Glycine transporter-1 controls nonsynaptic inhibitory actions of glycine receptors in the neonatal rat hippocampus

Journal of Neuroscience

Volumn 34, Issue 30, 2014, Pages 10003-10009

  Sipilä, Sampsa T ^a,b,c   Spoljaric, Albert ^c   Virtanen, Mari A ^c,d   Hiironniemi, Inkeri ^c   Kaila, Kai ^c  

^a UNIVERSITY OF OULU   (Finland)

^b OULU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Development; Glycine; Hippocampus; Newborn; Spontaneous activity; Tonic

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; BICUCULLINE; CALCIUM ION; GLYCINE; GLYCINE RECEPTOR; GLYCINE TRANSPORTER 1; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N [3 (4 FLUOROPHENYL) 3 (4 PHENYLPHENOXY) PROPYL] SARCOSINE; STRYCHNINE; TETRODOTOXIN; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; FEMALE; FREQUENCY MODULATION; FUNCTIONAL ELECTRICAL STIMULATION; GIANT DEPOLARIZING POTENTIAL; HIPPOCAMPAL CA3 REGION; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MEMBRANE ELECTROPHYSIOLOGY; NERVE CELL MEMBRANE POTENTIAL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SINGLE CHANNEL PATCH CLAMP; STRATUM PYRAMIDALE; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; VIDEO MICROSCOPY; VOLTAGE CLAMP TECHNIQUE;

DEVELOPMENT; GLYCINE; HIPPOCAMPUS; NEWBORN; SPONTANEOUS ACTIVITY; TONIC;

ANIMALS; ANIMALS, NEWBORN; FEMALE; GLYCINE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; HIPPOCAMPUS; MALE; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, GLYCINE;

EID: 84904556864     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0075-13.2014     Document Type: Article

References (55)

