The zebrafish shocked gene encodes a glycine transporter and is essential for the function of early neural circuits in the CNS

Journal of Neuroscience

Volumn 25, Issue 28, 2005, Pages 6610-6620

  Cui, Wilson W ^a   Low, Sean E ^a   Hirata, Hiromi ^a   Saint Amant, Louis ^a   Geisler, Robert ^b   Hume, Richard I ^a   Kuwada, John Y ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Behavior; Glycine transporter; Mutation; Strychnine; Zebrafish

Indexed keywords

CARRIER PROTEIN; GLYCINE TRANSPORTER; MESSENGER RNA; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE; GLYT1 GENE; GLYT2 GENE; LOCOMOTION; MISSENSE MUTATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OOCYTE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHOCKED GENE; XENOPUS; ZEBRA FISH;

ANIMALS; CENTRAL NERVOUS SYSTEM; EMBRYO, NONMAMMALIAN; EXTRACELLULAR FLUID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; GLYCINE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; MUSCLES; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; OOCYTES; PHENOTYPE; PHYSICAL STIMULATION; RECOMBINANT FUSION PROTEINS; RHOMBENCEPHALON; RNA, MESSENGER; SARCOSINE; SPINAL CORD; SWIMMING; XENOPUS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 22244477697     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5009-04.2005     Document Type: Article

References (62)

