An essential role for transcription before the MBT in Xenopus laevis

Developmental Biology

Volumn 357, Issue 2, 2011, Pages 478-491

  Skirkanich, Jennifer ^a   Luxardi, Guillaume ^b   Yang, Jing ^c   Kodjabachian, Laurent ^b   Klein, Peter S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CNRS   (France)

^c NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

Mesoderm; Midblastula transition (MBT); Nodal; Smad; VegT; Zygotic gene activation (ZGA)

Indexed keywords

CHORDIN; ENDODERMIN; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN BIX4; PROTEIN DERRIERE; PROTEIN NODAL; PROTEIN SOX17ALPHA; PROTEIN XNR5; PROTEIN XNR6; SMAD2 PROTEIN; SMAD3 PROTEIN; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR VEGT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE ACTIVATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GERM LAYER; MESENDODERM; MIDBLASTULA TRANSITION; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; XENOPUS LAEVIS;

DANIO RERIO; XENOPUS LAEVIS;

EID: 80052174584     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.06.010     Document Type: Article

References (79)

1. Agius E., Oelgeschläger M., Wessely O., Kemp C., De Robertis E.M. Endodermal Nodal-related signals and mesoderm induction in Xenopus. Development 2000, 127:1173-1183.
2. Akkers R.C., van Heeringen S.J., Jacobi U.G., Janssen-Megens E.M., Françoijs K.-J., Stunnenberg H.G., Veenstra G.J.C. A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev. Cell 2009, 17:425-434.
3. Andeol Y. Early transcription in different animal species: implication for transition from maternal to zygotic control in development. Roux's Arch. Dev. Biol. 1994, 204:3-10.
4. Bachvarova R., Davidson E.H., Allfrey V.G., Mirsky A.E. Activation of RNA synthesis associated with gastrulation. Proc. Natl. Acad. Sci. U. S. A. 1966, 55:358-365.
5. Birsoy B., Kofron M., Schaible K., Wylie C., Heasman J. Vg 1 is an essential signaling molecule in Xenopus development. Development 2006, 133:15-20.
6. Blythe S.A., Cha S.-W., Tadjuidje E., Heasman J., Klein P.S. β-catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. Dev. Cell 2010, 19:1-12.
7. Christian J.L., Moon R.T. Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. Genes Dev. 1993, 7:13-28.
8. Clegg K.B., Pikó L. RNA synthesis and cytoplasmic polyadenylation in the one-cell mouse embryo. Nature 1982, 295:343-344.
9. DaCosta Byfield S., Major C., Laping N.J., Roberts A.B. SB-505124 is a selective inhibitor of transforming growth factor-beta type I receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 2004, 65:744-752.
10. Darken R.S., Wilson P.A. Axis induction by wnt signaling: target promoter responsiveness regulates competence. Dev. Biol. 2001, 234:42-54.
11. Davidson E.H. Gene Activity in Early Development 1986, Academic Press. 3 ed.
12. De Renzis S., Elemento O., Tavazoie S., Wieschaus E.F. Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol. 2007, 5:e117.
13. Ding X., Hausen P., Steinbeisser H. Pre-MBT patterning of early gene regulation in Xenopus: the role of the cortical rotation and mesoderm induction. Mech. Dev. 1998, 70:15-24.
14. Dunican D.S., Ruzov A., Hackett J.A., Meehan R.R. xDnmt1 regulates transcriptional silencing in pre-MBT Xenopus embryos independently of its catalytic function. Development 2008, 135:1295-1302.
15. Edgar B.A., Schubiger G. Parameters controlling transcriptional activation during early Drosophila development. Cell 1986, 44:871-877.
16. Eimon P.M., Harland R.M. Effects of heterodimerization and proteolytic processing on Derrière and Nodal activity: implications for mesoderm induction in Xenopus. Development 2002, 129:3089-3103.
17. Faure S., Lee M.A., Keller T., ten Dijke P., Whitman M. Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development. Development 2000, 127:2917-2931.
18. Harrison M.M., Botchan M.R., Cline T.W. Grainyhead and Zelda compete for binding to the promoters of the earliest-expressed Drosophila genes. Dev. Biol. 2010, 345:248-255.
19. Heasman J., Kofron M., Wylie C. Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev. Biol. 2000, 222:124-134.
20. Heasman J., Wessely O., Langland R., Craig E.J., Kessler D.S. Vegetal localization of maternal mRNAs is disrupted by VegT depletion. Dev. Biol. 2001, 240:377-386.
21. Henry G.L., Melton D.A. Mixer, a homeobox gene required for endoderm development. Science 1998, 281:91-96.
22. Horb M.E., Thomsen G.H. A vegetally localized T-box transcription factor in Xenopus eggs specifies mesoderm and endoderm and is essential for embryonic mesoderm formation. Development 1997, 124:1689-1698.
