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LC–MS-based metabolome analysis on steroid metabolites from the starfish Patiria (=Asterina) pectinifera in conditions of active feeding and stresses

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Abstract

Introduction

Starfish are recognized as interesting source of natural steroid products with pharmaceutical potential. Polar steroid metabolites of starfish have unique chemical structures and exhibit various biological activities but their biological functions are controversial.

Objectives

The objective of this study was to investigate the response of polar steroid metabolome of the starfish Patiria (=Asterina) pectinifera on various environmental factors and stresses.

Methods

Here we first have applied MS-based environmental metabolomics to elucidate the metabolic changes of polar steroid metabolome of starfish. Using HPLC–ESI–Q/TOF–MS approach followed by statistical analysis including principal component analysis and partial least squares discriminant analysis for data classification and potential biomarkers selection, we investigated the changes induced by feeding, injury, variations in water temperature and salinity, and oxygen deficiency.

Results

According to multivariate and univariate statistical analysis the responses to feeding, injury and water heating were better expressed than the others and have some similarity in their action on the steroid metabolome of the starfish P. pectinifera. Most constituents of asterosaponin pool were reduced and most constituents of polyhydroxysteroid and related glycoside pool were increased at that.

Conclusion

Our results indicate that various metabolic changes in polar steroid constituents of P. pectinifera are induced by feeding and stresses. We believe that these responses are connected with biological multifunctionality of these compounds.

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References

  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289–300.

    Google Scholar 

  • Bundy, J. G., Davey, M. P., & Viant, M. R. (2009). Environmental metabolomics: A critical review and future perspectives. Metabolomics, 5(1), 3–21.

    Article  CAS  Google Scholar 

  • Cevallos-Cevallos, J. M., Reyes-De-Corcuera, J. I., Etxeberria, E., Danyluk, M. D., & Rodrick, G. E. (2009). Metabolomic analysis in food science: A review. Trends in Food Science & Technology, 20(11–12), 557–566.

    Article  CAS  Google Scholar 

  • Demeyer, M., De Winter, J., Caulier, G., Eeckhaut, I., Flammang, P., & Gerbaux, P. (2014). Molecular diversity and body distribution of saponins in the sea star Asterias rubens by mass spectrometry. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 168, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Demeyer, M., Wisztorski, M., Decroo, C., De Winter, J., Caulier, G., Hennebert, E., et al. (2015). Inter- and intra-organ spatial distributions of sea star saponins by MALDI imaging. Analytical and Bioanalytical Chemistry, 407(29), 8813–8824.

    Article  CAS  PubMed  Google Scholar 

  • Dong, G., Xu, T., Yang, B., et al. (2011). Chemical constituents and bioactivities of starfish. Chemistry & Biodiversity, 8(5), 740–791.

    Article  CAS  Google Scholar 

  • Durbin, B. P., Hardin, J. S., Hawkins, D. M., & Rocke, D. M. (2002). A variance-stabilizing transformation for gene-expression microarray data. Bioinformatics, 18, S105–S110.

    Article  PubMed  Google Scholar 

  • Fang, Z. Z., & Gonzalez, F. J. (2014). LC–MS-based metabolomics: An update. Archives of Toxicology, 88(8), 1491–1502.

    Article  CAS  PubMed  Google Scholar 

  • Franco, C. F., Santos, R., & Coelho, A. V. (2014). Proteolytic events are relevant cellular responses during nervous system regeneration of the starfish Marthasterias glacialis. Journal of Proteomics, 99, 1–25.

    Article  Google Scholar 

  • Goulitquer, S., Potin, P., & Tonon, T. (2012). Mass spectrometry-based metabolomics to elucidate functions in marine organisms and ecosystems. Marine Drugs, 10(4), 849–880.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey, C., Garneau, F.-X., & Himmelman, J. H. (1987). Chemodetection of the predatory seastar Leptasterias polaris by the whelk Buccinum undatum. Marine Ecology Progress Series, 40(1–2), 79–86.

    Article  Google Scholar 

  • Ivanchina, N. V., Kicha, A. A., Kalinovsky, A. I., Dmitrenok, P. S., Prokof’eva, N. G., & Stonik, V. A. (2001). New steroid glycosides from the starfish Asterias rathbuni. Journal of Natural Products, 64(7), 945–947.

    Article  CAS  PubMed  Google Scholar 

  • Ivanchina, N. V., Kicha, A. A., Kalinovsky, A. I., et al. (2000). Hemolytic polar steroidal constituents of the starfish Aphelasterias japonica. Journal of Natural Products, 63(8), 1178–1181.

    Article  CAS  PubMed  Google Scholar 

  • Ivanchina, N. V., Kicha, A. A., Malyarenko, T. V., Kalinovsky, A. I., Dmitrenok, P. S., & Stonik, V. A. (2013). Biosynthesis of polar steroids from the Far Eastern starfish Patiria (=Asterina) pectinifera. Cholesterol and cholesterol sulfate are converted into polyhydroxylated sterols and monoglycoside asterosaponin P1 in feeding experiments. Steroids, 78(12–13), 1183–1191.

