Abstract
Some species in the family Ascidiidae accumulate vanadium at concentrations in excess of 350 mM, which corresponds to about 107 times higher than that in seawater. In these species signet ring cells, with a single huge vacuole in which vanadium ion is contained, function as vanadium-accumulating cells, vanadocytes. To investigate the mechanism underlying this phenomenon, we performed an expressed sequence tag (EST) analysis of a complementary DNA library from vanadocytes of a vanadium-rich ascidian, Ascidia sydneiensis samea. We determined the nucleotide sequences of 1000 ESTs and performed a BLAST analysis against the SwissProt database. We found 93 clones of metal-related gene homologues, including the ferritin heavy subunit, hemocyanin, and metallothionein. Two ESTs, in particular, exhibited significant similarity to vanabins that have been extracted from A. sydneiensis samea blood cells as low molecular weight vanadium-binding proteins. We have named the genes encoding these ESTs vanabin3 and vanabin4. Immobilized metal ion affinity chromatography revealed that these novel vanabin homologues bind vanadium(IV) ions.
Similar content being viewed by others
References
P. Aisen M. Wessling-Resnick E.A. Leibold (1999) ArticleTitleIron metabolism. Bioinorg Chem 3 200–206 Occurrence Handle10.1016/S1367-5931(99)80033-7 Occurrence Handle1:CAS:528:DyaK1MXisVent7k%3D
S.F. Altschul T.L. Madden A.A. Schaffer J. Zhang Z. Zhang W. Miller D.J. Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694
D.B. Carlisle (1968) ArticleTitleVanadium and other metals in ascidians. Proc R Soc Lond B Biol Sci 171 31–42 Occurrence Handle1:CAS:528:DyaF1cXksFSjtL8%3D Occurrence Handle4385858
K. De Cremer M. Van Hulle C. Chery R. Cornelis K. Strijckmans R. Dams N. Lameire R. Vanholder (2002) ArticleTitleFractionation of vanadium complexes in serum, packed cells and tissues of Wistar rats by means of gel filtration and anion-exchange chromatography. J Biol Inorg Chem 7 884–890 Occurrence Handle10.1007/s00775-002-0376-9 Occurrence Handle1:CAS:528:DC%2BD38Xotlajtrg%3D Occurrence Handle12203026
P. Dehal Y. Satou R.K. Campbell J. Chapman B. Degnan A. De Tomaso B. Davidson A. Di Gregorio M. Gelpke D.M. Goodstein N Harafuji KEM, HoI Hastings I Ho K. Hotta W. Huang T. Kawashima P. Lemaire D. Martinez I.A. Meinertzhagen S. Necula M. Nonaka N. Putnam S. Rash H. Saiga M. Satake A. Terry L. Yamada H.G. Wang S. Awazu K. Azumi J. Boore M. Branno S. Chin-bow R. De Santis S. Doyle P. Francino D.N. Keys S. Haga H. Hayashi K. Hino K.S. Imai K. Inaba S. Kano K. Kobayashi M. Kobayashi B.I. Lee K.W. Makabe C. Manohar G. Matassi M. Medina Y. Mochizuki S. Mount T. Morishita S. Miura A. Nakayama S. Nishizaka H. Nomoto F. Ohta K. Oishi I. Rigoutsos M. Sano A. Sasaki Y. Sasakura E. Shoguchi T. Shin-I A. Spagnuolo D. Stainier M.M. Suzuki O. Tassy N. Takatori M. Tokuoka K. Yagi F. Yoshizaki S. Wada C. Zhang P.D. Hyatt F. Larimer C. Detter N. Doggett T. Glavina T. Hawkins P. Richardson S. Lucas Y. Kohara M. Levine N. Satoh D.S. Rokhsar (2002) ArticleTitleThe draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298 2157–2167 Occurrence Handle10.1126/science.1080049 Occurrence Handle1:CAS:528:DC%2BD38XpsVSkt7o%3D Occurrence Handle12481130
