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A dual-modal colorimetric and photothermal assay for glutathione based on MnO2 nanosheets synthesized with eco-friendly materials

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Abstract

We developed a dual-modal colorimetric and photothermal assay for glutathione (GSH) using MnO2 nanosheets prepared with environmentally friendly materials. The nanosheets were synthesized by using ascorbic acid present abundantly in lemon and orange juices to reduce KMnO4. The as-prepared MnO2 nanosheets display oxidase-like activity and can catalyze the oxidation reaction of 3,3′,5,5′-tetramethylbenzidine (TMB), yielding a blue oxidative product (oxTMB) that exhibits a UV–Vis absorption peak at 652 nm. In the presence of GSH, the MnO2 nanosheets are reduced and decomposed, resulting in a decrease in the peak intensity. The colorimetric assay offers a wide dynamic range (0.1–100 μM) and a detection limit of 100 nM. The MnO2 nanosheets are also efficient in converting photoenergy to thermal energy, with a photothermal conversion efficiency of 23.3%. The temperature change, after near-infrared (NIR) irradiation at 808 nm, can be easily measured by an inexpensive pen-type thermometer. This effect can also be used for GSH quantification and expands the GSH concentration detection to the range from 6.0 to 200 μM. The viability of our dual-modal assay for clinical applications was demonstrated with successful analyses of GSH in human serum samples.

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References

  1. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND. Glutathione metabolism and its implications for health. J Nutr. 2004;134(3):489–92.

    CAS  PubMed  Google Scholar 

  2. Teskey G, Abrahem R, Cao R, Gyurjian K, Islamoglu H, Lucero M, et al. Glutathione as a marker for human disease. In: Makowski GS, editor. Advances in clinical chemistry. 87. London, United Kingdom: Academic Press; 2018. p. 141–59.

    Google Scholar 

  3. Smeyne M, Smeyne RJ. Glutathione metabolism and Parkinson’s disease. Free Radic Biol Med. 2013;62:13–25.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Giustarini D, Colombo G, Garavaglia ML, Astori E, Portinaro NM, Reggiani F, et al. Assessment of glutathione/glutathione disulphide ratio and S-glutathionylated proteins in human blood, solid tissues, and cultured cells. Free Radic Biol Med. 2017;112:360–75.

    CAS  PubMed  Google Scholar 

  5. Borowczyk K, Wyszczelska-Rokiel M, Kubalczyk P, Glowacki R. Simultaneous determination of albumin and low-molecular-mass thiols in plasma by HPLC with UV detection. J Chromatogr B. 2015;981:57–64.

    Google Scholar 

  6. Hanko M, Svorc L, Plankova A, Mikus P. Overview and recent advances in electrochemical sensing of glutathione - a review. Anal Chim Acta. 2019;1062:1–27.

    CAS  PubMed  Google Scholar 

  7. Sanchez-Illana A, Mayr F, Cuesta-Garcia D, Pineiro-Ramos JD, Cantarero A, de la Guardia M, et al. On-capillary surface-enhanced Raman spectroscopy: determination of glutathione in whole blood microsamples. Anal Chem. 2018;90(15):9093–100.

    CAS  PubMed  Google Scholar 

  8. Deng R, Xie X, Vendrell M, Chang YT, Liu X. Intracellular glutathione detection using MnO2-nanosheet-modified upconversion nanoparticles. J Am Chem Soc. 2011;133(50):20168–71.

    CAS  PubMed  Google Scholar 

  9. Liu J, Meng L, Fei Z, Dyson PJ, Jing X, Liu X. MnO2 nanosheets as an artificial enzyme to mimic oxidase for rapid and sensitive detection of glutathione. Biosens Bioelectron. 2017;90:69–74.

    CAS  PubMed  Google Scholar 

  10. Yao C, Wang J, Zheng A, Wu L, Zhang X, Liu X. A fluorescence sensing platform with the MnO2 nanosheets as an effective oxidant for glutathione detection. Sens Actuators B Chem. 2017;252:30–6.

    CAS  Google Scholar 

  11. Ma Z, Wu T, Li P, Liu M, Huang S, Li H, et al. A dual (colorimetric and fluorometric) detection scheme for glutathione and silver (I) based on the oxidase mimicking activity of MnO2 nanosheets. Microchim Acta. 2019;186(8):498.

    Google Scholar 

  12. Liao S, Huang X, Yang H, Chen X. Nitrogen-doped carbon quantum dots as a fluorescent probe to detect copper ions, glutathione, and intracellular pH. Anal Bioanal Chem. 2018;410(29):7701–10.

    CAS  PubMed  Google Scholar 

  13. Wang Y, Liu Y, Ding F, Zhu X, Yang L, Zou P, et al. Colorimetric determination of glutathione in human serum and cell lines by exploiting the peroxidase-like activity of CuS-polydopamine-Au composite. Anal Bioanal Chem. 2018;410(20):4805–13.

