Gene regulatory network analysis reveals differences in site-specific cell fate determination in mammalian brain

Frontiers in Cellular Neuroscience

Volumn 8, Issue DEC, 2014, Pages

  Ertaylan, Gökhan ^a   Okawa, Satoshi ^a   Schwamborn, Jens C ^a   del Sol, Antonio ^a  

^a UNIVERSITY OF LUXEMBOURG   (Luxembourg)

Author keywords

Differentiation; Gene regulatory network; Neural stem cells; Neurogenesis; NSC; SGZ; SVZ

Indexed keywords

CELL NUCLEUS RECEPTOR; CELL SURFACE RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; VASCULOTROPIN;

ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CELL FATE; CELL TYPE; CINGULATE GYRUS; DATA ANALYSIS; DEGENERATIVE DISEASE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE INTERACTION; GENE ONTOLOGY; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HYBRIDIZATION; IN SITU HYBRIDIZATION; MALE; MICROARRAY HYBRIDIZATION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE POTENTIAL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; REGULATORY MECHANISM; SOMATOSENSORY CORTEX; SUBGRANULAR ZONE; SUBVENTRICULAR ZONE; THALAMUS; UPREGULATION;

EID: 84919427495     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00437     Document Type: Article

References (75)

1. Ables, J. L., Decarolis, N. A., Johnson, M. A., Rivera, P. D., Gao, Z., Cooper, D. C., et al. (2010). Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J. Neurosci. 30, 10484-10492. doi: 10.1523/JNEUROSCI.4721-09.2010
2. Ahn, S., and Joyner, A. L. (2005). In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437, 894-897. doi: 10.1038/nature03994
3. Altman, J., and Das, G. D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319-335. doi: 10.1002/cne.901240303
4. Alvarez-Buylla, A., Garcia-Verdugo, J. M., and Tramontin, A. D. (2001). A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2, 287-293. doi: 10.1038/35067582
5. Andreu-Agullo, C., Maurin, T., Thompson, C. B., and Lai, E. C. (2011). Ars2 maintains neural stem-cell identity through direct transcriptional activation of Sox2. Nature 481, 195-198. doi: 10.1038/nature10712
6. Berriz, G. F., Beaver, J. E., Cenik, C., Tasan, M., and Roth, F. P. (2009). Next generation software for functional trend analysis. J. Gerontol. 25, 3043-3044. doi: 10.1093/bioinformatics/btp498
7. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on varianceand bias. Bioinformatics 19, 185-193. doi: 10.1093/bioinformatics/19.2.185
8. Boulay, G., Dubuissez, M., Van Rechem, C., Forget, A., Helin, K., Ayrault, O., et al. (2012). Hypermethylated in Cancer 1 (HIC1) Recruits Polycomb Repressive Complex 2 (PRC2) to a subset of its target genes through interaction with Human Polycomb-like (hPCL) proteins. J. Biol. Chem. 287, 10509-10524. doi: 10.1074/jbc.M111.320234
9. Brill, M. S., Ninkovic, J., Winpenny, E., Hodge, R. D., Ozen, I., Yang, R., et al. (2009). Adult generation of glutamatergic olfactory bulb interneurons. Nat. Neurosci. 12, 1524-1533. doi: 10.1038/nn.2416
10. Brill, M. S., Snapyan, M., Wohlfrom, H., Ninkovic, J., Jawerka, M., Mastick, G. S., et al. (2008). A Dlx2- and Pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J. Neurosci. 28, 6439-6452. doi: 10.1523/JNEUROSCI.0700-08.2008
11. Cameron, H. A., Woolley, C. S., McEwen, B. S., and Gould, E. (1993). Differ- entiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56, 337-344. doi: 10.1016/0306-4522(93)90335-D
12. Christen, T., Bouzat, P., Pannetier, N., Coquery, N., Moisan, A., Lemasson, B., et al. (2014). Tissue oxygen saturation mapping with magnetic resonance imaging. J. Cereb. Blood Flow Metab. 34, 1550-1557. doi: 10.1038/jcbfm.2014.116
13. Crespo, I., and Del Sol, A. (2013). A general strategy for cellular reprogramming: the importance of transcription factor cross-repression. Stem Cells 31, 2127-2135. doi: 10.1002/stem.1473
