Sains Malaysiana 42(11)(2013): 1619–1624

 

Glutamatergic Transmission in the Avian Brain: Model for

Human Excitotoxicity Disorders Study

(Penghantaran Glutamatergik dalam Otak Burung: Model bagi Kajian Gangguan Eksitotoksisiti Manusia)

 

M.R. ISLAM1, Y. ATOJI2& J.M. ABDULLAH1*

1Department of Neurosciences, School of Medical Sciences, Universiti Sains Malaysia
16150 Kubang Kerian, Kelantan, Malaysia

2Laboratory of Veterinary Anatomy, Faculty of Applied Biological Sciences
Gifu University, Gifu 501-1193, Japan

Received: 14 June 2012 /Accepted: 17 March 2013

 

Diserahkan: 14 Jun 2012 /Diterima: 17 Mac 2013

 

 

ABSTRACT

Glutamatergic dysfunction has been suggested as a possible substrate of the pathophysiology of many neurodegenerative diseases, specifically since glutamatergic transmission is severely altered by the early degeneration of cortico-cortical connections and hippocampal projections in Alzheimer’s disease, schizophrenia and Huntington’s disease in humans. Of the multiple genes, vesicular glutamate transporters, glutamate receptors and excitatory amino acid transporters have a significant role in glutamatergic transmissions. The regional differences of glutamatergic neurons and glutamate receptor neurons suggest many glutamatergic projections in the avian brain. Glutamatergic target areas are expected to show high activity of glutamate transporters that remove the released glutamate from the synaptic clefts. The distribution of the glutamate-related genes indicates that many glutamatergic transmissions exist in the avian brain. This review provide insights of glutamatergic circuits in birds particularly in the pallial organization of glutamatergic neurons and connection with the striatum and hippocampal-septal pathway and comparison with those of mammalian brain which are responsible for Alzheimer’s disease, schizophrenia and Huntington’s disease in humans.

 

Keywords: Central nervous system, glutamate receptors, mRNA expression, neurons, vesicular glutamate transporters

 

 

ABSTRAK

Disfungsi Glutamatergik telah dicadangkan sebagai substrat patofisiologi yang mungkin untuk penyakit neurodegeneratif, khususnya kerana penghantaran glutamatergik banyak diubah oleh degenerasi awal sambungan kortikal kortiko dan unjuran hipokampal dalam penyakit Alzheimer, skizofrenia dan penyakit Huntington pada manusia. Daripada pelbagai gen yang ada, pembawa glutamat vesikular, reseptor glutamat dan pembawa asid amino berangsang mempunyai peranan penting dalam transmisi glutamatergik. Perbezaan serantau neuron glutamatergik dan neuron reseptor glutamat mencadangkan terdapat banyak unjuran glutamatergik wujud di dalam otak burung. Kawasan sasaran Glutamatergik dijangka menunjukkan aktiviti pengangkutan glutamat yang tinggi bagi membuang glutamat yang dikeluarkan dari celahan sinaptik. Taburan gen yang berkaitan glutamat menunjukkan bahawa banyak penghantaran glutamatergik wujud di dalam otak burung. Ulasan ini menyediakan gambaran tentang litar glutamatergik dalam burung terutamanya dalam organisasi palial neuron glutamatergik dan perkaitan dengan striatum dan laluan septal hipokampal serta perbandingan dengan otak mamalia yang bertanggungjawab bagi penyakit Alzheimer, skizofrenia dan penyakit Huntington pada manusia.

Kata kunci: Neuron; pembawa glutamat vesikular; reseptor glutamat; sistem saraf pusat; ungkapan mRNA

RUJUKAN

Aihara, Y., Mashima, H., Onda, H., Hisano, S., Kasuya, H., Hori, T., Yamada, S., Tomura, H., Yamada, Y., Inoue, I., Kojima, I. & Takada, J. 2000. Molecular cloning of a novel brain-type Na+-dependent inorganic phosphate cotransporter. Journal of Neurochemistry 74: 2622-2625.

Arriza, J.L., Eliasof, S., Kavanaugh, M.P. & Amara, S.G. 1997. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proceeding for National Academy of Science U.S.A. 94: 4155-4160.

