Koestner U et al. (2008), Semaphorin and neuropilin expression during ear...

XB-ART-38759

Dev Dyn 2008 Dec 01;23712:3853-63. doi: 10.1002/dvdy.21785.

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Semaphorin and neuropilin expression during early morphogenesis of Xenopus laevis.

Koestner U , Shnitsar I , Linnemannstöns K , Hufton AL , Borchers A .

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Semaphorins are major regulators of morphogenesis and are involved in a variety of processes ranging from the guidance of cell migration to the development of cancer. Since semaphorins were first characterized as repulsive neuronal guidance cues, their expression has been best documented in the nervous system. However, broader studies are lacking. Here, we describe the expression of 13 members of the semaphorin family and two neuropilin receptors during early Xenopus laevis development. No particular expression pattern defines any of the semaphorin classes, but many are dynamically expressed in distinct areas undergoing morphogenetic cell movements like the developing mesoderm and the migrating neural crest. Furthermore, the complementary expression patterns of Sema3A/Nrp1 and Sema3F/Nrp2 are maintained across hundreds of millions of years, possibly indicating a conserved role in the guidance of migrating neural crest cells.

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Species referenced: Xenopus laevis
Genes referenced: egr2 nrp1 nrp2 sema3a sema3c sema3d sema3f sema3fl sema4a sema4b sema4c sema4d sema4g sema5b sema6a sema6b sema6d twist1