P. Frank R.M.K. Carlson K.O. Hodgson (1986) ArticleTitleVanadyl ion EPR as a non-invasive probe of pH in intact vanadocytes from Ascidia ceratodes. Inorg Chem 25 470–478 Occurrence Handle1:CAS:528:DyaL28XhtVKlsrk%3D
K. Fukui T. Ueki H. Ohya H. Michibata (2003) ArticleTitleVanadium-binding protein in a vanadium-rich ascidian Ascidia sydneiensis samea: CW and pulsed EPR studies. J Am Chem Soc 125 6352–6353 Occurrence Handle10.1021/ja034507w Occurrence Handle1:CAS:528:DC%2BD3sXjtlKjt7s%3D Occurrence Handle12785759
J.K. Grady J. Shao P. Arosio P. Santambrogio N.D. Chasteen (2000) ArticleTitleVanadyl(IV) binding to mammalian ferritins: an EPR study aided by site-directed mutagenesis. J Inorg Biochem 80 107–113
M. Henze (1911) ArticleTitleUntersuchungen über das Blut der Ascidien I. Mitteilung. Die Vanadium-verbindungen der Blutkörperchen. Hoppe-Seyler’s Z Physiol Chem 72 494–501 Occurrence Handle1:CAS:528:DyaC3MXhvFekug%3D%3D
J. Hirata H. Michibata (1991) ArticleTitleValency of vanadium in the vanadocytes of Ascidia gemmata separated by density-gradient centrifugation. J Exp Zool 257 160–165 Occurrence Handle1:CAS:528:DyaK3MXkt1Khur4%3D
J.H.R. Kägi (1993) . K.Y. Suzuki N. Imura M. Kimura (Eds) Metallothionein III, Birkhäuser Basel, Switzerland 29–55
K. Kanamori H. Michibata (1994) ArticleTitleRaman spectroscopic study of the vanadium sulfate in blood cell homogenate of the ascidian, Ascidia gemmata. J Mar Biol Assoc UK 74 279–286
K. Kanamori K. Sakurai M. Kinoshita T. Uyama T. Ueki H. Michibata (1999) ArticleTitleDirect reduction from vanadium(V) to vanadium(IV) by NADPH in the presence of EDTA. A consideration of the reduction and accumulation of vanadium in the ascidian blood cells. J Inorg Biochem 77 157–161
T. Kanda Y. Nose J. Wuchiyama T. Uyama Y. Moriyama H. Michibata (1997) ArticleTitleIdentification of a vanadium-associated protein from the vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 14 37–42 Occurrence Handle1:CAS:528:DyaK2sXjtVKntb8%3D Occurrence Handle9200977
W. Liebrich AC. Brown D.P. Botes (1995) ArticleTitleCadmium-binding proteins from a tunicate, Pyura stolonifera. Comp Biochem Physiol 112C 35–42 Occurrence Handle1:CAS:528:DyaK2MXps1yjsbo%3D
K.W. Makabe T. Kawashima S. Kawashima T. Minokawa A. Adachi H. Kawamura H. Ishikawa R. Yasuda H. Yamamoto K. Kondoh S. Arioka Y. Sasakura A. Kobayashi K. Yagi K. Shojima Y. Kondoh S. Kido M. Tsujinami N. Nishimura M. Takahashi T. Nakamura M. Kanehisa M. Ogasawara T. Nishikata H. Nishida (2001) ArticleTitleLarge-scale cDNA analysis of the maternal genetic information in the egg of Halocynthia roretzi for a gene expression catalog for ascidian development. Development 128 2555–2567 Occurrence Handle11493572
J. Markl H. Decker (1992) Molecular structure of the arthropod hemocyaninis. C.P. Mangum (Eds) Adv Comp Environ Physiol 13; Blood and Tissue Oxygen Carriers, Springer Germany: Heidelberg 325–376
H. Michibata (1996) ArticleTitleThe mechanism of accumulation of vanadium by ascidians: some progress toward an understanding of this unusual phenomenon. Zool Sci 13 489–502 Occurrence Handle1:CAS:528:DyaK28XlvFOhtLs%3D
