Notch Exhibits Ligand Bias and Maneuvers Stage-Specific Steering of Neural Differentiation in Embryonic Stem Cells

REFERENCES

• Androutsellis-Theotokis, A., R. R. Leker, F. Soldner, D. J. Hoeppner, R. Ravin, S. W. Poser, M. A. Rueger, S. K. Bae, R. Kittappa, and R. D. McKay. 2006. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442:823–826.
   PubMed Web of Science ®Google Scholar
• Artavanis-Tsakonas, S., M. D. Rand, and R. J. Lake. 1999. Notch signaling: cell fate control and signal integration in development. Science 284:770–776.
   PubMed Web of Science ®Google Scholar
• Bhattacharya, S., A. Das, K. Mallya, and I. Ahmad. 2008. CNTF-mediated signaling regulates neuronal versus glial differentiation of retinal stem cells/progenitors by concentration-dependent recruitment of MAPK and Jak-STAT pathways in conjunction with Notch signaling. Stem Cells 26:2611–2624.
   PubMedGoogle Scholar
• Bonni, A., Y. Sun, M. Nadal-Vicens, A. Bhatt, D. Frank, I. Rozovsky, N. Stahl, G. Yancopoulos, and M. Greenberg. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278:477–483.
   PubMed Web of Science ®Google Scholar
• Chambers, I., D. Colby, M. Robertson, J. Nichols, S. Lee, S. Tweedie, and A. Smith. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643–655.
   PubMed Web of Science ®Google Scholar
• Ehebauer, M., P. Hayward, and A. Arias. 2006. Notch, a universal arbiter of cell fate decisions. Science 314:1414–1415.
   PubMed Web of Science ®Google Scholar
• Franklin, J. L., B. E. Berechid, F. B. Cutting, A. Presente, C. B. Chambers, D. R. Foltz, A. Ferreira, and J. S. Nye. 1999. Autonomous and non-autonomous regulation of mammalian neurite development by Notch1 and Delta1. Cell 9:1448–1457.
   Google Scholar
• Gaiano, N., and G. Fishell. 2002. The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25:471–490.
   PubMed Web of Science ®Google Scholar
• Grandbarbe, L., J. Bouissac, M. D. Rand, M. H. Angelis, S. Artavanis-Tsakonas, and E. Mohier. 2003. Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process. Development 130:1391–1402.
   PubMed Web of Science ®Google Scholar
• Gross, R. E., M. F. Mehler, P. C. Mabie, Z. Zang, L. Sanchi, and J. A. Kessler. 1996. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17:595–606.
   PubMed Web of Science ®Google Scholar
• Guo, M., L. Y. Jan, and Y. N. Jan. 1996. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17:27–41.
   PubMed Web of Science ®Google Scholar
• Hébert, J. M., M. Boyle, and G. R. Martin. 1991. mRNA localization studies suggest that murine FGF-5 plays a role in gastrulation. Development 112:407–415.
   PubMedGoogle Scholar
• Hellstrom, M., L. Phng, J. Hofmann, E. Wallgard, L. Coultas, P. Lindblom, J. Alva, A. Nilsson, L. Karlsson, N. Gaiano, K. Yoon, J. Rossant, M. Iruela-Arispe, M. Kalen, H. Gerhardt, and C. Betsholtz. 2007. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445:776–780.
   PubMed Web of Science ®Google Scholar
• Hooper, C., J. P. Chapple, S. Lovestone, and R. Killick. 2007. The Notch-1 intracellular domain is found in sub-nuclear bodies in SH-SY5Y neuroblastomas and in primary cortical neurons. Neurosci. Lett. 415:135–139.
   PubMed Web of Science ®Google Scholar
• Iso, T., L. Kedes, and Y. Hamamori. 2003. HES and HERP families: multiple effectors of the notch signaling pathway. J. Cell Physiol. 194:237–255.
   PubMed Web of Science ®Google Scholar
• Iso, T., Y. Hamamori, and L. Kedes. 2003. Notch signaling in vascular development. Arterioscler. Thromb. Vasc. Biol. 23:543–553.
   PubMed Web of Science ®Google Scholar
• Itoh, F., S. Itoh, M. J. Goumans, G. Valdimarsdottir, T. Iso, G. P. Dotto, Y. Hamamori, L. Kedes, M. Kato, and P. P. ten Dijke. 2004. Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J. 23:541–551.
   PubMed Web of Science ®Google Scholar
• Jaleco, A., H. Neves, E. Hooijberg, P. Gameiro, N. Clode, M. Haury, D. Henrique, and L. Parreira. 2001. Differential effects of Notch ligands Delta-1 and Jagged-1 in human lymphoid differentiation. J. Exp. Med. 194:991–1002.
   PubMed Web of Science ®Google Scholar
• Kamakura, S., K. Oishi, T. Yoshimatsu, M. Nakafuku, N. Masuyama, and Y. Gotoh. 2004. Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat. Cell Biol. 6:547–554.
   PubMed Web of Science ®Google Scholar
• Lenka, N., Z. J. Lu, P. Sasse, J. Hescheler, and B. K. Fleischmann. 2002. Quantitation and functional characterization of neural cells derived from ES cells using nestin enhancer-mediated targeting in vitro. J. Cell Sci. 115:1471–1485.
