Perivascular instruction of cell genesis and fate in the adult brain

Nature Neuroscience

Volumn 14, Issue 11, 2011, Pages 1382-1389

  Goldman, Steven A ^a   Chen, Zhuoxun ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; NITRIC OXIDE; PURINERGIC P2Y RECEPTOR;

ANGIOGENESIS; BRAIN DEVELOPMENT; CELL FATE; CELL INTERACTION; GLIA CELL; HUMAN; MOLECULAR INTERACTION; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; STEM CELL MOBILIZATION; STEM CELL NICHE;

ADULT STEM CELLS; ANIMALS; BLOOD VESSELS; BRAIN; CELL COMMUNICATION; CELL DIFFERENTIATION; HUMANS; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROGENESIS; NEURONS; STEM CELL NICHE;

EID: 80054986458     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2963     Document Type: Review

References (100)

1. Goldman, S.A. Adult neurogenesis: From canaries to the clinic. J. Neurobiol. 36, 267-286 (1998). (Pubitemid 28363236)
2. Gage, F.H. Mammalian neural stem cells. Science 287, 1433-1438 (2000). (Pubitemid 30127128)
3. Alvarez-Buylla, A., Garcia-Verdugo, J.M. & Tramontin, A. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2, 287-293 (2001). (Pubitemid 33673069)
4. Morshead, C.M. et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13, 1071-1082 (1994). (Pubitemid 24372126)
5. Sanai, N. et al. Unique astrocyte ribbon in adult human brain contains neural stem cells, but lacks chain migration. Nature 427, 740-744 (2004).
6. Luskin, M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11, 173-189 (1993). (Pubitemid 23222544)
7. Lois, C. & Alvarez-Buylla, A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA 90, 2074-2077 (1993). (Pubitemid 23070000)
8. Kirschenbaum, B. et al. In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb. Cortex 4, 576-589 (1994).
9. Pincus, D.W. et al. Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells. Ann. Neurol. 43, 576-585 (1998) (Pubitemid 28225548)
10. Eriksson, P.S. et al. Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317 (1998) (Pubitemid 28512114)
11. Roy N.S., et al. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat. Med. 6 271-277 (2000). (Pubitemid 30148618)
12. Ming, G.L. & Song, H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687702 (2011)
13. Nishiyama, A., Komitova, M., Suzuki, R. & Zhu, X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10, 9-22 (2009)
14. Goldman, S.A. Stem and progenitor cell-based therapy of the human central nervous system. Nat. Biotechnol. 23, 862-871 (2005)
15. Potten, C.S. & Loeffler, M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001-1020 (1990) (Pubitemid 120009472)
16. Doetsch, F., Petreanu, L., Caille, I., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36, 1021-1034 (2002) (Pubitemid 36044505)
17. Kronenberg, G. et al. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467, 455-463 (2003) (Pubitemid 37467122)
18. Nunes, M.C. et al. Identification and isolation of multipotential neural progenitorcells from the subcortical white matter of the adult human brain. Nat. Med. 9, 439-447 (2003) (Pubitemid 36460078)
19. Ihrie, R.A. & Alvarez-Buylla, A. Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70, 674-686 (2011)
20. Shen, Q. et al. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3, 289-300 (2008)
21. Tavazoie, M. et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279-288 (2008)
22. Palmer, T.D., Willhoite, A.R. & Gage, F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479-494 (2000)
23. Louissaint, A. Jr., Rao, S., Leventhal, C. & Goldman, S.A. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34, 945-960 (2002) (Pubitemid 34722284)
24. Leventhal, C., Rafii, S., Rafii, D., Shahar, A. & Goldman, S.A. Endothelial trophic supportof neuronal production and recruitment from the adult mammalian subependyma. Mol. Cell. Neurosci. 13, 450-464 (1999) (Pubitemid 29337211)
