D-serine diffusion through the blood-brain barrier: Effect on D-serine compartmentalization and storage

Neurochemistry International

Volumn 60, Issue 8, 2012, Pages 837-845

  Pernot, Pierre ^a,b   Maucler, Caroline ^a,b   Tholance, Yannick ^a,b,c   Vasylieva, Natalia ^a,b,d   Debilly, Gabriel ^a,b   Pollegioni, Loredano ^e,f   Cespuglio, Raymond ^a,b   Marinesco, Stéphane ^a,b  

^a LYON NEUROSCIENCE RESEARCH CENTER   (France)

^b UNIVERSITÉ LYON 1   (France)

^c HOSPICES CIVILS DE LYON   (France)

^d INSTITUT DES NANOTECHNOLOGIES DE LYON   (France)

^e UNIVERSITY OF INSUBRIA   (Italy)

^f POLITECNICO DI MILANO   (Italy)

Author keywords

Amperometry; Electrochemistry; In vivo; Interstitial fluid; Intracellular stores; Rat; Serum

Indexed keywords

DEXTRO SERINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSENSOR; BLOOD BRAIN BARRIER; BRAIN LATERAL VENTRICLE; BRAIN LEVEL; BRAIN TISSUE; CELL COMPARTMENTALIZATION; CEREBELLUM; CISTERNA MAGNA; COGNITION; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG DIFFUSION; EXTRACELLULAR SPACE; FRONTAL CORTEX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; INTRACELLULAR SPACE; MALE; MICROELECTRODE; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; STORAGE;

ANIMALS; BIOSENSING TECHNIQUES; BLOOD-BRAIN BARRIER; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; MALE; MICROELECTRODES; RATS; RATS, WISTAR; SERINE;

ANIMALIA; RATTUS;

EID: 84861211086     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.03.008     Document Type: Article

References (62)

