The Sox axis, Nodal signaling, and germ layer specification

Differentiation

Volumn 75, Issue 6, 2007, Pages 536-545

  Zhang, Chi ^a   Klymkowsky, Michael W ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Asymmetry; Embryogenesis; Germ layers; Nodal; Sox proteins; TGF ; Xenopus laevis

Indexed keywords

PROTEIN NODAL; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX3; TRANSCRIPTION FACTOR SOX7;

ANIMAL TISSUE; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; FEMALE; GENE INDUCTION; GERM LAYER; MESODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; TRANSCRIPTION REGULATION; XENOPUS LAEVIS;

DEUTEROSTOMIA; GASTROPODA; METAZOA; XEMA; XENOPUS (GENUS); XENOPUS LAEVIS;

EID: 34447344269     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2007.00190.x     Document Type: Article

References (92)

1. Agius, E., Oelgeschlager, M., Wessely, O., Kemp, C. De Robertis, E.M. (2000) Endodermal Nodal-related signals and mesoderm induction in Xenopus. Development 127 : 1173 1183.
2. Alexander, J. Stainier, D.Y. (1999) A molecular pathway leading to endoderm formation in zebrafish. Curr Biol 9 : 1147 1157.
3. Ambrosetti, D.C., Basilico, C. Dailey, L. (1997) Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on protein-protein interactions facilitated by a specific spatial arrangement of factor binding sites. Mol Cell Biol 17 : 6321 6329.
4. Angerer, L.M., Newman, L.A. Angerer, R.C. (2005) SoxB1 downregulation in vegetal lineages of sea urchin embryos is achieved by both transcriptional repression and selective protein turnover. Development 132 : 999 1008.
5. Argenton, F., Giudici, S., Deflorian, G., Cimbro, S., Cotelli, F. Beltrame, M. (2004) Ectopic expression and knockdown of a zebrafish sox21 reveal its role as a transcriptional repressor in early development. Mech Dev 121 : 131 142.
6. Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N. Lovell-Badge, R. (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17 : 126 140.
7. Bachant, J.B. (1993) Assembly and dynamics of keratin intermediate filaments in Xenopus laevis oocytes. University of Colorado, Boulder.
8. Bachant, J.B. Klymkowsky, M.W. (1996) The identification of a supratetrameric species as the major soluble form of keratin in Xenopus oocytes and rabbit reticulocyte lysates. J Cell Biol 132 : 153 165.
9. Bell, E., Munoz-Sanjuan, I., Altmann, C.R., Vonica, A. Brivanlou, A.H. (2003) Cell fate specification and competence by Coco, a maternal BMP, TGFbeta and Wnt inhibitor. Development 130 : 1381 1389.
10. Bowles, J., Schepers, G. Koopman, P. (2000) Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227 : 239 255.
11. Boyer, L.A., Lee, T.I., Cole, M.F., Johnstone, S.E., Levine, S.S., Zucker, J.P., Guenther, M.G., Kumar, R.M., Murray, H.L., Jenner, R.G., Gifford, D.K., Melton, D.A., Jaenisch, R Young, R.A. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122 : 947 956.
12. Brennan, J., Lu, C.C., Norris, D.P., Rodriguez, T.A., Beddington, R.S. Robertson, E.J. (2001) Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411 : 965 969.
13. Camus, A., Perea-Gomez, A., Moreau, A. Collignon, J. (2006) Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev Biol 295 : 743 755.
14. Cao, Y., Siegel, D. Knochel, W. (2006) Xenopus POU factors of subclass V inhibit activin/nodal signaling during gastrulation. Mech Dev 123 : 614 625.
15. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. Smith, A. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113 : 643 655.
16. Chen, C., Ware, S.M., Sato, A., Houston-Hawkins, D.E., Habas, R., Matzuk, M.M., Shen, M.M. Brown, C.W. (2006) The Vg1-related protein Gdf3 acts in a Nodal signaling pathway in the pre-gastrulation mouse embryo. Development 133 : 319 329.
17. Clements, D., Friday, R.V. Woodland, H.R. (1999) Mode of action of VegT in mesoderm and endoderm formation. Development 126 : 4903 4911.
18. Clements, D. Woodland, H.R. (2003) VegT induces endoderm by a self-limiting mechanism and by changing the competence of cells to respond to TGF-beta signals. Dev Biol 258 : 454 463.
19. Dent, J.A., Cary, R.B., Bachant, J.B., Domingo, A. Klymkowsky, M.W. (1992) Host cell factors controlling vimentin organization in the Xenopus oocyte. J Cell Biol 119 : 855 866.
20. Duboc, V. Lepage, T. (2006) A conserved role for the nodal signaling pathway in the establishment of dorso-ventral and left-right axes in deuterostomes. J Exp Zool B Mol Dev Evol. doi :.
21. Duboc, V., Rottinger, E., Besnardeau, L. Lepage, T. (2004) Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 6 : 397 410.
22. Dupont, S., Zacchigna, L., Cordenonsi, M., Soligo, S., Adorno, M., Rugge, M. Piccolo, S. (2005) Germ-layer specification and control of cell growth by Ectodermin, a Smad4 ubiquitin ligase. Cell 121 : 87 99.
23. Engleka, M.J., Craig, E.J. Kessler, D.S. (2001) VegT activation of Sox17 at the midblastula transition alters the response to nodal signals in the vegetal endoderm domain. Dev Biol 237 : 159 172.
24. Girard, F., Cremazy, F., Berta, P. Renucci, A. (2001) Expression pattern of the Sox31 gene during zebrafish embryonic development. Mech Dev 100 : 71 73.
25. Gurdon, J.B. Byrne, J.A. (2003) The first half-century of nuclear transplantation. Proc Natl Acad Sci USA 100 : 8048 8052.
26. Hilton, E., Rex, M. Old, R. (2003) VegT activation of the early zygotic gene Xnr5 requires lifting of Tcf-mediated repression in the Xenopus blastula. Mech Dev 120 : 1127 1138.
27. Hinkley, C.S., Martin, J.F., Leibham, D. Perry, M. (1992) Sequential expression of multiple POU proteins during amphibian early development. Mol Cell Biol 12 : 638 649.
28. Hudson, C., Clements, D., Friday, R.V., Stott, D. Woodland, H.R. (1997) Xsox17a and -b mediate endoderm formation in Xenopus. Cell 91 : 397 405.
29. Hwang, C.K., Wu, X., Wang, G., Kim, C.S. Loh, H.H. (2003) Mouse mu opioid receptor distal promoter transcriptional regulation by SOX proteins. J Biol Chem 278 : 3742 3750.
30. James, D., Levine, A.J., Besser, D. Hemmati-Brivanlou, A. (2005) TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132 : 1273 1282.
31. Joseph, E.M. Melton, D.A. (1997) Xnr4: a Xenopus nodal-related gene expressed in the Spemann organizer. Dev Biol 184 : 367 372.
32. Kanai-Azuma, M., Kanai, Y., Gad, J.M., Tajima, Y., Taya, C., Kurohmaru, M., Sanai, Y., Yonekawa, H., Yazaki, K. Tam, P.P., et al 2002) Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129 : 2367 2379.
33. Kenny, A.P., Kozlowski, D., Oleksyn, D.W., Angerer, L.M. Angerer, R.C. (1999) SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres. Development 126 : 5473 5483.
34. Kenny, A.P., Oleksyn, D.W., Newman, L.A., Angerer, R.C. Angerer, L.M. (2003) Tight regulation of SpSoxB factors is required for patterning and morphogenesis in sea urchin embryos. Dev Biol 261 : 412 425.