25. Ohab, J.J., Fleming, S., Blesch, A. & Carmichael, S. A neurovascular nichefor neurogenesis after stroke. J. Neurosci. 26, 13007-13016 (2006)
26. Bovetti, S. et al. Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb. J. Neurosci. 27, 5976-5980 (2007) (Pubitemid 46849744)
27. Snapyan, M. et al. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J. Neurosci. 29, 4172-4188(2009)
28. Shen, Q. et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340 (2004) (Pubitemid 38697433)
29. Goldman, S.A. & Nottebohm, F. Neuronal production, migration and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. USA 80, 2390-2394 (1983) (Pubitemid 13097195)
30. Cleaver O., Melton D. Endothelial signaling during development. Nat. Med. 9 661-668 (2003). (Pubitemid 36749214)
31. Calabrese, C. et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11, 69-82 (2007) (Pubitemid 46054518)
32. Cao, L. et al. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 36, 827-835 (2004) (Pubitemid 39014099)
33. Schänzer, A. et al. Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol. 14, 237-248 (2004) (Pubitemid 39095985)
34. Licht, T. et al. Reversible modulations ofneuronal plasticity by VEGF. Proc. Natl. Acad. Sci. USA 108, 50815086 (2011)
35. Wurmser, A.E. et al. Cell fusion-independent differentiation of neural stem cells to the endothelial lineage. Nature 430, 350-356 (2004) (Pubitemid 38937742)
36. Wang, R. et al. Glioblastoma stem-like cells give rise to tumor endothelium. Nature 468, 829-833 (2010)
37. Lin, J.H. et al. Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev. Biol. 302, 356-366 (2007) (Pubitemid 46096933)
38. Braun, N. et al. Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur. J. Neurosci. 17, 1355-1364 (2003) (Pubitemid 36560835)
39. Agresti, C. et al. Metabotropic P2 receptor activation regulates oligodendrocyte progenitor migration and development. Glia 50, 132-144 (2005) (Pubitemid 40695267)
40. Burnstock, G. Historical review: ATP as a neurotransmitter. Trends Pharmacol. Sci. 27, 166-176 (2006)
41. Packer, M.A. et al. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl. Acad. Sci. USA 100, 9566-9571 (2003) (Pubitemid 37033968)
42. Chen, J. et al. Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J. Neurosci. 25, 2366-2375 (2005) (Pubitemid 40322278)
43. Park, C. et al. Inhibition of neuronal nitric oxide synthase enhances cell proliferation in the dentate gyrus of the adrenalectomized rat. Neurosci. Lett. 309, 9-12 (2001) (Pubitemid 32728247)
44. Cheng, A., Wang, S., Cai J., Rao, M.S. & Mattson, M.P. Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev. Biol. 258, 319-333 (2003) (Pubitemid 36683134)
45. Moreno-López B., et al. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J. Neurosci. 24 85-95 (2004). (Pubitemid 38181673)
46. Torroglosa, A. et al. Nitric oxide decreases subventricular zone stem cell proliferation by inhibition of epidermal growth factor receptor and phosphoinositide-3-kinase/Akt pathway. Stem Cells 25, 88-97 (2007) (Pubitemid 46052978)
47. Li, Q., Ford, M.C., Lavik, E.B. & Madri, J.A. Modeling the neurovascular niche: VEGFand BDNF-mediated cross-talk between neural stem cells and endothelial cells: an in vitro study. J. Neurosci. Res. 84, 1656-1668 (2006) (Pubitemid 44892600)
48. Murillo-Carretero, M., Torroglosa, A., Castro, C., Villalobo, A. & Estrada, C. S-nitrosylation of the epidermal growth factor receptor: a regulatory mechanism of receptor tyrosine kinase activity. Free Radic. Biol. Med. 46, 471-479 (2009).
49. Reif, A. et al. Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behavior. Eur. J. Neurosci. 20, 885-895 (2004) (Pubitemid 39141296)
50. Zhu, D.Y., Liu, S.H., Sun, H.S. & Lu, Y.M. Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J. Neurosci. 23, 223-229 (2003) (Pubitemid 36050422)
