Genetic control of adult neurogenesis: Interplay of differentiation, proliferation and survival modulates new neurons function and memory circuits

Frontiers in Cellular Neuroscience

Volumn , Issue APR, 2013, Pages

  Farioli Vecchioli, Stefano ^a   Micheli, Laura ^a   Ceccarelli, Manuela ^a   Leonardi, Luca ^a   Tirone, Felice ^a  

^a CNR   (Italy)

Author keywords

Adult neurogenesis; Apoptosis; Btg1; Btg2; Dentate gyrus; Differentiation; Hippocampus; Learning and memory; PC3; Progenitor cells; Proliferation; Tis21

Indexed keywords

BRAIN NERVE CELL; BTG1 GENE; BTG2 GENE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; DENTATE GYRUS; GENE; GENETIC REGULATION; HIPPOCAMPUS; HUMAN; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; REVIEW; SUBVENTRICULAR ZONE;

EID: 84876444339     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00059     Document Type: Review

References (114)

1. Aimone, J. B., Deng, W., and Gage, F. H. (2011). Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70, 589-596
2. Aimone, J. B., Wiles, J., and Gage, F. H. (2006). Potential role for adult neurogenesis in the encoding of time in new memories. Nat. Neurosci. 9, 723-727
3. Alvarez-Buylla, A., and Lim, D. A. (2004). For the long run: maintaining germinal niches in the adult brain. Neuron 41, 683-686
4. Amaral, D. G., and Witter, M. P. 1995 Hippocampal formation. In: Paxinos G, editor. The rat nervous system, 2nd ed. San Diego: Academic Press.
5. Ambrogini, P., Cuppini, R., Cuppini, C., Ciaroni, S., Cecchini, T., Ferri, P., Sartini, S., and Del Grande, P. (2000). Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci. Lett. 286, 21-24
6. Ambrogini, P., Lattanzi, D., Ciuffoli, S., Agostini, D., Bertini, L., Stocchi, V., Santi, S., and Cuppini, R. (2004). 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
7. Amiri, A., Cho, W., Zhou, J., Birnbaum, S. G., Sinton, C. M., McKay, R. M., and Parada, L. F. (2012). Pten deletion in adult hippocampal neural stem/progenitor cells causes cellular abnormalities and alters neurogenesis. J Neurosci. 32, 5880-5890
8. Attardo, A., Fabel, K., Krebs, J., Haubensak, W., Huttner, W. B., and Kempermann, G. (2010). Tis21 expression marks not only populations of neurogenic precursor cells but also new postmitotic neurons in adult hippocampal neurogenesis. Cereb. Cortex. 20, 304-314
9. Becker, S. (2005). A computational principle for hippocampal learning and neurogenesis. Hippocampus 15, 722-738
10. Boss, B. D., Peterson, G. M., and Cowan, W. M. (1985). On the number of neurons in the dentate gyrus of the rat. Brain Res. 338, 144-150
11. Bradbury, A., Possenti, R., Shooter, E. M., and Tirone, F. (1991). Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization. Proc. Natl. Acad. Sci. U.S.A. 88, 3353-3357
12. Bruel-Jungerman, E., Rampon, C., and Laroche, S. (2007). Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses. Rev. Neurosci. 18, 93-114
13. Buanne, P., Corrente, G., Micheli, L., Palena, A., Lavia, P., Spadafora, C., Lakshmana, M. K., Rinaldi, A., Banfi, S., Quarto, M., Bulfone, A., and Tirone, F. (2000). Cloning of PC3B, a novel member of the PC3/BTG/TOB family of growth inhibitory genes, highly expressed in the olfactory epithelium. Genomics 68, 253-263
14. Cameron, H. A., Woolley, C. S., Mcewen, B. S., and Gould, E. (1993). Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56, 337-344
15. Canzoniere, D., Farioli-Vecchioli, S., Conti, F., Ciotti, M. T., Tata, A. M., Augusti-Tocco, G., Mattei, E., Lakshmana, M. K., Krizhanovsky, V., Reeves, S. A., Giovannoni, R., Castano, F., Servadio, A., Ben-Arie, N., and Tirone, F. (2004). Dual control of neurogenesis by PC3 through cell cycle inhibition and induction of Math1 J. Neurosci. 24, 3355-3369
16. Chawla, M. K., Guzowski, J. F., Ramirez-Amaya, V., Lipa, P., Hoffman, K. L., Marriott, L. K., Worley, P. F., McNaughton, B. L., and Barnes, C. A. (2005). Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15, 579-586
17. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D. Jr., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., and Bussey, T. J. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213
18. Corrente, G., Guardavaccaro, D., and Tirone, F. (2002) PC3 potentiates NGF induced differentiation and protects neurons from apoptosis. NeuroReport 13, 417-422