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	Figure 2. Expression of class-3 semaphorins in Xenopus laevis. Gastrula, neurula, and tadpole stage Xenopus laevis embryos were analyzed by whole mount in situ hybridization. Rows represent the expression pattern of the semaphorin indicated at the left side. Columns show different stages of Xenopus laevis development. Gastrula stage 11-12 embryos are shown with the dorsal side up. Neurula stage 14-15 and the left panel of neurula stage 16-19 embryos are shown from the dorsal side. The right panel of stage 16-19 neurula embryos presents an anterior view of the embryo shown at left. ba, branchial arches; e, eye; h, heart; m, somitogenic mesoderm; mh, midbrain hindbrain boundary; nt, neural tube; no, notochord; s, somites; sm, splanchnic mesoderm.
	Figure 3. Expression of class-4 semaphorins in Xenopus laevis. ba, branchial arches; cg, cement gland; e, eye; h, heart; m, somitogenic mesoderm; nt, neural tube; no, notochord; p, pronephros; pcv, posterior cardial vein; pnc, premigratory neural crest cells.
	Figure 4. Expression of Sema5B and the class-6 semaphorins in Xenopus laevis. ba, branchial arches; e, eye; no, notochord; op, otic placode; p, pronephros; pnc, premigratory neural crest cells; s, somites.
	Figure 5. Semaphorin expression in the mesoderm and notochord during neurula stages. A-G: Neurula stage embryos were stained by in situ hybridization and transversally sectioned. Left: Whole embryo, dashed line indicates the plane of the transverse section. Right: Enlargement of the neural tube area of the transverse section. A: Sema3A is expressed in the somitogenic mesoderm. B: Sema4B expression delineates the boundaries of the somitogenic mesoderm. C: Sema6B is expressed in the somitogenic mesoderm. D: Sema3F is expressed in the notochord as well as the spinal cord anlage and the archenteron roof. E-G: Sema4C, Sema4D, and Sema5B are expressed in the notochord. arc, archenteron roof cells; m, somitogenic mesoderm; no, notochord; sca, spinal cord anlage.
	Figure 6. Semaphorin expression in the mesoderm and notochord at tadpole stages. In situ hybridization of the whole embryo (left), dashed line indicates the plane of the transverse section (right). A: Sema3A is expressed in the somites and the splanchnic mesoderm. B: Sema4B expression in the mesoderm is replaced by pronephros, cement gland, otic placode, proctodeum, spinal cord, and gut expression. C: Sema6B is expressed in the somites and otic placode at late neurula stages. D: At tadpole stages, the somite expression is limited to the dorsal and lateral margins of the somites (white arrow). E: Sema3F expression is detected in the notochord, but also in the spinal cord, the hypochord, the posterior endoderm, and the branchial arches. F: Sema4C notochord expression is replaced by expression in the posterior cardinal vein, the heart, and the branchial arches. G: Sema4D expression is detected in the notochord. H: Sema5B expression in the notochord is replaced by spinal cord, pronephros, brain, and eye expression. ba, branchial arches; cg, cement gland; en, endoderm; g, gut; h, heart; hc, hypochord; no, notochord; op, otic placode; p, pronephros; pcv, posterior cardinal vein; pd, proctodeum; s, somites; sc, spinal cord; sm, splanchnic mesoderm.
	Figure 7. Semaphorins are expressed in close proximity to migrating cranial neural crest cells. In situ hybridization of tadpole-stage embryos; enlargements of the head are shown. Red arrows indicate migrating neural crest cells, white arrows indicate neurogenic placodes. A: Sema3A expression. Staining in the midbrain hindbrain boundary was confirmed by double in situ hybridization with engrailed (data not shown). B: Sema3C expression. C: Sema3D expression. D: Sema3F expression. Double in situ hybridization using Krox20 or engrailed antisense probes was used to confirm staining in the rhombomeres or the midbrain hindbrain boundary, respectively (data not shown and Q). E: Sema4A expression. F: Sema4B expression. G: Sema4C expression. H: Sema4G expression. I: Sema5B expression. K: Sema6A expression. L: Sema6B expression. M: Sema6D expression. N: Sema3A expression at early tadpole stage. O: Double in situ hybridization using a Sema3A (blue) and a twist (red) antisense probe at tadpole stage. Sema3A expression is localized posterior to the migrating twist-expressing neural crest cells (black arrow). P: For comparison twist expression at tadpole stage is shown. Q: Double in situ hybridization showing Sema3F (blue) expression adjacent to the anterior portion of the migrating Krox20-expressing (red) neural crest cells (black arrow). cg, cement gland; e, eye; mh, midbrain hindbrain boundary; op, otic placode; r3, rhombomere 3; r5, rhombomere 5.
	Figure 8. Neuropilin expression pattern in Xenopus laevis. A: Nrp1 expression at neurula stage, dorsal view of the embryo. B: Anterior view of A. C: Nrp1 expression in the posterior branchial arches at late neurula stage. D: Nrp1 expression at the tadpole stage. E: Higher magnification of the head shown in D. F: Nrp2 expression at the neurula stage. G: Anterior view of F. H: Nrp2 expression at late neurula stage. I: Nrp2 expression at tadpole stage. K: Higher magnification of the head shown in I. L: Schematic representation of the Sema3A/Nrp1 expression and the Sema3F/Nrp2 expression (M) of a stage-28 tadpole embryo. N: Transverse section through the trunk region of an Nrp1-expressing tadpole stage embryo. O: Transverse section showing somitic expression of Nrp2 in a tadpole stage embryo. P: Schematic picture of the Nrp1/Sema3A and Nrp2/Sema3F co-expression in a transverse section of the trunk of a tadpole-stage embryo. ba, branchial arches; cg, cement gland; en, endoderm; hc, hypochord; hy, hyoidal neural crest cells; ma, mandibular neural crest cells; mh, midbrain hindbrain boundary; nt, neural tube; no, notochord; pnc, premigratory neural crest cells; r3, rhombomere 3; r5, rhombomere 5; s, somites; sc, spinal cord.
