Delayed development of adult-generated granule cells in dentate gyrus

Journal of Neuroscience

Volumn 26, Issue 8, 2006, Pages 2326-2334

  Overstreet Wadiche, Linda S ^a   Bensen, AeSoon L ^a   Westbrook, Gary L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Activity dependent; Bromodeoxyuridine; Dentate gyrus; Depolarizing GABA; Development; GAD65; Giant depolarizing potential; Granule cell; Hippocampus; Neural stem cell; Neurogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMATE DECARBOXYLASE 65; TRANSCRIPTION FACTOR;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DENTATE GYRUS; DEVELOPMENTAL DISORDER; FUNCTIONAL ASSESSMENT; GRANULE CELL; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; AGING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CEREBELLUM NUCLEUS; COMPARATIVE STUDY; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; NERVE CELL; NERVE REGENERATION; PHYSIOLOGY; TIME;

AGING; ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; CELLS, CULTURED; CEREBELLAR NUCLEI; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; NERVE REGENERATION; NEURONS; TIME FACTORS;

EID: 33645640620     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4111-05.2006     Document Type: Article

References (56)

1. Adelsberger H, Garaschuk O, Konnerth A (2005) Calcium waves in resting newborn mice. Nat Neurosci 8:988-990.
2. Angevine Jr JB (1965) Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol Suppl 2:1-70.
3. Asada H, Kawamura Y, Maruyama K, Kume H, Ding R, Ji FY, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K (1996) 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 229:891-895.
4. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353-360.
5. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond) 416:303-325.
6. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
7. Cohen-Cory S (2002) The developing synapse: construction and modulation of synaptic structures and circuits. Science 298:770-776.
8. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
9. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC (2004) Excitation neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535-552.
10. Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074-10086.
11. Fujioka T, Fujioka A, Duman RS (2004) Activation of cAMP signaling facilitates the morphological maturation of newborn neurons in adult hippocampus. J Neurosci 24:319-328.
12. Gaudilliere B, Konishi Y, de la Iglesia N, Yao G, Bonni A (2004) A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis. Neuron 41:229-241.
13. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593.
14. Goldman SA (2005) Neurology and the stem cell debate. Neurology 64:1675-1676.
15. Guillery RW, Herrup K (1997) Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2-7.
16. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504-1508.
17. Hollrigel GS, Ross ST, Soltesz I (1998) Temporal patterns and depolarizing actions of spontaneous GABAA receptor activation in granule cells of the early postnatal dentate gyrus. J Neurophysiol 80:2340-2351.
18. Horch HW (2004) Local effects of BDNF on dendritic growth. Rev Neurosci 15:117-129.
19. Jin X, Hu H, Mathers PH, Agmon A (2003) Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J Neurosci 23:5662-5673.
20. Kash SF, Johnson RS, Tecott LH, Noebels JL, Mayfield RD, Hanahan D, Baekkeskov S (1997) Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 94:14060-14065.
21. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
22. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
23. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432:758-761.
24. Kruger GM, Mosher JT, Bixby S, Joseph N, Iwashita T, Morrison SJ (2002) Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35:657-669.
25. 2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 18:243-255.
26. Leinekugel X, Khalilov I, Ben-Ari, Khazipov R (1998) Giant depolarizing potentials: the septal pole of the hippocampus paces the activity of the developing intact septohippocampal complex in vitro. J Neurosci 18:6349-6357.
27. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsaki G (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296:2049-2052.
28. Liu X, Tilwalli S, Ye G, Lio PA, Pasternak JF, Trommer BL (2000) Morphologic and electrophysiologic maturation in developing dentate gyrus granule cells. Brain Res 856:202-212.
29. McAllister AK, Katz LC, Lo DC (1996) Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17:1057-1064.
30. Meijering M, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images cytometry. 58A:167-176.
31. Overstreet LS, Hentges ST, Bumaschny VF, de Souza FS, Smart JL, Santangelo AM, Low MJ, Westbrook GL, Rubinstein M (2004) A transgenic marker for newly born granule cells in dentate gyrus. J Neurosci 24:3251-3259.
32. Overstreet-Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol. 94:4528-4532.
33. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 9:715-727.
34. Pavlov I, Riekki R, Taira T (2004) Synergistic action of GABA-A and NMDA receptors in the induction of long-term depression in glutamatergic synapses in the newborn rat hippocampus. Eur J Neurosci 20:3019-3026.
35. Rakic P (2004) Immigration denied. Nature 427:685-686.
36. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK (2005) Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 21:464-476.
37. Redmond L, Kashani AH, Ghosh A (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34:999-1010.
38. Saghatelyan A, Roux P, Migliore M, Rochefort C, Desmaisons D, Charneau P, Shepherd GM, Lledo PM (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46:103-116.
39. Schlessinger AR, Cowan WM, Gottlieb DI (1975) An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159:149-175.
40. Seki T (2002) Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci Res 70:327-334.
41. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
42. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359-378.
43. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-1340.
44. Shieh PB, Hu SC, Bobb K, Timmusk T, Ghosh A (1998) Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20:727-740.
45. Soghomonian JJ, Martin DL (1998) Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci 19:500-505.
46. Song H-J, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44.
47. Staley KJ, Mody I (1992) Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J Neurophysiol 68:197-212.
48. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709-726.
49. Tian N, Petersen C, Kash S, Baekkeskov S, Copenhagen D, Nicoll R (1999) The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release. Proc Natl Acad Sci USA 96:12911-12916.
50. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803-815.
51. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
52. Wang LP, Kempermann G, Kettenmann H (2005) A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29:181-189.
53. Wong RO, Ghosh A (2002) Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3:803-812.
54. Ye GL, Yi S, Gamkrelidze G, Pasternak JF, Trommer BL (2005) AMPA and NMDA receptor-mediated currents in developing dentate gyrus granule cells. Brain Res Dev Brain Res 155:26-32.
55. Yu C, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
56. Zhao C, Teng EM, Summers Jr RG, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11.