Glutamate decarboxylase and its isoforms

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

The review summarizes current data on the properties, localization and physiological role of GABA synthesizing enzyme, glutamic acid decarboxylase, in mammalian tissues. Due to the high prevalence of the enzyme in the body’s cells and tissues, at the moment there is a large array of scattered experimental data, which needs to be processed and systematized. Presented data demonstrate the involvement of glutamate decarboxylase in different biochemical and physiological processes of the body. It has been demonstrated that the role of enzyme as the major component of the GABAergic neurotransmission in the central nervous system is the most intensively studied. However, there is only limited information regarding distribution and functional role of glutamate decarboxylase in the peripheral nervous system, and therefore requires additional research.

Full Text

Restricted Access

About the authors

Valeria A. Razenkova

Institute of Experimental Medicine

Author for correspondence.
Email: valeriya.raz@yandex.ru
ORCID iD: 0000-0002-3997-2232
SPIN-code: 8877-8902
Scopus Author ID: 57219609984
ResearcherId: AAH-1333-2021

Junior Research Associate, Department of General and Special Morphology

Russian Federation, 12 Academician Pavlov St., Saint Petersburg, 197022

Dmitrii E. Korzhevskii

Institute of Experimental Medicine

Email: DEK2@yandex.ru
ORCID iD: 0000-0002-2456-8165
SPIN-code: 3252-3029
Scopus Author ID: 12770589000
ResearcherId: C-2206-2012

MD, Dr. Sci. (Med.), Professor of the Russian Academy of Sciences, Head of the Laboratory of Functional Morphology of the Central and Peripheral Nervous System, Department of General and Special Morphology

