J, Dutar P, Billard JM (2010) Contribution of the D-serine-dependent pathway to the cellular mechanisms underlying cognitive aging. Front Aging Neurosci 2:1
53. Priestley T, Laughton P, Myers J, Le Bourdelles B, Kerby J, Whiting PJ (1995) Pharmacological properties of recombinant human N-methyl-D-Aspartate receptors comprising NR1a/NR2A and NR1a/NRB subunit assemblies expressed in permanently transfected mouse fibroblast cells. Mol Pharmacol 48(5):841–848
54. Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69(3):143–179
55. Serrano F, Klann E (2004) Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res Rev 3(4):431–443
56. Shankar S, Teyler TJ, Robbins N (1998) Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J Neurophysiol 79(1):334–341
57. Shleper M, Kartvelishvily E, Wolosker H (2005) D-serine is the dominant endogenous coagonist for NMDA receptor neurotoxicity in organotypic hippocampal slices. J Neurosci 25(41):9413–9417
58. Sierra-Mercado D, Dieguez D Jr, Barea-Rodriguez EJ (2008) Brief novelty exposure facilitates dentate gyrus LTP in aged rats. Hippocampus 18(8):835–843
59. Smith TD, Adams MM, Gallagher M, Morrison JH, Rapp PR (2000) Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J Neurosci 20(17):6587–6593
60. Turpin F, Dallerac G, Mothet JP (2012) Electrophysiological analysis of the modulation of NMDA-receptors function by D-serine and glycine in the central nervous system. Methods Mol Biol 794:299–312
61. Turpin FR, Potier B, Dulong JR, Sinet PM, Alliot J, Oliet SH, Dutar P, Epelbaum J, Mothet JP, Billard JM (2011) Reduced serine racemase expression contributes to age-related deficits in hippocampal cognitive function. Neurobiol Aging 32(8):1495–1504
62. Yang Y, Ge W, Chen Y, Zhang Z, Shen W, Wu C, Poo M, Duan S (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc Natl Acad Sci U S A 100(25):15194–15199
63. Yang Z, Krause M, Rao G, McNaughton BL, Barnes CA (2008) Synaptic commitment: developmentally regulated reciprocal changes in hippocampal granule cell NMDA and AMPA receptors over the lifespan. J Neurophysiol 99(6):2760–2768