35. Kloc, M., Wilk, K., Vargas, D., Shirato, Y., Bilinski, S. Etkin, L.D. (2005) Potential structural role of non-coding and coding RNAs in the organization of the cytoskeleton at the vegetal cortex of Xenopus oocytes. Development 132 : 3445 3457.
36. Klymkowsky, M.W., Maynell, L.A. Nislow, C. (1991) Cytokeratin phosphorylation, cytokeratin filament severing and the solubilization of the maternal mRNA Vg1. J Cell Biol 114 : 787 797.
37. Klymkowsky, M.W., Maynell, L.A. Polson, A.G. (1987) Polar asymmetry in the organization of the cortical cytokeratin system of Xenopus laevis oocytes and embryos. Development 100 : 543 557.
38. Kofron, M., Demel, T., Xanthos, J., Lohr, J., Sun, B., Sive, H., Osada, S., Wright, C., Wylie, C. Heasman, J. (1999) Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFbeta growth factors. Development 126 : 5759 5770.
39. Kumano, G. Smith, W.C. (2002) The nodal target gene Xmenf is a component of an FGF-independent pathway of ventral mesoderm induction in Xenopus. Mech Dev 118 : 45 56.
40. Kuroda, T., Tada, M., Kubota, H., Kimura, H., Hatano, S.Y., Suemori, H., Nakatsuji, N. Tada, T. (2005) Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 25 : 2475 2485.
41. Loose, M. Patient, R.K. (2004) A genetic regulatory network for Xenopus mesendodermal formation. Dev Biol 271 : 467 478.
42. Lowe, C.J., Wu, M., Salic, A., Evans, L., Lander, E., Stange-Thomann, N., Gruber, C.E., Gerhart, J. Kirschner, M. (2003) Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113 : 853 865.
43. Lu, C.C. Robertson, E.J. (2004) Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning. Dev Biol 273 : 149 159.
44. Matsui, T., Kanai-Azuma, M., Hara, K., Matoba, S., Hiramatsu, R., Kawakami, H., Kurohmaru, M., Koopman, P. Kanai, Y. (2006) Redundant roles of Sox17 and Sox18 in postnatal angiogenesis in mice. J Cell Sci 119 : 3513 3526.
45. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M. Yamanaka, S. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113 : 631 642.
46. Mukherjee, A., Melnattur, K.V., Zhang, M. Nambu, J.R. (2006) Maternal expression and function of the Drosophila sox gene Dichaete during oogenesis. Dev Dyn 235 : 2828 2835.
47. Murakami, A., Shen, H., Ishida, S. Dickson, C. (2004) SOX7 and GATA-4 are competitive activators of Fgf-3 transcription. J Biol Chem 279 : 28564 28573.
48. Nambu, P.A. Nambu, J.R. (1996) The Drosophila fish-hook gene encodes a HMG domain protein essential for segmentation and CNS development. Development 122 : 3467 3475.
49. Nieuwkoop, P.D. Faber, J. (1967) Normal table of Xenopus laevis (Daudin). North-Holland Publishing Company, Amsterdam.
50. Ohe, K., Lalli, E. Sassone-Corsi, P. (2002) A direct role of SRY and SOX proteins in pre-mRNA splicing. Proc Natl Acad Sci USA 99 : 1146 1151.
51. Okumura-Nakanishi, S., Saito, M., Niwa, H. Ishikawa, F. (2005) Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J Biol Chem 280 : 5307 5317.
52. Onuma, Y., Takahashi, S., Yokota, C. Asashima, M. (2002) Multiple nodal-related genes act coordinately in Xenopus embryogenesis. Dev Biol 241 : 94 105.
53. Parisi, S., D'Andrea, D., Lago, C.T., Adamson, E.D., Persico, M.G. Minchiotti, G. (2003) Nodal-dependent Cripto signaling promotes cardiomyogenesis and redirects the neural fate of embryonic stem cells. J Cell Biol 163 : 303 314.