Atoji, Y. 2011. Immunohistochemical localization of vesicular glutamate transporter 2 (vGluT2) in the central nervous system of the pigeon (Columba livia). Journal of Comparative Neurology 519: 2887-2905.

Atoji, Y. & Islam, M.R. 2009. Distribution of glutamate transporter 1 mRNA in the central nervous system of the pigeon (Columba livia). Journal of Chemical Neuroanatomy 37: 234-244.

Atoji, Y. & Wild, J.M. 2004. Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions. Journal of Comparative Neurology 475: 426-461.

Atoji, Y., Saito, S. & Wild, J.M. 2006. Fiber connections of the compact division of the posterior pallial amygda and lateral part of the bed nucleus of the stria terminalis in the pigeon (Columba livia). Journal of Comparative Neurology 499: 161-182.

Bai, L., Xu, H., Collins, J.F. & Ghishan, F.K. 2001. Molecular and functional analysis of a novel neuronal vesicular glutamate transporter. Journal of Biological Chemistry 276: 36764- 36769.

Barroso-Chinea, P., Castle, M., Aymerich, M.S., Péres-Manso, M., Erro, E., Tuñon, T. & Lanciego, J.L. 2007. Expression of the mRNAs encoding for the vesicular glutamate transporters 1 and 2 in the rat thalamus. Journal of Comparative Neurology 501: 703-715.

Berger, U.V. & Hediger, M.A. 1998. Comparative analysis of glutamate transporter expression in rat brain using differential double in situ hybridization. Anatomy and Embryology 198: 13-30.

Broman, J., Rinvik, E., Sassoe-Pognetto, M., Shandiz, H.K. & Ottersen, O.P. 2004. Glutamate. In The Rat Nervous System. 3rd ed., edited by Paxinos, G. San Diego: Elsevier Academic Press. pp 1269-1292.

Brustovetsky, T., Purl, K., Young, A., Shimizu, K. & Dubinsky, M. 2004. Dearth of glutamate transporters contributes to striatal excitotoxicity. Experimental Neurology 189: 222-230.

Cepeda, C., Wu, N., André, V.M., Cummings, D.M. & Levine, M.S. 2007. The corticostriatal pathway in Huntington’s disease. Progressive Neurobiology 81: 253-271.

Collingridge, G.L. & Lester, R.A.J. 1989. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacology Review 40: 143-210.

Conti, F., Minelli, A. & Brecha, N.C. 1994. Cellular localization and laminar distribution of AMPA glutamate receptor subunits mRNAs and proteins in the rat cerebral cortex. Journal of Comparative Neurology 350: 241-259.

Cornil, C., Foidart, A., Minet, A. & Balthazart, J. 2000. Immunohistochemical localization of ionotropic glutamate receptors subunits in the adult quail forebrain. Journal of Comparative Neurology 428: 577-608.

Danbolt, N.C., Storm-Mathisen, J. & Kanner, B.I. 1992. An [Na++K+] coupled L-glutamate transporter purified from rat brain is located in glial cell processes. Neuroscience 51: 295-310.

Difiglia, M. 1990. Excitotoxic injury of the neostriatum: A model for Huntington’s disease. Trends Neuroscience 13: 286-289.

Eastwood, S.L. & Harrison, P.J. 2005. Decreased expression of vesicular glutamate transporter 1 and complexin II mRNAs in schizophrenia: Further evidence for a synaptic pathology affecting glutamate neurons. Schizophrenia Research 73: 159-172.

Fairman, W.A., Vandenberg, R.J., Arriza, J.L., Kavanaugh, M.P. & Amara, S.G. 1995. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375: 599-603.

Francis, P.T., Sims, N.R., Procter, A.W. & Bowen, D.M. 1993. Cortical pyramidal neuron loss may cause glutamatergic hypoactivity and cognitive impairment in Alzheimer’s disease: Investigative and therapeutic perspectives. Journal of Neurochemistry 60: 1589-1604.

Fremeau, R.T. Jr., Troyer, M.D., Pahner, I., Nygaard, G.O., Tran, C.H., Reimer, R.J., Bellocchio, E.E., Fortin, D., Storm-Mathisen, J. & Edwards, R.H. 2001. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31: 247-260.

Genelassvili, G. & Schousboe, A. 1998. Cellular distribution and kinetic properties of high-affinity glutamate transporters. Brain Research Bulletin 45: 233-238.