    CAS  PubMed  Google Scholar 

  14. Jung HS, Chen X, Kim JS, Yoon J. Recent progress in luminescent and colorimetric chemosensors for detection of thiols. Chem Soc Rev. 2013;42(14):6019–31.

    CAS  PubMed  Google Scholar 

  15. Jiang D, Ni D, Rosenkrans ZT, Huang P, Yan X, Cai W. Nanozyme: new horizons for responsive biomedical applications. Chem Soc Rev. 2019;48(14):3683–704.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Deręgowska A, Depciuch J, Wojnarowska R, Polit J, Broda D, Nechai H, et al. Study of optical properties of a glutathione capped gold nanoparticles using linker (MHDA) by Fourier transform infrared spectroscopy and surface enhanced Raman scattering. Intl J Biotechnol Bioeng. 2013;7(1):80–3.

    Google Scholar 

  17. He Y, Zheng L. Gold nanoparticle-catalyzed clock reaction of methylene blue and hydrazine for visual chronometric detection of glutathione and cysteine. ACS Sustain Chem Eng. 2017;5(10):9355–9.

    CAS  Google Scholar 

  18. Bu Y, Zhu G, Li S, Qi R, Bhave G, Zhang D, et al. Silver-nanoparticle-embedded porous silicon disks enabled SERS signal amplification for selective glutathione detection. ACS Appl Nano Mater. 2018;1(1):410–7.

    CAS  PubMed  Google Scholar 

  19. Zhao X, Wu K, Lyu H, Zhang X, Liu Z, Fan G, et al. Porphyrin functionalized co (OH)2/GO nanocomposites as an excellent peroxidase mimic for colorimetric biosensing. Analyst. 2019;144(17):5284–91.

    CAS  PubMed  Google Scholar 

  20. Lian J, Liu P, Jin C, Shi Z, Luo X, Liu Q. Perylene diimide-functionalized CeO2 nanocomposite as a peroxidase mimic for colorimetric determination of hydrogen peroxide and glutathione. Microchim Acta. 2019;186(6):332.

    Google Scholar 

  21. Liu Y, Tian Y, Tian Y, Wang Y, Yang W. Carbon-dot-based nanosensors for the detection of intracellular redox state. Adv Mater. 2015;27(44):7156–60.

    CAS  PubMed  Google Scholar 

  22. Yang L, Chueng S-TD, Li Y, Patel M, Rathnam C, Dey G, et al. A biodegradable hybrid inorganic nanoscaffold for advanced stem cell therapy. Nature Comm. 2018;9:3147.

    Google Scholar 

  23. Wang L, Guan S, Weng Y, Xu S-M, Lu H, Meng X, et al. Highly efficient vacancy-driven photothermal therapy mediated by ultrathin MnO2 nanosheets. ACS Appl Mater Interfaces. 2019;11(6):6267–75.

    CAS  PubMed  Google Scholar 

  24. Tan X, Wang X, Zhang L, Liu L, Zheng G, Li H, et al. Stable and photothermally efficient antibody-covered Cu3(PO4)2@polydopamine nanocomposites for sensitive and cost-effective immunoassays. Anal Chem. 2019;91(13):8274–9.

    CAS  PubMed  Google Scholar 

  25. Liu X, Wang Q, Zhao H, Zhang L, Su Y, Lv Y. BSA-templated MnO2 nanoparticles as both peroxidase and oxidase mimics. Analyst. 2012;137(19):4552–8.

    CAS  PubMed  Google Scholar 

  26. Omomo Y, Sasaki T, Wang L, Watanabe M. Redoxable nanosheet crystallites of MnO2 derived via delamination of a layered manganese oxide. J Am Chem Soc. 2003;125(12):3568–75.

    CAS  PubMed  Google Scholar 

  27. Su Q, Pan B, Wan S, Zhang W, Lv L. Use of hydrous manganese dioxide as a potential sorbent for selective semoval of lead, cadmium, and zinc ions from water. J Colloid Interface Sci. 2010;349(2):607–12.

    CAS  PubMed  Google Scholar 

  28. Fan D, Shang C, Gu W, Wang E, Dong S. Introducing ratiometric fluorescence to MnO2 nanosheet-based biosensing: a simple, label-free ratiometric fluorescent sensor programmed by cascade logic circuit for ultrasensitive GSH detection. ACS Appl Mater Interfaces. 2017;9(31):25870–7.

    CAS  PubMed  Google Scholar 

  29. Liu Z, Zhang S, Lin H, Zhao M, Yao H, Zhang L, et al. Theranostic 2D ultrathin MnO2 nanosheets with fast responsibility to endogenous tumor microenvironment and exogenous NIR irradiation. Biomaterials. 2018;155:54–63.

