Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter February 14, 2017

Blood-brain barrier-supported neurogenesis in healthy and diseased brain

  • Elena A. Pozhilenkova , Olga L. Lopatina , Yulia K. Komleva , Vladimir V. Salmin and Alla B. Salmina EMAIL logo

Abstract

Adult neurogenesis is one of the most important mechanisms contributing to brain development, learning, and memory. Alterations in neurogenesis underlie a wide spectrum of brain diseases. Neurogenesis takes place in highly specialized neurogenic niches. The concept of neurogenic niches is becoming widely accepted due to growing evidence of the important role of the microenvironment established in the close vicinity to stem cells in order to provide adequate control of cell proliferation, differentiation, and apoptosis. Neurogenic niches represent the platform for tight integration of neurogenesis and angiogenesis supported by specific properties of cerebral microvessel endothelial cells contributing to establishment of partially compromised blood-brain barrier (BBB) for the adjustment of local conditions to the current metabolic needs of stem and progenitor cells. Here, we review up-to-date data on microvascular dynamics in activity-dependent neurogenesis, specific properties of BBB in neurogenic niches, endothelial-driven mechanisms of clonogenic activity, and future perspectives for reconstructing the neurogenic niches in vitro.

Acknowledgments

The study is supported by a grant of the Russian Science Foundation (project N 14-25-00054).

  1. Conflicts of interest statement: All authors declare that there are no actual or potential conflicts of interest concerning the work presented in this article.

References

Abbott, N.J. (2002). Astrocyte-endothelial interactions and blood-brain barrier permeability. J. Anat. 200, 629–638.10.1046/j.1469-7580.2002.00064.xSearch in Google Scholar PubMed PubMed Central

Abdollahi, H., Harris, L.J., Zhang, P., McIlhenny, S., Tulenko, T., and DiMuzio, P.J. (2011). The role of hypoxia in stem cell differentiation and therapeutics. J. Surg. Res. 165, 112–117.10.1016/j.jss.2009.09.057Search in Google Scholar PubMed PubMed Central

Alvarez, J.I., Dodelet-Devillers, A., Kebir, H., Ifergan, I., Fabre, P.J., Terouz, S., Sabbagh, M., Wosik, K., Bourbonnière, L., Bernard, M., et al. (2011). The hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 334, 1727–1731.10.1126/science.1206936Search in Google Scholar PubMed

Alvarez, Z., Castano, O., Castells, A.A., Mateos-Timoneda, M.A., Planell, J.A., Engel, E., and Alcantara, S. (2014). Neurogenesis and vascularization of the damaged brain using a lactate-releasing biomimetic scaffold. Biomaterials 35, 4769–4781.10.1016/j.biomaterials.2014.02.051Search in Google Scholar PubMed

Alvarez, Z., Hyroššová, P., Perales, J.C., and Alcántara, S. (2016). Neuronal progenitor maintenance requires lactate metabolism and PEPCK-M-directed cataplerosis. Cereb. Cortex 26, 1046–1058.10.1093/cercor/bhu281Search in Google Scholar PubMed

Ardelt, A.A., Bhattacharyya, B.J., Belmadani, A., Ren, D., and Miller, R.J. (2013). Stromal derived growth factor-1 (CXCL12) modulates synaptic transmission to immature neurons during post-ischemic cerebral repair. Exp. Neurol. 248, 246–253.10.1016/j.expneurol.2013.06.017Search in Google Scholar PubMed PubMed Central

Asai, M., Takeuchi, K., Saotome, M., Urushida, T., Katoh, H., Satoh, H., Hayashi, H., and Watanabe, H. (2009). Extracellular acidosis suppresses endothelial function by inhibiting store-operated Ca2+ entry via non-selective cation channels. Cardiovasc. Res. 83, 97–105.10.1093/cvr/cvp105Search in Google Scholar PubMed

Ashpole, N.M., Warrington, J.P., Mitschelen, M.C., Yan, H., Sosnowska, D., Gautam, T., Farley, J.A., Csiszar, A., Ungvari, Z., and Sonntag, W.E. (2014). Systemic influences contribute to prolonged microvascular rarefaction after brain irradiation: a role for endothelial progenitor cells. Am. J. Physiol. Heart Circ. Physiol. 307, H858–H868.10.1152/ajpheart.00308.2014Search in Google Scholar PubMed PubMed Central

Azim, K., Fischer, B., Hurtado-Chong, A., Draganova, K., Cantu, C., Zemke, M., Sommer, L., Butt, A., and Raineteau, O. (2014). Persistent Wnt/β-catenin signaling determines dorsalization of the postnatal subventricular zone and neural stem cell specification into oligodendrocytes and glutamatergic neurons. Stem Cells 32, 1301–1312.10.1002/stem.1639Search in Google Scholar PubMed

Badaut, J. and Bix, G.J. (2014). Vascular neural network phenotypic transformation after traumatic injury: potential role in long-term sequelae. Transl. Stroke Res. 5, 394–406.10.1007/s12975-013-0304-zSearch in Google Scholar PubMed PubMed Central

Bergersen, L.H. (2015). Lactate transport and signaling in the brain: potential therapeutic targets and roles in body-brain interaction. J. Cereb. Blood Flow Metab. 35, 176–185.10.1038/jcbfm.2014.206Search in Google Scholar PubMed PubMed Central

Biron, K.E., Dickstein, D.L., Gopaul, R., and Jefferies, W.A. (2011). Amyloid triggers extensive cerebral angiogenesis causing blood brain barrier permeability and hypervascularity in Alzheimer’s disease. PLoS One 6, e23789.10.1371/journal.pone.0023789Search in Google Scholar PubMed PubMed Central

Bjornsson, C.S., Apostolopoulou, M., Tian, Y., and Temple, S. (2015). It takes a village: constructing the neurogenic niche. Dev. Cell 32, 435–446.10.1016/j.devcel.2015.01.010Search in Google Scholar PubMed PubMed Central

Black, J.E., Isaacs, K.R., Anderson, B.J., Alcantara, A.A., and Greenough, W.T. (1990). Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl. Acad. Sci. U.S.A. 87, 5568–5572.10.1073/pnas.87.14.5568Search in Google Scholar PubMed PubMed Central

Boumezbeur, F., Petersen, K.F., Cline, G.W., Mason, G.F., Behar, K.L., Shulman, G.I., and Rothman, D.L. (2010). The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J. Neurosci. 30, 13983–13991.10.1523/JNEUROSCI.2040-10.2010Search in Google Scholar PubMed PubMed Central

Brown, B.N. and Badylak, S.F. (2014). Extracellular matrix as an inductive scaffold for functional tissue reconstruction. Transl. Res. 163, 268–285.10.1016/B978-0-12-800548-4.00002-4Search in Google Scholar

Bruel-Jungerman, E., Davis, S., Rampon, C., and Laroche, S. (2006). Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J. Neurosci. 26, 5888–5893.10.1523/JNEUROSCI.0782-06.2006Search in Google Scholar PubMed PubMed Central

Bullitt, E., Zeng, D., Gerig, G., Aylward, S., Joshi, S., Smith, J.K., Lin, W., and Ewend, M.G. (2005). Vessel tortuosity and brain tumor malignancy: a blinded study. Acad. Radiol. 12, 1232–1240.10.1016/j.acra.2005.05.027Search in Google Scholar PubMed PubMed Central

