Sonic Hedgehog modulates EGFR dependent proliferation of neural stem cells during late mouse embryogenesis through EGFR transactivation

Frontiers in Cellular Neuroscience

Volumn , Issue SEP, 2013, Pages

  Reinchisi, Gisela ^a,b,c   Parada, Margarita ^a,b   Lois, Pablo ^a   Oyanadel, Claudia ^b   Shaughnessy, Ronan ^b   Gonzalez, Alfonso ^b   Palma, Verónica ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Cancer; EGFR; Neural progenitors; Proliferation; Radial Glial cells; Shh; Transactivation

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GLIA CELL; HELA CELL; INTERNALIZATION; MOUSE; NEOCORTEX; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROMODULATION; NONHUMAN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSACTIVATION;

EID: 84885089031     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00166     Document Type: Article

References (56)

1. Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T., and Saltiel, A. R. (1995). PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270, 27489-27494. doi: 10.1074/jbc.270.46.27489
2. Alwan, H. A. J., van Zoelen, E. J. J., and van Leeuwen, J. E. M. (2003). Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J. Biol. Chem. 278, 35781-35790. doi: 10.1074/jbc.M301326200
3. Bigelow, R. L. H., Jen, E. Y., Delehedde, M., Chari, N. S., and McDonnell, T. J. (2005). Sonic hedgehog induces epidermal growth factor dependent matrix infiltration in HaCaT keratinocytes. J. Invest. Dermatol. 124, 457-465. doi: 10.1111/j.0022-202X.2004.23590.x
4. Buvinic, S., Bravo-Zehnder, M., Boyer, J. L., Huidobro-Toro, J. P., and González, A. (2007). Nucleotide P2Y1 receptor regulates EGF receptor mitogenic signaling and expression in epithelial cells. J. Cell Sci. 120, 4289-4301. doi: 10.1242/jcs.03490
5. Caric, D., Raphael, H., Viti, J., Feathers, A., Wancio, D., and Lillien, L. (2001). EGFRs mediate chemotactic migration in the developing telencephalon. Development 128, 4203-4216.
6. Carpenter, G. (1999). Employment of the epidermal growth factor receptor in growth factor-independent signaling pathways. J. Cell Biol. 146, 697-702. doi: 10.1083/jcb.146.4.697
7. Caviness, V. S. Jr., Takahashi, T., and Nowakowski, R. S. (1995). Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 18, 379-383. doi: 10.1016/0166-2236(95)93933-O
8. Chen, J. K., Taipale, J., Cooper, M. K., and Beachy, P. A. (2002). Inhibition of hedgehog signaling by direct binding of cyclopamine to smoothened. Genes Dev. 16, 2743-2748. doi: 10.1101/gad.1025302
9. Dahmane, N., Sánchez, P., Gitton, Y., Palma, V., Sun, T., Beyna, M., et al. (2001). The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 128, 5201-5212.
10. Daub, H., Weiss, F. U., Wallasch, C., and Ullrich, A. (1996). Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379, 557-560. doi: 10.1038/379557a0
11. Dave, R. K., Ellis, T., Toumpas, M. C., Robson, J. P., Julian, E., Adolphe, C., et al. (2011). Sonic hedgehog and notch signaling can cooperate to regulate neurogenic divisions of neocortical progenitors. PLoS ONE 6:e14680. doi: 10.1371/journal.pone.0014680
12. Doetsch, F., Caillé, I., Lim, D. A., García-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
13. Ellis, P., Fagan, B. M., Magness, S. T., Hutton, S., Taranova, O., Hayashi, S., et al. (2004). SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 26, 148-165. doi: 10.1159/000082134
14. Goh, L. K., and Sorkin, A. (2013). Endocytosis of receptor tyrosine kinases. Cold Spring Harb. Perspect. Biol. 5:a017459. doi: 10.1101/cshperspect.a017459
15. Graham, V., Khudyakov, J., Ellis, P., and Pevny, L. (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765. doi: 10.1016/S0896-6273(03)00497-5
16. Gschwind, A., Zwick, E., Prenzel, N., Leserer, M., and Ullrich, A. (2001). Cell communication networks: epidermal growth factor receptor transactivation as the paradigm for interreceptor signal transmission. Oncogene 20, 1594-1600. doi: 10.1038/sj.onc.1204192
