Regulation of neural stem cells in the human SVZ by trophic and morphogenic factors

Current Signal Transduction Therapy

Volumn 6, Issue 3, 2011, Pages 320-326

  Álvarez Palazuelos, Lucia E ^a   Robles Cervantes, Martha S ^b   Castillo Velázquez, Gabriel ^c   Rivas Souza, Mario ^b   Guzman Muniz, Jorge ^d   Moy Lopez, Norma ^d   González Castañeda, Rocío E ^a   Luquín, Sonia ^a   Gonzalez Perez, Oscar ^a,d  

^a UNIVERSITY OF GUADALAJARA   (Mexico)

^b Instituto Jalisciense de Ciencias Forenses   (Mexico)

^c NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^d UNIVERSIDAD DE COLIMA   (Mexico)

Author keywords

Astrocyte; Human; Neural stem cell; Neurodegenerative; Subventricular zone

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CD133 ANTIGEN; CILIARY NEUROTROPHIC FACTOR RECEPTOR; EPHRIN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE TRANSPORTER; INTERLEUKIN 4; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR; NERVE GROWTH FACTOR; NESTIN; NOGGIN; NOTCH RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR EMX2; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR SOX2; VASCULOTROPIN; VIMENTIN; WNT PROTEIN;

ARTICLE; ASTROCYTE; BRAIN LATERAL VENTRICLE; CELL COMPOSITION; CELL DIVISION; CELL FATE; CELL FUNCTION; CELL ISOLATION; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MACROGLIA; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE;

EID: 80054956260     PISSN: 15743624     EISSN: None     Source Type: Journal    
DOI: 10.2174/157436211797483958     Document Type: Article

References (114)

