Neirinckx, Virginie ; Université de Liège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Gothot, André ; Université de Liège > Département des sciences biomédicales et précliniques > Biologie de la coagulation et de l'hémostase
Wislet, Sabine ; Université de Liège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Rogister, Bernard ; Université de Liège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Language :
English
Title :
Are neural crest stem cells the missing link between hematopoietic and neurogenic niches?
Publication date :
June 2015
Journal title :
Frontiers in Cellular Neuroscience
eISSN :
1662-5102
Publisher :
Frontiers Research Foundation, Lausanne, Switzerland
Achilleos, A., and Trainor, P. A. (2012). Neural crest stem cells: discovery, properties and potential for therapy. Cell Res. 22, 288-304. doi: 10.1038/cr.2012.11
Aguirre, A., Rubio, M. E., and Gallo, V. (2010). Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467, 323-327. doi: 10.1038/nature09347
Anderson, D. J. (1994). Stem cells and transcription factors in the development of the mammalian neural crest. FASEB J. 8, 707-713.
Anthony, B. A., and Link, D. C. (2014). Regulation of hematopoietic stem cells by bone marrow stromal cells. Trends Immunol. 35, 32-37. doi: 10.1016/j.it.2013.10.002
Ara, T., Tokoyoda, K., Sugiyama, T., Egawa, T., Kawabata, K., and Nagasawa, T. (2003). Long-term hematopoietic stem cells require stromal cell-derived factor-1 for colonizing bone marrow during ontogeny. Immunity 19, 257-267. doi: 10.1016/S1074-7613(03)00201-2
Arai, F., Hirao, A., Ohmura, M., Sato, H., Matsuoka, S., Takubo, K., et al. (2004). Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118, 149-161. doi: 10.1016/j.cell.2004.07.004
Artavanis-Tsakonas, S., Rand, M. D., and Lake, R. J. (1999). Notch signaling: cell fate control and signal integration in development. Science 284, 770-776. doi: 10.1126/science.284.5415.770
Bagri, A., Gurney, T., He, X., Zou, Y. R., Littman, D. R., Tessier-Lavigne, M., et al. (2002). The chemokine SDF1 regulates migration of dentate granule cells. Development 129, 4249-4260.
Banisadr, G., Skrzydelski, D., Kitabgi, P., Rostene, W., and Parsadaniantz, S. M. (2003). Highly regionalized distribution of stromal cell-derived factor-1/CXCL12 in adult rat brain: constitutive expression in cholinergic, dopaminergic and vasopressinergic neurons. Eur. J. Neurosci. 18, 1593-1606. doi: 10.1046/j.1460-9568.2003.02893.x
Belmadani, A., Tran, P. B., Ren, D., Assimacopoulos, S., Grove, E. A., and Miller, R. J. (2005). The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J. Neurosci. 25, 3995-4003. doi: 10.1523/JNEUROSCI.4631-04.2005
Benton, J. L., Kery, R., Li, J., Noonin, C., Soderhall, I., and Beltz, B. S. (2014). Cells from the immune system generate adult-born neurons in crayfish. Dev. Cell 30, 322-333. doi: 10.1016/j.devcel.2014.06.016
Bigas, A., and Espinosa, L. (2012). Hematopoietic stem cells: to be or Notch to be. Blood 119, 3226-3235. doi: 10.1182/blood-2011-10-355826
Calvi, L. M., Adams, G. B., Weibrecht, K. W., Weber, J. M., Olson, D. P., Knight, M. C., et al. (2003). Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846. doi: 10.1038/nature02040
Caplan, A. I. (1991). Mesenchymal stem cells. J. Orthop. Res. 9, 641-650. doi: 10.1002/jor.1100090504
Chadwick, K., Wang, L., Li, L., Menendez, P., Murdoch, B., Rouleau, A., et al. (2003). Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102, 906-915. doi: 10.1182/blood-2003-03-0832
