Non-invasive neural stem cells become invasive in vitro by combined FGF2 and BMP4 signaling

Journal of Cell Science

Volumn 126, Issue 16, 2013, Pages 3533-3540

  Sailer, Martin H M ^a,b   Gerber, Alexandra ^a   Tostado, Cristóbal ^a   Hutter, Gregor ^a,b   Cordier, Dominik ^b   Mariani, Luigi ^a,b   Ritz, Marie Françoise ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

BMP4; FGF2; Invasion; Migration; Neural stem cell

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 2; PODOPLANIN; TENASCIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; EPITHELIAL MESENCHYMAL TRANSITION; FOREBRAIN; GENE REPRESSION; GLIOBLASTOMA; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; NEURAL CREST CELL; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

BMP4; FGF2; INVASION; MIGRATION; NEURAL STEM CELL;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CELL MOVEMENT; FEMALE; FIBROBLAST GROWTH FACTOR 2; HUMANS; IMMUNOHISTOCHEMISTRY; NEURAL STEM CELLS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84883355806     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.125757     Document Type: Article

References (58)

1. Andrae, J., Gallini, R. and Betsholtz, C. (2008). Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22, 1276-1312.
2. Annovazzi, L., Mellai, M., Caldera, V., Valente, G. and Schiffer, D. (2011). SOX2 expression and amplification in gliomas and glioma cell lines. Cancer Genomics Proteomics 8, 139-147.
3. Astarita, J. L., Acton, S. E. and Turley, S. J. (2012). Podoplanin: emerging functions in development, the immune system, and cancer. Front Immunol. 3, 283.
4. Borello, U. and Pierani, A. (2010). Patterning the cerebral cortex: traveling with morphogens. Curr. Opin. Genet. Dev. 20, 408-415.
5. Couly, G. F. and Le Douarin, N. M. (1987). Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic human congenital abnormalities. Dev. Biol. 120, 198-214.
6. Das, S., Srikanth, M. and Kessler, J. A. (2008). Cancer stem cells and glioma. Nat. Clin. Pract. Neurol. 4, 427-435.
7. Davis, A. A. and Temple, S. (1994). A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372, 263-266.
8. Dupin, E. and Coelho-Aguiar, J. M. (2013). Isolation and differentiation properties of neural crest stem cells. Cytometry A 83, 38-47.
9. Dupin, E. and Sommer, L. (2012). Neural crest progenitors and stem cells: from early development to adulthood. Dev. Biol. 366, 83-95.
10. Ford-Perriss, M., Abud, H. and Murphy, M. (2001). Fibroblast growth factors in the developing central nervous system. Clin. Exp. Pharmacol. Physiol. 28, 493-503.
11. Furuta, Y., Piston, D. W. and Hogan, B. L. (1997). Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124, 2203-2212.
12. Gaiano, N. (2008). Strange bedfellows: Reelin and Notch signaling interact to regulate cell migration in the developing neocortex. Neuron 60, 189-191.
13. Grove, E. A. and Fukuchi-Shimogori, T. (2003). Generating the cerebral cortical area map. Annu. Rev. Neurosci. 26, 355-380.
14. Guillemot, F. (2005). Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr. Opin. Cell Biol. 17, 639-647.
15. Han, S. P., Kim, J. H., Han, M. E., Sim, H. E., Kim, K. S., Yoon, S., Baek, S. Y., Kim, B. S. and Oh, S. O. (2011). SNAI1 is involved in the proliferation and migration of glioblastoma cells. Cell. Mol. Neurobiol. 31, 489-496.
16. Hébert, J. M. and Fishell, G. (2008). The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci. 9, 678-685.
17. Hegi, M. E., Rajakannu, P. and Weller, M. (2012). Epidermal growth factor receptor: a re-emerging target in glioblastoma. Curr. Opin. Neurol. 25, 774-779.