    CAS  PubMed  Google Scholar 

  30. Zeng J, Goldfeld D, Xia Y. A plasmon-assisted optofluidic (PAOF) system for measuring the photothermal conversion efficiencies of gold nanostructures and controlling an electrical switch. Angew Chem Int Ed Engl. 2013;52(15):4169–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Wang S, Riedinger A, Li H, Fu C, Liu H, Li L, et al. Plasmonic copper sulfide nanocrystals exhibiting near-infrared photothermal and photodynamic therapeutic effects. ACS Nano. 2015;9(2):1788–800.

    CAS  PubMed  Google Scholar 

  32. Hessel CM, Pattani VP, Rasch M, Panthani MG, Koo B, Tunnell JW, et al. Copper selenide nanocrystals for photothermal therapy. Nano Lett. 2011;11(6):2560–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang Y, Dai C, Liu W, Wang Y, Ding F, Zou P, et al. Ultrathin films of a metal-organic framework prepared from 2-methylimidazole, manganese (II) and cobalt (II) with strong oxidase-mimicking activity for colorimetric determination of glutathione and glutathione reductase activity. Microchim Acta. 2019;186(6):340.

    Google Scholar 

  34. Beiraghi-Toosi A, Askarian R, Sadrabadi Haghighi F, Safarian M, Kalantari F, Hashemy SI. Burn-induced oxidative stress and serum glutathione depletion; a cross sectional study. Emerg. 2018;6(1):e54.

    Google Scholar 

  35. Scibior D, Skrzycki M, Podsiad M, Czeczot H. Glutathione level and glutathione-dependent enzyme activities in blood serum of patients with gastrointestinal tract tumors. Clin Biochem. 2008;41(10–11):852–8.

    CAS  PubMed  Google Scholar 

  36. Perry RR, Mazetta JA, Levin M, Barranco SC. Glutathione levels and variability in breast tumors and normal tissue. Cancer. 1993;72(3):783–7.

    CAS  PubMed  Google Scholar 

  37. Ellman G, Lysko H. A precise method for the determination of whole blood and plasma sulfhydryl groups. Anal Biochem. 1979;93(1):98–102.

    CAS  PubMed  Google Scholar 

  38. Owen JB, Butterfield DA. Measurement of oxidized/reduced glutathione ratio. Methods Mol Biol. 2010;648:269–77.

    CAS  PubMed  Google Scholar 

  39. Harris DC. Quantitative chemical analysis. 8th ed. W. H. Freeman and Company: New York, U. S. A; 2010.

    Google Scholar 

  40. Wang Y, Jiang K, Zhu J, Zhang L, Lin H. A FRET-based carbon dot-MnO2 nanosheet architecture for glutathione sensing in human whole blood samples. Chem Comm. 2015;51(64):12748–51.

    CAS  PubMed  Google Scholar 

  41. Calikoglu M, Unlu A, Tamer L, Ercan B, Bugdayci R, Atik U. The levels of serum vitamin C, malonyldialdehyde and erythrocyte reduced glutathione in chronic obstructive pulmonary disease and in healthy smokers. Clin Chem Lab Med. 2002;40(10):1028–31.

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge the TEM analysis provided by Dr. Huailin Fan (University of Jinan) and editorial assistance provided by Dr. Feimeng Zhou (University of Jinan).

Funding

We receive financial support from the Nature Science Foundation of China (Nos. 21906065, 21802052, and 21802051), the Natural Science Foundation of Shandong Province of China (Nos. ZR2019MB066 and ZR2019QB007), and the Shandong Provincial Program of Talent-Leading Teams.

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Authors and Affiliations

  1. Institute of Surface Analysis and Chemical Biology, University of Jinan, Jinan, 250022, Shandong, China

    Dandan Liu, Qingqing Tu, Xiaoying Wang, Qing Kang, Pengcheng Wang & Wenjuan Guo

  2. Department of Oncology and Radiotherapy, Shandong Provincial Qianfoshan Hospital, The First Hospital Affiliated with Shandong First Medical University, Jinan, 250014, Shandong, China

    Ying Han

  3. State Key Laboratory of Biobased Material and Green Papermaking, Qilu University of Technology, Jinan, 250353, Shandong, China

    Xiaoying Wang

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  1. Dandan Liu
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  2. Qingqing Tu
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  4. Xiaoying Wang
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  7. Wenjuan Guo
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Correspondence to Pengcheng Wang or Wenjuan Guo.

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The current study was in accordance with the 1964 Helsinki declaration and approved by the Medical Ethics Committee of Shandong Provincial Qianfoshan Hospital, affiliated with Shandong First Medical University. Written informed consent was obtained from each participant.

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Liu, D., Tu, Q., Han, Y. et al. A dual-modal colorimetric and photothermal assay for glutathione based on MnO2 nanosheets synthesized with eco-friendly materials. Anal Bioanal Chem 412, 8443–8450 (2020). https://doi.org/10.1007/s00216-020-02982-1

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