Paradoxical roles of serine racemase and d -serine in the G93A mSOD1 mouse model of amyotrophic lateral sclerosis

Journal of Neurochemistry

Volumn 120, Issue 4, 2012, Pages 598-610

  Thompson, Misty ^a,b   Marecki, John C ^a,b   Marinesco, Stephane ^c   Labrie, Viviane ^d   Roder, John C ^e,f   Barger, Steven W ^a,g   Crow, John P ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c UNIVERSITÉ LYON 1   (France)

^d CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^e MOUNT SINAI HOSPITAL   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

^g GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

Author keywords

ALS; d serine; DAO; excitotoxicity; serine racemase; SOD1

Indexed keywords

ALANINE SERINE CYSTEINE TRANSPORTER 1 PROTEIN; CARRIER PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; RACEMASE; SERINE; SERINE RACEMASE; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE ACTIVITY; GENE DELETION; GENE FUNCTION; GENE MUTATION; MALE; MOUSE; NEUROPATHOLOGY; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; PROTEIN DEGRADATION; RACEMIZATION; SPINAL CORD; SURVIVAL TIME;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROGLIA; MUTATION; RACEMASES AND EPIMERASES; SERINE; SUPEROXIDE DISMUTASE; UP-REGULATION;

MUS;

EID: 84855954670     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07601.x     Document Type: Article

References (40)

