D-Serine in the aging hippocampus

Journal of Pharmaceutical and Biomedical Analysis

Volumn 116, Issue , 2015, Pages 18-24

  Billard, Jean Marie ^a  

^a CENTRE DE PSYCHIATRIE ET NEUROSCIENCES   (France)

Author keywords

Aging; CA3 CA1 synapses; Dentate gyrus; Memory; NMDA receptors

Indexed keywords

ACETYLCYSTEINE; AMINO ACID; DEXTRO SERINE; GLYCINE; RACEMASE; REACTIVE OXYGEN METABOLITE; SERINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGING; AMNESIA; BINDING SITE; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LOUVAIN RAT; NERVE CELL PLASTICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TISSUE LEVEL; ANIMAL; CHEMISTRY; HUMAN; MEMORY; METABOLISM; PATHOLOGY; PHYSIOLOGY; STEREOISOMERISM;

AGING; ANIMALS; HIPPOCAMPUS; HUMANS; MEMORY; OXIDATIVE STRESS; RECEPTORS, N-METHYL-D-ASPARTATE; SERINE; STEREOISOMERISM;

EID: 84945437450     PISSN: 07317085     EISSN: 1873264X     Source Type: Journal    
DOI: 10.1016/j.jpba.2015.02.013     Document Type: Review

References (88)