17. Heo, J. S., Lee, M. Y., and Han, H. J. (2007). Sonic hedgehog stimulates mouse embryonic stem cell proliferation by cooperation of Ca2+/protein kinase C and epidermal growth factor receptor as well as Gli1 activation. Stem Cells 25, 3069-3080. doi: 10.1634/stemcells.2007-0550
18. Huangfu, D., and Anderson, K. V. (2006). Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133, 3-14. doi: 10.1242/dev.02169
19. Ihrie, R. A., and Alvarez-Buylla, A. (2008). Cells in the astroglial lineage are neural stem cells. Cell Tissue Res. 331, 179-191. doi: 10.1007/s00441-007-0461-z
20. Imura, T., Kornblum, H. I., and Sofroniew, M. V. (2003). The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J. Neurosci. 23, 2824-2832.
21. Izumi, Y., Hirata, M., Hasuwa, H., Iwamoto, R., Umata, T., Miyado, K., et al. (1998). A metalloprotease-disintegrin, MDC9/meltrin-gamma/ADAM9 and PKCdelta are involved in TPA-induced ectodomain shedding of membrane-anchored heparin-binding EGF-like growth factor. EMBO J. 17, 7260-7272. doi: 10.1093/emboj/17.24.7260
22. Komada, M., Saitsu, H., Kinboshi, M., Miura, T., Shiota, K., and Ishibashi, M. (2008). Hedgehog signaling is involved in development of the neocortex. Development 135, 2717-2727. doi: 10.1242/dev.015891
23. Lappano, R., and Maggiolini, M. (2011). G protein-coupled receptors: novel targets for drug discovery in cancer. Nat. Rev. Drug Discov. 10, 47-60. doi: 10.1038/nrd3320
24. Lillien, L., and Gulacsi, A. (2006). Environmental signals elicit multiple responses in dorsal telencephalic progenitors by threshold-dependent mechanisms. Cereb. Cortex 16(Suppl. 1), i74-i81. doi: 10.1093/cercor/bhj169
25. Madshus, I. H., and Stang, E. (2009). Internalization and intracellular sorting of the EGF receptor: a model for understanding the mechanisms of receptor trafficking. J. Cell Sci. 122, 3433-3439. doi: 10.1242/jcs.050260
26. Mangelberger, D., Kern, D., Loipetzberger, A., Eberl, M., and Aberger, F. (2012). Cooperative Hedgehog-EGFR signaling. Front. Biosci. 17, 90-99. doi: 10.2741/3917
27. Martínez, C., Cornejo, V. H., Lois, P., Ellis, T., Solis, N. P., Wainwright, B. J., et al. (2013). Proliferation of murine midbrain neural stem cells depends upon an endogenous sonic hedgehog (Shh) source. PLoS ONE 8:e65818. doi: 10.1371/journal.pone.0065818
28. McCarthy, N. (2012). Cancer stem cells: tracing clones. Nat. Rev. Cancer 12, 579. doi: 10.1038/nrc3354
29. Mimeault, M., and Batra, S. K. (2010). Frequent deregulations in the hedgehog signaling network and cross-talks with the epidermal growth factor receptor pathway involved in cancer progression and targeted therapies. Pharmacol. Rev. 62, 497-524. doi: 10.1124/pr.109.002329
30. Norambuena, A., Metz, C., Jung, J. E., Silva, A., Otero, C., Cancino, J., et al. (2010). Phosphatidic acid induces ligand-independent epidermal growth factor receptor endocytic traffic through PDE4 activation. Mol. Biol. Cell 21, 2916-2929. doi: 10.1091/mbc.E10-02-0167
31. Norambuena, A., Metz, C., Vicuña, L., Silva, A., Pardo, E., Oyanadel, C., et al. (2009). Galectin-8 induces apoptosis in Jurkat T cells by phosphatidic acid-mediated ERK1/2 activation supported by protein kinase A down-regulation. J. Biol. Chem. 284, 12670-12679. doi: 10.1074/jbc.M808949200
32. Ogden, S. K., Fei, D. L., Schilling, N. S., Ahmed, Y. F., Hwa, J., and Robbins, D. J. (2008). G protein Galphai functions immediately downstream of Smoothened in Hedgehog signalling. Nature 456, 967-970. doi: 10.1038/nature07459
33. Oliver, T. G., and Wechsler-Reya, R. J. (2004). Getting at the root and stem of brain tumors. Neuron 42, 885-888. doi: 10.1016/j.neuron.2004.06.011
34. Palma, V., Lim, D. A., Dahmane, N., Sánchez, P., Brionne, T. C., Herzberg, C. D., et al. (2005). Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development132, 335-344. doi: 10.1242/dev.01567