1. Altman J, Das GD. 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 1966; 126: 337-89.
2. Goldman SA, Nedergaard M. Newly generated neurons of the adult songbird brain become functionally active in long-term culture. Brain Res Dev Brain Res 1992; 68: 217-23.
3. Perez-Canellas MM, Garcia-Verdugo JM. Adult neurogenesis in the telencephalon of a lizard: a [3H]thymidine autoradiographic and bromodeoxyuridine immunocytochemical study. Brain Res Dev Brain Res 1996; 93: 49-61. (Pubitemid 26188233)
4. 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. (Pubitemid 33673069)
5. Ponti G, Aimar P, Bonfanti L. Cellular composition and cytoarchitecture of the rabbit subventricular zone and its extensions in the forebrain. J Comp Neurol 2006; 498: 491-507. (Pubitemid 44232690)
6. Siwak-Tapp CT, Head E, Muggenburg BA, et al. Neurogenesis decreases with age in the canine hippocampus and correlates with cognitive function. Neurobiol Learn Mem 2007; 88: 249-59. (Pubitemid 47223756)
7. Ara J, Fekete S, Zhu A, et al. Characterization of neural stem/ progenitor cells expressing VEGF and its receptors in the subventricular zone of newborn piglet brain. Neurochem Res 2010; 35: 1455-70.
8. Gould E, Reeves AJ, Graziano MS, et al. Neurogenesis in the neocortex of adult primates. Science 1999; 286: 548-52.
9. Curtis MA, Waldvogel HJ, Synek B, et al. A histochemical and immunohistochemical analysis of the subependymal layer in the normal and Huntington's disease brain. J Chem Neuroanat 2005; 30: 55-66. (Pubitemid 40943569)
10. Sanai N, Tramontin AD, Quinones-Hinojosa A, et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004; 427: 740-44. (Pubitemid 38294593)
11. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, et al. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 2006; 494: 415-34. (Pubitemid 41794059)
12. Emsley JG, Mitchell BD, Kempermann G, et al. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 2005; 75: 321-41. (Pubitemid 40733268)
13. Gritti A, Bonfanti L, Doetsch F, et al. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 2002; 22: 437-45. (Pubitemid 34049081)
14. Kelsch W, Lin CW, Mosley CP, et al. A critical period for activitydependent synaptic development during olfactory bulb adult neurogenesis. J Neurosci 2009; 29: 11852-8.
15. Luskin MB, Boone MS. Rate and pattern of migration of lineallyrelated olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem Senses 1994; 19: 695-714.
16. Curtis MA, Kam M, Nannmark U, et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007; 315: 1243-9. (Pubitemid 46364256)
17. Sanai N, Berger MS, Garcia-Verdugo JM, et al. Comment on "Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension". Science 2007; 318: 93; author reply 393.
18. Ihrie RA, Alvarez-Buylla A. Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 2008; 331: 179-91. (Pubitemid 350265483)
19. Marti-Fabregas J, Romaguera-Ros M, Gomez-Pinedo U, et al. Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology 2010; 74: 357-65.
20. Picard-Riera N, Nait-Oumesmar B, Baron-Van Evercooren A. Endogenous adult neural stem cells: limits and potential to repair the injured central nervous system. J Neurosci Res 2004; 76: 223-31. (Pubitemid 38451210)
21. Alvarez-Buylla A, Herrera DG, Wichterle H. The subventricular zone: source of neuronal precursors for brain repair. Prog Brain Res 2000; 127: 1-11. (Pubitemid 35461253)
22. Reynolds BA, Rietze RL. Neural stem cells and neurospheres-reevaluating the relationship. Nat Methods 2005; 2: 333-6. (Pubitemid 41130977)
23. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255: 1707-10.
24. Miller FD, Gauthier-Fisher A. Home at last: neural stem cell niches defined. Cell Stem Cell 2009; 4: 507-10.
25. Taupin P. Adult neural stem cells, neurogenic niches, and cellular therapy. Stem Cell Rev 2006; 2: 213-19.
26. Ferrari D, Binda E, De Filippis L, et al. Isolation of neural stem cells from neural tissues using the neurosphere technique. Curr Protoc Stem Cell Biol Chapter 2010; 2: Unit2D 6.
27. Chaichana KL, Capilla-Gonzalez V, Gonzalez-Perez O, et al. Preservation of glial cytoarchitecture from ex vivo human tumor and non-tumor cerebral cortical explants: A human model to study neurological diseases. J Neurosci Methods 2007; 164: 261-70. (Pubitemid 47016655)
28. Quinones-Hinojosa A, Sanai N, Gonzalez-Perez O, et al. The human brain subventricular zone: stem cells in this niche and its organization. Neurosurg Clin N Am 2007; 18: 15-20, vii. (Pubitemid 46164760)
