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생화학분자생물학회 (Korean Society for Biochemistry and Molecular Biology)
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Cell-intrinsic signals that regulate adult neurogenesis in vivo: insights from inducible approaches

  • Johnson, Madeleine A. (Department of Psychiatry, University of Texas Southwestern Medical Center) ;
  • Ables, Jessica L. (Department of Psychiatry, University of Texas Southwestern Medical Center) ;
  • Eisch, Amelia J. (Department of Psychiatry, University of Texas Southwestern Medical Center)
  • 발행 : 2009.05.31
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초록

The process by which adult neural stem cells generate new and functionally integrated neurons in the adult mammalian brain has been intensely studied, but much more remains to be discovered. It is known that neural progenitors progress through distinct stages to become mature neurons, and this progression is tightly controlled by cell-cell interactions and signals in the neurogenic niche. However, less is known about the cell-intrinsic signaling required for proper progression through stages of adult neurogenesis. Techniques have recently been developed to manipulate genes specifically in adult neural stem cells and progenitors in vivo, such as the use of inducible transgenic mice and viral-mediated gene transduction. A critical mass of publications utilizing these techniques has been reached, making it timely to review which molecules are now known to play a cell-intrinsic role in regulating adult neurogenesis in vivo. By drawing attention to these isolated molecules (e.g. Notch), we hope to stimulate a broad effort to understand the complex and compelling cascades of intrinsic signaling molecules important to adult neurogenesis. Understanding this process opens the possibility of understanding brain functions subserved by neurogenesis, such as memory, and also of harnessing neural stem cells for repair of the diseased and injured brain.

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참고문헌

  1. Altman, J. and Das, G. D. (1966) Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 126, 337-389 https://doi.org/10.1002/cne.901260302
  2. Nottebohm, F. (2002) Neuronal replacement in adult brain. Brain Res. Bull. 57, 737-749 https://doi.org/10.1016/S0361-9230(02)00750-5
  3. Kempermann, G. (2005) Adult neurogenesis: stem cells and neuronal development in the adult brain; Kempermann G. (ed.), p. 448 Oxford University, USA
  4. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A. and Gage, F. H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317 https://doi.org/10.1038/3305
  5. Curtis, M. A., Kam, M., Nannmark, U., Anderson, M. F., Axell, M. Z., Wikkelso, C., Holtas, S., van Roon-Mom, W. M., Bjork-Eriksson, T., Nordborg, C., Frisen, J., Dragunow, M., Faull, R. L. and Eriksson, P. S. (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315, 1243-1249 https://doi.org/10.1126/science.1136281
  6. Roybon, L., Hjalt, T., Stott, S., Guillemot, F., Li, J. Y. and Brundin, P. (2009) Neurogenin2 directs granule neuroblast production and amplification while NeuroD1 specifies neuronal fate during hippocampal neurogenesis. PLoS. ONE 4, e4779 https://doi.org/10.1371/journal.pone.0004779
  7. Kempermann, G. (2004) Stem cells in the healthy and diseased adult brain. Nervenheilkunde 23, 90-93
  8. Ortega-Perez, I., Murray, K. and Lledo, P. M. (2007) The how and why of adult neurogenesis. J. Mol. Histol. 38, 555-562 https://doi.org/10.1007/s10735-007-9114-5
  9. Ko, H. G., Jang, D. J., Son, J., Kwak, C., Choi, J. H., Ji, Y. H., Lee, Y. S., Son, H. and Kaang, B. K. (2009) Effect of ablated hippocampal neurogenesis on the formation and extinction of contextual fear memory. Mol. Brain 2, 1 https://doi.org/10.1186/1756-6606-2-1
  10. Eisch, A. J. (2002) Adult neurogenesis: implications for psychiatry. Prog. Brain Res. 138, 315-342 https://doi.org/10.1016/S0079-6123(02)38085-3
  11. Eisch, A. J., Cameron, H. A., Encinas, J. M., Meltzer, L. A., Ming, G. L. and Overstreet-Wadiche, L. S. (2008) Adult neurogenesis, mental health, and mental illness: hope or hype? J. Neurosci. 28, 11785-11791 https://doi.org/10.1523/JNEUROSCI.3798-08.2008
  12. Vandenbosch, R., Borgs, L., Beukelaers, P., Belachew, S., Moonen, G., Nguyen, L. and Malgrange, B. (2009) Adult neurogenesis and the diseased brain. Curr. Med. Chem. 16, 652-666 https://doi.org/10.2174/092986709787458371
