Ror family receptor tyrosine kinases regulate the maintenance of neural progenitor cells in the developing neocortex

Journal of Cell Science

Volumn 125, Issue 8, 2012, Pages 2017-2029

  Endo, Mitsuharu ^a   Doi, Ryosuke ^a   Nishita, Michiru ^a   Minami, Yasuhiro ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Neurogenesis; NPCs; Ror1; Ror2; Signaling; Wnt5a

Indexed keywords

BETA CATENIN; BETA TUBULIN; BROXURIDINE; DISHEVELLED 2; EOMESODERMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN TYROSINE KINASE; ROR1 PROTEIN; ROR2 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE INACTIVATION; GENE SILENCING; MOUSE; NEOCORTEX; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; EYE PROTEINS; HOMEODOMAIN PROTEINS; MICE; MICE, INBRED ICR; NEOCORTEX; NEURAL STEM CELLS; NEUROGENESIS; PAIRED BOX TRANSCRIPTION FACTORS; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84863100330     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.097782     Document Type: Article

References (56)

1. Al-Shawi, R., Ashton, S. V., Underwood, C. and Simons, J. P. (2001). Expression of the Ror1 and Ror2 receptor tyrosine kinase genes during mouse development. Dev. Genes Evol. 211, 161-171.
2. Bertrand, N., Castro, D. S. and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.
3. Bryja, V., Schulte, G., Rawal, N., Grahn, A. and Arenas, E. (2007). Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J. Cell Sci. 120, 586-595.
4. Cadigan, K. M. and Nusse, R. (1997). Wnt signaling: a common theme in animal development. Genes Dev. 11, 3286-3305.
5. Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A., Bulfone, A., Kowalczyk, T. and Hevner, R. F. (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247-251.
6. Forrester, W. C., Dell, M., Perens, E. and Garriga, G. (1999). A C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature 400, 881-885.
7. Forrester, W. C., Kim, C. and Garriga, G. (2004). The Caenorhabditis elegans Ror RTK CAM-1 inhibits EGL-20/Wnt signaling in cell migration. Genetics 168, 1951-1962.
8. Fougerousse, F., Bullen, P., Herasse, M., Lindsay, S., Richard, I., Wilson, D., Suel, L., Durand, M., Robson, S., Abitbol, M. et al. (2000). Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Hum. Mol. Genet. 9, 165-173.
9. Fukuda, T., Chen, L., Endo, T., Tang, L., Lu, D., Castro, J. E., Widhopf, G. F., 2nd, Rassenti, L. Z., Cantwell, M. J., Prussak, C. E. et al. (2008). Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal antigen and receptor for Wnt5a. Proc. Natl. Acad. Sci. USA 105, 3047-3052.
10. Gonzalez-Sancho, J. M., Brennan, K. R., Castelo-Soccio, L. A. and Brown, A. M. (2004). Wnt proteins induce dishevelled phosphorylation via an LRP5/6- independent mechanism, irrespective of their ability to stabilize beta-catenin. Mol. Cell. Biol. 24, 4757-4768.
11. Green, J. L., Kuntz, S. G. and Sternberg, P. W. (2008). Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol. 18, 536-544.
12. Grumolato, L., Liu, G., Mong, P., Mudbhary, R., Biswas, R., Arroyave, R., Vijayakumar, S., Economides, A. N. and Aaronson, S. A. (2010). Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev. 24, 2517-2530.
13. Guillemot, F. (2005). Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr. Opin. Cell Biol. 17, 639-647.
14. Guillemot, F. (2007). Cell fate specification in the mammalian telencephalon. Prog. Neurobiol. 83, 37-52.
15. Hirabayashi, Y., Itoh, Y., Tabata, H., Nakajima, K., Akiyama, T., Masuyama, N. and Gotoh, Y. (2004). The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131, 2791-2801.
16. Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K. and Kageyama, R. (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 30, 3489-3498.
17. Israsena, N., Hu, M., Fu, W., Kan, L. and Kessler, J. A. (2004). The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev. Biol. 268, 220-231.
