Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors

Nature Communications

Volumn 1, Issue 1, 2010, Pages

  Bhattaram, Pallavi ^a   Penzo Méndez, Alfredo ^a   Sock, Elisabeth ^b   Colmenares, Clemencia ^a   Kaneko, Kotaro J ^c   Vassilev, Alex ^c   DePamphilis, Melvin L ^c   Wegner, Michael ^b   Lefebvre, Véronique ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TEAD2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX; TRANSCRIPTION FACTOR SOX11; TRANSCRIPTION FACTOR SOX12; TRANSCRIPTION FACTOR SOX4; UNCLASSIFIED DRUG; SOX11 PROTEIN, MOUSE; SOX12 PROTEIN, MOUSE; SOX4 PROTEIN, MOUSE;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL LINEAGE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; GENE ACTIVATION; GENE INACTIVATION; MESENCHYMAL STEM CELL; MESENCHYME CELL; MOUSE; NERVE CELL; NONHUMAN; ORGANOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CELL CYCLE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; OSTEOBLAST; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL CYCLE; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EMBRYO, MAMMALIAN; MESENCHYMAL STEM CELLS; MICE; NEURONS; ORGANOGENESIS; OSTEOBLASTS; SOXC TRANSCRIPTION FACTORS;

EID: 84873734770     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1008     Document Type: Article

References (58)