1. Bado, P., Madeira, C., Vargas-Lopes, C., Moulin, T.C., Wasilewska-Sampaio, A.P., Maretti, L., de Oliveira, R.V., Amaral, O.B., Panizzutti, R., 2011. Effects of low-dose D-serine on recognition and working memory in mice. Psychopharmacol. (Berl.) 218, 461-470.
2. Bauer, D., Hamacher, K., Broer, S., Pauleit, D., Palm, C., Zilles, K., Coenen, H.H., Langen, K.J., 2005. Preferred stereoselective brain uptake of D-serine - a modulator of glutamatergic neurotransmission. Nucl. Med. Biol. 32, 793-797. (Pubitemid 41505312)
3. Bergersen, L.H., Morland, C., Ormel, L., Rinholm, J.E., Larsson, M., Wold, J.F., Roe, A.T., Stranna, A., Santello, M., Bouvier, D., Ottersen, O.P., Volterra, A., Gundersen, V., 2011. Immunogold Detection of L-Glutamate and D-serine in Small Synaptic- Like Microvesicles in Adult Hippocampal Astrocytes. Cereb Cortex.
4. Borland, L.M., Shi, G., Yang, H., Michael, A.C., 2005. Voltammetric study of extracellular dopamine near microdialysis probes acutely implanted in the striatum of the anesthetized rat. J. Neurosci. Methods 146, 149-158. (Pubitemid 41373452)
5. Ciriacks, C.M., Bowser, M.T., 2004. Monitoring D-serine dynamics in the rat brain using online microdialysis-capillary electrophoresis. Anal. Chem. 76, 6582-6587. (Pubitemid 39507247)
6. Ciriacks, C.M., Bowser, M.T., 2006. Measuring the effect of glutamate receptor agonists on extracellular D-serine concentrations in the rat striatum using online microdialysis-capillary electrophoresis. Neurosci. Lett. 393, 200-205. (Pubitemid 41821108)
7. Coyle, J.T., Tsai, G., 2004. NMDA receptor function, neuroplasticity, and the pathophysiology of schizophrenia. Int. Rev. Neurobiol. 59, 491-451.
8. Czeredys, M., Mysiorek, C., Kulikova, N., Samluk, L., Berezowski, V., Cecchelli, R., Nalecz, K.A., 2008. A polarized localization of amino acid/carnitine transporter B(0, +) (ATB(0,+)) in the blood-brain barrier. Biochem. Biophys. Res. Commun. 376, 267-270.
9. Danysz, W., Parsons, C.G., 1998. Glycine and N-methyl-D-aspartate receptors: physiological significance and possible therapeutic applications. Pharmacol. Rev. 50, 597-664. (Pubitemid 29028813)
10. Ferraris, D., Duvall, B., Ko, Y.S., Thomas, A.G., Rojas, C., Majer, P., Hashimoto, K., Tsukamoto, T., 2008. Synthesis and biological evaluation of D-amino acid oxidase inhibitors. J. Med. Chem. 51, 3357-3359. (Pubitemid 351874993)
11. Foltyn, V.N., Bendikov, I., De Miranda, J., Panizzutti, R., Dumin, E., Shleper, M., Li, P., Toney, M.D., Kartvelishvily, E., Wolosker, H., 2005. Serine racemase modulates intracellular D-serine levels through an alpha, beta-elimination activity. J. Biol. Chem. 280, 1754-1763.
12. Fukasawa, Y., Segawa, H., Kim, J.Y., Chairoungdua, A., Kim, D.K., Matsuo, H., Cha, S.H., Endou, H., Kanai, Y., 2000. Identification and characterization of a Na(+)- independent neutral amino acid transporter that associates with the 4F2 heavy chain and exhibits substrate selectivity for small neutral D- and L-amino acids. J. Biol. Chem. 275, 9690-9698. (Pubitemid 30185202)
13. Fukushima, T., Kawai, J., Imai, K., Toyo'oka, T., 2004. Simultaneous determination of D- and L-serine in rat brain microdialysis sample using a column-switching HPLC with fluorimetric detection. Biomed. Chromatogr. 18, 813-819. (Pubitemid 40089852)
14. Ganote, C.E., Peterson, D.R., Carone, F.A., 1974. The nature of D-serine-induced nephrotoxicity. Am. J. Pathol. 77, 269-282.