1. Applegarth DA, Poon S (1975) Interpretation of elevated blood glycine levels in children. Clin Chim Acta 63:49-54. CrossRef Medline
2. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416:303-325. Medline
3. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87:1215-1284. CrossRef Medline
4. Betz H, Laube B (2006) Glycine receptors: recent insights into their structural organization and functional diversity. J Neurochem 97:1600-1610. CrossRef Medline
5. Betz H, Gomeza J, Armsen W, Scholze P, Eulenburg V (2006) Glycine transporters: essential regulators of synaptic transmission. Biochem Soc Trans 34:55-58. CrossRef Medline
6. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61:820-838. CrossRef Medline
7. Bolea S, Avignone E, Berretta N, Sanchez-Andres JV, Cherubini E (1999) Glutamate controls the induction of GABA-mediated giant depolarizing potentials through AMPA receptors in neonatal rat hippocampal slices. J Neurophysiol 81:2095-2102. Medline
8. Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, Represa A, Ben-Ari Y, Cossart R (2009) GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326:1419-1424. CrossRef Medline
9. Brickley SG, Mody I (2012) Extrasynaptic GABA(A) receptors: their function in the CNS and implications for disease. Neuron 73:23-34. CrossRef Medline
10. Chattipakorn SC, McMahon LL (2002) Pharmacological characterization of glycine-gated chloride currents recorded in rat hippocampal slices. J Neurophysiol 87:1515-1525. Medline
11. Choi YH, Chang N, Anderson GH (1999) An intragastric amino acid mixture influences extracellular amino acid profiles in the lateral hypothalamic area of freely moving rats. Can J Physiol Pharmacol 77:827-834. CrossRef Medline
12. +-and SNAREindependent release of GABA and glutamate prior to synapse formation. Neuron 36:1051-1061. CrossRef Medline
13. Eichler SA, Kirischuk S, Jüttner R, Schafermeier PK, Legendre P, Lehmann TN, Gloveli T, Grantyn R, Meier JC (2008) Glycinergic tonic inhibition of hippocampal neurons with depolarizing GABAergic transmission elicits histopathological signs of temporal lobe epilepsy. J Cell Mol Med 12: 2848-2866. CrossRef Medline
14. Eulenburg V, Armsen W, Betz H, Gomeza J (2005) Glycine transporters: essential regulators of neurotransmission. Trends Biochem Sci 30:325-333. CrossRef Medline
15. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229. CrossRef Medline
16. Fatima-Shad K, Barry PH (1992) A patch-clamp study of GABA-and strychnine-sensitive glycine-activated currents in post-natal tissuecultured hippocampal neurons. Proc Biol Sci 250:99-105. CrossRef Medline
17. Flint AC, Liu X, Kriegstein AR (1998) Nonsynaptic glycine receptor activation during early neocortical development. Neuron 20:43-53. CrossRef Medline
18. Gaiarsa JL, Corradetti R, Cherubini E, Ben-Ari Y (1990) The allosteric glycine site of theN-methyl-D-aspartate receptor modulates GABAergicmediated synaptic events in neonatal rat CA3 hippocampal neurons. Proc Natl Acad Sci U S A 87:343-346. CrossRef Medline
19. Gomeza J, Hülsmann S, Ohno K, Eulenburg V, Szöke K, Richter D, Betz H (2003) Inactivation of the glycine transporter 1 gene discloses vital role of glial glycine uptake in glycinergic inhibition. Neuron 40:785-796. CrossRef Medline
20. Guastella J, Brecha N, Weigmann C, Lester HA, Davidson N (1992) Cloning, expression, and localization of a rat brain high-affinity glycine transporter. Proc Natl Acad Sci U S A 89:7189-7193. CrossRef Medline
21. Harsing LG Jr, Gacsalyi I, Szabo G, Schmidt E, Sziray N, Sebban C, TesolinDecros B, Matyus P, Egyed A, Spedding M, Levay G (2003) The glycine transporter-1 inhibitors NFPS and org 24461: a pharmacological study. Pharmacol Biochem Behav 74:811-825. CrossRef Medline
22. Ito S, Cherubini E (1991) Strychnine-sensitive glycine responses of neonatal rat hippocampal neurones. J Physiol 440:67-83. Medline
23. Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325:529-531. CrossRef Medline
24. Karnani MM, Apergis-Schoute J, Adamantidis A, Jensen LT, de Lecea L, Fugger L, Burdakov D (2011) Activation of central orexin/hypocretin neurons by dietary amino acids. Neuron 72:616-629. CrossRef Medline
25. Keck T, Lillis KP, Zhou YD, White JA (2008) Frequency-dependent glycinergic inhibition modulates plasticity in hippocampus. J Neurosci 28: 7359-7369. CrossRef Medline
26. Khalilov I, Dzhala V, Ben-Ari Y, Khazipov R (1999) Dual role of GABA in the neonatal rat hippocampus. Dev Neurosci 21:310-319. CrossRef Medline
27. Korman SH, Gutman A (2002) Pitfalls in the diagnosis of glycine encephalopathy (non-ketotic hyperglycinemia). Dev Med Child Neurol 44:712-720. CrossRef Medline
28. Lamsa K, Palva JM, Ruusuvuori E, Kaila K, Taira T (2000) Synaptic GABA(A) activation inhibits AMPA-kainate receptor-mediated bursting in the newborn (P0-P2) rat hippocampus. J Neurophysiol 83:359-366. Medline
29. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsáki G (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296:2049-2052. CrossRef Medline
30. Lynch JW (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol Rev 84:1051-1095. CrossRef Medline
31. Marchionni I, Omrani A, Cherubini E (2007) In the developing rat hippocampus a tonic GABAA-mediated conductance selectively enhances the glutamatergic drive of principal cells. J Physiol 581:515-528. CrossRef Medline
32. Mohns EJ, Blumberg MS (2008) Synchronous bursts of neuronal activity in the developing hippocampus: modulation by active sleep and association with emerging gamma and theta rhythms. J Neurosci 28:10134-10144. CrossRef Medline
33. Mori M, Gähwiler BH, Gerber U (2002) Beta-alanine and taurine as endogenous agonists at glycine receptors in rat hippocampus in vitro. J Physiol 539:191-200. CrossRef Medline
34. Owens DF, Liu X, Kriegstein AR (1999) Changing properties of GABA(A) receptor-mediated signaling during early neocortical development. J Neurophysiol 82:570-583. Medline
35. Scain AL, Le Corronc H, Allain AE, Muller E, Rigo JM, Meyrand P, Branchereau P, Legendre P (2010) Glycine release from radial cells modulates the spontaneous activity and its propagation during early spinal cord development. J Neurosci 30:390-403. CrossRef Medline
36. Semyanov A, Walker MC, Kullmann DM, Silver RA (2004) Tonically active GABAA receptors: modulating gain and maintaining the tone. Trends Neurosci 27:262-269. CrossRef Medline
37. Sergeeva OA, Fleischer W, Chepkova AN, Warskulat U, Häussinger D, Siebler M, Haas HL (2007) GABAA-receptor modification in taurine transporter knockout mice causes striatal disinhibition. J Physiol 585:539-548. CrossRef Medline
38. Sipilä ST, Huttu K, Soltesz I, Voipio J, Kaila K (2005) Depolarizing GABA acts on intrinsically bursting pyramidal neurons to drive giant depolarizing potentials in the immature hippocampus. J Neurosci 25:5280-5289. CrossRef Medline
39. + current. Eur J Neurosci 23:2330-2338. CrossRef Medline
40. Sipilä ST, Schuchmann S, Voipio J, Yamada J, Kaila K (2006b) The cationchloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J Physiol 573:765-773. CrossRef Medline
41. Sipilä ST, Voipio J, Kaila K (2007) GAT-1 acts to limit a tonic GABA(A) current in rat CA3 pyramidal neurons at birth. Eur J Neurosci 25:717-722. CrossRef Medline
42. Sipilä ST, Huttu K, Yamada J, Afzalov R, Voipio J, Blaesse P, Kaila K (2009) Compensatory enhancement of intrinsic spiking upon NKCC1 disruption in neonatal hippocampus. J Neurosci 29:6982-6988. CrossRef Medline
43. Sipilä S, Huttu K, Voipio J, Kaila K (2004) GABA uptake via GABA transporter-1 modulates GABAergic transmission in the immature hippocampus. J Neurosci 24:5877-5880. CrossRef Medline
44. Song W, Chattipakorn SC, McMahon LL (2006) Glycine-gated chloride channels depress synaptic transmission in rat hippocampus. J Neurophysiol 95:2366-2379. CrossRef Medline
45. Supplisson S, Bergman C (1997) Control of NMDA receptor activation by a glycine transporter co-expressed inXenopusoocytes. J Neurosci 17:4580-4590. Medline
46. Takahashi T, Momiyama A (1991) Single-channel currents underlying glycinergic inhibitory postsynaptic responses in spinal neurons. Neuron 7:965-969. CrossRef Medline
47. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, Khazipov R (2003) Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90:2964-2972. CrossRef Medline
48. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hübner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314: 1788-1792. CrossRef Medline
49. Valeeva G, Abdullin A, Tyzio R, Skorinkin A, Nikolski E, Ben-Ari Y, Khazipov R (2010) Temporal coding at the immature depolarizing GABAergic synapse. Front Cell Neurosci 4:17. CrossRef Medline
50. Valeeva G, Valiullina F, Khazipov R (2013) Excitatory actions of GABA in the intact neonatal rodent hippocampus in vitro. Front Cell Neurosci 7:20. CrossRef Medline
51. - channels are randomly activated by continuous GABA secretion in cultured embryonic rat hippocampal neurons. Neurosci Lett 155:199-203. CrossRef Medline
52. Warskulat U, Heller-Stilb B, Oermann E, Zilles K, Haas H, Lang F, Häussinger D (2007) Phenotype of the taurine transporter knockout mouse. Methods Enzymol 428:439-458. CrossRef Medline
53. Xu TL, Gong N (2010) Glycine and glycine receptor signaling in hippocampal neurons: diversity, function and regulation. Prog Neurobiol 91:349-361. CrossRef Medline
54. Zafra F, Aragón C, Olivares L, Danbolt NC, Giménez C, Storm-Mathisen J (1995) Glycine transporters are differentially expressed among CNS cells. J Neurosci 15:3952-3969. Medline
55. Zhang LH, Gong N, Fei D, Xu L, Xu TL (2008) Glycine uptake regulates hippocampal network activity via glycine receptor-mediated tonic inhibition. Neuropsychopharmacology 33:701-711. CrossRef Medline