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Expression of Ciona intestinalis variable region-containing chitin-binding proteins during development of the gastrointestinal tract and their role in host-microbe interactions.

Liberti A, Melillo D, Zucchetti I, Natale L, Dishaw LJ, Litman GW, De Santis R, Pinto MR - PLoS ONE (2014)

Bottom Line: The expression of VCBP-A and -C is detected first in discrete areas of larva endoderm and becomes progressively localized during differentiation in the stomach and intestine, marking the development of gut tracts.In "small adults" (1-2 cm juveniles) expression of VCBP-C persists and VCBP-A gradually diminishes, ultimately replaced by expression of VCBP-B.A potential role for VCBPs in gut-microbiota interactions and homeostasis is indicated.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Physiology and Evolution, Stazione Zoologica Anton Dohrn, Villa Comunale, Napoli, Italy.

ABSTRACT
Variable region-containing chitin-binding proteins (VCBPs) are secreted, immune-type molecules that have been described in both amphioxus, a cephalochordate, and sea squirt, Ciona intestinalis, a urochordate. In adult Ciona, VCBP-A, -B and -C are expressed in hemocytes and the cells of the gastrointestinal tract. VCBP-C binds bacteria in the stomach lumen and functions as an opsonin in vitro. In the present paper the expression of VCBPs has been characterized during development using in situ hybridization, immunohistochemical staining and quantitative polymerase chain reaction (qPCR) technologies. The expression of VCBP-A and -C is detected first in discrete areas of larva endoderm and becomes progressively localized during differentiation in the stomach and intestine, marking the development of gut tracts. In "small adults" (1-2 cm juveniles) expression of VCBP-C persists and VCBP-A gradually diminishes, ultimately replaced by expression of VCBP-B. The expression of VCBP-A and -C in stage 7-8 juveniles, at which point animals have already started feeding, is influenced significantly by challenge with either Gram-positive or -negative bacteria. A potential role for VCBPs in gut-microbiota interactions and homeostasis is indicated.

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WISH of VCBP-A and -C at larval stage and at early stages of metamorphosis.In the early-middle swimming larva, VCBP-A (A) and VCBP-C (E) are expressed in the dorsal endodermal cells and in the posterior lateral endoderm, respectively. Cross sections cut at the level of the dotted lines confirm these expression patterns (B and F). At the ER stage VCBP-A (C) and VCBP-C (G) are localized in the intestine disc, with an overlapping pattern. At the BLR stage, VCBP-A (D) is expressed in the primordium of the stomach, and VCBP-C (H) in the primordium of the intestine. NS, nervous system; arrow, sensory organs. (Scale bars: A, C-E, G, H, 50 µm; B and F, 15 µm).
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pone-0094984-g002: WISH of VCBP-A and -C at larval stage and at early stages of metamorphosis.In the early-middle swimming larva, VCBP-A (A) and VCBP-C (E) are expressed in the dorsal endodermal cells and in the posterior lateral endoderm, respectively. Cross sections cut at the level of the dotted lines confirm these expression patterns (B and F). At the ER stage VCBP-A (C) and VCBP-C (G) are localized in the intestine disc, with an overlapping pattern. At the BLR stage, VCBP-A (D) is expressed in the primordium of the stomach, and VCBP-C (H) in the primordium of the intestine. NS, nervous system; arrow, sensory organs. (Scale bars: A, C-E, G, H, 50 µm; B and F, 15 µm).

Mentions: In situ hybridization (ISH) with VCBP-A, -B and -C riboprobes does not detect transcripts in defined territories at the 44-cell, 110-cell, gastrula and tailbud stages (data not shown). At the early-middle larval stage (free swimming larva) (stage 27–28, FABA2 developmental staging, http://chordate.bpni.bio.keio.ac.jp/faba2/2.2/top.html), VCBP-A mRNA is expressed in some dorsal endodermal cells lining the area corresponding to the neck of the nervous system (Fig. 2A and B); slight variations in both extent and intensity are seen, depending on the specimen examined. By contrast, VCBP-C is expressed in the posterior lateral region of endoderm facing the mesenchyme pouches (Fig. 2E and F). The expression patterns can be interpreted further in semi-thin transverse sections in which VCBP-A expression is localized in endodermal cells at the border of the larval nervous system (Fig. 2B), whereas VCBP-C expression is confined to a few more ventrally located cells (Fig. 2F).