   PubMedGoogle Scholar
• Lenka, N., and S. K. Ramasamy. 2007. Neural induction from ES cells portrays default commitment but instructive maturation. PLoS One 2:e1349.
   PubMed Web of Science ®Google Scholar
• Louvi, A., and S. Artavanis-Tsakonas. 2006. Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 7:93–102.
   PubMed Web of Science ®Google Scholar
• Lowell, S., A. Benchoua, B. Heavey, and A. G. Smith. 2006. Notch promotes neural lineage entry by pluripotent embryonic stem cells. PLoS Biol. 4:e121.
   PubMedGoogle Scholar
• McCright, B., J. Lozier, and T. Gridley. 2002. A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 129:1075–1082.
   PubMed Web of Science ®Google Scholar
• Mitsui, K., Y. Tokuzawa, H. Itoh, K. Segawa, M. Murakami, K. Takahashi, M. Maruyama, M. Maeda, and S. Yamanaka. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631–642.
   PubMed Web of Science ®Google Scholar
• Mizutani, K., K. Yoon, L. Dang, A. Tokunaga, and N. Gaiano. 2007. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449:351–355.
   PubMed Web of Science ®Google Scholar
• Morrison, S., S. Perez, Z. Qiao, J. Verdi, C. Hicks, G. Weinmaster, and D. Anderson. 2000. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101:499–510.
   PubMed Web of Science ®Google Scholar
• Neves, H., F. Weerkamp, A. C. Gomes, B. A. Naber, P. Gameiro, J. D. Becker, P. Lucio, N. Clode, J. J. van Dongen, F. J. Staal, and L. Parreira. 2006. Effects of Delta1 and Jagged1 on early human hematopoiesis: correlation with expression of notch signaling-related genes in CD34+ cells. Stem Cells 24:1328–1337.
   PubMedGoogle Scholar
• Nichols, J., B. Zevnik, K. Anastassiadis, H. Niwa, D. Klewe-Nebenius, I. Chambers, H. Schöler, and A. Smith. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379–391.
   PubMed Web of Science ®Google Scholar
• Oda, T., A. G. Elkahloun, B. L. Pike, K. Okajima, I. D. Krantz, A. Genin, D. A. Piccoli, P. S. Meltzer, N. B. Spinner, F. S. Collins, and S. C. Chandrasekharappa. 1997. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat. Genet. 16:242.
   Google Scholar
• Ohtsuka, T., M. Ishibashi, G. Gradwohl, S. Nakanishi, F. Guillemot, and R. Kageyama. 1999. Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J. 18:2196–2207.
   PubMedGoogle Scholar
• Oka, C., T. Nakano, A. Wakeham, J. L. de la Pompa, C. Mori, T. Sakai, S. Okazaki, M. Kawaichi, K. Shiota, T. W. Mak, and T. Honjo. 1995. Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development 121:3291–3301.
   PubMedGoogle Scholar
• Rajan, P., D. M. Panchision, L. F. Newell, and R. D. McKay. 2003. BMPs signal alternately through a SMAD or FRAP-STAT pathway to regulate fate choice in CNS stem cells. J. Cell Biol. 161:911–921.
   PubMedGoogle Scholar
• Reya, T., S. J. Morrison, M. F. Clarke, and I. L. Weissman. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105–111.
   PubMed Web of Science ®Google Scholar
• Schmitt, T. M., and J. Zúñiga-Pflücker. 2002. Induction of T cell development from hematopoietic progenitor cells by Delta-like-1 in vitro. Immunity 17:749–756.
   PubMed Web of Science ®Google Scholar
• Schroeter, E., J. Kisslinger, and R. Kopan. 1998. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393:382–386.
   PubMed Web of Science ®Google Scholar
• Tian, G., C. Sobotka-Briner, J. Zysk, X. Liu, C. Birr, M. Sylvester, P. Edwards, C. Scott, and B. Greenberg. 2002. Linear non-competitive inhibition of solubilized human γ-secretase by pepstatin A methylester, L685458, sulfonamides, and benzodiazepines. J. Biol. Chem. 277:31499–31505.
   PubMed Web of Science ®Google Scholar
• Tropepe, V., S. Hitoshi, C. Sirard, T. W. Mak, J. Rossant, and D. van der Kooy. 2001. Direct neural fate specification from embryonic stem cells. Neuron 30:65–78.
   PubMed Web of Science ®Google Scholar
• Varnum-Finney, B., L. Wu, M. Yu, C. Brashem-Stein, S. Staats, D. Flowers, J. Griffin, and I. Bernstein. 2000. Immobilization of Notch ligand, Delta-1, is required for induction of notch signaling. J. Cell Sci. 113:4313–4318.
   PubMedGoogle Scholar
• Weinmaster, G., and C. Kintner. 2003. Modulation of notch signaling during somitogenesis. Annu. Rev. Cell Dev. Biol. 19:367–395.
   PubMed Web of Science ®Google Scholar
• Ying, Q. L., J. Nichols, I. Chambers, and A. Smith. 2003. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115:281–292.
   PubMed Web of Science ®Google Scholar