The vascular niche in adult neurogenesis

Mechanisms of Development

Volumn 138, Issue , 2015, Pages 56-62

  Licht, Tamar ^a   Keshet, Eli ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Adult neurogenesis; Angiogenesis; Neural stem cells; Neurovascular unit

Indexed keywords

EPHRIN B2; TRANSCRIPTION FACTOR HES 1; VASCULOTROPIN;

ARTICLE; ASTROCYTE; BLOOD FLOW; BRAIN BLOOD VESSEL; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL RENEWAL; CHOROID PLEXUS; CYTOPLASM; DENTATE GYRUS; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; GRANULE CELL; HIPPOCAMPUS; HUMAN; IN VIVO STUDY; LEARNING; MEMORY; MORPHOLOGY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; OLFACTORY BULB; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; VASCULARIZATION; ANIMAL; BRAIN; PHYSIOLOGY; STEM CELL NICHE;

ANIMALS; BRAIN; HUMANS; NEUROGENESIS; NEURONS; STEM CELL NICHE;

EID: 84983095294     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2015.06.001     Document Type: Article

References (69)

1. Aimone J.B., Li Y., Lee S.W., Clemenson G.D., Deng W., Gage F.H. Regulation and function of adult neurogenesis: from genes to cognition. Physiol. Rev. 2014, 94:991-1026.
2. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J. Comp. Neurol. 1969, 136:269-293.
3. Andreu-Agullo 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. 2009, 12:1514-1523.
4. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 2002, 8:963-970.
5. Bjornsson C.S., Apostolopoulou M., Tian Y., Temple S. It takes a village: constructing the neurogenic niche. Dev. Cell 2015, 32:435-446.
6. Bonaguidi M.A., Wheeler M.A., Shapiro J.S., Stadel R.P., Sun G.J., Ming G.L., Song H. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011, 145:1142-1155.
7. Bouab M., Paliouras G.N., Aumont A., Forest-Berard K., Fernandes K.J. Aging of the subventricular zone neural stem cell niche: evidence for quiescence-associated changes between early and mid-adulthood. Neuroscience 2011, 173:135-149.
8. Bovetti S., Hsieh Y.C., Bovolin P., Perroteau I., Kazunori T., Puche A.C. Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb. J. Neurosci. 2007, 27:5976-5980.
9. Bozoyan L., Khlghatyan J., Saghatelyan A. Astrocytes control the development of the migration-promoting vasculature scaffold in the postnatal brain via VEGF signaling. J. Neurosci. 2012, 32:1687-1704.
10. Cao L., Jiao X., Zuzga D.S., Liu Y., Fong D.M., Young D., During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 2004, 36:827-835.
11. Codega P., Silva-Vargas V., Paul A., Maldonado-Soto A.R., Deleo A.M., Pastrana E., Doetsch F. Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron 2014, 82:545-559.
12. Colin-Castelan D., Phillips-Farfan B.V., Gutierrez-Ospina G., Fuentes-Farias A.L., Baez-Saldana A., Padilla-Cortes P., Melendez-Herrera E. EphB4 is developmentally and differentially regulated in blood vessels throughout the forebrain neurogenic niche in the mouse brain: implications for vascular remodeling. Brain Res. 2011, 1383:90-98.
13. Crouch E.E., Liu C., Silva-Vargas V., Doetsch F. Regional and stage-specific effects of prospectively purified vascular cells on the adult V-SVZ neural stem cell lineage. J. Neurosci. 2015, 35:4528-4539.
14. Delgado A.C., Ferron S.R., Vicente D., Porlan E., Perez-Villalba A., Trujillo C.M., D'Ocon P., Farinas I. Endothelial NT-3 delivered by vasculature and CSF promotes quiescence of subependymal neural stem cells through nitric oxide induction. Neuron 2014, 83:572-585.
15. Ding L., Saunders T.L., Enikolopov G., Morrison S.J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012, 481:457-462.
16. Douet V., Kerever A., Arikawa-Hirasawa E., Mercier F. Fractone-heparan sulphates mediate FGF-2 stimulation of cell proliferation in the adult subventricular zone. Cell Prolif. 2013, 46:137-145.
17. Dranovsky A., Picchini A.M., Moadel T., Sisti A.C., Yamada A., Kimura S., Leonardo E.D., Hen R. Experience dictates stem cell fate in the adult hippocampus. Neuron 2011, 70:908-923.
18. Encinas J.M., Michurina T.V., Peunova N., Park J.H., Tordo J., Peterson D.A., Fishell G., Koulakov A., Enikolopov G. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 2011, 8:566-579.
19. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317.
20. Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., Kuo C.J., Palmer T.D. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 2003, 18:2803-2812.
21. Fuentealba L.C., Obernier K., Alvarez-Buylla A. Adult neural stem cells bridge their niche. Cell Stem Cell 2012, 10:698-708.
22. Goldman S.A., Chen Z. Perivascular instruction of cell genesis and fate in the adult brain. Nat. Neurosci. 2011, 14:1382-1389.
23. Gomez-Gaviro M.V., Scott C.E., Sesay A.K., Matheu A., Booth S., Galichet C., Lovell-Badge R. Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1317-1322.
24. Goshen I., Kreisel T., Ben-Menachem-Zidon O., Licht T., Weidenfeld J., Ben-Hur T., Yirmiya R. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatry 2008, 13:717-728.
25. Grade S., Weng Y.C., Snapyan M., Kriz J., Malva J.O., Saghatelyan A. Brain-derived neurotrophic factor promotes vasculature-associated migration of neuronal precursors toward the ischemic striatum. PLoS One 2013, 8:e55039.
26. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., Greenberg D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11946-11950.
27. Jin K., Sun Y., Xie L., Batteur S., Mao X.O., Smelick C., Logvinova A., Greenberg D.A. Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2003, 2:175-183.
28. Katsimpardi L., Litterman N.K., Schein P.A., Miller C.M., Loffredo F.S., Wojtkiewicz G.R., Chen J.W., Lee R.T., Wagers A.J., Rubin L.L. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 2014, 344:630-634.
29. Kazanis I., Lathia J.D., Vadakkan T.J., Raborn E., Wan R., Mughal M.R., Eckley D.M., Sasaki T., Patton B., Mattson M.P., Hirschi K.K., Dickinson M.E., ffrench-Constant C. Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J. Neurosci. 2010, 30:9771-9781.
30. Kerever A., Schnack J., Vellinga D., Ichikawa N., Moon C., Arikawa-Hirasawa E., Efird J.T., Mercier F. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 2007, 25:2146-2157.
31. Kokovay E., Goderie S., Wang Y., Lotz S., Lin G., Sun Y., Roysam B., Shen Q., Temple S. Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 2010, 7:163-173.
32. Lacar B., Young S.Z., Platel J.C., Bordey A. Gap junction-mediated calcium waves define communication networks among murine postnatal neural progenitor cells. Eur. J. Neurosci. 2011, 34:1895-1905.
33. Lacar B., Herman P., Hartman N.W., Hyder F., Bordey A. S phase entry of neural progenitor cells correlates with increased blood flow in the young subventricular zone. PLoS One 2012, 7:e31960.
34. Lacar B., Herman P., Platel J.C., Kubera C., Hyder F., Bordey A. Neural progenitor cells regulate capillary blood flow in the postnatal subventricular zone. J. Neurosci. 2012, 32:16435-16448.
35. Licht T., Eavri R., Goshen I., Shlomai Y., Mizrahi A., Keshet E. VEGF is required for dendritogenesis of newly born olfactory bulb interneurons. Development 2010, 137:261-271.
36. Licht T., Goshen I., Avital A., Kreisel T., Zubedat S., Eavri R., Segal M., Yirmiya R., Keshet E. Reversible modulations of neuronal plasticity by VEGF. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5081-5086.
37. Licht T., Dor-Wollman T., Ben-Zvi A., Rothe G., Keshet E. Vessel maturation schedule determines vulnerability to neuronal injuries of prematurity. J. Clin. Invest. 2015, 125:1319-1328.
38. Livneh Y., Adam Y., Mizrahi A. Odor processing by adult-born neurons. Neuron 2014, 81:1097-1110.
39. Llorens-Martin M., Torres-Aleman I., Trejo J.L. Exercise modulates insulin-like growth factor 1-dependent and -independent effects on adult hippocampal neurogenesis and behaviour. Mol. Cell. Neurosci. 2010, 44:109-117.
40. Lopez-Lopez C., LeRoith D., Torres-Aleman I. Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9833-9838.
41. Louissaint A., Rao S., Leventhal C., Goldman S.A. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 2002, 34:945-960.
42. Lugert S., Basak O., Knuckles P., Haussler U., Fabel K., Gotz M., Haas C.A., Kempermann G., Taylor V., Giachino C. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 2010, 6:445-456.
43. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 1999, 22:105-122.