1. Basu A. C., Tsai G. E., Ma C. L., et al. (2009) Targeted disruption of serine racemase affects glutamatergic neurotransmission and behavior. Mol. Psychiatry 14, 719-727.
2. Boillee S., Vande Velde C., and, Cleveland D. W., (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52, 39-59. (Pubitemid 44466358)
3. Crow J. P., Calingasan N. Y., Chen J., Hill J. L., and, Beal M. F., (2005) Manganese porphyrin given at symptom onset markedly extends survival of ALS mice. Ann. Neurol. 58, 258-265. (Pubitemid 41098883)
4. Dawson R. M. C., Elliott D. C., Elliott W. H., and, Jones K. M., (1986) Data for Biochemical Research, 3rd edn, p. 122. Clarendon Press, Oxford.
5. Di Giorgio F. P., Carrasco M. A., Siao M. C., Maniatis T., and, Eggan K., (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat. Neurosci. 10, 608-614. (Pubitemid 46652442)
6. Fadda E., Danysz W., Wroblewski J. T., and, Costa E., (1988) Glycine and D-serine increase the affinity of N-methyl-D-aspartate sensitive glutamate binding sites in rat brain synaptic membranes. Neuropharmacology 27, 1183-1185. (Pubitemid 18261183)
7. Foltyn V. N., Bendikov I., De Miranda J., Panizzutti R., Dumin E., Shleper M., Li P., Toney M. D., Kartvelishvily E., and, Wolosker H., (2005) Serine racemase modulates intracellular D-serine levels through an α,β-elimination activity. J. Biol. Chem. 280, 1754-1763.
8. +-dependent glutamate transporter GLT1 by a neuroimmunophilin ligand results in neuroprotection. Neurobiol. Dis. 21, 556-567. (Pubitemid 43277539)
9. Gurney M. E., Pu H., Chiu A. Y., et al. (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264, 1772-1775. (Pubitemid 24227760)
10. Hashimoto A., Oka T., and, Nishikawa T., (1995) Endogenous D-serine in rat brain: N-methyl-D-aspartate receptor-related distributed and aging. Neuroscience 66, 635-643.
11. Heath P. R., and, Shaw P. J., (2002) Update on the glutamatergic neurotransmitter system and the role of excitotoxicity in Amyotrophic lateral Sclerosis. Muscle Nerve 26, 438-458.
12. Helboe L., Egebjer J., Moller M., and, Thomsen C., (2003) Distribution and pharmacology of alanine-serine-cysteine transporter 1 (asc-1) in rodent brain. Eur. J. Neurosci. 18, 2227-2238. (Pubitemid 38117396)
13. Horio M. K., Fujita Y., Ishima T., Inoue R., Mori H., and, 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.
14. Inoue R., Hashimoto K., Harai T., and, Mori H., (2008) NMDA and amyloid 1-42 induced neurotoxicity is attenuated in serine racemase knock-out mice. J. Neurosci. 28, 14486-14491.
15. Kleckner N. W., and, Dingledine R., (1988) Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241, 835-837.
16. Labrie V., Fukumura R., Rastogi A., et al. (2009) Serine racemase is associated with schizophrenia susceptibility in humans and in a mouse model. Hum. Mol. Genet. 18, 3227-3243.
17. Lerma J., Zukin R. S., and, Bennett M. V., (1990) Glycine decreases desensitization of N-methyl-D-aspartate (NMDA) receptors expressed in Xenopus oocytes and is required for NMDA responses. Proc. Natl Acad. Sci. USA 87, 2354-2358.
18. Lin C. L., Bristol L. A., Jin L., Dykes-Hoberg M., Crawford T., Clawson L., and, Rothstein J. D., (1998) Aberrant RNA processing in a neurodegenerative disease: the cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron 20, 589-602. (Pubitemid 28153087)
19. Martineau M., Baux G., and, Mothet J. P., (2006) D-serine signaling in the brain: friend or foe. Trends Neurosci. 29, 481-491. (Pubitemid 44118443)
20. Mitchell J., Paul P., Chen H. J., et al. (2010) Familial amyotrophic lateral sclerosis is associated with a mutation in D-amino acid oxidase. Proc. Natl Acad. Sci. USA 107, 7556-7561.
21. Miya K., Inoue R., Takata Y., Abe M., Natsume R., Sakimura K., Hongou K., Miyawaki T., and, Mori H., (2008) Serine racemase is predominantly localized in neurons in mouse brain. J. Comp. Neurol. 510, 641-654.
22. Mothet J. P., Pollegioni L., Ouanounou G., Martineau M., Fossier P., and, Baux G., (2005) Glutamate receptors activation triggers a calcium-and SNARE protein-dependent release of the gliotransmitter D-serine. Proc. Natl Acad. Sci. USA 102, 5606-5611. (Pubitemid 40530304)
23. Mustafa A. K., van Rossum D. B., Patterson R. L., Maag D., Ehmsen J. T., Gazi S. K., Chakraborty A., Barrow R. K., Amzel L. M., and, Snyder S. H., (2009) Glutamatergic regulation of serine racemase via reversal of PIP2 inhibition. Proc. Natl Acad. Sci. USA 106, 2921-2926.
24. Mustafa A. K., Ahmad A. S., Zeynalov E., Gazi S. K., Sikka G., Ehmsen J. T., Barrow R. K., Coyle J. T., Snyder S. H., and, Doré S., (2010) Serine racemase deletion protects against cerebral ischemia and excitotoxicity. J. Neurosci. 30, 1413-1416.
25. Nagai M., Re D. B., Nagata T., Chalazonitis A., Jessell T. M., Wichterle H., and, Przedborski S., (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 10, 615-622. (Pubitemid 46652435)
26. Nakauchi J., Matsuo H., Kim D. K., et al. (2000) Cloning and characterization of human brain Na(+)-independent transporter for small neutral amino acids that transports D-serine with high affinity. Neurosci. Lett. 287, 231-235. (Pubitemid 30339391)
27. Panizzutti R., De Miranda J., Ribeiro C. S., Engelender S., and, Wolosker H., (2001) A new strategy to decrease N-methyl-D-aspartate (NMDA) receptor coactivation: inhibition of D-serine synthesis by converting serine racemase into an eliminase. Proc. Natl Acad. Sci. USA 98, 5294-5299. (Pubitemid 32397122)
28. Pernot P., Mothet J. P., Schuvailo O., Soldatkin A., Pollegioni L., Pilone M., Adeline M. T., Cespuglio R., and, Marinesco S., (2008) Characterization of a yeast D-amino acid oxidase microbiosensor for D-serine detection in the central nervous system. Anal. Chem. 80, 1589-1597. (Pubitemid 351429564)
29. Pollegioni L., and, Sacchi S., (2010) Metabolism of the neuromodulator D-serine. Cell. Mol. Life Sci. 67, 2387-2404.
30. Pollegioni L., Falbo A., and, Pilone M. S., (1992) Specificity and kinetics of Rhodotorula gracilis D-amino acid oxidase. Biochim. Biophys. Acta 1120, 11-16.
31. Rao S. D., and, Weiss J. H., (2004) Excitotoxic and oxidative cross-talk between motor neurons and glia in ALS pathogenesis. Trends Neurosci. 27, 17-23. (Pubitemid 38036974)
32. Rothstein J. D., Tsai G., Kuncl R. W., Clawson L., Cornblath D. R., Drachman D. B., Pestronk A., Stauch B. L., and, Coyle J. T., (1990) Abnormal excitatory amino acid metabolism in amyotrophic lateral sclerosis. Ann. Neurol. 28, 18-25. (Pubitemid 20222147)
33. Rothstein J. D., Patel S., Regan M. R., et al. (2005) Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433, 73-77. (Pubitemid 40101145)
34. Rutter A. R., Fradley R. L., Garrett E. M., Chapman K. L., Lawrence J. M., Rosahl T. W., and, Patel S., (2007) Evidence from gene knockout studies implicates Asc-1 as the primary transporter mediating D-serine uptake in the mouse CNS. Eur. J. Neurosci. 25, 1757-1766. (Pubitemid 46550015)
35. Sasabe J., Chiba T., Yamada M., Okamoto K., Nishimoto I., Matsuoka M., and, Aiso S., (2007) D-serine is a key determinant of glutamate toxicity in amyotrophic lateral sclerosis. EMBO J. 26, 4149-4159. (Pubitemid 47462099)
36. Schell M. J., Molliver M. E., and, Snyder S. H., (1995) D-serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc. Natl Acad. Sci. USA 92, 3948-3952.
37. Stout A. K., Raphael H. M., Kanterewicz B. I., Klann E., and, Reynolds I. J., (1998) Glutamate-induced amyotrophic lateral sclerosis requires mitochondrial calcium uptake. Nat. Neurosci. 1, 366-373.
38. Strisovsky K., Jirásková J., Mikulová A., Rulísek L., and, Konvalinka J., (2005) Dual substrate and reaction specificity in mouse serine racemase: identification of high-affinity dicarboxylate substrate and inhibitors and analysis of the α,β- eliminase activity. Biochemistry 44, 13091-13100. (Pubitemid 41377289)
39. Wu S. Z., Bodles A. M., Porter M. M., Griffin W. S., Basile A. S., and, Barger S. W., (2004) Induction of serine racemase expression and D-serine release from microglia by amyloid beta-peptide. J. Neuroinflamm. 1, 2-12.
40. Xie X., Dumas T., Tang L., et al. (2005) Lack of the alanine-serine- cysteine transporter 1 causes tremors, seizures, and early postnatal death in mice. Brain Res. 1052, 212-221. (Pubitemid 41116780)