Chalazonitis, A., and Kessler, J. A. (2012). Pleiotropic effects of the bone morphogenetic proteins on development of the enteric nervous system. Dev. Neurobiol. 72, 843-856. doi: 10.1002/dneu.22002
Crisan, M., Yap, S., Casteilla, L., Chen, C. W., Corselli, M., Park, T. S., et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301-313. doi: 10.1016/j.stem.2008.07.003
Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716. doi: 10.1016/S0092-8674(00)80783-7
Durand, C., Robin, C., Bollerot, K., Baron, M. H., Ottersbach, K., and Dzierzak, E. (2007). Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells. Proc. Natl. Acad. Sci. U.S.A. 104, 20838-20843. doi: 10.1073/pnas.0706923105
Emerson, S. G. (2007). Thrombopoietin, HSCs, and the osteoblast niche: holding on loosely, but not letting G0. Cell Stem Cell1, 599-600. doi: 10.1016/j.stem.2007.11.010
Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., et al. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. doi: 10.1038/3305
Ernst, A., Alkass, K., Bernard, S., Salehpour, M., Perl, S., Tisdale, J., et al. (2014). Neurogenesis in the striatum of the adult human brain. Cell 156, 1072-1083. doi: 10.1016/j.cell.2014.01.044
Escot, S., Blavet, C., Hartle, S., Duband, J. L., and Fournier-Thibault, C. (2013). Misregulation of SDF1-CXCR4 signaling impairs early cardiac neural crest cell migration leading to conotruncal defects. Circ. Res. 113, 505-516. doi: 10.1161/CIRCRESAHA.113.301333
Frenette, P. S., Subbarao, S., Mazo, I. B., von Andrian, U. H., and Wagner, D. D. (1998). Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc. Natl. Acad. Sci. U.S.A. 95, 14423-14428. doi: 10.1073/pnas.95.24.14423
Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438. doi: 10.1126/science.287.5457.1433
Goffart, N., Kroonen, J., di Valentin, E., Dedobbeleer, M., Denne, A., Martinive, P., et al. (2015). Adult mouse subventricular zones stimulate glioblastoma stem cells specific invasion through CXCL12/CXCR4 signaling. Neurooncology 17, 81-94. doi: 10.1093/neuonc/nou144
Goffart, N., Kroonen, J., and Rogister, B. (2013). Glioblastoma-initiating cells: relationship with neural stem cells and the micro-environment. Cancers 5, 1049-1071. doi: 10.3390/cancers5031049
Goldman, D. C., Bailey, A. S., Pfaffle, D. L., Al Masri, A., Christian, J. L., and Fleming, W. H. (2009). BMP4 regulates the hematopoietic stem cell niche. Blood 114, 4393-4401. doi: 10.1182/blood-2009-02-206433
Greenbaum, A., Hsu, Y. M., Day, R. B., Schuettpelz, L. G., Christopher, M. J., Borgerding, J. N., et al. (2013). CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495, 227-230. doi: 10.1038/nature11926
Gross, R. E., Mehler, M. F., Mabie, P. C., Zang, Z., Santschi, L., and Kessler, J. A. (1996). Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17, 595-606. doi: 10.1016/S0896-6273(00)80193-2
Hansen, D. V., Lui, J. H., Parker, P. R., and Kriegstein, A. R. (2010). Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554-561. doi: 10.1038/nature08845
Hong, C. S., and Saint-Jeannet, J. P. (2005). Sox proteins and neural crest development. Semin. Cell Dev. Biol. 16, 694-703. doi: 10.1016/j.semcdb.2005.06.005
Isern, J., Garcia-Garcia, A., Martin, A. M., Arranz, L., Martin-Perez, D., Torroja, C., et al. (2014). The neural crest is a source of mesenchymal stem cells with specialized hematopoietic stem cell niche function. elife 3:e03696. doi: 10.7554/eLife.03696
Jiang, Y., Prosper, F., and Verfaillie, C. M. (2000). Opposing effects of engagement of integrins and stimulation of cytokine receptors on cell cycle progression of normal human hematopoietic progenitors. Blood 95, 846-854. doi: 10.1182/blood-2009-06-226373