    Article  CAS  PubMed  Google Scholar 

  • Ivanchina, N. V., Kicha, A. A., & Stonik, V. A. (2011). Steroid glycosides from marine organisms. Steroids, 76(5), 425–454.

    Article  CAS  PubMed  Google Scholar 

  • Kamleh, M. A., Dow, J. A. T., & Watson, D. G. (2009). Applications of mass spectrometry in metabolomic studies of animal model and invertebrate systems. Briefings in Functional Genomics & Proteomics, 8(1), 28–48.

    Article  CAS  Google Scholar 

  • Kessner, D., Chambers, M., Burke, R., Agus, D., & Mallick, P. (2008). ProteoWizard: Open source software for rapid proteomics tools development. Bioinformatics, 24(21), 2534–2536.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kicha, A. A., Ivanchina, N. V., Gorshkova, I. A., Ponomarenko, L. P., Likhatskaya, G. N., & Stonik, V. A. (2001a). The distribution of free sterols, polyhydroxysteroids and steroid glycosides in various body components of the starfish Patiria (=Asterina) pectinifera. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 128(1), 43–52.

    Article  CAS  Google Scholar 

  • Kicha, A. A., Ivanchina, N. V., Kalinovsky, A. I., Dmitrenok, P. S., & Stonik, V. A. (2001b). Sulfated steroid compounds from the starfish Aphelasterias japonica of the Kuril population. Russian Chemical Bulletin, 50(4), 724–727.

    Article  CAS  Google Scholar 

  • Lankadurai, B. P., Nagato, E. G., & Simpson, M. J. (2013). Environmental metabolomics: An emerging approach to study organism responses to environmental stressors. Environmental Reviews, 21(3), 180–205.

    Article  CAS  Google Scholar 

  • Mackie, A. M., Lasker, R., & Grant, P. T. (1968). Avoidance reactions of a mollusc Buccinum undatum to saponin-like surface-active substances in extracts of the starfish Asterias rubens and Marthasterias glacialis. Comparative Biochemistry and Physiology, 26, 415–428.

    Article  CAS  Google Scholar 

  • Mackie, A. M., Singh, H. T., & Owen, J. M. (1977). Studies on the distribution, biosynthesis and function of steroidal saponins in echinoderms. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 56(1), 9–14.

    Article  CAS  Google Scholar 

  • Micallef, L., & Rodgers, P. (2014). eulerAPE: Drawing area-proportional 3-Venn diagrams using ellipses. PLoS ONE, 9(7), e101717.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller, M. G. (2007). Environmental metabolomics: A SWOT analysis (strengths, weaknesses, opportunities, and threats). Journal of Proteome Research, 6(2), 540–545.

    Article  CAS  PubMed  Google Scholar 

  • Minale, L., Riccio, R., & Zollo, F. (1993). Steroidal oligoglycosides and polyhydroxysteroids from Echinoderms. Fortschritte der Chemie Organischer Naturstoffe, 62, 75–308.

    CAS  PubMed  Google Scholar 

  • Naruse, M., Suetomo, H., Matsubara, T., Sato, T., Yanagawa, H., Hoshi, M., & Matsumoto, M. (2010). Acrosome reaction-related steroidal saponin, Co-ARIS, from the starfish induces structural changes in microdomains. Development Biology, 347(1), 147–153.

    Article  CAS  Google Scholar 

  • Nicholson, J. K., & Lindon, J. C. (2008). Systems biology—metabonomics. Nature, 455(7216), 1054–1056.

    Article  CAS  PubMed  Google Scholar 

  • Palyanova, N. V., Pankova, T. M., Starostina, M. V., Kicha, A. A., Ivanchina, N. V., & Stonik, V. A. (2013). Neuritogenic and neuroprotective effects of polar steroids from the Far East starfishes Patiria pectinifera and Distolasterias nipon. Marine Drugs, 11(5), 1440–1455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patti, G. J., Yanes, O., & Siuzdak, G. (2012). Metabolomics: The apogee of the omics trilogy. Nature Reviews Molecular Cell Biology, 13(4), 263–269.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pluskal, T., Castillo, S., Villar-Briones, A., & Oresic, M. (2010). MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics, 11, 395.

    Article  PubMed  PubMed Central  Google Scholar 

  • Popov, R. S., Ivanchina, N. V., Kicha, A. A., Malyarenko, T. V., Dmitrenok, P. S., & Stonik, V. A. (2014). Metabolite profiling of polar steroid constituents in the Far Eastern starfish Aphelasterias japonica using LC–ESI MS/MS. Metabolomics, 10(6), 1152–1168.

    Article  CAS  Google Scholar 

  • Popov, R. S., Ivanchina, N. V., Kicha, A. A., Malyarenko, T. V., Dmitrenok, P. S., & Stonik, V. A. (2016). LC-ESI MS/MS profiling of polar steroid metabolites of the Far Eastern starfish Patiria (=Asterina) pectinifera. Metabolomics, 12(2), 21.