  13. Kempermann, G., Krebs, J. and Fabel, K. (2008) The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr. Opin. Psychiatry 21, 290-295 https://doi.org/10.1097/YCO.0b013e3282fad375
  14. Ormerod, B. K., Palmer, T. D. and Caldwell, M. A. (2008) Neurodegeneration and cell replacement. Philos. Trans R. Soc. Lond B. Biol. Sci. 363, 153-170 https://doi.org/10.1098/rstb.2006.2018
  15. Abrous, D. N., Koehl, M. and Le Moal, M. (2005) Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85, 523-569 https://doi.org/10.1152/physrev.00055.2003
  16. Ming, G. L. and Song, H. (2005) Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28, 223-250 https://doi.org/10.1146/annurev.neuro.28.051804.101459
  17. Gould, E. (2007) How widespread is adult neurogenesis in mammals? Nat. Rev. Neurosci. 8, 481-488 https://doi.org/10.1038/nrn2147
  18. Ehninger, D. and Kempermann, G. (2008) Neurogenesis in the adult hippocampus. Cell Tissue Res. 331, 243-250 https://doi.org/10.1007/s00441-007-0478-3
  19. Imayoshi, I., Sakamoto, M., Ohtsuka, T. and Kageyama, R. (2009) Continuous neurogenesis in the adult brain. Dev. Growth Differ. 51, 379-386 https://doi.org/10.1111/j.1440-169X.2009.01094.x
  20. Quinones-Hinojosa, A., Sanai, N., Soriano-Navarro, M., Gonzalez-Perez, O., Mirzadeh, Z., Gil-Perotin, S., Romero- Rodriguez, R., Berger, M. S., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2006) Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol. 494, 415-434 https://doi.org/10.1002/cne.20798
  21. Lledo, P. M., Alonso, M. and Grubb, M. S. (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7, 179-193 https://doi.org/10.1038/nrn1867
  22. Toni, N., Teng, E. M., Bushong, E. A., Aimone, J. B., Zhao, C., Consiglio, A., van Praag, H., Martone, M. E., Ellisman, M. H. and Gage, F. H. (2007) Synapse formation on neurons born in the adult hippocampus. Nat. Neurosci. 10, 727-734 https://doi.org/10.1038/nn1908
  23. Kempermann, G., Jessberger, S., Steiner, B. and Kronenberg, G. (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27, 447-452 https://doi.org/10.1016/j.tins.2004.05.013
  24. Alvarez-Buylla, A. and Lim, D. A. (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41, 683-686 https://doi.org/10.1016/S0896-6273(04)00111-4
  25. Breunig, J. J., Sarkisian, M. R., Arellano, J. I., Morozov, Y. M., Ayoub, A. E., Sojitra, S., Wang, B., Flavell, R. A., Rakic, P. and Town, T. (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 13127-13132 https://doi.org/10.1073/pnas.0804558105
  26. Hagg, T. (2009) From neurotransmitters to neurotrophic factors to neurogenesis. Neuroscientist 15, 20-27 https://doi.org/10.1177/1073858408324789
  27. Maccioni, R. B., Otth, C., Concha, II and Munoz, J. P. (2001) The protein kinase Cdk5. Structural aspects, roles in neurogenesis and involvement in Alzheimer's pathology. Eur. J. Biochem. 268, 1518-1527 https://doi.org/10.1046/j.1432-1327.2001.02024.x
  28. Yoon, K. and Gaiano, N. (2005) Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 8, 709-715 https://doi.org/10.1038/nn1475
  29. Gage, F. H., Coates, P. W., Palmer, T. D., Kuhn, H. G., Fisher, L. J., Suhonen, J. O., Peterson, D. A., Suhr, S. T. and Ray, J. (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl. Acad. Sci. U.S.A. 92, 11879-11883 https://doi.org/10.1073/pnas.92.25.11879
  30. Cameron, H. A. and McKay, R. D. (1999) Restoring production of hippocampal neurons in old age. Nat. Neurosci. 2, 894-897 https://doi.org/10.1038/13197
  31. Luo, J., Daniels, S. B., Lennington, J. B., Notti, R. Q. and Conover, J. C. (2006) The aging neurogenic subventricular zone. Aging. Cell 5, 139-152 https://doi.org/10.1111/j.1474-9726.2006.00197.x
  32. Alvarez-Buylla, A., Garcia-Verdugo, J. M. and Tramontin, A. D. (2001) A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2, 287-293 https://doi.org/10.1038/35067582
  33. Temple, S. (2001) The development of neural stem cells. Nature 414, 112-117 https://doi.org/10.1038/35102174
  34. Gotz, M. and Barde, Y. A. (2005) Radial glial cells defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 46, 369-372 https://doi.org/10.1016/j.neuron.2005.04.012
  35. Duan, X., Kang, E., Liu, C. Y., Ming, G. L. and Song, H. (2008) Development of neural stem cell in the adult brain.Curr. Opin. Neurobiol. 18, 108-115 https://doi.org/10.1016/j.conb.2008.04.001
