Advertisement

Acta Biologica Hungarica

, Volume 69, Issue 1, pp 1–15 | Cite as

Age-Related and Function-Dependent Regional Alterations of Free L- and D-Aspartate in Postembryonic Chick Brain

  • Gergely ZacharEmail author
  • Tamás Jakó
  • István Vincze
  • Zsolt Wagner
  • Tamás Tábi
  • Eszter Bálint
  • Szilvia Mezey
  • Éva Szökő
  • András Csillag
Article
  • 1 Downloads

Abstract

D-aspartate (D-Asp) modulates adult neural plasticity and embryonic brain development by promoting cell proliferation, survival and differentiation. Here, developmental changes of the excitatory amino acids (EAAs) L-Glu, L-Asp and D-Asp were determined during the frst postembryonic days, a time window for early learning, in selected brain regions of domestic chickens after chiral separation and capillary electrophoresis. Extracellular concentration (ECC) of EAAs was measured in microdialysis samples from freely moving chicks. ECC of D-Asp (but not L-EAAs) decreased during the frst week of age, with no considerable regional or learning-related variation. ECC of L-Asp and L-Glu (but not of D-Asp) were elevated in the mSt/Ac in response to a rewarding stimulus, suggesting importance of Asp-Glu co-release in synaptic plasticity of basal ganglia. Potassium-evoked release of D-Asp, with a protracted transient, was also demonstrated. D-Asp constitutes greater percentage of total aspartate in the extracellular space than in whole tissue extracts, thus the bulk of D-Asp detected in tissue appears in the extracellular space. Conversely, only a fraction of tissue L-EAAs can be detected in extracellular space. The lack of changes in tissue D-Asp following avoidance learning indicates a tonic, rather than phasic, mechanism in the neuromodulatory action of this amino acid.