H. Michibata J. Hirata M. Uesaka T. Numakunai H. Sakurai (1987) ArticleTitleSeparation of vanadocytes: determination and characterization of vanadium ion in the separated blood cells of ascidian, Ascidia ahodori. J Exp Zool 244 33–38
H. Michibata Y. Iwata J. Hirata (1991) ArticleTitleIsolation of highly acidic and vanadium-containing blood cells from among several types of blood cell from Ascidiidae species by density-gradient centrifugation. J Exp Zool 257 306–313
H. Michibata T. Terada N. Anada K. Yamakawa T. Numakunai (1986) ArticleTitleThe accumulation and distribution of vanadium, iron, and manganese in some solitary ascidians. Biol Bull 171 672–681 Occurrence Handle1:CAS:528:DyaL2sXhtFKktLs%3D
H. Michibata T. Uyama J. Hirata (1990) ArticleTitleVanadium containing cells (vanadocytes) show no fluorescence due to the tunichrome in the ascidian Ascidia sydneiensis samea. Zool Sci 7 55–61 Occurrence Handle1:CAS:528:DyaK3cXkt1Wjur8%3D
H. Michibata N. Yamaguchi T. Uyama T. Ueki (2003) ArticleTitleMolecular biological approaches to the accumulation and reduction of vanadium by ascidians. Coordination Chem Rev 234 41–51 Occurrence Handle10.1016/S0010-8545(02)00278-3
T. Nishikata L. Yamada Y. Mochizuki Y. Satou T. Shin-I Y. Kohara N. Satoh (2001) ArticleTitleProfiles of maternal expressed genes in fertilized eggs of Ciona intestinalis. Dev Biol 238 315–33l Occurrence Handle1:CAS:528:DC%2BD3MXntFKqsL8%3D Occurrence Handle11784013
M. Ogasawara A. Sasaki H. Metoki . Shin-I T. . Y. Kohara N. Satoh Y. Satou (2002) ArticleTitleGene expression profiles in young adult Ciona intestinalis. Dev Genes Evol 212 173–185 Occurrence Handle10.1007/s00427-002-0230-7 Occurrence Handle12012232
E. Sabbioni J. Rade F. Bertolero (1980) ArticleTitleRelationships between iron and vanadium metabolism: the exchange of vanadium between transferrin and ferritin. J Inorg Biochem 12 307–315
E. Sabbioni E. Marafante (1981) ArticleTitleRelations between iron and vanadium metabolism: in vivo incorporation of vanadium into iron proteins of the rat. J Toxicol Environ Health 8 419–429 Occurrence Handle1:CAS:528:DyaL38XjtVSi Occurrence Handle7345166
Y. Satou N. Takatori L. Yamada Y. Mochizuki M. Hamaguchi H. Ishikawa S. Chiba K. Imai S. Kano D.S. Murakami A. Nakayama A. Nishino Y. Sasakura G. Satoh T. Shimotori T. Shin-I E. Shoguchi M.M. Suzuki N. Takada N. Utsumi N. Yoshida H. Saiga Y. Kohara N. Satoh (2001) ArticleTitleGene expression profiles in Ciona intestinalis tailbud embryos. Dev Biol 238 315–331 Occurrence Handle1:CAS:528:DC%2BD3MXntFKqsL8%3D Occurrence Handle11784013
K. Takamura N. Oka A. Akagi K. Okamoto T. Okada T. Fukuoka A. Hogaki D. Naito Y. Oobayashi N. Satoh (2001) ArticleTitleEST analysis of genes that are expressed in the neural complex of Ciona intestinalis adults. Zool Sci 18 1231–1236 Occurrence Handle1:CAS:528:DC%2BD38XhsVKrtrY%3D Occurrence Handle11911079
T. Ueki K. Takemoto B. Fayard M. Salomé A. Yamamoto H. Kihara J. Susini S. Scippa T. Uyama H. Michibata (2002) ArticleTitleScanning x-ray microscopy of living and freeze-dried blood cells in two vanadium-rich ascidian species, Phallusia mammillata and Ascidia sydneiensis samea. Zool Sci 19 27–35 Occurrence Handle12025401
T. Ueki T. Uyama K. Kanamori H. Michibata (1998) ArticleTitleIsolation of cDNAs encoding subunits A and B of the vacuolar-type ATPase from the vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 15 823–829 Occurrence Handle1:CAS:528:DyaK1MXivVSqs7k%3D
