McLin VA et al. (2008), Expression of complement components coincides w...

XB-ART-38791

Int J Dev Biol 2008 Jan 01;528:1123-33. doi: 10.1387/ijdb.072465v.

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Expression of complement components coincides with early patterning and organogenesis in Xenopus laevis.

McLin VA , Hu CH , Shah R , Jamrich M .

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The complement system is the central component of innate immunity and an important player in the adaptive immunity of vertebrates. We analyzed the expression patterns of several key members of the complement cascade during Xenopus development. We found extensive expression of these molecules already during gastrula/early neurula stage. Remarkably, several genes also showed an organ-specific expression pattern during early organogenesis. Early expression is notable for two different expression patterns in the neuroectoderm. In one group, there is early strong neural plate and neural precursor expression. This is the case of properdin, C1qA, C3 and C9. The second pattern, seen with C1qR and C6, is noteworthy for its expression at the periphery of the neural plate, in the presumptive neural crest. Two genes stand out for their predominantly mesodermal expression. C3aR, the message for the cognate receptor for C3 in the complement cascade, is expressed at the same time as C3, but in a complementary, reciprocal pattern in the mesoderm. C1qA expression also predominates in somites, pronephros, visceral mesoderm and ventral blood islands. Finally, several genes are characterized by later expression in developing organs. C1qR displays a reticular pattern consistent with expression in the developing vasculature. The late expression of C1qA and C3bC4b is strongest in the pronephros. Finally, the expression of properdin in the hindbrain and in the developing lens are novel findings. The expression patterns of these molecules suggest that these components of the complement system may have in Xenopus a so far undefined developmental role.

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Species referenced: Xenopus laevis
Genes referenced: abcc8 c1qa c3 c3ar1 c9 cd93 cfi cfp tbx2 uqcc6