29. Imitola J, Snyder EY, Khoury SJ. Genetic programs and responses of neural stem/progenitor cells during demyelination: potential insights into repair mechanisms in multiple sclerosis. Physiol Genomics 2003; 14: 171-97. (Pubitemid 37345227)
30. Ahmed S. The culture of neural stem cells. J Cell Biochem 2009; 106: 1-6.
31. Levison SW, Druckman SK, Young GM, et al. Neural stem cells in the subventricular zone are a source of astrocytes and oligodendrocytes, but not microglia. Dev Neurosci 2003; 25: 184-96. (Pubitemid 37100213)
32. Menn B, Garcia-Verdugo JM, Yaschine C, et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 2006; 26: 7907-18. (Pubitemid 44315160)
33. Nait-Oumesmar B, Decker L, Lachapelle F, et al. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 1990; 11: 4357-66.
34. Mirzadeh Z, Merkle FT, Soriano-Navarro M, et al. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008; 3: 265-78.
35. Abrous DN, Koehl M, Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 2005; 85: 523-69. (Pubitemid 40404636)
36. Landgren H, Curtis MA. Locating and labeling neural stem cells in the brain. J Cell Physiol 2011; 226: 1-7.
37. Beckervordersandforth R, Tripathi P, Ninkovic J, et al. fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 2010; 7: 744-58.
38. Ninkovic J, Mori T, Gotz M. Distinct modes of neuron addition in adult mouse neurogenesis. J Neurosci 2007; 27: 10906-11. (Pubitemid 47535849)
39. Garcia AD, Doan NB, Imura T, et al. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 2004; 7: 1233-41. (Pubitemid 39426243)
40. Bentivoglio M, Mazzarello P. The history of radial glia. Brain Res Bull 1999; 49: 305-15.
41. Strojnik T, Rosland GV, Sakariassen PO, et al. Neural stem cell markers, nestin and musashi proteins, in the progression of human glioma: correlation of nestin with prognosis of patient survival. Surg Neurol 2007; 68: 133-43; discussion 143-34. (Pubitemid 47087905)
42. Ayuso-Sacido A, Roy NS, Schwartz TH, et al. Long-term expansion of adult human brain subventricular zone precursors. Neurosurgery 2008; 62: 223-9; discussion 229-31. (Pubitemid 351640341)
43. Coskun V, Wu H, Blanchi B, et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci U S A 2008; 105: 1026-31. (Pubitemid 351282075)
44. Huang Q, Dong J, Zhu YD, et al. [Isolation and culture of tumor stem cells from human brain glioma tissues]. Zhonghua Zhong Liu Za Zhi 2006; 28: 331-3.
45. van den Berge SA, Middeldorp J, Zhang CE, et al. Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell 2010; 9: 313-26.
46. Boer K, Middeldorp J, Spliet WG, et al. Immunohistochemical characterization of the out-of frame splice variants GFAP Delta164/Deltaexon 6 in focal lesions associated with chronic epilepsy. Epilepsy Res 2010; 90: 99-109.
47. Roelofs RF, Fischer DF, Houtman SH, et al. Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 2005; 52: 289-300. (Pubitemid 43076221)
48. Macnicol MC, Cragle CE, Macnicol. A Context-dependent regulation of Musashi-mediated mRNA translation and cell cycle regulation. Cell Cycle 2011; 10. In press
49. Kim JB, Zaehres H, Wu G, et al. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 2008; 454: 646-50.
50. Avilion AA, Nicolis SK, Pevny LH, et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17: 126-40. (Pubitemid 36062514)
51. Nichols J, Zevnik B, Anastassiadis K, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998; 95: 379-91. (Pubitemid 28507326)
52. Capela A, Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002; 35: 865-875.
53. Yanagisawa M, Yu RK. The expression and functions of glycoconjugates in neural stem cells. Glycobiology 2007; 17: 57R-74R. (Pubitemid 47050656)
54. Leonard BW, Mastroeni D, Grover A, et al. Subventricular zone neural progenitors from rapid brain autopsies of elderly subjects with and without neurodegenerative disease. J Comp Neurol 2009; 515: 269-94.
55. Weickert CS, Webster MJ, Colvin SM, et al. Localization of epidermal growth factor receptors and putative neuroblasts in human subependymal zone. J Comp Neurol 2000; 423: 359-72.
56. Feldmann RE, Jr., Mattern R. The human brain and its neural stem cells postmortem: from dead brains to live therapy. Int J Legal Med 2006; 120: 201-11.
