Aging of the subventricular zone neural stem cell niche

Aging and Disease

Volumn 2, Issue 1, 2011, Pages 49-63

  Conover, Joanne C ^a   Shook, Brett A ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Aging; Demyelinating lesions; Ependymal damage; Neural stem cells; Neurogenesis; Parkinson's disease; Stroke; Subventricular zone

Indexed keywords

MAMMALIA;

EID: 84917674645     PISSN: None     EISSN: 21525250     Source Type: Journal    
DOI: None     Document Type: Review

References (118)

1. Aimone JB, Wiles J, Gage FH (2009). Computational influence of adult neurogenesis on memory encoding. Neuron, 61: 187-202
2. Clelland CD, Choi M, Romberg C, Clemenson GD, Jr., Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science, 325: 210-213
3. Deng W, Saxe MD, Gallina IS, Gage FH (2009). Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci, 29: 13532-13542
4. Garthe A, Behr J, Kempermann G (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One, 4: e5464
5. Kriegstein A, Alvarez-Buylla A (2009). The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci, 32: 149-184
6. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410: 372-376
7. Conover JC, Notti RQ (2008). The neural stem cell niche. Cell Tissue Res, 331: 211-224
8. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004). Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci, 24: 8354-8365
9. Ihrie RA, Alvarez-Buylla A (2008). Cells in the astroglial lineage are neural stem cells. Cell Tissue Res, 331: 179-191
10. Doetsch F, Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (1997). Cellular composition and three-dimensional organization of hte subventricular germinal zone in the adult mammalian brain. J. Neuroscience, 17: 5046-5061
11. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A (1998). Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol, 36: 234-248
12. Doetsch R, 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
13. Imura T, Kornblum HI, Sofroniew MV (2003). The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci, 23: 2824-2832
14. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain Cell Stem Cell, 3: 265-278
15. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S (2008). Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell, 3: 289-300
16. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F (2008). A specialized vascular niche for adult neural stem cells. Cell Stem Cell, 3: 279-288
17. Kokovay E, Goderie S, Wang Y, Lotz S, Lin G, Sun Y, Roysam B, Shen Q, Temple S (2010). Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell, 7: 163-173
18. Merkle FT, Mirzadeh Z, Alvarez-Buylla A (2007). Mosaic organization of neural stem cells in the adult brain. Science, 317: 381-384
19. Doetsch F, Alvarez-Buylla A (1996). Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci U S A, 93: 14895-14900.
20. Lois C, Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (1996). Chain migration of neuronal precursors. Science, 271: 978-981
21. Luskins MB (1993). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron, 11: 173-189
22. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008). Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci, 11: 1153-1161
23. Nam HS, Benezra R (2009). High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell, 5: 515-526
24. Boyle M, Wong C, Rocha M, Jones DL (2007). Neural differentiation, NCAM-mediated adhesion, and gap junctional communication in neuroectoderm. A study in vitro. Cell Stem Cell, 1: 470-478
25. Keane RW, Mehta PP, Rose B, Honig LS, Loewenstein WR, Rutishauser U (1988). J Cell Biol, 106: 1307-1319
26. Song X, Zhu CH, Doan C, Xie T (2002). Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science, 296: 1855-1857
27. Wilson A, Murphy MJ, Oskarsson T, Kaloulis K, Bettess MD, Oser GM, Pasche AC, Knabenhans C, Macdonald HR, Trumpp A (2004). c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev, 18: 2747-2763
28. Moore KA, Lemischka IR (2006). Stem cells and their niches. Science, 311: 1880-1885
29. Morrison SJ, Spradling AC (2008). Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell, 132: 598-611
30. Spradling A, Drummond-Barbosa D, Kai T (2001). Stem cells find their niche. Nature, 414: 98-104
31. Baker KL, Daniels SB, Lennington JB, Lardaro T, Czap A, Notti RQ, Cooper O, Isacson O, Frasca S, Jr., Conover JC (2006). Neuroblast protuberances in the subventricular zone of the regenerative MRL/MpJ mouse. J Comp Neurol, 498: 747-761
32. Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC (2006). The aging neurogenic subventricular zone. Aging Cell, 5: 139-152
33. Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, Gravel C, Berthod F, Gotz M, Barker PA, Parent A, Saghatelyan A (2009). Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci, 29: 4172-4188
34. 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
35. Mercier F, Kitasako JT, Hatton GI (2002). Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J Comp Neurol, 451: 170-188
36. Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F (2007). Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells, 25: 2146-2157
37. Luo J, Shook BA, Daniels SB, Conover JC (2008). Subventricular zone-mediated ependyma repair in the adult mammalian brain. J Neurosci, 28: 3804-3813
38. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS (2007). Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science, 315: 1243-1249
39. Kam M, Curtis MA, McGlashan SR, Connor B, Nannmark U, Faull RL (2009). The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat, 37: 196-205
40. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, 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
41. Roelofs RF, Fischer DF, Houtman SH, Sluijs JA, Van Haren W, Van Leeuwen FW, Hol EM (2005). Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia, 52: 289-300
42. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004). Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature, 427: 740-744
43. Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z (2009). Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci, 29: 4408-4419
44. Tropepe V, Craig, C.G., Morshead, C.M., and van der Kooy, D. (1997). Transforming growth factor-a null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci., 17: 7850-7859
45. Sahin E, Depinho RA (2010). Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature, 464: 520-528
46. Buchkovich KJ, Greider CW (1996). Telomerase regulation during entry into the cell cycle in normal human T cells. Mol Biol Cell, 7: 1443-1454
47. Jacobs JJ, de Lange T (2004). Significant role for p16INK4a in p53-independent telomere-directed senescence. Curr Biol, 14: 2302-2308
48. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW (1994). Specific association of human telomerase activity with immortal cells and cancer. Science, 266: 2011-2015
49. Lee HW, Blasco MA, Gottlieb GJ, Horner JW, 2nd, Greider CW, DePinho RA (1998). Essential role of mouse telomerase in highly proliferative organs. Nature, 392: 569-574
50. Caporaso GL, Lim DA, Alvarez-Buylla A, Chao MV (2003). Telomerase activity in the subventricular zone of adult mice. Mol Cell Neurosci, 23: 693-702
51. Ferron SR, Marques-Torrejon MA, Mira H, Flores I, Taylor K, Blasco MA, Farinas I (2009). Telomere shortening in neural stem cells disrupts neuronal differentiation and neuritogenesis. J Neurosci, 29: 14394-14407
52. Ferron S, Mira H, Franco S, Cano-Jaimez M, Bellmunt E, Ramirez C, Farinas I, Blasco MA (2004). Telomere shortening and chromosomal instability abrogates proliferation of adult but not embryonic neural stem cells. Development, 131: 4059-4070
53. Janzen V, Forkert R, Fleming HE, Saito Y, Waring MT, Dombkowski DM, Cheng T, DePinho RA, Sharpless NE, Scadden DT (2006). Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature, 443: 421-426
54. Li X, Tang X, Jablonska B, Aguirre A, Gallo V, Luskin MB (2009). p27(KIP1) regulates neurogenesis in the rostral migratory stream and olfactory bulb of the postnatal mouse. J Neurosci, 29: 2902-2914
55. Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ (2006). Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature, 443: 448-452
56. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004). Neural stem cell detection, characterization, and age-elated changes in the subventricular zone of mice. J Neurosci, 24: 1726-1733
57. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med, 8: 963-970
58. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001). Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A, 98: 4710-4715
59. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA (2006). Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A, 103: 13198-13202
60. Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, Sawamoto K (2010).Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells, 28: 545-554