Burgess, R.J., Agathocleous, M., and Morrison, S.J. (2014). Metabolic regulation of stem cell function. J. Intern. Med. 276, 12–24.10.1111/joim.12247Search in Google Scholar PubMed PubMed Central

Campos-Bedolla, P., Walter, F.R., Veszelka, S., and Deli, M.A. (2014). Role of the blood-brain barrier in the nutrition of the central nervous system. Arch. Med. Res. 45, 610–638.10.1016/j.arcmed.2014.11.018Search in Google Scholar PubMed

Candelario, K.M., Shuttleworth, C.W., and Cunningham, L.A. (2013). Neural stem/progenitor cells display a low requirement for oxidative metabolism independent of hypoxia inducible factor-1α expression. J. Neurochem. 125, 420–429.10.1111/jnc.12204Search in Google Scholar PubMed PubMed Central

Ceradini, D.J., Kulkarni, A.R., Callaghan, M.J., Tepper, O.M., Bastidas, N., Kleinman, M.E., Capla, J.M., Galiano, R.D., Levine, J.P., and Gurtner, G.C. (2004). Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10, 858–864.10.1038/nm1075Search in Google Scholar PubMed

Chambers, R.A. and Conroy, S.K. (2007). Network modeling of adult neurogenesis: shifting rates of neuronal turnover optimally gears network learning according to novelty gradient. J. Cogn. Neurosci. 19, 1–12.10.1162/jocn.2007.19.1.1Search in Google Scholar PubMed PubMed Central

Chen, A., Dong, L., Leffler, N.R., Asch, A.S., Witte, O.N., and Yang, L.V. (2011). Activation of GPR4 by acidosis increases endothelial cell adhesion through the cAMP/Epac pathway. PLoS One 6, e27586.10.1371/journal.pone.0027586Search in Google Scholar PubMed PubMed Central

Chen, C.-C.V., Chen, Y.-C., Hsiao, H.-Y., Chang, C., and Chern, Y. (2013). Neurovascular abnormalities in brain disorders: highlights with angiogenesis and magnetic resonance imaging studies. J. Biomed. Sci. 20, 47.10.1186/1423-0127-20-47Search in Google Scholar PubMed PubMed Central

Chen, B.H., Park, J.H., Cho, J.H., Kim, I.H., Lee, J.C., Lee, T.K., Ahn, J.H., Tae, H.J., Shin, B.N., Kim, J.D., et al. (2016). Tanshinone I enhances neurogenesis in the mouse hippocampal dentate gyrus via increasing Wnt-3, phosphorylated glycogen synthase kinase-3β and β-catenin immunoreactivities. Neurochem. Res. 41, 1958–1968.10.1007/s11064-016-1906-0Search in Google Scholar PubMed

Chi, Y., Zhang, X., Zhang, Z., Mitsui, T., Kamiyama, M., Takeda, M., and Yao, J. (2016). Connexin43 hemichannels contributes to the disassembly of cell junctions through modulation of intracellular oxidative status. Redox Biol. 9, 198–209.10.1016/j.redox.2016.08.008Search in Google Scholar PubMed PubMed Central

Choi, H.W., Kim, J.H., Chung, M.K., Hong, Y.J., Jang, H.S., Seo, B.J., Jung, T.H., Kim, J.S., Chung, H.M., Byun, S.J., et al. (2015a). Mitochondrial and metabolic remodeling during reprogramming and differentiation of the reprogrammed cells. Stem Cells Dev. 24, 1366–1373.10.1089/scd.2014.0561Search in Google Scholar PubMed

Choi, H.Y., Saha, S.K., Kim, K., Kim, S., Yang, G.-M., Kim, B., Kim, J.-h., and Cho, S.-G. (2015b). G protein-coupled receptors in stem cell maintenance and somatic reprogramming to pluripotent or cancer stem cells. BMB Rep. 48, 68–80.10.5483/BMBRep.2015.48.2.250Search in Google Scholar PubMed PubMed Central

Chou, C.-H. and Modo, M. (2016). Human neural stem cell-induced endothelial morphogenesis requires autocrine/paracrine and juxtacrine signaling. Sci. Rep. 6, 29029.10.1038/srep29029Search in Google Scholar PubMed PubMed Central

Crouch, E.E., Liu, C., Silva-Vargas, V., and Doetsch, F. (2015). Regional and stage-specific effects of prospectively purified vascular cells on the adult V-SVZ neural stem cell lineage. J. Neurosci. 35, 4528–4539.10.1523/JNEUROSCI.1188-14.2015Search in Google Scholar PubMed PubMed Central

D’Arcangelo, D., Facchiano, F., Barlucchi, L.M., Melillo, G., Illi, B., Testolin, L., Gaetano, C., and Capogrossi, M.C. (2000). Acidosis inhibits endothelial cell apoptosis and function and induces basic fibroblast growth factor and vascular endothelial growth factor expression. Circ. Res. 86, 312–318.10.1161/01.RES.86.3.312Search in Google Scholar

Daneman, R., Agalliu, D., Zhou, L., Kuhnert, F., Kuo, C.J., and Barres, B.A. (2009). Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 106, 641–646.10.1073/pnas.0805165106Search in Google Scholar PubMed PubMed Central

Deng, J., Zhang, J., Feng, C., Xiong, L., and Zuo, Z. (2014). Critical role of matrix metalloprotease-9 in chronic high fat diet-induced cerebral vascular remodelling and increase of ischaemic brain injury in mice. Cardiovasc. Res. 103, 473–484.10.1093/cvr/cvu154Search in Google Scholar PubMed PubMed Central

Di Santo, S., Seiler, S., Fuchs, A.-L., Staudigl, J., and Widmer, H.R. (2014). The secretome of endothelial progenitor cells promotes brain endothelial cell activity through PI3-kinase and MAP-kinase. PLoS One 9, e95731.10.1371/journal.pone.0095731Search in Google Scholar PubMed PubMed Central

Diaz, R., Miguel, P.M., Deniz, B.F., Confortim, H.D., Barbosa, S., Mendonca, M.C., da Cruz-Hofling, M.A., and Pereira, L.O. (2016). Environmental enrichment attenuates the blood brain barrier dysfunction induced by the neonatal hypoxia-ischemia. Int. J. Dev. Neurosci. 53, 35–45.10.1016/j.ijdevneu.2016.06.006Search in Google Scholar PubMed

Ding, Y.H., Li, J., Zhou, Y., Rafols, J.A., Clark, J.C., and Ding, Y. (2006). Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr. Neurovasc. Res. 3, 15–23.10.2174/156720206775541787Search in Google Scholar PubMed

Dong, L., Li, Z., Leffler, N.R., Asch, A.S., Chi, J.T., and Yang, L.V. (2013). Acidosis activation of the proton-sensing GPR4 receptor stimulates vascular endothelial cell inflammatory responses revealed by transcriptome analysis. PLoS One 8, e61991.10.1371/journal.pone.0061991Search in Google Scholar PubMed PubMed Central

Dorr, A., Thomason, L.A., Koletar, M.M., Joo, I.L., Steinman, J., Cahill, L.S., Sled, J.G., and Stefanovic, B. (2016). Effects of voluntary exercise on structure and function of cortical microvasculature. J. Cereb. Blood Flow Metab. [Epub ahead of print]. pii: 0271678X16669514.10.1177/0271678X16669514Search in Google Scholar PubMed PubMed Central