57. Chaichana KL, Guerrero-Cazares H, Capilla-Gonzalez V, et al. Intra-operatively obtained human tissue: protocols and techniques for the study of neural stem cells. J Neurosci Methods 2009; 180: 116-25.
58. Pastrana E, Cheng LC, Doetsch F. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci U S A 2009; 106: 6387-92.
59. Danilov AI, Gomes-Leal W, Ahlenius H, et al. Ultrastructural and antigenic properties of neural stem cells and their progeny in adult rat subventricular zone. Glia 2009; 57: 136-52.
60. Rhoton AL, Jr. The lateral and third ventricles. Neurosurgery 2002; 51: S207-71.
61. Kam M, Curtis MA, McGlashan SR, et al. The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat 2009; 37: 196-205.
62. Guerrero-Cazares H, Soriano-Navarro M, Zamora-Berridi G, et al. Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol 2011; 519: In press.
63. Gonzalez-Perez O, Jauregui-Huerta F, Galvez-Contreras AY. Immune system modulates the function of adult neural stem cells. Curr Immunol Rev 2010; 6: 167-73.
64. Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, et al. Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 2009; 27: 2032-43.
65. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, et al. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006; 51: 187-99. (Pubitemid 44063617)
66. Brannvall K, Bogdanovic N, Korhonen L, et al. 19-Nortestosterone influences neural stem cell proliferation and neurogenesis in the rat brain. Eur J Neurosci 2005; 21: 871-78. (Pubitemid 40461040)
67. Brannvall K, Korhonen L, Lindholm D. Estrogen-receptordependent regulation of neural stem cell proliferation and differentiation. Mol Cell Neurosci 2002; 21: 512-20. (Pubitemid 36062736)
68. Yu S, Patchev AV, Wu Y, Lu J, et al. Depletion of the neural precursor cell pool by glucocorticoids. Ann Neurol 2010; 67: 21-30.
69. Tomycz ND, Friedlander RM. Novel neurogenesis drugs uncovered from in vivo chemical library screen. Neurosurgery 2010; 67: N16-18.
70. Taupin P. Neurogenic drugs and compounds. Recent Pat CNS Drug Discov 2010; 5: 253-57.
71. Li E, Hristova K. Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies. Biochemistry 2006; 45: 6241-51. (Pubitemid 43787791)
72. Bath KG, Lee FS. Neurotrophic factor control of adult SVZ neurogenesis. Dev Neurobiol 2010; 70: 339-49.
73. Jackson EL, Alvarez-Buylla A. Characterization of adult neural stem cells and their relation to brain tumors. Cells Tissues Organs 2008; 188: 212-24. (Pubitemid 351962244)
74. Lu H, Li M, Song T, et al. Retrovirus delivered neurotrophin-3 promotes survival, proliferation and neuronal differentiation of human fetal neural stem cells . Brain Res Bull 2008; 77: 158-64.
75. Mudo G, Bonomo A, Di Liberto V, et al. The FGF-2/FGFRs neurotrophic system promotes neurogenesis in the adult brain. J Neural Transm 2009; 116: 995-1005.
76. Werry EL, Enjeti S, Halliday GM, et al. Effect of age on proliferation-regulating factors in human adult neurogenic regions. J Neurochem 2010; 115: 956-64.
77. Galvao RP, Garcia-Verdugo JM, Alvarez-Buylla A. Brain-derived neurotrophic factor signaling does not stimulate subventricular zone neurogenesis in adult mice and rats. J Neurosci 2008; 28: 13368-83.
78. Liard O, Segura S, Pascual A, et al. In vitro isolation of neural precursor cells from the adult pig subventricular zone. J Neurosci Methods 2009; 182: 172-79.
79. Sun D, Bullock MR, McGinn MJ, et al. Basic fibroblast growth factor-enhanced neurogenesis contributes to cognitive recovery in rats following traumatic brain injury. Exp Neurol 2009; 216: 56-65.
80. Ishii Y, Matsumoto Y, Watanabe R, et al. Characterization of neuroprogenitor cells expressing the PDGF beta-receptor within the subventricular zone of postnatal mice. Mol Cell Neurosci 2008; 37: 507-18.
81. Nait-Oumesmar B, Picard-Riera N, Kerninon C, et al. The role of SVZ-derived neural precursors in demyelinating diseases: from animal models to multiple sclerosis. J Neurol Sci 2008; 265: 26-31.
82. Gonzalez-Perez O, Quinones-Hinojosa A. Dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia 2010; 58: 975-83.
83. Namiecinska M, Marciniak K, Nowak JZ. [VEGF as an angiogenic, neurotrophic, and neuroprotective factor]. Postepy Hig Med Dosw (Online) 2005; 59: 573-83.
84. Jin K, Zhu Y, Sun Y, et al. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and. Proc Natl Acad Sci U S A 2002; 99: 11946-50. (Pubitemid 34994504)
85. Mani N, Khaibullina A, Krum JM, et al. Vascular endothelial growth factor enhances migration of astroglial cells in subventricular zone neurosphere cultures. J Neurosci Res 2010; 88: 248-57.