1. Adams RH, Sato K, Shimada S, Tohyama M, Puschel AW, Betz H (1995) Gene structure and glial expression of the glycine transporter GlyT1 in embryonic and adult rodents. J Neurosci 15:2524-2532.
2. Applegarth DA, Toone JR (2004) Glycine encephalopathy (nonketotic hyperglycinaemia): review and update. J Inherit Metab Dis 27:417-422.
3. Aragon C, Lopez-Corcuera B (2003) Structure, function and regulation of glycine neurotransporters. Eur J Pharmacol 479:249-262.
4. Aubrey KR, Vandenberg RJ (2001) N[3-(4′-fluorophenyl)-3-(4′- phenyl-phenoxy)propyl]sarcosine (NFPS) is a selective persistent inhibitor of glycine transport. Br J Pharmacol 134:1429-1436.
5. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353-360.
6. Bergeron R, Meyer TM, Coyle JT, Greene RW (1998) Modulation of N-methyl-D-aspartate receptor function by glycine transport. Proc Natl Acad Sci USA 95:15730-15734.
7. Bernhardt R, Chitnis A, Lindamer L, Kuwada J (1990) Identification of spinal neurons in the embryonic and larval zebrafish. J Comp Neurol 302:603-616.
8. Borowsky B, Mezey E, Hoffman BJ (1993) Two glycine transporter variants with distinct localization in the CNS and peripheral tissues are encoded by a common gene. Neuron 10:851-863.
9. Buss RR, Drapeau P (2000) Physiological properties of zebrafish embryonic red and white muscle fibers during early development. J Neurophysiol 84:1545-1557.
10. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA, Zhang D (2002) Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415:793-798.
11. Chen L, Muhlhauser M, Yang CR (2003) Glycine tranporter-1 blockade potentiates NMDA-mediated responses in rat prefrontal cortical neurons in vitro and in vivo. J Neurophysiol 89:691-703.
12. Corey DR, Abrams JM (2001) Morpholino antisense oligonucleotides: tools for investigating vertebrate development. Genome Biol 2:REVIEWS1015.
13. Cui WW, Saint-Amant L, Kuwada JY (2004) shocked gene is required for the function of a premotor network in the zebrafish CNS. J Neurophysiol 92:2898-2908.
14. Drapeau P, Ali DW, Buss RR, Saint-Amant L (1999) In vivo recording from identifiable neurons of the locomotor network in the developing zebrafish. J Neurosci Methods 88:1-13.
15. Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737-752.
16. Geisler R (2002) Mapping and cloning. In: Zebrafish, a practical approach. Oxford: Oxford UP.
17. Gomeza J, Hulsmann S, Ohno K, Eulenburg V, Szoke 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.
18. Granato M, van Eeden F, Schach U, Trowe T, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg C, Jiang Y, Kane D, Kelsh R, Mullins M, Odenthal J, Nusslein-Volhard C (1996) Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123:399-413.
19. Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573-586.
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 USA 89:7189-7193.
21. Higashijima S, Masino MA, Mandel G, Fetcho JR (2003) Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J Neurophysiol 90:3986-3997.
22. Higashijima SI, Mandel G, Fetcho JR (2004a) Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J Comp Neurol 480:1-18.
23. Higashijima SI, Schaefer M, Fetcho JR (2004b) Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish. J Comp Neurol 480:19-37.
24. 2+ pump SERCA1. Development 131:5457-5468.
25. - -dependent neurotransmitter transporters in bovine retina: identification and localization by in situ hybridization histochemistry. Vis Neurosci 12:1135-1142.
26. Jursky F, Nelson N (1995) Localization of glycine neurotransmitter transporter (GLYT2) reveals correlation with the distribution of glycine receptor. J Neurochem 64:1026-1033.
27. Jursky F, Nelson N (1996) Developmental expression of the glycine transporters GLYT1 and GLYT2 in mouse brain. J Neurochem 67:336-344.
28. Kim KM, Kingsmore SF, Han H, Yang-Feng TL, Godinot N, Seldin MF, Caron MG, Giros B (1994) Cloning of the human glycine transporter type 1: molecular and pharmacological characterization of novel isoform variants and chromosomal localization of the gene in the human and mouse genomes. Mol Pharmacol 45:608-617.
29. Kimmel C, Powell S, Metcalfe W (1982) Brain neurons which project to the spinal cord in young larvae of the zebrafish. J Comp Neurol 205:112-127.
30. Kimmel C, Ballard W, Kimmel S, Ullmann B, Schilling T (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310.
31. Kinney GG, Sur C, Burno M, Mallorga PJ, Williams JB, Figueroa DJ, Wittmann M, Lemaire W, Conn PJ (2003) The glycine transporter type 1 inhibitor N-[3-(4′-fluorophenyl)-3-(4′-phenylphenoxy)propyl]sarcosine potentiates NMDA receptor-mediated responses in vivo and produces an antipsychotic profile in rodent behavior. J Neurosci 23:7586-7591.
32. Legendre P (2001) The glycinergic inhibitory synapse. Cell Mol Life Sci 58:760-793.