1. Burke S.N., Barnes C.A. Senescent synapses and hippocampal circuit dynamics. Trends Neurosci. 2010, 33:153-161.
2. Driscoll I., Hamilton D.A., Petropoulos H., Yeo R.A., Brooks W.M., Baumgartner R.N., Sutherland R.J. The aging hippocampus: cognitive, biochemical and structural findings. Cereb. Cortex 2003, 13:1344-1351.
3. Jolles J. Cognitive, emotional and behavioral dysfunctions in aging and dementia. Prog. Brain Res. 1986, 70:15-39.
4. Billard J.M. Ageing, hippocampal synaptic activity and magnesium. Magnes. Res. 2006, 19:199-215.
5. Barnes C.A. Long-term potentiation and the ageing brain. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2003, 358:765-772.
6. Foster T.C. Biological markers of age-related memory deficits: treatment of senescent physiology. CNS Drugs 2006, 20:153-166.
7. Lynch M.A. Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta?. Prog. Neurobiol. 1998, 56:571-589.
8. Izquierdo I., Medina J.H. Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol. Learn. Mem. 1995, 63:19-32.
9. Kim S.J., Linden D.J. Ubiquitous plasticity and memory storage. Neuron 2007, 56:582-592.
10. Collingridge G.L., Bliss T.V. Memory of NMDA receptors and LTP. Trends Neurosci. 1995, 18:54-56.
11. Gustafsson B., Wigstrom H. Long-term potentiation in the hippocampal CA1 region: its induction and early temporal development. Prog. Brain Res. 1990, 83:223-232.
12. Herron C.E., Lester R.A., Coan E.J., Collingridge G.L. Frequency-dependent involvement of NMDA receptors in the hippocamus: a novel synaptic mechanism. Nature 1986, 322:265-268.
13. Malenka R.C., Nicoll R.A. NMDA receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 1993, 16:521-527.
14. Morris R.G., Davis S., Butcher S.P. Hippocampal synaptic plasticity and NMDA receptors: a role in information storage?. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1990, 329:187-204.
15. Barnes C.A., Rao G., Shen J. Age-related decrease in the N-methyl-d-aspartate R-mediated excitatory postsynaptic potentials in hippocampal region CA1. Neurobiol. Aging 1997, 18:445-452.
16. Clayton D.A., Mesches M.H., Alvarez E., Bickford P.C., Browning M.D. A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer-344 rat. J. Neurosci. 2002, 22:3628-3637.
17. Freret T., Billard J.M., Schumann-Bard P., Dutar P., Dauphin F., Boulouard M., Bouet V. Rescue of cognitive aging by long-lasting environmental enrichment exposure initiated before median lifespan. Neurobiol. Aging 2012, 33:1005.e1-1005.e10.
18. Potier B., Poindessous-Jazat F., Dutar P., Billard J.M. NMDA receptor activation in the aged rat hippocampus. Exp. Gerontol. 2000, 35:1185-1199.
19. Johnson J.W., Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 1987, 325:529-531.
20. Paoletti P. Molecular basis of NMDA receptor functional diversity. Eur. J. Neurosci. 2011, 33:1351-1365.
21. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 2010, 62:405-496.
22. Segovia G., Porras A., Del Arco A., Mora F. Glutamatergic neurotransmission in aging: a critical perspective. Mech. Ageing Dev. 2001, 122:1-29.
23. Basu A.C., Tsai G.E., Ma C.L., Ehmsen J.T., Mustafa A.K., Han L., Jiang Z.I., Benneyworth M.A., Froimowitz M.P., Lange N., Snyder S.H., Bergeron R., Coyle J.T. Targeted disruption of serine racemase affects glutamatergic neurotransmission and behavior. Mol. Psychiatry 2009, 14:719-727.
24. Fossat P., Turpin F.R., Sacchi S., Dulong J., Shi T., Rivet J.M., Sweedler J.V., Pollegioni L., Millan M.J., Oliet S.H., Mothet J.P. Glial d-serine gates NMDA receptors at excitatory synapses in prefrontal cortex. Cereb. Cortex 2012, 22:595-606.
25. Le Bail M., Martineau M., Sacchi S., Yatsenko N., Radzishevsky I., Conrod S., Ait Ouares K., Wolosker H., Pollegioni L., Billard J., Mothet J. Identity of the NMDA receptor coagonist is synapse specific and developmentally regulated in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E204-E2013.
26. Mothet J.P., Parent A.T., Wolosker H., Brady R.O., Linden D.J., Ferris C.D., Rogawski M.A., Snyder S.H. d-Serine is an endogenous ligand of the glycine site of the N-methyl-d-aspartate receptor. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4926-4931.
