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Stress response in the ascidian Ciona intestinalis: transcriptional profiling of genes for the heat shock protein 70 chaperone system under heat stress and endoplasmic reticulum stress

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Cell Stress and Chaperones Aims and scope

Abstract

The genome of Ciona intestinalis contains eight genes for HSP70 superfamily proteins, 36 genes for J-proteins, a gene for a J-like protein, and three genes for BAG family proteins. To understand the stress responses of genes in the HSP70 chaperone system comprehensively, the transcriptional profiles of these 48 genes under heat stress and endoplasmic reticulum (ER) stress were studied using real-time reverse transcriptase–polymerase chain reaction (RT-PCR) analysis. Heat stress treatment increased the messenger RNA (mRNA) levels of six HSP70 superfamily genes, eight J-protein family genes, and two BAG family genes. In the cytoplasmic group of the DnaK subfamily of the HSP70 family, Ci-HSPA1/6/7-like was the only heat-inducible gene and Ci-HSPA2/8 was the only constitutively active gene which showed striking simplicity in comparison with other animals that have been examined genome-wide so far. Analyses of the time course and temperature dependency of the heat stress responses showed that the induction of Ci-HSPA1/6/7-like expression rises to a peak after heat stress treatment at 28°C (10°C upshift from control temperature) for 1 h. ER stress treatment with Brefeldin A, a drug that is known to act as ER stress inducer, increased the mRNA levels of four HSP70 superfamily genes and four J-protein family genes. Most stress-inducible genes are conserved between Ciona and vertebrates, as expected from a close evolutionary relationship between them. The present study characterized the stress responses of HSP70 chaperone system genes in Ciona for the first time and provides essential data for comprehensive understanding of the functions of the HSP70 chaperone system.

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Acknowledgment

The authors thank Kazuko Hirayama and all members of the Maizuru Fisheries Research Station of Kyoto University for culturing of C. intestinalis; Yutaka Satou for cDNA resources; and Lixy Yamada for experimental advice. This work was supported by NBRP (National Bioresource Project) and KAKENHI [Grants-in-Aid for Young Scientists (B), 20770183] from MEXT, Japan.

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  1. Department of Bioscience, Faculty of Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga, 526-0829, Japan

    Tetsuya Fujikawa, Takeo Munakata, Shin-ichi Kondo & Shuichi Wada

  2. Marine Genomics Unit, Okinawa Institute of Science and Technology Promotion Corporation, Uruma, Okinawa, 904-2234, Japan

    Nori Satoh

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  1. Tetsuya Fujikawa
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  2. Takeo Munakata
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Correspondence to Shuichi Wada.

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Supplementary Fig. S1

Phylogenetic tree of ER-resident lectin chaperones constructed based on the full-length sequences of human, mouse, D. melanogaster, and C. intestinalis sequences. The number at each branch indicates the percentage of times that a node was supported in 1,000 bootstrap pseudoreplications. Percentages less than 49% are omitted for simplicity. Ciona proteins are indicated by large black dots. Proteins of other animals are designated with the accession number registered in public databases followed by abbreviation of the species (HS for human, MM for mouse, and DM for D. melanogaster) and gene name. An unrooted tree is shown as a rooted tree for simplicity. The scale bar indicates an evolutionary distance of 0.1 amino acid substitutions per position (EPS 81 kb)

High resolution image

Supplementary Fig. S2

Phylogenetic tree of PERK and related kinases constructed based on the kinase domain sequences of human, mouse, and C. intestinalis. The number at each branch indicates the percentage of times that a node was supported in 1,000 bootstrap pseudoreplications. Percentages less than 49% are omitted for simplicity. Ciona proteins are indicated by large black dots. Proteins of other animals are designated with the accession number registered in public databases, followed by abbreviation of the species (HS for human and MM for mouse) and gene name. An unrooted tree is shown as a rooted tree for simplicity. Bars on the right indicate gene groups. Genes for the PKR, GCN2, and HRI groups are added to the analysis as outgroups. The scale bar indicates an evolutionary distance of 0.05 amino acid substitutions per position (EPS 79 kb)

High resolution image

Supplementary Fig. S3

Phylogenetic tree of IRE1 proteins constructed based on the full-length sequences of human, mouse, C. intestinalis, C. elegans, and D. melanogaster. The number at each branch indicates the percentage of times that a node was supported in 1,000 bootstrap pseudoreplications. Percentages less than 49% are omitted for simplicity. Ciona protein is indicated by a large black dot. Proteins of other animals are designated with the accession number registered in public databases, followed by abbreviation of the species (HS for human, MM for mouse, DM for D. melanogaster, and CE for C. elegans) and gene name. An unrooted tree is shown as a rooted tree for simplicity. Bars on the right indicate gene groups. The scale bar indicates an evolutionary distance of 0.05 amino acid substitutions per position (EPS 74 kb)

High resolution image

Supplementary Table S1

Primers used for real time RT-PCR (DOC 75 kb)

Supplementary Table S2

EST counts (out of 336188) of genes for the HSP70 chaperone system (DOC 84 kb)

Supplementary Table S3

Genes for ER-resident lectin chaperones in the C. intestinalis genome (DOC 26 kb)

Supplementary Table S4

Domain configurations of ER-resident lectin chaperones in Ciona and humans (DOC 26 kb)

Supplementary Table S5

Genes for ER stress sensors in the C. intestinalis genome (DOC 28 kb)

Supplementary Table S6

Domain configurations of ER stress sensors in C. intestinalis and humans (DOC 28 kb)

Supplementary Table S7

Sequences used for analysis (DOC 24 kb)

Supplementary Table S8

Comparison of stress responses of HSP70 chaperone system genes in Ciona and vertebrates (DOC 153 kb)

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Fujikawa, T., Munakata, T., Kondo, Si. et al. Stress response in the ascidian Ciona intestinalis: transcriptional profiling of genes for the heat shock protein 70 chaperone system under heat stress and endoplasmic reticulum stress. Cell Stress and Chaperones 15, 193–204 (2010). https://doi.org/10.1007/s12192-009-0133-x

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