Russian Federation, 12 Academician Pavlov St., Saint Petersburg, 197022

References

  1. Grimmelikhuijzen CJP, Cazzamali G, Williamson M, et al. Invertebrate Neurohormone GPCRs. In: Encyclopedia of Neuroscience. London: Elsevier; 2009. P. 205–212. doi: 10.1016/B978-008045046-9.01445-5
  2. Gainetdinov RR, Hoener MC, Berry MD. Trace amines and their receptors. Pharmacol Rev. 2018;70(3):549–620. doi: 10.1124/PR.117.015305
  3. Nuñez M, del Olmo A, Calzada J. Biogenic amines. In: Encyclopedia of Food and Health. London: Elsevier; 2016. P. 416–423. doi: 10.1016/B978-0-12-384947-2.00070-2
  4. Kleppner SR, Tobin AJ. GABA. In: Ramachandran VS, ed. Encyclopedia of the Human Brain. Academic Press: New York; 2002. P. 353–367. doi: 10.1016/B0-12-227210-2/00150-3
  5. Davidoff RA. Studies of neurotransmitter actions (GABA, glycine, and convulsants). Res Publ Assoc Res Nerv Ment Dis. 1983;61:53–85.
  6. Magnaghi V, Ballabio M, Consoli A, et al. GABA receptor-mediated effects in the peripheral nervous system: A cross-interaction with neuroactive steroids. J Mol Neurosci. 2006;28(1):89–102. doi: 10.1385/JMN:28:1:89
  7. Tanaka C, Taniyama K. The role of GABA in the peripheral nervous system. In: GABA Outside the CNS. Berlin, Heidelberg: Springer Berlin Heidelberg; 1992. P. 3–17. doi: 10.1007/978-3-642-76915-3_1
  8. Jin Z, Korol SV. GABA signalling in human pancreatic islets. Front Endocrinol (Lausanne). 2023;14:1059110. doi: 10.3389/FENDO.2023.1059110
  9. Al-Kuraishy H, Hussian N, Al-Naimi M, et al. The potential role of pancreatic γ-aminobutyric acid (GABA) in diabetes mellitus: a critical reappraisal. Int J Prev Med. 2021;12(1):19. doi: 10.4103/ijpvm.IJPVM_278_19
  10. Zwanzger P, Rupprecht R. Selective GABAergic treatment for panic? Investigations in experimental panic induction and panic disorder. J Psychiatry Neurosci. 2005;30(3):167–175.
  11. Möhler H. The rise of a new GABA pharmacology. Neuropharmacology. 2011;60(7–8):1042–1049. doi: 10.1016/J.NEUROPHARM.2010.10.020
  12. Suhareva BS, Darij EL, Hristoforov RR. Glutamate decarboxylase: structure and catalytic properties. Uspehi biologicheskoj himii. 2001;41:131–162. (In Russ.)
  13. Braunshtejn AE, Shemjakin MM. Theory on amino acid metabolism processes catalyzed by pyridoxine enzymes. Biohimija. 1953;18(4):393–411. EDN: RSNQOB
  14. Steward FC, Thompson JF, Dent CE. γ-Aminobutyric acid: a constituent of potato tubers? Science. 1949;110:439–440.
  15. Awapara J, Landua AJ, Fuerst R, Seale B. Free gamma-aminobutyric acid in brain. J Biol Chem. 1950;187(1):35–39.
  16. Roberts E, Frankel S. gamma-Aminobutyric acid in brain: its formation from glutamic acid. J Biol Chem. 1950;187(1):55–63.
  17. Udenfriend S. Identification of gamma-aminobutyric acid in brain by the isotope derivative method. J Biol Chem. 1950;187(1):65–69.
  18. Bazemore AW, Elliott KAC, Florey E. Isolation of factor I. J Neurochem. 1957;1(4):334–339. doi: 10.1111/j.1471-4159.1957.tb12090.x
  19. Krnjević K, Schwartz S. Is gamma-aminobutyric acid an inhibitory transmitter? Nature. 1966;211(5056):1372–1374. doi: 10.1038/2111372A0
  20. Kelly JS, Krnjević K. Effects of gamma-aminobutyric acid and glycine on cortical neurons. Nature. 1968;219(5161):1372–1374. doi: 10.1038/2191380A0
  21. Gale EF. The production of amines by bacteria. Biochem J. 1940;34(3):392–413. doi: 10.1042/bj0340392
  22. Gale EF. Amino-acid decarboxylases. Br Med Bull. 1953;9(2):135–137. doi: 10.1093/oxfordjournals.bmb.a074329
  23. Taylor ES, Gale EF. Studies on bacterial amino-acid decarboxylases: 6. Codecarboxylase content and action of inhibitors. Biochem J. 1945;39(1):52–58. doi: 10.1042/BJ0390052