Keywords

D-aspartic acid avian brain postembryonic development arcopallium amygdala 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Ádám, A. S., Csillag, A. (2006) Differential distribution of L-aspartate- and L-glutamate-immunoreactive structures in the arcopallium and medial striatum of the domestic chick (Gallus domesticus). J. Comp. Neurol. 498, 266–276.PubMedGoogle Scholar
  2. 2.
    Balázs, D., Csillag, A., Gerber, G. (2012) L-aspartate effects on single neurons and interactions with glutamate in striatal slice preparation from chicken brain. Brain Res. 1474, 1–7.PubMedGoogle Scholar
  3. 3.
    Bálint, E., Csillag, A. (2007) Nucleus accumbens subregions: hodological and immunohistochemical study in the domestic chick (Gallus domesticus). Cell Tissue Res. 327, 221–230.PubMedGoogle Scholar
  4. 4.
    Bateson, P. (1966) The characteristics and context of imprinting. Biol. Rev. 41, 177–220.PubMedGoogle Scholar
  5. 5.
    Csillag, A. (1999) Striato-telencephalic and striato-tegmental circuits: relevance to learning in domestic chicks. Behav. Brain Res. 98, 227–236.PubMedGoogle Scholar
  6. 6.
    Daisley, J. N., Gruss, M., Rose, S. P. R., Braun, K. (1998) Passive avoidance training and recall are associated with increased glutamate levels in the intermediate medial hyperstriatum centrale of the day-old chick. Neural Plast. 6, 53–61.PubMedPubMedCentralGoogle Scholar
  7. 7.
    D’Aniello, A. (2007) D-Aspartic acid: an endogenous amino acid with an important neuroendocrine role. Brain Res. Rev. 53, 215–234.PubMedGoogle Scholar
  8. 8.
    D’Aniello, A., Guiditta, A. (1977) Identifcation of D-aspartic acid in the brain of Octopus vulgaris Lam. J. Neurochem. 29, 1053–1057.PubMedGoogle Scholar
  9. 9.
    D’Aniello, S., Somorjai, I., Garcia-Fernàndez, J., Topo, E., D’Aniello, A. (2011) D-Aspartic acid is a novel endogenous neurotransmitter. FASEB J. 25, 1014–1027.PubMedGoogle Scholar
  10. 10.
    Dermon, C. R., Zikopoulos, B., Panagis, L., Harrison, E., Lancashire, C. L., Mileusnic, R., Stewart, M. G. (2002) Passive avoidance training enhances cell proliferation in 1-day-old chicks. Eur. J. Neurosci. 16, 1267–1274.Google Scholar
  11. 11.
    Dunlop, D. S., Neidle, A., McHale, D., Dunlop, D. M., Lajtha, A. (1986) The presence of free D-aspartic acid in rodents and man. Biochem. Biophys. Res. Commun. 141, 27–32.Google Scholar
  12. 12.
    Errico, F., Rossi, S., Napolitano, F., Catuogno, V., Topo, E., Fisone, G., D’Aniello, A., Centonze, D., Usiello, A. (2008) D-aspartate prevents corticostriatal long-term depression and attenuates schizophrenia-like symptoms induced by amphetamine and MK-801. J. Neurosci. 28, 10404–10414.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Errico, F. et al. (2014) Free D-aspartate regulates neuronal dendritic morphology, synaptic plasticity, gray matter volume and brain activity in mammals. Transl. Psychiatry 4, e417.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Fagg, G. E., Matus, A. (1984) Selective association of N-methyl aspartate and quisqualate types of L-glutamate receptor with brain postsynaptic densities. Proc. Natl. Acad. Sci. USA 81, 6876–6880.PubMedGoogle Scholar
  15. 15.
    Fujii, N. (2005) D-amino acid in elderly tissues. Biol. Pharm. Bull. 28, 1585–1589.PubMedGoogle Scholar
  16. 16.
    Gibbs, M., Johnston, A. N. B., Mileusnic, R., Crowe, S. F. (2008) A comparison of protocols for passive and discriminative avoidance learning tasks in the domestic chick. Brain Res. Bull. 76, 198–207.PubMedGoogle Scholar
  17. 17.
    Gundersen, V., Storm-Mathisen, J. (2000) Chapter II Aspartate-neurochemical evidence for a transmitter role. In: Ottersen, O. P., Storm-Mathisen, J. (eds), Handbook of Chemical Neuroanatomy, vol. 18. Amsterdam, Elsevier. pp. 45–62.Google Scholar
  18. 18.
    Hanics, J., Bálint, E., Milanovich, D., Zachar, G., Adám, A., Csillag, A. (2012) Amygdalofugal axon terminals immunoreactive for L-aspartate or L-glutamate in the nucleus accumbens of rats and domestic chickens: a comparative electron microscopic immunocytochemical study combined with anterograde pathway tracing. Cell Tissue Res. 350, 409–423.PubMedGoogle Scholar
  19. 19.
    Hanics, J., Teleki, G., Alpár, A., Székely, A. D., Csillag, A. (2016) Multiple amygdaloid divisions of arcopallium send convergent projections to the nucleus accumbens and neighboring subpallial amygdala regions in the domestic chicken: a selective pathway tracing and reconstruction study. Brain Struct. Funct. 222, 301–315.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Hashimoto, A., Kumashiro, S., Nishikawa, T., Oka, T., Takahashi, K., Mito, T., Takashima, S., Doi, N., Mizutani, Y., Yamazaki, T., Kaneko, T., Ootomo, E. (1993) Embryonic development and postnatal changes in free D-aspartate and D-serine in the human prefrontal cortex. J. Neurochem. 61, 348–351.PubMedGoogle Scholar
  21. 21.
    Hashimoto, A., Oka, T., Nishikawa, T. (1995) Anatomical distribution and postnatal changes in endogenous free D-Aspartate and D-Serine in rat-brain and periphery. Eur. J. Neurosci. 7, 1657–1663.PubMedGoogle Scholar
  22. 22.
    Horn, G. (2004) Pathways of the past: the imprint of memory. Nat. Rev. Neurosci. 5, 108–120.PubMedGoogle Scholar
  23. 23.
    Ito, T., Hayashida, M., Kobayashi, S., Muto, N., Hayashi, A., Yoshimura, T., Mori, H. (2016) Serine racemase is involved in D-aspartate biosynthesis. J. Biochem. 160, 345–353.PubMedGoogle Scholar
