Roles of Ets-1 and p70S6 kinase in chondrogenic and gliogenic specification of mouse mesencephalic neural crest cells

Mechanisms of Development

Volumn 127, Issue 3-4, 2010, Pages 169-182

  Sugiura, Keisuke ^a   Ito, Kazuo ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Akt pathway; Chondrogenesis; Erk pathway; Ets 1; Fibroblast growth factors; Gliogenesis; Mesencephalic neural crest cells; Mouse; Notch signaling; P70S6 kinase

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE 3; NOTCH RECEPTOR; PROTEIN KINASE B; S6 KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR ETS 1;

ANIMAL CELL; ARTICLE; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EXPRESSION VECTOR; GANGLION; GENE EXPRESSION; GENE FUNCTION; GLIOGENESIS; MESENCEPHALON; MESENCHYME CELL; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINEAGE; CHONDROCYTES; FIBROBLAST GROWTH FACTOR 2; MESENCEPHALON; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURAL CREST; NEUROGLIA; PROTO-ONCOGENE PROTEIN C-ETS-1; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 77950952761     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2010.01.002     Document Type: Article

References (60)

1. Artavanis-Tsakonas S., Rand M.D., Lake R.J. Notch signaling: cell fate control and signal integration in development. Science 1999, 284:770-776.
2. Bobick B.E., Kulyk W.M. MEK-ERK signaling plays diverse roles in the regulation of facial chondrogenesis. Exp. Cell Res. 2006, 312:1079-1092.
3. Breau M.A., Pietri T., Stemmler M.P., Thiery J.P., Weston J.A. A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc. Natl. Acad. Sci. USA 2008, 105(22):7750-7755.
4. Carballada R., Yasuo H., Lemaire P. Phosphatidylinositol-3 kinase acts in parallel to the ERK MAP kinase in the FGF pathway during Xenopus mesoderm induction. Development 2001, 128:35-44.
5. Chan Y., Li X., Eswarakumar V.P., Seger R., Lonai P. Fibroblast growth factor (FGF) signaling through PI 3-kinase and Akt/PKB is required for embryoid body differentiation. Oncogene 2000, 19:3750-3756.
6. Cobb M.H., Boulton T.G., Robbins D.J. Extracellular signal-regulated kinases: ERKs in progress. Cell Regul. 1991, 2:965-978.
7. DeSilva D.R., Jones E.A., Favata M.F., Jaffee B.D., Magolda R.L., Trzaskos J.M., Scherle P.A. Inhibition of mitogen-activated protein kinase kinase blocks T cell proliferation but does not induce or prevent anergy. J. Immunol. 1998, 160:4175-4181.
8. Dudley D.T., Pang L., Decker S.J., Bridges A.J., Saltiel A.R. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 1995, 92:7686-7689.
9. Eswarakumar V.P., Lax I., Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 2005, 16:139-149.
10. Fafeur V., Tulasne D., Quéva C., Vercamer C., Dimster V., Mattot V., Stéhelin D., Desbiens X., Vandenbunder B. The ETS1 transcription factor is expressed during epithelial-mesenchymal transitions in the chick embryo and is MDCK epithelial cells. Cell Growth Differ. 1997, 8:655-665.
11. Favata M.F., Horiuchi K.Y., Manos E.J., Daulerio A.J., Stradley D.A., Feeser W.S., Van Dyk D.E., Pitts W.J., Earl R.A., Hobbs F., Copeland R.A., Magolda R.L., Scherle P.A., Trzaskos J.M. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 1998, 273(29):18623-18632.
12. Fitzgerald K., Harrington A., Leder P. Ras pathway signals are required for Notch-mediated oncogenesis. Oncogene 2000, 19:4191-4198.
13. Foltz D.R., Santiago M.C., Berechid B.E., Nye J.S. Glycogen synthase kinase-3β modulates Notch signaling and stability. Curr. Biol. 2002, 12:1006-1011.
14. Gagnon A., Lau S., Sorisky A. Rapamycin-sensitive phase of 3T3-L1 preadipocyte differentiation after clonal expansion. J. Cell. Physiol. 2001, 189:14-22.