  24. Lichstein HC, Gunsalus IC, Umbreit WW. Function of the vitamin B6 group: pyridoxal phosphate (codecarboxylase) in transamination. J Biol Chem. 1945;161(1):311–320. doi: 10.1016/S0021-9258(17)41545-6
  25. Najjar VA, Fisher J. Studies on L-glutamic acid decarboxylase from Escherichia coli. J Biol Chem. 1954;206(1):215–219.
  26. Shukuya R, Schwert GW. Glutamic acid decarboxylase: I. Isolation procedure and properties of an enzyme. J Biol Chem. 1960;235(6):1649–1652. doi: 10.1016/S0021-9258(19)76856-2
  27. Shukuya R, Schwert GW. Glutamic acid decarboxylase: III. The inactivation of the enzyme at low temperatures. J Biol Chem. 1960;235:1658–1661.
  28. Denner LA, Wu JY. Two forms of rat brain glutamic acid decarboxylase differ in their dependence on free pyridoxal phosphate. J Neurochem. 1985;44(3):957–965. doi: 10.1111/j.1471-4159.1985.tb12910.x
  29. Wu JY, Matsuda T, Roberts E. Purification and characterization of glutamate decarboxylase from mouse brain. J Biol Chem. 1973;248(9):3029–3034. doi: 10.1016/S0021-9258(19)44004-0
  30. Spink DC, Porter TG, Wu SJ, Martin DL. Characterization of three kinetically distinct forms of glutamate decarboxylase from pig brain. Biochem J. 1985;231(3):695–703. doi: 10.1042/BJ2310695
  31. Heinämäki AA, Malila SI, Tolonen KM, et al. Resolution and purification of taurine- and GABA-synthesizing decarboxylases from calf brain. Neurochem Res. 1983;8(2):207–218. doi: 10.1007/BF00963921
  32. Blindermann J M, Maitre M, Ossola L, Mandel P. Purification and some properties of L-glutamate decarboxylase from human brain. Eur J Biochem. 1978;86(1):143–152. doi: 10.1111/j.1432-1033.1978.tb12293.x
  33. Chu WC, Metzler DE. Enzymatically active truncated cat brain glutamate decarboxylase: expression, purification, and absorption spectrum. Arch Biochem Biophys. 1994;313(2):287–295. doi: 10.1006/ABBI.1994.1390
  34. Malashkevich VN, De Biase D, Markovic-Housley Z, et al. Crystallization and preliminary X-ray analysis of the beta-isoform of glutamate decarboxylase from Escherichia coli. Acta Crystallogr D Biol Crystallogr. 1998;54(Pt 5):1020–1022. doi: 10.1107/S0907444998003497
  35. Soghomonian JJ, Martin DL. Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci. 1998;19(12):500–505. doi: 10.1016/S0165-6147(98)01270-X
  36. Fenalti G, Law RHP, Buckle AM, et al. GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop. Nat Struct Mol Biol. 2007;14(4):280–286. doi: 10.1038/nsmb1228
  37. Wu JY, Denner L, Lin CT, Song G. L-Glutamate decarboxylase from brain. Methods Enzymol. 1985;113:3–10. doi: 10.1016/S0076-6879(85)13004-1
  38. Ilg T, Berger M, Noack S, et al. Glutamate decarboxylase of the parasitic arthropods Ctenocephalides felis and Rhipicephalus microplus: Gene identification, cloning, expression, assay development, identification of inhibitors by high throughput screening and comparison with the orthologs from Drosophila melanogaster and mouse. Insect Biochem Mol Biol. 2013;43(2):162–177. doi: 10.1016/J.IBMB.2012.11.001
  39. Astegno A, Capitani G, Dominici P. Functional roles of the hexamer organization of plant glutamate decarboxylase. Biochim Biophys Acta. 2015;1854(9):1229–1237. doi: 10.1016/J.BBAPAP.2015.01.001
  40. Coleman ST, Fang TK, Rovinsky SA, et al. Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J Biol Chem. 2001;276(1):244–250. doi: 10.1074/JBC.M007103200
  41. Sun L, Bai Y, Zhang X, et al. Characterization of three glutamate decarboxylases from Bacillus spp. for efficient γ-aminobutyric acid production. Microb Cell Fact. 2021;20(1):153. doi: 10.1186/S12934-021-01646-8