14. Crespo, I., Krishna, A., Le Béchec, A., and del Sol, A. (2013). Predicting missing expression values in gene regulatory networks using a discrete logic modeling optimization guided by network stable states. Nucleic Acids Res. 41:e8. doi: 10.1093/nar/gks785
15. Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., and Malenka, RC. (2004). Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42, 535-552. doi: 10.1016/S0896-6273(04)00266-1
16. 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
17. Doetsch, F., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1997). Cellular composition and three-dimensional organization of the sub- ventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046-5061.
18. Edgar, R., Domrachev, M., and Lash, A. E. (2002). Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210. doi: 10.1093/nar/30.1.207
19. Engelen, E., Akinci, U., Bryne, J. C., Hou, J., Gontan, C., Moen, M., et al. (2011). Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat. Genet. 43, 607-611. doi: 10.1038/ng.825
20. Fournier, N. M., and Duman, R. S. (2012). Role of vascular endothelial growth factor in adult hippocampal neurogenesis: implications for the pathophysiology and treatment of depression. Behav. Brain Res. 227, 440-449. doi: 10.1016/j.bbr.2011.04.022
21. Fukuda, S., Kato, F., Tozuka, Y., Yamaguchi, M., Miyamoto, Y., and Hisatsune, T. (2003). Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J. Neurosci. 23, 9357-9366.
22. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438. doi: 10.1126/science.287.5457.1433
23. Gage, F. H., Kempermann, G., Palmer, T. D., Peterson, D. A., and Ray, J. (1998). Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 36, 249-266.
24. Gao, Z., Ure, K., Ables, J. L., Lagace, D. C., Nave, K. A., Goebbels, S., et al. (2009). Neurod1 is essential for the survival and maturation of adult-born neurons. Nat. Neurosci. 12, 1090-1092. doi: 10.1038/nn.2385
25. Gritti, A., Frolichsthal-Schoeller, P., Galli, R., Parati, E. A., Cova, L., Pagano, S. F., et al. (1999). Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J. Neurosci. 19, 3287-3297.
26. Hamson, D. K., Wainwright, S. R., Taylor, J. R., Jones, B. A., Watson, N. V., and Galea, L. A. M. (2013). Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats. Endocrinology 154, 3294-3304. doi: 10.1210/en.2013-1129
27. Hsieh, J. (2012). Orchestrating transcriptional control of adult neurogenesis. Genes Dev. 26, 1010-1021. doi: 10.1101/gad.187336.112
28. Huang, S., Guo, Y.-P., May, G., and Enver, T. (2006). Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev. Biol. 305, 695-713. doi: 10.1016/j.ydbio.2007.02.036
29. Ikeya, M., Lee, S. M., Johnson, J. E., McMahon, A. P., and Takada, S. (1997). Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966-970. doi: 10.1038/40146
30. Jin, K., Zhu, Y., Sun, Y., Mao, X. O., Xie, L., and Greenberg, D. A. (2002). Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 99, 11946-11950. doi: 10.1073/pnas.182296499
31. Kalyani, A., Hobson, K., and Rao, M. S. (1997). Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev. Biol. 186, 202-223. doi: 10.1006/dbio.1997.8592
32. Kaneko, S., Li, G., Son, J., Xu, C.-F., Margueron, R., Neubert, T. A., et al. (2010). Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev. 24, 2615-2620. doi: 10.1101/gad.1983810
33. Kempermann, G., Jessberger, S., Steiner, B., and Kronenberg, G. (2004). Milestones of neuronal development in the adult hippocam- pus. Trends Neurosci. 27, 447-452. doi: 10.1016/j.tins.2004.05.013
34. Klempin, F., Marr, R. A., and Peterson, D. A. (2012). Modification of Pax6 and Olig2 expression in adult hippocampal neurogenesis selectively induces stem cell fate and alters both neuronal and glial populations. Stem Cells 30, 500-509. doi: 10.1002/stem.1005
