Vesicular uptake of N-Acetylaspartylglutamate is catalysed by sialin (SLC17A5)

Biochemical Journal

Volumn 454, Issue 1, 2013, Pages 31-38

  Lodder Gadaczek, Julia ^a   Gieselmann, Volkmar ^a   Eckhardt, Matthias ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

N Acetylaspartylglutamate; Neuropeptide; Sialin

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; LIPOSOME; N ACETYLASPARTYLGLUTAMIC ACID; PROTEOLIPOSOME; RNA DIRECTED DNA POLYMERASE; SIALIC ACID; SIALIN; UNCLASSIFIED DRUG; VALINOMYCIN; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CATALYSIS; CELL SURFACE; CONTROLLED STUDY; ENZYME RECONSTITUTION; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SYNAPSE VESICLE;

ANIMALS; BRAIN CHEMISTRY; CATALYTIC DOMAIN; DIPEPTIDES; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGANIC ANION TRANSPORTERS; SYMPORTERS; SYNAPTIC VESICLES;

EID: 84880870923     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130300     Document Type: Article

References (43)

1. Neale, J. H., Olszewski, R. T., Zuo, D., Janczura, K. J., Profaci, C. P., Lavin, K. M., Madore, J. C. and Bzdega, T. (2011) Advances in understanding the peptide neurotransmitter NAAG and appearance of a new member of the NAAG neuropeptide family. J. Neurochem. 118, 490-498.
2. Tsai, G., Forloni, G., Robinson, M. B., Stauch, B. L. and Coyle, J. T. (1988) Calcium-dependent evoked release of N-[3H]acetylaspartylglutamate from the optic pathway. J. Neurochem. 51, 1956-1959.
3. Williamson, L. C. and Neale, J. H. (1988) Ultrastructural localization of N-Acetylaspartylglutamate in synaptic vesicles of retinal neurons. Brain Res. 456, 375-381.
4. Williamson, L. C. and Neale, J. H. (1988) Calcium-dependent release of N-Acetylaspartylglutamate from retinal neurons upon depolarization. Brain Res. 475, 151-155.
5. Zollinger, M., Amsler, U., Do, K. Q., Streit, P. and Cuenod, M. (1988) Release of N-Acetylaspartylglutamate on depolarization of rat brain slices. J. Neurochem. 51, 1919-1923.
6. Neale, J. H., Olszewski, R. T., Gehl, L. M., Wroblewska, B. and Bzdega, T. (2005) The neurotransmitter N-Acetylaspartylglutamate in models of pain, ALS, diabetic neuropathy, CNS injury and schizophrenia. Trends Pharmacol. Sci. 26, 477-484.
7. Forloni, G., Grzanna, R., Blakely, R. D. and Coyle, J. T. (1987) Co-localization of N-Acetyl-Aspartyl-glutamate in central cholinergic, noradrenergic, and serotonergic neurons. Synapse 1, 455-460.
8. Moffett, J. R. and Namboodiri, A. M. (2006) Expression of N-Acetylaspartate and N-Acetylaspartylglutamate in the nervous system. Adv. Exp. Med. Biol. 576, 7-26.
9. Bruno, V., Wroblewska, B., Wroblewski, J. T., Fiore, L. and Nicoletti, F. (1998) Neuroprotective activity of N-Acetylaspartylglutamate in cultured cortical cells. Neuroscience 85, 751-757.
10. Slusher, B. S., Vornov, J. J., Thomas, A. G., Hurn, P. D., Harukuni, I., Bhardwaj, A., Traystman, R. J., Robinson, M. B., Britton, P., Lu, X. C. et al. (1999) Selective inhibition of NAALADase, which converts NAAG to glutamate, reduces ischemic brain injury. Nat. Med. 5, 1396-1402.
11. Thomas, A. G., Vornov, J. J., Olkowski, J. L., Merion, A. T. and Slusher, B. S. (2000) N-Acetylated α-linked acidic dipeptidase converts N-Acetylaspartylglutamate from a neuroprotectant to a neurotoxin. J. Pharmacol. Exp. Ther. 295, 16-22.