35. Palma, V., and Ruiz i Altaba, A. (2004). Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 131, 337-345. doi: 10.1242/dev.00930
36. Pennock, S., and Wang, Z. (2003). Stimulation of cell proliferation by endosomal epidermal growth factor receptor as revealed through two distinct phases of signaling. Mol. Cell. Biol. 23, 5803-5815. doi: 10.1128/MCB.23.16.5803-5815.2003
37. Piper, R. C., and Luzio, J. P. (2007). Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr. Opin. Cell Biol. 19, 459-465. doi: 10.1016/j.ceb.2007.07.002
38. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C., et al. (1999). EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-888. doi: 10.1038/47260
39. Reynolds, B. A., and Weiss, S. (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175, 1-13. doi: 10.1006/dbio.1996.0090
40. Roepstorff, K., Grandal, M. V., Henriksen, L., Knudsen, S. L. J., Lerdrup, M., Grøvdal, L., et al. (2009). Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 10, 1115-1127. doi: 10.1111/j.1600-0854.2009.00943.x
41. Ruiz i Altaba, A., Mas, C., and Stecca, B. (2007). The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol. 17, 438-447. doi: 10.1016/j.tcb.2007.06.007
42. Rush, J. S., Quinalty, L. M., Engelman, L., Sherry, D. M., and Ceresa, B. P. (2012). Endosomal accumulation of the activated epidermal growth factor receptor (EGFR) induces apoptosis. J. Biol. Chem. 287, 712-722. doi: 10.1074/jbc.M111.294470
43. Salazar, G., and González, A. (2002). Novel mechanism for regulation of epidermal growth factor receptor endocytosis revealed by protein kinase A inhibition. Mol. Biol. Cell 13, 1677-1693. doi: 10.1091/mbc.01-08-0403
44. Schlessinger, J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103, 211-225. doi: 10.1016/S0092-8674(00)00114-8
45. Schnidar, H., Eberl, M., Klingler, S., Mangelberger, D., Kasper, M., Hauser-Kronberger, C., et al. (2009). Epidermal growth factor receptor signaling synergizes with Hedgehog/GLI in oncogenic transformation via activation of the MEK/ERK/JUN pathway. Cancer Res. 69, 1284-1292. doi: 10.1158/0008-5472.CAN-08-2331
46. Scita, G., and Di Fiore, P. P. (2010). The endocytic matrix. Nature 463, 464-473. doi: 10.1038/nature08910
47. Seger, R., and Krebs, E. G. (1995). The MAPK signaling cascade. FASEB J. 9, 726-735.
48. Sigismund, S., Algisi, V., Nappo, G., Conte, A., Pascolutti, R., Cuomo, A., et al. (2013). Threshold-controlled ubiquitination of the EGFR directs receptor fate. EMBO J. 32, 2140-2157. doi: 10.1038/emboj.2013.149
49. Sigismund, S., Argenzio, E., Tosoni, D., Cavallaro, E., Polo, S., and Di Fiore, P. P. (2008). Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 15, 209-219. doi: 10.1016/j.devcel.2008.06.012
50. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., et al. (2005). Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. U.S.A. 102, 2760-2765. doi: 10.1073/pnas.0409817102
51. Sorkin, A., and Goh, L. K. (2008). Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 314, 3093-3106. doi: 10.1016/j.yexcr.2008.08.013
52. Traverse, S., Seedorf, K., Paterson, H., Marshall, C. J., Cohen, P., and Ullrich, A. (1994). EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Curr. Biol. 4, 694-701. doi: 10.1016/S0960-9822(00)00154-8
53. Vescovi, A. L., Galli, R., and Reynolds, B. A. (2006). Brain tumour stem cells. Nat. Rev. Cancer 6, 425-436. doi: 10.1038/nrc1889
54. Ward, W. H., Cook, P. N., Slater, A. M., Davies, D. H., Holdgate, G. A., and Green, L. R. (1994). Epidermal growth factor receptor tyrosine kinase. Investigation of catalytic mechanism, structure-based searching and discovery of a potent inhibitor. Biochem. Pharmacol. 48, 659-666. doi: 10.1016/0006-2952(94)90042-6
55. Wegner, C. S., Rodahl, L. M. W., and Stenmark, H. (2011). ESCRT proteins and cell signalling. Traffic 12, 1291-1297. doi: 10.1111/j.1600-0854.2011.01210.x
56. Yarden, Y., and Sliwkowski, M. X. (2001). Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137. doi: 10.1038/35052073