  42. Boura M, Brensone D, Karatzas KAG. A novel role for the glutamate decarboxylase system in Listeria monocytogenes; protection against oxidative stress. Food Microbiol. 2020;85:103284. doi: 10.1016/J.FM.2019.103284
  43. Petroff OAC. GABA and glutamate in the human brain. Neuroscientist. 2002;8(6):562–573. doi: 10.1177/1073858402238515
  44. Bu DF, Erlander MG, Hitz BC, et al. Two human glutamate decarboxylases, 65-kDa GAD and 67-kDa GAD, are each encoded by a single gene. Proc Natl Acad Sci. 1992;89(6):2115–2119. doi: 10.1073/PNAS.89.6.2115
  45. Kanaani J, Diacovo MJ, El-Husseini AED, et al. Palmitoylation controls trafficking of GAD65 from Golgi membranes to axon-specific endosomes and a Rab5a-dependent pathway to presynaptic clusters. J Cell Sci. 2004;117(Pt 10):2001–2013. doi: 10.1242/JCS.01030
  46. Namchuk M, Lindsay LA, Turck CW, et al. Phosphorylation of serine residues 3, 6, 10, and 13 distinguishes membrane anchored from soluble glutamic acid decarboxylase 65 and is restricted to glutamic acid decarboxylase 65alpha. J Biol Chem. 1997;272(3): 1548–1557. doi: 10.1074/JBC.272.3.1548
  47. Solimena M, Aggujaro D, Muntzel C, et al. Association of GAD-65, but not of GAD-67, with the Golgi complex of transfected Chinese hamster ovary cells mediated by the N-terminal region. Proc Natl Acad Sci. 1993;90(7):3073–3077. doi: 10.1073/PNAS.90.7.3073
  48. Lee S-E, Lee Y, Lee GH. The regulation of glutamic acid decarboxylases in GABA neurotransmission in the brain. Arch Pharm Res. 2019;42(12): 1031–1039. doi: 10.1007/s12272-019-01196-z
  49. Kanaani J, Cianciaruso C, Phelps EA, et al. Compartmentalization of GABA synthesis by GAD67 differs between pancreatic beta cells and neurons. PLoS One. 2015;10(2):e0117130. doi: 10.1371/journal.pone.0117130
  50. Kanaani J, Kolibachuk J, Martinez H, Baekkeskov S. Two distinct mechanisms target GAD67 to vesicular pathways and presynaptic clusters. J Cell Biol. 2010;190(5):911–925. doi: 10.1083/JCB.200912101
  51. Porter TG, Spink DC, Martin SB, Martin DL. Transaminations catalysed by brain glutamate decarboxylase. Biochem J. 1985;231(3):705–712. doi: 10.1042/BJ2310705
  52. Battaglioli G, Liu H, Martin DL. Kinetic differences between the isoforms of glutamate decarboxylase: Implications for the regulation of GABA synthesis. J Neurochem. 2003;86(4):879–887. doi: 10.1046/j.1471-4159.2003.01910.x
  53. Szabo G, Katarova Z, Greenspan R. Distinct protein forms are produced from alternatively spliced bicistronic glutamic acid decarboxylase mRNAs during development. Mol Cell Biol. 1994;14(11):7535. doi: 10.1128/MCB.14.11.7535
  54. Chessler SD, Lernmark Å. Alternative splicing of GAD67 results in the synthesis of a third form of glutamic-acid decarboxylase in human islets and other non-neural tissues. J Biol Chem. 2000;275(7):5188–5192. doi: 10.1074/JBC.275.7.5188
  55. Korpershoek E, Verwest AM, Ijzendoorn Y, et al. Expression of GAD67 and novel GAD67 splice variants during human fetal pancreas development: GAD67 expression in the fetal pancreas. Endocr Pathol. 2007;18(1):31–36. doi: 10.1007/S12022-007-0003-Y
  56. Popp A, Urbach A, Witte OW, Frahm C. Adult and embryonic GAD transcripts are spatiotemporally regulated during postnatal development in the rat brain. PLoS One. 2009;4(2):e4371. doi: 10.1371/JOURNAL.PONE.0004371
  57. Bosma PT, Blázquez M, Collins MA, et al. Multiplicity of glutamic acid decarboxylases (GAD) in vertebrates: molecular phylogeny and evidence for a new GAD paralog. Mol Biol Evol. 1999;16(3):397–404. doi: 10.1093/OXFORDJOURNALS.MOLBEV.A026120
  58. Grone BP, Maruska KP. Three distinct glutamate decarboxylase genes in vertebrates. Sci Rep. 2016;6:30507. doi: 10.1038/SREP30507
  59. Agner C. GABA in the nervous system: The view at fifty years. J Neurol Sci. 2001;190(1–2):101. doi: 10.1016/S0022-510X(01)00582-2