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	Fig. 1. Developmental expression of C1qA. (A) Bissected gastrula. Dorsal is to the right. Expression is restricted to the marginal zone mesoderm indicated by the arrow;(b) blastpore, (m) mesoderm. (B) Stage 28 embryo. Anterior is to the left and dorsalto the top. There is strong expression in the cephalic structures, especially in the branchial arches (ba) and in the otic vesicle (ov). Expression in the intersomitic veins is visible (isv). Pronephric expression has begun (pr). The small arrows indicate expression in the pronephric duct. (C) Stage 35 embryo shows detailed expression in pronephros (pr) and duct. At this stage, expression in the lateral muscle presursors (small arrows) is visible ventral to the duct. (D) Transverse section through an age- matched embryo to (C). The section is at the level of the pronephros. Dorsal is to the top. Somitic expression is most pronounced in the cells adjacent to the neural tube (nt) as indicated by the small arrows, and in the pronephros (pr). There is no staining in the notochord (n). (E) Ventral view of a stage 35 embryo reveals staining consistent with ventral blood island expression (arrow).
	Fig. 2. Developmental expression of C1qR. Anterior is to the left and dorsal to the top unless otherwise specified. (A) Tailbud embryo. Marked expression in the mandibular seg- ment of the neural crest is indicated (ma). Double arrows indicate punctate ventral staining consistent with early vascular precursor expression. Expression in the dorsal cardinal vein is indicated (dcv). (B) Transverse section through the head of embryo in (A) (solid black line). Dorsal is to the top. The developing mesencephalon or mid-brain is labeled (mb). The small arrow to the right of the figure points to mandibular segment expression, dorsal to the developing eye (e). Expression in the head mesenchyme is shown, onsistent with neural crest expression. (C) Section through the trunk of a tailbud embryo (shown in D). Dorsal is to the top. The dorsal cardinal vein is indicated (dcv). Small struc- tures with a lumen in the lateral plate mesoderm (lpm) are consistent with expression in the developing vessels of vitelline network (vvn); (en) endoderm, (n) notochord. (D) Tailbud embryo showing expression throughout the devel- oping vasculature. In addition to the ventral vitelline net- work, both the common (ccv) and the posterior (pcv) cardinal veins show strong expression. There is some expression in the intersomitic veins as indicated by the small arrow. Expression in the branchial arches is labeled (ba). (E) Expression in the vasculature of the larval gut. The reticular pattern of the developing splanchnic vasculature is indicated in the foregut (f) but visible throughout, including in the liver and pancreatic buds. Expression is strongest in the lung bud. (li) liver, (lu) lung, (pa) pancreas.
	Fig. 3. Developmental expression of C3 from gastrula to organ bud stage. (A) Dorsal view of stage 10 embryo. Anterior is to the top. There is early, punctate expression of C3 in the neuroectoderm (ne); (b) blastopore. (B) Midline view of a bisected gastrula; dorsal is to the right. C3 is expressed in dorsal ectoderm and dorsal mesoderm (m). (C) Dorsal view of stage 13 embryo shows complex expression pattern in and around the neural plate (np). Anterior is to the left. (D) Sagital view of early neurula embryo shows expression in anterior endoderm (ae) and continued expression in neuroectoderm at the top. Anterior is to the left and dorsal to the top. (E) Anterior view of stage 17 embryo showing defined expression in both neural crest (nc) and neural groove (ng). Dorsal is to the top. (F) Frontal section through the embryo in (E) shows gene expression in neural crest (nc). Dorsal is to the top. (G) Stage 27 embryo shows expression in the mandibular and branchial segments of anterior neural crest. Hyoid segment is visible between the mandibular (ma) and branchial segments (br). At this stage there is strong endodermal expression (en). (H) Isolated gut tube from stage 42 embryo shows strong expression in liver and presumptive intestine, with sparing of foregut and pancreas. (f) foregut, (i) presumptive intestine, (li) liver, (lu) lung, (pa) pancreas.
	Fig. 4. Developmental expression of C3aR from gastrula to organ bud stage. (A) Whole mount in situ hybridization on a stage 10 gastrula showing expression predominantly in the marginal zone (mz); (b) blastopore. (B) Bissecting the gastrula revealed that the expression is mesodermal (m). In both (A,B) dorsal is to the right. (C) Stage 25 embryo showing expression in both the branchial segment of the neural crest (br) and in the otic vesicle (ov). Anterior is to the left, dorsal to the top. The arrow indicates early ventral blood island expression (VBI). (D) Stage 32 embryo. In addition to strong expression in cephalic structures, the presumptive liver area (li) is sur- rounded by cells expressing C3aR message. Arrow shows VBI expression. (E) Ventral view of same stage 32 embryo showing detail of VBI expression (arrow); head is to the top. (F) Isolated gut tube showing C3aR expression throughout the foregut (f) and presumptive intestine (i), (pa) pancreas. Anterior is to the left. (G) A section through the presumptive liver area (indicated in D) shows expression in lateral plate meso- derm (lpm) surrounding the anterior endoderm (ae). (H) Section through isolated gut showing staining in visceral mesoderm (vm), surrounding the presumptive intestine.
	Fig. 5 (Left). Developmental expression of C3bC4bi. (A) Anterior view of a neurula stage embryo shows strong expression in the endoderm (en) lateral and ventral to the neural plate (np). (B) Transverse section of an early tailbud embryo in the presumptive trunk area. Dorsal is to the top. Expression is in the peripheral endoderm (large arrow) and in the archenteron roof (small arrow). Double arrows indicate early expression in presumptive kidney domains. (C) Tailbud embryo. Anterior is to the left. Endodermal expression is more extensive although not yet uniform. Expression in branchial arches (ba), the otic vesicle (ov), the pronephros (pr), and the pronephric duct (prd) are indicated. (D) Section through the proximal trunk of a tailbud embryo highlighting strong expression in the developing kidney. Dorsal is to the top; (n) notochord, (s) somite. (E) Isolated larval gut reveals strong expression in presumptive intestine (i) and liver (li), but no expression in foregut (f) and distal most segment of the developing intestine.
	Fig. 6 (Right). Developmental expression of Properdin. Anterior is to the left and dorsal to the top unless otherwise specified. (A) Anterior view of a neurula stage embryo. Arrow indicates neural crest expression. (B) Late neurula/early tadpole stage embryo. Arrows indicate expression in mandibular, hyoid and mandibular segments of anterior neural crest (from anterior to posterior). (C) Tailbud embryo shows strong cephalic expression. Intense expression in developing eye (e) and hindbrain (hb) are indicated. The ventral arrow highlights beginning expression in the anterior endoderm. (D) Cross section through the hindbrain of the embryo in (C). Dorsal is to the top. Expression is limited to the dorsal most part of the neural tube, in the periventricular cells of the hindbrain; (v) ventricle. (E) Section through the developing eye of a tailbud embryo shows strong expression in the lens. Anterior is to the right. (F) In the isolated larval gut expression is confined to the liver bud only (li); (f) foregut, (i) presumptive intestine, (pa) pancreas.
	Fig. 7. Developmental expression of C9 from gastrula to organ bud stage. Anterior is to the left and dorsal to the top unless otherwise indicated. (A) Dorsal view of stage 10 embryo showing early spotted expression dorsal ectoderm. Anterior is to the top. (B) Anterior view of stage 17 embryo showing discrete neural crest (nc) and neural groove expression (ng). (C) Anterior view of stage 19-20 embryo. The three segments of the anterior neural crest show discrete expression at this stage. Mandibular segment ex- pression surrounds the presumptive eye field (e). (D) Lateral view of stage 22 embryo shows expression in mandibular (ma) and branchial segments (br) of anterior migrating neural crest. There is discrete hyoid expression noticeable between those two seg- ments. (E) Stage 27 embryo. Neural crest expression is seen in all three segments, as well as in the otic vesicle (ov), the lens (l), and the endoderm (en). (F) Stage 35 embryo shows strong liver and endodermal expression. (G) Isolated gut tube shows liver (li) and intestinal expression sparing the foregut (f), but no distal intestinal (proctodeum) expression (arrow); (lu) lung, (pa) pancreatic bud.
	cfi (complement factor I) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 14, anterior view, dorsal up.
	cfi (complement factor I) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 28, lateral view, anterior left, dorsal up.
	cfp (complement factor properdin) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 17-18, anterior view, dorsal up.
	cfp (complement factor properdin) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 20, lateral view, anterior left, dorsal up.

	c9 (complement component 9) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 10, anterio-dorsal view, dorsal up.
	c9 (complement component 9) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 17, anterior view, dorsal up.
	c9 (complement component 9) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 19-20, anterior view, dorsal up.
	c9 (complement component 9) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 22, lateral view, anterior left, dorsal up.
	c9 (complement component 9) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 27, anterior left, lateral view, dorsal up.

	c3 (complement component 3) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 10, anterior-dorsal view, dorsal up.
	c3 (complement component 3) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 11.5, mid-sagital section, dorsal right.
	c3 (complement component 3) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 13, dorsal view, anterior left.
	c3 (complement component 3) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 17, anterior view, dorsal up.
	c3 (complement component 3) gene expression in Xenopus laevis embryo via in situ hybridization, NF stage 27, lateral view, anterior left, dorsal right.