Skip to main content
SpringerLink
Log in

2-D/2-D heterostructured biomimetic enzyme by interfacial assembling Mn3(PO4)2 and MXene as a flexible platform for realtime sensitive sensing cell superoxide

  • Research Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

It is critical for fabricating flexible biosensors with both high sensitivity and good selectivity to realize real-time monitoring superoxide anion (O2•−), a specific reactive oxygen species that plays critical roles in various biological processes. This work delicately designs a Mn3(PO4)2/MXene heterostructured biomimetic enzyme by assembling two-dimensional (2-D) Mn3(PO4)2 nanosheets with biomimetic activity and 2-D MXene nanosheets with high conductivity and abundant functional groups. The 2-D nature of the two components with strong interfacial interaction synergistically enables the heterostructure an excellent flexibility with retained 100% of the response when to reach a bending angle up to 180°, and 96% of the response after 100 bending/relaxing cycles. It is found that the surface charge state of the heterostructure promotes the adsorption of O2•−, while the high-energy active site improves electrochemical oxidation of O2•−. The Mn3(PO4)2/MXene as a sensing platform towards O2•− achieves a high sensitivity of 64.93 µA·µM−1·cm−2, a wide detection range of 5.75 nM to 25.93 µM, and a low detection limit of 1.63 nM. Finally, the flexible heterostructured sensing platform realizes real-time monitoring of O2•− in live cell assays, offering a promising flexible biosensor towards exploring various biological processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Zhang, Y. J.; He, P.; Luo, M.; Xu, X. W.; Dai, G. Z.; Yang, J. L. Highly stretchable polymer/silver nanowires composite sensor for human health monitoring. Nano Res. 2020, 13, 919–926.

    CAS  Google Scholar 

  2. Das, P. S.; Chhetry, A.; Maharjan, P.; Rasel, M. S.; Park, J. Y. A laser ablated graphene-based flexible self-powered pressure sensor for human gestures and finger pulse monitoring. Nano Res. 2019, 12, 1789–1795.

    CAS  Google Scholar 

  3. Yang, Y. R.; Gao, W. Wearable and flexible electronics for continuous molecular monitoring. Chem. Soc. Rev. 2019, 48, 1465–1491.

    CAS  Google Scholar 

  4. Guo, Y. C.; Fang, Z. Q.; Du, M. D.; Yang, L.; Shao, L. H.; Zhang, X. R.; Li, L; Shi, J. D.; Tao, J. S.; Wang, J. F. et al. Flexible and biocompatible nanopaper-based electrode arrays for neural activity recording. Nano Res. 2018, 11, 5604–5614.

    CAS  Google Scholar 

  5. Yu, Y.; Nyein, H. Y. Y.; Gao, W.; Javey, A. Flexible electrochemical bioelectronics: The rise of in situ bioanalysis. Adv. Mater. 2020, 32, 1902083.

    CAS  Google Scholar 

  6. Hsu, M. S.; Chen, Y. L.; Lee, C. Y.; Chiu, H. T. Gold nanostructures on flexible substrates as electrochemical dopamine sensors. ACS Appl. Mater. Interfaces 2012, 4, 5570–5575.

    CAS  Google Scholar 

  7. Kurdekar, A. D.; Chunduri, L. A. A.; Manohar, C. S.; Haleyurgirisetty, M. K.; Hewlett, I. K.; Venkataramaniah, K. Streptavidin-conjugated gold nanoclusters as ultrasensitive fluorescent sensors for early diagnosis of HIV infection. Sci. Adv. 2018, 4, eaar6280.

    CAS  Google Scholar 

  8. Lan, Y.; Yang, Y.; Wang, Y.; Wu, Y.; Cao, Z. Y.; Huo, S.; Jiang, L. H.; Guo, Y. C.; Wu, Y. Q.; Yan, B. et al. High-temperature-annealed flexible carbon nanotube network transistors for high-frequency wearable wireless electronics. ACS Appl. Mater. Interfaces 2020, 12, 26145–26152.

    CAS  Google Scholar 

  9. Wang, Z. R.; Hao, Z.; Yu, S. F.; De Moraes, C. G.; Suh, L. H.; Zhao, X. Z.; Lin, Q. An ultraflexible and stretchable aptameric graphene nanosensor for biomarker detection and monitoring. Adv. Funct. Mater. 2019, 29, 1905202.

    CAS  Google Scholar 

  10. Liu, Y.; Nie, Y. X.; Wang, M. K.; Zhang, Q.; Ma, Q. Distance-dependent plasmon-enhanced electrochemiluminescence biosensor based on MoS2 nanosheets. Biosens. Bioelectron. 2020, 148, 111823.

    CAS  Google Scholar 

  11. Li, Y.; Zhao, L. H.; Yao, Y.; Guo, X. F. Single-molecule nanotechnologies: An evolution in biological dynamics detection. ACS Appl. Bio Mater. 2020, 3, 68–85.

