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Modeling the distribution of malachite green in zebrafish using matrix-assisted laser desorption/ionization mass spectrometry imaging

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Abstract

Understanding the spatial distribution of bioactive small molecules is indispensable for elucidating their biological or pharmaceutical roles. Here, a rapid and effective analysis strategy was introduced to study the distribution of veterinary drugs in aquatic products. Malachite green (MG), one of the most widely used veterinary drugs in aquaculture, was selected as the targeted compound. Zebrafish (Danio rerio) was used as a model organism. After an exposure test, the matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) technique was applied to directly analyze the content changes of malachite green in zebrafish tissues. The reliable relationship of exposure time and content change of MG was described precisely by the extended Freundlich equation. The process of modeling was discussed in detail, and some important parameters or trend information was obtained, including the maximum content of MG in different fish tissues, time to maximum content, elimination time, equilibrium content, and so on. With a simplification of sample pretreatment, this research strategy can be used for monitoring the spatial distribution of veterinary drugs and related metabolites of laboratory-exposed fish. The obtained model can provide a perspective for rational drug use in aquaculture and precise drug residue detection in production activities.

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References

  1. Cohen MSGC, Kashuba ADM, Blower S, Paxton L. Narrative review: Antiretroviral therapy to prevent the sexual transmission of HIV-1. Ann Intern Med. 2007;146:591–601.

    Article  PubMed  Google Scholar 

  2. Mortensen AS, Letcher RJ, Cangialosi MV, Chu S, Arukwe A. Tissue bioaccumulation patterns, xenobiotic biotransformation and steroid hormone levels in Atlantic salmon (Salmo salar) fed a diet containing perfluoroactane sulfonic or perfluorooctane carboxylic acids. Chemosphere. 2011;83:1035–44.

    Article  CAS  PubMed  Google Scholar 

  3. Zhao H, Liu S, Chen J, Jiang J, Xie Q, Quan X. Biological uptake and depuration of sulfadiazine and sulfamethoxazole in common carp (Cyprinus carpio). Chemosphere. 2015;120:592–7.

    Article  CAS  PubMed  Google Scholar 

  4. Maclachlan DJ, Mueller U. A refined approach to estimate exposure for use in calculating the maximum residue limit of veterinary drugs. Regul Toxicol Pharmacol. 2012;62:99–106.

    Article  CAS  PubMed  Google Scholar 

  5. Grabowski T, Jaroszewski JJ, Piotrowski W, Feder M. Qualitative structure residue relationship analysis in the determination of the maximum residue limit of veterinary drugs. Chemosphere. 2012;87:312–8.

    Article  CAS  PubMed  Google Scholar 

  6. Culp SJ, Beland FA. Malachite green: a toxicological review. J Am Coll Toxicol. 1996;15:219–38.

    Article  Google Scholar 

  7. Alderman DJ. Malachite green: a review. J Fish Dis. 2010;8:289–98.

    Article  Google Scholar 

  8. Lanzing W. Observations on malachite green in relation to its application to fish diseases. Hydrobiologia. 1965;25:426–41.

    Article  Google Scholar 

  9. Doroszkiewicz-Fiedoruk J, Masowiecka J, Rodziewicz L. Determination of malachite green and leukomalachite green residues in fish muscle by high-performance liquid chromatography method. Rocz Panstw Zakl Hig. 2009;60:325–8.

    CAS  PubMed  Google Scholar 

  10. Fallah AA, Barani A. Determination of malachite green residues in farmed rainbow trout in Iran. Food Control. 2014;40:100–5.

    Article  CAS  Google Scholar 

  11. Andersen WC, Turnipseed SB, Roybal JE. Quantitative and confirmatory analyses of malachite green and leucomalachite green residues in fish and shrimp. J Agric Food Chem. 2006;54:4517–23.

    Article  CAS  PubMed  Google Scholar 

  12. Hlavek RR, Bulkley RV. Effects of malachite green on leucocyte abundance in rainbow trout, Salmo gairdneri (Richardson). J Fish Biol. 2006;17:431–44.

    Article  Google Scholar 

  13. Doerge DR, Churchwell MI, Gehring TA, Yu MP, Plakas SM. Analysis of malachite green and metabolites in fish using liquid chromatography atmospheric pressure chemical ionization mass spectrometry. Rapid Commun Mass SP. 1998;12:1625–34.

    Article  CAS  Google Scholar 

  14. Xu RN, Fan L, Rieser MJ, El-Shourbagy TA. Recent advances in high-throughput quantitative bioanalysis by LC-MS/MS. J Pharmaceut Biomed. 2007;44:342–55.

    Article  CAS  Google Scholar 

  15. Solon EG, Schweitzer A, Stoeckli M, Prideaux B. Autoradiography, MALDI-MS, and SIMS-MS imaging in pharmaceutical discovery and development. AAPS J. 2010;12:11–26.