18. Kageyama, R., Ohtsuka, T., Hatakeyama, J. and Ohsawa, R. (2005). Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306, 343-348.
19. Kani, S., Oishi, I., Yamamoto, H., Yoda, A., Suzuki, H., Nomachi, A., Iozumi, K., Nishita, M., Kikuchi, A., Takumi, T. et al. (2004). The receptor tyrosine kinase Ror2 associates with and is activated by casein kinase Iepsilon. J. Biol. Chem. 279, 50102-50109.
20. Keeble, T. R., Halford, M. M., Seaman, C., Kee, N., Macheda, M., Anderson, R. B., Stacker, S. A. and Cooper, H. M. (2006). The Wnt receptor Ryk is required for Wnt5a-mediated axon guidance on the contralateral side of the corpus callosum. J. Neurosci. 26, 5840-5848.
21. Kennerdell, J. R., Fetter, R. D. and Bargmann, C. I. (2009). Wnt-Ror signaling to SIA and SIB neurons directs anterior axon guidance and nerve ring placement in C. elegans. Development 136, 3801-3810.
22. Koga, M., Take-uchi, M., Tameishi, T. and Ohshima, Y. (1999). Control of DAF-7 TGF-(alpha) expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans. Development 126, 5387-5398.
23. Kuwahara, A., Hirabayashi, Y., Knoepfler, P. S., Taketo, M.M., Sakai, J., Kodama, T. and Gotoh, Y. (2010). Wnt signaling and its downstream target N-myc regulate basal progenitors in the developing neocortex. Development 137, 1035-1044.
24. Lee, S. M., Tole, S., Grove, E. and McMahon, A. P. (2000). A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127, 457-467.
25. Lyu, J., Yamamoto, V. and Lu, W. (2008). Cleavage of the Wnt receptor Ryk regulates neuronal differentiation during cortical neurogenesis. Dev. Cell 15, 773-780.
26. Matsuda, T., Nomi, M., Ikeya, M., Kani, S., Oishi, I., Terashima, T., Takada, S. and Minami, Y. (2001). Expression of the receptor tyrosine kinase genes, Ror1 and Ror2, during mouse development. Mech. Dev. 105, 153-156.
27. Matsuda, T., Suzuki, H., Oishi, I., Kani, S., Kuroda, Y., Komori, T., Sasaki, A., Watanabe, K. and Minami, Y. (2003). The receptor tyrosine kinase Ror2 associates with the melanoma-associated antigen (MAGE) family protein Dlxin-1 and regulates its intracellular distribution. J. Biol. Chem. 278, 29057-29064.
28. McKay, S. E., Hislop, J., Scott, D., Bulloch, A. G., Kaczmarek, L. K., Carew, T. J. and Sossin, W. S. (2001). Aplysia ror forms clusters on the surface of identified neuroendocrine cells. Mol. Cell. Neurosci. 17, 821-841.
29. Mikels, A. J. and Nusse, R. (2006). Purified Wnt5a protein activates or inhibits betacatenin-TCF signaling depending on receptor context. PLoS Biol. 4, e115.
30. Minami, Y., Oishi, I., Endo, M. and Nishita, M. (2010). Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: their implications in developmental morphogenesis and human diseases. Dev. Dyn. 239, 1-15.
31. Miyata, T., Kawaguchi, D., Kawaguchi, A. and Gotoh, Y. (2010). Mechanisms that regulate the number of neurons during mouse neocortical development. Curr. Opin. Neurobiol. 20, 22-28.
32. Munji, R. N., Choe, Y., Li, G., Siegenthaler, J. A. and Pleasure, S. J. (2011). Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J. Neurosci. 31, 1676-1687.
33. Nelson, W. J. and Nusse, R. (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487.
34. Nishita, M., Yoo, S. K., Nomachi, A., Kani, S., Sougawa, N., Ohta, Y., Takada, S., Kikuchi, A. and Minami, Y. (2006). Filopodia formation mediated by receptor tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J. Cell Biol. 175, 555-562.
35. Nishita, M., Itsukushima, S., Nomachi, A., Endo, M., Wang, Z., Inaba, D., Qiao, S., Takada, S., Kikuchi, A. and Minami, Y. (2010). Ror2/Frizzled complex mediates Wnt5a-induced AP-1 activation by regulating Dishevelled polymerization. Mol. Cell. Biol. 30, 3610-3619.
36. Nomachi, A., Nishita, M., Inaba, D., Enomoto, M., Hamasaki, M. and Minami, Y. (2008). Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J. Biol. Chem. 283, 27973-27981.