51. Carreira, B.P. et al. Nitric oxide stimulates the proliferation of neural stem cells bypassing the epidermal growth factor receptor. Stem Cells 28, 1219-1230 (2010)
52. Luo, C.X. et al. Bidirectional regulation of neurogenesis by neuronal nitric oxide synthase derived from neurons and neural stem cells. Stem Cells 28, 2041-2052 (2010)
53. Charles N., et al. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 6 141-152 (2010).
54. Eyler C.E. et al. Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell 146, 5366 (2011)
55. Dawson, D.W. et al. Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285, 245-248 (1999) (Pubitemid 29329995)
56. Ramírez-Castillejo, C. et al. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci. 9, 331-339 (2006) (Pubitemid 43290962)
57. Andreu-Agulló, C., Morante-Redolat, J.M., Delgado, A.C. & Farinas, I. Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat. Neurosci. 12, 1514-1523 (2009)
58. Ables, J.L., Breunig, J., Eisch, A.J. & Rakic, P. Not(ch) just development: Notch signaling in the adult brain. Nat. Rev. Neurosci. 12, 269283 (2011)
59. Noguera-Troise, I. et al. Blockade of Dll4 inhibits tumor growth by promoting nonproductive angiogenesis. Nature 444, 1032-1037 (2006) (Pubitemid 46018516)
60. Ridgway, J. et al. Inhibition of Dll4 signaling inhibits tumor growth by deregulating angiogenesis. Nature 444, 1083-1087 (2006) (Pubitemid 46018529)
61. Klein, R., Conway, D., Parada, L.F. & Barbacid, M. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61, 647-656(1990)
62. Young, K.M., Merson, T.D., Sotthibundhu, A., Coulson, E.J. & Bartlett, P.F. p75 neurotrophin receptor expression defines a population of BDNF-responsive neurogenic precursor cells. J. Neurosci. 27 5146-5155 (2007) (Pubitemid 46741778)
63. Galvao, R.P., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Brain-derived neurotrophic factor signaling does not stimulate subventricular zone neurogenesis in adult mice and rats. J. Neurosci. 28, 13368-13383 (2008)
64. Chiaramello, S. et al. BDNF/TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signaling pathways. Eur. J. Neurosci. 26, 1780-1790 (2007) (Pubitemid 47493201)
65. Donovan, M.H., Yamaguchi, M. & Eisch, A.J. Dynamic expression of TrkB receptor protein on proliferating and maturing cells in the adult mouse dentate gyrus. Hippocampus 18, 435-4392008) (Pubitemid 351671402)
66. Ahmed, S., Reynolds, B.A. & Weiss, S. BDNF enhances the differentiation, but not the survival, of CNS stem cell-derived neuronal precursors. J. Neurosci. 15, 5765-5778 (1995)
67. Kirschenbaum, B. & Goldman, S.A. Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl. Acad. Sci. USA 92, 210-214 (1995)
68. Emsley, J.G. & Hagg, T. a6b1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp. Neurol. 183, 273-285 (2003). (Pubitemid 37205070)
69. Whitman, M.C., Fan, W., Rela, L., Rodriguez-Gil, D.J. & Greer, C.A. Blood vessels form a migratory scaffold in the rostral migratory stream. J. Comp. Neurol. 516, 94-104 (2009)
70. Kokovay, E. et al. Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 7, 163-173 (2010)
71. Lim, D.A. et al. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713-726 (2000) (Pubitemid 32038066)
72. Mirzadeh, Z., Merkle, F.T., Soriano-Navarro, M., Garcia-Verdugo, J.M. &Alvarez- Buylla, A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3, 265-278 (2008)
73. Han, Y.G. et al. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat. Neurosci. 11, 277-284 (2008)
74. Lehtinen, M.K. et al. The cerebrospinal fluid provides a proliferativeniche for neural progenitor cells. Neuron 69, 893905 (2011)
75. Doetsch, F., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Cellular composition and threedimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046-5061 (1997) (Pubitemid 27263818)
76. Quinones-Hinojosa, A. et al. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol. 494, 415-434 (2006) (Pubitemid 41794059)