23. Houston D.W., Kofron M., Resnik E., Langland R., Destree O., Wylie C., Heasman J. Repression of organizer genes in dorsal and ventral Xenopus cells mediated by maternal XTcf3. Development 2002, 129:4015-4025.
24. Howard L., Rex M., Clements D., Woodland H.R. Regulation of the Xenopus Xsox17alpha(1) promoter by co-operating VegT and Sox17 sites. Dev. Biol. 2007, 310:402-415.
25. Hudson C., Clements D., Friday R.V., Stott D., Woodland H.R. Xsox17alpha and -beta mediate endoderm formation in Xenopus. Cell 1997, 91:397-405.
26. Inman G.J., Nicolás F.J., Callahan J.F., Harling J.D., Gaster L.M., Reith A.D., Laping N.J., Hill C.S. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 2002, 62:65-74.
27. Jones E.A., Woodland H.R. Development of the ectoderm in Xenopus: tissue specification and the role of cell association and division. Cell 1986, 44:345-355.
28. Jones C.M., Kuehn M.R., Hogan B.L., Smith J.C., Wright C.V. Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. Development 1995, 121:3651-3662.
29. Kimelman D. On the fast track to organizer gene expression. Dev. Cell 2010, 19:190-192.
30. Kimelman D., Griffin K.J. Mesoderm induction: a postmodern view. Cell 1998, 94:419-421.
31. Kimelman D., Kirschner M., Scherson T. The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 1987, 48:399-407.
32. Kofron M., Demel T., Xanthos J., Lohr J., Sun B., Sive H., Osada S., Wright C., Wylie C., Heasman J. Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFbeta growth factors. Development 1999, 126:5759-5770.
33. Kofron M., Wylie C., Heasman J. The role of Mixer in patterning the early Xenopus embryo. Development 2004, 131:2431-2441.
34. Lee M.A., Heasman J., Whitman M. Timing of endogenous activin-like signals and regional specification of the Xenopus embryo. Development 2001, 128:2939-2952.
35. Leung T., Bischof J., Söll I., Niessing D., Zhang D., Ma J., Jäckle H., Driever W. Bozozok directly represses bmp2b transcription and mediates the earliest dorsoventral asymmetry of bmp2b expression in zebrafish. Development 2003, 130:3639-3649.
36. Liang H.-L., Nien C.-Y., Liu H.-Y., Metzstein M.M., Kirov N., Rushlow C. The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 2008, 456:400.
37. Luxardi G., Marchal L., Thome V., Kodjabachian L. Distinct Xenopus Nodal ligands sequentially induce mesendoderm and control gastrulation movements in parallel to the Wnt/PCP pathway. Development 2010, 137:417-426.
38. Marchal L., Luxardi G., Thome V., Kodjabachian L. BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17437-17442.
39. Mathavan S., Lee S.G.P., Mak A., Miller L.D., Murthy K.R.K., Govindarajan K.R., Tong Y., Wu Y.L., Lam S.H., Yang H., Ruan Y., Korzh V., Gong Z., Liu E.T., Lufkin T. Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet. 2005, 1:260-276.
40. Nakakura N., Miura T., Yamana K., Ito A., Shiokawa K. Synthesis of heterogeneous mRNA-like RNA and low-molecular-weight RNA before the midblastula transition in embryos of Xenopus laevis. Dev. Biol. 1987, 123:421-429.
41. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 1982, 30:675-686.
42. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 1982, 30:687-696.
43. Nieuwkoop P., Faber J. Normal Table of Xenopus laevis (Daudin) 1994, Garland Publishing Inc., New York.
44. Osada S.I., Saijoh Y., Frisch A., Yeo C.Y., Adachi H., Watanabe M., Whitman M., Hamada H., Wright C.V. Activin/nodal responsiveness and asymmetric expression of a Xenopus nodal-related gene converge on a FAST-regulated module in intron 1. Development 2000, 127:2503-2514.
45. Porcher A., Abu-Arish A., Huart S., Roelens B., Fradin C., Dostatni N. The time to measure positional information: maternal hunchback is required for the synchrony of the bicoid transcriptional response at the onset of zygotic transcription. Development 2010, 137:2795-2804.
46. Pritchard D.K., Schubiger G. Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev. 1996, 10:1131-1142.
47. Rex M., Hilton E., Old R. Multiple interactions between maternally-activated signalling pathways control Xenopus nodal-related genes. Int. J. Dev. Biol. 2002, 46:217-226.
48. Rosa A., Spagnoli F.M., Brivanlou A.H. The miR-430/427/302 family controls mesendodermal fate specification via species-specific target selection. Dev. Cell 2009, 16:517-527.
49. Saka Y., Hagemann A.I., Piepenburg O., Smith J.C. Nuclear accumulation of Smad complexes occurs only after the midblastula transition in Xenopus. Development 2007, 134:4209-4218.
50. Sampath K., Cheng A.M., Frisch A., Wright C.V. Functional differences among Xenopus nodal-related genes in left-right axis determination. Development 1997, 124:3293-3302.
