Expression of the glycinergic system during the course of embryonic development in the mouse spinal cord and its co-localization with GABA immunoreactivity

Journal of Comparative Neurology

Volumn 496, Issue 6, 2006, Pages 832-846

  Allain, Anne Emilie ^a   Baïri, Alexia ^a   Meyrand, Pierre ^a   Branchereau, Pascal ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

GABA; Glycine; Inhibitory amino acid; Ontogeny

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; GLYCINE RECEPTOR;

ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; CELL POPULATION; EMBRYO DEVELOPMENT; GABAERGIC TRANSMISSION; IMMUNOREACTIVITY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMITTER RELEASE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPINAL CORD; SPINAL CORD VENTRAL HORN; TISSUE DISTRIBUTION;

EID: 33646496149     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.20967     Document Type: Article

References (74)

1. Allain AE, Bairi A, Meyrand P, Branchereau P. 2004. Ontogenic changes of the GABAergic system in the embryonic mouse spinal cord. Brain Res 1000:134-147.
2. Allain AE, Meyrand P, Branchereau P. 2005. Ontogenic changes of the spinal GABAergic cell population are controlled by the serotonin (5-HT) system: implication of 5-HT1 receptor family. J Neurosci 25:8714-8724.
3. Antal M, Berki AC, Horvath L, O'Donovau MJ. 1994. Developmental changes in the distribution of gamma-aminobutyric acid-immunoreactive neurons in the embryonic chick lumbosacral spinal cord. J Comp Neurol 343:228-236.
4. Aoki E, Semba R, Kashiwamata S. 1989. When does GABA-like immunoreactivity appear in the rat cerebellar GABAergic neurons? Brain Res 502:245-251.
5. Aprison MH. 1990. The discovery of the neurotransmitter role of glycine. In: Ottersen OP, Storm-Mathisen J, editors. Glycine neurotransmission. New York: John Wiley. p 1-13.
6. Baccei ML, Fitzgerald M. 2004. Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn. J Neurosci 24:4749-4757.
7. Becker CM. 1992. Selective neurotoxicity: convulsants acting at the inhibitory glycine receptors. In: Herken HF, Hucho F, editors. Handbook of experimental pharmacology. New York: Springer. p 539-575.
8. Behar TN, Schaffner AE, Colton CA, Somogyi R, Olah Z, Lehel C, Barker JL. 1994. GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons. J Neurosci 14:29-38.
9. Berki AC, O'Donovan MJ, Antal M. 1995. Developmental expression of glycine immunoreactivity and its colocalization with GABA in the embryonic chick lumbosacral spinal cord. J Comp Neurol 362:583-596.
10. Beyer C, Roberts LA, Komisaruk BR. 1985. Hyperalgesia induced by altered glycinergic activity at the spinal cord. Life Sci 37:875-882.
11. Binor E, Heathcote RD. 2001. Development of GABA-immunoreactive neuron patterning in the spinal cord. J Comp Neurol 438:1-11.
12. Bohlhalter S, Mohler H, Fritschy JM. 1994. Inhibitory neurotransmission in rat spinal cord: co-localization of glycine- and GABAA-receptors at GABAergic synaptic contacts demonstrated by triple immunofluorescence staining. Brain Res 642:59-69.
13. Branchereau P, Morin D, Bonnot A, Ballion B, Chapron J, Viala D. 2000. Development of lumbar rhythmic networks: from embryonic to neonate locomotor-like patterns in the mouse. Brain Res Bull 53:711-718.
14. Branchereau P, Chapron J, Meyrand P. 2002. Descending 5-hydroxytryptamine raphe inputs repress the expression of serotonergic neurons and slow the maturation of inhibitory systems in mouse embryonic spinal cord. J Neurosci 22:2598-2606.
15. Burger PM, Hell J, Mehl E, Krasel C, Lottspeich F, Jahn R. 1991. GABA and glycine in synaptic vesicles: storage and transport characteristics. Neuron 7:287-293.
16. Chronwall B, Wolff JR. 1980. Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat. J Comp Neurol 190:187-208.
17. Cobas A, Fairen A, Alvarez-Bolado G, Sanchez MP. 1991. Prenatal development of the intrinsic neurons of the rat neocortex: a comparative study of the distribution of GABA-immunoreactive cells and the GABAA receptor. Neuroscience 40:375-397.
18. Code RA, Burd GD, Rubel EW. 1989. Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J Comp Neurol 284:504-518.
19. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15.
20. Colin I, Rostaing P, Augustin A, Triller A. 1998. Localization of components of glycinergic synapses during rat spinal cord development. J Comp Neurol 398:359-372.
21. Cowley KC, Schmidt BJ. 1995. Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J Neurophysiol 74:1109-1117.
22. Del Rio JA, Soriano E, Ferrer I. 1992. Development of GABA-immunoreactivity in the neocortex of the mouse. J Comp Neurol 326: 501-526.
23. Dumoulin A, Rostaing P, Bedet C, Levi S, Isambert MF, Henry JP, Triller A, Gasnier B. 1999. Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci 112:811-823.
24. Ganguly K, Schinder AF, Wong ST, Poo M. 2001. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105:521-532.
25. Gao BX, Ziskind-Conhaim L. 1995. Development of glycine- and GABA-gated currents in rat spinal motoneurons. J Neurophysiol 74:113-121.
26. Gao BX, Stricker C, Ziskind-Conhaim L. 2001. Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J Neurophysiol 86:492-502.
27. Gonzalez-Forero D, Alvarez FJ. 2005. Differential postnatal maturation of GABAA, glycine receptor, and mixed synaptic currents in renshaw cells and ventral spinal interneurons. J Neurosci 25:2010-2023.
28. Hanson MG, Landmesser LT. 2003. Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 23:587-600.
29. Higashijima S, Mandel G, Fetcho JR. 2004. Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J Comp Neurol 480:1-18.
30. Hinckley C, Seebach B, Ziskind-Conhaim L, 2005. Distinct roles of glycinergic and GABAergic inhibition in coordinating locomotor-like rhythms in the neonatal mouse spinal cord. Neuroscience 131:745-758.
31. Jonas P, Bischofberger J, Sandkuhler J. 1998. Corelease of two fast neurotransmitters at a central synapse. Science 281:419-424.
32. Jong YJ, Thampy KG, Barnes EM, Jr. 1986. Ontogeny of GABAergic neurons in chick brain: studies in vivo and in vitro. Brain Res 390:83-90.
33. Kandler K, Friauf E. 1995. Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15:6890-6904.
34. Kotak VC, Korada S, Schwartz IR, Sanes DH. 1998. A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J Neurosci 18:4646-4655.
35. Krnjevic K. 1981. Transmitter in motor systems. In: Geiger SR, editor. Handbook of physiology. Baltimore: American Society of Physiology. p 107-154.
36. Lauder JM, Han VK, Henderson P, Verdoorn T, Towle AC. 1986. Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 19:465-493.
37. Legendre P. 2001. The glycinergic inhibitory synapse. Cell Mol Life Sci 58:760-793.
38. Lewis CA, Faber DS. 1993. GABA responses and their partial occlusion by glycine in cultured rat medullary neurons. Neuroscience 52:83-96.
39. Lundgren P, Mattsson MO, Johansson L, Ottersen OP, Sellstrom A. 1995. Morphological and GABA-immunoreactive development of the embryonic chick telencephalon. Int J Dev Neurosci 13:463-472.
40. Ma W, Behar T, Barker JL. 1992. Transient expression of GABA immunoreactivity in the developing rat spinal cord. J Comp Neurol 325:271-290.
41. Malosio ML, Marqueze-Pouey B, Kuhse J, Betz H. 1991. Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J 10:2401-2409.
42. Meier E, Jorgensen OS, Schousboe A. 1987. Effect of repeated treatment with a gamma-aminobutyric acid receptor agonist on postnatal neural development in rats. J Neurochem 49:1462-1470.
43. Myers CP, Lewcock JW, Hanson MG, Gosgnach S, Aimone JB, Gage FH, Lee KF, Landmesser LT, Pfaff SL. 2005. Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 46:37-49.
44. Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H. 2004. Developmental switch from GABA to glycine release in single Central synaptic terminals. Nat Neurosci 7:17-23.
45. Nakayama K, Nishimaru H, Kudo N. 2002. Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22:10388-10398.
46. Nishimaru H, Iizuka M, Ozaki S, Kudo N. 1996. Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J Physiol (Lond) 497:131-143.
47. Nishimaru H, Takizawa H, Kudo N. 2000. 5-Hydroxytryptamine-induced locomotor rhythm in the neonatal mouse spinal cord in vitro. Neurosci Lett 280:187-190.