	nrp2 (neurophillin 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 20, dorsal view, anterior up,
	sema4g (sema domain, immunoglobulin domain (Ig), transmembrane domain (TM) and short cytoplasmic domain, (semaphorin) 4G) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 30, lateral view, head region anterior right, dorsal up
	sema3a (semaphorin 3A) gene expression in Xenopus laevis embryos, NF stage 14 - 15, as assayed by in situ hybridization, dorsal view, anterior up.
	sema3a (ssemaphorin 3A) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, anterior view, dorsal up.
	sema3a (semaphorin 3A) gene expression in Xenopus laevis embryos, NF stage 23-27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema3a (semaphorin 3A) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema3c (semaphorin 3C) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, dorsal view, anterior up.
	sema3c (semaphorin 3C) gene expression in Xenopus laevis embryos, NF stage 23 - 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema3c (semaphorin 3C) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema3d (semaphorin 3D) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, anterior view, dorsal up.
	sema3d (semaphorin 3D) gene expression in Xenopus laevis embryos, NF stage 23 -27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema3d (semaphorin 3D) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema3f (semaphorin 3F like) gene expression in Xenopus laevis embryos, NF stage 14 - 15, as assayed by in situ hybridization, dorsal view, anterior up.
	sema3f (semaphorin 3F like) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, anterior view, dorsal up.
	sema3f (semaphorin 3F like) gene expression in Xenopus laevis embryos, NF stage 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema3fl (semaphorin 3F like) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4a (sema domain, immunoglobulin domain (Ig), short basic domain, secreted, (semaphorin) 4A) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, dorsal view, dorsal up.
	sema4a ( sema domain, immunoglobulin domain (Ig), transmembrane domain (TM) and short cytoplasmic domain, (semaphorin) 4A) gene expression in Xenopus laevis embryos, NF stage 23 - 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4a (sema domain, immunoglobulin domain (Ig), transmembrane domain (TM) and short cytoplasmic domain, (semaphorin) 4A) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4B (semaphorin 4B) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, anterior view, dorsal up.
	sema4B (semaphorin 4B) gene expression in Xenopus laevis embryos, NF stage 23 - 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4B (semaphorin 4B) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4C (semaphorin 4C) gene expression in Xenopus laevis embryos, NF stage 11 - 12, as assayed by in situ hybridization, vegetal view, dorsal up.
	sema4C (semaphorin 4C) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, dorsal view, anterior up.
	sema4C (semaphorin 4C) gene expression in Xenopus laevis embryos, NF stage 23 - 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4C (semaphorin 4C) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4d (semaphorin 4D) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, dorsal view, anterior up.
	sema4d (semaphorin 4D) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema4g (semaphorin 4G) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema5b (semaphorin 5B) gene expression in Xenopus laevis embryos, NF stage 11 - 12, as assayed by in situ hybridization, vegetal view, dorsal up.
	sema5b (semaphorin 5B) gene expression in Xenopus laevis embryos, NF stage 14 - 15, as assayed by in situ hybridization, dorsal view, anterior up.
	sema5b (semaphorin 5B) gene expression in Xenopus laevis embryos, NF stage 23 - 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema5b (semaphorin 5B) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema6a (semaphorin 6A) gene expression in Xenopus laevis embryos, NF stage 16 - 19, as assayed by in situ hybridization, dorsal view, anterior up.
	sema6a (semaphorin 6A) gene expression in Xenopus laevis embryos, NF stage 23 - 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema6a (semaphorin 6A) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema6b (sema domain, transmembrane domain (TM), and cytoplasmic domain, (semaphorin) 6B) gene expression in Xenopus laevis embryos, NF stage 23 - 27, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema6b (sema domain, transmembrane domain (TM), and cytoplasmic domain, (semaphorin) 6B) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.
	sema6d (semaphorin 6D) gene expression in Xenopus laevis embryos, NF stage 11 - 12, as assayed by in situ hybridization, vegetal view, dorsal up.
	sema6d (semaphorin 6D) gene expression in Xenopus laevis embryos, NF stage 28 - 32, as assayed by in situ hybridization, lateral view, anterior right, dorsal up.