Katayama, Y., Battista, M., Kao, W. M., Hidalgo, A., Peired, A. J., Thomas, S. A., et al. (2006). Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124, 407-421. doi: 10.1016/j.cell.2005.10.041
Khurana, S., Melacarne, A., Yadak, R., Schouteden, S., Notelaers, T., Pistoni, M., et al. (2014). SMAD signaling regulates CXCL12 expression in the bone marrow niche, affecting homing and mobilization of hematopoietic progenitors. Stem Cells 32, 3012-3022. doi: 10.1002/stem.1794
Kiel, M. J., and Morrison, S. J. (2008). Uncertainty in the niches that maintain haematopoietic stem cells. Nat. Rev. Immunol. 8, 290-301. doi: 10.1038/nri2279
Kiel, M. J., Radice, G. L., and Morrison, S. J. (2007). Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell 1, 204-217. doi: 10.1016/j.stem.2007.06.001
Kiel, M. J., Yilmaz, O. H., Iwashita, T., Yilmaz, O. H., Terhorst, C., and Morrison, S. J. (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109-1121. doi: 10.1016/j.cell.2005.05.026
Kipanyula, M. J., Kimaro, W. H., Yepnjio, F. N., Aldebasi, Y. H., Farahna, M., Nwabo Kamdje, A. H., et al. (2014). Signaling pathways bridging fate determination of neural crest cells to glial lineages in the developing peripheral nervous system. Cell. Signal. 26, 673-682. doi: 10.1016/j.cellsig.2013.12.007
Klingener, M., Chavali, M., Singh, J., McMillan, N., Coomes, A., Dempsey, P. J., et al. (2014). N-cadherin promotes recruitment and migration of neural progenitor cells from the SVZ neural stem cell niche into demyelinated lesions. J. Neurosci. 34, 9590-9606. doi: 10.1523/JNEUROSCI.3699-13.2014
Kokovay, E., Goderie, S., Wang, Y., Lotz, S., Lin, G., Sun, Y., et al. (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. doi: 10.1016/j.stem.2010.05.019
Kokovay, E., Wang, Y., Kusek, G., Wurster, R., Lederman, P., Lowry, N., et al. (2012). VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. Cell Stem Cell 11, 220-230. doi: 10.1016/j.stem.2012.06.016
Kolodziej, A., Schulz, S., Guyon, A., Wu, D. F., Pfeiffer, M., Odemis, V., et al. (2008). Tonic activation of CXC chemokine receptor 4 in immature granule cells supports neurogenesis in the adult dentate gyrus. J. Neurosci. 28, 4488-4500. doi: 10.1523/JNEUROSCI.4721-07.2008
Kosacka, J., Figiel, M., Engele, J., Hilbig, H., Majewski, M., and Spanel-Borowski, K. (2005). Angiopoietin-1 promotes neurite outgrowth from dorsal root ganglion cells positive for Tie-2 receptor. Cell Tissue Res. 320, 11-19. doi: 10.1007/s00441-004-1068-2
Kosacka, J., Nowicki, M., Kacza, J., Borlak, J., Engele, J., and Spanel-Borowski, K. (2006). Adipocyte-derived angiopoietin-1 supports neurite outgrowth and synaptogenesis of sensory neurons. J. Neurosci. Res. 83, 1160-1169. doi: 10.1002/jnr.20811
Le Belle, J. E., Orozco, N. M., Paucar, A. A., Saxe, J. P., Mottahedeh, J., Pyle, A. D., et al. (2011). Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell8, 59-71. doi: 10.1016/j.stem.2010.11.028
L'Episcopo, F., Tirolo, C., Testa, N., Caniglia, S., Morale, M. C., Deleidi, M., et al. (2012). Plasticity of subventricular zone neuroprogenitors in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) mouse model of Parkinson's disease involves cross talk between inflammatory and Wnt/beta-catenin signaling pathways: functional consequences for neuroprotection and repair. J. Neurosci. 32, 2062-2085. doi: 10.1523/JNEUROSCI.5259-11.2012
Li, W., Cogswell, C. A., and LoTurco, J. J. (1998). Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J. Neurosci. 18, 8853-8862.