54. Pennisi, D., Bowles, J., Nagy, A., Muscat, G. Koopman, P. (2000a) Mice null for sox18 are viable and display a mild coat defect. Mol Cell Biol 20 : 9331 9336.
55. Pennisi, D., Gardner, J., Chambers, D., Hosking, B., Peters, J., Muscat, G., Abbott, C. Koopman, P. (2000b) Mutations in Sox18 underlie cardiovascular and hair follicle defects in ragged mice. Nat Genet 24 : 434 437.
56. Penzel, R., Oschwald, R., Chen, Y., Tacke, L. Grunz, H. (1997) Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int J Dev Biol 41 : 667 677.
57. Pfendler, K.C., Catuar, C.S., Meneses, J.J. Pedersen, R.A. (2005) Overexpression of Nodal promotes differentiation of mouse embryonic stem cells into mesoderm and endoderm at the expense of neuroectoderm formation. Stem Cell Dev 14 : 162 172.
58. Rodda, D.J., Chew, J.L., Lim, L.H., Loh, Y.H., Wang, B., Ng, H.H. Robson, P. (2005) Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280 : 24731 24737.
59. Russell, S.R., Sanchez-Soriano, N., Wright, C.R. Ashburner, M. (1996) The Dichaete gene of Drosophila melanogaster encodes a SOX-domain protein required for embryonic segmentation. Development 122 : 3669 3676.
60. Sasai, Y., Lu, B., Piccolo, S. De Robertis, E.M. (1996) Endoderm induction by the organizer-secreted factors chordin and noggin in Xenopus animal caps. EMBO J 15 : 4547 4555.
61. Schepers, G.E., Teasdale, R.D. Koopman, P. (2002) Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell 3 : 167 170.
62. Schier, A.F. (2003) Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol 19 : 589 621.
63. Shivdasani, R.A. (2002) Molecular regulation of vertebrate early endoderm development. Dev Biol 249 : 191 203.
64. Sinner, D., Rankin, S., Lee, M. Zorn, A.M. (2004) Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 131 : 3069 3080.
65. Sive, H.L., Grainger, R.M. Harland, R.M. (2000) Early development of Xenopus laevis: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
66. Smith, J.C., Price, B.M., Green, J.B., Weigel, D. Herrmann, B.G. (1991) Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67 : 79 87.
67. Stennard, F., Carnac, G. Gurdon, J.B. (1996) The Xenopus T-box gene, Antipodean, encodes a vegetally localised maternal mRNA and can trigger mesoderm formation. Development 122 : 4179 4188.
68. Stennard, F., Zorn, A.M., Ryan, K., Garrett, N. Gurdon, J.B. (1999) Differential expression of VegT and Antipodean protein isoforms in Xenopus. Mech Dev 86 : 87 98.
69. Suri, C., Haremaki, T. Weinstein, D.C. (2005) Xema, a foxi-class gene expressed in the gastrula stage Xenopus ectoderm, is required for the suppression of mesendoderm. Development 132 : 2733 2742.
70. Tada, S., Era, T., Furusawa, C., Sakurai, H., Nishikawa, S., Kinoshita, M., Nakao, K., Chiba, T. Nishikawa, S. (2005) Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132 : 4363 4374.
71. Takahashi, S., Yokota, C., Takano, K., Tanegashima, K., Onuma, Y., Goto, J. Asashima, M. (2000) Two novel nodal-related genes initiate early inductive events in Xenopus Nieuwkoop center. Development 127 : 5319 5329.
72. Taniguchi, K., Hiraoka, Y., Ogawa, M., Sakai, Y., Kido, S. Aiso, S. (1999) Isolation and characterization of a mouse SRY-related cDNA, mSox7. Biochim Biophys Acta 1445 : 225 231.
73. Vallier, L., Reynolds, D. Pedersen, R.A. (2004) Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway. Dev Biol 275 : 403 421.