  36. Jordan, J. D., Ma, D. K., Ming, G. L. and Song, H. (2007) Cellular niches for endogenous neural stem cells in the adult brain. CNS. Neurol. Disord. Drug. Targets 6, 336-341 https://doi.org/10.2174/187152707783220866
  37. Riquelme, P. A., Drapeau, E. and Doetsch, F. (2008) Brain micro-ecologies: neural stem cell niches in the adult mammalian brain. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363, 123-137 https://doi.org/10.1098/rstb.2006.2016
  38. Basak, O. and Taylor, V. (2009) Stem cells of the adult mammalian brain and their niche. Cell Mol. Life Sci. 66, 1057-1072 https://doi.org/10.1007/s00018-008-8544-x
  39. Alvarez-Buylla, A., Kohwi, M., Nguyen, T. M. and Merkle, F. T. (2008) The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb. Symp. Quant. Biol. 357-366. doi: 10.1101/sqb.2008.73. 019
  40. Morrison, S. J. and Spradling, A. C. (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132, 598-611 https://doi.org/10.1016/j.cell.2008.01.038
  41. Fan, X. T., Xu, H. W., Cai, W. Q., Yang, H. and Liu, S. (2004) Antisense Noggin oligodeoxynucleotide administration decreases cell proliferation in the dentate gyrus of adult rats. Neurosci. Lett. 366, 107-111 https://doi.org/10.1016/j.neulet.2004.05.043
  42. Galvao, R. P., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2008) Brain-derived neurotrophic factor signaling does not stimulate subventricular zone neurogenesis in adult mice and rats. J. Neurosci. 28, 13368-13383 https://doi.org/10.1523/JNEUROSCI.2918-08.2008
  43. Lie, D. C., Colamarino, S. A., Song, H. J., Desire, L., Mira, H., Consiglio, A., Lein, E. S., Jessberger, S., Lansford, H., Dearie, A. R. and Gage, F. H. (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375 https://doi.org/10.1038/nature04108
  44. Suhonen, J., Ray, J., Blomer, U., Gage, F. H. and Kaspar, B. (2006) Ex vivo and in vivo gene delivery to the brain. Curr. Protoc. Hum. Genet. Chapter 13, Unit 13.3.1-13.3.25
  45. Tashiro, A., Zhao, C. and Gage, F. H. (2006) Retrovirusmediated single-cell gene knockout technique in adult newborn neurons in vivo. Nat. Protoc. 1, 3049-3055 https://doi.org/10.1038/nprot.2006.473
  46. 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 https://doi.org/10.1038/4151030a
  47. van Hooijdonk, L. W., Ichwan, M., Dijkmans, T. F., Schouten, T. G., de Backer, M. W., Adan, R. A., Verbeek, F. J., Vreugdenhil, E. and Fitzsimons, C. P. (2009) Lentivirusmediated transgene delivery to the hippocampus reveals sub-field specific differences in expression. BMC. Neurosci. 10, 2 https://doi.org/10.1186/1471-2202-10-2
  48. Consiglio, A., Gritti, A., Dolcetta, D., Follenzi, A., Bordignon, C., Gage, F. H., Vescovi, A. L. and Naldini, L. (2004) Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc. Natl. Acad. Sci. U.S.A. 101, 14835-14840 https://doi.org/10.1073/pnas.0404180101
  49. Geraerts, M., Eggermont, K., Hernandez-Acosta, P., Garcia- Verdugo, J. M., Baekelandt, V. and Debyser, Z. (2006) Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum. Gene Ther. 17, 635-650 https://doi.org/10.1089/hum.2006.17.635
  50. Kafri, T., van Praag, H., Gage, F. H. and Verma, I. M. (2000) Lentiviral vectors: regulated gene expression. Mol. Ther. 1, 516-521 https://doi.org/10.1006/mthe.2000.0083
  51. Namba, T., Mochizuki, H., Onodera, M., Mizuno, Y., Namiki, H. and Seki, T. (2005) The fate of neural progenitor cells expressing astrocytic and radial glial markers in the postnatal rat dentate gyrus. Eur. J. Neurosci. 22, 1928-1941 https://doi.org/10.1111/j.1460-9568.2005.04396.x
  52. 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 https://doi.org/10.1016/S1044-7431(03)00060-5
  53. Brown, J. P., Couillard-Despres, S., Cooper-Kuhn, C. M., Winkler, J., Aigner, L. and Kuhn, H. G. (2003) Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467, 1-10 https://doi.org/10.1002/cne.10874
  54. Feil, S., Valtcheva, N. and Feil, R. (2009) Inducible cre mice. Methods Mol. Biol. 530, 1-21 https://doi.org/10.1007/978-1-59745-471-1_1
  55. Mori, T., Tanaka, K., Buffo, A., Wurst, W., Kuhn, R. and Gotz, M. (2006) Inducible gene deletion in astroglia and radial glia--a valuable tool for functional and lineage analysis. Glia. 54, 21-34 https://doi.org/10.1002/glia.20350
  56. Hirrlinger, P. G., Scheller, A., Braun, C., Hirrlinger, J. and Kirchhoff, F. (2006) Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen- inducible DNA recombinase variant CreERT2. Glia. 54, 11-20 https://doi.org/10.1002/glia.20342