  60. Best JG, Stagg CJ, Dennis A. Other significant metabolites: myo-inositol, GABA, glutamine, and lactate. In: Stagg C, Rothman D, editors. Magnetic Resonance Spectroscopy: Tools for Neuroscience Research and Emerging Clinical Applications. New York: Academic Press; 2014. P. 122–138.
  61. Pinal CS, Tobin AJ. Uniqueness and redundancy in GABA production. Perspect Dev Neurobiol. 1998;5(2–3):109–118.
  62. Martin DL, Rimvall K. Regulation of γ-aminobutyric acid synthesis in the brain. J Neurochem. 1993;60(2):395–407. doi: 10.1111/j.1471-4159.1993.tb03165.x
  63. Tavazzani E, Tritto S, Spaiardi P, et al. Glutamic acid decarboxylase 67 expression by a distinct population of mouse vestibular supporting cells. Front Cell Neurosci. 2014;8:110972. doi: 10.3389/fncel.2014.00428
  64. Holman HA, Wan Y, Rabbitt RD. Developmental GAD2 expression reveals progenitor-like cells with calcium waves in mammalian crista ampullaris. iScience. 2020;23(8):101407. doi: 10.1016/J.ISCI.2020.101407
  65. Tochitani S, Kondo S. Immunoreactivity for GABA, GAD65, GAD67 and Bestrophin-1 in the meninges and the choroid plexus: implications for non-neuronal sources for GABA in the developing mouse brain. PLoS One. 2013;8(2):e56901. doi: 10.1371/journal.pone.0056901
  66. Lee S, Yoon BE, Berglund K, et al. Channel-mediated tonic GABA release from glia. Science. 2010;330(6005):790–796. doi: 10.1126/science.1184334
  67. Razenkova VA, Korzhevskii DE. Morphological changes in GABAergic structures of the rat brain during postnatal development. Neurochem J. 2022;16(1):58–67. EDN: EZJMQC doi: 10.31857/S1027813322010101
  68. Erdö SL, Wolff JR. γ-Aminobutyric acid outside the mammalian brain. J Neurochem. 1990;54(2):363–372. doi: 10.1111/j.1471-4159.1990.tb01882.x
  69. Sakai Y, Hira Y, Matsushima S. Central GABAergic innervation of the mammalian pineal gland: A light and electron microscopic immunocytochemical investigation in rodent and nonrodent species. J Comp Neurol. 2001;430(1):72–84. doi: 10.1002/1096-9861(20010129)430:1<72::AID-CNE1015>3.0.CO;2-T
  70. Yu H, Benitez SG, Jung SR, et al. GABAergic signaling in the rat pineal gland. J Pineal Res. 2016;61(1):69–81. doi: 10.1111/JPI.12328
  71. Li S, Kumar P, Joshee S, et al. Endothelial cell-derived GABA signaling modulates neuronal migration and postnatal behavior. Cell Res. 2018;28(2):221–248. doi: 10.1038/cr.2017.135
  72. Sen S, Roy S, Bandyopadhyay G, et al. γ-Aminobutyric acid is synthesized and released by the endothelium. Circ Res. 2016;119(5):621–634. doi: 10.1161/CIRCRESAHA.116.308645
  73. Todd AJ, Watt C, Spike RC, Sieghart W. Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci. 1996;16(3):974–982. doi: 10.1523/JNEUROSCI.16-03-00974.1996
  74. Mackie M, Hughes DI, Maxwell DJ, et al. Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neuroscience. 2003;119(2):461–472. doi: 10.1016/s0306-4522(03)00174-x
  75. Shimizu-Okabe C, Kobayashi S, Kim J, et al. Developmental formation of the GABAergic and glycinergic networks in the mouse spinal cord. Int J Mol Sci. 2022;23(2):834. doi: 10.3390/ijms23020834
  76. Désarmenien M, Feltz P, Occhipinti G, et al. Coexistence of GABAA and GABAB receptors on A delta and C primary afferents. Br J Pharmacol. 1984;81(2):327–333. doi: 10.1111/j.1476-5381.1984.tb10082.x
  77. Liske S, Morris ME. Extrasynaptic effects of GABA (gamma-aminobutyric acid) agonists on myelinated axons of peripheral nerve. Can J Physiol Pharmacol. 1994;72(4):368–374. doi: 10.1139/Y94-054
  78. Magnaghi V, Ballabio M, Cavarretta ITR, et al. GABAB receptors in Schwann cells influence proliferation and myelin protein expression. Eur J Neurosci. 2004;19(10):2641–2649. doi: 10.1111/J.0953-816X.2004.03368.x
