Molecular and functional characterization of GAD67-expressing, newborn granule cells in mouse dentate gyrus

Frontiers in Neural Circuits

Volumn , Issue MAR, 2013, Pages

  Cabezas, Carolina ^a,b,c   Irinopoulou, Theano ^a,b,c   Cauli, Bruno ^b,d   Poncer, Jean Christophe ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DU FER À MOULIN   (France)

^d CNRS   (France)

Author keywords

Adult neurogenesis; Dentate gyrus; GABA; GAD; Granule cells

Indexed keywords

4 AMINOBUTYRIC ACID; ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMATE DECARBOXYLASE 67;

AMINO ACID SYNTHESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; DENTATE GYRUS; GABAERGIC TRANSMISSION; GRANULAR CELL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MITOSIS; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; ONTOGENY; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 84875311839     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00060     Document Type: Article

References (64)

1. Altman, J., and Bayer, S.A. (1990). Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301, 365-381.
2. Ambrogini, P., Lattanzi, D., Ciuffoli, S., Agostini, D., Bertini, L., Stocchi, V., Santi, S., and Cuppini, R. (2004a). Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res 1017, 21-31.
3. Ambrogini, P., Orsini, L., Mancini, C., Ferri, P., Ciaroni, S., and Cuppini, R. (2004b). Learning may reduce neurogenesis in adult rat dentate gyrus. Neurosci Lett 359, 13-16.
4. Ango, F., Di Cristo, G., Higashiyama, H., Bennett, V., Wu, P., and Huang, Z.J. (2004). Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119, 257-272.
5. Ankri, N., Legendre, P., Faber, D.S., and Korn, H. (1994). Automatic detection of spontaneous synaptic responses in central neurons. J Neurosci Methods 52, 87-100.
6. Boulland, J.L., Qureshi, T., Seal, R.P., Rafiki, A., Gundersen, V., Bergersen, L.H., Fremeau, R.T., Jr., Edwards, R.H., Storm-Mathisen, J., and Chaudhry, F.A. (2004). Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480, 264-280.
7. Cabezas, C., Irinopoulou, T., Gauvain, G., and Poncer, J.C. (2012). Presynaptic but not postsynaptic GABA signaling at unitary mossy fiber synapses. J Neurosci 32, 11835-11840.
8. Cauli, B., Audinat, E., Lambolez, B., Angulo, M.C., Ropert, N., Tsuzuki, K., Hestrin, S., and Rossier, J. (1997). Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17, 3894-3906.
9. Cauli, B., Porter, J.T., Tsuzuki, K., Lambolez, B., Rossier, J., Quenet, B., and Audinat, E. (2000). Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci U S A 97, 6144-6149.
10. Chattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G.W., Kuhlman, S.J., Welker, E., and Huang, Z.J. (2004). Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24, 9598-9611.
11. Couillard-Despres, S., Winner, B., Karl, C., Lindemann, G., Schmid, P., Aigner, R., Laemke, J., Bogdahn, U., Winkler, J., Bischofberger, J., and Aigner, L. (2006). Targeted transgene expression in neuronal precursors: watching young neurons in the old brain. Eur J Neurosci 24, 1535-1545.
12. Dayer, A.G., Ford, A.A., Cleaver, K.M., Yassaee, M., and Cameron, H.A. (2003). Short-term and longterm survival of new neurons in the rat dentate gyrus. J Comp Neurol 460, 563-572.
13. Duveau, V., Laustela, S., Barth, L., Gianolini, F., Vogt, K.E., Keist, R., Chandra, D., Homanics, G.E., Rudolph, U., and Fritschy, J.M. (2011). Spatiotemporal specificity of GABAA receptormediated regulation of adult hippocampal neurogenesis. Eur J Neurosci 34, 362-373.
14. Esposito, M.S., Piatti, V.C., Laplagne, D.A., Morgenstern, N.A., Ferrari, C.C., Pitossi, F.J., and Schinder, A.F. (2005). Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25, 10074-10086.
15. Fisher, R.A., and Yates, F. (1963). Statistical Tables for Biological, agricultural and medical research. London: Hafner press.
16. Fremeau, R.T., Jr., Kam, K., Qureshi, T., Johnson, J., Copenhagen, D.R., Storm-Mathisen, J., Chaudhry, F.A., Nicoll, R.A., and Edwards, R.H. (2004). Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304, 1815-1819.
17. Fukuda, S., Kato, F., Tozuka, Y., Yamaguchi, M., Miyamoto, Y., and Hisatsune, T. (2003). Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23, 9357-9366.
18. Gallopin, T., Fort, P., Eggermann, E., Cauli, B., Luppi, P.H., Rossier, J., Audinat, E., Muhlethaler, M., and Serafin, M. (2000). Identification of sleep-promoting neurons in vitro. Nature 404, 992-995.
19. Ge, S., Goh, E.L., Sailor, K.A., Kitabatake, Y., Ming, G.L., and Song, H. (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589-593.
20. Ge, S., Pradhan, D.A., Ming, G.L., and Song, H. (2007). GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30, 1-8.
21. Glykys, J., Mann, E.O., and Mody, I. (2008). Which GABA(A) receptor subunits are necessary for tonic inhibition in the hippocampus? J Neurosci 28, 1421-1426.
22. Gutierrez, R. (2005). The dual glutamatergic-GABAergic phenotype of hippocampal granule cells. Trends Neurosci 28, 297-303.
23. Gutierrez, R., Romo-Parra, H., Maqueda, J., Vivar, C., Ramirez, M., Morales, M.A., and Lamas, M. (2003). Plasticity of the GABAergic phenotype of the glutamatergic granule cells of the rat dentate gyrus. J Neurosci 23, 5594-5598.
24. He, H., Mahnke, A.H., Doyle, S., Fan, N., Wang, C.C., Hall, B.J., Tang, Y.P., Inglis, F.M., Chen, C., and Erickson, J.D. (2012). Neurodevelopmental Role for VGLUT2 in Pyramidal Neuron Plasticity, Dendritic Refinement, and in Spatial Learning. J Neurosci 32, 15886-15901.
25. Herd, M.B., Haythornthwaite, A.R., Rosahl, T.W., Wafford, K.A., Homanics, G.E., Lambert, J.J., and Belelli, D. (2008). The expression of GABAA beta subunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells. J Physiol 586, 989-1004.
26. Hill, E.L., Gallopin, T., Ferezou, I., Cauli, B., Rossier, J., Schweitzer, P., and Lambolez, B. (2007). Functional CB1 receptors are broadly expressed in neocortical GABAergic and glutamatergic neurons. J Neurophysiol 97, 2580-2589.
27. Hollrigel, G.S., and Soltesz, I. (1997). Slow kinetics of miniature IPSCs during early postnatal development in granule cells of the dentate gyrus. J Neurosci 17, 5119-5128.
28. Huckfeldt, R.M., Schubert, T., Morgan, J.L., Godinho, L., Di Cristo, G., Huang, Z.J., and Wong, R.O. (2009). Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat Neurosci 12, 35-43.
29. Jessberger, S., Zhao, C., Toni, N., Clemenson, G.D., Jr., Li, Y., and Gage, F.H. (2007). Seizureassociated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci 27, 9400-9407.
30. Karagiannis, A., Gallopin, T., David, C., Battaglia, D., Geoffroy, H., Rossier, J., Hillman, E.M., Staiger, J.F., and Cauli, B. (2009). Classification of NPY-expressing neocortical interneurons. J Neurosci 29, 3642-3659.
31. Kempermann, G., Jessberger, S., Steiner, B., and Kronenberg, G. (2004). Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27, 447-452.
32. Kullmann, D.M., Ruiz, A., Rusakov, D.M., Scott, R., Semyanov, A., and Walker, M.C. (2005). Presynaptic, extrasynaptic and axonal GABAA receptors in the CNS: where and why? Prog Biophys Mol Biol 87, 33-46.
33. Lamas, M., Gomez-Lira, G., and Gutierrez, R. (2001). Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes. Brain Res Mol Brain Res 93, 209-214.
34. Lambolez, B., Audinat, E., Bochet, P., Crepel, F., and Rossier, J. (1992). AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247-258.
35. Lledo, P.M., Alonso, M., and Grubb, M.S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7, 179-193.
36. Marin-Burgin, A., Mongiat, L.A., Pardi, M.B., and Schinder, A.F. (2012). Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335, 1238-1242.
37. Meera, P., Wallner, M., and Otis, T.S. (2011). Molecular basis for the high THIP/gaboxadol sensitivity of extrasynaptic GABA(A) receptors. J Neurophysiol 106, 2057-2064.
38. Mori, M., Abegg, M.H., Gahwiler, B.H., and Gerber, U. (2004). A frequency-dependent switch from inhibition to excitation in a hippocampal unitary circuit. Nature 431, 453-456.
39. Nakamura, K., Hioki, H., Fujiyama, F., and Kaneko, T. (2005). Postnatal changes of vesicular glutamate transporter (VGluT)1 and VGluT2 immunoreactivities and their colocalization in the mouse forebrain. J Comp Neurol 492, 263-288.
40. Overstreet-Wadiche, L.S., Bensen, A.L., and Westbrook, G.L. (2006). Delayed development of adultgenerated granule cells in dentate gyrus. J Neurosci 26, 2326-2334.
41. Overstreet-Wadiche, L.S., and Westbrook, G.L. (2006). Functional maturation of adult-generated granule cells. Hippocampus 16, 208-215.
42. Overstreet, L.S., Hentges, S.T., Bumaschny, V.F., De Souza, F.S., Smart, J.L., Santangelo, A.M., Low, M.J., Westbrook, G.L., and Rubinstein, M. (2004). A transgenic marker for newly born granule cells in dentate gyrus. J Neurosci 24, 3251-3259.
43. Overstreet Wadiche, L., Bromberg, D.A., Bensen, A.L., and Westbrook, G.L. (2005). GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94, 4528-4532.
44. Palmiter, R.D., and Brinster, R.L. (1986). Germ-line transformation of mice. Annu Rev Genet 20, 465-499.
45. Parent, J.M. (2007). Adult neurogenesis in the intact and epileptic dentate gyrus. Prog Brain Res 163, 529-540.
46. Ruiz, A., Campanac, E., Scott, R.S., Rusakov, D.A., and Kullmann, D.M. (2010). Presynaptic GABAA receptors enhance transmission and LTP induction at hippocampal mossy fiber synapses. Nat Neurosci 13, 431-438.
47. Ruiz, A., Fabian-Fine, R., Scott, R., Walker, M.C., Rusakov, D.A., and Kullmann, D.M. (2003). GABAA receptors at hippocampal mossy fibers. Neuron 39, 961-973.
48. Safiulina, V.F., Fattorini, G., Conti, F., and Cherubini, E. (2006). GABAergic signaling at mossy fiber synapses in neonatal rat hippocampus. J Neurosci 26, 597-608.
49. Sandler, R., and Smith, A.D. (1991). Coexistence of GABA and glutamate in mossy fiber terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 303, 177-192.
50. Schwarzer, C., and Sperk, G. (1995). Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 69, 705-709.
51. Sloviter, R.S., Dichter, M.A., Rachinsky, T.L., Dean, E., Goodman, J.H., Sollas, A.L., and Martin, D.L. (1996). Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 373, 593-618.
52. Sperk, G., Schwarzer, C., Heilman, J., Furtinger, S., Reimer, R.J., Edwards, R.H., and Nelson, N. (2003). Expression of plasma membrane GABA transporters but not of the vesicular GABA transporter in dentate granule cells after kainic acid seizures. Hippocampus 13, 806-815.
53. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K., and Kaneko, T. (2003). Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467, 60-79.
54. Thorndike (1953). Who belongs in the family? Psychometrika 18, 267-276.
55. Tyner, C.F. (1975). The naming of neurons: applications of taxonomic theory to the study of cellular populations. Brain Behav Evol 12, 75-96.
56. Uchigashima, M., Fukaya, M., Watanabe, M., and Kamiya, H. (2007). Evidence against GABA release from glutamatergic mossy fiber terminals in the developing hippocampus. J Neurosci 27, 8088-8100.
57. Walker, M.C., Ruiz, A., and Kullmann, D.M. (2001). Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fiber synapses. Neuron 29, 703-715.
58. Ward, J.H. (1963). Hierarchical grouping to optimize an objective function. American statistical association journal.
59. Weston, M.C., Nehring, R.B., Wojcik, S.M., and Rosenmund, C. (2011). Interplay between VGLUT isoforms and endophilin A1 regulates neurotransmitter release and short-term plasticity. Neuron 69, 1147-1159.
60. Wu, Y., Wang, W., Diez-Sampedro, A., and Richerson, G.B. (2007). Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56, 851-865.
61. Zander, J.F., Munster-Wandowski, A., Brunk, I., Pahner, I., Gomez-Lira, G., Heinemann, U., Gutierrez, R., Laube, G., and Ahnert-Hilger, G. (2010). Synaptic and vesicular coexistence of VGLUT and VGAT in selected excitatory and inhibitory synapses. J Neurosci 30, 7634-7645.
62. Zhang, H., Nei, H., and Dougherty, P.M. (2010). A p38 mitogen-activated protein kinase-dependent mechanism of disinhibition in spinal synaptic transmission induced by tumor necrosis factoralpha. J Neurosci 30, 12844-12855.
63. Zhao, C., Teng, E.M., Summers, R.G., Jr., Ming, G.L., and Gage, F.H. (2006). Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26, 3-11.
64. Zhao, S., Zhou, Y., Gross, J., Miao, P., Qiu, L., Wang, D., Chen, Q., and Feng, G. (2010). Fluorescent labeling of newborn dentate granule cells in GAD67-GFP transgenic mice: a genetic tool for the study of adult neurogenesis. PLoS One 5.