Ebong, E.E. and DePaola, N. (2013). Specificity in the participation of connexin proteins in flow-induced endothelial gap junction communication. Pflüger’s Arch. 465, 1293–1302.10.1007/s00424-013-1245-9Search in Google Scholar PubMed

Ehret, F., Vogler, S., and Kempermann, G. (2015). A co-culture model of the hippocampal neurogenic niche reveals differential effects of astrocytes, endothelial cells and pericytes on proliferation and differentiation of adult murine precursor cells. Stem Cell Res. 15, 514–521.10.1016/j.scr.2015.09.010Search in Google Scholar PubMed

Ennis, S.R., Ren, X.D., and Betz, A.L. (1996). Mechanisms of sodium transport at the blood-brain barrier studied with in situ perfusion of rat brain. J. Neurochem. 66, 756–763.10.1046/j.1471-4159.1996.66020756.xSearch in Google Scholar PubMed

Ertaylan, G., Okawa, S., Schwamborn, J.C., and del Sol, A. (2014). Gene regulatory network analysis reveals differences in site-specific cell fate determination in mammalian brain. Front. Cell. Neurosci. 8, 437.10.3389/fncel.2014.00437Search in Google Scholar PubMed PubMed Central

Ezan, P., Andre, P., Cisternino, S., Saubamea, B., Boulay, A.C., Doutremer, S., Thomas, M.A., Quenech’du, N., Giaume, C., and Cohen-Salmon, M. (2012). Deletion of astroglial connexins weakens the blood-brain barrier. J. Cereb. Blood Flow Metab. 32, 1457–1467.10.1038/jcbfm.2012.45Search in Google Scholar PubMed PubMed Central

Fiorelli, R., Azim, K., Fischer, B., and Raineteau, O. (2015). Adding a spatial dimension to postnatal ventricular-subventricular zone neurogenesis. Development 142, 2109–2120.10.1242/dev.119966Search in Google Scholar PubMed

Fukumura, D., Xu, L., Chen, Y., Gohongi, T., Seed, B., and Jain, R.K. (2001). Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res. 61, 6020–6024.Search in Google Scholar

Gerhart, D.Z., Enerson, B.E., Zhdankina, O.Y., Leino, R.L., and Drewes, L.R. (1997). Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats. Am. J. Physiol. 273, E207–E213.10.1152/ajpendo.1997.273.1.E207Search in Google Scholar PubMed

Ghandour, M.S., Langley, O.K., Zhu, X.L., Waheed, A., and Sly, W.S. (1992). Carbonic anhydrase IV on brain capillary endothelial cells: a marker associated with the blood-brain barrier. Proc. Natl. Acad. Sci. U.S.A. 89, 6823–6827.10.1073/pnas.89.15.6823Search in Google Scholar PubMed PubMed Central

Gil-Mohapel, J., Brocardo, P.S., Choquette, W., Gothard, R., Simpson, J.M., and Christie, B.R. (2013). Hippocampal neurogenesis levels predict WATERMAZE search strategies in the aging brain. PLoS One 8, e75125.10.1371/journal.pone.0075125Search in Google Scholar PubMed PubMed Central

Giuliani, A., Moroncini, F., Mazzoni, S., Belicchi, M.L.C., Villa, C., Erratico, S., Colombo, E., Calcaterra, F., Brambilla, L., Torrente, Y., et al. (2014). Polyglycolic acid-polylactic acid scaffold response to different progenitor cell in vitro cultures: a demonstrative and comparative X-ray synchrotron radiation phase-contrast microtomography study. Tissue Eng. C Methods 20, 308–316.10.1089/ten.tec.2013.0213Search in Google Scholar

Goldberg, J.S. and Hirschi, K.K. (2009). Diverse roles of the vasculature within the neural stem cell niche. Regen. Med. 4, 879–897.10.2217/rme.09.61Search in Google Scholar PubMed PubMed Central

Gomes, L.C., Benedetto, G.D., and Scorrano, L. (2011). During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 13, 589–598.10.1038/ncb2220Search in Google Scholar PubMed PubMed Central

Guerra, M.M., Henzi, R., Ortloff, A., Lichtin, N., Vío, K., Jiménez, A.J., Dominguez-Pinos, M.D., González, C., Jara, M.C., Hinostroza, F., et al. (2015). Cell junction pathology of neural stem cells is associated with ventricular zone disruption, hydrocephalus, and abnormal neurogenesis. J. Neuropathol. Exp. Neurol. 74, 653–671.10.1097/NEN.0000000000000203Search in Google Scholar PubMed

Hagihara, H., Takao, K., Walton, N.M., Matsumoto, M., and Miyakawa, T. (2013). Immature dentate gyrus: an endophenotype of neuropsychiatric disorders. Neural Plasticity 2013, 318596.10.1155/2013/318596Search in Google Scholar PubMed PubMed Central

Harb, R., Whiteus, C., Freitas, C., and Grutzendler, J. (2013). In vivo imaging of cerebral microvascular plasticity from birth to death. J. Cereb. Blood Flow Metab. 33, 146–156.10.1038/jcbfm.2012.152Search in Google Scholar PubMed PubMed Central

Harjes, U., Bridges, E., McIntyre, A., Fielding, B.A., and Harris, A.L. (2014). Fatty acid binding protein 4, a point of convergence for angiogenic and metabolic signalling pathways in endothelial cells. J. Biol. Chem. 289, 1–19.10.1074/jbc.M114.576512Search in Google Scholar PubMed PubMed Central

Hopkins, A.M., DeSimone, E., Chwalek, K., and Kaplan, D.L. (2015). 3D in vitro modeling of the central nervous system. Progr. Neurobiol. 125, 1–25.10.1016/j.pneurobio.2014.11.003Search in Google Scholar PubMed PubMed Central

Hu, C., Fan, L., Cen, P., Chen, E., Jiang, Z., and Li, L. (2016). Energy metabolism plays a critical role in stem cell maintenance and differentiation. Int. J. Mol. Sci. 17, 253.10.3390/ijms17020253Search in Google Scholar PubMed PubMed Central

Huang, J., Li, Y., Tang, Y., Tang, G., Yang, G.Y., and Wang, Y. (2013a). CXCR4 antagonist AMD3100 protects blood-brain barrier integrity and reduces inflammatory response after focal ischemia in mice. Stroke 44, 190–197.10.1161/STROKEAHA.112.670299Search in Google Scholar PubMed

Huang, W.H., Chang, M.C., Tsai, K.S., Hung, M.C., Chen, H.L., and Hung, S.C. (2013b). Mesenchymal stem cells promote growth and angiogenesis of tumors in mice. Oncogene 32, 4343–4354.10.1038/onc.2012.458Search in Google Scholar PubMed

Inoue, K., Okamoto, M., Shibato, J., Lee, M.C., Matsui, T., Rakwal, R., and Soya, H. (2015). Long-term mild, rather than intense, exercise enhances adult hippocampal neurogenesis and greatly changes the transcriptomic profile of the hippocampus. PLoS One 10, e0128720.10.1371/journal.pone.0128720Search in Google Scholar PubMed PubMed Central

Ito, K. and Suda, T. (2014). Metabolic requirements for the maintenance of self-renewing stem cells. Nat. Rev. Mol. Cell Biol. 15, 243–256.10.1038/nrm3772Search in Google Scholar PubMed PubMed Central