  79. Magnaghi V, Parducz A, Frasca A, et al. GABA synthesis in Schwann cells is induced by the neuroactive steroid allopregnanolone. J Neurochem. 2010;112(4):980–990. doi: 10.1111/J.1471-4159.2009.06512.x
  80. Schousboe A, Waagepetersen HS. Gamma-Aminobutyric Acid (GABA). In: Reference Module in Neuroscience and Biobehavioral Psychology. 2017. P. 511–515. doi: 10.1016/B978-0-12-809324-5.02341-5
  81. Vandenbergh DJ, Mori N, Anderson DJ. Co-expression of multiple neurotransmitter enzyme genes in normal and immortalized sympathoadrenal progenitor cells. Dev Biol. 1991;148(1):10–22. doi: 10.1016/0012-1606(91)90313-R
  82. Häppölä O, Karhula T, Päivärinta H, et al. L-glutamate decarboxylase immunoreactivity in the sympathoadrenal system. In: GABA Outside the CNS. Berlin, Heidelberg: Springer Berlin Heidelberg; 1992 P. 65–82. doi: 10.1007/978-3-642-76915-3_5
  83. Tillakaratne NJK, Medina-Kauwe L, Gibson KM. Gamma-aminobutyric acid (GABA) metabolism in mammalian neural and nonneural tissues. Comp Biochem Physiol Part A Physiol. 1995;112(2):247–263. doi: 10.1016/0300-9629(95)00099-2
  84. Metzeler K, Agoston A, Gratzl M. An intrinsic gamma-aminobutyric acid (GABA)ergic system in the adrenal cortex: findings from human and rat adrenal glands and the NCI-H295R cell line. Endocrinology. 2004;145(5):2402–2411. doi: 10.1210/en.2003-1413
  85. Harada K, Matsuoka H, Fujihara H, et al. GABA signaling and neuroactive steroids in adrenal medullary chromaffin cells. Front Cell Neurosci. 2016;10:100. doi: 10.3389/fncel.2016.00100
  86. Geigerseder C, Doepner R, Thalhammer A, et al. Evidence for a GABAergic system in rodent and human testis: local GABA production and GABA receptors. Neuroendocrinology. 2003;77(5):314–323. doi: 10.1159/000070897
  87. Doepner RFG, Geigerseder C, Frungieri MB, et al. Insights into GABA receptor signalling in TM3 Leydig cells. Neuroendocrinology. 2005;81(6):381–390. doi: 10.1159/000089556
  88. Erdö SL, Joo F, Wolff JR. Immunohistochemical localization of glutamate decarboxylase in the rat oviduct and ovary: further evidence for non-neural GABA systems. Cell Tissue Res. 1989;255(2):431–434. doi: 10.1007/BF00224128
  89. Pléau JM, Esling A, Geutkens S, et al. Pancreatic hormone and glutamic acid decarboxylase expression in the mouse thymus: a real-time PCR study. Biochem Biophys Res Commun. 2001;283(4):843–848. doi: 10.1006/BBRC.2001.4884
  90. Maemura K, Yanagawa Y, Obata K, et al. Antigen-presenting cells expressing glutamate decarboxylase 67 were identified as epithelial cells in glutamate decarboxylase 67-GFP knock-in mouse thymus. Tissue Antigens. 2006;67(3):198–206. doi: 10.1111/J.1399-0039.2006.00548.x
  91. Breed ER, Lee ST, Hogquist KA. Directing T cell fate: how thymic antigen presenting cells coordinate thymocyte selection. Semin Cell Dev Biol. 2018;84:2. doi: 10.1016/J.SEMCDB.2017.07.045
  92. Razenkova VA, Korzhevskii DE. Visualisation of GABAergic neurons and synapses in the rat brain using immunohistochemistry for two forms of glutamate decarboxylase. Medical academic journal. 2021;21(2):63–73. EDN: UYCYLC doi: 10.17816/MAJ70770
  93. Korzhevskii DE, Grigor’ev IP, Gusel’nikova VV, et al. Immunohistochemical markers for neurobiology. Medical academic journal. 2020;19(4):7–24. EDN: BQAXWZ doi: 10.17816/MAJ16548
  94. Kubota Y. Untangling GABAergic wiring in the cortical microcircuit. Curr Opin Neurobiol. 2014;26:7–14. doi: 10.1016/j.conb.2013.10.003
  95. Mower GD, Guo Y. Comparison of the expression of two forms of glutamic acid decarboxylase (GAD67 and GAD65) in the visual cortex of normal and dark-reared cats. Dev Brain Res. 2001;126(1):65–74. doi: 10.1016/S0165-3806(00)00139-5