Gerfen, C.R. 2004. Basal Ganglia. In The Rat Nervous System. 3rd ed., edited by Paxinos, G. San Diego: Elsevier Academic Press.

Gras, C., Herzog, E., Bellenchi, G.C., Bernard, V., Ravassard, P., Pohl, M., Gasnier, B., Giros, B. & El Mestikawy, S. 2002). A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. Journal of Neuroscience 22: 5442-5451.

Headley, P.M. & Grillner, S. 1990. Excitatory amino acids and synaptic transmission: The evidence for a physiological function. Trends Pharmacological Science 11: 205-211.

Herzog, E., Gilchrist, J., Gras, C., Muzerelle, A., Ravassard, P., Giros, B., Gaspar, P. & El Mestikawy, S. 2004. Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123: 983-1002.

Hisano, S., Hoshi, K., Ikeda, Y., Maruyama, D., Kanemoto, M., Ichijo, H., Kojima, I., Takeda, J. & Nogami, H. 2000. Regional expression of a gene encoding a neuron-specific Na+-dependent inorganic phosphate cotransporter (DNPI) in the rat forebrain. Molecular Brain Research 83: 34-43.

Islam, M.R. & Atoji, Y. 2008. Distribution of vesicular glutamate transporter 2 and glutamate receptor 1 mRNA in the central nervous system of the pigeon (Columba livia). Journal of Comparative Neurology 511: 658-677.

Kanai, Y. & Hediger, M.A. 1992. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360: 467-471.

Kanai, Y. & Hediger, M.A. 2004. The glutamate/neutral amino acid transport family SLC1: molecular, physiological and pharmacological aspects. European Journal of Physiology 447: 469-479.

Kaneko, T., Fujiyama, F. & Hioki, H. 2002. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. Journal of Comparative Neurology 444: 39-62.

Keinänen, K., Wisden, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T.A., Sakmann, B. & Seeburg, P.H. 1990. A family of AMPA-selective glutamate receptors. Science 249: 556-560.

Kerwin, R., Patel, S. & Meldrum, B. 1990. Quantitative auto radiographic analysis of glutamate binding sites in the hippocampal formation in normal and schizophrenic brain post mortem. Neuroscience 39: 25-32.

Kim, A.H., Kerchner, G.A. & Choi, D.W. 2002). Blocking Excitotoxicity. In CNS Neuroproteciton, edited by Marcoux, F.W. & Choi, D.W. New York: Springer.

Laverghetta, A.V., Toledo, C.A.B., Veenman, C.L., Yamamoto, K., Wang, H. & Reiner, A. 2006. Cellular localization of AMPA type glutamate receptor subunits in the basal ganglia of pigeons (Columba livia). Brain Behavior Evolution 67: 10-38.

Lehre, K.P., Levy, L.M., Ottersen, O.P., Storm-Mathisen, J. & Danbolt, N.C. 1995. Differential expression of two glial glutamate transporters in the rat bran: Quantitative and immunocytochemical observations. Journal of Neuroscience 15: 1835-1853.

Martin, L.J., Blackstone, C.D., Levey, A.I., Huganir, R.L. & Price, D.L. 1993. AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53: 327-358.

McShea, A., Zelasko, D.A., Gerst, J.L. & Smith, M.A. 1999. Signal transduction abnormalities in Alzheimer’s disease: Evidence of a pathogenic stimuli. Brain Research 815: 237–242.

Meador-Woodruff, J.H. & Healy, D.J. 2000. Glutamate receptor expression in schizophrenic brain. Brain Research Review 31: 288-294.

Medina, L. 2007. Do birds and reptiles possess homologues of mammalian visual, somatosensory, and motor cortices? In Evolution of Nervous Systems. A Comprehensive Reference, edited by Kaas, J.H. San Diego: Elsevier Academic Press.

Ni, B., Rosteck, P.R. Jr., Nadi, N.S. & Paul, S.M. 1994. Cloning and expression of a cDNA encoding a brain-specific Na+- dependent inorganic phosphate cotransporter. Proceeding of National Academy of Science, U.S.A. 91: 5607-5611.

