Mesogenin 1 is a master regulator of paraxial presomitic mesoderm differentiation

Development (Cambridge)

Volumn 141, Issue 22, 2014, Pages 4285-4297

  Chalamalasetty, Ravindra B ^a   Garriock, Robert J ^a   Dunty, William C ^a   Kennedy, Mark W ^a   Jailwala, Parthav ^b   Si, Han ^b   Yamaguchi, Terry P ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

bHLH transcription factor; Differentiation; Embryonic stem cell; EMT; Motility; Mouse; Paraxial mesoderm; PSM; Somite; Wnt

Indexed keywords

MESOGENIN 1; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; LUCIFERASE; MSGN1 PROTEIN, MOUSE; WNT3A PROTEIN; WNT3A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; EMBRYO; MESODERM; MOUSE; NEURAL TUBE; NONHUMAN; NOTOCHORD; NUCLEOTIDE SEQUENCE; PARAXIAL PRESOMITIC MESODERM; PROGENY; STEM CELL; ZEBRA FISH; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; EMBRYOLOGY; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; METABOLISM; MICROARRAY ANALYSIS; NERVOUS SYSTEM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUCIFERASES; MESODERM; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MUSCLE, SKELETAL; NERVOUS SYSTEM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WNT3A PROTEIN;

EID: 84908406776     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.110908     Document Type: Article

References (52)