35. Kohwi, M., Osumi, N., Rubenstein, J. L. R., and Alvarez-Buylla, A. (2005). Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J. Neurosci. 25, 6997-7003. doi: 10.1523/JNEUROSCI.1435-05.2005
36. Kriegstein, A., and Alvarez-Buylla, A. (2009). The glial nature of em- bryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184. doi: 10.1146/annurev.neuro.051508.135600
37. Léotoing, L., Manin, M., Monté, D., Baron, S., Communal, Y., Lours, C., et al. (2007). Crosstalk between androgen receptor and epidermal growth factor receptor-signalling pathways: a molecular switch for epithelial cell differentiation. J. Mol. Endocrinol. 39, 151-162. doi: 10.1677/JME-07-0021
38. Lie, D. C., Colamarino, S. A., Song, H. J., Desire, L., Mira, H., Consiglio, A., et al. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375. doi: 10.1038/nature04108
39. Lledo, P. M., Merkle, F. T., and Alvarez-Buylla, A. (2008). Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 31, 392-400. doi: 10.1016/j.tins.2008.05.006
40. Lois, C., and Alvarez-Buylla, A. (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. U.S.A. 90, 2074-2077. doi: 10.1073/pnas.90.5.2074
41. Lois, C., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1996). Chain migration of neuronal precursors. Science271, 978-981. doi: 10.1126/science.271.5251.978
42. Ma, D. K., Jang, M. H., Guo, J. U., Kitabatake, Y., Chang, M. L., Pow-Anpongkul, N., et al. (2009). Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077. doi: 10.1126/science.1166859
43. Ma, D. K., Ming, G. L., and Song, H. (2005). Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr. Opin. Neurobiol. 15, 514-520. doi: 10.1016/j.conb.2005.08.003
44. Mackenzie, F., and Ruhrberg, C. (2012). Diverse roles for VEGF-A in the nervous system. Development 139, 1371-1380. doi: 10.1242/dev.072348
45. Mazumdar, J., O’Brien, W. T., Johnson, R. S., LaManna, J. C., Chavez, J. C., Klein, P. S., et al. (2010). O2 regulates stem cells through Wnt/β-catenin signalling. Nat. Cell Biol. 12, 1007-1013. doi: 10.1038/ncb2102
46. Merkle, F. T., Mirzadeh, Z., and Alvarez-Buylla, A. (2007). Mosaic orga- nization of neural stem cells in the adult brain. Science 317, 381-384. doi: 10.1126/science.1144914
47. Merkle, F. T., Tramontin, A. D., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2004). Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl. Acad. Sci. U.S.A. 101, 17528-17532. doi: 10.1073/pnas.0407893101
48. Miller, J. A., Nathanson, J., Franjic, D., Shim, S., Dalley, R. A., Shapouri, S., et al. (2013). Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. Development 140, 4633-4644. doi: 10.1242/dev.097212
49. Mira, H., Andreu, Z., Suh, H., Lie, D. C., Jessberger, S., Consiglio, A., et al. (2010). Signaling through BMPR-IA regulates quies- cence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7, 78-89. doi: 10.1016/j.stem.2010.04.016
50. Miyata, T., Maeda, T., and Lee, J. E. (1999). NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev. 13, 1647-1652. doi: 10.1101/gad.13.13.1647
51. Morrens, J., Van Den Broeck, W., and Kempermann, G. (2012). Glial cells in adult neurogenesis. Glia 60, 159-174. doi: 10.1002/glia.21247
52. Nomura, T., Goritz, C., Catchpole, T., Henkemeyer, M., and Frisen, J. (2010). EphB signaling controls lineage plasticity of adult neural stem cell niche cells. Cell Stem Cell 7, 730-743. doi: 10.1016/j.stem.2010.11.009
53. Palmer, T. D., Willhoite, A. R., and Gage, F. H. (2000). Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479-494. doi: 10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3
54. Pastrana, E., Cheng, L.-C., and Doetsch, F. (2009). Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc. Natl. Acad. Sci. U.S.A. 106, 6387-6392. doi: 10.1073/pnas.0810407106
55. Pereira, J. D., Sansom, S. N., Smith, J., Dobenecker, M.-W., Tarakhovsky, A., and Livesey, F. J. (2010). Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 107, 15957-15962. doi: 10.1073/pnas.1002530107