44. Mercier F., Douet V. Bone morphogenetic protein-4 inhibits adult neurogenesis and is regulated by fractone-associated heparan sulfates in the subventricular zone. J. Chem. Neuroanat. 2014, 57-58:54-61.
45. Mercier F., Kitasako J.T., Hatton G.I. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J. Comp. Neurol. 2002, 451:170-188.
46. Mignone J.L., Kukekov V., Chiang A.S., Steindler D., Enikolopov G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol. 2004, 469:311-324.
47. 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 2008, 3:265-278.
48. Ottone C., Krusche B., Whitby A., Clements M., Quadrato G., Pitulescu M.E., Adams R.H., Parrinello S. Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells. Nat. Cell Biol. 2014, 16(11):1045-1056.
49. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 2000, 425:479-494.
50. Pereira A.C., Huddleston D.E., Brickman A.M., Sosunov A.A., Hen R., McKhann G.M., Sloan R., Gage F.H., Brown T.R., Small S.A. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5638-5643.
51. Petrik D., Yun S., Latchney S.E., Kamrudin S., LeBlanc J.A., Bibb J.A., Eisch A.J. Early postnatal in vivo gliogenesis from nestin-lineage progenitors requires cdk5. PLoS One 2013, 8:e72819.
52. Ponti G., Obernier K., Alvarez-Buylla A. Lineage progression from stem cells to new neurons in the adult brain ventricular-subventricular zone. Cell Cycle 2013, 12:1649-1650.
53. Ramirez-Castillejo C., Sanchez-Sanchez F., Andreu-Agullo C., Ferron S.R., Aroca-Aguilar J.D., Sanchez P., Mira H., Escribano J., Farinas I. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci. 2006, 9:331-339.
54. Shen Q., Goderie S.K., 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, 304:1338-1340.
55. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.M., Goderie S.K., Roysam B., Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300.
56. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J.C., Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003, 299:117-120.
57. Sierra A., Encinas J.M., Deudero J.J., Chancey J.H., Enikolopov G., Overstreet-Wadiche L.S., Tsirka S.E., Maletic-Savatic M. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010, 7:483-495.
58. Snapyan M., Lemasson M., Brill M.S., Blais M., Massouh M., Ninkovic J., Gravel C., Berthod F., Gotz M., Barker P.A., Parent A., Saghatelyan A. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J. Neurosci. 2009, 29:4172-4188.
59. Spalding K.L., Bergmann O., Alkass K., Bernard S., Salehpour M., Huttner H.B., Bostrom E., Westerlund I., Vial C., Buchholz B.A., Possnert G., Mash D.C., Druid H., Frisen J. Dynamics of hippocampal neurogenesis in adult humans. Cell 2013, 153:1219-1227.
60. Tang W., Zeve D., Suh J.M., Bosnakovski D., Kyba M., Hammer R.E., Tallquist M.D., Graff J.M. White fat progenitor cells reside in the adipose vasculature. Science 2008, 322:583-586.
61. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., Garcia-Verdugo J.M., Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3:279-288.
62. Udo H., Yoshida Y., Kino T., Ohnuki K., Mizunoya W., Mukuda T., Sugiyama H. Enhanced adult neurogenesis and angiogenesis and altered affective behaviors in mice overexpressing vascular endothelial growth factor 120. J. Neurosci. 2008, 28:14522-14536.
63. Van der Borght K., Kobor-Nyakas D.E., Klauke K., Eggen B.J., Nyakas C., Van der Zee E.A., Meerlo P. Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 2009, 19:928-936.
64. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 1999, 2:266-270.
65. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 2005, 25:8680-8685.
66. Villeda S.A., Luo J., Mosher K.I., Zou B., Britschgi M., Bieri G., Stan T.M., Fainberg N., Ding Z., Eggel A., Lucin K.M., Czirr E., Park J.S., Couillard-Despres S., Aigner L., Li G., Peskind E.R., Kaye J.A., Quinn J.F., Galasko D.R., Xie X.S., Rando T.A., Wyss-Coray T. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 2011, 477:90-94.
67. Vivar C., van Praag H. Functional circuits of new neurons in the dentate gyrus. Front. Neural Circuits 2013, 7:15.
68. 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. 2009, 516:94-104.
69. Yoshida S., Sukeno M., Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007, 317:1722-1726.