33. Legendre P, Korn H (1994) Glycinergic inhibitory synaptic currents and related receptor channels in the zebrafish brain. Eur J Neurosci 6:1544-1557.
34. Lim R, Hoang P, Berger AJ (2004) Blockade of glycine transporter-1 (GLYT-1) potentiates NMDA receptor-mediated synaptic transmission in hypoglossal motorneurons. J Neurophysiol 92:2530-2537.
35. Lopez-Corcuera B, Nunez E, Martinez-Maza R, Geerlings A, Aragon C (2001) Substrate-induced conformational changes of extracellular loop 1 in the glycine transporter GLYT2. J Biol Chem 276:43463-43470.
36. Luna VM, Wang M, Ono F, Gleason MR, Dallman JE, Mandel G, Brehm P (2004) Persistent electrical coupling and locomotory dysfunction in the zebrafish mutant shocked. J Neurophysiol 92:2003-2009.
37. Martina M, Gorfinkel Y, Halman S, Lowe JA, Periyalwar P, Schmidt CJ, Bergeron R (2004) Glycine transporter type 1 blockade changes NMDA receptor-mediated responses and LTP in hippocampal CA1 pyramidal cells by altering extracellular glycine levels. J Physiol (Lond) 557:489-500.
38. Mayer ML, Vyklicky Jr L, Clements J (1989) Regulation of NMDA receptor desensitization in mouse hippocampal neurons by glycine. Nature 338:425-427.
39. Melamed N, Kanner BI (2004) Transmembrane domains I and II of the gamma-aminobutyric acid transporter GAT-4 contain molecular determinants of substrate specificity. Mol Pharmacol 65:1452-1461.
40. Mendelson B (1985) Soma position is correlated with time of development in three types of identified reticulospinal neurons. Dev Biol 112:489-493.
41. Metcalfe W, Mendelson B, Kimmel C (1986) Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J Comp Neurol 251:147-159.
42. Neuhauss SC, Biehlmaier O, Seeliger MW, Das T, Kohler K, Harris WA, Baier H (1999) Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. J Neurosci 19:8603-8615.
43. O'Malley D, Kao Y, Fetcho JR (1996) Imaging the functional organization of zebrafish hindbrain segments during escape behaviors. Neuron 17:1145-1155.
44. Pow DV, Hendrickson AE (2000) Expression of glycine and the glycine transporter glyt-1 in the developing rat retina. Vis Neurosci 17:1-9.
45. Ribera AB, Nusslein-Volhard C (1998) Zebrafish touch-insensitive mutants reveal an essential role for the developmental regulation of sodium current. J Neurosci 18:9181-9191.
46. Ritter DA, Bhatt DH, Fetcho JR (2001) In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements. J Neurosci 21:8956-8965.
47. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
48. Roux MJ, Supplisson S (2000) Neuronal and glial glycine transporters have different stoichiometries. Neuron 25:373-383.
49. Roux MJ, Martinez-Maza R, Le Goff A, Lopez-Corcuera B, Aragon C, Supplisson S (2001) The glial and the neuronal glycine transporters differ in their reactivity to sulfhydryl reagents. J Biol Chem 276:17699-17705.
50. Saint-Amant L, Drapeau P (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37:622-632.
51. Saint-Amant L, Drapeau P (2000) Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. J Neurosci 20:3964-3972.
52. Saint-Amant L, Drapeau P (2001) Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 31:1035-1046.
53. Sato Y, Zhang Y-W, Androutsellis-Theotokis A, Rudnick G (2004) Analysis of transmembrane domain 2 of rat serotonin transporter by cysteine scanning mutagenesis. J Biol Chem 279:22926-22933.
54. Shafizadeh E, Paw BH, Foott H, Liao EC, Barut BA, Cope JJ, Zon LI, Lin S (2002) Characterization of zebrafish merlot/chablis as non-mammalian vertebrate models for severe congenital anemia due to protein 4.1 deficiency. Development 129:4359-4370.
55. Smith KE, Borden LA, Hartig PR, Branchek T, Weinshank RL (1992) Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron 8:927-935.
56. Supplisson S, Bergman C (1997) Control of NMDA receptor activation by a glycine transporter coexpressed in Xenopus oocytes. J Neurosci 17:4580-4590.
57. Talbot WS, Schier AF (1999) Positional cloning of mutated zebrafish genes. Methods Cell Biol 60:259-286.
58. Tsai G, Ralph-Williams RJ, Martina M, Bergeron R, Berger-Sweeney J, Dunham KS, Jiang Z, Caine SB, Coyle JT (2004) Gene knockout of glycine transporter 1: characterization of the behavioral phenotype. Proc Natl Acad Sci USA 101:8485-8490.
59. Westerfield M (1993) The zebrafish book, Ed 3. Eugene, OR: University of Oregon.
60. Zafra F, Gomeza J, Olivares L, Aragon C, Gimenez C (1995a) Regional distribution and developmental variation of the glycine transporters GLYT1 and GLYT2 in the rat CNS. Eur J Neurosci 7:1342-1352.
61. Zafra F, Aragon C, Olivares L, Danbolt NC, Gimenez C, Storm-Mathisen J (1995b) Glycine transporters are differentially expressed among CNS cells. J Neurosci 15:3952-3969.
62. Zhang J, Talbot WS, Schier AF (1998) Positional cloning identifies zebrafish one-eyed pinhead as a permissive EGF-related ligand required during gastrulation. Cell 92:241-251.