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Antioxidant and antidiabetic activities of vanadium binding proteins purified from the sea squirt Halocynthia roretzi

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Abstract

Sea squirts accumulate vanadium compounds with potent antidiabetic activity, which are involved in immune defense. In this study, vanadium concentrations of fresh blood plasma, intestine, and muscle of the sea squirt Halocynthia roretzi were 6.3, 3.7 and 2.1 mg/kg respectively. Two vanadium binding proteins (VBPs) from blood plasma and intestine were purified through (NH4)2SO4 precipitation, and DEAE-Sepharose ion exchange and Sephacryl S-200 HR gel filtration chromatography, in that order. The purity and yield of the intestine and blood plasma vanadium binding proteins, VBPintestine and VBPblood plasma, were 13.4 folds and 7.1%, and 20.9 folds and 6.8%, respectively. There were two protein bands on the sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS-PAGE) with molecular weights of 24.3 and 68.8 kDa and one with 96.7 kDa on the native-PAGE of VBPblood plasma, whereas only one protein band of VBPintestine on the SDS-PAGE with 26.5 kDa. Antioxidant activities of VBPs were lower than that of ascorbic acid. Both VBPs exerted strong inhibitory activity against Saccharomyces cerevisiae and mild against Bacillus stearothermophilus and rat intestinal α-glucosidase. IC50 values of VBPintestine and VBPblood plasma against S. cerevisiae α‐glucosidase were 28.34 and 12.60 μg/ml, respectively. The K m , V max , k cat , and k cat /K m values of VBPintestine and VBPblood plasma were 4.29, 0.036, 6.58 and 1.53 × 103, and 7.63 mM, 0.057 mM/min, 10.41 s−1 and 1.36 × 103 (M sec)−1, respectively. There was a synergistic interaction between VBPblood plasma and VBPintestine on rat intestinal α-glucosidase inhibitory activity.

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References

  • Akkari H, Chir FB, Rekik M, Hamza H, Darghouth MA, Gharbi M (2016) Potential anthelmintic effect of Capparis spinosa (Capparidaceae) as related to its polyphenolic content and antioxidant activity. Vet Med Czech 61(6):308–316

    Article  CAS  Google Scholar 

  • Arndt C, Koristka S, Bachman H (2012) Native polyacrylamide gels. Methods Mol Biol 869:49–53

    Article  CAS  Google Scholar 

  • Bellomo E, Singh KB, Massarotti A, Hogstrand C, Maret W (2016) The metal face of protein tyrosine phosphatase. Coord Chem Rev 327–328:70–83

    Article  Google Scholar 

  • Crans DC, Smee JJ, Gaidamauskas E, Yang L (2004) The chemistry and biochemistry of vanadium and the biological activities exerted by vanadium compounds. Chem Rev 104(2):849–902

    Article  CAS  Google Scholar 

  • Francik R, Krosniak M, Barlik M, Kuda A, Grybo R, Librowski T (2011) Impact of vanadium complexes treatment on the oxidative stress factors in wistar rats plasma. Bioinorg Chem App 2011:1–8

    Article  Google Scholar 

  • Hodson PV (1988) The effect of metal metabolism on uptake, disposition and toxicity in fish. Aquat Toxicol 11:3–18

    Article  CAS  Google Scholar 

  • Kaur A, Dhari J, Sharma OP. Gupta GD, Kharb V (2012) In-vitro anti-oxidant and free radical scavenging activity of lycopene https://www.researchgate.net/publication/265793569_In-vitro_Anti-oxidant_and_Free_Radical_Scavenging_Activity_of_Lycopene. Accessed 30 June 2017

  • Kawee-ai A, Kuntiva A, Kim SK (2013) Anticholinesterase and antioxidant activities of fucoxanthin purified from the microalga Phaeodactylum tricornutum. Nat Prod Commun 8(10):1381–1386

    CAS  Google Scholar 

  • Kazeem MI, Adamson JO, Ogunwande IA (2013) Modes of inhibition of α-amylase and α-glucosidase by aqueous extract of Morinda lucida Benth leaf. Biomed Res Int 2013:1–6

    Article  Google Scholar 

  • Konishi I, Hosokawa M, Sashima T, Kobayashi H, Miyashita K (2006) Halocynthia-xanthin and fucoxanthinol isolated from Halocynthia roretzi induce apoptosis in human leukemia, breast and colon cancer cells. Comp Biochem Physiol C: Toxicol Pharmacol 142(1–2):53–59

    Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantitation. Methods Mol Biol 32:9–15

    CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  Google Scholar 

  • Li W, Sun YN, Yan XT, Yang SY, Jo SH, Kwon YN, Kim YH (2014) Rat intestinal sucrase and α-glucosidase inhibitory activities of isocoumarin and flavonoids from the Zanthoxylum Schinifolium stems. Bull Korean Chem Soc 35(1):316–318

    Article  Google Scholar 

  • Lineweaver H, Burk D (1934) The determination of enzyme disassociation constants. J Am Chem Soc 56:658–666

    Article  CAS  Google Scholar 

  • Liu Y, Xu H, Xu J, Guo Y, Xue Y, Wang J, Xue C (2015a) Vanadium-binding protein from vanadium-enriched sea cucumber Apostichopus Japonicus inhibits adipocyte differentiation through activating WNT/β-catenin pathway. J Funct Foods 17:504–513

    Article  Google Scholar 

  • Liu Y, Zhou Q, Xu J, Xue Y (2015b) Assessment of total and organic vanadium levels and their bioaccumulation in edible sea cucumbers: tissues distribution, inter-species-specific, locational differences and seasonal variations. Environ Geochem Health 38(1):111–122

    Article  Google Scholar 

  • Liu Y, Zhou Q, Yanlei Z, Yiming W, Jingfeng W, Jie X, Changhu X (2016) Enrichment, distribution of vanadium-containing protein in vanadium-enriched sea cucumber Apostichopus japonicus and the ameliorative effect on insulin resistance. Biol Trace Elem Res 171(1):167–175

    Article  CAS  Google Scholar 

  • Martinez-Irujo JJ, Villahermosa ML, Mercapide J, Cabodevilla JF, Santiago E (1998) Analysis of the combined effect of two linear inhibitors on a single enzyme. Biochem J 329:689–698

    Article  CAS  Google Scholar 

  • Michibata H, Terada T, Anada A, Yamakawa K, Numakunai T (1986) The accumulation and distribution of vanadium, iron, and manganese in some solitary ascidians. Biol Bull 171:672–681

    Article  CAS  Google Scholar 

  • Mizrahi L, Achituv Y (1989) Effect of heavy metals ions on enzyme activity in the mediterranean mussel, Donax trunculus. Bull Environ Contam Toxicol 42(6):854–859

    Article  CAS  Google Scholar 

  • Nguyen TH, Kim SM (2015) α-Glucosidase inhibitory activities of fatty acids purified from the internal organ of sea cucumber Stichopus japonicus. J Food Sci 80:H841–H847

    Article  CAS  Google Scholar 

  • Odate S, Pawlik JR (2007) The role of vanadium in the chemical defense of the solitary tunicate Phallusia nigra. J Chem Ecol 33(3):643–654

    Article  CAS  Google Scholar 

  • Oyaizu M (1986) Studies on products of browning reactions: antioxidant activities of products of browning reaction prepared from glucosamine. Jpn J Nutr 44:307–315

    Article  CAS  Google Scholar 

  • Pessoa JC, Garribba E, Santos MFA, Silva TS (2015) Vanadium and proteins: uptake, transport, structure, activity and function. Coord Chem Rev 301–302:49–86

    Article  Google Scholar 

  • Peters KG, Davis MG, Howard BW, Pokross M, Rastogi V, Diven C, Greis KD (2003) Mechanism of insulin sensitization by BMOV (bis maltolato oxo vanadium); unliganded vanadium (VO4) as the active component. J Inorg Biochem 96(2–3):321–330

    Article  CAS  Google Scholar 

  • Pritsch K, Günthardt-Goerg MS, Munch JC, Schloter M (2006) Influence of heavy metals and acid rain on enzymatic activities in the mycorrhizosphere of model forest ecosystems. For Snow Landsc Res 80(3):289–304

    Google Scholar 

  • Silverman RB (2002) APPENDIX I—enzyme kinetics. In: Silverman RB (ed) Organic chemistry of enzyme-catalyzed reactions. Academic Press, San Diego, pp 563–596. http://www.sciencedirect.com/science/article/pii/B978008051336250005X. Accessed 30 June 2017

  • Ueki T, Michibata H (2011) Molecular mechanism of the transport and reduction pathway of vanadium in ascidians. Coord Chem Rev 255(19–20):2249–2257

    Article  CAS  Google Scholar 

  • Ueki T, Adachi T, Kawano S, Aoshima M, Yamaguchi N (2003) Vanadium-binding proteins (vanabins) from a vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1626:43–50

    Article  CAS  Google Scholar 

  • Ueki T, Satake M, Kamino K, Michibata H (2008) Sequence variation of vanabin2-like vanadium-binding proteins in blood cells of the vanadium-accumulating ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1780:1010–1015

    Article  CAS  Google Scholar 

  • Wazalwar SS, Bhave NS (2012) Microwave assisted synthesis and antioxidant activity of vanadium (IV) complexes of amino acid schiff bases. Synth React Inorg Met Org Chem 42(8):1098–1104

    Article  CAS  Google Scholar 

  • Yoshihara M, Ueki T, Watanable T, Yamaguchi N, Kamino K, Michibata H (2005) VanabinP, a novel vanadium-binding protein in the blood plasma of an ascidian, ascidia sydneinsis samea. Biochim Biophys Acta 1730:206–214

    Article  CAS  Google Scholar 

  • Yoshihara M, Ueki T, Yamaguchi N, Kamino K, Michibata H (2008) Characterization of a novel vanadium-binding protein (VBP-129) from blood plasma of the vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1780(2):256–263

    Article  CAS  Google Scholar 

  • Yoshinaga M, Ueki T, Michibata H (2007) Metal binding ability of glutathione transferases conserved between two animal species, the vanadium-rich ascidian Ascidia sydneiensis samea and the schistosome Schistosoma japonicum. Biochim Biophys Acta 1770:1413–1418

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was a part of the project titled ‘Future Marine Technology Development’ funded by the Ministry of Oceans and Fisheries, Republic of Korea.

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Authors and Affiliations

  1. Department of Chemistry, University of Colombo, Colombo 03, Sri Lanka

    Minoli Anuththara Gunasinghe

  2. Department of Marine Food Science and Technology, Gangneung-Wonju National University, Gangneung, 25457, Republic of Korea

    Minoli Anuththara Gunasinghe & Sang Moo Kim

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  1. Minoli Anuththara Gunasinghe
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  2. Sang Moo Kim
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Correspondence to Sang Moo Kim.

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Gunasinghe, M.A., Kim, S.M. Antioxidant and antidiabetic activities of vanadium binding proteins purified from the sea squirt Halocynthia roretzi. J Food Sci Technol 55, 1840–1849 (2018). https://doi.org/10.1007/s13197-018-3099-9

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  • DOI: https://doi.org/10.1007/s13197-018-3099-9

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