15. Gelfin, E., Kaufman, Y., Korn-Lubetzki, I., Bloch, B., Kremer, I., Javitt, D.C., Heresco- Levy, U., 2011. D-Serine adjuvant treatment alleviates behavioural and motor symptoms in Parkinson's disease. Int. J. Neuropsychopharmacol., 1-7.
16. Hamase, K., Konno, R., Morikawa, A., Zaitsu, K., 2005. Sensitive determination of Damino acids in mammals and the effect of D-amino-acid oxidase activity on their amounts. Biol. Pharm. Bull. 28, 1578-1584. (Pubitemid 41324112)
17. Hashimoto, A., 2002. Effect of the intracerebroventricular and systemic administration of L-serine on the concentrations of D- and L-serine in several brain areas and periphery of rat. Brain Res. 955, 214-220. (Pubitemid 35284852)
18. Hashimoto, A., Nishikawa, T., Oka, T., Takahashi, K., Hayashi, T., 1992. Determination of free amino acid enantiomers in rat brain and serum by high-performance liquid chromatography after derivatization with N-tert.-butyloxycarbonyl-Lcysteine and o-phthaldialdehyde. J. Chromatogr. 582, 41-48.
19. Hashimoto, A., Oka, T., Nishikawa, T., 1995. Extracellular concentration of endogenous free D-serine in the rat brain as revealed by in vivo microdialysis. Neuroscience 66, 635-643.
20. Hashimoto, K., Fujita, Y., Horio, M., Kunitachi, S., Iyo, M., Ferraris, D., Tsukamoto, T., 2009. Co-administration of a D-amino acid oxidase inhibitor potentiates the efficacy of D-serine in attenuating prepulse inhibition deficits after administration of dizocilpine. Biol. Psychiatry 65, 1103-1106.
21. Hashimoto, K., Fukushima, T., Shimizu, E., Okada, S., Komatsu, N., Okamura, N., Koike, K., Koizumi, H., Kumakiri, C., Imai, K., Iyo, M., 2004. Possible role of Dserine in the pathophysiology of Alzheimer's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 28, 385-388. (Pubitemid 38130146)
22. Hatanaka, T., Huang, W., Nakanishi, T., Bridges, C.C., Smith, S.B., Prasad, P.D., Ganapathy, M.E., Ganapathy, V., 2002. Transport of D-serine via the amino acid transporter ATB(0,+) expressed in the colon. Biochem. Biophys. Res. Commun. 291, 291-295. (Pubitemid 34694403)
23. Hawkins, B.T., Egleton, R.D., 2006. Fluorescence imaging of blood-brain barrier disruption. J. Neurosci. Methods 151, 262-267. (Pubitemid 43294448)
24. Henneberger, C., Papouin, T., Oliet, S.H., Rusakov, D.A., 2010. Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232-236.
25. Heresco-Levy, U., Javitt, D.C., Ebstein, R., Vass, A., Lichtenberg, P., Bar, G., Catinari, S., Ermilov, M., 2005. D-Serine efficacy as add-on pharmacotherapy to risperidone and olanzapine for treatment-refractory schizophrenia. Biol. Psychiatry 57, 577-585. (Pubitemid 40409697)
26. Heresco-Levy, U., Vass, A., Bloch, B., Wolosker, H., Dumin, E., Balan, L., Deutsch, L., Kremer, I., 2009. Pilot controlled trial of D-serine for the treatment of post-traumatic stress disorder. Int. J. Neuropsychopharmacol. 12, 1275-1282.
27. Horio, M., Kohno, M., Fujita, Y., Ishima, T., Inoue, R., Mori, H., Hashimoto, K., 2011. Levels of D-serine in the brain and peripheral organs of serine racemase (Srr) knock-out mice. Neurochem. Int. 59, 853-859.
28. Kasai, Y., Tachikawa, M., Hirose, S., Akanuma, S., Hosoya, K., 2011. Transport systems of serine at the brain barriers and in brain parenchymal cells. J. Neurochem. 118, 304-313.
29. Katsuki, H., Watanabe, Y., Fujimoto, S., Kume, T., Akaike, A., 2007. Contribution of endogenous glycine and D-serine to excitotoxic and ischemic cell death in rat cerebrocortical slice cultures. Life Sci. 81, 740-749. (Pubitemid 47285193)
