Koga M et al. (2012), High cell-autonomy of the anterior endomesoderm...

XB-ART-45957

Dev Growth Differ 2012 Sep 01;547:717-29. doi: 10.1111/j.1440-169X.2012.01372.x.

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High cell-autonomy of the anterior endomesoderm viewed in blastomere fate shift during regulative development in the isolated right halves of four-cell stage Xenopus embryos.

Koga M , Nakashima T , Matsuo S , Takeya R , Sumimoto H , Sakai M , Kageura H .

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The isolated right half (RH) or left half (LH) of Xenopus embryos can undergo regulation so as to form well-proportioned larvae. To assess how the combined actions of maternal determinants and cell-cell interactions contribute to form the well-proportioned larvae, we quantitatively compared four-cell stage blastomere fate between normal larvae and regulated larvae from RH embryos. In normal larvae, the clones of the right dorsal blastomere (RD) and right ventral blastomere (RV) were located unilaterally. In contrast, in regulated larvae: (i) the RD clone exclusively occupied the anterior endomesoderm (AE) derivatives, coinciding no RV progeny in those derivatives of normal larvae. The clone bilaterally populated tissues along the dorsal midline, which characteristically included the medial regions of both somites adjoining the notochord, with higher percentages on the right and anterior sides. (ii) The RV clone extensively compensated for the missing left side at the expense of its right side contribution, and bilaterally occupied the ventroposterior and also dorsal regions excluding the AE derivatives. This clone considerably populated, with altered orientations, the derivatives of the left half gastrocoel roof plate (GRP), the left half GRP being essential for laterality determination. These results show that the high cell-autonomy in the AE constitutes a mechanism common to both normal and regulative development. In regulated larvae, cell-cell interactions shifted the midlines on the dorsal side slightly and the ventral side to a greater extent. The cell lineage difference in the left half GRP could result in a different utilization of maternal determinants in that area.

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Species referenced: Xenopus laevis
Genes referenced: fubp1 gopc nos1 nos3 tbx2