1. Barrallo-Gimeno, A. and Nieto, M. A. (2005). The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132, 3151-3161.
2. Batlle, E., Sancho, E., Francí, C., Domínguez, D., Monfar, M., Baulida, J. and García De Herreros, A. (2000). The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89.
3. Belteki, G., Haigh, J., Kabacs, N., Haigh, K., Sison, K., Costantini, F., Whitsett, J., Quaggin, S. E. and Nagy, A. (2005). Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction. Nucleic Acids Res. 33, e51.
4. Biris, K. K. and Yamaguchi, T. P. (2014). Two-color in situ hybridization of wholemount mouse embryos. Methods Mol. Biol. 1092, 17-30.
5. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O. and Kemler, R. (2001). Inactivation of the betacatenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264.
6. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S. and Brabletz, T. (2008).Areciprocal repression between ZEB1 andmembers of the miR- 200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589.
7. Cambray, N. and Wilson, V. (2007). Two distinct sources for a population of maturing axial progenitors. Development 134, 2829-2840.
8. Cano, A., Pérez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F. and Nieto, M. A. (2000). The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83.
9. Chalamalasetty, R. B., Dunty, W. C., Jr, Biris, K. K., Ajima, R., Iacovino, M., Beisaw, A., Feigenbaum, L., Chapman, D. L., Yoon, J. K., Kyba, M. et al. (2011). The Wnt3a/beta-catenin target gene Mesogenin1 controls the segmentation clock by activating a Notch signalling program. Nat. Commun. 2, 390.
10. Chapman, D. L. and Papaioannou, V. E. (1998). Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature 391, 695-697.
11. Dale, J. K., Malapert, P., Chal, J., Vilhais-Neto, G., Maroto, M., Johnson, T., Jayasinghe, S., Trainor, P., Herrmann, B. and Pourquié, O. (2006). Oscillations of the snail genes in the presomitic mesoderm coordinate segmental patterning and morphogenesis in vertebrate somitogenesis. Dev. Cell 10, 355-366.
12. De Craene, B. and Berx, G. (2013). Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer 13, 97-110.
13. Dequéant, M. L. and Pourquié, O. (2008). Segmental patterning of the vertebrate embryonic axis. Nat. Rev. Genet. 9, 370-382.
14. Dodd, J., Jessell, T. M. and Placzek, M. (1998). The when and where of floor plate induction. Science 282, 1654-1657.
15. Dunty, W. C., Jr, Biris, K. K., Chalamalasetty, R. B., Taketo, M. M., Lewandoski, M. and Yamaguchi, T. P. (2008). Wnt3a/beta-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 135, 85-94.
16. Dunty, W. C., Jr, Kennedy, M. W. L., Chalamalasetty, R. B., Campbell, K. and Yamaguchi, T. P. (2014). Transcriptional profiling of Wnt3a mutants identifies Sp transcription factors as essential effectors of the Wnt/beta-catenin pathway in neuromesodermal stem cells. PLoS ONE 9, e87018.
17. Eckert, M. A., Lwin, T. M., Chang, A. T., Kim, J., Danis, E., Ohno-Machado, L. and Yang, J. (2011). Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 19, 372-386.
18. Ema, M., Takahashi, S. and Rossant, J. (2006). Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors. Blood 107, 111-117.
19. Esteban, M. A., Bao, X., Zhuang, Q., Zhou, T., Qin, B. and Pei, D. (2012). The mesenchymal-to-epithelial transition in somatic cell reprogramming. Curr. Opin. Genet. Dev. 22, 423-428.
20. Fior, R., Maxwell, A. A., Ma, T. P., Vezzaro, A., Moens, C. B., Amacher, S. L., Lewis, J. and Saude, L. (2012). The differentiation and movement of presomitic mesoderm progenitor cells are controlled by Mesogenin 1. Development 139, 4656-4665.
21. Fong, A. P., Yao, Z., Zhong, J. W., Cao, Y., Ruzzo, W. L., Gentleman, R. C. and Tapscott, S. J. (2012). Genetic and epigenetic determinants of neurogenesis and myogenesis. Dev. Cell 22, 721-735.
22. Fujimoto, H. and Yanagisawa, K. O. (1979). Effect of the T-mutation on histogenesis of the mouse embryo under the testis capsule. J. Embryol. Exp. Morphol. 50, 21-30.
23. Galceran, J., Farinas, I., Depew, M. J., Clevers, H. and Grosschedl, R. (1999). Wnt3a-/–like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev. 13, 709-717.
24. Guaita, S., Puig, I., Franci, C., Garrido, M., Dominguez, D., Batlle, E., Sancho, E., Dedhar, S., de Herreros, A. G. and Baulida, J. (2002). Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J. Biol. Chem. 277, 39209-39216.
25. Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M. and Taketo, M. M. (1999). Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942.
26. Iacovino, M., Bosnakovski, D., Fey, H., Rux, D., Bajwa, G., Mahen, E., Mitanoska, A., Xu, Z. and Kyba, M. (2011). Inducible cassette exchange: a rapid and efficient system enabling conditional gene expression in embryonic stem and primary cells. Stem Cells 29, 1580-1588.