30. Kim, P.M., Aizawa, H., Kim, P.S., Huang, A.S., Wickramasinghe, S.R., Kashani, A.H., Barrow, R.K., Huganir, R.L., Ghosh, A., Snyder, S.H., 2005. Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration. Proc. Natl. Acad. Sci. USA 102, 2105-2110. (Pubitemid 40262019)
31. Kirschner, D.L., Wilson, A.L., Drew, K.L., Green, T.K., 2009. Simultaneous efflux of endogenous D-ser and L-glu from single acute hippocampus slices during oxygen glucose deprivation. J. Neurosci. Res..
32. Labrie, V., Wong, A.H., Roder, J.C., 2011. Contributions of the D-serine pathway to schizophrenia. Neuropharmacology.
33. Lane, H.Y., Lin, C.H., Huang, Y.J., Liao, C.H., Chang, Y.C., Tsai, G.E., 2010. A randomized, double-blind, placebo-controlled comparison study of sarcosine (N-methylglycine) and D-serine add-on treatment for schizophrenia. Int. J. Neuropsychopharmacol. 13, 451-460.
34. Martineau, M., Galli, T., Baux, G., Mothet, J.P., 2008. Confocal imaging and tracking of the exocytotic routes for D-serine-mediated gliotransmission. Glia 56, 1271- 1284.
35. Matsuda, S., Matsuzawa, D., Nakazawa, K., Sutoh, C., Ohtsuka, H., Ishii, D., Tomizawa, H., Iyo, M., Shimizu, E., 2010. D-Serine enhances extinction of auditory cued fear conditioning via ERK1/2 phosphorylation in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 895-902.
36. Miya, K., Inoue, R., Takata, Y., Abe, M., Natsume, R., Sakimura, K., Hongou, K., Miyawaki, T., Mori, H., 2008. Serine racemase is predominantly localized in neurons in mouse brain. J. Comp. Neurol. 510, 641-654.
37. Mothet, J.P., Parent, A.T., Wolosker, H., Brady, R.O.J., Linden, D.J., Ferris, C.D., Rogawski, M.A., Snyder, S.H., 2000. D-Serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc. Natl. Acad. Sci. USA 97, 4926-4931. (Pubitemid 30238659)
38. Nicholson, C., Sykova, E., 1998. Extracellular space structure revealed by diffusion analysis. Trends Neurosci. 21, 207-215. (Pubitemid 28191815)
39. Oliet, S.H., Mothet, J.P., 2006. Molecular determinants of D-serine-mediated gliotransmission: from release to function. Glia 54, 726-737. (Pubitemid 44629635)
40. Orozco-Ibarra, M., Medina-Campos, O.N., Sanchez-Gonzalez, D.J., Martinez- Martinez, C.M., Floriano-Sanchez, E., Santamaria, A., Ramirez, V., Bobadilla, N.A., Pedraza-Chaverri, J., 2007. Evaluation of oxidative stress in D-serine induced nephrotoxicity. Toxicology 229, 123-135. (Pubitemid 44911082)
41. Panatier, A., Theodosis, D.T., Mothet, J.P., Touquet, B., Pollegioni, L., Poulain, D.A., Oliet, S.H., 2006. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775-784.
42. Pernot, P., Mothet, J.P., Schuvailo, O., Soldatkin, A., Pollegioni, L., Pilone, M., Adeline, M.T., Cespuglio, R., Marinesco, S., 2008. Characterization of a yeast D-amino acid oxidase microbiosensor for D-serine detection in the central nervous system. Anal. Chem. 80, 9.
43. Pollegioni, L., Falbo, A., Pilone, M.S., 1992. Specificity and kinetics of Rhodotorula gracilis D-amino acid oxidase. Biochim. Biophys. Acta 1120, 11-16.
44. Pollegioni, L., Molla, G., Campaner, S., Martegani, E., Pilone, M.S., 1997. Cloning, sequencing and expression in E. coli of a D-amino acid oxidase cDNA from Rhodotorula gracilis active on cephalosporin C. J. Biotechnol. 58, 115-123. (Pubitemid 27466022)
45. Pollegioni, L., Molla, G., Sacchi, S., Rosini, E., Verga, R., Pilone, M.S., 2008. Properties and applications of microbial D-amino acid oxidases: current state and perspectives. Appl. Microbiol. Biotechnol. 78, 1-16.