Jefferies, W.A., Price, K.A., Biron, K.E., Fenninger, F., Pfeifer, C.G., and Dickstein, D.L. (2013). Adjusting the compass: new insights into the role of angiogenesis in Alzheimer’s disease. Alzheimer’s Res. Ther. 5, 64–64.10.1186/alzrt230Search in Google Scholar PubMed PubMed Central

Jiang, S., Xia, R., Jiang, Y., Wang, L., and Gao, F. (2014). Vascular endothelial growth factors enhance the permeability of the mouse blood-brain barrier. PLoS One 9, e86407.10.1371/journal.pone.0086407Search in Google Scholar PubMed PubMed Central

Jing, Z., Xu, H., Chen, X., Zhong, Q., Huang, J., Zhang, Y., Guo, W., Yang, Z., Ding, S., Chen, P., et al. (2016). The proton-sensing g-protein coupled receptor GPR4 promotes angiogenesis in head and neck cancer. PLoS One 11, e0152789.10.1371/journal.pone.0152789Search in Google Scholar PubMed PubMed Central

Joshi, R. and Tavana, H. (2015). Microengineered embryonic stem cells niche to induce neural differentiation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2015, 3557–3560.10.1109/EMBC.2015.7319161Search in Google Scholar PubMed

Karagiannis, A., Sylantyev, S., Hadjihambi, A., Hosford, P.S., Kasparov, S., and Gourine, A.V. (2016). Hemichannel-mediated release of lactate. J. Cereb. Blood Flow Metab. 36, 1202–1211.10.1177/0271678X15611912Search in Google Scholar PubMed PubMed Central

Karimi, M., Bahrami, S., Mirshekari, H., Basri, S.M., Nik, A.B., Aref, A.R., Akbari, M., and Hamblin, M.R. (2016). Microfluidic systems for stem cell-based neural tissue engineering. Lab. Chip 16, 2551–2571.10.1039/C6LC00489JSearch in Google Scholar PubMed PubMed Central

Kerr, A.L., Steuer, E.L., Pochtarev, V., and Swain, R.A. (2010). Angiogenesis but not neurogenesis is critical for normal learning and memory acquisition. Neuroscience 171, 214–226.10.1016/j.neuroscience.2010.08.008Search in Google Scholar PubMed

Khacho, M., Tarabay, M., Patten, D., Khacho, P., MacLaurin, J.G., Guadagno, J., Bergeron, R., Cregan, S.P., Harper, M.-E., Park, D.S., et al. (2014). Acidosis overrides oxygen deprivation to maintain mitochondrial function and cell survival. Nat. Commun. 5, 3550.10.1038/ncomms4550Search in Google Scholar PubMed PubMed Central

Khacho, M., Clark, A., Svoboda, D.S., Azzi, J., MacLaurin, J.G., Meghaizel, C., Sesaki, H., Lagace, D.C., Germain, M., Harper, M.E., et al. (2016). Mitochondrial dynamics impacts stem cell identity and fate decisions by regulating a nuclear transcriptional program. Cell Stem Cell 19, 232–247.10.1016/j.stem.2016.04.015Search in Google Scholar PubMed

Khilazheva, E.D., Boytsova, E.B., Pozhilenkova, E.A., Solonchuk, Y.R., and Salmina, A.B. (2015). The model of neurovascular unit in vitro consisting of three cells types. Tsitologiia 57, 710–713.Search in Google Scholar

Kim, D.-Y., Rhee, I., and Paik, J. (2014). Metabolic circuits in neural stem cells. Cell. Mol. Life Sci. 71, 4221–4241.10.1007/s00018-014-1686-0Search in Google Scholar PubMed PubMed Central

Kirby, E.D., Kuwahara, A.A., Messer, R.L., and Wyss-Coray, T. (2015). Adult hippocampal neural stem and progenitor cells regulate the neurogenic niche by secreting VEGF. Proc. Natl. Acad. Sci. U.S.A. 112, 4128–4133.10.1073/pnas.1422448112Search in Google Scholar PubMed PubMed Central

Kirste, I., Nicola, Z., Kronenberg, G., Walker, T.L., Liu, R.C., and Kempermann, G. (2015). Is silence golden? Effects of auditory stimuli and their absence on adult hippocampal neurogenesis. Brain Struct. Funct. 220, 1221–1228.10.1007/s00429-013-0679-3Search in Google Scholar PubMed PubMed Central

Knobloch, M., Braun, S.M., Zurkirchen, L., von Schoultz, C., Zamboni, N., Arauzo-Bravo, M.J., Kovacs, W.J., Karalay, O., Suter, U., Machado, R.A., et al. (2013). Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis. Nature 493, 226–230.10.1038/nature11689Search in Google Scholar PubMed PubMed Central

Kokovay, E., Goderie, S., Wang, Y., Lotz, S., Lin, G., Sun, Y., Roysam, B., Shen, Q., and 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, 163–173.10.1016/j.stem.2010.05.019Search in Google Scholar PubMed PubMed Central

Kostenis, E. (2004). Novel clusters of receptors for sphingosine-1-phosphate, sphingosylphosphorylcholine, and (lyso)-phosphatidic acid: new receptors for “old” ligands. J. Cell. Biochem. 92, 923–936.10.1002/jcb.20092Search in Google Scholar PubMed

Koutsakis, C. and Kazanis, I. (2016). How necessary is the vasculature in the life of neural stem and progenitor cells? Evidence from evolution, development and the adult nervous system. Front. Cell. Neurosci. 10, 35.10.3389/fncel.2016.00035Search in Google Scholar PubMed PubMed Central

Krezymon, A., Richetin, K., Halley, H., Roybon, L., Lassalle, J.-M., Francès, B., Verret, L., and Rampon, C. (2013). Modifications of hippocampal circuits and early disruption of adult neurogenesis in the Tg2576 mouse model of Alzheimer’s disease. PLoS One 8, e76497.10.1371/journal.pone.0076497Search in Google Scholar PubMed PubMed Central

Kunze, A., Congreso, M.R., Hartmann, C., Wallraff-Beck, A., Hüttmann, K., Bedner, P., Requardt, R., Seifert, G., Redecker, C., Willecke, K., et al. (2009). Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 106, 11336–11341.10.1073/pnas.0813160106Search in Google Scholar PubMed PubMed Central

Kuvacheva, N.V., Morgun, A.V., Komleva, Y.K., Khilazheva, E.D., Gorina, Y.V., Lopatina, O.L., Arutyunyan, S.A., and Salmina, A.B. (2015). In vitro modeling of brain progenitor cell development under the effect of environmental factors. Bull. Exp. Biol. Med. 159, 546–549.10.1007/s10517-015-3012-8Search in Google Scholar PubMed

Kuznetsov, A.V., Javadov, S., Guzun, R., Grimm, M., and Saks, V. (2013). Cytoskeleton and regulation of mitochondrial function: the role of β-tubulin II. Front. Physiol. 4, 82.10.3389/fphys.2013.00082Search in Google Scholar PubMed PubMed Central

Lam, T.I., Wise, P.M., and O’Donnell, M.E. (2009). Cerebral microvascular endothelial cell Na/H exchange: evidence for the presence of NHE1 and NHE2 isoforms and regulation by arginine vasopressin. Am. J. Physiol. Cell Physiol. 297, C278–289.10.1152/ajpcell.00093.2009Search in Google Scholar PubMed PubMed Central