27. Jones, S. (2004). An overview of the basic helix-loop-helix proteins. Genome Biol. 5, 226.
28. Lim, J. and Thiery, J. P. (2012). Epithelial-mesenchymal transitions: insights from development. Development 139, 3471-3486.
29. Lindsley, R. C., Gill, J. G., Murphy, T. L., Langer, E. M., Cai, M., Mashayekhi, M., Wang, W., Niwa, N., Nerbonne, J. M., Kyba, M. et al. (2008). Mesp1 coordinately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell 3, 55-68.
30. McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M. and Bejerano, G. (2010). GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501.
31. Mugford, J. W., Sipilä, P., McMahon, J. A. and McMahon, A. P. (2008). Osr1 expression demarcates a multi-potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1-dependent nephron progenitor compartment within the mammalian kidney. Dev. Biol. 324, 88-98.
32. Nicolas, J. F., Mathis, L., Bonnerot, C. and Saurin, W. (1996). Evidence in the mouse for self-renewing stem cells in the formation of a segmented longitudinal structure, the myotome. Development 122, 2933-2946.
33. Nowotschin, S., Ferrer-Vaquer, A., Concepcion, D., Papaioannou, V. E. and Hadjantonakis, A.-K. (2012). Interaction of Wnt3a, Msgn1 and Tbx6 in neural versus paraxial mesoderm lineage commitment and paraxial mesoderm differentiation in the mouse embryo. Dev. Biol. 367, 1-14.
34. Palmer, M. B., Majumder, P., Green, M. R.,Wade,P. A. and Boss, J.M. (2007). A 3′ enhancer controls snail expression in melanomacells. CancerRes. 67, 6113-6120.
35. Perantoni, A. O., Timofeeva, O., Naillat, F., Richman, C., Pajni-Underwood, S., Wilson, C., Vainio, S., Dove, L. F. and Lewandoski, M. (2005). Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development 132, 3859-3871.
36. Sakurai, H., Era, T., Jakt, L. M., Okada, M., Nakai, S., Nishikawa, S. and Nishikawa, S.-I. (2006). In vitro modeling of paraxial and lateral mesoderm differentiation reveals early reversibility. Stem Cells 24, 575-586.
37. Soriano, P. (1997). The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124, 2691-2700.
38. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
39. Takada, S., Stark, K. L., Shea, M. J., Vassileva, G., McMahon, J. A. and McMahon, A. P. (1994). Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8, 174-189.
40. Takebe, A., Era, T., Okada, M., Jakt, L. M., Kuroda, Y. and Nishikawa, S.-I. (2006). Microarray analysis of PDGFR alpha+ populations in ES cell differentiation culture identifies genes involved in differentiation of mesoderm and mesenchyme including ARID3b that is essential for development of embryonic mesenchymal cells. Dev. Biol. 293, 25-37.
41. Takemoto, T., Uchikawa, M., Yoshida, M., Bell, D. M., Lovell-Badge, R., Papaioannou, V. E. and Kondoh, H. (2011). Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470, 394-398.
42. Tzouanacou, E., Wegener, A., Wymeersch, F. J., Wilson, V. and Nicolas, J.-F. (2009). Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev. Cell 17, 365-376.
43. Wehn, A. K. and Chapman, D. L. (2010). Tbx18 and Tbx15 null-like phenotypes in mouse embryos expressing Tbx6 in somitic and lateral plate mesoderm. Dev. Biol. 347, 404-413.
44. Whiting, J., Marshall, H., Cook, M., Krumlauf, R., Rigby, P. W., Stott, D. and Allemann, R. K. (1991). Multiple spatially specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression. Genes Dev. 5, 2048-2059.
45. Wilkinson, D. G., Bhatt, S. and Herrmann, B. G. (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657-659.
46. Wilson, V., Olivera-Martinez, I. and Storey, K. G. (2009). Stem cells, signals and vertebrate body axis extension. Development 136, 1591-1604.
47. Wittler, L., Shin, E.-H., Grote, P., Kispert, A., Beckers, A., Gossler, A., Werber, M. and Herrmann, B. G. (2007). Expression of Msgn1 in the presomitic mesoderm is controlled by synergism of WNT signalling and Tbx6. EMBO Rep. 8, 784-789.
48. Yabe, T. and Takada, S. (2012). Mesogenin causes embryonic mesoderm progenitors to differentiate during development of zebrafish tail somites. Dev. Biol. 370, 213-222.
49. Yamaguchi, T. P., Takada, S., Yoshikawa, Y., Wu, N. and McMahon, A. P. (1999). T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 13, 3185-3190.
50. Yoon, J. K. and Wold, B. (2000). The bHLH regulator pMesogenin1 is required for maturation and segmentation of paraxial mesoderm. Genes Dev. 14, 3204-3214.
51. Yoon, J. K., Moon, R. T. and Wold, B. (2000). The bHLH class protein pMesogenin1 can specify paraxial mesoderm phenotypes. Dev. Biol. 222, 376-391.
52. Yoshikawa, Y., Fujimori, T., McMahon, A. P. and Takada, S. (1997). Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse. Dev. Biol. 183, 234-242.