46. Rutter, A.R., Fradley, R.L., Garrett, E.M., Chapman, K.L., Lawrence, J.M., Rosahl, T.W., Patel, S., 2007. Evidence from gene knockout studies implicates Asc-1 as the primary transporter mediating d-serine reuptake in the mouse CNS. Eur. J. Neurosci. 25, 1757-1766. (Pubitemid 46550015)
47. Sasabe, J., Chiba, T., Yamada, M., Okamoto, K., Nishimoto, I., Matsuoka, M., Aiso, S., 2007. D-Serine is a key determinant of glutamate toxicity in amyotrophic lateral sclerosis. EMBO J. 26, 4149-4159. (Pubitemid 47462099)
48. Schell, M.J., Brady Jr., R.O., Molliver, M.E., Snyder, S.H., 1997. D-Serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J. Neurosci. 17, 1604-1615. (Pubitemid 27089806)
49. 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, 9413-9417. (Pubitemid 41464754)
50. Smith, Q.R., 2000. Transport of glutamate and other amino acids at the blood-brain barrier. J. Nutr. 130, 1016S-1022S. (Pubitemid 30173636)
51. Smith, Q.R., Momma, S., Aoyagi, M., Rapoport, S.I., 1987. Kinetics of neutral amino acid transport across the blood-brain barrier. J. Neurochem. 49, 1651-1658. (Pubitemid 17161391)
52. Smith, S.M., Uslaner, J.M., Yao, L., Mullins, C.M., Surles, N.O., Huszar, S.L., McNaughton, C.H., Pascarella, D.M., Kandebo, M., Hinchliffe, R.M., Sparey, T., Brandon, N.J., Jones, B., Venkatraman, S., Young, M.B., Sachs, N., Jacobson, M.A., Hutson, P.H., 2009. The behavioral and neurochemical effects of a novel Damino acid oxidase inhibitor compound 8 [4H-thieno [3,2-b]pyrrole-5- carboxylic acid] and D-serine. J. Pharmacol. Exp. Ther. 328, 921-930.
53. Tayarani, I., Lefauconnier, J.M., Roux, F., Bourre, J.M., 1987. Evidence for an alanine, serine, and cysteine system of transport in isolated brain capillaries. J. Cereb. Blood Flow Metab. 7, 585-591.
54. Thompson, M., Marecki, J.C., Marinesco, S., Labrie, V., Roder, J.C., Barger, S.W., Crow, J.P., 2011. Paradoxical roles of serine racemase and D-serine in the G93A mSOD1 mouse model of ALS. J. Neurochem..
55. Tsai, G., Yang, P., Chung, L.C., Lange, N., Coyle, J.T., 1998. D-Serine added to antipsychotics for the treatment of schizophrenia. Biol. Psychiatry 44, 1081-1089. (Pubitemid 28547143)
56. Tsai, P.S., Kaufhold, J.P., Blinder, P., Friedman, B., Drew, P.J., Karten, H.J., Lyden, P.D., Kleinfeld, D., 2009. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels. J. Neurosci. 29, 14553-14570.
57. Utsunomiya-Tate, N., Endou, H., Kanai, Y., 1996. Cloning and functional characterization of a system ASC-like Na+-dependent neutral amino acid transporter. J. Biol. Chem. 271, 14883-14890.
58. Vasylieva, N., Barnych, B., Meiller, A., Maucler, C., Pollegioni, L., Lin, J.S., Barbier, D., Marinesco, S., 2011. Covalent enzyme immobilization by poly(ethylene glycol) diglycidyl ether (PEGDE) for microelectrode biosensor preparation. Biosens. Bioelectron. 26, 3993-4000.
59. Williams, S.M., Diaz, C.M., Macnab, L.T., Sullivan, R.K., Pow, D.V., 2006. Immunocytochemical analysis of D-serine distribution in the mammalian brain reveals novel anatomical compartmentalizations in glia and neurons. Glia 53, 401-411.
60. Wolosker, H., 2011. Serine racemase and the serine shuttle between neurons and astrocytes. Biochim. Biophys. Acta 1814, 1558-1566.
61. Yang, F.Y., Lee, Y.S., Cherng, C.G., Cheng, L.Y., Chang, W.T., Chuang, J.Y., Kao, G.S., Yu, L., 2010. D-Cycloserine, sarcosine and D-serine diminish the expression of cocaine-induced conditioned place preference. J. Psychopharmacol..
62. Zhang, Z., Gong, N., Wang, W., Xu, L., Xu, T.L., 2008. Bell-shaped D-serine actions on hippocampal long-term depression and spatial memory retrieval. Cereb Cortex 18, 2391-2401.