  57. Lagace, D. C., Whitman, M. C., Noonan, M. A., Ables, J. L., DeCarolis, N. A., Arguello, A. A., Donovan, M. H., Fischer, S. J., Farnbauch, L. A., Beech, R. D., DiLeone, R. J., Greer, C. A., Mandyam, C. D. and Eisch, A. J. (2007) Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 27, 12623-12629 https://doi.org/10.1523/JNEUROSCI.3812-07.2007
  58. Ganat, Y. M., Silbereis, J., Cave, C., Ngu, H., Anderson, G. M., Ohkubo, Y., Ment, L. R. and Vaccarino, F. M. (2006) Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J. Neurosci. 26, 8609-8621 https://doi.org/10.1523/JNEUROSCI.2532-06.2006
  59. Chen, J., Kelz, M. B., Zeng, G., Sakai, N., Steffen, C., Shockett, P. E., Picciotto, M. R., Duman, R. S. and Nestler, E. J. (1998) Transgenic animals with inducible, targeted gene expression in brain. Mol. Pharmacol. 54, 495-503 https://doi.org/10.1124/mol.54.3.495
  60. Yu, T. S., Dandekar, M., Monteggia, L. M., Parada, L. F. and Kernie, S. G. (2005) Temporally regulated expression of Cre recombinase in neural stem cells. Genesis 41, 147-153 https://doi.org/10.1002/gene.20110
  61. Sprengel, R. and Hasan, M. T. (2007) Tetracycline-controlled genetic switches. Handb. Exp. Pharmacol. 178, 49-72 https://doi.org/10.1007/978-3-540-35109-2_3
  62. Lagace, D. C., Benavides, D. R., Kansy, J. W., Mapelli, M., Greengard, P., Bibb, J. A. and Eisch, A. J. (2008) Cdk5 is essential for adult hippocampal neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 18567-18571 https://doi.org/10.1073/pnas.0810137105
  63. Bergami, M., Rimondini, R., Santi, S., Blum, R., Gotz, M. and Canossa, M. (2008) Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc. Natl. Acad. Sci. U.S.A. 105, 15570-15575 https://doi.org/10.1073/pnas.0803702105
  64. Beech, R. D., Cleary, M. A., Treloar, H. B., Eisch, A. J., Harrist, A. V., Zhong, W., Greer, C. A., Duman, R. S. and Picciotto, M. R. (2004) Nestin promoter/enhancer directs transgene expression to precursors of adult generated periglomerular neurons. J. Comp. Neurol. 475, 128-141 https://doi.org/10.1002/cne.20179
  65. Sun, Y., Chen, X. and Xiao, D. (2007) Tetracycline-inducible expression systems: new strategies and practices in the transgenic mouse modeling. Acta. Biochim. Biophys. Sin. (Shanghai) 39, 235-246 https://doi.org/10.1111/j.1745-7270.2007.00258.x
  66. Zhu, Z., Zheng, T., Lee, C. G., Homer, R. J. and Elias, J. A. (2002) Tetracycline-controlled transcriptional regulation systems: advances and application in transgenic animal modeling. Semin. Cell Dev. Biol. 13, 121-128 https://doi.org/10.1016/S1084-9521(02)00018-6
  67. Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., Mori, K., Ikeda, T., Itohara, S. and Kageyama, R. (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 11, 1153-1161 https://doi.org/10.1038/nn.2185
  68. Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C. H., Kernie, S. G., Bassel-Duby, R. and Parada, L. F. (2008) TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59, 399-412 https://doi.org/10.1016/j.neuron.2008.06.023
  69. Zhang, C. L., Zou, Y., He, W., Gage, F. H. and Evans, R. M. (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451, 1004-1007 https://doi.org/10.1038/nature06562
  70. Carlen, M., Meletis, K., Barnabe-Heider, F. and Frisen, J. (2006) Genetic visualization of neurogenesis. Exp. Cell Res. 312, 2851-2859 https://doi.org/10.1016/j.yexcr.2006.05.012
  71. Imayoshi, I., Ohtsuka, T., Metzger, D., Chambon, P. and Kageyama, R. (2006) Temporal regulation of Cre recombinase activity in neural stem cells. Genesis 44, 233-238 https://doi.org/10.1002/dvg.20212
  72. Radtke, F., Schweisguth, F. and Pear, W. (2005) The Notch 'gospel'. EMBO. Rep. 6, 1120-1125 https://doi.org/10.1038/sj.embor.7400585
  73. Bray, S. J. (2006) Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689 https://doi.org/10.1038/nrm2009
  74. Kageyama, R., Ohtsuka, T., Hatakeyama, J. and Ohsawa, R. (2005) Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306, 343-348 https://doi.org/10.1016/j.yexcr.2005.03.015
  75. Artavanis-Tsakonas, S., Rand, M. D. and Lake, R. J. (1999) Notch signaling: cell fate control and signal integration in development. Science 284, 770-776 https://doi.org/10.1126/science.284.5415.770
  76. Alexson, T. O., Hitoshi, S., Coles, B. L., Bernstein, A. and van der Kooy, D. (2006) Notch signaling is required to maintain all neural stem cell populations--irrespective of spatial or temporal niche. Dev. Neurosci. 28, 34-48 https://doi.org/10.1159/000090751