27. Papouin T., Ladepeche L., Ruel J., Sacchi S., Labasque M., Hanini M., Groc L., Pollegioni L., Mothet J.P., Oliet S.H. Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 2012, 150:633-646.
28. Balu D.T., Basu A.C., Corradi J.P., Cacace A.M., Coyle J.T. The NMDA receptor co-agonists, d-serine and glycine, regulate neuronal dendritic architecture in the somatosensory cortex. Neurobiol. Dis. 2012, 45:671-682.
29. Yang S., Qiao H., Wen L., Zhou W., Zhang Y. d-Serine enhances impaired long-term potentiation in CA1 subfield of hippocampal slices from aged senescence-accelerated mouse prone/8. Neurosci. Lett. 2005, 379:7-12.
30. Billard J.M. d-Serine signalling as a prominent determinant of neuronal-glial dialogue in the healthy and diseased brain. J. Cell. Mol. Med. 2008, 12:1872-1884.
31. Bouet V., Freret T., Dutar P., Billard J.M., Boulouard M. Continuous enriched environment improves learning and memory in adult NMRI mice through theta-burst-related LTP independent mechanisms but is not efficient in advanced aged animals. Mech. Ageing Dev. 2011, 132:240-248.
32. Moore C.I., Browning M.D., Rose G.M. Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 344 rats. Hippocampus 1993, 3:57-66.
33. Tombaugh G.C., Rowe W.B., Chow A.R., Michael T.H., Rose G.M. Theta-frequency synaptic potentiation in CA1 in vitro distinguishes cognitively impaired from unimpaired aged Fischer 344 rats. J. Neurosci. 2002, 22:9932-9940.
34. Yang Y.J., Wu P.F., Long L.H., Yu D.F., Wu W.N., Hu Z.L., Fu H., Xie N., Jin Y., Ni L., Wang J.Z., Wang F., Chen J.G. Reversal of aging-associated hippocampal synaptic plasticity deficits by reductants via regulation of thiol redox and NMDA receptor function. Aging Cell 2010, 9:709-721.
35. Haxaire C., Turpin F.R., Potier B., Kervern M., Sinet P.M., Barbanel G., Mothet J.P., Dutar P., Billard J.M. Reversal of age-related oxidative stress prevents hippocampal synaptic plasticity deficits by protecting d-serine-dependent NMDA receptor activation. Aging Cell 2012, 11:336-344.
36. Junjaud G., Rouaud E., Turpin F., Mothet J.P., Billard J.M. Age-related effects of the neuromodulator d-serine on neurotransmission and synaptic potentiation in the CA1 hippocampal area of the rat. J. Neurochem. 2006, 98:1159-1166.
37. Mothet J.P., Rouaud E., Sinet P.M., Potier B., Jouvenceau A., Dutar P., Videau C., Epelbaum J., Billard J.M. A critical role for the glial-derived neuromodulator d-serine in the age-related deficits of cellular mechanisms of learning and memory. Aging Cell 2006, 5:267-274.
38. Turpin F.R., Potier B., Dulong J.R., Sinet P.M., Alliot J., Oliet S.H., Dutar P., Epelbaum J., Mothet J.P., Billard J.M. Neurobiol. Aging 2011, 32:1495-1504.
39. Billard J.M., Rouaud E. Eur. J. Neurosci. 2007, 25:2260-2268.
40. Potier B., Turpin F.R., Sinet P.M., Rouaud E., Mothet J.P., Videau C., Epelbaum J., Dutar P., Billard J.M. Front. Aging Neurosci. 2010, 2:1.
41. Barnes C.A. Plasticity in the aging central nervous system. Int. Rev. Neurobiol. 2001, 45:339-354.
42. Billard J.M. Long-term depression in the hippocampal CA1 of aged rats, revisited: contribution of temporal constraints related to slice preparations. PLoS ONE 2010, 5:e9843.
43. Eckles-Smith K., Clayton D., Bickford P., Browning M.D. Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Brain Res. Mol. Brain Res. 2000, 78:154-162.
44. Clayton D.A., Grosshans D.R., Browning M.D. Aging and surface expression of hippocampal NMDA receptors. J. Biol. Chem. 2002, 277:14367-14369.
45. Magnusson K.R. Declines in mRNA expression of different subunits may account for differential effects of aging on agonist and antagonist binding to the NMDA receptor. J. Neurosci. 2000, 20:1666-1674.
46. Krasteniakov N.V., Martina M., Bergeron R. Role of glycine site of the N-methyl-d-aspartate receptor in synaptic plasticity induced by pairing. Eur. J. Neurosci. 2005, 21:2782-2792.
47. Watanabe Y., Saito H., Abe K. Effects of glycine and structurally related amino acids on generation of long-term potentiation in rat hippocampal slices. Eur. J. Pharmacol. 1992, 223:179-184.