74. Waddington, C.H. (1957) The strategy of the genes. George Allen & Unwin, London.
75. Wardle, F.C. Smith, J.C. (2004) Refinement of gene expression patterns in the early Xenopus embryo. Development 131 : 4687 4696.
76. Wegner, M. Stolt, C.C. (2005) From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci 28 : 583 588.
77. Weng, W. Stemple, D.L. (2003) Nodal signaling and vertebrate germ layer formation. Birth Defects Res Part C Embryo Today 69 : 325 332.
78. Whitfield, T.T., Heasman, J. Wylie, C.C. (1995) Early embryonic expression of XLPOU-60, a Xenopus POU-domain protein. Dev Biol 169 : 759 769.
79. Williams, D.C. Jr., Cai, M. Clore, G.M. (2004) Molecular basis for synergistic transcriptional activation by Oct1 and Sox2 revealed from the solution structure of the 42-kDa Oct1.Sox2.Hoxb1-DNA ternary transcription factor complex. J Biol Chem 279 : 1449 1457.
80. Xanthos, J.B., Kofron, M., Wylie, C. Heasman, J. (2001) Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128 : 167 180.
81. Yamamoto, M., Saijoh, Y., Perea-Gomez, A., Shawlot, W., Behringer, R.R., Ang, S.L., Hamada, H. Meno, C. (2004) Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428 : 387 392.
82. Yang, J., Tan, C., Darken, R.S., Wilson, P.A. Klein, P.S. (2002) Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. Development 129 : 5743 5752.
83. Young, N., Hahn, C.N., Poh, A., Dong, C., Wilhelm, D., Olsson, J., Muscat, G.E., Parsons, P., Gamble, J.R. Koopman, P. (2006) Effect of disrupted SOX18 transcription factor function on tumor growth, vascularization, and endothelial development. J Natl Cancer Inst 98 : 1060 1067.
84. Yuan, H., Corbi, N., Basilico, C. Dailey, L. (1995) Developmental- specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 9 : 2635 2645.
85. Zamparini, A.L., Watts, T., Gardner, C.E., Tomlinson, S.R., Johnston, G.I. Brickman, J.M. (2006) Hex acts with beta-catenin to regulate anteroposterior patterning via a Groucho-related co-repressor and Nodal. Development 133 : 3709 3722.
86. Zhang, C., Basta, T., Fawcett, S.R. Klymkowsky, M.W. (2005a) SOX7 is an immediate-early target of VegT and regulates Nodal expression in Xenopus. Dev Biol 278 : 526 541.
87. Zhang, C., Basta, T., Hernandez-Lagunas, L., Simpson, P., Stemple, D.L., Artinger, K.B. Klymkowsky, M.W. (2004) Repression of nodal expression by maternal B1-type SOXs regulates germ layer formation in Xenopus and zebrafish. Dev Biol 273 : 23 37.
88. Zhang, C., Basta, T., Jensen, E.D. Klymkowsky, M.W. (2003) The beta-catenin/VegT-regulated early zygotic gene Xnr5 is a direct target of SOX3 regulation. Development 130 : 5609 5624.
89. Zhang, C., Basta, T. Klymkowsky, M.W. (2005b) SOX7 and SOX18 are essential for cardiogenesis in Xenopus. Dev Dyn 234 : 878 891.
90. Zhang, C., Carl, T.F., Trudeau, E.D., Simmet, T. Klymkowsky, M.W. (2006) An NF-kappaB and slug regulatory loop active in early vertebrate mesoderm. PLoS ONE 1 : e106.
91. Zhang, J., Houston, D.W., King, M.L., Payne, C., Wylie, C. Heasman, J. (1998) The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 94 : 515 524.
92. Zorn, A.M., Barish, G.D., Williams, B.O., Lavender, P., Klymkowsky, M.W. Varmus, H.E. (1999) Regulation of Wnt signaling by Sox proteins: XSox17 alpha/beta and XSox3 physically interact with beta-catenin. Mol Cell 4 : 487 498.