12. Berent-Spillson, A., Robinson, A. M., Golovoy, D., Slusher, B., Rojas, C. and Russell, J. W. (2004) Protection against glucose-induced neuronal death by NAAG and GCP II inhibition is regulated by mGluR3. J. Neurochem. 89, 90-99.
13. Bergeron, R. and Coyle, J. T. (2012) NAAG, NMDA receptor and psychosis. Curr. Med. Chem. 19, 1360-1364.
14. Neale, J. H. (2011) N-Acetylaspartylglutamate is an agonist at mGluR3 in vivo and in vitro. J. Neurochem. 119, 891-895.
15. Johnson, E. C. (2011) N-Acetylaspartylglutamate is not demonstrated to be a selective mGlu3 receptor agonist. J. Neurochem. 119, 896-898.
16. Baslow, M. H. and Burlina, A. P. (2012) N-Acetylaspartate metabolism underlays the structural and functional units of the vertebrate brain: A bioenergetic rationale for clinical observations of changes in the neuronal biomarker "NAA" in many human brain disorders. Bioenerg. Open Access 1, 102.
17. Andrew, R. D., Labron, M. W., Boehnke, S. E., Carnduff, L. and Kirov, S. A. (2007) Physiological evidence that pyramidal neurons lack functional water channels. Cereb. Cortex 17, 787-802.
18. Jessen, F., Fingerhut, N., Sprinkart, A. M., K̈uhn, K. U., Petrovsky, N., Maier, W., Schild, H. H., Block, W., Wagner, M. and Tr̈aber, F. (2011) N-Acetylaspartylglutamate (NAAG) and N-Acetylaspartate (NAA) in patients with schizophrenia. Schizophr. Bull. 39, 197-205.
19. Wolf, N. I., Willemsen, M. A., Engelke, U. F., van der Knaap, M. S., Pouwels, P. J., Harting, I., Zschocke, J., Sistermans, E. A., Rating, D. and Wevers, R. A. (2004) Severe hypomyelination associated with increased levels of N-Acetylaspartylglutamate in CSF. Neurology 62, 1503-1508.
20. Burlina, A. P., Ferrari, V., Burlina, A. B., Ermani, M., Boespflug-Tanguy, O. and Bertini, E. (2006) N-Acetylaspartylglutamate (NAAG) in Pelizaeus-Merzbacher disease. Adv. Exp. Med. Biol. 576, 353-359.
21. Mochel, F., Engelke, U. F., Barritault, J., Yang, B., McNeill, N. H., Thompson, J. N., Vanderver, A., Wolf, N. I., Willemsen, M. A., Verheijen, F. W. et al. (2010) Elevated CSF N-Acetylaspartylglutamate in patients with free sialic acid storage diseases. Neurology 74, 302-305.
22. Sartori, S., Burlina, A. B., Salviati, L., Trevisson, E., Toldo, I., Laverda, A. M. and Burlina, A. P. (2008) Increased level of N- Acetylaspartylglutamate (NAAG) in the CSF of a patient with Pelizaeus- Merzbacher-like disease due to mutation in the GJA12 gene. Eur. J. Paediatr. Neurol. 12, 348-350.
23. Becker, I., Lodder, J., Gieselmann, V. and Eckhardt, M. (2010) Molecular characterization of N-Acetylaspartylglutamate synthetase. J. Biol. Chem. 285, 29156-29164.
24. Collard, F., Stroobant, V., Lamosa, P., Kapanda, C. N., Lambert, D. M., Muccioli, G. G., Poupaert, J. H., Opperdoes, F. and van Schaftingen, E. (2010) Molecular identification of N-Acetylaspartylglutamate synthase and β-citrylglutamate synthase. J. Biol. Chem. 285, 29826-29833.
25. Lodder-Gadaczek, J., Becker, I., Gieselmann, V., Wang-Eckhardt, L. and Eckhardt, M. (2011) N-Acetylaspartylglutamate synthetase II synthesizes N-Acetylaspartylglutamylglutamate. J. Biol. Chem. 286, 16693-16706.
26. Becker, I., Wang-Eckhardt, L., Yaghootfam, A., Gieselmann, V. and Eckhardt, M. (2008) Differential expression of (dihydro)ceramide synthases in mouse brain: oligodendrocyte-specific expression of CerS2/Lass2. Histochem. Cell Biol. 129, 233-241.