Expression of Ciona intestinalis variable region-containing chitin-binding proteins during development of the gastrointestinal tract and their role in host-microbe interactions.

Liberti A, Melillo D, Zucchetti I, Natale L, Dishaw LJ, Litman GW, De Santis R, Pinto MR - PLoS ONE (2014)

WISH of VCBP-A and -C at larval stage and at early stages of metamorphosis.In the early-middle swimming larva, VCBP-A (A) and VCBP-C (E) are expressed in the dorsal endodermal cells and in the posterior lateral endoderm, respectively. Cross sections cut at the level of the dotted lines confirm these expression patterns (B and F). At the ER stage VCBP-A (C) and VCBP-C (G) are localized in the intestine disc, with an overlapping pattern. At the BLR stage, VCBP-A (D) is expressed in the primordium of the stomach, and VCBP-C (H) in the primordium of the intestine. NS, nervous system; arrow, sensory organs. (Scale bars: A, C-E, G, H, 50 µm; B and F, 15 µm).
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4008424&req=5

pone-0094984-g002: WISH of VCBP-A and -C at larval stage and at early stages of metamorphosis.In the early-middle swimming larva, VCBP-A (A) and VCBP-C (E) are expressed in the dorsal endodermal cells and in the posterior lateral endoderm, respectively. Cross sections cut at the level of the dotted lines confirm these expression patterns (B and F). At the ER stage VCBP-A (C) and VCBP-C (G) are localized in the intestine disc, with an overlapping pattern. At the BLR stage, VCBP-A (D) is expressed in the primordium of the stomach, and VCBP-C (H) in the primordium of the intestine. NS, nervous system; arrow, sensory organs. (Scale bars: A, C-E, G, H, 50 µm; B and F, 15 µm).
Mentions: In situ hybridization (ISH) with VCBP-A, -B and -C riboprobes does not detect transcripts in defined territories at the 44-cell, 110-cell, gastrula and tailbud stages (data not shown). At the early-middle larval stage (free swimming larva) (stage 27–28, FABA2 developmental staging, http://chordate.bpni.bio.keio.ac.jp/faba2/2.2/top.html), VCBP-A mRNA is expressed in some dorsal endodermal cells lining the area corresponding to the neck of the nervous system (Fig. 2A and B); slight variations in both extent and intensity are seen, depending on the specimen examined. By contrast, VCBP-C is expressed in the posterior lateral region of endoderm facing the mesenchyme pouches (Fig. 2E and F). The expression patterns can be interpreted further in semi-thin transverse sections in which VCBP-A expression is localized in endodermal cells at the border of the larval nervous system (Fig. 2B), whereas VCBP-C expression is confined to a few more ventrally located cells (Fig. 2F).

Bottom Line: The expression of VCBP-A and -C is detected first in discrete areas of larva endoderm and becomes progressively localized during differentiation in the stomach and intestine, marking the development of gut tracts.In "small adults" (1-2 cm juveniles) expression of VCBP-C persists and VCBP-A gradually diminishes, ultimately replaced by expression of VCBP-B.A potential role for VCBPs in gut-microbiota interactions and homeostasis is indicated.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Physiology and Evolution, Stazione Zoologica Anton Dohrn, Villa Comunale, Napoli, Italy.

ABSTRACT
Variable region-containing chitin-binding proteins (VCBPs) are secreted, immune-type molecules that have been described in both amphioxus, a cephalochordate, and sea squirt, Ciona intestinalis, a urochordate. In adult Ciona, VCBP-A, -B and -C are expressed in hemocytes and the cells of the gastrointestinal tract. VCBP-C binds bacteria in the stomach lumen and functions as an opsonin in vitro. In the present paper the expression of VCBPs has been characterized during development using in situ hybridization, immunohistochemical staining and quantitative polymerase chain reaction (qPCR) technologies. The expression of VCBP-A and -C is detected first in discrete areas of larva endoderm and becomes progressively localized during differentiation in the stomach and intestine, marking the development of gut tracts. In "small adults" (1-2 cm juveniles) expression of VCBP-C persists and VCBP-A gradually diminishes, ultimately replaced by expression of VCBP-B. The expression of VCBP-A and -C in stage 7-8 juveniles, at which point animals have already started feeding, is influenced significantly by challenge with either Gram-positive or -negative bacteria. A potential role for VCBPs in gut-microbiota interactions and homeostasis is indicated.

Show MeSH