48. Nagata Y., Uehara T., Kitamura Y., Nomura Y., Horiike K. d-Serine content and d-[3H]serine binding in the brain regions of the senescence-accelerated mouse. Mech. Ageing Dev. 1998, 104:115-124.
49. Schell M.J., Brady R.O., Molliver M.E., Snyder S.H. d-Serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J. Neurosci. 1997, 17:1604-1615.
50. Hashimoto A., Nishikawa T., Konno R., Niwa A., Yasumura Y., Oka T., Takahashi K. Free d-serine, d-aspartate and d-alanine in central nervous system and serum in mutant mice lacking d-amino acid oxidase. Neurosci. Lett. 1993, 152:33-36.
51. Wolosker H., Blackshaw S., Snyder S.H. Serine racemase: a glial enzyme synthesizing d-serine to regulate glutamate-N-methyl-d-aspartate neurotransmission. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13409-13414.
52. Wolosker H., Sheth K.N., Takahashi M., Mothet J.P., Brady R.O., Ferris C.D., Snyder S.H. Purification of serine racemase: biosynthesis of the neuromodulator d-serine. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:721-725.
53. Balu D.T., Li Y., Puhl M.D., Benneyworth M.A., Basu A.C., Takagi S., Bolshakov V.Y., Coyle J.T. Multiple risk pathways for schizophrenia converge in serine racemase knockout mice, a mouse model of NMDA receptor hypofunction. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E2400-E2409.
54. Benneyworth M.A., Li Y., Basu A.C., Bolshakov V.Y., Coyle J.T. Cell selective conditional null mutations of serine racemase demonstrate a predominate localization in cortical glutamatergic neurons. Cell. Mol. Neurobiol. 2012, 32:613-624.
55. Labrie V., Clapcote S.J., Roder J.C. Mutant mice with reduced NMDA-NR1 glycine affinity or lack of d-amino acid oxidase function exhibit altered anxiety-like behaviors. Pharmacol. Biochem. Behav. 2009, 91:610-620.
56. Alliot J., Boghossian S., Jourdan D., Veyrat-Durebex C., Pickering G., Meynial-Denis D., Gaumet N. The LOU/c/jall rat as an animal model of healthy aging?. J. Gerontol. A: Biol. Sci. Med. Sci. 2002, 57:B312-B320.
57. Dubeau S., Ferland G., Gaudreau P., Beaumont E., Lesage F. Cerebrovascular hemodynamic correlates of aging in the Lou/c rat: a model of healthy aging. Neuroimage 2011, 56:1892-1901.
58. Silhol M., Arancibia S., Perrin D., Maurice T., Alliot J., Tapia-Arancibia L. Effect of aging on brain-derived neurotrophic factor, proBDNF, and their receptors in the hippocampus of Lou/C rats. Rejuvenation Res. 2008, 11:1031-1040.
59. Kollen M., Stephan A., Faivre-Bauman A., Loudes C., Sinet P.M., Alliot J., Billard J.M., Epelbaum J., Dutar P., Jouvenceau A. Preserved memory capacities in aged Lou/C/Jall rats. Neurobiol. Aging 2010, 31:129-142.
60. Menard C., Quirion R., Bouchard S., Ferland G., Gaudreau P. Glutamatergic signaling and low prodynorphin expression are associated with intact memory and reduced anxiety in rat models of healthy aging. Front. Aging Neurosci. 2014, 6:81.
61. Paban V., Billard J.M., Bouet V., Freret T., Boulouard M., Chambon C., Loriod B., Alescio-Lautier B. Genomic transcriptional profiling in LOU/C/Jall rats identifies genes for successful aging. Brain Struct. Funct. 2013, 218:1501-1512.
62. Billard J.M. Serine racemase as a prime target for age-related memory deficits. Eur. J. Neurosci. 2013, 37:1931-1938.
63. Boghossian S., Nzang Nguema G., Jourdan D., Alliot J. Old as mature LOU/c/jall rats enhance protein selection in response to a protein deprivation. Exp. Gerontol. 2002, 37:1431-1440.
64. Kalani R., Judge S., Carter C., Pahor M., Leeuwenburgh C. Effects of caloric restriction and exercise on age-related, chronic inflammation assessed by C-reactive protein and interleukin-6. J. Gerontol. A: Biol. Sci. Med. Sci. 2006, 61:211-217.
65. Droge W., Schipper H.M. Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell 2007, 6:361-370.
66. Benzi G., Moretti A. Age- and peroxidative stress-related modifications of the cerebral enzymatic activities linked to mitochondria and the glutathione system. Free Radic. Biol. Med. 1995, 19:77-101.
67. Fariello R.G. Peroxidative stress and cerebral aging. Int. J. Clin. Pharmacol. Res. 1990, 10:49-51.