15. Gerasimovskaya E.V., Tucker D.A., Weiser-Evans M., Wenzlau J.M., Klemm D.J., Banks M., Stenmark K.R. Extracellular ATP-induced proliferation of adventitial fibroblasts requires phosphoinositide 3-kinase, Akt, mammalian target of rapamycin, and p70 S6 kinase signaling pathways. J. Biol. Chem. 2005, 280:1838-1848.
16. Hall B.K. The Neural Crest in Development and Evolution 1999, Springer, New York.
17. Horikawa T., Sheen T.S., Takeshita H., Sato H., Furukawa M., Yoshizaki T. Induction of c-Met proto-oncogene by Epstein-Barr virus latent membrane protein-1 and the correlation with cervical lymph node metastasis of nasopharyngeal carcinoma. Am. J. Pathol. 2001, 159:27-33.
18. Hosoi H., Dilling M.B., Shikata T., Liu L.N., Shu L., Ashmun R.A., Germain G.S., Abraham R.T., Houghton P.J. Rapamycin causes poorly reversible inhibition of mTOR and induces p53-independent apoptosis in human rhabdomyosarcoma cells. Cancer Res. 1999, 59:886-894.
19. Ijuin K., Nakanishi K., Ito K. Different downstream pathways for Notch signaling are required for gliogenic and chondrogenic specification of mouse mesencephalic neural crest cells. Mech. Dev. 2008, 125:462-474.
20. Ishibashi M., Moriyoshi K., Sasai Y., Shiota K., Nakanishi S., Kageyama R. Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J. 1994, 13:1799-1805.
21. Ito K., Morita T. Role of retinoic acid in mouse neural crest cell development in vitro. Dev. Dyn. 1995, 204:211-218.
22. Kageyama R., Ohtsuka T. The Notch-Hes pathway in mammalian neural development. Cell Res. 1999, 9:179-188.
23. Kanayasu-Toyoda T., Yamaguchi T., Uchida E., Hayakawa T. Commitment of neutrophilic differentiation and proliferation of HL-60 cells coincides with expression of transferrin receptor. J. Biol. Chem. 1999, 274:25471-25480.
24. Kato H., Taniguchi Y., Kurooka H., Minoguchi S., Sakai T., Nomura-Okazaki S., Tamura K., Honjo T. Involvement of RBP-J in biological functions of mouse Notch1 and its derivatives. Development 1997, 124:4133-4141.
25. Kim J., Lo L., Dormand E., Anderson D.J. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 2003, 38:17-31.
26. Kubota Y., Morita T., Ito K. New monoclonal antibody (4E9R) identifies mouse neural crest cells. Dev. Dyn. 1996, 206:368-378.
27. Kubota Y., Ito K. Chemotactic migration of mesencephalic neural crest cells in the mouse. Dev. Dyn. 2000, 217:170-179.
28. Le Douarin N.M., Kalcheim C. The Neural Crest 1999, Cambridge University Press, Cambridge. second ed.
29. Le Douarin N.M., Dupin E. Multipotentiality of neural crest. Curr. Opin. Genet. Dev. 2003, 13:529-536.
30. Le Lièvre C.S., Le Douarin N.M. Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J. Embryol. Exp. Morphol. 1975, 34:125-154.
31. Lehman J.A., Calvo V., Gomez-Cambronero J. Mechanism of ribosomal p70S6 kinase activation by granulocyte macrophage colony-stimulating factor in neutrophils. J. Biol. Chem. 2003, 278:28130-28138.
32. Maka M., Stolt C.C., Wegner M. Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Dev. Biol. 2005, 277:155-169.
33. Matsuno K., Diederich R.J., Go M.J., Blaumueller C.M., Artavanis-Tsakonas S. Deltex acts as a positive regulator of Notch signaling through interactions with the Notch ankyrin repeats. Development 1995, 121:2633-2644.
34. Miele L., Osborne B. Arbiter of differentiation and death: Notch signaling meets apoptosis. J. Cell. Physiol. 1999, 181:393-409.
35. Mohammadi M., McMahon G., Sun L., Tang C., Hirth P., Yeh B.K., Hubbard S.R., Schlessinger J. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 1997, 276:955.
36. Murakami S., Kan M., Mckeehan W.L., de Crombrugghe B. Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. USA 2000, 97:1113-1118.
37. Nah H.D., Rodgers B.J., Kulyk W.M., Kream B.E., Kosher R.A., Upholt W.B. In situ hybridization analysis of the expression of the type II collagen gene in the developing chick limb bud. Coll. Relat. Res. 1988, 8:277-294.