Lim, D. A., Tramontin, A. D., Trevejo, J. M., Herrera, D. G., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2000). Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713-726. doi: 10.1016/S0896-6273(00)00148-3
Liu, X. S., Chopp, M., Zhang, R. L., Hozeska-Solgot, A., Gregg, S. C., Buller, B., et al. (2009). Angiopoietin 2 mediates the differentiation and migration of neural progenitor cells in the subventricular zone after stroke. J. Biol. Chem. 284, 22680-22689. doi: 10.1074/jbc.M109.006551
Ma, Q., Jones, D., Borghesani, P. R., Segal, R. A., Nagasawa, T., Kishimoto, T., et al. (1998). Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 95, 9448-9453. doi: 10.1073/pnas.95.16.9448
Mayor, R., and Theveneau, E. (2013). The neural crest. Development 140, 2247-2251. doi: 10.1242/dev.091751
McKeown, S. J., Wallace, A. S., and Anderson, R. B. (2013). Expression and function of cell adhesion molecules during neural crest migration. Dev. Biol. 373, 244-257. doi: 10.1016/j.ydbio.2012.10.028
Melo Rde, C., Longhini, A. L., Bigarella, C. L., Baratti, M. O., Traina, F., Favaro, P., et al. (2014). CXCR7 is highly expressed in acute lymphoblastic leukemia and potentiates CXCR4 response to CXCL12. PLoS ONE 9:e85926. doi: 10.1371/journal.pone.0085926
Mendez-Ferrer, S., Michurina, T. V., Ferraro, F., Mazloom, A. R., Macarthur, B. D., Lira, S. A., et al. (2010). Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466, 829-834. doi: 10.1038/nature09262
Milner, L. A., Kopan, R., Martin, D. I., and Bernstein, I. D. (1994). A human homologue of the Drosophila developmental gene, Notch, is expressed in CD34+ hematopoietic precursors. Blood 83, 2057-2062.
Morrison, S. J., Csete, M., Groves, A. K., Melega, W., Wold, B., and Anderson, D. J. (2000a). Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. J. Neurosci. 20, 7370-7376.
Morrison, S. J., Perez, S. E., Qiao, Z., Verdi, J. M., Hicks, C., Weinmaster, G., et al. (2000b). Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499-510. doi: 10.1016/S0092-8674(00)80860-0
Muguruma, Y., Yahata, T., Miyatake, H., Sato, T., Uno, T., Itoh, J., et al. (2006). Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment.Blood 107, 1878-1887. doi: 10.1182/blood-2005-06-2211
Nagoshi, N., Shibata, S., Kubota, Y., Nakamura, M., Nagai, Y., Satoh, E., et al. (2008). Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2, 392-403. doi: 10.1016/j.stem.2008.03.005
Nakagawa, S., and Takeichi, M. (1998). Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125, 2963-2971.
Nilsson, S. K., Johnston, H. M., and Coverdale, J. A. (2001). Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 97, 2293-2299. doi: 10.1182/blood.V97.8.2293
Noisa, P., Lund, C., Kanduri, K., Lund, R., Lahdesmaki, H., Lahesmaa, R., et al. (2014). Notch signaling regulates the differentiation of neural crest from human pluripotent stem cells. J. Cell Sci. 127, 2083-2094. doi: 10.1242/jcs.145755
Olesnicky Killian, E. C., Birkholz, D. A., and Artinger, K. B. (2009). A role for chemokine signaling in neural crest cell migration and craniofacial development. Dev. Biol. 333, 161-172. doi: 10.1016/j.ydbio.2009.06.031
Porlan, E., Marti-Prado, B., Morante-Redolat, J. M., Consiglio, A., Delgado, A. C., Kypta, R., et al. (2014). MT5-MMP regulates adult neural stem cell functional quiescence through the cleavage of N-cadherin. Nat. Cell Biol. 16, 629-638. doi: 10.1038/ncb2993
Radice, G. L., Rayburn, H., Matsunami, H., Knudsen, K. A., Takeichi, M., and Hynes, R. O. (1997). Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181, 64-78. doi: 10.1006/dbio.1996.8443
Raible, D. W. (2006). Development of the neural crest: achieving specificity in regulatory pathways. Curr. Opin. Cell Biol. 18, 698-703. doi: 10.1016/j.ceb.2006.09.003
