Adult neurogenesis: Basic concepts of signaling

Cell Cycle

Volumn 5, Issue 7, 2006, Pages 722-728

  Bordey, Angélique ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Blood vessel; Development; GABA; Hippocampus; Migration; Olfactory bulb; Progenitor; Proliferation; Stem cell

Indexed keywords

ADULTHOOD; BRAIN FUNCTION; BRAIN INJURY; BRAIN REGION; CELL COMMUNICATION; CELL STRUCTURE; CELL TYPE; EMBRYO DEVELOPMENT; ENVIRONMENT; EXTRACELLULAR MATRIX; GLIA; HUMAN; INFORMATION PROCESSING; MATURITY; MEMORY; MOLECULAR DYNAMICS; MOLECULE; NERVE CELL PLASTICITY; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROTRANSMISSION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION;

EID: 33645725577     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.7.2614     Document Type: Review

References (118)

1. Boulder Committee. Embryonic vertebrate central nervous system: Revised terminology. Anat Rec 1970; 166:257-61.
2. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 1969; 137:433-57.
3. Bryans WA. Mitotic activity in the brain of the adult rat. Anatomical Record 1959; 133:65-73.
4. Luskin MB. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993; 11:173-89.
5. Swarzenski BC, O'Malley KL, Todd RD. PTX-sensitive regulation of neurite outgrowth by the dopamine D3 receptor. Neuroreport 1996; 7:573-6.
6. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia VJ, Berger MS, Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004; 427:740-4.
7. Kirschenbaum B, Nedergaard M, Preuss A, Barami K, Fraser RA, Goldman SA. In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb Cortex 1994; 4:576-89.
8. Allen E. Cessation of mitosis in central nervous system of the albino rat. J Comp Neurol 1912; 22:547-68.
9. Smart I. The subependymal layer of the mouse brain and its cellular production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 1961; 116:325-49.
10. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994; 264:1145-8.
11. Doetsch F, Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA 1996; 93:14895-900.
12. Peretto P, Merighi A, Fasolo A, Bonfanti L. The subependymal layer in rodents: A site of structural plasticity and cell migration in the adult mammalian brain. Brain Res Bull 1999; 49:221-43.
13. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255:1707-10.
14. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der KD. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 1994; 13:1071-82.
15. Altman J. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 1963; 145:573-91.
16. Kishi K. Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J Comp Neurol 1987; 258:112-24.
17. Privat A, Leblond CP. The subependymal layer and neighboring region in the brain of the young rat. J Comp Neurol 1972; 146:277-302.
18. Blakemore WF. The ultrastructure of the subependymal plate in the rat. J Anat 1969; 104:423-33.
19. Sucher NJ, Deitcher DL. PCR and patch-clamp analysis of single neurons. Neuron 1995; 14:1095-1100.
20. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996; 271:978-81.
21. Jankovski A, Sotelo C. Subventricular zone-olfactory bulb migratory pathway in the adult mouse: Cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Neurol 1996; 371:376-96.
22. Peretto P, Merighi A, Fasolo A, Bonfanti L. Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull 1997; 42:9-21.
23. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 1997; 17:5046-61.
24. Mercier F, Kitasako JT, Hatton GI. Anatomy of the brain neurogenic zones revisited: Fractones and the fibroblast/macrophage network. J Comp Neurol 2002; 451:170-88.
25. Bonfanti L, Theodosis DT. Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 1994; 62:291-305.
26. Yang HK, Sundholm-Peters NL, Goings GE, Walker AS, Hyland K, Szele FG. Distribution of doublecortin expressing cells near the lateral ventricles in the adult mouse brain. J Neurosci Res 2004; 76:282-95.