19. Cortes, U., Moyret-Lalle, C., Falette, N., Duriez, C., Ghissassi, F. E., Barnas, C., Morel, A. P., Hainaut, P., Magaud, J. P., and Puisieux, A. (2000). BTG gene expression in the p53-dependent and -independent cellular response to DNA damage. Mol. Carcinog. 27, 57-64
20. Creer, D. J., Romberg, C., Saksida, L. M., van Praag, H., and Bussey, T. J. (2010). Running enhances spatial pattern separation in mice. Proc. Natl. Acad. Sci. U.S.A. 107, 2367-2372
21. Döbrössy, M. D., Drapeau, E., Aurousseau, C., Le Moal, M., Piazza, P. V., and Abrous, D. N. (2003). Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol. Psychiatry 8, 974-982
22. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716
23. Dupret, D., Fabre, A., Döbrössy, M. D., Panatier, A., Rodríguez, J. J., Lamarque, S., Lemaire, V., Oliet, S. H., Piazza, P. V., and Abrous, D. N. (2007). Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol. 5(8), e214
24. Dupret, D., Montaron, M. F., Drapeau, E., Aurousseau, C., Le Moal, M., Piazza, P. V., and Abrous, D. N. (2005). Methylazoxymethanol acetate does not fully block cell genesis in the young and aged dentate gyrus. Eur. J. Neurosci. 22, 778-783.
25. el-Ghissassi, F., Valsesia-Wittmann, S., Falette, N., Duriez, C., Walden, P. D., and Puisieux, A. (2002). BTG2(TIS21/PC3) induces neuronal differentiation and prevents apoptosis of terminally differentiated PC12 cells. Oncogene 21, 6772-6778
26. Espósito, 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
27. Farioli-Vecchioli, S., Cinà, I., Ceccarelli, M., Micheli, L., Leonardi, L., Ciotti, M. T., De Bardi, M., Di Rocco, C., Pallini, R., Cavallaro, S., and Tirone, F. (2012a). Tis21 knock-out enhances the frequency of medulloblastoma in Patched1 heterozygous mice by inhibiting the Cxcl3-dependent migration of cerebellar neurons. J. Neurosci. 32, 15547-15564
28. Farioli-Vecchioli, S., Micheli, L., Saraulli, D., Ceccarelli, M., Cannas, S., Scardigli, R., Leonardi, L., Cinà, I., Costanzi, M., Ciotti, M. T., Moreira, P., Rouault, J.-P., Cestari, V., and Tirone, F. (2012b) Btg1 is required to maintain the pool of stem and progenitor cells of the dentate gyrus and subventricular zone. Front. Neurosci. 6, 124
29. Farioli-Vecchioli, S., Saraulli, D., Costanzi, M., Leonardi, L., Cinà, I., Micheli, L., Nutini, M., Longone, P., Oh, S. P., Cestari, V., and Tirone, F. (2009). Impaired terminal differentiation of hippocampal granule neurons and defective contextual memory in PC3/Tis21 knockout mice. PLoS One 4(12), e8339
30. Farioli-Vecchioli, S., Saraulli, D., Costanzi, M., Pacioni, S., Cinà, I., Aceti, M., Micheli, L., Bacci, A., Cestari, V., and Tirone, F. (2008). The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol. 6(10), e246
31. Farioli-Vecchioli, S., Tanori, M., Micheli, L., Mancuso, M., Leonardi, L., Saran, A., Ciotti, M. T., Ferretti, E., Gulino, A., Pazzaglia, S., and Tirone, F. (2007). Inhibition of medulloblastoma tumorigenesis by the antiproliferative and pro-differentiative gene PC3 FASEB J. 21, 2215-2225
32. Filippov, V., Kronenberg, G., Pivneva, T., Reuter, K., Steiner, B., Wang, L. P., Yamaguchi, M., Kettenmann, H., and Kempermann, G. (2003) Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 23, 373-382
33. Fletcher, B. S., Lim, R. W., Varnum, B. C., Kujubu, D. A., Koski, R. A., and Herschman, H. R. (1991). Structure and expression of TIS21, a primary response gene induced by growth factors and tumor promoters. J. Biol. Chem. 266, 14511-14518
34. Frankland, P. W., and Bontempi, B. (2005). The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119-130
35. 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
36. Garthe, A., Behr, J., and Kempermann, G. (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 4(5), e5464 Epub 2009 May 7
37. 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
38. Ge, S., Yang, C. H., Hsu, K. S., Ming, G. L., and Song, H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54, 559-566
39. Gobeske, K. T., Das, S., Bonaguidi, M. A., Weiss, C., Radulovic, J., Disterhoft, J. F., and Kessler, J. A. (2009). BMP signaling mediates effects of exercise on hippocampal neurogenesis and cognition in mice. PLoS One 4(10), e7506