Noga, J.T., Hyde, T.M., Herman, M.M., Spurney, C.F., Bigelow, L.B., Weinberger, D.R. & Kleinman, J.E. 1997. Glutamate receptors in the postmortem striatum of schizophrenic, suicide, and control brains. Synapse 27: 168-176.

Obrenovitch, T.P. & Urenjak, J. 1997. Is high extracellular glutamate the key to excitotoxicity in traumatic brain injury? Journal of Neurotrauma 14: 677-698.

Ottiger, H.P., Gerfin-Moser, A., Del Principe, F., Dutly, F. & Streit, P. 1995. Molecular cloning and differential expression patterns of avian glutamate receptor mRNAs. Journal of Neurochemistry 64: 2413-2426.

Perry, G., Roder, H. & Nunomura, A. 1999. Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. NeuroReport 10: 2411-2415.

Pines, G., Danbolt, N.C., Bjørås, M., Zhang, Y., Bandahan, A., Eide, L., Koepsell, H., Storm-Mathisen, J., Seeberg, E. & Kanner, B.I. 1992. Cloning and expression of a rat brain L-glutamate transporter. Nature 360: 464-467.

Rogers, S.W., Hughes, T.E., Hollmann, M., Gasic, G.P., Deneris, E.S. & Heinemann, S. 1991. The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain. Journal of Neuroscience 11: 2713-2724.

Sato, K., Kiyama, H. & Tohyama, M. 1993. The differential expression patterns of messenger RNAs encoding non-N-methyl-D-aspartate glutamate receptor subunits (GluR1–4) in the rat brain. Neuroscience 52: 515-539.

Schmitt, A., Asan, E., Lesch, K.P. & Kugler, P. 2002. A splice variant of glutamate transporter GLT1/EAAT2 expressed in neurons: Cloning and localization in rat nervous system. Neuroscience 109: 45-61.

Smith, R.E., Haroutunian, V., Davis, K.L. & Meador-Woodruff, J.H. 2001. Vesicular glutamate transporter transcript expression in the thalamus in schizophrenia. NeuroReport 12: 2885-2889.

Storck, T., Schutle, S., Hofmann, K. & Stoffel, W. 1992. Structure, expression, and functional analysis of a Na+-dependent glutamate/aspartate transporter from rat brain. Proceeding of National Academy of Science, U.S.A. 89: 10955-10959.

Takamori, S. 2006. VGLUTs: ‘exciting’ times for glutamatergic research? Neuroscience Research 55: 343-351.

Takamori, S., Rhee, J.S., Rosenmund, C. & Jahn, R. 2000. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407: 189-194.

Theiss, C., Hellmann, B. & Güntürkün, O. 1998. The differential distribution of AMPA-receptor subunits in the tectofugal system of the pigeon. Brain Research 785: 114-128.

Toledo, C.A.B., Pezzini, R., Santos, R.C. & Britto, L.R.G. 2002. Expression of AMPA-type glutamate receptors in pretectal nuclei of the chick brain. Brain Research Bulletin 57: 359- 361.

Torp, R., Hoover, F., Danbolt, N.C., Storm-Mathisen, J. & Ottersen, O.P. 1997. Differential distribution of the glutamate transporters GLT1 and rEAAC1 in rat cerebral cortex and thalamus: An in situ hybridization analysis. Anatomy & Embryology 195: 317-326.

Veenman, C.L., Wild, J.M. & Reiner, A. 1995. Organization of the avian ‘corticostriatal’ projection system: A retrograde and anterograde pathway tracing study in pigeons. Journal of Comparative Neurology 354: 87-126.

Wada, K., Sakaguchi, H., Jarvis, E.D. & Hagiwara, M. 2004. Differential expression of glutamate receptors in avian neural pathways for learned vocalization. Journal of Comparative Neurology 476: 44-64.

Witter, M.P. & Amaral, D.G. 2004. Hippocampal Formation. In The Rat Nervous System 3rd ed., edited by Paxinos, G. San Diego: Elsevier Academic Press.

Zhu, X., Rottkamp, C.A. & Hartzler, A. 2001. Activation of MKK6, an upstream activator of p38, in Alzheimer’s disease. Journal of Neurochemistry 79: 311-318.

 

 

*Pengarang untuk surat-menyurat: email: brainsciences@gmail.com

 

 

 

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