Fluorescent labeling of both GABAergic and glycinergic neurons in vesicular GABA transporter (VGAT)-Venus transgenic mouse

Neuroscience

Volumn 164, Issue 3, 2009, Pages 1031-1043

  Wang, Y ^a   Kakizaki, T ^a   Sakagami, H ^b   Saito, K ^a,c   Ebihara, S ^d   Kato, M ^e   Hirabayashi, M ^e   Saito, Y ^a   Furuya, N ^a   Yanagawa, Y ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

fluorescent protein; inhibitory neurons; label; promoter; transgenic mouse; vesicular GABA transporter

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE 67; GLYCINE; GREEN FLUORESCENT PROTEIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL FUNCTION; CELL LABELING; CELL STRUCTURE; COCHLEAR NUCLEUS; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; GABAERGIC SYSTEM; HIPPOCAMPUS; IMMUNOREACTIVITY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

ANIMALS; BACTERIAL PROTEINS; BRAIN; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; GLYCINE; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; NEURONS; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; SPECIES SPECIFICITY; STAINING AND LABELING; UP-REGULATION; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 70350560328     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.09.010     Document Type: Article

References (46)

1. Acuna-Goycolea C., Tamamaki N., Yanagawa Y., Obata K., and van den Pol A.N. Mechanisms of NPY, PYY3-36, and PP inhibition of identified GFP-expressing GABA neurons in the hypothalamic neuroendocrine arcuate nucleus. J Neurosci 25 (2005) 7406-7419
2. Aoki E., Semba R., Keino H., Kato K., and Kashiwamata S. Glycine-like immunoreactivity in the rat auditory pathway. Brain Res 442 (1988) 63-71
3. Asada H., Kawamura Y., Maruyama K., Kume H., Ding R., Ji F.Y., Kanbara N., Kuzume H., Sanbo M., Yagi T., and Obata K. Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem Biophys Res Commun 229 (1996) 891-895
4. Aubrey K.R., Rossi F.M., Ruivo R., Alboni S., Bellenchi G.C., Le Goff A., Gasnier B., and Supplisson S. The transporters GlyT2 and VIAAT cooperate to determine the vesicular glycinergic phenotype. J Neurosci 27 (2007) 6273-6281
5. Berghuis P., Rajnicek A.M., Morozov Y.M., Ross R.A., Mulder J., Urban G.M., Monory K., Marsicano G., Matteoli M., Canty A., Irving A.J., Katona I., Yanagawa Y., Rakic P., Lutz B., Mackie K., and Harkany T. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316 (2007) 1212-1216
6. Bessis A., Salmon A.M., Zoli M., Le Novere N., Picciotto M., and Changeux J.P. Promoter elements conferring neuron-specific expression of the beta 2-subunit of the neuronal nicotinic acetylcholine receptor studied in vitro and in transgenic mice. Neuroscience 69 (1995) 807-819
7. Brinster R.L., Chen H.Y., Trumbauer M.E., Yagle M.K., and Palmiter R.D. Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs. Proc Natl Acad Sci U S A 82 (1985) 4438-4442
8. Brown R.E., McKenna J.T., Winston S., Basheer R., Yanagawa Y., Thakkar M.M., and McCarley R.W. Characterization of GABAergic neurons in rapid-eye-movement (REM) sleep controlling regions of the brainstem reticular formation in GAD67-GFP knock-in mice. Eur J Neurosci 27 (2008) 352-363
9. Bu D.F., Erlander M.G., Hitz B.C., Tillakaratne N.J., Kaufman D.L., Wagner-McPherson C.B., Evans G.A., and Tobin A.J. Two human glutamate decarboxylases, 65-kDa GAD and 67-kDa GAD, are each encoded by a single gene. Proc Natl Acad Sci U S A 89 (1992) 2115-2119
10. Chattopadhyaya B., Di Cristo G., Higashiyama H., Knott G.W., Kuhlman S.J., Welker E., and Huang Z.J. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24 (2004) 9598-9611
11. Chattopadhyaya B., Di Cristo G., Wu C.Z., Knott G., Kuhlman S., Fu Y., Palmiter R.D., and Huang Z.J. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54 (2007) 889-903
12. Chaudhry F.A., Reimer R.J., Bellocchio E.E., Danbolt N.C., Osen K.K., Edwards R.H., and Storm-Mathisen J. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18 (1998) 9733-9750
13. Chen T.S., Zeng S.Q., Luo Q.M., Zhang Z.H., and Zhou W. High-order photobleaching of green fluorescent protein inside live cells in two-photon excitation microscopy. Biochem Biophys Res Commun 291 (2002) 1272-1275
14. Dumoulin A., Rostaing P., Bedet C., Lévi S., Isambert M.F., Henry J.P., Triller A., and Gasnier B. Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci 112 (1999) 811-823
15. Ebihara S., Obata K., and Yanagawa Y. Mouse vesicular GABA transporter gene: genomic organization, transcriptional regulation, and chromosomal localization. Mol Brain Res 110 (2003) 126-139
16. Esclapez M., Tillakaratne N.J., Kaufman D.L., Tobin A.J., and Houser C.R. Comparative localization of 2 forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14 (1994) 1834-1855
17. + conductance: a study using glutamate decarboxylase 67-green fluorescent protein knock-in mice. Neuroscience 157 (2008) 781-797