  77. Carlson, M. E. and Conboy, I. M. (2007) Regulating the Notch pathway in embryonic, adult and old stem cells. Curr. Opin. Pharmacol. 7, 303-309 https://doi.org/10.1016/j.coph.2007.02.004
  78. Corbin, J. G., Gaiano, N., Juliano, S. L., Poluch, S., Stancik, E. and Haydar, T. F. (2008) Regulation of neural progenitor cell development in the nervous system. J. Neurochem. 106, 2272-2287 https://doi.org/10.1111/j.1471-4159.2008.05522.x
  79. Breunig, J. J., Silbereis, J., Vaccarino, F. M., Sestan, N. and Rakic, P. (2007) Notch regulates cell fate and dendrite morphology of newborn neurons in the postnatal dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 104, 20558-20563 https://doi.org/10.1073/pnas.0710156104
  80. Salama-Cohen, P., Arevalo, M. A., Meier, J., Grantyn, R. and Rodriguez-Tebar, A. (2005) NGF controls dendrite development in hippocampal neurons by binding to p75 NTR and modulating the cellular targets of Notch. Mol. Biol. Cell 16, 339-347 https://doi.org/10.1091/mbc.E04-05-0438
  81. Salama-Cohen, P., Arevalo, M. A., Grantyn, R. and Rodriguez-Tebar, A. (2006) Notch and NGF/p75NTR control dendrite morphology and the balance of excitatory/inhibitory synaptic input to hippocampal neurones through Neurogenin 3. J. Neurochem. 97, 1269-1278 https://doi.org/10.1111/j.1471-4159.2006.03783.x
  82. Schousboe, A. and Waagepetersen, H. S. (2006) Glial modulation of GABAergic and glutamat ergic neurotransmission. Curr. Top. Med. Chem. 6, 929-934 https://doi.org/10.2174/156802606777323719
  83. Hartfuss, E., Galli, R., Heins, N. and Gotz, M. (2001) Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229, 15-30 https://doi.org/10.1006/dbio.2000.9962
  84. 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 https://doi.org/10.1126/science.1083328
  85. Jessberger, S., Toni, N., Clemenson, G. D., Jr., Ray, J. and Gage, F. H. (2008) Directed differentiation of hippocampal stem/progenitor cells in the adult brain. Nat. Neurosci. 11, 888-893 https://doi.org/10.1038/nn.2148
  86. Pleasure, S. J., Collins, A. E. and Lowenstein, D. H. (2000) Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J. Neurosci. 20, 6095-6105
  87. Kim, E. J., Leung, C. T., Reed, R. R. and Johnson, J. E. (2007) In vivo analysis of Ascl1 defined progenitors reveals distinct developmental dynamics during adult neurogenesis and gliogenesis. J. Neurosci. 27, 12764-12774 https://doi.org/10.1523/JNEUROSCI.3178-07.2007
  88. Chambers, C. B., Peng, Y., Nguyen, H., Gaiano, N., Fishell, G. and Nye, J. S. (2001) Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128, 689-702
  89. Carlen, M., Meletis, K., Goritz, C., Darsalia, V., Evergren, E., Tanigaki, K., Amendola, M., Barnabe-Heider, F., Yeung, M. S., Naldini, L., Honjo, T., Kokaia, Z., Shupliakov, O., Cassidy, R. M., Lindvall, O. and Frisen, J. (2009) Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat. Neurosci. 12, 259- 267 https://doi.org/10.1038/nn.2268
  90. Cicero, S. and Herrup, K. (2005) Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation. J. Neurosci. 25, 9658-9668 https://doi.org/10.1523/JNEUROSCI.1773-05.2005
  91. Zhang, J. and Herrup, K. (2008) Cdk5 and the non-catalytic arrest of the neuronal cell cycle. Cell Cycle 7, 3487-3490 https://doi.org/10.4161/cc.7.22.7045
  92. Xie, Z., Samuels, B. A. and Tsai, L. H. (2006) Cyclin-dependent kinase 5 permits efficient cytoskeletal remodeling-- a hypothesis on neuronal migration. Cereb. Cortex. 16 (Suppl. 1), i64-68
  93. Dhariwala, F. A. and Rajadhyaksha, M. S. (2008) An unusual member of the Cdk family: Cdk5. Cell Mol. Neurobiol. 28, 351-369 https://doi.org/10.1007/s10571-007-9242-1
  94. Ohshima, T., Ward, J. M., Huh, C. G., Longenecker, G., Veeranna, Pant, H. C., Brady, R. O., Martin, L. J. and Kulkarni, A. B. (1996) Targeted disruption of the cyclin- dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. U.S.A. 93, 11173-11178 https://doi.org/10.1073/pnas.93.20.11173
  95. Jessberger, S., Aigner, S., Clemenson, G. D., Jr., Toni, N., Lie, D. C., Karalay, O., Overall, R., Kempermann, G. and Gage, F. H. (2008) Cdk5 regulates accurate maturation of newborn granule cells in the adult hippocampus. PLoS Biol. 6, e272 https://doi.org/10.1371/journal.pbio.0060272
  96. Sananbenesi, F., Fischer, A., Wang, X., Schrick, C., Neve, R., Radulovic, J. and Tsai, L. H. (2007) A hippocampal Cdk5 pathway regulates extinction of contextual fear. Nat. Neurosci. 10, 1012-1019 https://doi.org/10.1038/nn1943