Lange, C., Turrero Garcia, M., Decimo, I., Bifari, F., Eelen, G., Quaegebeur, A., Boon, R., Zhao, H., Boeckx, B., Chang, J., et al. (2016). Relief of hypoxia by angiogenesis promotes neural stem cell differentiation by targeting glycolysis. EMBO J. 35, 924–941.10.15252/embj.201592372Search in Google Scholar PubMed PubMed Central

Larson, T.A., Thatra, N.M., Lee, B.H., and Brenowitz, E.A. (2014). Reactive neurogenesis in response to naturally occurring apoptosis in an adult brain. J. Neurosci. 34, 13066–13076.10.1523/JNEUROSCI.3316-13.2014Search in Google Scholar PubMed PubMed Central

Lee, C., Hu, J., Ralls, S., Kitamura, T., Loh, Y.P., Yang, Y., Mukouyama, Y.-s., and Ahn, S. (2012). The molecular profiles of neural stem cell niche in the adult subventricular zone. PLoS One 7, e50501.10.1371/journal.pone.0050501Search in Google Scholar PubMed PubMed Central

Lezi, E., Lu, J., Selfridge, J.E., Burns, J.M., and Swerdlow, R.H. (2013). Lactate administration reproduces specific brain and liver exercise-related changes. J. Neurochem. 127, 91–100.10.1111/jnc.12394Search in Google Scholar PubMed PubMed Central

Li, Q., Ford, M.C., Lavik, E.B., and Madri, J.A. (2006). Modeling the neurovascular niche: VEGF- and BDNF-mediated cross-talk between neural stem cells and endothelial cells: an in vitro study. J. Neurosci. Res. 84, 1656–1668.10.1002/jnr.21087Search in Google Scholar PubMed

Li, G., Simon, M.J., Cancel, L.M., Shi, Z.-D., Ji, X., Tarbell, J.M., Morrison, B., and Fu, B.M. (2010a). Permeability of endothelial and astrocyte cocultures: in vitro blood-brain barrier models for drug delivery studies. Ann. Biomed. Eng. 38, 2499–2511.10.1007/s10439-010-0023-5Search in Google Scholar PubMed PubMed Central

Li, W., Prakash, R., Kelly-Cobbs, A.I., Ogbi, S., Kozak, A., El-Remessy, A.B., Schreihofer, D.A., Fagan, S.C., and Ergul, A. (2010b). Adaptive cerebral neovascularization in a model of type 2 diabetes: relevance to focal cerebral ischemia. Diabetes 59, 228–235.10.2337/db09-0902Search in Google Scholar PubMed PubMed Central

Li, N., Zhang, Q., Gao, S., Song, Q., Huang, R., Wang, L., Liu, L., Dai, J., Tang, M., and Cheng, G. (2013). Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci. Rep. 3, 1604.10.1038/srep01604Search in Google Scholar PubMed PubMed Central

Li, L., Candelario, K.M., Thomas, K., Wang, R., Wright, K., Messier, A., and Cunningham, L.A. (2014). Hypoxia inducible factor-1α (HIF-1α) is required for neural stem cell maintenance and vascular stability in the adult mouse SVZ. J. Neurosci. 34, 16713–16719.10.1523/JNEUROSCI.4590-13.2014Search in Google Scholar PubMed PubMed Central

Li, Y.-F., Ren, L.-N., Guo, G., Cannella, L.A., Chernaya, V., Samuel, S., Liu, S.-X., Wang, H., and Yang, X.-F. (2015). Endothelial progenitor cells in ischemic stroke: an exploration from hypothesis to therapy. J. Hematol. Oncol. 8, 33.10.1186/s13045-015-0130-8Search in Google Scholar PubMed PubMed Central

Liesa, M. and Shirihai, O.S. (2013). Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 17, 491–506.10.1016/j.cmet.2013.03.002Search in Google Scholar PubMed PubMed Central

Lin, R., Cai, J., Nathan, C., Wei, X., Schleidt, S., Rosenwasser, R., and Iacovitti, L. (2015). Neurogenesis is enhanced by stroke in multiple new stem cell niches along the ventricular system at sites of high BBB permeability. Neurobiol. Dis. 74, 229–239.10.1016/j.nbd.2014.11.016Search in Google Scholar PubMed

Liu, Z., Sneve, M., Haroldson, T.A., Smith, J.P., and Drewes, L.R. (2016). Regulation of monocarboxylic acid transporter 1 trafficking by the canonical Wnt/β-catenin pathway in rat brain endothelial cells requires cross-talk with notch signaling. J. Biol. Chem. 291, 8059–8069.10.1074/jbc.M115.710277Search in Google Scholar PubMed PubMed Central

Luo, J., Hu, X., Zhang, L., Li, L., Zheng, H., Li, M., and Zhang, Q. (2014). Physical exercise regulates neural stem cells proliferation and migration via SDF-1α/CXCR4 pathway in rats after ischemic stroke. Neurosci. Lett. 578, 203–208.10.1016/j.neulet.2014.06.059Search in Google Scholar PubMed

Magavi, S.S., Leavitt, B.R., and Macklis, J.D. (2000). Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951–955.10.1038/35016083Search in Google Scholar PubMed

Maheu, M., Devorak, J., Freibauer, A., Davoli, M.A., Turecki, G., and Mechawar, N. (2015). Increased doublecortin (DCX) expression and incidence of DCX-immunoreactive multipolar cells in the subventricular zone-olfactory bulb system of suicides. Front. Neuroanat. 9, 74. DOI: 10.3389/fnana.2015.00074.10.3389/fnana.2015.00074Search in Google Scholar PubMed PubMed Central

Mancuso, M.R., Kuhnert, F., and Kuo, C.J. (2008). Developmental angiogenesis of the central nervous system. Lymphat. Res. Biol. 6, 173–180.10.1089/lrb.2008.1014Search in Google Scholar PubMed PubMed Central

Masamoto, K., Takuwa, H., Seki, C., Taniguchi, J., Itoh, Y., Tomita, Y., Toriumi, H., Unekawa, M., Kawaguchi, H., Ito, H., et al. (2014). Microvascular sprouting, extension, and creation of new capillary connections with adaptation of the neighboring astrocytes in adult mouse cortex under chronic hypoxia. J. Cereb. Blood Flow Metab. 34, 325–331.10.1038/jcbfm.2013.201Search in Google Scholar PubMed PubMed Central

Mercier, F. (2016). Fractones: extracellular matrix niche controlling stem cell fate and growth factor activity in the brain in health and disease. Cell. Mol. Life Sci. 73, 4661–4674.10.1007/s00018-016-2314-ySearch in Google Scholar PubMed

Mercier, F., Kitasako, J.T., and Hatton, G.I. (2002). Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J. Comp. Neurol. 451, 170–188.10.1002/cne.10342Search in Google Scholar PubMed

Minami, H., Tashiro, K., Okada, A., Hirata, N., Yamaguchi, T., Takayama, K., Mizuguchi, H., and Kawabata, K. (2015). Generation of brain microvascular endothelial-like cells from human induced pluripotent stem cells by co-culture with C6 glioma cells. PLoS One 10, e0128890.10.1371/journal.pone.0128890Search in Google Scholar PubMed PubMed Central

Miyata, S. (2015). New aspects in fenestrated capillary and tissue dynamics in the sensory circumventricular organs of adult brains. Front. Neurosci. 9, 390.10.3389/fnins.2015.00390Search in Google Scholar PubMed PubMed Central