18. Hirata, E., Arakawa, Y., Shirahata, M., Yamaguchi, M., Kishi, Y., Okada, T., Takahashi, J. A., Matsuda, M. and Hashimoto, N. (2009). Endogenous tenascin-C enhances glioblastoma invasion with reactive change of surrounding brain tissue. Cancer Sci. 100, 1451-1459.
19. Hulleman, E., Quarto, M., Vernell, R., Masserdotti, G., Colli, E., Kros, J. M., Levi, D., Gaetani, P., Tunici, P., Finocchiaro, G. et al. (2009). A role for the transcription factor HEY1 in glioblastoma. J. Cell. Mol. Med. 13, 136-146.
20. Johe, K. K., Hazel, T. G., Muller, T., Dugich-Djordjevic, M. M. and McKay, R. D. (1996). Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10, 3129-3140.
21. Johnston, A. L., Lun, X., Rahn, J. J., Liacini, A., Wang, L., Hamilton, M. G., Parney, I. F., Hempstead, B. L., Robbins, S. M., Forsyth, P. A. et al. (2007). The p75 neurotrophin receptor is a central regulator of glioma invasion. PLoS Biol. 5, e212.
22. Kim, J.-H., Panchision, D. M., Kittappa, R. and McKay, R. D. (2003). Generating CNS neurons from embryonic, fetal and adult stem cells. In Differentiation of Embryonic Stem Cells. New York, NY: Academic Press.
23. Kleinman, H. K., McGarvey, M. L., Liotta, L. A., Robey, P. G., Tryggvason, K. and Martin, G. R. (1982). Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21, 6188-6193.
24. Le Douarin, N. M. and Kalcheim, C. (1999). The Neural Crest. Cambridge University Press.
25. Lee, K. J. and Jessell, T. M. (1999). The specification of dorsal cell fates in the vertebrate central nervous system. Annu. Rev. Neurosci. 22, 261-294.
26. Liu, J. S. (2011). Molecular genetics of neuronal migration disorders. Curr. Neurol. Neurosci. Rep. 11, 171-178.
27. Mariani, L., Beaudry, C., McDonough, W. S., Hoelzinger, D. B., Demuth, T., Ross, K. R., Berens, T., Coons, S. W., Watts, G., Trent, J. M. et al. (2001). Glioma cell motility is associated with reduced transcription of proapoptotic and proliferation genes: a cDNA microarray analysis. J. Neurooncol. 53, 161-176.
28. Marin, F. and Nieto, M. A. (2004). Expression of chicken slug and snail in mesenchymal components of the developing central nervous system. Dev. Dyn. 230, 144-148.
29. Mishima, K., Kato, Y., Kaneko, M. K., Nishikawa, R., Hirose, T. and Matsutani, M. (2006). Increased expression of podoplanin in malignant astrocytic tumors as a novel molecular marker of malignant progression. Acta Neuropathol. 111, 483-488.
30. Morrison, R. S., Yamaguchi, F., Saya, H., Bruner, J. M., Yahanda, A. M., Donehower, L. A. and Berger, M. (1994). Basic fibroblast growth factor and fibroblast growth factor receptor I are implicated in the growth of human astrocytomas. J. Neurooncol. 18, 207-216.
31. Morrison, S. J., White, P. M., Zock, C. and Anderson, D. J. (1999). Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96, 737-749.
32. Nakada, M., Nakada, S., Demuth, T., Tran, N. L., Hoelzinger, D. B. and Berens, M. E. (2007). Molecular targets of glioma invasion. Cell. Mol. Life Sci. 64, 458-478.
33. Nazarenko, I., Hede, S. M., He, X., Hedrén, A., Thompson, J., Lindström, M. S. and Nistér, M. (2012). PDGF and PDGF receptors in glioma. Ups. J. Med. Sci. 117, 99-112.
34. Nieto, M. A. (2002). The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166.
35. Nieto, M. A. (2009). Epithelial-mesenchymal transitions in development and disease: old views and new perspectives. Int. J. Dev. Biol. 53, 1541-1547.
36. Panchision, D. M. and McKay, R. D. (2002). The control of neural stem cells by morphogenic signals. Curr. Opin. Genet. Dev. 12, 478-487.