  97. Goldman, S. A. (1998) Adult neurogenesis: from canaries to the clinic. J. Neurobiol. 36, 267-286 https://doi.org/10.1002/(SICI)1097-4695(199808)36:2<267::AID-NEU12>3.0.CO;2-B
  98. Tonchev, A. B., Yamashima, T., Guo, J., Chaldakov, G. N. and Takakura, N. (2007) Expression of angiogenic and neurotrophic factors in the progenitor cell niche of adult monkey subventricular zone. Neuroscience 144, 1425- 1435 https://doi.org/10.1016/j.neuroscience.2006.10.052
  99. Giuliani, A., D'Intino, G., Paradisi, M., Giardino, L. and Calza, L. (2004) p75 (NTR)-immunoreactivity in the subventricular zone of adult male rats: expression by cycling cells. J. Mol. Histol. 35, 749-758 https://doi.org/10.1007/s10735-004-9609-2
  100. Okano, H. J., Pfaff, D. W. and Gibbs, R. B. (1996) Expression of EGFR-, p75NGFR-, and PSTAIR (cdc2)-like immunoreactivity by proliferating cells in the adult rat hippocampal formation and forebrain. Dev. Neurosci. 18, 199-209 https://doi.org/10.1159/000111408
  101. Donovan, M. H., Yamaguchi, M. and Eisch, A. J. (2008) Dynamic expression of TrkB receptor protein on proliferating and maturing cells in the adult mouse dentate gyrus. Hippocampus 18, 435-439 https://doi.org/10.1002/hipo.20410
  102. Malberg, J. E., Eisch, A. J., Nestler, E. J. and Duman, R. S. (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104-9110
  103. Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C. and Croll, S. (2005) Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192, 348-356 https://doi.org/10.1016/j.expneurol.2004.11.016
  104. Bath, K. G., Mandairon, N., Jing, D., Rajagopal, R., Kapoor, R., Chen, Z. Y., Khan, T., Proenca, C. C., Kraemer, R., Cleland, T. A., Hempstead, B. L., Chao, M. V. and Lee, F. S. (2008) Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J. Neurosci. 28, 2383-2393 https://doi.org/10.1523/JNEUROSCI.4387-07.2008
  105. Sotthibundhu, A., Li, Q. X., Thangnipon, W. and Coulson, E. J. (2008) Abeta (1-42) stimulates adult SVZ neurogenesis through the p75 neurotrophin receptor. Neurobiol. Aging published online: doi: 10.1016/j.neurobiolaging.2008.02.004
  106. Patapoutian, A. and Reichardt, L. F. (2001) Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11, 272-280 https://doi.org/10.1016/S0959-4388(00)00208-7
  107. Reichardt, L. F. (2006) Neurotrophin-regulated signalling pathways. Philos. Trans R. Soc. Lond. B. Biol. Sci. 361, 1545-1564 https://doi.org/10.1098/rstb.2006.1894
  108. Skaper, S. D. (2008) The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS. Neurol. Disord Drug Targets 7, 46-62 https://doi.org/10.2174/187152708783885174
  109. Li, G. and Pleasure, S. J. (2005) Morphogenesis of the dentate gyrus: what we are learning from mouse mutants. Dev. Neurosci. 27, 93-99 https://doi.org/10.1159/000085980
  110. Morris, D. C., Zhang, Z. G., Wang, Y., Zhang, R. L., Gregg, S., Liu, X. S. and Chopp, M. (2007) Wnt expression in the adult rat subventricular zone after stroke. Neurosci. Lett. 418, 170-174 https://doi.org/10.1016/j.neulet.2007.03.039
  111. Madsen, T. M., Newton, S. S., Eaton, M. E., Russell, D. S. and Duman, R. S. (2003) Chronic electroconvulsive seizure up-regulates beta-catenin expression in rat hippocampus: role in adult neurogenesis. Biol. Psychiatry 54, 1006-1014 https://doi.org/10.1016/S0006-3223(03)00700-5
  112. Wexler, E. M., Geschwind, D. H. and Palmer, T. D. (2008) Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation. Mol. Psychiatry 13, 285-292 https://doi.org/10.1038/sj.mp.4002093
  113. Lim, D. A., Tramontin, A. D., Trevejo, J. M., Herrera, D. G., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713-726 https://doi.org/10.1016/S0896-6273(00)00148-3
  114. Bonaguidi, M. A., Peng, C. Y., McGuire, T., Falciglia, G., Gobeske, K. T., Czeisler, C. and Kessler, J. A. (2008) Noggin expands neural stem cells in the adult hippocampus. J. Neurosci. 28, 9194-9204 https://doi.org/10.1523/JNEUROSCI.3314-07.2008
  115. Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D., Jr., Consiglio, A., Lie, D. C., Squire, L. R. and Gage, F. H. (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Mem. 16, 147-154 https://doi.org/10.1101/lm.1172609
  116. Colak, D., Mori, T., Brill, M. S., Pfeifer, A., Falk, S., Deng, C., Monteiro, R., Mummery, C., Sommer, L. and Gotz, M. (2008) Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J. Neurosci. 28, 434-446 https://doi.org/10.1523/JNEUROSCI.4374-07.2008