1. Bernardo, M. E., Locatelli, F. & Fibbe, W. E. Mesenchymal stromal cells. Ann. NY Acad. Sci. 1 176, 101-117 (2009).
2. Kuhn, N. Z. & Tuan, R. S. Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis. J. Cell. Physiol. 222, 268-277 (2010).
3. Rogers, C. D., Moody, S. A. & Casey, E. S. Neural induction and factors that stabilize a neural fate. Birth Defects Res. C Embryo Today 8 7, 249-262 (2009).
4. Wegner, M. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res. 27, 1409-1420 (1999).
5. Lefebvre, V., Dumitriu, B., Penzo-M é ndez, A., Han, Y. & Pallavi, B. Control of cell fate and diff erentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int. J. Biochem. Cell Biol. 3 9, 2195-2214 (2007).
6. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fi broblast cultures by defi ned factors. Cell 1 26, 663-676 (2006).
7. Sekido, R. & Lovell-Badge, R. Sex determination and SRY: down to a wink and a nudge? T rends Genet. 2 5, 19-29 (2009).
8. Lefebvre, V. & Smits, P. Transcriptional control of chondrocyte fate and diff erentiation. Birth Defects Res. C Embryo Today 75, 200-212 (2005).
9. Francois, M., Koopman, P. & Beltrame, M. SoxF genes: key players in the development of the cardio-vascular system. Int. J. Biochem. Cell. Biol. 42, 445-448 (2010).
10. Penzo-M é ndez, A. I. Critical roles for SoxC transcription factors in development and cancer. Int. J. Biochem. Cell Biol. 42, 425-428 (2010).
11. Dy, P. et al. The three SoxC proteins- Sox4, Sox11 and Sox12-exhibit overlapping expression patterns and molecular properties. Nucleic Acids Res. 36, 3101-3117 (2008).
12. Hoser, M. et al. Sox12 deletion in the mouse reveals nonreciprocal redundancy with the related Sox4 and Sox11 transcription factors. Mol. Cell Biol. 28, 4675-4687 (2008).
13. Hargrave, M. et al. Expression if the Sox11 gene in mouse embryos suggests roles in neuronal maturation and epithelio-mesenchymal induction. D ev. Dyn. 210, 79-86 (1997).
14. Sock, E. et al. Gene targeting reveals a widespread role for the high-mobilitygroup transcription factor Sox11 in tissue remodeling. M ol. Cell Biol. 2 4, 6635-6644 (2004).
15. Schilham, M. W. et al. Defects in cardiac outfl ow tract formation and pro-Blymphocyte expansion in mice lacking Sox-4. Nature 3 80, 711-714 (1996).
16. Schilham, M. W., Moerer, P., Cumano, A. & Clevers, H. C. Sox-4 facilitates thymocyte diff erentiation. Eur. J. Immunol. 2 7, 1292-1295 (1997).
17. Wilson, M. E. et al. The HMG box transcription factor Sox4 contributes to the development of the endocrine pancreas. Diabetes 54, 3402-3409 (2005).
18. Nissen-Meyer, L. S. et al. Osteopenia, decreased bone formation and impaired osteoblast development in Sox4 heterozygous mice. J. Cell Sci. 1 20, 2785-2795 (2007).
19. Bergsland, M., Werme, M., Malewicz, M., Perlmann, T. & Muhr, J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 20, 3475-3486 (2006).
20. Lee, C. J., Appleby, V. J., Orme, A. T., Chan, W. I. & Scotting, P. J. Diff erential expression of SOX4 and SOX11 in medulloblastoma. J. Neurooncol. 57, 201-214 (2002).
21. Weigle, B. et al. Highly specifi c overexpression of the transcription factor SOX11 in human malignant gliomas. Oncol. Rep. 13, 139-144 (2005).
22. Hide, T. et al. Sox11 prevents tumorigenesis of glioma-initiating cells by inducing neuronal diff erentiation. Cancer Res. 69, 7953-7959 (2009).
23. Wang, X. et al. The subcellular Sox11 distribution pattern identifi es subsets of mantle cell lymphoma: correlation to overall survival. B r. J. Haematol. 1 43, 248-252 (2008).
24. Liu, P. et al. Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res. 66, 4011-4019 (2006).
25. Andersen, C. L. et al. Dysregulation of the transcription factors SOX4, CBFB and SMARCC1 correlates with outcome of colorectal cancer. B r. J. Cancer 1 00, 511-523 (2009).
26. Pramoonjago, P., Baras, A. S. & Moskaluk, C. A. Knockdown of Sox4 expression by RNAi induces apoptosis in ACC3 cells. Oncogene 25, 5626-5639 (2006).
27. de Bont, J. M. et al. Diff erential expression and prognostic signifi cance of SOX genes in pediatric medulloblastoma and ependymoma identifi ed by microarray analysis. N euro. Oncol. 1 0, 648-660 (2008).
28. Pan, X. et al. Induction of SOX4 by DNA damage is critical for p53 stabilization and function. Proc. Natl. Acad. Sci USA 1 06, 3788-3793 (2009).
29. Penzo-M é ndez, A., Dy, P., Pallavi, B. & Lefebvre, V. Generation of mice harboring a Sox4 conditional null allele. Genesis 4 5, 776-780 (2007).