Ramasamy, S. K., Kusumbe, A. P., and Adams, R. H. (2014). Regulation of tissue morphogenesis by endothelial cell-derived signals. Trends Cell Biol. 25, 148-157. doi: 10.1016/j.tcb.2014.11.007
Renstrom, J., Kroger, M., Peschel, C., and Oostendorp, R. A. (2010). How the niche regulates hematopoietic stem cells. Chem. Biol. Interact. 184, 7-15. doi: 10.1016/j.cbi.2009.11.012
Rezzoug, F., Seelan, R. S., Bhattacherjee, V., Greene, R. M., and Pisano, M. M. (2011). Chemokine-mediated migration of mesencephalic neural crest cells. Cytokine 56, 760-768. doi: 10.1016/j.cyto.2011.09.014
Rosa, A. I., Goncalves, J., Cortes, L., Bernardino, L., Malva, J. O., and Agasse, F. (2010). The angiogenic factor angiopoietin-1 is a proneurogenic peptide on subventricular zone stem/progenitor cells. J. Neurosci. 30, 4573-4584. doi: 10.1523/JNEUROSCI.5597-09.2010
Sacchetti, B., Funari, A., Michienzi, S., di Cesare, S., Piersanti, S., Saggio, I., et al. (2007). Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131, 324-336. doi: 10.1016/j.cell.2007.08.025
Sadlon, T. J., Lewis, I. D., and D'Andrea, R. J. (2004). BMP4: its role in development of the hematopoietic system and potential as a hematopoietic growth factor. Stem Cells 22, 457-474. doi: 10.1634/stemcells.22-4-457
Sailer, M. H., Hazel, T. G., Panchision, D. M., Hoeppner, D. J., Schwab, M. E., and McKay, R. D. (2005). BMP2 and FGF2 cooperate to induce neural-crest-like fates from fetal and adult CNS stem cells. J. Cell Sci. 118, 5849-5860. doi: 10.1242/jcs.02708
Sanchez-Martin, L., Sanchez-Mateos, P., and Cabanas, C. (2013). CXCR7 impact on CXCL12 biology and disease. Trends Mol. Med. 19, 12-22. doi: 10.1016/j.molmed.2012.10.004
Schofield, R. (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4, 7-25.
Schonemeier, B., Schulz, S., Hoellt, V., and Stumm, R. (2008). Enhanced expression of the CXCl12/SDF-1 chemokine receptor CXCR7 after cerebral ischemia in the rat brain. J. Neuroimmunol. 198, 39-45. doi: 10.1016/j.jneuroim.2008.04.010
Schwarting, G. A., Henion, T. R., Nugent, J. D., Caplan, B., and Tobet, S. (2006). Stromal cell-derived factor-1 (chemokine C-X-C motif ligand 12) and chemokine C-X-C motif receptor 4 are required for migration of gonadotropin-releasing hormone neurons to the forebrain. J. Neurosci. 26, 6834-6840. doi: 10.1523/JNEUROSCI.1728-06.2006
Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y., Abramova, N., et al. (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340. doi: 10.1126/science.1095505
Shen, Q., Wang, Y., Kokovay, E., Lin, G., Chuang, S. M., Goderie, S. K., et al. (2008). Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3, 289-300. doi: 10.1016/j.stem.2008.07.026
Shou, J., Rim, P. C., and Calof, A. L. (1999). BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nat. Neurosci. 2, 339-345. doi: 10.1038/7251
Silva-Vargas, V., Crouch, E. E., and Doetsch, F. (2013). Adult neural stem cells and their niche: a dynamic duo during homeostasis, regeneration, and aging. Curr. Opin. Neurobiol. 23, 935-942. doi: 10.1016/j.conb.2013.09.004
Simmons, P. J., Masinovsky, B., Longenecker, B. M., Berenson, R., Torok-Storb, B., and Gallatin, W. M. (1992). Vascular cell adhesion molecule-1 expressed by bone marrow stromal cells mediates the binding of hematopoietic progenitor cells. Blood80, 388-395.
Stier, S., Ko, Y., Forkert, R., Lutz, C., Neuhaus, T., Grunewald, E., et al. (2005). Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J. Exp. Med. 201, 1781-1791. doi: 10.1084/jem.20041992
Stumm, R. K., Zhou, C., Ara, T., Lazarini, F., Dubois-Dalcq, M., Nagasawa, T., et al. (2003). CXCR4 regulates interneuron migration in the developing neocortex. J. Neurosci. 23, 5123-5130.