40. Gutiérrez, R., Romo-Parra, H., Maqueda, J., Vivar, C., Ramìrez, 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
41. Guzowski, J. F., Miyashita, T., Chawla, M. K., Sanderson, J., Maes, L. I., Houston, F. P., Lipa, P., McNaughton, B. L., Worley, P. F., and Barnes, C. A. (2006). Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc. Natl. Acad. Sci. U.S.A. 103, 1077-1082
42. Guzowski, J. F., Timlin, J. A., Roysam, B., McNaughton, B. L., Worley, P. F., and Barnes, C. A. (2005). Mapping behaviorally relevant neural circuits with immediateearly gene expression. Curr. Opin. Neurobiol. 15, 599-606
43. Hämmerle, B., and Tejedor, F. J. (2007). A novel function of DELTA-NOTCH signalling mediates the transition from proliferation to neurogenesis in neural progenitor cells. PLoS ONE 2(11), e1169
44. Hastings, N. B., and Gould, E. (1999). Rapid extension of axons into the CA3 region by adult generated granule cells. J. Comp. Neurol. 413, 146-154
45. Henze, D. A., Wittner, L., and Buzsaki, G. (2002). Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 5, 790-5
46. Iacopetti, P., Barsacchi, G., Tirone, F., Maffei, L., and Cremisi, F. (1994). Developmental expression of PC3 gene is correlated with neuronal cell birthday. Mech. Dev. 47, 127-137
47. Iacopetti, P., Michelini, M., Stuckmann, I., Oback, B., Aaku-Saraste, E., and Huttner, W. B. (1999). Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identities single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl. Acad. Sci. U.S.A. 96, 4639-4644
48. Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K., and Kageyama, R. (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 30, 3489-3498
49. Ishizuka, N., Weber, J., and Amaral, D. G. (1990). Organization of intrahippocampal pro-jections originating from CA3 pyramidal cells in the rat. J. Comp. Neurol. 295, 580-623
50. Jacobs, D. M., Sano, M., Dooneief, G., Marder, K., Bell, K. L., and Stern, Y. (1995). Neuropsychological detection and characterization of preclinical Alzheimer's disease. Neurology 45, 957-962
51. Kee, N., Teixeira, C. M., Wang, A. H., and Frankland, P. W. (2007). Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10, 355-362
52. Kempermann, G., Jessberger, S., Steiner, B., and Kronenberg, G. (2004). Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27, 447-452
53. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495
54. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997b). Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc.Natl.Acad. Sci.U.S.A. 94, 10409-10414
55. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1998). Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18, 3206-3212
56. Kim, W. R., Park, O. H., Choi, S., Choi, S. Y., Park, S. K., Lee, K. J., Rhyu, I. J., Kim, H., Lee, Y. K., Kim, H. T., Oppenheim, R. W., and Sun, W. (2009). The maintenance of specific aspects of neuronal function and behavior is dependent on programmed cell death of adult-generated neurons in the dentate gyrus. Eur. J. Neurosci. 29, 1408-1421
57. Kippin, T. E., Martens, D. J., and van der Kooy, D. (2005). p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 19, 756-767
58. Kronenberg, G., Reuter, K., Steiner, B., Brandt, M. D., Jessberger, S., Yamaguchi, M., and Kempermann, G. (2003). Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467, 455-463
59. Kuhn, H. G., Dickinson-Anson, H., and Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033
60. Laplagne, D. A., Espósito, M. S., Piatti, V. C., Morgenstern, N. A., Zhao, C., van Praag, H., Gage, F. H., and Schinder, A. F. (2006). Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4(12), e409
61. Laplagne, D. A., Kamienkowski, J. E., Espósito, M. S., Piatti, V. C., Zhao, C., Gage, F. H., and Schinder, A. F. (2007). Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur. J. Neurosci. 25, 2973-2981
62. Lazarov, O. and Demars, M. P. (2012). All in the family: how the APPs regulate neurogenesis. Front. Neurosci. 6, 81
63. Lee, E. Y., Hu, N., Yuan, S. S., Cox, L. A., Bradley, A., Lee, W. H., and Herrup, K. (1994). Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes Dev. 8, 2008-2021
64. Leutgeb, J. K., Leutgeb, S., Moser, M. B., and Moser, E. I. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966