Mohyeldin, A., Garzón-Muvdi, T., and Quiñones-Hinojosa, A. (2010). Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7, 150–161.10.1016/j.stem.2010.07.007Search in Google Scholar PubMed

Montagne, A., Barnes, S.R., Sweeney, M.D., Halliday, M.R., Sagare, A.P., Zhao, Z., Toga, A.W., Jacobs, R.E., Liu, C.Y., Amezcua, L., et al. (2015). Blood-brain barrier breakdown in the aging human hippocampus. Neuron 85, 296–302.10.1016/j.neuron.2014.12.032Search in Google Scholar PubMed PubMed Central

Morgun, A.V., Ruzaeva, V.A., Boitsova, E.B., Taranushenko, T.E., Martynova, G.P., Tohidpour, A., and Salmina, A.B. (2015). Current opportunities in the identification of novel molecular targets for pharmacological correction of blood-brain barrier permeability. Eksp. Klin. Farmakol. 78, 41–50.Search in Google Scholar

Muffley, L.A., Pan, S.-C., Smith, A.N., Ga, M., Hocking, A.M., and Gibran, N.S. (2012). Differentiation state determines neural effects on microvascular endothelial cells. Exp. Cell. Res. 318, 2085–2093.10.1016/j.yexcr.2012.06.002Search in Google Scholar PubMed PubMed Central

Muoio, V., Persson, P.B., and Sendeski, M.M. (2014). The neurovascular unit – concept review. Acta Physiol. 210, 790–798.10.1111/apha.12250Search in Google Scholar PubMed

Nagasawa, K., Chiba, H., Fujita, H., Kojima, T., Saito, T., Endo, T., and Sawada, N. (2006). Possible involvement of gap junctions in the barrier function of tight junctions of brain and lung endothelial cells. J. Cell. Physiol. 208, 123–132.10.1002/jcp.20647Search in Google Scholar PubMed

Ndubuizu, O.I., Tsipis, C.P., Li, A., and LaManna, J.C. (2010). Hypoxia inducible factor-1 (HIF-1) independent microvascular angiogenesis in the aged rat brain. Brain Res. 1366, 101–109.10.1016/j.brainres.2010.09.064Search in Google Scholar PubMed PubMed Central

Nicola, Z., Fabel, K., and Kempermann, G. (2015). Development of the adult neurogenic niche in the hippocampus of mice. Front. Neuroanat. 9, 53.10.3389/fnana.2015.00053Search in Google Scholar

Okajima, F. (2013). Regulation of inflammation by extracellular acidification and proton-sensing GPCRs. Cell. Signalling 25, 2263–2271.10.1016/j.cellsig.2013.07.022Search in Google Scholar

Ottone, C. and Parrinello, S. (2015). Multifaceted control of adult SVZ neurogenesis by the vascular niche. Cell Cycle 14, 2222–2225.10.1080/15384101.2015.1049785Search in Google Scholar

Ottone, C., Krusche, B., Whitby, A., Clements, M., Quadrato, G., Pitulescu, M.E., Adams, R.H., and Parrinello, S. (2014). Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells. Nat. Cell Biol. 16, 1045–1056.10.1038/ncb3045Search in Google Scholar

Oyarce, K., Bongarzone, E.R., and Nualart, F. (2014). Unconventional neurogenic niches and neurogenesis modulation by vitamins. J. Stem Cell Res. Ther. 4, 184.Search in Google Scholar

Page, S., Munsell, A., and Al-Ahmad, A.J. (2016). Cerebral hypoxia/ischemia selectively disrupts tight junctions complexes in stem cell-derived human brain microvascular endothelial cells. Fluids Barriers CNS 13, 16.10.1186/s12987-016-0042-1Search in Google Scholar

Palmer, T.D., Willhoite, A.R., and Gage, F.H. (2000). Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479–494.10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3Search in Google Scholar

Palmiotti, C.A., Prasad, S., Naik, P., Abul, K.M.D., Sajja, R.K., Achyuta, A.H., and Cucullo, L. (2014). In vitro cerebrovascular modeling in the 21st century: current and prospective technologies. Pharm. Res. 31, 3229–3250.10.1007/s11095-014-1464-6Search in Google Scholar

Patel, R. and Alahmad, A.J. (2016). Growth-factor reduced Matrigel source influences stem cell derived brain microvascular endothelial cell barrier properties. Fluids Barriers CNS 13, 6.10.1186/s12987-016-0030-5Search in Google Scholar

Pierret, C., Morrison, J.A., Rath, P., Zigler, R.E., Engel, L.A., Fairchild, C.L., Shi, H., Maruniak, J.A., and Kirk, M.D. (2010). Developmental cues and persistent neurogenic potential within an in vitro neural niche. BMC Dev. Biol. 10, 5.10.1186/1471-213X-10-5Search in Google Scholar

Plane, J.M., Andjelkovic, A.V., Keep, R.F., and Parent, J.M. (2010). Intact and injured endothelial cells differentially modulate postnatal murine forebrain neural stem cells. Neurobiol. Dis. 37, 218–227.10.1016/j.nbd.2009.10.008Search in Google Scholar

Qiao, J., Huang, F., Naikawadi, R.P., Kim, K.S., Said, T., and Lum, H. (2006). Lysophosphatidylcholine impairs endothelial barrier function through the G protein-coupled receptor GPR4. Am. J. Physiol. Lung Cell Mol. Physiol. 291, L91–L101.10.1152/ajplung.00508.2005Search in Google Scholar PubMed

Rafii, S., Butler, J.M., and Ding, B.S. (2016). Angiocrine functions of organ-specific endothelial cells. Nature 529, 316–325.10.1038/nature17040Search in Google Scholar PubMed PubMed Central

Ravella, A., Ringstedt, T., Brion, J.P., Pandolfo, M., and Herlenius, E. (2015). Adult neural precursor cells form connexin-dependent networks that improve their survival. Neuroreport 26, 928–936.10.1097/WNR.0000000000000451Search in Google Scholar PubMed

Redzic, Z. (2011). Molecular biology of the blood-brain and the blood-cerebrospinal fluid barriers: similarities and differences. Fluids Barriers CNS 8, 3.10.1186/2045-8118-8-3Search in Google Scholar PubMed PubMed Central

Regalado-Santiago, C., Juarez-Aguilar, E., Olivares-Hernandez, J.D., and Tamariz, E. (2016). Mimicking neural stem cell niche by biocompatible substrates. Stem Cells Int. 2016, 1513285.10.1155/2016/1513285Search in Google Scholar PubMed PubMed Central

Ren, J., Zhang, Y., Cai, H., Ma, H., Zhao, D., Zhang, X., Li, Z., Wang, S., Wang, J., Liu, R., et al. (2014). RNAi targeting GPR4 influences HMEC-1 gene expression by microarray analysis. Int. J. Clin. Exp. Med. 7, 607–615.Search in Google Scholar

Rhett, J.M., Jourdan, J., and Gourdie, R.G. (2011). Connexin 43 connexon to gap junction transition is regulated by zonula occludens-1. Mol. Biol. Cell 22, 1516–1528.10.1091/mbc.e10-06-0548Search in Google Scholar

Rinaldi, F., Hartfield, E.M., Crompton, L.A., Badger, J.L., Glover, C.P., Kelly, C.M., Rosser, A.E., Uney, J.B., and Caldwell, M.A. (2014). Cross-regulation of Connexin43 and beta-catenin influences differentiation of human neural progenitor cells. Cell Death Dis. 5, e1017.10.1038/cddis.2013.546Search in Google Scholar PubMed PubMed Central