77. Rasika, S., Alvarez-Buylla, A. & Nottebohm, F. BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron 22, 53-62 (1999) (Pubitemid 29070093)
78. Hartog, T.E. et al. Brain-derived neurotrophic factor signaling in the HVC is required for testosterone-induced song of female canaries. J. Neurosci. 29, 15511-15519 (2009)
79. Bergers, G. et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2, 737-744 (2000)
80. Kim, D.H. et al. Testosterone-induced matrix metalloproteinase activation is a checkpoint for neuronal addition to the adult songbird brain. J. Neurosci. 28, 208-216 (2008)
81. Wang L., et al. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin- activated endothelial cells promote neural progenitor cell migration. J. Neurosci. 26 5996-6003 (2006). (Pubitemid 44318365)
82. Jin, K. et al. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. USA 98, 4710-4715 (2001) (Pubitemid 32295041)
83. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. & Lindvall, O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963-970 (2002) (Pubitemid 35033700)
84. Parent, J.M., Vexler, Z.S., Gong, C., Derugin, N. & Ferriero, D.M. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52, 802-813 (2002) (Pubitemid 35403191)
85. Yamashita T., et al. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J. Neurosci. 26 6627-6636 (2006). (Pubitemid 44318344)
86. Chmielnicki,E., Benraiss, A., Economides, A.N. & Goldman, S.A. Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J. Neurosci. 24, 2133-2142 (2004) (Pubitemid 38314545)
87. Wang, X. et al. P2X7 receptor inhibition improves recovery after spinal cord injury. Nat. Med. 10, 821-827 (2004) (Pubitemid 39070855)
88. Greenberg, D.A. & Jin, K. From angiogenesis to neuropathology. Nature 438, 954-959 (2005) (Pubitemid 43093961)
89. Monje, M.L. & Palmer, T. Radiation injury and neurogenesis. Curr. Opin. Neurol. 16, 129134 (2003)
90. Monje, M.L., Toda, H. & Palmer, T. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302, 1760-1765 (2003) (Pubitemid 37505739)
91. Sim, F.J. et al.Complementary patterns of gene expression by adult human oligodendrocyte progenitor cells and their white matter environment. Ann. Neurol. 59, 763-779 (2006) (Pubitemid 43673154)
92. Poimenidi, E., Hatziapostolou, M. & Papadimitriou, E. Serum stimulates Pleiotrophin gene expression in an AP-1-dependent manner in human endothelial and glioblastoma cells. Anticancer Res. 29, 349-354 (2009)
93. Chang, Y. et al. Secretion of pleiotrophin stimulates breast cancer progression through remodeling of the tumor microenvironment. Proc. Natl. Acad. Sci. USA 104, 10888-10893 (2007) (Pubitemid 47175196)
94. Arai, K. & Lo, E.H. An oligovascular niche cerebral endothelial cells promote the survival and proliferation of oligodendrocyte precursor cells. J. Neurosci. 29, 4351-4355 (2009)
95. Gadea, A., Aguirre, A., Haydar, T.F. & Gallo, V. Endothelin-1 regulates oligodendrocyte development. J. Neurosci. 29, 10047-10062 (2009)
96. Aerts, I. et al. The expression of ecto-nucleotide pyrophosphatase/ phosphodiesterase 1 (E-NPP1) is correlated with astrocytic tumor grade. Clin. Neurol. Neurosurg. 113, 224-229 (2011)
97. Bao, S. et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 66, 7843-7848 (2006) (Pubitemid 44299144)
98. Gilbertson, R.J. & Rich, J.N. Making a tumor's bed: glioblastoma stem cells and the vascular niche. Nat. Rev. Cancer 7, 733-736 (2007) (Pubitemid 47463683)
99. Cho, S.R. et al. Induction of neostriatal neurogenesis slows disease progression in a transgenic murine model of Huntington disease. J. Clin. Invest. 117, 2889-2902 (2007).
100. Im, S.H. et al. Induction ofstriatal neurogenesis enhances functional recovery in an adult animal model of neonatal hypoxic-ischemic brain injury. Neuroscience 169, 259-268 (2010).