  117. Millar, J. K., Wilson-Annan, J. C., Anderson, S., Christie, S., Taylor, M. S., Semple, C. A., Devon, R. S., Clair, D. M., Muir, W. J., Blackwood, D. H. and Porteous, D. J. (2000) Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet 9, 1415-1423 https://doi.org/10.1093/hmg/9.9.1415
  118. Duan, X., Chang, J. H., Ge, S., Faulkner, R. L., Kim, J. Y., Kitabatake, Y., Liu, X. B., Yang, C. H., Jordan, J. D., Ma, D. K., Liu, C. Y., Ganesan, S., Cheng, H. J., Ming, G. L., Lu, B. and Song, H. (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130, 1146-1158 https://doi.org/10.1016/j.cell.2007.07.010
  119. Mao, Y., Ge, X., Frank, C. L., Madison, J. M., Koehler, A. N., Doud, M. K., Tassa, C., Berry, E. M., Soda, T., Singh, K. K., Biechele, T., Petryshen, T. L., Moon, R. T., Haggarty, S. J. and Tsai, L. H. (2009) Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta catenin signaling. Cell 136, 1017-1031 https://doi.org/10.1016/j.cell.2008.12.044
  120. Gao, X., Arlotta, P., Macklis, J. D. and Chen, J. (2007) Conditional knock-out of beta-catenin in postnatal-born dentate gyrus granule neurons results in dendritic malformation. J. Neurosci. 27, 14317-14325 https://doi.org/10.1523/JNEUROSCI.3206-07.2007
  121. Platel, J. C., Lacar, B. and Bordey, A. (2007) GABA and glutamate signaling: homeostatic control of adult forebrain neurogenesis. J. Mol. Histol. 38, 602-610
  122. Vicini, S. (2008) The role of GABA and glutamate on adult neurogenesis. J. Physiol. 586, 3737-3738 https://doi.org/10.1113/jphysiol.2008.159046
  123. Tashiro, A., Sandler, V. M., Toni, N., Zhao, C. and Gage, F. H. (2006) NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442, 929-933 https://doi.org/10.1038/nature05028
  124. Cameron, H. A., McEwen, B. S. and Gould, E. (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci. 15, 4687-4692
  125. T. D. and Malenka, R. C. (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42, 535-552 https://doi.org/10.1016/S0896-6273(04)00266-1
  126. Joo, J. Y., Kim, B. W., Lee, J. S., Park, J. Y., Kim, S., Yun, Y. J., Lee, S. H., Rhim, H. and Son, H. (2007) Activation of NMDA receptors increases proliferation and differentiation of hippocampal neural progenitor cells. J. Cell Sci. 120, 1358-1370 https://doi.org/10.1242/jcs.002154
  127. Gandhi, R., Luk, K. C., Rymar, V. V. and Sadikot, A. F. (2008) Group I mGluR5 metabotropic glutamate receptors regulate proliferation of neuronal progenitors in specific forebrain developmental domains. J. Neurochem. 104, 155-172
  128. Ye, G. L., Yi, S., Gamkrelidze, G., Pasternak, J. F. and Trommer, B. L. (2005) AMPA and NMDA receptor-mediated currents in developing dentate gyrus granule cells. Brain Res. Dev. Brain. Res. 155, 26-32 https://doi.org/10.1016/j.devbrainres.2004.12.002
  129. Suzuki, M., Nelson, A. D., Eickstaedt, J. B., Wallace, K., Wright, L. S. and Svendsen, C. N. (2006) Glutamate enhances proliferation and neurogenesis in human neural progenitor cell cultures derived from the fetal cortex. Eur. J. Neurosci. 24, 645-653 https://doi.org/10.1111/j.1460-9568.2006.04957.x
  130. Di Giorgi-Gerevini, V., Melchiorri, D., Battaglia, G., Ricci-Vitiani, L., Ciceroni, C., Busceti, C. L., Biagioni, F., Iacovelli, L., Canudas, A. M., Parati, E., De Maria, R. and Nicoletti, F. (2005) Endogenous activation of metabotropic glutamate receptors supports the proliferation and survival of neural progenitor cells. Cell Death Differ 12, 1124-1133 https://doi.org/10.1038/sj.cdd.4401639
  131. Owens, D. F. and Kriegstein, A. R. (2002) Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715-727 https://doi.org/10.1038/nrn919
  132. Markwardt, S. and Overstreet-Wadiche, L. (2008) GABA ergic signalling to adult-generated neurons. J. Physiol. 586, 3745-3749 https://doi.org/10.1113/jphysiol.2008.155713
  133. Wang, D. D. and Kriegstein, A. R. (2009) Defining the Role of GABA in Cortical Development. J. Physiol. 587, 1873-1879 https://doi.org/10.1113/jphysiol.2008.167635
  134. 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 https://doi.org/10.1016/j.tins.2006.11.001
  135. Lee, H., Chen, C. X., Liu, Y. J., Aizenman, E. and Kandler, K. (2005) KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur. J. Neurosci. 21, 2593-2599 https://doi.org/10.1111/j.1460-9568.2005.04084.x