Rosell, A., Morancho, A., Navarro-Sobrino, M., Martínez-Saez, E., Hernández-Guillamon, M., Lope-Piedrafita, S., Barceló, V., Borrás, F., Penalba, A., García-Bonilla, L., et al. (2013). Factors secreted by endothelial progenitor cells enhance neurorepair responses after cerebral ischemia in mice. PLoS One 8, e73244.10.1371/journal.pone.0073244Search in Google Scholar PubMed PubMed Central

Ryu, J.R., Hong, C.J., Kim, J.Y., Kim, E.-K., Sun, W., and Yu, S.-W. (2016a). Control of adult neurogenesis by programmed cell death in the mammalian brain. Mol. Brain 9, 43.10.1186/s13041-016-0224-4Search in Google Scholar PubMed PubMed Central

Ryu, S., Lee, S.H., Kim, S.U., and Yoon, B.W. (2016b). Human neural stem cells promote proliferation of endogenous neural stem cells and enhance angiogenesis in ischemic rat brain. Neural Regen. Res. 11, 298–304.10.4103/1673-5374.177739Search in Google Scholar PubMed PubMed Central

Sa, J.V., Kleiderman, S., Brito, C., Sonnewald, U., Leist, M., Teixeira, A.P., and Alves, P.M. (2016). Quantification of metabolic rearrangements during neural stem cells differentiation into astrocytes by metabolic flux analysis. Neurochem. Res. DOI: 10. 1007/ s11064-016-1907-z (In press).Search in Google Scholar

Salmina, A.B., Morgun, A.V., Kuvacheva, N.V., Lopatina, O.L., Komleva, Y.K., Malinovskaya, N.A., and Pozhilenkova, E.A. (2014). Establishment of neurogenic microenvironment in the neurovascular unit: the connexin 43 story. Rev. Neurosci. 25, 97–111.10.1515/revneuro-2013-0044Search in Google Scholar

Salmina, A.B., Kuvacheva, N.V., Morgun, A.V., Komleva, Y.K., Pozhilenkova, E.A., Lopatina, O.L., Gorina, Y.V., Taranushenko, T.E., and Petrova, L.L. (2015). Glycolysis-mediated control of blood-brain barrier development and function. Int. J. Biochem. Cell Biol. 64, 174–184.10.1016/j.biocel.2015.04.005Search in Google Scholar

Sawada, M., Matsumoto, M., and Sawamoto, K. (2014). Vascular regulation of adult neurogenesis under physiological and pathological conditions. Front. Neurosci. 8, 53.10.3389/fnins.2014.00053Search in Google Scholar

Schneider, J.W., Goetsch, S.C., Leng, X., Ludwig, S.M., Russell, J.L., Yang, C.-P., and Zhang, Q.-J. (2012). Coupling hippocampal neurogenesis to brain ph through proneurogenic small molecules that regulate proton sensing G protein-coupled receptors. ACS Chem. Neurosci. 3, 557–568.10.1021/cn300025aSearch in Google Scholar

Schoors, S., Bruning, U., Missiaen, R., Queiroz, K.C., Borgers, G., Elia, I., Zecchin, A., Cantelmo, A.R., Christen, S., Goveia, J., et al. (2015). Fatty acid carbon is essential for dNTP synthesis in endothelial cells. Nature 520, 192–197.10.1038/nature14362Search in Google Scholar

Schultheiss, C., Abe, P., Hoffmann, F., Mueller, W., Kreuder, A.E., Schutz, D., Haege, S., Redecker, C., Keiner, S., Kannan, S., et al. (2013). CXCR4 prevents dispersion of granule neuron precursors in the adult dentate gyrus. Hippocampus 23, 1345–1358.10.1002/hipo.22180Search in Google Scholar

Seabrook, T.J., Littlewood-Evans, A., Brinkmann, V., Pöllinger, B., Schnell, C., and Hiestand, P.C. (2010). Angiogenesis is present in experimental autoimmune encephalomyelitis and pro-angiogenic factors are increased in multiple sclerosis lesions. J. Neuroinflamm. 7, 95–95.10.1186/1742-2094-7-95Search in Google Scholar

Shao, X., Gao, D., Chen, Y., Jin, F., Hu, G., Jiang, Y., and Liu, H. (2016). Development of a blood-brain barrier model in a membrane-based microchip for characterization of drug permeability and cytotoxicity for drug screening. Anal Chim. Acta 934, 186–193.10.1016/j.aca.2016.06.028Search in Google Scholar

Sharma, H.S., Cervos-Navarro, J., and Dey, P.K. (1991). Increased blood-brain barrier permeability following acute short-term swimming exercise in conscious normotensive young rats. Neurosci. Res. 10, 211–221.10.1016/0168-0102(91)90058-7Search in Google Scholar

Shin, Y., Yang, K., Han, S., Park, H.J., Seok Heo, Y., Cho, S.W., and Chung, S. (2014). Reconstituting vascular microenvironment of neural stem cell niche in three-dimensional extracellular matrix. Adv. Healthc. Mater. 3, 1457–1464.10.1002/adhm.201300569Search in Google Scholar PubMed

Shiraishi, T., Verdone, J.E., Huang, J., Kahlert, U.D., Hernandez, J.R., Torga, G., Zarif, J.C., Epstein, T., Gatenby, R., McCartney, A., et al. (2015). Glycolysis is the primary bioenergetic pathway for cell motility and cytoskeletal remodeling in human prostate and breast cancer cells. Oncotarget 6, 130–143.10.18632/oncotarget.2766Search in Google Scholar PubMed PubMed Central

Soares, R.V., Do, T.M., Mabondzo, A., Pons, G., and Chhun, S. (2016). Ontogeny of ABC and SLC transporters in the microvessels of developing rat brain. Fundam. Clin. Pharmacol. 30, 107–116.10.1111/fcp.12175Search in Google Scholar PubMed

Sonveaux, P., Copetti, T., De Saedeleer, C.J., Végran, F., Verrax, J., Kennedy, K.M., Moon, E.J., Dhup, S., Danhier, P., Frérart, F., et al. (2012). Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis. PLoS One 7, e33418.10.1371/journal.pone.0033418Search in Google Scholar PubMed PubMed Central

Stamatovic, S.M., Keep, R.F., and Andjelkovic, A.V. (2008). Brain endothelial cell-cell junctions: how to “open” the blood brain barrier. Curr. Neuropharmacol. 6, 179–192.10.2174/157015908785777210Search in Google Scholar PubMed PubMed Central

Stapor, P., Wang, X., Goveia, J., Moens, S., and Carmeliet, P. (2014). Angiogenesis revisited – role and therapeutic potential of targeting endothelial metabolism. J. Cell Sci. 127, 4331–4341.10.1242/jcs.153908Search in Google Scholar PubMed

Stolp, H.B. and Molnár, Z. (2015). Neurogenic niches in the brain: help and hindrance of the barrier systems. Front. Neurosci. 9, 20.10.3389/fnins.2015.00020Search in Google Scholar PubMed PubMed Central

Sulejczak, D., Chrapusta, S.J., Kozlowski, W., and Frontczak-Baniewicz, M. (2016). Surgical injury-induced early neocortical microvascular changes and characteristics of the cells populating the peri-lesion zone. Acta Neurobiol. Exp. (Warsaw) 76, 125–141.10.21307/ane-2017-012Search in Google Scholar PubMed