51. Sasai Y., Lu B., Steinbeisser H., Geissert D., Gont L.K., De Robertis E.M. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 1994, 79:779-790.
52. Sasai Y., Lu B., Piccolo S., De Robertis E.M. Endoderm induction by the organizer-secreted factors chordin and noggin in Xenopus animal caps. EMBO J. 1996, 15:4547-4555.
53. Schohl A., Fagotto F. Beta-catenin, MAPK and Smad signaling during early Xenopus development. Development 2002, 129:37-52.
54. Shen M.M. Nodal signaling: developmental roles and regulation. Development 2007, 134:1023-1034.
55. Sible J.C., Anderson J.A., Lewellyn A.L., Maller J.L. Zygotic transcription is required to block a maternal program of apoptosis in Xenopus embryos. Dev. Biol. 1997, 189:335-346.
56. Sive H.L., Grainger R.M., Harland R.M. Early Development of Xenopus Laevis: a Laboratory Manual 2000, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
57. Sive H.L., Grainger R.M., Harland R.M. Animal cap Isolation from Xenopus laevis. Cold Spring Harb. Protoc. 2007, 10.1101/pdb.prot4744.
58. Smith J.C., Price B.M., Green J.B., Weigel D., Herrmann B.G. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 1991, 67:79-87.
59. Stennard F., Zorn A.M., Ryan K., Garrett N., Gurdon J.B. Differential expression of VegT and Antipodean protein isoforms in Xenopus. Mech. Dev. 1999, 86:87-98.
60. Sun B.I., Bush S.M., Collins-Racie L.A., LaVallie E.R., DiBlasio-Smith E.A., Wolfman N.M., McCoy J.M., Sive H.L. derrière: a TGF-beta family member required for posterior development in Xenopus. Development 1999, 126:1467-1482.
61. Tadros W., Lipshitz H.D. The maternal-to-zygotic transition: a play in two acts. Development 2009, 136:3033-3042.
62. Takahashi S., Yokota C., Takano K., Tanegashima K., Onuma Y., Goto J., Asashima M. Two novel nodal-related genes initiate early inductive events in Xenopus Nieuwkoop center. Development 2000, 127:5319-5329.
63. Takahashi S., Onuma Y., Yokota C., Westmoreland J.J., Asashima M., Wright C.V.E. Nodal-related gene Xnr5 is amplified in the Xenopus genome. Genesis 2006, 44:309-321.
64. Taneyhill L.A., Adams M.S. Investigating regulatory factors and their DNA binding affinities through real time quantitative PCR (RT-QPCR) and chromatin immunoprecipitation (ChIP) assays. Methods Cell Biol. 2008, 87:367-389.
65. ten Bosch J.R., Benavides J.A., Cline T.W. The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 2006, 133:1967-1977.
66. Tracey W.D., Ning X., Klingler M., Kramer S.G., Gergen J.P. Quantitative analysis of gene function in the Drosophila embryo. Genetics 2000, 154:273-284.
67. Vastenhouw N.L., Zhang Y., Woods I.G., Imam F., Regev A., Liu X.S., Rinn J., Schier A.F. Chromatin signature of embryonic pluripotency is established during genome activation. Nature 2010, 464:922-926.
68. Veenstra G.J. Early embryonic gene transcription in Xenopus. Adv. Dev. Biol. Biochem. 2002, 12:85-105.
69. Watabe T., Nishihara A., Mishima K., Yamashita J., Shimizu K., Miyazawa K., Nishikawa S.-I., Miyazono K. TGF-beta receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J. Cell Biol. 2003, 163:1303-1311.
70. Weeks D.L., Melton D.A. A maternal mRNA localized to the vegetal hemisphere in Xenopus eggs codes for a growth factor related to TGF-beta. Cell 1987, 51:861-867.
71. Whitman M. Nodal signaling in early vertebrate embryos: themes and variations. Dev. Cell 2001, 1:605-617.
72. Wylie C., Kofron M., Payne C., Anderson R., Hosobuchi M., Joseph E., Heasman J. Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos. Development 1996, 122:2987-2996.
73. Xanthos J.B., Kofron M., Wylie C., Heasman J. Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 2001, 128:167-180.
74. Xanthos J.B., Kofron M., Tao Q., Schaible K., Wylie C., Heasman J. The roles of three signaling pathways in the formation and function of the Spemann Organizer. Development 2002, 129:4027-4043.
75. Yang J., Tan C., Darken R.S., Wilson P.A., Klein P.S. Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. Development 2002, 129:5743-5752.
76. Yasuo H., Lemaire P. A two-step model for the fate determination of presumptive endodermal blastomeres in Xenopus embryos. Curr. Biol. 1999, 9:869-879.
77. Yasuo H., Lemaire P. Role of Goosecoid, Xnot and Wnt antagonists in the maintenance of the notochord genetic programme in Xenopus gastrulae. Development 2001, 128:3783-3793.
78. Zhang J., Houston D.W., King M.L., Payne C., Wylie C., Heasman J. The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 1998, 94:515-524.
79. Zorn A.M., Wells J.M. Molecular basis of vertebrate endoderm development. Int. Rev. Cytol. 2007, 259:49-111.