27. Bolteus AJ, Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 2004; 24:7623-31.
28. Braun N, Sevigny J, Mishra SK, Robson SC, Barth SW, Gerstberger R, Hammer K, Zimmermann H. Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur J Neurosci 2003; 17:1355-64.
29. Liu X, Wang Q, Haydar TF, Bordey A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci 2005; 8:1179-87.
30. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J Comp Neurol 1971; 141:283-312.
31. Rakic P. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 1971; 33:471-6.
32. Rakic P, Cameron RS, Komuro H. Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr Opin Neurobiol 1994; 4:63-9.
33. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004; 478:359-78.
34. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000; 425:479-94.
35. Wurmser AE, Palmer TD, Gage FH. Neuroscience: Cellular interactions in the stem cell niche. Science 2004; 304:1253-5.
36. Virgintino D, Maiorano E, Errede M, Vimercati A, Greco P, Selvaggi L, Roncali L, Bertossi M. Astroglia-microvessel relationship in the developing human telencephalon. Int J Dev Biol 1998; 42:1165-8.
37. Chanas-Sacre G, Rogister B, Moonen G, Leprince P. Radial glia phenotype: Origin, regulation, and transdifferentiation. J Neurosci Res 2000; 61:357-63.
38. Schmechel DE, Rakic P. A Golgi study of radial glial cells in developing monkey telencephalon: Morphogenesis and transformation into astrocytes. Anat Embryol (Berl) 1979; 156:115-52.
39. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999; 97:703-16.
40. Capela A, Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002; 35:865-75.
41. Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA. Identification of a multi-potent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 2000; 97:13883-8.
42. Chiasson BJ, Tropepe V, Morshead CM, van der KD. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 1999; 19:4462-71.
43. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002; 36:1021-34.
44. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 2004; 7:1233-41.
45. Coskun V, Wu H, Biancotti JC, Krueger RC, Kumar S, de Vellis J, Sun YE. CD133 expressing adult neural stem cells in the postnatal forebrain ependyma. Soc Neurosci Abstr 2005; 15:141.
46. Alvarez-Buylla A, Seri B, Doetsch F. Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 2002; 57:751-8.
47. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001; 2:287-93.
48. Alvarez-Buylla A, Theelen M, Nottebohm F. Proliferation "hot spots" in adult avian ventricular zone reveal radial cell division. Neuron 1990; 5:101-9.
49. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001; 21:7153-60.
50. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001; 409:714-20.
51. Malatesta P, Hartfuss E, Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000; 127:5253-63.
52. Hartfuss E, Galli R, Heins N, Gotz M. Characterization of CNS precursor subtypes and radial glia. Dev Biol 2001; 229:15-30.
53. Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 2004; 101:17528-32.
54. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 2005; 25:10-8.
55. Gates MA, Thomas LB, Howard EM, Laywell ED, Sajin B, Faissner A, Gotz B, Silver J, Steindler DA. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J Comp Neurol 1995; 361:249-66.
56. Wallraff A, Odermatt B, Willecke K, Steinhauser C. Distinct types of astroglial cells in the hippocampus differ in gap junction coupling. Glia 2004; 48:36-43.
57. Montgomery DL. Astrocytes: Forms, functions, and roles in disease. Vet Pathol 1994; 31:145-67.
58. Hagg T. Molecular regulation of adult CNS neurogenesis: An integrated view. Trends Neurosci 2005; 28:589-95.
59. Nguyen L, Malgrange B, Breuskin I, Bettendorff L, Moonen G, Belachew S, Rigo JM. Autocrine/paracrine activation of the GABA(A) receptor inhibits the proliferation of neurogenic polysialylated neural cell adhesion molecule-positive (PSA-NCAM+) precursor cells from postnatal striatum. J Neurosci 2003; 23:3278-94.