37. Panchision, D. M., Pickel, J. M., Studer, L., Lee, S. H., Turner, P. A., Hazel, T. G. and McKay, R. D. (2001). Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev. 15, 2094-2110.
38. Piccirillo, S. G., Reynolds, B. A., Zanetti, N., Lamorte, G., Binda, E., Broggi, G., Brem, H., Olivi, A., Dimeco, F. and Vescovi, A. L. (2006). Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444, 761-765.
39. Quinn, J. C., Molinek, M., Mason, J. O. and Price, D. J. (2009). Gli3 is required autonomously for dorsal telencephalic cells to adopt appropriate fates during embryonic forebrain development. Dev. Biol. 327, 204-215.
40. Raff, M. C., Miller, R. H. and Noble, M. (1983). A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396.
41. Raica, M., Cimpean, A. M. and Ribatti, D. (2008). The role of podoplanin in tumor progression and metastasis. Anticancer Res. 28 5B, 2997-3006.
42. Rakic, P., Ayoub, A. E., Breunig, J. J. and Dominguez, M. H. (2009). Decision by division: making cortical maps. Trends Neurosci. 32, 291-301.
43. Ray, J., Baird, A. and Gage, F. H. (1997). A 10-amino acid sequence of fibroblast growth factor 2 is sufficient for its mitogenic activity on neural progenitor cells. Proc. Natl. Acad. Sci. USA 94, 7047-7052.
44. Reid, C. B., Liang, I. and Walsh, C. (1995). Systematic widespread clonal organization in cerebral cortex. Neuron 15, 299-310.
45. Rempel, S. A., Golembieski, W. A., Ge, S., Lemke, N., Elisevich, K., Mikkelsen, T. and Gutiérrez, J. A. (1998). SPARC: a signal of astrocytic neoplastic transformation and reactive response in human primary and xenograft gliomas. J. Neuropathol. Exp. Neurol. 57, 1112-1121.
46. 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.
47. Sánchez-Tilló, E., Liu, Y., de Barrios, O., Siles, L., Fanlo, L., Cuatrecasas, M., Darling, D. S., Dean, D. C., Castells, A. and Postigo, A. (2012). EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness. Cell. Mol. Life Sci. 69, 3429-3456.
48. Sauka-Spengler, T. and Bronner-Fraser, M. (2008). A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9, 557-568.
49. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
50. Schwartzbaum, J. A., Fisher, J. L., Aldape, K. D. and Wrensch, M. (2006). Epidemiology and molecular pathology of glioma. Nat. Clin. Pract. Neurol. 2, 494-503; quiz 1 p following 516.
51. Serbedzija, G. N., Bronner-Fraser, M. and Fraser, S. E. (1992). Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116, 297-307.
52. Shahi, M. H., Lorente, A. and Castresana, J. S. (2008). Hedgehog signalling in medulloblastoma, glioblastoma and neuroblastoma. Oncol. Rep. 19, 681-688.
53. Sur, M. and Rubenstein, J. L. (2005). Patterning and plasticity of the cerebral cortex. Science 310, 805-810.
54. Vescovi, A. L., Reynolds, B. A., Fraser, D. D. and Weiss, S. (1993). bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11, 951-966.
55. Vescovi, A. L., Galli, R. and Reynolds, B. A. (2006). Brain tumour stem cells. Nat. Rev. Cancer 6, 425-436.
56. Wong, C. E., Paratore, C., Dours-Zimmermann, M. T., Rochat, A., Pietri, T., Suter, U., Zimmermann, D. R., Dufour, S., Thiery, J. P., Meijer, D. et al. (2006). Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J. Cell Biol. 175, 1005-1015.
57. Yamada, N., Kato, M., ten Dijke, P., Yamashita, H., Sampath, T. K., Heldin, C. H., Miyazono, K. and Funa, K. (1996). Bone morphogenetic protein type IB receptor is progressively expressed in malignant glioma tumours. Br. J. Cancer 73, 624-629.
58. Yang, H. W., Menon, L. G., Black, P. M., Carroll, R. S. and Johnson, M. D. (2010). SNAI2/Slug promotes growth and invasion in human gliomas. BMC Cancer 10, 301.