30. O'Gorman, S., Dagenais, N. A., Qian, M. & Marchuk, Y Protamine-Cre recombinase transgenes effi ciently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl. Acad. Sci. USA 94, 14602-14607 (1997).
31. De Vries, W. N. et al. Expression of Cre recombinase in mouse oocytes: a means to study maternal eff ect genes. G enesis 2 6, 110-112 (2000).
32. Ahn, K., Mishina, Y., Hanks, M. C., Behringer, R. R. & Crenshaw, E. B. III. BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development 1 28, 4449-4461 (2001).
33. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. & McMahon, A. P. Modifi cation of gene activity in mouse embryos in utero by a tamoxifeninducible form of Cre recombinase. C urr. Biol. 8, 1323-1326 (1998).
34. Mao, X., Fujiwara, Y. & Orkin, S. H. Improved reporter strain for monitoring Cre recombinase-mediated DNA excisions in mice. Proc. Natl. Acad. Sci. USA 96, 5037-5042 (1999).
35. Logan, M. et al. Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80 (2002).
36. Zhao, B., Lei, Q.-Y. & Guan, K.-L. The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr. Opin. Cell Biol. 2 0, 638-646 (2008).
37. Kaneko, K. J., Kohn, M. J., Liu, C. & DePamphilis, M. L. Transcription factor TEAD2 is involved in neural tube closure. Genesis 4 5, 577-587 (2007).
38. Sawada, A. et al. Redundant roles of Tead1 and Tead2 in notochord development and the regulation of cell proliferation and survival. Mol. Cell. Biol. 2 8, 3177-3189 (2008).
39. Vassilev, A., Kaneko, K. J., Shu, H., Zhao, Y. & DePamphilis, M. L. TEAD/ TEF transcription factors utilize the activation domain of YAP65, a Src/Yesassociated protein localized in the cytoplasm. Genes Dev. 15, 1229-1241 (2001).
40. Avilion, A. A. et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 1 7, 126-140 (2003).
41. Masui, S. et al. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat. Cell Biol. 9, 625-635 (2007).
42. Ikushima, H. et al. Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell 5, 504-514 (2009).
43. Hoser, M. et al. Prolonged glial expression of Sox4 in the CNS leads to architectural cerebellar defects and ataxia. J. Neurosci. 2 7, 5495-5505 (2007).
44. Potzner, M. R. et al. Prolonged Sox4 expression in oligodendrocytes interferes with normal myelination in the central nervous system. Mol. Cell. Biol. 27, 5316-5326 (2007).
45. Kondoh, H. & Kamachi, Y. SOX-partner code for cell specifi cation: Regulatory target selection and underlying molecular mechanisms. Int. J. Biochem. Cell. Biol. 4 2, 391-399 (2010).
46. Liao, Y.-L. et al. Identifi cation of SOX4 target genes using phylogenetic footprinting-based prediction from expression microarrays suggests that overexpression of SOX4 potentiates metastasis in hepatocellular carcinoma. Oncogene 2 7, 5578-5589 (2008).
47. Cheah, S. S. & Behringer, R. R. Contemporary gene targeting strategies for the novice. Mol. Biotechnol. 1 9, 297-304 (2001).
48. Meyers, E. N., Lewandoski, M. & Martin, G. R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. N at. Genet. 1 8, 136-141 (1998).
49. Hogan, B., Beddington, R., Costantini, F. & Lacy, E. Manipulating the Mouse Embryo: A Laboratory Manual 2nd edn. 373-375 (Cold Spring Harbor Laboratory Press, 1994).
50. Albrecht, U., Eichele, G., Helms, J. A. & Lu, H. C. V isualization of Gene Expression Patterns by In Situ Hybridization. In Molecular and Cellular Methods in Developmental Toxicology (ed. Daston, G.P.) 23-48 (CRC Press, Boca Raton, FL, 1997).
51. Ducy, P. et al. A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. G enes Dev. 13, 1025-1036.
52. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(- Delta Delta C(T)). M ethods 2 5, 402-408 (2001).
53. Kuschert, S., Rowitch, D. H., Haenig, B., McMahon, A. P. & Kispert, A. Characterization of Pax-2 regulatory sequences that direct transgene expression in the Wolffi an duct and its derivatives. D ev. Biol. 2 29, 128-140 (2001).
54. Ott, M. O., Bober, E., Lyons, G., Arnold, H. & Buckingham, M. Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 1 11, 1097-1107 (1991).
55. Echelard, Y. et al. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 7 5, 1417-1430 (1993).
56. Sawada, A. et al. Tead proteins activate the Foxa2 enhancer in the node in cooperation with a second factor. D evelopment 1 32, 4719-4729 (2005).
57. Caballero, R. et al. Combinatorial eff ects of splice variants modulate function of Aiolos. J. Cell Sci. 120, 2619-2630 (2007).
58. Han, Y. & Lefebvre, V. L-Sox5 and Sox6 drive expression of the aggrecan gene in cartilage by securing binding of Sox9 to a far-upstream enhancer. Mol. Cell Biol. 2 8, 4999-5013 (2008).