27. Yaghootfam, A., Gieselmann, V. and Eckhardt, M. (2005) Delay of myelin formation in arylsulphatase A-deficient mice. Eur. J. Neurosci. 21, 711-720.
28. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7, 2745-2752.
29. Hell, J. W., Maycox, P. R. and Jahn, R. (1990) Energy dependence and functional reconstitution of the γ -Aminobutyric acid carrier from synaptic vesicles. J. Biol. Chem. 265, 2111-2117.
30. Hell, J. W., Maycox, P. R., Stadler, H. and Jahn, R. (1988) Uptake of GABA by rat brain synaptic vesicles isolated by a new procedure. EMBO J. 7, 3023-3029.
31. Miyaji, T., Echigo, N., Hiasa, M., Senoh, S., Omote, H. and Moriyama, Y. (2008) Identification of a vesicular aspartate transporter. Proc. Natl. Acad. Sci. U.S.A. 105, 11720-11724.
32. Moriyama, Y., Iwamoto, A., Hanada, H., Maeda, M. and Futai, M. (1991) One-step purification of Escherichia coli H+ -ATPase and its reconstitution into liposomes with neurotransmitter transporters. J. Biol. Chem. 266, 22141-22146.
33. Schnick, C. (2002) Strukturuntersuchungen an der F0F1-ATP-synthase aus Escherichia coli. Ph.D. Thesis, Heinrich Heine University D̈usseldorf, Germany.
34. Kottra, G. and Daniel, H. (2001) Bidirectional electrogenic transport of peptides by the proton-coupled carrier PEPT1 in Xenopus laevis oocytes: its asymmetry and symmetry. J. Physiol. 536, 495-503.
35. Morin, P., Sagne, C. and Gasnier, B. (2004) Functional characterization of wild-type and mutant human sialin. EMBO J. 23, 4560-4570.
36. Wreden, C. C., Wlizla, M. and Reimer, R. J. (2005) Varied mechanisms underlie the free sialic acid storage disorders. J. Biol. Chem. 280, 1408-1416.
37. Prolo, L. M., Vogel, H. and Reimer, R. J. (2009) The lysosomal sialic acid transporter sialin is required for normal CNS myelination. J. Neurosci. 29, 15355-15365.
38. Mochel, F., Boildieu, N., Barritault, J., Sarret, C., Eymard-Pierre, E., Seguin, F., Schiffmann, R. and Boespflug-Tanguy, O. (2010) Elevated CSF N-Acetylaspartylglutamate suggests specific molecular diagnostic abnormalities in patients with white matter diseases. Biochim. Biophys. Acta 1802, 1112-1117.
39. Verheijen, F. W., Verbeek, E., Aula, N., Beerens, C. E., Havelaar, A. C., Joosse, M., Peltonen, L., Aula, P., Galjaard, H., van der Spek, P. J. and Mancini, G. M. (1999) A new gene, encoding an anion transporter, is mutated in sialic acid storage diseases. Nat. Genet. 23, 462-465.
40. Aula, N., Kopra, O., Jalanko, A. and Peltonen, L. (2004) Sialin expression in the CNS implicates extralysosomal function in neurons. Neurobiol. Dis. 15, 251-261.
41. Morland, C., Nordengen, K., Larsson, M., Prolo, L. M., Farzampour, Z., Reimer, R. J. and Gundersen, V. (2013) Vesicular uptake and exocytosis of L-Aspartate is independent of sialin. FASEB J. 27, 1264-1274.
42. Qin, L., Liu, X., Sun, Q., Fan, Z., Xia, D., Ding, G., Ong, H. L., Adams, D., Gahl, W. A., Zheng, C. et al. (2012) Sialin (SLC17A5) functions as a nitrate transporter in the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 109, 13434-13439.
43. Cassidy, M. and Neale, J. H. (1993) Localization and transport of N-Acetylaspartylglutamate in cells of whole murine brain in primary culture. J. Neurochem. 60, 1631-1638.