37. Oishi, I., Sugiyama, S., Liu, Z. J., Yamamura, H., Nishida, Y. and Minami, Y. (1997). A novel Drosophila receptor tyrosine kinase expressed specifically in the nervous system. Unique structural features and implication in developmental signaling. J. Biol. Chem. 272, 11916-11923.
38. Oishi, I., Takeuchi, S., Hashimoto, R., Nagabukuro, A., Ueda, T., Liu, Z. J., Hatta, T., Akira, S., Matsuda, Y., Yamamura, H. et al. (1999). Spatio-temporally regulated expression of receptor tyrosine kinases, mRor1, mRor2, during mouse development: implications in development and function of the nervous system. Genes Cells 4, 41-56.
39. Oishi, I., Suzuki, H., Onishi, N., Takada, R., Kani, S., Ohkawara, B., Koshida, I., Suzuki, K., Yamada, G., Schwabe, G. C. et al. (2003). The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8, 645-654.
40. Paganoni, S. and Ferreira, A. (2005). Neurite extension in central neurons: a novel role for the receptor tyrosine kinases Ror1 and Ror2. J. Cell Sci. 118, 433-446.
41. Paganoni, S., Bernstein, J. and Ferreira, A. (2010). Ror1-Ror2 complexes modulate synapse formation in hippocampal neurons. Neuroscience 165, 1261-1274.
42. Pfenninger, C. V., Roschupkina, T., Hertwig, F., Kottwitz, D., Englund, E., Bengzon, J., Jacobsen, S. E. and Nuber, U. A. (2007). CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 67, 5727-5736.
43. Qian, X., Shen, Q., Goderie, S. K., He, W., Capela, A., Davis, A. A. and Temple, S. (2000). Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28, 69-80.
44. Ren, D., Minami, Y. and Nishita, M. (2011). Critical role of Wnt5a-Ror2 signaling in motility and invasiveness of carcinoma cells following Snail-mediated epithelialmesenchymal transition. Genes Cells 16, 304-315.
45. Ross, S. E., Greenberg, M. E. and Stiles, C. D. (2003). Basic helix-loop-helix factors in cortical development. Neuron 39, 13-25.
46. Saito, T. and Nakatsuji, N. (2001). Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240, 237-246.
47. Sakurai, K. and Osumi, N. (2008). The neurogenesis-controlling factor, Pax6, inhibits proliferation and promotes maturation in murine astrocytes. J. Neurosci. 28, 4604-4612.
48. Sato, A., Yamamoto, H., Sakane, H., Koyama, H. and Kikuchi, A. (2010). Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J. 29, 41-54.
49. Schulte, G., Bryja, V., Rawal, N., Castelo-Branco, G., Sousa, K. M. and Arenas, E. (2005). Purified Wnt-5a increases differentiation of midbrain dopaminergic cells and dishevelled phosphorylation. J. Neurochem. 92, 1550-1553.
50. Semenov, M. V., Habas, R., Macdonald, B. T. and He, X. (2007). SnapShot: noncanonical Wnt signaling pathways. Cell 131, 1378.
51. Shimizu, T., Kagawa, T., Inoue, T., Nonaka, A., Takada, S., Aburatani, H. and Taga, T. (2008). Stabilized beta-catenin functions through TCF/LEF proteins and the Notch/RBP-Jkappa complex to promote proliferation and suppress differentiation of neural precursor cells. Mol. Cell. Biol. 28, 7427-7441.
52. Song, S., Zhang, B., Sun, H., Li, X., Xiang, Y., Liu, Z., Huang, X. and Ding, M. (2010). A Wnt-Frz/Ror-Dsh pathway regulates neurite outgrowth in Caenorhabditis elegans. PLoS Genet. 6, e1001056.
53. Veeman, M. T., Axelrod, J. D. and Moon, R. T. (2003). A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5, 367-377.
54. Viti, J., Gulacsi, A. and Lillien, L. (2003). Wnt regulation of progenitor maturation in the cortex depends on Shh or fibroblast growth factor 2. J. Neurosci. 23, 5919-5927
55. Wilson, C., Goberdhan, D. C. and Steller, H. (1993). Dror, a potential neurotrophic receptor gene, encodes a Drosophila homolog of the vertebrate Ror family of Trkrelated receptor tyrosine kinases. Proc. Natl. Acad. Sci. USA 90, 7109-7113.
56. Woodhead, G. J., Mutch, C. A., Olson, E. C. and Chenn, A. (2006). Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J. Neurosci. 26, 12620-12630.