    Article  CAS  PubMed  Google Scholar 

  16. Drexler DM, Tannehill-Gregg SH, Wang L, Brock BJ. Utility of quantitative whole-body autoradiography (QWBA) and imaging mass spectrometry (IMS) by matrix-assisted laser desorption/ionization (MALDI) in the assessment of ocular distribution of drugs. J Pharmacol Toxicol Methods. 2011;63:205–8.

    Article  CAS  PubMed  Google Scholar 

  17. Rudin M, Weissleder R. Molecular imaging in drug discovery and development. Nat Rev Drug Discov. 2003;2:123–31.

    Article  CAS  PubMed  Google Scholar 

  18. Leblond F, Davis SC, Valdés P, Pogue BW. Pre-clinical whole-body fluorescence imaging: review of instruments, methods and applications. J Photochem Photobiol B. 2010;98:77–94.

    Article  CAS  PubMed  Google Scholar 

  19. Sekar RB. Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations. J Cell Biol. 2003;160:629–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zavaleta CL, Smith BR, Walton I, Doering W, Davis G, Shojaei B, Natan MJ, Gambhir SS. Multiplexed imaging of surface enhanced Raman scattering nanotags in living mice using noninvasive Raman spectroscopy. Proc Natl Acad Sci U S A. 2009;106:13511–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Keren S, Zavaleta C, Cheng Z, Zerda A, Gheysens O, Gambhir SS. Noninvasive molecular imaging of small living subjects using Raman spectroscopy. Proc Natl Acad Sci U S A. 2008;105:5844–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Caprioli RM, Farmer TB, Gile J. Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS. Anal Chem. 1997;69:4751–60.

    Article  CAS  PubMed  Google Scholar 

  23. Li N, Nie H, Jiang L, Ruan G, Liu H. Recent advances of ambient ionization mass spectrometry imaging in clinical research. J Sep Sci. 2020;43:3146–63.

    Article  CAS  PubMed  Google Scholar 

  24. Prideaux B, Stoeckli M. Mass spectrometry imaging for drug distribution studies. J Proteome. 2012;75:4999–5013.

    Article  CAS  Google Scholar 

  25. Silvia G, Valentina P, Lavinia M, Melinda M, Luigi F, Giuseppe C, Sonja V, Simonetta L, Roberta F, Massimo Z. A nanostructured matrices assessment to study drug distribution in solid tumor tissues by mass spectrometry imaging. Nanomater (Basel). 2017;7:71.

    Article  Google Scholar 

  26. Handberg E, Chingin K, Wang N, Dai X, Chen H. Mass spectrometry imaging for visualizing organic analytes in food. Mass Spectrom Rev. 2015;34:641–58.

    Article  CAS  PubMed  Google Scholar 

  27. Yoshimura Y, Goto-Inoue N, Moriyama T, Zaima N. Significant advancement of mass spectrometry imaging for food chemistry. Food Chem. 2016;210:200–11.

    Article  CAS  PubMed  Google Scholar 

  28. Deng Y, He M, Feng F, Feng X, Zhang Y, Zhang F. The distribution and changes of glycoalkaloids in potato tubers under different storage time based on MALDI-TOF mass spectrometry imaging. Talanta. 2020;121453.

  29. Zhou C, Wu H, Zhang XH, Zhang Y, Xu W. High-throughput and direct sample screening using a laser spray ionization miniature mass spectrometer. Anal Chem. 2019;91:8808–13.

    Article  CAS  PubMed  Google Scholar 

  30. Nemes P, Vertes A. Ambient mass spectrometry for in vivo local analysis and in situ molecular tissue imaging. Trends Anal Chem. 2012;34:22–34.

    Article  CAS  Google Scholar 

  31. Sarvaiya VN, Sadariya KA, Rana MP, Thaker AM. Zebrafish as model organism for drug discovery and toxicity testing: a review. Vet Clin Sci. 2014;2:31–8.

    Google Scholar 

  32. Rzagalinski I, Volmer DA. Quantification of low molecular weight compounds by MALDI imaging mass spectrometry – a tutorial review. BBA-Proteins Proteom. 1865;2016:726–39.

    Google Scholar 

  33. Bokhart MT, Rosen E, Thompson C, Sykes C, Kashuba A, Muddiman DC. Quantitative mass spectrometry imaging of emtricitabine in cervical tissue model using infrared matrix-assisted laser desorption electrospray ionization. Anal Bioanal Chem. 2015;407:2073–84.

    Article  CAS  PubMed  Google Scholar 

  34. Sibbesen E. Some new equations to describe phosphate sorption by soils. J Soil Sci. 1981;32:67–74.

    Article  CAS  Google Scholar 

  35. Cherrak O, Ghennioui H, Abarkan E, Universit A. Levenberg-Marquardt algorithm. Tutoral on Lm Algorithm. 2004;11:101–10.

    Google Scholar 

  36. Mitrowska K, Posyniak A. Malachite green: pharmacological and toxicological aspects and residue control. Med Weter. 2005;61:742–5.

    Google Scholar 

  37. Calvano CD, Monopoli A, Cataldi T, Palmisano F. MALDI matrices for low molecular weight compounds: an endless story? Anal Bioanal Chem. 2018;410:4015–38.