86. Triaca V, Tirassa P, Aloe L. Presence of nerve growth factor and TrkA expression in the SVZ of EAE rats: evidence for a possible functional significance. Exp Neurol 2005; 191: 53-64. (Pubitemid 39612392)
87. Emsley JG, Hagg T. Endogenous and exogenous ciliary neurotrophic factor enhances forebrain neurogenesis in adult mice. Exp Neurol 2003; 183: 298-310. (Pubitemid 37205072)
88. Bauer S, Kerr BJ, Patterson PH. The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci 2007; 8: 221-32. (Pubitemid 46294661)
89. Nakashima K. [Mechanism of neural stem cell fate specification]. Tanpakushitsu Kakusan Koso 2004; 49: 718-26.
90. Bauer S. Cytokine control of adult neural stem cells. Ann N Y Acad Sci 2009; 1153: 48-56.
91. Bonaguidi MA, McGuire T, Hu M, et al. LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 2005; 132: 5503-14. (Pubitemid 43125877)
92. Cate HS, Sabo JK, Merlo D, et al. Modulation of bone morphogenic protein signalling alters numbers of astrocytes and oligodendroglia in the subventricular zone during cuprizone-induced demyelination. J Neurochem 2010; 115: 11-22.
93. Lim DA, Huang YC, Alvarez-Buylla A. The adult neural stem cell niche: lessons for future neural cell replacement strategies. Neurosurg Clin N Am 2007; 18: 81-92, ix. (Pubitemid 46172427)
94. Ueki T, Tanaka M, Yamashita K, et al. A novel secretory factor, Neurogenesin-1, provides neurogenic environmental cues for neural stem cells in the adult hippocampus. J Neurosci 2003; 23: 11732-40. (Pubitemid 38021300)
95. Conover JC, Doetsch F, Garcia-Verdugo JM, et al. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 2000; 3: 1091-97.
96. Adachi K, Mirzadeh Z, Sakaguchi M, et al. Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 2007; 25: 2827-36. (Pubitemid 350127867)
97. Piccin D, Morshead CM. Wnt Signaling Regulates Symmetry of Division of Neural Stem Cells in the Adult Brain and in Response to Injury. Stem Cells 2010; In press
98. Lai K, Kaspar BK, Gage FH, et al. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 2003; 6: 21-7. (Pubitemid 36026328)
99. Ahn S, Joyner AL . In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005; 437: 894-97. (Pubitemid 41486765)
100. Hor CH, Tang BL. Sonic hedgehog as a chemoattractant for adult NPCs. Cell Adh Migr 2010; 4: 1-3.
101. Aguirre A, Rubio ME, Gallo V. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 2010; 467: 323-27.
102. Watts C, McConkey H, Anderson L, et al. Anatomical perspectives on adult neural stem cells. J Anat 2005; 207: 197-208. (Pubitemid 41300995)
103. Gangemi RM, Daga A, Muzio L, et al. Effects of Emx2 inactivation on the gene expression profile of neural precursors. Eur J Neurosci 2006; 23: 325-34.
104. Li L, Liu F, Ross AH. PTEN regulation of neural development and CNS stem cells. J Cell Biochem 2003; 88: 24-8. (Pubitemid 36015071)
105. Renault VM, Rafalski VA, Morgan AA, et al. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 2009; 5: 527-39.
106. Craig CG, Tropepe V, Morshead CM, et al. growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 1996; 16: 2649-58. (Pubitemid 26122682)
107. Baron W, Metz B, Bansal R, et al. PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol Cell Neurosci 2000; 15: 314-29. (Pubitemid 30193804)
108. Lachapelle F, Avellana-Adalid V, Nait-Oumesmar B, et al. Fibroblast growth factor-2 (FGF-2) and platelet-derived growth factor AB (PDGF AB) promote adult SVZ-derived oligodendrogenesis. Mol Cell Neurosci 2002; 20: 390-403. (Pubitemid 34971557)
109. Ben-Hur T. Immunomodulation by neural stem cells. J Neurol Sci 2008; 265: 102-4.
110. Liu SY, Zhang ZY, Song YC, et al. SVZa neural stem cells differentiate into distinct lineages in response to BMP4. Exp Neurol 2004; 190: 109-21.
111. Hirabayashi Y, Gotoh Y. Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 2010; 11: 377-88.
112. Russo I, Barlati S, Bosetti F. Effects of Neuroinflammation on the Regenerative Capacity of Brain Stem Cells. J Neurochem 2010: In press
113. Skold MK, Kanje M. Vascular endothelial growth factor in central nervous system injuries -a vascular growth factor getting nervous? Curr Neurovasc Res 2008; 5: 246-59.
114. Rossi F, Cattaneo E. Opinion: neural stem cell therapy for neurological diseases: dreams and reality. Nat Rev Neurosci 2002; 3: 401-9. (Pubitemid 135706637)