38. Nakanishi K., Chan Y.S., Ito K. Notch signaling is required for the chondrogenic specification of mouse mesencephalic neural crest cells. Mech. Dev. 2007, 124:190-203.
39. Nye J.S., Kopan R., Axel R. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 1994, 120:2421-2430.
40. Ohtsuka T., Ishibashi M., Gradwohl G., Nakanishi S., Guillemot F., Kageyama R. Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J. 1999, 18:2196-2207.
41. Ota M., Ito K. Induction of neurogenin-1 expression by sonic hedgehog: its role in development of trigeminal sensory neurons. Dev. Dyn. 2003, 227:544-551.
42. Ota M., Ito K. BMP and FGF-2 regulate neurogenin-2 expression and the differentiation of sensory neurons and glia. Dev. Dyn. 2006, 235:646-655.
43. Paumelle R., Tulasne D., Kherrouche Z., Plaza S., Leroy C., Reveneau S., Vandenbunder B., Fafeur V. Hepatocyte growth factor/scatter factor activates the ETS1 transcription factor by a RAS-RAF-MEK-ERK signaling pathway. Oncogene 2002, 21:2309-2319.
44. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 2001, 22:153-183.
45. Peyssonnaux C., Eychène A. The Raf/MEK/ERK pathway: new concepts of activation. Biol. Cell 2001, 93:53-62.
46. s6k. FEBS Lett. 1997, 410:78-82.
47. Röttinger E., Besnardeau L., Lepage T. A Raf/MEK/ERK signaling pathway is required for development of the sea urchin embryo micromere lineage through phosphorylation of the transcription factor Ets. Development 2004, 131:1075-1087.
48. Sarkar S., Petiot A., Copp A., Ferretti P., Thorogood P. FGF2 promotes skeletogenic differentiation of cranial neural crest cells. Development 2001, 128:2143-2152.
49. Sasai Y., Kageyama R., Tagawa Y., Shigemoto R., Nakanishi S. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 1992, 6:2620-2634.
50. Schaeffer H.J., Weber M.J. Mitogen-activated protein kinase: specific messages from ubiquitous messengers. Mol. Cell. Biol. 1999, 19:2435-2444.
51. Stamatovic S.M., Keep R.F., Mostarica-Stojkovic M., Andjelkovic A.V. CCL2 regulates angiogenesis via activation of Ets-1 transcription factor. J. Immunol. 2006, 177:2651-2661.
52. Tahtakran S.A., Selleck M.A. Ets-1 expression is associated with cranial neural crest migration and vasulogenesis in the chick embryo. Gene Expr. Patterns 2003, 3:455-458.
53. Tanaka K., Oda N., Iwasaka C., Abe M., Sato Y. Induction of Ets-1 in endothelial cells during reendothelialization after denuding injury. J. Cell. Physiol. 1998, 176:235-244.
54. Théveneau E., Duband J.L., Altabef M. Ets-1 confers cranial features on neural crest delamination. PLoS One 2007, 2(11):e1142.
55. Tsokas P., Ma T., Iyengar R., Landau E.M., Blitzer R.D. Mitogen-activated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway. J. Neurosci. 2007, 27:5885-5894.
56. Vlahos C.J., Matter W.F., Hui K.Y., Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 1994, 269:5241-5248.
57. Yamamoto N., Yamamoto S., Inagaki F., Kawaichi M., Fukamizu A., Kishi N., Matsuno K., Nakamura K., Weinmaster G., Okano H., Nakafuku M. Role of Deltex-1 as a transcriptional regulator downstream of the Notch receptor. J. Biol. Chem. 2001, 276:45031-45040.
58. Yamamoto-Yamaguchi Y., Okabe-Kado J., Kasukabe T., Honma Y. Induction of differentiation of human myeloid leukemia cells by immunosuppressant macrolides (rapamycin and FK506) and calcium/calmodulin-dependent kinase inhibitors. Exp. Hematol. 2001, 29:582-588.
59. Zahr E., Molano R.D., Pileggi A., Ichii H., Jose S.S., Bocca N., An W., Gonzalez-Quintana J., Fraker C., Ricordi C., Inverardi L. Rapamycin impairs in vivo proliferation of islet beta-cells. Transplantation 2007, 84:1576-1583.
60. S6K following exposure to UVA irradiation. J. Biol. Chem. 2001, 276:20913-20923.