Tajerian, M. and Clark, J.D. (2015). Novel cytogenic and neurovascular niches due to blood-brain barrier compromise in the chronic pain brain. Mol. Pain 11, 63.10.1186/s12990-015-0066-6Search in Google Scholar PubMed PubMed Central

Tavazoie, M., Van der Veken, L., Silva-Vargas, V., Louissaint, M., Colonna, L., Zaidi, B., Garcia-Verdugo, J.M., and Doetsch, F. (2008). A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279–288.10.1016/j.stem.2008.07.025Search in Google Scholar PubMed PubMed Central

Taylor, C.J., Nicola, P.A., Wang, S., Barrand, M.A., and Hladky, S.B. (2006). Transporters involved in regulation of intracellular pH in primary cultured rat brain endothelial cells. J. Physiol. 576, 769–785.10.1113/jphysiol.2006.117374Search in Google Scholar PubMed PubMed Central

Tsukamoto, T. and Nigam, S.K. (1997). Tight junction proteins form large complexes and associate with the cytoskeleton in an ATP depletion model for reversible junction assembly. J. Biol. Chem. 272, 16133–16139.10.1074/jbc.272.26.16133Search in Google Scholar PubMed

Uhernik, A.L., Tucker, C., and Smith, J.P. (2011). Control of MCT1 function in cerebrovascular endothelial cells by intracellular pH. Brain Res. 1376, 10–22.10.1016/j.brainres.2010.12.060Search in Google Scholar PubMed

van Praag, H., Shubert, T., Zhao, C., and Gage, F.H. (2005). Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25, 8680–8685.10.1523/JNEUROSCI.1731-05.2005Search in Google Scholar PubMed PubMed Central

Vazana, U., Veksler, R., Pell, G.S., Prager, O., Fassler, M., Chassidim, Y., Roth, Y., Shahar, H., Zangen, A., Raccah, R., et al. (2016). Glutamate-mediated blood-brain barrier opening: implications for neuroprotection and drug delivery. J. Neurosci. 36, 7727–7739.10.1523/JNEUROSCI.0587-16.2016Search in Google Scholar PubMed PubMed Central

Vegran, F., Boidot, R., Michiels, C., Sonveaux, P., and Feron, O. (2011). Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-κB/IL-8 pathway that drives tumor angiogenesis. Cancer Res. 71, 2550–2560.10.1158/0008-5472.CAN-10-2828Search in Google Scholar PubMed

Wanet, A., Arnould, T., Najimi, M., and Renard, P. (2015). Connecting mitochondria, metabolism, and stem cell fate. Stem Cells Dev. 24, 1957–1971.10.1089/scd.2015.0117Search in Google Scholar PubMed PubMed Central

Wang, H.H., Su, C.H., Wu, Y.J., Li, J.Y., Tseng, Y.M., Lin, Y.C., Hsieh, C.L., Tsai, C.H., and Yeh, H.I. (2013). Reduction of connexin43 in human endothelial progenitor cells impairs the angiogenic potential. Angiogenesis 16, 553–560.10.1007/s10456-013-9335-zSearch in Google Scholar PubMed

Wang, L.-L., Chen, D., Lee, J., Gu, X., Alaaeddine, G., Li, J., Wei, L., and Yu, S.P. (2014). Mobilization of endogenous bone marrow derived endothelial progenitor cells and therapeutic potential of parathyroid hormone after ischemic stroke in mice. PLoS One 9, e87284.10.1371/journal.pone.0087284Search in Google Scholar PubMed PubMed Central

Wang, Q., Yang, L., and Wang, Y. (2015). Enhanced differentiation of neural stem cells to neurons and promotion of neurite outgrowth by oxygen-glucose deprivation. Int. J. Dev. Neurosci. 43, 50–57.10.1016/j.ijdevneu.2015.04.009Search in Google Scholar PubMed

Wang, J., Chen, Y., Yang, Y., Xiao, X., Chen, S., Zhang, C., Jacobs, B., Zhao, B., and Bihl, J. (2016). Endothelial progenitor cells and neural progenitor cells synergistically protect cerebral endothelial cells from Hypoxia/reoxygenation-induced injury via activating the PI3K/Akt pathway. Mol. Brain 9, 12.10.1186/s13041-016-0193-7Search in Google Scholar PubMed PubMed Central

Watanabe, K., Nakamura, M., Okano, H., and Toyama, Y. (2007). Establishment of three-dimensional culture of neural stem/progenitor cells in collagen type-1 Gel. Restor. Neurol. Neurosci. 25, 109–117.Search in Google Scholar

Watters, A.K., Rom, S., Hill, J.D., Dematatis, M.K., Zhou, Y., Merkel, S.F., Andrews, A.M., Cena, J., Potula, R., Skuba, A., et al. (2015). Identification and dynamic regulation of tight junction protein expression in human neural stem cells. Stem Cells Dev 24, 1377–1389.10.1089/scd.2014.0497Search in Google Scholar

Weidenfeller, C., Svendsen, C.N., and Shusta, E.V. (2007). Differentiating embryonic neural progenitor cells induce blood-brain barrier properties. J. Neurochem. 101, 555–565.10.1111/j.1471-4159.2006.04394.xSearch in Google Scholar

Willis, C.L. (2011). Glia-induced reversible disruption of blood-brain barrier integrity and neuropathological response of the neurovascular unit. Toxicol. Pathol. 39, 172–185.10.1177/0192623310385830Search in Google Scholar

Xiong, Y., Mahmood, A., and Chopp, M. (2010). Angiogenesis, neurogenesis and brain recovery of function following injury. Curr. Opin. Investig. Drugs (London) 11, 298–308.Search in Google Scholar

Young, S.Z., Taylor, M.M., and Bordey, A. (2011). Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur. J. Neurosci. 33, 1123–1132.10.1111/j.1460-9568.2011.07611.xSearch in Google Scholar

Yuan, T.F., Liang, Y.X., Tay, D., So, K.F., and Ellis-Behnke, R. (2015). Specialized vasculature in the rostral migratory stream as a neurogenic niche and scaffold for neuroblast migration. Cell Transplant 24, 377–390.10.3727/096368915X686878Search in Google Scholar

Zhang, J. and Jiao, J. (2015). Molecular biomarkers for embryonic and adult neural stem cell and neurogenesis. BioMed Res. Int. 2015, 727542.10.1155/2015/727542Search in Google Scholar

Zhang, K., Zhou, Y., Zhao, T., Wu, L., Huang, X., Wu, K., Xu, L., Li, D., Liu, S., Zhao, Y., et al. (2015). Reduced cerebral oxygen content in the DG and SVZ in situ promotes neurogenesis in the adult rat brain in vivo. PLoS One 10, e0140035.10.1371/journal.pone.0140035Search in Google Scholar

Zhu, L.L., Wu, L.Y., Yew, D.T., and Fan, M. (2005). Effects of hypoxia on the proliferation and differentiation of NSCs. Mol. Neurobiol. 31, 231–242.10.1385/MN:31:1-3:231Search in Google Scholar

Received: 2016-10-26
Accepted: 2016-12-23
Published Online: 2017-2-14
Published in Print: 2017-5-24

©2017 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 26.4.2024 from https://www.degruyter.com/document/doi/10.1515/revneuro-2016-0071/html
Scroll to top button