    Article  Google Scholar 

  • Quinones, M. P., & Kaddurah-Daouk, R. (2009). Metabolomics tools for identifying biomarkers for neuropsychiatric diseases. Neurobiology of Diseases, 35(2), 165–176.

    Article  CAS  Google Scholar 

  • Sandvoss, M., Weltring, A., Preiss, A., Levsen, K., & Wuensch, G. (2001). Combination of matrix solid-phase dispersion extraction and direct on-line liquid chromatography–nuclear magnetic resonance spectroscopy–tandem mass spectrometry as a new efficient approach for the rapid screening of natural products: application to the total asterosaponin fraction of the starfish Asterias rubens. Journal of Chromatography A, 917(1–2), 75–86.

    Article  CAS  PubMed  Google Scholar 

  • Shao, Y., Li, C., Chen, X., Zhang, P., Li, Y., Li, T., & Jiang, J. (2015). Metabolomic responses of sea cucumber Apostichopus japonicus to thermal stresses. Aquaculture, 435, 390–397.

    Article  CAS  Google Scholar 

  • Spratlin, J. L., Serkova, N. J., & Eckhardt, S. G. (2009). Clinical applications of metabolomics in oncology: A review. Clinical Cancer Research, 15(2), 431–440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stonik, V. A. (2001). Marine polar steroids. Russ. Chemical Reviews, 70(8), 673–715.

    CAS  Google Scholar 

  • Stonik, V. A., Ivanchina, N. V., & Kicha, A. A. (2008). New polar steroids from starfish. Natural Products Communications, 3(10), 1587–1610.

    CAS  Google Scholar 

  • Storey, J. D., & Tibshirani, R. (2003). Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences, 100(16), 9440–9445.

    Article  CAS  Google Scholar 

  • Theodoridis, G. A., Gika, H. G., Want, E. J., & Wilson, I. D. (2012). Liquid chromatography–mass spectrometry based global metabolite profiling: A review. Analytica Chimica Acta, 711, 7–16.

    Article  CAS  PubMed  Google Scholar 

  • van den Berg, R. A., Hoefsloot, H. C. J., Westerhuis, J. A., Smilde, A. K., & van der Werf, M. J. (2006). Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genomics, 7, 142.

    Article  PubMed  PubMed Central  Google Scholar 

  • Veselkov, K. A., Vingara, L. K., Masson, P., et al. (2011). Optimized preprocessing of ultra-performance liquid chromatography/mass spectrometry urinary metabolic profiles for improved information recovery. Analytical Chemistry, 83(15), 5864–5872.

    Article  CAS  PubMed  Google Scholar 

  • Viant, M. R. (2007). Metabolomics of aquatic organisms: the new ‘omics’ on the block. Marine Ecology Progress Series, 332, 301–306.

    Article  CAS  Google Scholar 

  • Viant, M. R. (2008). Recent developments in environmental metabolomics. Molecular BioSystems, 4(10), 980–986.

    Article  CAS  PubMed  Google Scholar 

  • Viant, M. R., & Sommer, U. (2013). Mass spectrometry based environmental metabolomics: A primer and review. Metabolomics, 9, 144–158.

    Article  CAS  Google Scholar 

  • Voogt, P. A., & Huiskamp, R. (1979). Sex-dependence and seasonal variation of saponins in the gonads of the starfish Asterias rubens: Their relation to reproduction. Comparative Biochemistry and Physiology, 62, 1049–1055.

    Article  Google Scholar 

  • Xia, J. G., Mandal, R., Sinelnikov, I. V., Broadhurst, D., & Wishart, D. S. (2012). MetaboAnalyst 2.0—a comprehensive server for metabolomic data analysis. Nucleic Acids Research, 40(W1), W127–W133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia, J. G., Sinelnikov, I. V., Han, B., & Wishart, D. S. (2015). MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Research, 43(W1), W251–W257.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, A. H., Sun, H., Wang, P., Han, Y., & Wang, X. J. (2012). Modern analytical techniques in metabolomics analysis. Analyst, 137(2), 293–300.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, B., Xiao, J. F., Tuli, L., & Ressom, H. W. (2012). LC-MS-based metabolomics. Molecular BioSystems, 8(2), 470–481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The study was supported by the Grant No. 14-04-00341-a from the RFBR. We sincerely thanks to Vasily A. Avilov for help in data preprocessing and Dr. Valery G. Voinov for his assistance in editing this manuscript.

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Correspondence to Pavel S. Dmitrenok.

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Popov, R.S., Ivanchina, N.V., Kicha, A.A. et al. LC–MS-based metabolome analysis on steroid metabolites from the starfish Patiria (=Asterina) pectinifera in conditions of active feeding and stresses. Metabolomics 12, 106 (2016). https://doi.org/10.1007/s11306-016-1048-z

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