  136. Kriegstein, A. R. and Owens, D. F. (2001) GABA may act as a self-limiting trophic factor at developing synapses. Sci. STKE. 95, PE1 https://doi.org/10.1126/stke.2001.95.pe1
  137. Tozuka, Y., Fukuda, S., Namba, T., Seki, T. and Hisatsune, T. (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47, 803-815 https://doi.org/10.1016/j.neuron.2005.08.023
  138. Deisseroth, K. and Malenka, R. C. (2005) GABA excitation in the adult brain: a mechanism for excitationneurogenesis coupling. Neuron 47, 775-777 https://doi.org/10.1016/j.neuron.2005.08.029
  139. Doetsch, F. and Hen, R. (2005) Young and excitable: the function of new neurons in the adult mammalian brain. Curr. Opin. Neurobiol. 15, 121-128 https://doi.org/10.1016/j.conb.2005.01.018
  140. 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 https://doi.org/10.1152/jn.00633.2005
  141. Ge, S., Sailor, K. A., Ming, G. L. and Song, H. (2008) Synaptic integration and plasticity of new neurons in the adult hippocampus. J. Physiol. 586, 3759-3765 https://doi.org/10.1113/jphysiol.2008.155655
  142. 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 https://doi.org/10.1038/nature04404
  143. Akiba, Y., Sasaki, H., Huerta, P. T., Estevez, A. G., Baker, H. and Cave, J. W. (2009) gamma-Aminobutyric acid-mediated regulation of the activity-dependent olfactory bulb dopaminergic phenotype. J. Neurosci. Res. published online: doi: 10.1002/jnr.22055
  144. Carlezon, W. A., Jr., Duman, R. S. and Nestler, E. J. (2005) The many faces of CREB. Trends. Neurosci. 28, 436-445 https://doi.org/10.1016/j.tins.2005.06.005
  145. Giachino, C., De Marchis, S., Giampietro, C., Parlato, R., Perroteau, I., Schutz, G., Fasolo, A. and Peretto, P. (2005) cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J. Neurosci. 25, 10105-10118 https://doi.org/10.1523/JNEUROSCI.3512-05.2005
  146. Nakagawa, S., Kim, J. E., Lee, R., Chen, J., Fujioka, T., Malberg, J., Tsuji, S. and Duman, R. S. (2002) Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J. Neurosci. 22, 9868-9876
  147. Ahn, S., Olive, M., Aggarwal, S., Krylov, D., Ginty, D. D. and Vinson, C. (1998) A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus- dependent transcription of c-fos. Mol. Cell Biol. 18, 967-977 https://doi.org/10.1128/MCB.18.2.967
  148. Mioduszewska, B., Jaworski, J. and Kaczmarek, L. (2003) Inducible cAMP early repressor (ICER) in the nervous system--a transcriptional regulator of neuronal plasticity and programmed cell death. J. Neurochem. 87, 1313-1320 https://doi.org/10.1046/j.1471-4159.2003.02116.x
  149. Gur, T. L., Conti, A. C., Holden, J., Bechtholt, A. J., Hill, T. E., Lucki, I., Malberg, J. E. and Blendy, J. A. (2007) cAMP response element-binding protein deficiency allows for increased neurogenesis and a rapid onset of antidepressant response. J. Neurosci. 27, 7860-7868
  150. Alberini, C. M. (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 89, 121-145 https://doi.org/10.1152/physrev.00017.2008
  151. Kim, J. H., Lee, J. H., Park, J. Y., Park, C. H., Yun, C. O., Lee, S. H., Lee, Y. S. and Son, H. (2005) Retrovirally transduced NCAM140 facilitates neuronal fate choice of hippocampal progenitor cells. J. Neurochem. 94, 417-424 https://doi.org/10.1111/j.1471-4159.2005.03208.x
  152. Seki, T. (2002) Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J. Neurosci. Res. 69, 772-783 https://doi.org/10.1002/jnr.10366
  153. Kuhn, H. G., Winkler, J., Kempermann, G., Thal, L. J. and Gage, F. H. (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17, 5820-5829
  154. Mudo, G., Bonomo, A., Di Liberto, V., Frinchi, M., Fuxe, K. and Belluardo, N. (2009) The FGF-2/FGFRs neurotrophic system promotes neurogenesis in the adult brain. J. Neural. Transm. published online: doi: 10.1007/s00702-009-0207-z
  155. Fabel, K., Tam, B., Kaufer, D., Baiker, A., Simmons, N., Kuo, C. J. and Palmer, T. D. (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 18, 2803-2812 https://doi.org/10.1111/j.1460-9568.2003.03041.x
  156. Warner-Schmidt, J. L. and Duman, R. S. (2007) VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc. Natl. Acad. Sci. U.S.A. 104, 4647-4652 https://doi.org/10.1073/pnas.0610282104

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  29. APP transgenic modeling of Alzheimer’s disease: mechanisms of neurodegeneration and aberrant neurogenesis vol.214, pp.2-3, 2010, https://doi.org/10.1007/s00429-009-0232-6
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