48. Obata K, Oide M, Tanaka H. 1978. Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture. Brain Res 144:179-184.
49. O'Brien JA, Berger AJ. 1999. Cotransmission of GABA and glycine to brain stem motoneurons. J Neurophysiol 82:1638-1641.
50. Ornung G, Shupliakov O, Linda H, Ottersen OP, Storm-Mathisen J, Ulfhake B, Cullheim S. 1996. Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: a postembedding electron microscopic study. J Comp Neurol 365:413-426.
51. Ornung G, Shupliakov O, Ottersen OP, Storm-Mathisen J, Cullheim S. 1994. Immunohistochemical evidence for coexistence of glycine and GABA in nerve terminals on cat spinal motoneurones: an ultrastructural study. Neuroreport 5:889-892.
52. Peduzzi JD. 1988. Genesis of GABA-immunoreactive neurons in the ferret visual cortex. J Neurosci 8:920-931.
53. Pourcho RG, Goebel DJ, Jojich L, Hazlett JC. 1992. Immunocytochemical evidence for the involvement of glycine in sensory centers of the rat brain. Neuroscience 46:643-656.
54. Pow DV, Wright LL, Vaney DI. 1995. The immunocytochemical detection of amino-acid neurotransmitters in paraformaldehyde-fixed tissues. J Neurosci Methods 56:115-123.
55. Rampon C, Luppi PH, Fort P, Peyron C, Jouvet M. 1996. Distribution of glycine-immunoreactive cell bodies and fibers in the rat brain. Neuroscience 75:737-755.
56. Ritter B, Zhang W. 2000. Early postnatal maturation of GABAA-mediated inhibition in the brainstem respiratory rhythm-generating network of the mouse. Eur J Neurosci 12:2975-2984.
57. Rivera C, Voipio J, Kaila K. 2005. Two developmental switches in GABAergic signaling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562:27-36.
58. Rozenberg F, Robain O, Jardin L, Ben-Ari Y. 1989. Distribution of GABAergic neurons in late fetal and early postnatal rat hippocampus. Dev Brain Res 50:177-187.
59. Russier M, Kopysova IL, Ankri N, Ferrand N, Debanne D. 2002. GABA and glycine co-release optimizes functional inhibition in rat brainstem motoneurons in vitro. J Physiol 541:123-137.
60. Schwartz ML, Meinecke DL. 1992. Early expression of GABA-containing neurons in the prefrontal and visual cortices of rhesus monkeys. Cereb Cortex 2:16-37.
61. Sernagor E, Chub N, Ritter A, O'Donovan MJ. 1995. Pharmacological characterization of the rhythmic synaptic drive onto lumbosacral motoneurons in the chick embryo spinal cord. J Neurosci 15:7452-7464.
62. Sewards TV, Sewards M. 2002. Separate, parallel sensory and hedonic pathways in the mammalian somatosensory system. Brain Res Bull 58:243-260.
63. Singer JH, Berger AJ. 2000. Development of inhibitory synaptic transmission to motoneurons. Brain Res Bull 53:553-560.
64. Spoerri PE. 1988. Neurotrophic effects of GABA in cultures of embryonic chick brain and retina. Synapse 2:11-22.
65. Stein V, Hermans-Borgmeyer I, Jentsch TJ, Hubner CA. 2004. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468:57-64.
66. Taal W, Holstege JC. 1994. GABA and glycine frequently colocalize in terminals on cat spinal motoneurons. Neuroreport 5:2225-2228.
67. Todd AJ. 1996. GABA and glycine in synaptic glomeruli of the rat spinal dorsal horn. Eur J Neurosci 8:2492-2498.
68. Todd AJ, Sullivan AC. 1990. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296:496-505.
69. Tran TS, Alijani A, Phelps PE. 2003. Unique developmental patterns of GABAergic neurons in rat spinal cord. J Comp Neurol 456:112-126.
70. van den Pol AN, Gorcs T. 1988. Glycine and glycine receptor immunoreactivity in brain and spinal cord. J Neurosci 8:472-492.
71. Van Eden CG, Mrzljak L, Voorn P, Uylings HB. 1989. Prenatal development of GABA-ergic neurons in the neocortex of the rat. J Comp Neurol 289:213-227.
72. Wu WL, Ziskind-Conhaim L, Sweet MA. 1992. Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12:3935-3945.
73. Yamashita A, Hayashi M. 1996. Ontogeny of GABA-immunoreactive cells in the primate cerebellar cortex: comparison with somatostatin-immunoreactivity. Anat Embryol (Berl) 194:215-222.
74. Zeilhofer HU, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bosl MR, Fritschy JM. 2005. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 482:123-141.