65. Lin, W. J., Gary, J. D., Yang, M. C., Clarke, S., and Herschman, H. R. (1996). The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J. Biol. Chem. 271, 15034-15044
66. Madsen, T. M., Kristjansen, P. E., Bolwig, T. G, and Wörtwein, G. (2003). Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119, 635-642
67. Manns, M., Bichler, Z., Leske, O., and Heumann, R. (2010). Neuronal Ras activation inhibits adult hippocampal progenitor cell division and impairs spatial short-term memory. Genes Brain Behav. 9, 525-536
68. Marr, D., 1971 Simple memory: a theory for archicortex. Phil. Trans. R. Soc., London B 262, 23-81
69. Matsuda, S., Rouault, J., Magaud, J., and Berthet, C. (2001). In search of a function for the TIS21/PC3/BTG1/TOB family. FEBS Lett. 497, 67-72
70. Miyashita, T., Kubik, S., Lewandowski, G., and Guzowski, J. F. (2008). Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol. Learn. Mem. 89, 269-284
71. Mongiat, L. A., Esposito, M. S., Lombardi, G., and Schinder, A. F. (2009). Reliable activation of immature neurons in the adult hippocampus. PLoS ONE 4, e5320
72. Moscovitch, M., Rosenbaum, R. S., Gilboa, A., Addis, D. R., Westmacott, R., Grady, C., McAndrews, M. P., Levine, B., Black, S., Winocur, G., and Nadel, L. (2005). Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J. Anat. 207, 35-66
73. Mu, Y., and Gage, F. H. (2011). Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol. Neurodegener. 6, 85
74. Nadel, L., and Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217-227
75. Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., Rodriguez Barrera, V., Chittajallu, R., Iwamoto, K. S., McBain, C. J., Fanselow, M. S., and Tonegawa, S. (2012). Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149, 188-201
76. 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
77. Passeri, D., Marcucci, A., Rizzo, G., Billi, M., Panigada, M., Leonardi, L., Tirone, F., and Grignani, F. (2006). Btg2 enhances retinoic acid-induced differentiation by modulating histone H4 methylation and acetylation. Mol. Cell. Biol. 26, 5023-5032
78. Petrik, D., Jiang, Y., Birnbaum, S. G., Powell, C. M., Kim, M. S., Hsieh, J., and Eisch, A. J. (2012). Functional and mechanistic exploration of an adult neurogenesispromoting small molecule. FASEB J. 26, 3148-3162
79. Prévôt, D., Morel, A. P., Voeltzel, T., Rostan, M. C., Rimokh, R., Magaud, J. P., and Corbo, L. (2001). Relationships of the antiproliferative proteins BTG1 and BTG2 with CAF1, the human homolog of a component of the yeast CCR4 transcriptional complex: involvement in estrogen receptor alpha signaling pathway. J. Biol. Chem. 276, 9640-9648
80. Prévôt, D., Voeltzel, T., Birot, A. M., Morel, A. P., Rostan, M. C., Magaud, J. P., and Corbo, L. (2000). The leukemia-associated protein Btg1 and the p53-regulated protein Btg2 interact with the homeoprotein Hoxb9 and enhance its transcriptional activation. J. Biol. Chem. 275, 147-153
81. Qian, Z., Gilbert, M. E., Colicos, M. A., Kandel, E. R., and Kuhl, D. (1993). Tissueplasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361, 453-457
82. Raber, J., Rola, R., LeFevour, A., Morhardt, D., Curley, J., Mizumatsu, S., VandenBerg, S. R., and Fike, J. R. (2004). Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res. 162, 39-47
83. Rapp, P. R., Deroche, P. S., Mao, Y., and Burwell, R. D. (2002). Neuron number in the parahippocampal region is preserved in aged rats with spatial learning deficits. Cereb. Cortex. 12, 1171-1179
84. Rolls, E. T., and Kesner, R. P. (2006). A computational theory of hippocampal function, and empirical tests of the theory. Prog. Neurobiol. 79, 1-48 Epub 2006 Jun 14
85. Rolls, E. T. (2010). A computational theory of episodic memory formation in the hippocampus. Behav. Brain Res. 215, 180-196
86. Rouault, J. P., Falette, N., Guehennuux, F, Guillot, C., Rimokh, R., Wang, Q., Berthet, C., Moyret-Lalle, C., Savatier, P., Pain, B., Shaw, P., Berger, R., Samarut, J., Magaud, J. P., Ozturk, M., Samarut, C., and Puisieux, A. 1996 Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat. Genet. 14, 482-486
87. Rouault, J. P., Prevot, D., Berthet, C., Birot, A. M., Billaud, M., Magaud, J. P., and Corbo, L. (1998). Interaction of BTG1 and p53-regulated BTG2 gene products with mCaf1, the murine homolog of a component of the yeast CCR4 transcriptional regulatory complex. J. Biol. Chem. 273, 22563-22569