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	Fig. 1. Nomenclature of the blastomeres and embryos receiving a tracer injection. (a, b) Graphical representation of the animal pole view of a right half (RH) embryo (a) and a normal embryo (b) at the four-cell stage, and the nomenclature of the right blastomeres. (c, d) Animal pole views of a right dorsal blasto- mere-labeled RH embryo (c; RH-RD) and a right dorsal blasto- mere-labeled whole (normal) embryo (d; W-RD) at the eight-cell stage. The orientations are the same in all of the embryos. D, dorsal; L, left; R, right; RD, right dorsal blastomere; RV, right ventral blastomere; V, ventral.
	Fig. 2. Representative distributions of the labeled blastomere progeny in the ectoderm of regulated right half (RH) and normal embryos at the late gastrula or early neurula stage. (a, c) A right dorsal blastomere-labeled regulated embryo (RH-RD) at stage (St.) 13. (b, d) A right dorsal blastomere-labeled whole (normal) embryo (W-RD) at St. 15. (e, g) A right ventral blastomere-labeled regulated embryo (RH-RV) at St. 15 and 14. (f, h) A right ventral blastomere-labeled whole embryo (W-RV) at St. 18 and 17. The dashed lines indicate the margin of the neural plate or the top of the neural fold. Embryos are viewed from the anterior (a, b, e, f) and dorsal (c, d, g, h) sides. A, anterior; L, left; P, posterior; R, right.
	Fig. 3. The completely patterned tailbud larvae and analyzed levels by transverse sectioning. (a�d) External views of a com- pletely patterned (dorsoanterior index (DAI) 5, Kao & Elinson 1988) identical RH-RD tailbud larva (a, c; stage 27) and an identi- cal W-RD larva (b, d; stage 26). Note that the fluorescence derives from not only the epidermis but also the inner tissues, due to the thinness of the epidermis at this stage. The magnifica- tion in a�d is the same, and the samples are viewed from the right side (a, b) and left side (c, d). (e) Levels of transverse sec- tions analyzed along the anteroposterior axis. The numbered sec- tions cut through the following tissues or locations: 1, telencephalon; 2, diencephalon, pharyngeal endoderm anterior to the first visceral pouch; 3, retina, cement gland, mesencephalon, first visceral pouch; 4, ear vesicle, rhombencephalon, heart; 5, pronephric anlage, liver; 6, 7, 8, the intervals between sections 5 and 9 are all the same; 9, anus; 10, the position halfway between Nos. 9 and 11; 11, chordoneural hinge. The abbrevia- tions for the larvae are the same as in Figures 1 and 2.
	Fig. 4. Section images showing representative distributions of the labeled blastomere progeny in regulated and normal tailbud larvae. (a�f) RH-RD. (g�l) RH-RV. (m�r) W-RD. (s�x) W-RV. The numbers on the uppermost line indicate the analyzed section levels (Fig. 3). The right and the left sides in the panels coincide with those in the embryos, with the dorsal being the top and the ventral the bottom. The abbreviations for the larvae are the same as in Figures 1 and 2.
	Fig. 5. Averaged distribution maps of the blastomere clones in regulated and normal tailbud larvae. The gradation in blue or red indi- cates the population percentage of the RD or RV clone (the right upper corner of the figure). The numbers on the upper line indicate the analyzed section levels (Fig. 3). The rectangles in the upper right corner of the panels, at levels 5�10, show the magnified tissues around the hypochord. The abbreviations at the left end of the panel lines and the orientations of the embryos in the panels are the same as in Figures 1, 2, and 4, respectively. ha, heart anlage; hm, head mesenchyme; hy, hypochord; l, liver; n, notochord; p, pronephric anlage; s, somite.
	Fig. 6. Distribution of the right ventral blastomere progeny in the notochord and hypochord of regulated and normal larvae. (a�d) The labeled progeny distribution in RH-RV. In the notochord, the RV descendants are distributed in the ventral (a, level 9), right (b, level 6), center and left (c, level 6) regions in three independent larvae, but are not seen in another larva (d, level 6). In the hypo- chord, a descendant cell is seen in (a) and (b), but not in (c) and (d). (e, f) The labeled progeny distribution in an identical W-RV. In the notochord, no RV descendent is seen in either section. In the hypochord, a descendant cell is seen at level 8 (e), but not at level 7 (f). The abbreviations and orientations of the larvae are the same as in Figures 1, 2, and 4, respectively.
	Fig. 7. The putative prospective midlines and distribution of the right blastomere clones on the gastrocoel roof in RH embryos and normal embryos. The densities of the blue and red dots represent the cell-percentages of the RD and RV clones. The left and right half of the panels in the two panel lines show an RH embryo (a) or a regulated RH embryo (c, d), and normal embryos (b, e, f), respectively. (a, b) Animal views of the four-cell stage embryos. The prospective dorsal and ventral midlines are represented with the blue and red arrowheads. (c�f) The gastrocoel roof at stage 15, cut transversely into anterior (c, e) and posterior (d, f) parts. Prospective tissues in the fate maps (Shook et al. 2004; permission from Elsevier) were colored only in normal embryo (e, f): the gastrocoel roof plate (GRP) con- sists of the prospective regions for the ventral part of the notochord (magenta), the hypochord (gray), and the medial ventral cells of the somites (yellow). The lateral endodermal crests (LECs) (yellow green) that derived from the supra-blastoporal endoderm and the endo- derm that originated from the sub-blastoporal region (green) serially flank the GRP. At later stage, the prospective hypochord segments fuse in the ventral position to the notochord (Fig. 5, rectangles), and LECs form the most dorsal regions in the yolky endoderm on both sides. A, anterior; D, dorsal; L, left; P, posterior; R, right; V, ventral.