18. Kolston J., Osen K.K., Hackney C.M., Ottersen O.P., and Storm-Mathisen J. An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat Embryol (Berl) 186 (1992) 443-465
19. Legendre P. The glycinergic inhibitory synapse. Cell Mol Life Sci 58 (2001) 760-793
20. López-Bendito G., Sturgess K., Erdélyi F., Szabó G., Molnár Z., and Paulsen O. Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb Cortex 14 (2004) 1122-1133
21. Ma Y., Hu H., Berrebi A.S., Mathers P.H., and Agmon A. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26 (2006) 5069-5082
22. Marowsky A., Yanagawa Y., Obata K., and Vogt K.E. A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function. Neuron 48 (2005) 1025-1037
23. McIntire D.L., Reimer R.J., Schuske K., Edwards R.H., and Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 389 (1997) 870-876
24. Moore J.K., Osen K.K., Storm-Mathisen J., and Ottersen O.P. Gamma-aminobutyric acid and glycine in the baboon cochlear nuclei: an immunocytochemical colocalization study with reference to interspecies differences in inhibitory systems. J Comp Neurol 369 (1996) 497-519
25. Mugnaini E. GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: light and electron microscopic immunocytochemistry. J Comp Neurol 235 (1985) 61-81
26. Nagai T., Ibata K., Park E.S., Kubota M., Mikoshiba K., and Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20 (2002) 87-90
27. Nakayama H., Hashimoto K., Miyazaki T., Yanagawa Y., Obata K., Watanabe M., and Kano M. Strength of GABAergic transmission influences climbing fiber synapse elimination during cerebellar development. Neurosci Res Suppl 58 (2007) S52
28. Oliva Jr. A.A., Jiang M., Lam T., Smith K.L., and Swann J.W. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20 (2000) 3354-3368
29. Ono M., Yanagawa Y., and Koyano K. GABAergic neurons in inferior colliculus of the GAD67-GFP "knock-in" mouse: electrophysiological and morphological properties. Neurosci Res 51 (2005) 475-492
30. Parrish-Aungst S., Shipley M.T., Erdelyi F., Szabo G., and Puche A.C. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501 (2007) 825-836
31. Raguz S., Hobbs C., Yagüe E., Ioannou P.A., Walsh F.S., and Antoniou M. Muscle-specific locus control region activity associated with the human desmin gene. Dev Biol 201 (1998) 26-42
32. Roberts E., and Kuriyama K. Biochemical-physiological correlations in studies of the gamma-aminobutyric acid system. Brain Res 8 (1968) 1-35
33. Sagné C., El Mestikawy S., Isambert M.F., Hamon M., Henry J.P., Giros B., and Gasnier B. Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett 417 (1997) 177-183
34. Sakagami H., Matsuya S., Nishimura H., Suzuki R., and Kondo H. Somatodendritic localization of the mRNA for EFA6A, a guanine nucleotide exchange protein for ARF6, in rat hippocampus and its involvement in dendritic formation. Eur J Neurosci 19 (2004) 863-870
35. Takahashi R., Ito K., Fujiwara Y., Kodaira K., Kodaira K., Hirabayashi M., and Ueda M. Generation of transgenic rats with YACs and BACs: preparation procedures and integrity of microinjected DNA. Exp Anim 49 (2000) 229-233
36. Takamori S., Riedel D., and Jahn R. Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. J Neurosci 20 (2000) 4904-4911
37. Tamamaki N., Nakamura K., Furuta T., Asamoto K., and Kaneko T. Neurons in Golgi-stain-like images revealed by GFP-adenovirus infection in vivo. Neurosci Res 38 (2000) 231-236
38. Tamamaki N., Yanagawa Y., Tomioka R., Miyazaki J., Obata K., and Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467 (2003) 60-79
39. Tanaka D.H., Maekawa K., Yanagawa Y., Obata K., and Murakami F. Multidirectional and multizonal migration of GABAergic interneurons in the developing cerebral cortex. Development 133 (2006) 2167-2176
40. Uematsu M., Hirai Y., Karube F., Ebihara S., Kato M., Abe K., Obata K., Yoshida S., Hirabayashi M., Yanagawa Y., and Kawaguchi Y. Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic Venus-expressing rats. Cereb Cortex 18 (2008) 315-330
41. Wojcik S.M., Katsurabayashi S., Guillemin I., Friauf E., Rosenmund C., Brose N., and Rhee J.S. A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50 (2006) 575-587
42. Xu Y.H., and Grabowski G.A. Translational inefficiency of acid beta-glucosidase mRNA in transgenic mammalian cells. Mol Genet Metab 64 (1998) 87-98
43. Yamanaka H., Yanagawa Y., and Obata K. Development of stellate and basket cells and their apoptosis in mouse cerebellar cortex. Neurosci Res 50 (2004) 13-22
44. Yanagawa Y., Kobayashi T., Kamei T., Ishii K., Nishijima M., Takaku A., Kobayashi T., and Tamura S. Structure and alternative promoters of the mouse glutamic acid decarboxylase 67 gene. Biochem J 326 (1997) 573-578
45. Young A, Sun QQ (in press) GABAergic inhibitory interneurons in the posterior piriform cortex of the GAD67-GFP mouse. Cereb Cortex, in press.
46. Zeilhofer H.U., Studler B., Arabadzisz D., Schweizer C., Ahmadi S., Layh B., Bösl M.R., and Fritschy J.M. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 482 (2005) 123-141