68. Mustafa A.K., Kumar M., Selvakumar B., Ho G.P., Ehmsen J.T., Barrow R.K., Amzel L.M., Snyder S.H. Nitric oxide S-nitrosylates serine racemase, mediating feedback inhibition of d-serine formation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2950-2955.
69. Cocco T., Sgobbo P., Clemente M., Lopriore B., Grattagliano I., Di Paola M., Villani G. Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with N-acetylcysteine. Free Radic. Biol. Med. 2005, 38:796-805.
70. Barnes C.A., Rao G., Houston F.P. LTP induction threshold change in old rats at the perforant path-granule cell synapse. Neurobiol. Aging 2000, 21:613-620.
71. Barnes C.A., Rao G., McNaughton B.L. Functional integrity of NMDA-dependent LTP induction mechanisms across the lifespan of F-344 rats. Learn. Mem. 1996, 3:124-137.
72. Clayton D.A., Browning M.D. Deficits in the expression of the NR2B subunit in the hippocampus of aged Fisher 344 rats. Neurobiol. Aging 2001, 22:165-168.
73. Griffin R., Nally R., Nolan Y., McCartney Y., Linden J., Lynch M.A. The age-related attenuation in long-term potentiation is associated with microglial activation. J. Neurochem. 2006, 99:1263-1272.
74. Lynch M.A. Analysis of the mechanisms underlying the age-related impairment in long-term potentiation in the rat. Rev. Neurosci. 1998, 9:169-201.
75. Shankar S., Teyler T.J., Robbins N. Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J. Neurophysiol. 1998, 79:334-341.
76. Barnes C.A. Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci. 1994, 17:13-18.
77. Labarriere M., Thomas F., Dutar P., Pollegioni L., Wolosker H., Billard J.M. Circuit-specific changes in d-serine-dependent activation of the N-methyl-d-aspartate receptor in the aging hippocampus. Age (Dordrecht, Netherlands) 2014, 36:9698.
78. Geinisman Y., de Toledo-Morrell L., Morrell F. Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:3027-3031.
79. Lippa C.F., Hamos J.E., Pulaski-Salo D., DeGennaro L.J., Drachman D.A. Alzheimer's disease and aging: effects on perforant pathway perikarya and synapses. Neurobiol. Aging 1992, 13:405-411.
80. Gazzaley A.H., Siegel S.J., Kordower J.H., Mufson E.J., Morrison J.H. 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. 1996, 93:3121-3125.
81. Morrison J.H., Gazzaley A.H. Age-related alterations of the N-methyl-d-aspartate receptor in the dentate gyrus. Mol. Psychiatry 1996, 1:356-358.
82. Aura J., Riekkinen M., Riekkinen P. Tetrahydroaminoacridine and d-cycloserine stimulate acquisition of water maze spatial navigation in aged rats. Eur. J. Pharmacol. 1998, 342:15-20.
83. Baxter M.G., Lanthorn T.H., Frick K.M., Golski S., Wan R.Q., Olton D.S. d-Cycloserine, a novel cognitive enhancer, improves spatial memory in aged rats. Neurobiol. Aging 1994, 15:207-213.
84. Thompson L.T., Disterhoft J.F. Age- and dose-dependent facilitation of associative eyeblink conditioning by d-cycloserine in rabbits. Behav. Neurosci. 1997, 111:1303-1312.
85. Krug A.W., Volker K., Dantzler W.H., Silbernagl S. Why is d-serine nephrotoxic and alpha-aminoisobutyric acid protective?. Am. J. Physiol.: Renal Physiol. 2007, 293:F382-F390.
86. Lewis W.C., Calden G., Thurston J.R., Gilson W.E. Psychiatric and neurological reactions to cycloserine in the treatment of tuberculosis. Dis. Chest 1957, 32:172-182.
87. Adage T., Trillat A.C., Quattropani A., Perrin D., Cavarec L., Shaw J., Guerassimenko O., Giachetti C., Greco B., Chumakov I., Halazy S., Roach A., Zaratin P. In vitro and in vivo pharmacological profile of AS057278, a selective d-amino acid oxidase inhibitor with potential anti-psychotic properties. Eur. Neuropsychopharmacol. 2008, 18:200-214.
88. Smith S.M., Uslaner J., Yao L., Mullins C., Surles N., Huszar S., McNaughton C., Pascarella D., Kandebo M., Hinchliffe R., Sparey T., Brandon N.J., Jones B., Venkatraman S., Young M.B., Sachs N., Jacobson M., Hutson P.H. The behavioral and neurochemical effects of a novel d-amino acid oxidase inhibitor 4H-thieno [3,2-b] pyrrole-5-carboxylic acid (compound 8) and d-serine. J. Pharmacol. Exp. Ther. 2009, 328:921-930.