61. Macas J, Nern C, Plate KH, Momma S (2006). Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain J Neurosci, 26: 13114-13119
62. Marti-Fabregas J, Romaguera-Ros M, Gomez-Pinedo U, Martinez-Ramirez S, Jimenez-Xarrie E, Marin R, Marti-Vilalta JL, Garcia-Verdugo JM (2010). Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology, 74: 357-365
63. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002). Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol, 52: 802-813
64. Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, Lapointe M, Chopp M (2001). A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol, 50: 602-611
65. Minnerup J, Heidrich J, Wellmann J, Rogalewski A, Schneider A, Schabitz WR (2008). Meta-analysis of the efficacy of granulocyte-colony stimulating factor in animal models of focal cerebral ischemia. Stroke, 39: 1855-1861
66. Shyu WC, Lin SZ, Yang HI, Tzeng YS, Pang CY, Yen PS, Li H (2004). Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation, 110: 1847-1854
67. Popa-Wagner A, Stocker K, Balseanu AT, Rogalewski A, Diederich K, Minnerup J, Margaritescu C, Schabitz WR (2010). Effects of granulocyte-colony stimulating factor after stroke in aged rats. Stroke, 41: 1027-1031
68. Kaneko N, Sawamoto K (2009). Adult neurogenesis and its alteration under pathological conditions. Neurosci Res, 63: 155-164
69. Locatelli F, Bersano A, Ballabio E, Lanfranconi S, Papadimitriou D, Strazzer S, Bresolin N, Comi GP, Corti S (2009). Stem cell therapy in stroke. Cell Mol Life Sci, 66: 757-772
70. Zhang RL, Zhang ZG, Chopp M (2008). Ischemic stroke and neurogenesis in the subventricular zone. Neuropharmacology, 55: 345-352
71. Bjorklund A, Dunnett SB (2007). Dopamine neuron systems in the brain: an update. Trends Neurosci, 30: 194-202
72. Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, Hirsch EC (2004). Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci, 7: 726-735
73. Ohtani N, Goto T, Waeber C, Bhide PG (2003). Dopamine modulates cell cycle in the lateral ganglionic eminence. J Neurosci, 23: 2840-2850
74. Popolo M, McCarthy DM, Bhide PG (2004). Influence of dopamine on precursor cell proliferation and differentiation in the embryonic mouse telencephalon. Dev Neurosci, 26: 229-244
75. Baker SA, Baker KA, Hagg T (2004). Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur J Neurosci, 20: 575-579
76. Winner B, Geyer M, Couillard-Despres S, Aigner R, Bogdahn U, Aigner L, Kuhn G, Winkler J (2006). Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb. Exp Neurol, 197: 113-121
77. Freundlieb N, Francois C, Tande D, Oertel WH, Hirsch EC, Hoglinger GU (2006). Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J Neurosci, 26: 2321-2325
78. Coronas V, Bantubungi K, Fombonne J, Krantic S, Schiffmann SN, Roger M (2004). Dopamine D3 receptor stimulation promotes the proliferation of cells derived from the post-natal subventricular zone. J Neurochem, 91: 1292-1301
79. O'Keeffe GC, Tyers P, Aarsland D, Dalley JW, Barker RA, Caldwell MA (2009). Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. Proc Natl Acad Sci U S A, 106: 8754-8759
80. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006). Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci, 26: 7907-7918
81. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Van Evercooren AB (1999). Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci, 11: 4357-4366
82. Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, Liblau R, Pham-Dinh D, Evercooren AB (2002). Proc Natl Acad Sci U S A, 99: 13211-13216
83. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009). Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci, 10: 9-22
84. Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor KA, Ming GL, Song H, Gallo V (2010). Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci, 13: 541-550
85. Bartzokis G (2004). Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease. Neurobiol Aging, 25: 5-18; author reply 49-62
86. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci, 25: 10-18
87. Bruni JE (1998). Ependymal development, proliferation, and functions: a review. Microsc Res Tech, 41: 2-13
88. Bruni JE, Del Bigio MR, Clattenburg RE (1985). Ependyma: normal and pathological. Brain Res, 356: 1-19
89. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1999). Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A, 96: 11619-11624
90. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabe-Heider F, Yeung MS, Naldini L, Honjo T, Kokaia Z, Shupliakov O, Cassidy RM, Lindvall O, Frisen J (2009). Nat Neurosci, 12: 259-267
91. Anderson MF, Aberg MA, Nilsson M, Eriksson PS (2002). Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res Dev Brain Res, 134: 115-122
92. Doetsch F (2003). A niche for adult neural stem cells. Curr Opin Genet Dev, 13: 543-550
93. Petersen PH, Zou K, Hwang JK, Jan YN, Zhong W (2002). Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature, 419: 929-934
94. Temple S (2001). The development of neural stem cells. Nature, 414: 112-117
95. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD (2006). Notch signalling regulates stem cell numbers in vitro and in vivo. Nature, 442: 823-826
96. Louvi A, Artavanis-Tsakonas S (2006). Notch signalling in vertebrate neural development. Nat Rev Neurosci, 7: 93-102
97. Lutolf S, Radtke F, Aguet M, Suter U, Taylor V (2002). Notch1 is required for neuronal and glial differentiation in the cerebellum. Development, 129: 373-385
98. Mizutani K, Yoon K, Dang L, Tokunaga A, Gaiano N (2007). Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature, 449: 351-355
99. Basak O, Taylor V (2007). Identification of self-replicating multipotent progenitors in the embryonic nervous system by high Notch activity and Hes5 expression. Eur J Neurosci, 25: 1006-1022
100. Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Gotz M, Haas CA, Kempermann G, Taylor V, Giachino C (2010). Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell, 6: 445-456
101. Balordi F, Fishell G (2007). Mosaic removal of hedgehog signaling in the adult SVZ reveals that the residual wild-type stem cells have a limited capacity for self-renewal. J Neurosci, 27: 14248-14259
102. Balordi F, Fishell G (2007). Hedgehog signaling in the subventricular zone is required for both the maintenance of stem cells and the migration of newborn neurons. J Neurosci, 27: 5936-5947
103. Lai K, Kaspar BK, Gage FH, Schaffer DV (2003). Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci, 6: 21-27
104. Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, McMahon AP, Fishell G (2003). Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron, 39: 937-950
105. Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, Herzberg CD, Gitton Y, Carleton A, Alvarez-Buylla A, Ruiz i Altaba A (2005). Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development, 132: 335-344
106. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A (2008). Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci, 11: 277-284
107. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D (1996). In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci, 16: 2649-2658
108. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron, 36: 1021-1034
109. Fallon J, Reid S, Kinyamu R, Opole I, Opole R, Baratta J, Korc M, Endo TL, Duong A, Nguyen G, Karkehabadhi M, Twardzik D, Patel S, Loughlin S (2000). In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci U S A, 97: 14686-14691
110. Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2009). pidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells, 27: 2032-2043
111. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (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
112. Aguirre A, Dupree JL, Mangin JM, Gallo V (2007). A functional role for EGFR signaling in myelination and remyelination. Nat Neurosci, 10: 990-1002
113. Aguirre A, Rizvi TA, Ratner N, Gallo V (2005). Overexpression of the epidermal growth factor receptor confers migratory properties to nonmigratory postnatal neural progenitors. J Neurosci, 25: 11092-11106
114. Cantarella C, Cayre M, Magalon K, Durbec P (2008). Intranasal HB-EGF administration favors adult SVZ cell mobilization to demyelinated lesions in mouse corpus callosum. Dev Neurobiol, 68: 223-236
115. Cooper O, Isacson O (2004). Intrastriatal transforming growth factor alpha delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci, 24: 8924-8931
116. Falk A, Frisen J (2002). Amphiregulin is a mitogen for adult neural stem cells. J Neurosci Res, 69: 757-762
117. Kornblum HI, Hussain RJ, Bronstein JM, Gall CM, Lee DC, Seroogy KB (1997). Prenatal ontogeny of the epidermal growth factor receptor and its ligand, transforming growth factor alpha, in the rat brain. J Comp Neurol, 380: 243-261
118. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003). Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell, 2: 175-183