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Differential gene regulation by VIV and VV ions in the branchial sac, intestine, and blood cells of a vanadium-rich ascidian, Ciona intestinalis

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Abstract

Ascidians are hyperaccumulators that have been studied in detail. Proteins and genes involved in the accumulation process have been identified, but regulation of gene expression related to vanadium accumulation remains unknown. To gain insights into the regulation of gene expression by vanadium in a genome-wide manner, we performed a comprehensive study on the effect of excess vanadium ions on a vanadium-rich ascidian, Ciona intestinalis, using a microarray. RT-PCR and enzyme activity assay were performed from the perspective of redox and accumulation of metal ions in each tissue. Glutathione metabolism-related proteins were significantly up-regulated by VIV treatment. Several genes involved in the transport of vanadium and protons, such as Nramp and V-ATPase, were significantly up-regulated by VIV treatment. We observed significant up-regulation of glutathione synthesis and degradation pathways in the intestine and branchial sac. In blood cells, expression of Ci-Vanabin4, glutathione reductase activity, glutathione levels, and vanadium concentration increased after VIV treatment. VIV treatment induced significant changes related to vanadium exclusion, seclusion, and redox pathways in the intestine and branchial sac. It also induced an enhancement of the vanadium reduction and accumulation cascade in blood cells. These differential responses in each tissue in the presence of excess vanadium ions suggest that vanadium accumulation and reduction may have regulatory functions. This is the first report on the gene regulation by the treatment of vanadium-rich ascidians with excess vanadium ions. It provided much information for the mechanism of regulation of gene expression related to vanadium accumulation.

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Acknowledgments

We thank Ms. K. Hirayama and Dr. Yutaka Satou at Kyoto University and the staff at the Maizuru Fisheries Research Station, Kyoto University, Maizuru Bay, Kyoto, Japan, for providing C. intestinalis, through the National Bio-Resource Project (NBRP) of the MEXT, Japan. This work was supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (#21570077 to H. M. and #20570070 to T. U.) and a grant from the Toray Science Foundation (03-4402 to T. U.).

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Authors and Affiliations

  1. Molecular Physiology Laboratory, Department of Biological Science, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima, 739-8526, Japan

    Satoshi Kume, Tatsuya Ueki, Hiroki Matsuoka & Hitoshi Michibata

  2. Marine Genomics Unit, Okinawa Institute of Science and Technology, Graduate University, 1919-1 Tancha, Onna-son, Kunigami-gun, Okinawa, 904-0495, Japan

    Mayuko Hamada & Nori Satoh

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  1. Satoshi Kume
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  2. Tatsuya Ueki
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  3. Hiroki Matsuoka
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  4. Mayuko Hamada
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  5. Nori Satoh
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  6. Hitoshi Michibata
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Correspondence to Tatsuya Ueki.

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Kume, S., Ueki, T., Matsuoka, H. et al. Differential gene regulation by VIV and VV ions in the branchial sac, intestine, and blood cells of a vanadium-rich ascidian, Ciona intestinalis . Biometals 25, 1037–1050 (2012). https://doi.org/10.1007/s10534-012-9569-z

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