60. Stewart RR, Hoge GJ, Zigova T, Luskin MB. Neural progenitor cells of the neonatal rat anterior subventricular zone express functional GABA(A) receptors. J Neurobiol 2002; 50:305-22.
61. A receptor activation. J Physiol (Lond) 2003; 550:785-800.
62. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA 1999; 96:11619-24.
63. Barker JL, Behar T, Li YX, Liu QY, Ma W, Maric D, Maric I, Schaffner AE, Serafini R, Smith SV, Somogyi R, Vautrin JY, Wen XL, Xian H. GABAergic cells and signals in CNS development. Perspect Dev Neurobiol 1998; 5:305-22.
64. Owens DF, Kriegstein AR. Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 2002; 3:715-27.
65. Ben Ari Y. Excitatory actions of gaba during development: The nature of the nurture. Nat Rev Neurosci 2002; 3:728-39.
66. Kettenmann H, Backus KH, Schachner M. Gamma-aminobutyric acid opens Cl-channels in cultured astrocytes. Brain Res 1987; 404:1-9.
67. Bekar LK, Walz W. Intracellular chloride modulates A-type potassium currents in astrocytes. Glia 2002; 39:207-16.
68. Marty A, Llano I. Excitatory effects of GABA in established brain networks. Trends Neurosci 2005; 28:284-9.
69. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005; 47:803-15.
70. Wang LP, Kempermann G, Kettenmann H. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 2005; 29:181-9.
71. Nguyen L, Rigo JM, Rocher V, Belachew S, Malgrange B, Rogister B, Leprince P, Moonen G. Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 2001; 305:187-202.
72. Meier E, Hertz L, Schousboe A. Neurotransmitters as developmental signals. Neurochem Int 1991; 19:1-15.
73. Haydar TF, Wang F, Schwartz ML, Rakic P. Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 2000; 20:5764-74.
74. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995; 15:1287-98.
75. Haydar TF, Wang F, Schwartz ML, Rakic P. Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 2000; 20:5764-74.
76. Bardakdjian J, Tardy M, Pimoule C, Gonnard P. GABA metabolism in cultured glial cells. Neurochem Res 1979; 4:517-27.
77. Kopp HG, Avecilla ST, Hooper AT, Rafii S. The bone marrow vascular niche: Home of HSC differentiation and mobilization. Physiology (Bethesda) 2005; 20:349-56.
78. Louissaint Jr A, Rao S, Leventhal C, Goldman SA. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 2002; 34:945-60.
79. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246:1306-9.
80. Breier G, Albrecht U, Sterrer S, Risau W. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 1992; 114:521-32.
81. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004; 304:1338-40.
82. Leventhal C, Rafii S, Rafii D, Shahar A, Goldman SA. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 1999; 13:450-64.
83. Wu DK, Maciag T, de Vellis J. Regulation of neuroblast proliferation by hormones and growth factors in chemically defined medium. J Cell Physiol 1988; 136:367-72.
84. Peterson DA. Stem cells in brain plasticity and repair. Curr Opin Pharmacol 2002; 2:34-42.
85. Gould E, Tanapat P, Rydel T, Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry 2000; 48:715-20.
86. Goy RW. Early hormonal influences on the dvelopment of sexual and sex related behavior. In: Schmitt FO, ed. Neurosciences: Second study program. New York: Rockefeller University Press, 1970:196-207.
87. Goldman PS, Brown RM. the influence of neonatal androgen on the development of cortical function in the Rhesus Monkey. Soc Neurosci Abstr 1975; 1:495.
88. Ventura R, Harris KM. Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 1999; 19:6897-906.
89. Reichenbach A, Siegel A, Rickmann M, Wolff JR, Noone D, Robinson SR. Distribution of Bergmann glial somata and processes: Implications for function. J Hirnforsch 1995; 36:509-17.
90. Spacek J. Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol (Berl) 1985; 171:245-52.