88. Rouault, J. P., Rimokh, R., Tessa, C., Paranhos, G., French, M., Duret, L., Garoccio, M., Germain, D., Samarut, J., and Magaud, J. P. (1992). BTG1, a member of a new family of antiproliferative genes. EMBO J. 11, 1663-1670
89. Rudkin, B. B., Lazarovici, P., Levi, B. Z., Abe, Y., Fujita, K., and Guroff, G. (1989). Cell cycle-specific action of nerve growth factor in PC12 cells: differentiation without proliferation. EMBO J. 8, 3319-3325
90. Sahay, A., Wilson, D. A., and Hen, R. (2011). Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70, 582-588
91. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C., and Hen R. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809
92. Saxe, M. D., Battaglia, F., Wang, J. W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D, Sofroniew, M. V., Kandel, E. R., Santarelli, L., Hen, R., and Drew, M. R. (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 103, 17501-17506
93. Saxe, M. D., Malleret, G., Vronskaya, S., Mendez, I., Garcia, A. D., Sofroniew, M. V., Kandel, E. R., and Hen, R. (2007). Paradoxical influence of hippocampal neurogenesis on working memory. Proc. Natl. Acad. Sci. U.S.A. 104, 4642-4646
94. Schmidt-Hieber, C., Jonas, P., and Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429, 184-187
95. Selvaraj, V., Jiang, P., Chechneva, O., Lo, U. G., and Deng, W. (2012). Differentiating human stem cells into neurons and glial cells for neural repair. Front. Biosci. 17, 65-89
96. Seri, B., Garcia-Verdugo, J. M, McEwen, B. S., and Alvarez-Buylla, A. (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21, 7153-7160
97. Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., and Gould, E. (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376
98. Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., and Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocampal dependent learning. Hippocampus 12, 578-584
99. Sionov, R. V., Hayon, I. L., and Haupt, Y. The Regulation of p53 Growth Suppression. In: Madame Curie Bioscience Database [Internet]. Austin (TX): Landes Bioscience; 2000-. Available from: http://www.ncbi.nlm.nih.gov/books/NBK6412/
100. Sirri, A., Bianchi, V., Pelizzola, M., Mayhaus, M., Ricciardi-Castagnoli, P., Toniolo, D., and D'Adamo, P. (2010). Temporal gene expression profile of the hippocampus following trace fear conditioning. Brain Res. 1308, 14-23
101. Snyder, J. S., Hong, N. S., McDonald, R. J., and Wojtowicz, J. M. (2005). A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843-852
102. Snyder, J. S., Kee, N., and Wojtowicz, J. M. (2001). Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol. 85, 2423-2431
103. Tashiro, A., Makino, H., and Gage, F. H. (2007). Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci. 27, 3252-3259
104. Tirone, F. (2001). The gene PC3(TIS21/BTG2), prototype member of the PC3/BTG/TOB family: regulator in control of cell growth, differentiation, and DNA repair? J. Cell. Physiol. 187, 155-165
105. Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., Gage, F. H., and Schinder, A. F. (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci. 11, 901-907
106. Treves, A., Tashiro, A., Witter, M. P, and Moser, E. I. (2008). What is the mammalian dentate gyrus good for? Neuroscience 154, 1155-1172
107. Vallès, A., Boender, A. J., Gijsbers, S., Haast, R. A., Martens, G. J., and de Weerd, P. (2011). Genomewide analysis of rat barrel cortex reveals time-and layer-specific mRNA expression changes related to experience-dependent plasticity. J. Neurosci. 31, 6140-6158.
108. van Praag, H., Christie, B. R., Sejnowski, T. J., and Gage, F. H. (1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 13427-13431.
109. van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034
110. Wang, J. W., David, D. J., Monckton, J. E., Battaglia, F., and Hen, R. (2008). Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J. Neurosci. 28, 1374-1384
111. Wang, S, Scott, B. W., and Wojtowicz, J. M. (2000). Heterogenous properties of dentate granule neurons in the adult rat. J. Neurobiol. 42, 248-257
112. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660
113. 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
114. 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(9). doi, pii, e12506.