  96. Houser CR, Hendry SHC, Jones EG, Vaughn JE. Morphological diversity of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. J Neurocytol. 1983;12(4):617–638. doi: 10.1007/BF01181527
  97. Warm D, Schroer J, Sinning A. GABAergic interneurons in early brain development: conducting and orchestrated by cortical network activity. Front Mol Neurosci. 2022;14:807969. doi: 10.3389/FNMOL.2021.807969
  98. Xu G, Broadbelt KG, Haynes RL, et al. Late development of the GABAergic system in the human cerebral cortex and white matter. J Neuropathol Exp Neurol. 2011;70(10):841–858. doi: 10.1097/NEN.0b013e31822f471c
  99. Schwarzer C, Berresheim U, Pirker S, et al. Distribution of the major gamma-aminobutyric acid(A) receptor subunits in the basal ganglia and associated limbic brain areas of the adult rat. J Comp Neurol. 2001;433(4):526–549. doi: 10.1002/CNE.1158
  100. Kim JS, Bak IJ, Hassler R, Okada Y. Role of γ-aminobutyric acid (GABA) in the extrapyramidal motor system. 2. Some evidence for the existence of a type of GABA-rich strio-nigral neurons. Exp Brain Res. 1971;14(1):95–104. doi: 10.1007/bf00234913
  101. Shabanov PD, Lebedev AA. Structural and functional organization of the extended amygdala system and its role in reinforcement. Reviews on clinical pharmacology and drug therapy. 2007;5(1):2–16. (In Russ.) EDN: HZLMGD
  102. Bon YeI, Zimatkin SM. Structure and development of the rat hyppocampus. Journal of the Grodno State Medical University. 2018;16(2):132–138. EDN: XMLIKL doi: 10.25298/2221-8785-2018-16-2-132-138
  103. Fukuda T, Heizmann CW, Kosaka T. Quantitative analysis of GAD65 and GAD67 immunoreactivities in somata of GABAergic neurons in the mouse hippocampus proper (CA1 and CA3 regions), with special reference to parvalbumin-containing neurons. Brain Res. 1997;764(1–2):237–243. doi: 10.1016/S0006-8993(97)00683-5
  104. Wang X, Gao F, Zhu J, et al. Immunofluorescently labeling glutamic acid decarboxylase 65 coupled with confocal imaging for identifying GABAergic somata in the rat dentate gyrus — A comparison with labeling glutamic acid decarboxylase 67. J Chem Neuroanat. 2014;61–62:51–63. doi: 10.1016/j.jchemneu.2014.07.002
  105. Kajita Y, Mushiake H. Heterogeneous GAD65 expression in subtypes of GABAergic neurons across layers of the cerebral cortex and hippocampus. Front Behav Neurosci. 2021;15:236. doi: 10.3389/FNBEH.2021.750869
  106. Miwa H, Kobayashi K, Hirai S, et al. GAD67-mediated GABA synthesis and signaling impinges on directing basket cell axonal projections toward Purkinje Cells in the cerebellum. Cerebellum. 2021;21(6):905–919. doi: 10.1007/s12311-021-01334-8
  107. Hirono M, Saitow F, Kudo M, et al. Cerebellar globular cells receive monoaminergic excitation and monosynaptic inhibition from Purkinje cells. PLoS One. 2012;7(1):e29663. doi: 10.1371/journal.pone.0029663
  108. Korzhevskiy DE, Gilerovich YeG, Kirik OV, et al. Simultaneous demonstration of glutamate decarboxylase and synaptophysin in paraffin sections of rat cerebellum. Morfologiya. 2015;147(1):74–77. EDN: TIJLSJ
  109. Tamamaki N, Yanagawa Y, Tomioka R, et al. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol. 2003;467(1):60–79. doi: 10.1002/cne.10905
  110. Colasante G, Collombat P, Raimondi V, et al. Arx Is a direct target of Dlx2 and thereby contributes to the tangential migration of GABAergic interneurons. J Neurosci. 2008;28(42):10674–10686. doi: 10.1523/JNEUROSCI.1283-08.2008

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 74760 от 29.12.2018 г.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies