GABA-mediated induction of early neuronal markers expression in postnatal rat progenitor cells in culture

Neuroscience

Volumn 224, Issue , 2012, Pages 210-222

  Ramirez M ^a   Hernandez Montoya J ^a   Sanchez Serrano S L ^a   Ordaz, B ^b   Ferraro, S ^a   Quintero, H ^a   Pena Ortega F ^b   Lamas, M ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

Author keywords

CREB; GABA; Histone acetyltransferase; M ller glia; Neural progenitors; Retina

Indexed keywords

4 AMINOBUTYRIC ACID; BETA TUBULIN; BETAIII TUBULIN; CALCIUM; CALCIUM CHANNEL L TYPE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HISTONE H4; NEUROGENIC DIFFERENTIATION FACTOR; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL COUNT; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; EPIGENETICS; GLIA CELL; HIPPOCAMPUS; HISTONE ACETYLATION; IMMUNOCYTOCHEMISTRY; MUELLER CELL; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RETINA STEM CELL; SIGNAL TRANSDUCTION; STEM CELL; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; NEURONS; RATS; RATS, LONG-EVANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84866514570     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.08.044     Document Type: Article

References (61)

1. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 2002, 9:728-739.
2. Bernardos R.I., Barthel L.K., Meyers J.R., Raymond P.A. Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 2007, 27:7028-7040.
3. Best J.L., Amezcua C.A., Mayr B., Flechner L., Murawsky C.M., Emerson B., Zor T., Gardner K.H., Montminy M. Identification of small-molecule antagonists that inhibit an activator:coactivator interaction. Proc Natl Acad Sci U S A 2004, 101(51):17622-17627.
4. Bordey A. Enigmatic GABAergic networks in adult neurogenic zones. Brain Res Rev 2007, 1:124-134.
5. Carrillo-Reid L., Tecuapetla F., Tapia D., Hernández-Cruz A., Galarraga E., Drucker-Colin R., Bargas J. Encoding network states by striatal cell assemblies. J Neurophysiol 2008, 99(3):1435-1450.
6. Cepko C.L., Austin C.P., Yang X., Alexiades M., Ezzeddine D. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 1996, 93:589-595.
7. Das A.V., Mallya K.B., Zhao X., Ahmad F., Bhattacharya S., Thoreson W.B., Hedge G.V., Ahmad I. Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 2006, 299:284-302.
8. Eilers J., Plant T.D., Marandi N., Konnerth A. GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones. J Physiol 2001, 536:429-437.
9. Fischer A.J., Reh T.A. Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nature Neurosci 2001, 4:247-252.
10. Fischer A.J., McGuire C.R., Dierks B.D., Reh T.A. Insulin and fibroblast growth factor 2 activate a neurogenic program in Müller glia of the chicken retina. J Neurosci 2002, 22(21):9387-9398.
11. Fischer A.J., Wang S.Z., Reh T.A. NeuroD induces the expression of visinin and calretinin by proliferating cells derived from toxin-damaged chicken retina. Dev Dyn 2004, 229(3):555-563.
12. Fischer A.J., Bongini R. Turning Müller glia into neural progenitors in the retina. Mol Neurobiol 2010, 42:199-209.
13. Giachino C., De Marchis S., Giampietro C., Parlato R., Perroteau I., Schütz G., Fasolo A., Peretto P. cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J Neurosci 2005, 25(44):10105-10118.
14. Gonzalez G.A., Montminy M.R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989, 59(4):675-680.
15. Gottlicher M., Minucci S., Zhu P., Kramer O.H., Schimpf A., Giavara S., Sleeman J.P., Lo Coco F., Nervi C., Pelicci P.G., Heinzel T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 2001, 20:6969-6978.
16. Greka A., Lipton S.A., Zhang D. Expression of GABA(C) receptor rho1 and rho2 subunits during development of the mouse retina. Eur J Neurosci 2000, 12:3575-3582.
17. Guo C., Stella S.L., Hirano A.A., Brecha N.C. Plasmalemmal and vesicular gamma-aminobutyric acid transporter expression in the developing mouse retina. J Comp Neurol 2009, 512(1):6-26.
18. Gutierrez C., McNally M., Canto-Soler M.V. Cytoskeleton proteins previously considered exclusive to ganglion cells are transiently expressed by all retinal neuronal precursors. BMC Dev Biol 2011, 22(11):46.
19. Hardingham G.E., Cruzalegui F.H., Chawla S., Bading H. Mechanisms controlling gene expression by nuclear calcium signals. Cell Calcium 1998, 23(2-3):131-134.
20. Hicks D., Courtois Y. The growth and behaviour of rat retinal Muller cells in vitro. 1. An improved method for isolation and culture. Exp Eye Res 1990, 51(2):119-129.
21. Hsieh J., Nakashima K., Kuwabara T., Mejia E., Gage F.H. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 2004, 101(47):16659-16664.
22. i in retinal neurons of postnatal rabbits. Vis Neurosci 1996, 13:441-447.
23. A receptor antagonists alter developing cone photoreceptor development in neonatal rabbit retina. Vis Neurosci 2000, 17:925-935.
24. Jagasia R., Steib K., Englberger E., Herold S., Faus-Kessler T., Saxe M., Gage F.H., Song H., Lie D.C. GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci 2009, 29(25):7966-7977.
25. Johannessen M., Delghandi M.P., Moens U. What turns CREB on?. Cell Signal 2004, 16(11):1211-1227.
26. Johnson J., Tian N., Caywood M.S., Reimer R.J., Edwards R.H., Copenhagen D.R. Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci 2003, 23:518-529.
27. Karl M.O., Hayes S., Nelson B.R., Tan K., Buckingham B., Reh T.A. Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci USA 2008, 105:19508-19513.
28. Karne A., Oakley D.M., Wong G.K., Wong R.O. Immunocytochemical localization of GABA, GABAA receptors, and synapse-associated proteins in the developing and adult ferret retina. Vis Neurosci 1997, 14:1097-1108.
29. Kasper L.H., Lerach S., Wang J., Wu S., Jeevan T., Brindle P.K. CBP/p300 double null cells reveal effect of coactivator level and diversity on CREB transactivation. EMBO J 2010, 29(21):3660-3672.
30. Lamas M., Lee-Rivera I., Ramírez M., López-Colomé A.M. d-Serine regulates CREB phosphorylation through NMDA receptor activation in glial cells from the retina. Neurosci Lett 2007, 427:55-60.
31. Marquardt T., Gruss P. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci 2002, 25:32-38.
32. Martins R.A.P., Pearson R.A. Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Res 2008, 1192:37-60.
33. Mejía-Toiber J., Márquez-Ramos J.A., Díaz-Muñoz M., Peña F., Aguilar M.B., Giordano M. Glutamatergic excitation and GABA release from a transplantable cell line. Cell Transplant 2010, 19(10):1307-1323.
34. Merz K., Herold S., Lie D.C. CREB in adult neurogenesis - master and partner in the development of adult-born neurons?. Eur J Neurosci 2011, 33(6):1078-1086.
35. Mitchell C.K., Huang B., Redburn-Johnson D.A. GABA(A) receptor immunoreactivity is transiently expressed in the developing outer retina. Vis Neurosci 1999, 16:1083-1088.
36. Mitchell C.K., Redburn D.A. GABA and GABA-A receptors are maximally expressed in association with cone synaptogenesis in neonatal rabbit retina. Brain Res Dev Brain Res 1996, 95:63-71.
37. Monnin J., Morand-Villeneuve N., Michel G., Hicks D., Versaux-Botteri C. Production of neurospheres from mammalian Müller cells in culture. Neurosci Lett 2007, 421:22-26.
38. Nakagawa S., Kim J.E., Lee R., Chen J., Fujioka T., Malberg J., Tsuji S., Duman R.S. Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 2002, 22(22):9868-9876.
39. Nakagawa S., Kim J.E., Lee R., Malberg J.E., Chen J., Steffen C., Zhang Y.J., Nestler E.J., Duman R.S. Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 2002, 22(9):3673-3682.
40. Nelson B.R., Ueki Y., Reardon S., Karl M.O., Georgi S., Hartman B.H., Lamba D.A., Reh T.A. Genome-wide analysis of Müller glial differentiation reveals a requirement for notch signaling in postmitotic cells to maintain the glial fate. PLoS One 2011, 6(8):e22817. 10.1371/journal.pone.0022817.
41. Nuñez J.L., McCarthy M.M. Evidence for an extended duration of GABA-mediated excitation in the developing male versus female hippocampus. Dev Neurobiol 2007, 67(14):1879-1890.
42. Obrietan K., Gao X.B., Van Den Pol A.N. Excitatory actions of GABA increase BDNF expression via a MAPK-CREB-dependent mechanism - a positive feedback circuit in developing neurons. J Neurophysiol 2002, 88(2):1005-1015.
43. Ogryzko V.V., Schiltz R.L., Russanova V., Howard B.H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996, 87(5):953-959.
44. Owens D.F., Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nat Rev Neurosci 2002, 3:715-727.
45. Peña F., Ordaz B., Balleza-Tapia H., Bernal-Pedraza R., Márquez-Ramos A., Carmona-Aparicio L., Giordano M. Beta-amyloid protein (25-35) disrupts hippocampal network activity: role of Fyn-kinase. Hippocampus 2010, 20(1):78-96.
46. Phiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 2001, 276:36734-36741.
47. Ramirez M., Lamas M. NMDA receptor mediates proliferation and CREB phosphorylation in postnatal Müller glia-derived retinal progenitors. Mol Vis 2009, 15:713-721.
48. 3H-GABA-accumulating cells in rabbit retina. J Comp Neurol 1986, 243:41-57.
49. Redburn-Johnson D. GABA as a developmental neurotransmitter in the outer plexiform layer of the vertebrate retina. Perspect Dev Neurobiol 1998, 5:261-267.
50. Reichling D.B., Kyrozis A., Wang J., MacDermott A.B. Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J Physiol 1994, 476(3):411-421.
51. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., Pirvola U., Saarma M., Kaila K. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999, 397(6716):251-255.
52. Salazar P., Velasco-Velázquez M.A., Velasco I. GABA effects during neuronal differentiation of stem cell. Neurochem Res 2008, 33(8):1546-1557.
53. Simon M.V., De Genaro P., Abraham C.E., de los Santos B., Rotstein N.P., Politi L.E. Müller glial cells induce stem cell properties in retinal progenitors in vitro and promote their further differentiation into photoreceptors. J Neurosci Res 2012, 90:407-421.
54. Takeda M., Takamiya A., Jiao J.-w., Cho K.S., Trevino S.G., Matsuda T., Chen D.F. α-Aminoadipate induces progenitor cell properties of Müller glia in adult mice. Invest Ophthalmol Vis Res 2008, 49:1142-1150.
55. Tozuka Y., Fukuda S., Namba T., Seki T., Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005, 47(6):803-815.
56. Young T.L., Cepko C.L. A role for ligand-gated ion channels in rod photoreceptor development. Neuron 2004, 41:867-879.
57. Young S.Z., Platel J.C., Nielsen J.V., Jensen N.A., Bordey A. GABA(A) increases calcium in subventricular zone astrocyte-like cells through L- and T-type voltage-gated calcium channels. Front Cell Neurosci 2010, 8:4-8.
58. A receptor activation. J Physiol 2003, 550:785-800.
59. Wu Y., Cutting G.R. Developmentally regulated expression of GABA receptor rho1 and rho2 subunits, L7 and cone-rod homeobox (CRX) genes in mouse retina. Brain Res 2001, 912:1-8.
60. Zhang L.L., Pathak H.R., Coulter D.A., Freed M.A., Vardi N. Shift of intracellular chloride concentration in ganglion and amacrine cells of developing mouse retina. J Neurophysiol 2006, 95:2404-2416.
61. Zhang L.L., Delpire E., Vardi N. NKCC1 does not accumulate chloride in developing retinal neurons. J Neurophysiol 2007, 98(1):266-277.