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Gene expression profiles of FABP genes in protochordates, Ciona intestinalis and Branchiostoma belcheri

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Abstract

Fatty-acid-binding proteins (FABPs) are small intracellular proteins associated with the transportation of fatty acids. Members of the FABPs share similar amino acid sequences and tertiary structures and form, together with a member of the cellular retinol-binding proteins (CRBPs), the intracellular-lipid-binding protein (iLBP) family. In vertebrates, several types of FABP have been isolated and classified into three subfamilies: 2–4. In invertebrates, several FABP-related proteins have been reported in protostomes and amphioxus; however, little is known about the relationship between their phylogenetic positions and expression patterns. We have performed a genome-wide survey of FABP-related genes in protochordates: amphioxus Branchiostoma belcheri and the ascidian Ciona intestinalis. Comprehensive BLAST searches in NCBI and the Ciona Ghost Database by using amino acid sequences of all FABPs have revealed that the ascidian C. intestinalis and amphioxus B. belcheri contain six and seven FABP-related genes in their haploid genomes, respectively. Expression pattern analyses by whole-mount in situ hybridization in Ciona transparent juveniles and serial-section in situ hybridizations in adult amphioxus have revealed that all genes are mainly expressed in the postpharyngeal digestive tract. In particular, the expression of FABP-related genes of subfamily-2 (liver/ileum type) and subfamily-3 (intestinal type) in the ascidian pyloric gland and amphioxus hepatic cecum provides insight into the evolution of hepatic-related structures of chordates and FABP-related genes.

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Acknowledgments

We thank staff members of the Aizu Marine Biological Station of Kumamoto University, staff members of the National Research Institute of Aquaculture, and Prof. Kinya Yasui for their help in collecting adult amphioxus specimens. We are also grateful to Prof. Nori Satoh and Kazuko Hirayama for providing the Ciona cDNA clones and juvenile specimens. Finally, we thank Aya Ishihara for her help in the identification of Ciona FABP-related genes and with the in situ hybridization procedure for Ciona juveniles.

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  1. The Graduate School of Advanced Integration Science, Chiba University, Yayoi-cho 1-33, Inage-ku, Chiba, 263-8522, Japan

    Wataru Orito, Fuyuko Ohhira & Michio Ogasawara

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  1. Wataru Orito
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  2. Fuyuko Ohhira
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  3. Michio Ogasawara
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Correspondence to Michio Ogasawara.

Electronic supplementary material

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Supplementary Fig. 1

Phylogenetic relationships of FABP-related proteins of ascidian C. intestinalis. Relevant Ciona gene models are indicated in bold with underlining. Phylogenetic relationships are assessed by the neighbor-joining method with bootstrap values (×1000). Subfamilies and types of iLBP-related proteins are indicated beside the human proteins (Hs human [Homo sapiens], Mm mouse [Mus musculus], Gg chick [Gallus gallus], Xl frog [Xenopus laevis], Dr zebrafish [Danio rerio], Ci ascidian [C. intestinalis] (PDF 49 kb)

Supplementary Fig. 2

Expression of ascidian FABP genes in early juveniles of C. intestinalis. Expression of each gene starts around the two-protostigmata stage. Expression patterns in early juveniles (upper panels) resemble those of 2nd ascidian stages (lower panels). White arrowheads indicate relevant expression of each gene. Bars 100 μm (upper panel), 500 μm (lower panel) (PDF 469 kb)

Supplementary Fig. 3

Serial sections of the pyloric gland with expression signals of KH.C7.15. Left panel Position and orientation of the numbered sections (as atrial siphon, bwm body-wall muscle, d dorsal, en endostyle, esp esophagus, int intestine, st stomach, l left, pg pyloric gland, px pharynx, r right, v ventral). Bars 100 μm (PDF 87 kb)

Supplementary Fig. 4

Three-dimensional (3D) models of KH.C7.153 expression regions in the pyloric gland and intestine. a Combination of regions with expression of KH.C7.153 in the pyloric gland (magenta) and intestine (sky blue). b Intestinal expression (sky blue) of KH.C7.153. c Intestinal expression (sky blue) of KH.C7.153 (yellow). d All regions of expression (magenta, sky blue) of KH.C7.153 with intestine (yellow) (PDF 371 kb)

Supplementary Fig. 5

Whole-mount in situ hybridization (WISH) analysis of amphioxus FABP genes using mixed specimens. Four adult individuals are sectioned at 2 mm thickness, and mixed and, then, specimens for WISH are randomly provided for seven genes. Discontinuous expression patterns (red underlines) based on the adjacent sections are observed for some genes. Representation of FABP gene expression is based on this experiment. The expression level is measured as three levels: strong, moderate, and none. Expression levels of strong, moderate, and none are indicated by the color intensities of black, gray, and white, respectively (PDF 344 kb)

Supplementary Fig. 6

Comparison of FABP gene expression patterns between two individuals of adult amphioxus. Each individual is divided into 2-mm-thick sections, and all section specimens are used for WISH analysis. Expression patterns of the same gene are similar but not identical between two individuals. The expression level is measured as three levels: strong, moderate, and none. Expression levels of strong, moderate, and none are indicated by the color intensities of black, gray, and white, respectively (PDF 812 kb)

Supplementary Fig. 7

Representation showing FABP gene expression patterns in amphioxus B. belcheri. Results of the expression analyses (ex. 1–3) are compared. The expression level is measured as three levels: strong, moderate, and none. Expression levels of strong, moderate, and none are indicated by the color intensities of black, gray, and white, respectively (PDF 112 kb)

Supplementary Fig. 8

Phylogenetic relationships of FABP-related proteins in metazoan species. Names of genes for which expression patterns were analyzed in this study are indicated in bold and underlined. Amino acid sequences of FABP-related proteins in human, ascidian, amphioxus, sea urchin, nematode, fly, and trematoda are used for phylogenetic analysis based on the neighbor-joining method, and relationships are assessed by using bootstrap values (×1000). Subfamilies and types of iLBP-related proteins are indicated beside the human proteins. Subfamily-2 and subfamily-3 are closely related and seem to be separate from other subfamilies, 1 and 4 (Hs human [Homo sapiens], Ci ascidian [C. intestinalis], Cs ascidian [Ciona savignyi], Bb amphioxus [B. belcheri], Bf amphioxus [B. floridae], Sp sea urchin [Strongylocentrotus purpuratus], Ce nematode [Caenorhabditis elegans], Sj blood fluke [Schistosoma japonicum], Dm fruit fly [Drosophila melanogaster]) (PDF 65 kb)

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Orito, W., Ohhira, F. & Ogasawara, M. Gene expression profiles of FABP genes in protochordates, Ciona intestinalis and Branchiostoma belcheri . Cell Tissue Res 362, 331–345 (2015). https://doi.org/10.1007/s00441-015-2198-4

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