Sugiyama, T., Kohara, H., Noda, M., and Nagasawa, T. (2006). Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25, 977-988. doi: 10.1016/j.immuni.2006.10.016
Suri, C., Jones, P. F., Patan, S., Bartunkova, S., Maisonpierre, P. C., Davis, S., et al. (1996). Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180. doi: 10.1016/S0092-8674(00)81813-9
Tabe, Y., and Konopleva, M. (2014). Advances in understanding the leukaemia microenvironment. Br. J. Haematol. 164, 767-778. doi: 10.1111/bjh.12725
Tamplin, O. J., Durand, E. M., Carr, L. A., Childs, S. J., Hagedorn, E. J., Li, P., et al. (2015). Hematopoietic stem cell arrival triggers dynamic remodeling of the perivascular niche. Cell 160, 241-252. doi: 10.1016/j.cell.2014.12.032
Tavazoie, M. L., van der Veken Silva-Vargas, V., Louissaint, M., Colonna, L., Zaidi, B., et al. (2008). A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279-288. doi: 10.1016/j.stem.2008.07.025
Testaz, S., Delannet, M., and Duband, J. (1999). Adhesion and migration of avian neural crest cells on fibronectin require the cooperating activities of multiple integrins of the (beta)1 and (beta)3 families. J. Cell Sci. 112(Pt 24), 4715-4728.
Torossian, F., Anginot, A., Chabanon, A., Clay, D., Guerton, B., Desterke, C., et al. (2014). CXCR7 participates in CXCL12-induced CD34+ cell cycling through beta-arrestin-dependent Akt activation. Blood 123, 191-202. doi: 10.1182/blood-2013-05-500496
Uccelli, A., Moretta, L., and Pistoia, V. (2008). Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 8, 726-736. doi: 10.1038/nri2395
Ulyanova, T., Scott, L. M., Priestley, G. V., Jiang, Y., Nakamoto, B., Koni, P. A., et al. (2005). VCAM-1 expression in adult hematopoietic and nonhematopoietic cells is controlled by tissue-inductive signals and reflects their developmental origin.Blood 106, 86-94. doi: 10.1182/blood-2004-09-3417
Unsicker, K., Huber, K., Schober, A., and Kalcheim, C. (2013). Resolved and open issues in chromaffin cell development.Mech. Dev. 130, 324-329. doi: 10.1016/j.mod.2012.11.004
Vilz, T. O., Moepps, B., Engele, J., Molly, S., Littman, D. R., and Schilling, K. (2005). The SDF-1/CXCR4 pathway and the development of the cerebellar system. Eur. J. Neurosci. 22, 1831-1839. doi: 10.1111/j.1460-9568.2005.04378.x
Wislet-Gendebien, S., Laudet, E., Neirinckx, V., Alix, P., Leprince, P., Glejzer, A., et al. (2012). Mesenchymal stem cells and neural crest stem cells from adult bone marrow: characterization of their surprising similarities and differences. Cell. Mol. Life Sci. 69, 2593-2608. doi: 10.1007/s00018-012-0937-1
Yagita, Y., Sakurai, T., Tanaka, H., Kitagawa, K., Colman, D. R., and Shan, W. (2009). N-cadherin mediates interaction between precursor cells in the subventricular zone and regulates further differentiation. J. Neurosci. Res. 87, 3331-3342. doi: 10.1002/jnr.22044
Yamazaki, S., Ema, H., Karlsson, G., Yamaguchi, T., Miyoshi, H., Shioda, S., et al. (2011). Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147, 1146-1158. doi: 10.1016/j.cell.2011.09.053
Young, S. Z., Taylor, M. M., and Bordey, A. (2011). Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur. J. Neurosci. 33, 1123-1132. doi: 10.1111/j.1460-9568.2011.07611.x
Zapata, A. G., Alfaro, D., and Garcia-Ceca, J. (2012). Biology of stem cells: the role of microenvironments. Adv. Exp. Med. Biol. 741, 135-151. doi: 10.1007/978-1-4614-2098-9_10
Zhang, J., Niu, C., Ye, L., Huang, H., He, X., Tong, W. G., et al. (2003). Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836-841. doi: 10.1038/nature02041
Zhang, J., Shemezis, J. R., McQuinn, E. R., Wang, J., Sverdlov, M., and Chenn, A. (2013). AKT activation by N-cadherin regulates beta-catenin signaling and neuronal differentiation during cortical development. Neural Dev. 8:7. doi: 10.1186/1749-8104-8-7
Zhang, J., Woodhead, G. J., Swaminathan, S. K., Noles, S. R., McQuinn, E. R., Pisarek, A. J., et al. (2010). Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Dev. Cell 18, 472-479. doi: 10.1016/j.devcel.2009.12.025
Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660. doi: 10.1016/j.cell.2008.01.033