T. Ueki T. Uyama K. Yamamoto K. Kanamori H. Michibata (2000) ArticleTitleExclusive expression of transketolase in the vanadocytes of the vanadium-rich ascidian, Ascidia sydneiensis samea. Biochim Biophys Acta 1494 83–90 Occurrence Handle10.1016/S0167-4781(00)00222-0 Occurrence Handle1:CAS:528:DC%2BD3MXptFek Occurrence Handle11072071
T. Ueki T. Uyama K. Kanamori H. Michibata (2001) ArticleTitleSubunit C of the vacuolar-type ATPase from the vanadium-rich ascidian Ascidia sydneiensis samea rescued the pH sensitivity of yeast ma5 mutants. Mar Biotechnol 3 316–321 Occurrence Handle1:CAS:528:DC%2BD3MXmt1Sksr8%3D
T. Ueki T. Adachi S. Kawano M Aoshima N. Yamaguchi K. Kanamori H. Michibata (2003) ArticleTitleVanadium-binding proteins (vanabins) from a vanadium-rich ascidian, Ascidia sydneiensis samea. Biochim Biophys Acta 1626 43–50 Occurrence Handle10.1016/S0167-4781(03)00036-8 Occurrence Handle1:CAS:528:DC%2BD3sXivFCqs7s%3D Occurrence Handle12697328
T. Uyama T. Kinoshita H. Takahashi N. Satoh K. Kanamori H. Michibata (1998a) ArticleTitle6-Phosphogluconate dehydrogenase is a 45-kDa antigen recognized by a monoclonal antibody S4D5 specific to vanadocytes in the vanadium-rich ascidian, Ascidia sydneiensis samea. J Biochem 124 377–382 Occurrence Handle1:CAS:528:DyaK1cXmtlSksL4%3D
T. Uyama Y. Moriyama M. Futai H. Michibata (1994) ArticleTitleImmunological detection of a vacuolar-type H+-ATPase in the vanadocytes of the ascidian Ascidia sydneiensis samea. J Exp Zool 270 148–154
T. Uyama T. Ueki H. Takahashi Y. Suhama K. Kanamori H. Michibata (1998b) ArticleTitleA 100-kDa antigen recognized by a newly prepared monoclonal antibody specific to the vanadocytes of the vanadium-rich ascidian, Ascidia sydneiensis samea, is glycogen phosphorylase. Zool Sci 15 815–821 Occurrence Handle1:CAS:528:DyaK1MXivVSqs7g%3D
T. Uyama K. Yamamoto K. Kanamori H. Michibata (1998c) ArticleTitleGlucose-6-phosphate dehydrogenase in the pentose phosphate pathway is localized in vanadocytes of vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 15 441–446 Occurrence Handle1:CAS:528:DyaK1cXntVCjtLs%3D
K.E. van Holde K.I. Miller (1995) ArticleTitleHemocyanins. Adv Prot Chem 47 1–81 Occurrence Handle1:CAS:528:DyaK28XlvFOhuw%3D%3D
N. Yamaguchi A. Togi T. Ueki T. Uyama H. Michibata (2002) ArticleTitleExpressed sequence tag analysis of blood cells in the vanadium-rich ascidian, A. sydneiensis samea—a survey of genes for metal accumulation. Zool Sci 19 1001–1008 Occurrence Handle1:CAS:528:DC%2BD3sXjsVWnurY%3D Occurrence Handle12362053
Acknowledgements
We thanks Mr. K. Morita and the staff of the Otsuchi Marine Research Center for their cooperation in collecting the materials. This work was supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology, of Japan (1440244 and 14340264 to H.M.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yamaguchi, N., Kamino, K., Ueki, T. et al. Expressed Sequence Tag Analysis of Vanadocytes in a Vanadium-Rich Ascidian, Ascidia sydneiensis samea . Mar. Biotechnol. 6, 165–174 (2004). https://doi.org/10.1007/s10126-003-0024-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-003-0024-6