  24. 24.
    Matsushima, T., Izawa, E.-I., Yanagihara, S. (2001) D1-receptor dependent synaptic potentiation in the basal ganglia of quail chick. NeuroReport 12, 2831–2837.PubMedGoogle Scholar
  25. 25.
    McCabe, B. J. (2013) Imprinting. Interdiscip. Rev. Cogn. Sci. 4, 375–390.Google Scholar
  26. 26.
    Mezey, S., Krivokuca, D., Balint, E., Adorjan, A., Zachar, G., Csillag, A. (2012) Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus). J. Comp. Neurol. 520, 100–116.PubMedGoogle Scholar
  27. 27.
    Miller J. A. (1950) Do tumor proteins contain D-amino acids? A review of the controversy. Cancer Res. 10, 65–72.PubMedGoogle Scholar
  28. 28.
    Nadler, J. V., Vaca, K. W., White, W. F., Lynch, G. S., Cotman, C. W. (1976) Aspartate and glutamate as possible transmitters of excitatory hippocampal afferents. Nature 260, 538–540.PubMedGoogle Scholar
  29. 29.
    Nakamori, T., Maekawa, F., Sato, K., Tanaka, K., Ohki-Hamazaki, H. (2013) Neural basis of imprinting behavior in chicks. Dev. Growth Differ. 55, 198–206.PubMedGoogle Scholar
  30. 30.
    Neidle, A., Dunlop, D. S. (1990) Developmental changes in free D-aspartic acid in the chicken embryo and in the neonatal rat. Life Sci. 46, 1517–1522.Google Scholar
  31. 31.
    Nuzzo, T. et al. (2017) Decreased free D-aspartate levels are linked to enhanced D-aspartate oxidase activity in the dorsolateral prefrontal cortex of schizophrenia patients. npj Schizophrenia 3, 16.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Puelles, L. (2007) The chick brain in stereotaxic coordinates. Academic Press, San Diego.Google Scholar
  33. 33.
    Punzo, D., Errico, F., Cristino, L., Sacchi, S., Keller, S., Belardo, C., Luongo, L., Nuzzo, T., Imperatore, R., Florio, E., De Novellis, V., Affnito, O., Migliarini, S., Maddaloni, G., Sisalli, M. J., Pasqualetti, M., Pollegioni, L., Maione, S., Chiariotti, L., Usiello, A. (2016) Age-related changes in D-Aspartate oxidase promoter methylation control extracellular D-Aspartate levels and prevent precocious cell death during brain aging. J. Neurosci. 36, 3064–3078.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Radzishevsky, I., Sason, H., Wolosker, H. (2013) D-serine: physiology and pathology. Curr. Opin. Clin. Nutr. Metab. Care. 16, 72–75.PubMedGoogle Scholar
  35. 35.
    Reiner, A. (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377–414.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Rose, S. P. (2000) God’s organism? The chick as a model system for memory studies. Learn. Mem. 7, 1–17.PubMedGoogle Scholar
  37. 37.
    Schell, M. J., Cooper, O. B., Snyder, S. H. (1997) D-aspartate localizations imply neuronal and neuroendocrine roles. Proc. Natl. Acad. Sci. USA 94, 2013–2018.PubMedGoogle Scholar
  38. 38.
    Stewart, M. G., Rusakov, D. A. (1995) Morphological changes associated with stages of memory formation in the chick following passive avoidance training. Behav. Brain Res. 66, 21–28.PubMedGoogle Scholar
  39. 39.
    Topo, E., Soricelli, A., Di Maio, A., D’Aniello, E., Di Fiore, M. M., D’Aniello, A. (2010) Evidence for the involvement of D-aspartic acid in learning and memory of rat. Amino acids 38, 1561–1569.PubMedGoogle Scholar
  40. 40.
    Venero, C., Sandi, C. (1997) Effects of NMDA and AMPA receptor antagonists on corticosterone facilitation of long-term memory in the chick. Eur. J. Neurosci. 9, 1923–1928.PubMedGoogle Scholar
  41. 41.
    Wagner, Z., Tabi, T., Zachar, G., Csillag, A., Szoko, E. (2011) Comparison of quantitative performance of three fuorescence labels in CE/LIF analysis of aspartate and glutamate in brain microdi-alysate. Electrophoresis 32, 2816–2822.PubMedGoogle Scholar
  42. 42.
    Wagner, Z., Tabi, T., Jako, T., Zachar, G., Csillag, A., Szoko, E. (2012) Chiral separation and determination of excitatory amino acids in brain samples by CE-LIF using dual cyclodextrin system. Anal. Bioanal. Chem. 404, 2363–2368.PubMedGoogle Scholar
  43. 43.
    Wolosker, H., D’Aniello, A., Snyder, S. H. (2000) D-aspartate disposition in neuronal and endocrine tissues: ontogeny, biosynthesis and release. Neuroscience 100, 183–189.PubMedGoogle Scholar
  44. 44.
    Yamanaka, M., Miyoshi, Y., Ohide, H., Hamase, K., Konno, R. (2012) D-Amino acids in the brain and mutant rodents lacking D-amino-acid oxidase activity. Amino Acids 43, 1811–1821.PubMedGoogle Scholar
  45. 45.
    Zachar, G., Wagner, Z., Tabi, T., Balint, E., Szoko, E., Csillag, A. (2012) Differential changes of extracellular aspartate and glutamate in the striatum of domestic chicken evoked by high potassium or distress: An in vivo microdialysis study. Neurochem. Res. 37, 1730–1737.PubMedGoogle Scholar
  46. 46.
    Zachar, G., Tóth, A. S., Balogh, M., Csillag, A. (2017) Effect of nucleus accumbens lesions on socially motivated behaviour of young domestic chicks. Eur. J. Neurosci. 45, 1606–1612.PubMedGoogle Scholar

Copyright information

© Akadémiai Kiadó Zrt. 2018

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Gergely Zachar
    • 1
    Email author
  • Tamás Jakó
    • 2
  • István Vincze
    • 2
  • Zsolt Wagner
    • 2
  • Tamás Tábi
    • 2
  • Eszter Bálint
    • 1
  • Szilvia Mezey
    • 1
  • Éva Szökő
    • 2
  • András Csillag
    • 1
  1. 1.Department of Anatomy, Histology and EmbryologySemmelweis UniversityBudapestHungary
  2. 2.Department of PharmacodynamicsSemmelweis UniversityBudapestHungary

Personalised recommendations