56. Raballo, R., Rhee, J., Lyn-Cook, R., Leckman, J. F., Schwartz, M. L., and Vaccarino, F. M. (2000). Basic fibroblast growth factor (FGF-2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J. Neurosci. 20, 5012-5023.
57. Ramos, A. D., Diaz, A., Nellore, A., Delgado, R. N., Park, K.-Y., Gonzales-Roybal, G., et al. (2013). Integration of genome-wide approaches identifies lncrnas of adult neural stem cells and their progeny in vivo. Cell Stem Cell 12, 616-628. doi: 10.1016/j.stem.2013.03.003
58. Rao, M. S. (1999). Multipotent and restricted precursors in the central nervous system. Anat. Rec. 257, 137-148.
59. Rao, M. S., and Mayer-Proschel, M. (1997). Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev. Biol. 188, 48-63. doi: 10.1006/dbio.1997.8597
60. Roeder, I., and Glauche, I. (2006). Towards an understanding of lineage specification in hematopoietic stem cells: a mathematical model for the interaction of transcription factors GATA-1 and PU.1. J. Theor. Biol. 241, 852-865. doi: 10.1016/j.jtbi.2006.01.021
61. Seri, B., Garciìa-Verdugo, J. M., McEwen, B. S., and Alvarez-Buylla, A. (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21, 7153-7160.
62. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504. doi: 10.1101/gr.1239303
63. Song, H., Stevens, C. F., and Gage, F. H. (2002). Astroglia induce neuro- genesis from adult neural stem cells.Nature 417, 39-44. doi: 10.1038/417039a
64. Spassky, N., Merkle, F. T., Flames, N., Tramontin, A. D., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J. Neurosci. 25, 10-18. doi: 10.1523/JNEUROSCI.1108-04.2005
65. Sugino, K., Hempel, C. M., Miller, M. N., Hattox, A. M., Shapiro, P., Wu, C., et al. (2006). Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 9, 99-107. doi: 10.1038/nn1618
66. Suh, Y., Obernier, K., Hölzl-Wenig, G., Mandl, C., Herrmann, A., Wörner, K., et al. (2009). Interaction between DLX2 and EGFR regulates proliferation and neurogenesis of SVZ precursors. Mol. Cell. Neurosci. 42, 308-314. doi: 10.1016/j.mcn.2009.08.003
67. Tchorz, J. S., Tome, M., Cloëtta, D., Sivasankaran, B., Grzmil, M., Huber, R. M., et al. (2012). Constitutive Notch2 signaling in neural stem cells promotes tumorigenic features and astroglial lineage entry. Cell Death Dis. 3, e325. doi: 10.1038/cddis.2012.65
68. Temple, S. (2001). The development of neural stem cells. Nature 414, 112-117. doi: 10.1038/35102174
69. Tozuka, Y., Fukuda, S., Namba, T., Seki, T., and Hisatsune, T. (2005). GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47, 803-815. doi: 10.1016/j.neuron.2005.08.023
70. Tropepe, V., Sibilia, M., Ciruna, B. G., Rossant, J., Wagner, E. F., and van der Kooy, D. (1999). Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev. Biol. 208, 166-188. doi: 10.1006/dbio.1998.9192
71. Valenta, T., Lukas, J., Doubravska, L., Fafilek, B., and Korinek, V. (2006). HIC1 attenuates Wnt signaling by recruitment of TCF-4 and β-catenin to the nuclear bodies. EMBO J. 25, 2326-2337. doi: 10.1038/sj.emboj.7601147
72. Warner-Schmidt, J. L., and Duman, R. S. (2007). VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc. Natl. Acad. Sci. U.S.A. 104, 4647-4652. doi: 10.1073/pnas.0610282104
73. Wechsler-Reya, R. J., and Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog. Neuron 22, 103-114. doi: 10.1016/S0896-6273(00)80682-0
74. Zhang, X., Yalcin, S., Lee, D.-F., Yeh, T.-Y. J., Lee, S.-M., Su, J., et al. (2011). FOXO1 is an essential regulator of pluripotency in human embryonic stem cells. Nat. Cell Biol. 13, 1092-1099. doi: 10.1038/ncb2293
75. Zinovyev, A., Viara, E., Calzone, L., and Barillot, E. (2008). BiNoM: a Cytoscape plugin for manipulating and analyzing biological networks. J. Gerontol. 24, 876-877. doi: 10.1093/bioinformatics/btm553