    Article  CAS  PubMed  Google Scholar 

  38. Bienvenut WV, Déon C, Pasquarello C, Campbell JM, Hochstrasser DF. Matrix-assisted laser desorption/ionization-tandem mass spectrometry with high resolution and sensitivity for identification and characterization of proteins. Proteomics. 2015;2:868–76.

    Article  Google Scholar 

  39. Kind T, Tsugawa H, Cajka T, Ma Y, Lai Z, Mehta SS, Wohlgemuth G, Ba Rupal DK, Showalter MR, Arita M. Identification of small molecules using accurate mass MS/MS search. Mass Spectrom Rev. 2017;37:513–32.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Plakas SM, Doerge DR, Turnipseed SB. Disposition and metabolism of malachite green and other therapeutic dyes in fish. Acs National Meeting Book of Abstracts. 1999;215:U55–5.

  41. Kim JY, Lee SY, Kim H, Park JW, Lim DK, Moon DW. Biomolecular imaging of regeneration of zebrafish caudal fins using high spatial resolution ambient mass spectrometry. Anal Chem. 2018;90:12723–30.

    Article  CAS  PubMed  Google Scholar 

  42. Ratkowsky DA. A statistical study of seven curves for describing the sorption of phosphate by soil. Eur J Soil Sci. 1986;37:183–9.

    Article  CAS  Google Scholar 

  43. Adeyi J, Abdullah, Choong L. Simultaneous adsorption of cationic dyes from binary solutions by thiourea-modified poly (acrylonitrile-co-acrylic acid): detailed isotherm and kinetic studies. Materials. 2019;12:2903.

    Article  CAS  PubMed Central  Google Scholar 

  44. Pandey PK, Ndegwa RM, Alldredge JR, Pitts R, Soupir ML. Modeling effects of granules on the start-up of anaerobic digestion of dairy wastewater with Langmuir and extended Freundlich equations. Bioprocess Biosyst Eng. 2010;33:833–45.

    Article  CAS  PubMed  Google Scholar 

  45. Kumar S, Zafar M, Prajapati JK, Kumar S, Kannepalli S. Modeling studies on simultaneous adsorption of phenol and resorcinol onto granular activated carbon from simulated aqueous solution. J Hazard Mater. 2011;185:287–94.

    Article  CAS  PubMed  Google Scholar 

  46. Gonalves BL, Gonalves C, Rosim RE, Oliveira C, Corassin CH. Evaluations of different sources of Saccharomyces cerevisiae to binding capacity of aflatoxin B1 utilizing their adsorption isotherms. J Food Chem Nanotechnol. 2017;3:126–32.

    Google Scholar 

  47. Bowman M. Guide to using drugs, biologics, and other chemicals in aquaculture. 2011.

    Google Scholar 

  48. Schnick RA. Use of chemicals in fish management and fish culture. Xenobiotics in Fish. 1999.

  49. JöNsson ME, BrunströM B, Brandt I. The zebrafish gill model: induction of CYP1A, EROD and PAH adduct formation. Aquat Toxicol. 2009;91:62–70.

    Article  PubMed  Google Scholar 

  50. S M Plakas, K R El Said, G R Stehly, W H Gingerich, JLA. Uptake, tissue distribution, and metabolism of malachite green in the channel catfish (Ictalurus punctatus). Can J Fish Aquat Sci 1996;53:1427–1433.

  51. Eliceiri BP, Gonzalez AM, Baird A. Zebrafish model of the blood-brain barrier: morphological and permeability studies. Methods Mol Biol. 2011;686:371–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by the National Key Research and Development Program of China (No. 2018YFC1603500), the National “Ten thousand Plan” Scientific and Technological Innovation Leading Talent Project (Feng Zhang), and the Shandong Provincial Key Research and Development Program (SPKR&DP) (No. 2019JZZY020903). The authors would like to acknowledge Prof. Wei Yong and Dr. Shige Xing for their support and suggestions.

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  1. Muyi He and Xiujuan Wang contributed equally to this work.

Authors and Affiliations

  1. Institute of Food Safety, Chinese Academy of Inspection and Quarantine, Beijing, 100176, China

    Muyi He, Xiujuan Wang, Yu Bian, Minli Yang, Yamei Deng, Tong Liu, Yinlong Li, Fengming Chen, Bozhou Xu, Meixia Xu & Feng Zhang

  2. College of Pharmacy, China Medical University, Shenyang, 110000, China

    Yu Bian & Yamei Deng

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  1. Muyi He
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Correspondence to Feng Zhang.

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Ethics approval for the experimentation reported herein was obtained from the Animal Compliance Office (Chinese Academy of Inspection and Quarantine).

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He, M., Wang, X., Bian, Y. et al. Modeling the distribution of malachite green in zebrafish using matrix-assisted laser desorption/ionization mass spectrometry imaging. Anal Bioanal Chem 413, 7021–7030 (2021). https://doi.org/10.1007/s00216-021-03664-2

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