91. Xu-Friedman MA, Harris KM, Regehr WG. Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J Neurosci 2001; 21:6666-72.
92. Nilsson M, Eriksson PS, Ronnback L, Hansson E. GABA induces Ca2+ transients in astrocytes. Neuroscience 1993; 54:605-14.
93. Fraser DD, Duffy S, Angelides KJ, Perez-Velazquez JL, Kettenmann H, MacVicar BA. GABAA/benzodiazepine receptors in acutely isolated hippocampal astrocytes. J Neurosci 1995; 15:2720-32.
94. Borden LA. GABA transporter heterogeneity: Pharmacology and cellular localization. Neurochem Int 1996; 29:335-56.
95. Kinney GA, Spain WJ. Synaptically evoked GABA transporter currents in neocortical glia. J Neurophysiol 2002; 88:2899-908.
96. Dingledine R, Korn SJ. Gamma-aminobutyric acid uptake and the termination of inhibitory synaptic potentials in the rat hippocampal slice. J Physiol (Lond) 1985; 366:387-409.
97. Hablitz JJ, Lebeda FJ. Role of uptake in gamma-aminobutyric acid (GABA)-mediated responses in guinea pig hippocampal neurons. Cell Mol Neurobiol 1985; 5:353-71.
98. Rekling JC, Jahnsen H, Mosfeldt Laursen A. The effect of two lipophilic gamma-aminobutyric acid uptake blockers in CA1 of the rat hippocampal slice. Br J Pharmacol 1990; 99:103-6.
99. Riquelme R, Miralles CP, de Blas AL. Bergmann glia GABA(A) receptors concentrate on the glial processes that wrap inhibitory synapses. J Neurosci 2002; 22:10720-30.
100. Mong JA, Nunez JL, McCarthy MM. GABA mediates steroid-induced astrocyte differentiation in the neonatal rat hypothalamus. J Neuroendocrinol 2002; 14:45-55.
101. Runquist M, Alonso G. Gabaergic signaling mediates the morphological organization of astrocytes in the adult rat forebrain. Glia 2003; 41:137-51.
102. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7:41-53.
103. Wang DD, Krueger DD, Bordey A. Biophysical properties and ionic signature of neuronal progenitors of the postnatal subventricular zone in situ. J Neurophysiol 2003; 90:2291-302.
104. Goldman PS, Rakic PT. Impact of the outside world upon the developing primate brain. Perspective from neurobiology. Bull Menninger Clin 1979; 43:20-8.
105. Lewis MH. Environmental complexity and central nervous system development and function. Ment Retard Dev Disabil Res Rev 2004; 10:91-5.
106. Penn AA, Shatz CJ. Brain waves and brain wiring: The role of endogenous and sensory-driven neural activity in development. Pediatr Res 1999; 45:447-58.
107. Barnea A, Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 1994; 91:11217-21.
108. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997; 386:493-5.
109. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 1999; 39:569-78.
110. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999; 2:266-70.
111. Rochefort C, Gheusi G, Vincent JD, Lledo PM. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 2002; 22:2679-89.
112. Brown J, Cooper-Kuhn CM, Kempermann G, van Praag H, Winkler J, Gage FH, Kuhn HG. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003; 17:2042-6.
113. Boonstra R, Galea L, Matthews S, Wojtowicz JM. Adult neurogenesis in natural populations. Can J Physiol Pharmacol 2001; 79:297-302.
114. Cameron HA, McEwen BS, Gould E. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 1995; 15:4687-92.
115. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2005.
116. Sgoifo A, de Boer SF, Haller J, Koolhaas JM. Individual differences in plasma catecholamine and corticosterone stress responses of wild-type rats: Relationship with aggression. Physiol Behav 1996; 60:1403-7.
117. Heale VR, Vanderwolf CH, Kavaliers M. Components of weasel and fox odors elicit fast wave bursts in the dentate gyrus of rats. Behav Brain Res 1994; 63:159-65.
118. Altman J. Postnatal growth and differentiation of the mammalian brain, with implications for a morphological theory of memory. In: Quarton GC, et al, eds. The Neurosciences. New York: Rockefeller University Press, 1967:723-743.