    Google Scholar 

  12. Li, H. T.; Huang, Y. Y.; Hou, G. H.; Xiao, A. X.; Chen, P. W.; Liang, H.; Huang, Y. G.; Zhao, X. T.; Liang, L. L.; Feng, X. H. et al. Singlemolecule detection of biomarker and localized cellular photothermal therapy using an optical microfiber with nanointerface. Sci. Adv. 2019, 5, eaax4659.

    CAS  Google Scholar 

  13. He, X. P.; Zhu, B. W.; Zang, Y.; Li, J.; Chen, G. R.; Tian, H.; Long, Y. T. Dynamic tracking of pathogenic receptor expression of live cells using pyrenyl glycoanthraquinone-decorated graphene electrodes. Chem. Sci. 2015, 6, 1996–2001.

    CAS  Google Scholar 

  14. Yang, L.; Mih, N.; Anand, A.; Park, J. H.; Tan, J.; Yurkovich, J. T.; Monk, J. M.; Lloyd, C. J.; Sandberg, T. E.; Seo, S. W. et al. Cellular responses to reactive oxygen species are predicted from molecular mechanisms. Proc. Natl. Acad. Sci. USA 2019, 116, 14368–14373.

    CAS  Google Scholar 

  15. Guo, C. X.; Zheng, X. T.; Lu, Z. S.; Lou, X. W.; Li, C. M. Biointerface by cell growth on layered graphene-artificial peroxidase-protein nanostructure for in situ quantitative molecular detection. Adv. Mater. 2010, 22, 5164–5167.

    CAS  Google Scholar 

  16. Cheng, W. W.; Teng, X.; Lu, C. Structurally ordered catalyst-amplified chemiluminescence signals. Anal. Chem. 2020, 92, 5456–5463.

    CAS  Google Scholar 

  17. Chen, L. Y.; Cho, M. K.; Wu, D.; Kim, H. M.; Yoon, J. Two-photon fluorescence probe for selective monitoring of superoxide in live cells and tissues. Anal. Chem. 2019, 91, 14691–14696.

    CAS  Google Scholar 

  18. Rahman, M. A.; Kothalam, A.; Choe, E. S.; Won, M. S.; Shim, Y. B. Stability and sensitivity enhanced electrochemical in vivo superoxide microbiosensor based on covalently co-immobilized lipid and cytochrome c. Anal. Chem. 2012, 84, 6654–6660.

    CAS  Google Scholar 

  19. Yildirim, O.; Derkus, B. Triazine-based 2D covalent organic frameworks improve the electrochemical performance of enzymatic biosensors. J. Mater. Sci. 2020, 55, 3034–3044.

    CAS  Google Scholar 

  20. Yang, H. X.; Hou, J. G.; Wang, Z. H.; Zhang, T. T.; Xu, C. X. An ultrasensitive biosensor for superoxide anion based on hollow porous PtAg nanospheres. Biosens. Bioelectron. 2018, 117, 429–435.

    CAS  Google Scholar 

  21. Luo, Y. P.; Tian, Y.; Rui, Q. Electrochemical assay of superoxide based on biomimetic enzyme at highly conductive TiO2 nanoneedles: From principle to applications in living cells. Chem. Commun. 2009, 3014–3016.

  22. Barnese, K.; Gralla, E. B.; Cabelli, D. E.; Valentine, J. S. Manganous phosphate acts as a superoxide dismutase. J. Am. Chem. Soc. 2008, 130, 4604–4606.

    CAS  Google Scholar 

  23. Ma, X. Q.; Hu, W. H.; Guo, C. X.; Yu, L.; Gao, L. X.; Xie, J. L.; Li, C. M. DNA-templated biomimetic enzyme sheets on carbon nanotubes to sensitively in situ detect superoxide anions released from cells. Adv. Funct. Mater. 2014, 24, 5897–5903.

    CAS  Google Scholar 

  24. Zou, Z.; Ma, X. Q.; Zou, L.; Shi, Z. Z.; Sun, Q. Q.; Liu, Q.; Liang, T. T.; Li, C. M. Tailoring pore structures with optimal mesopores to remarkably promote DNA adsorption guiding the growth of active Mn3(PO4)2 toward sensitive superoxide biomimetic enzyme sensors. Nanoscale 2019, 11, 2624–2630.

    CAS  Google Scholar 

  25. Wang, Y.; Wang, D.; Sun, L. H.; Xue, P.; Wang, M. Q.; Lu, Z. S.; Wang, F.; Xia, Q. Y.; Xu, M. W.; Bao, S. J. Constructing high effective nano-Mn3(PO4)2-chitosan in situ electrochemical detection interface for superoxide anions released from living cell. Biosens. Bioelectron. 2019, 133, 133–140.

    CAS  Google Scholar 

  26. Cai, X.; Wang, Z. X.; Zhang, H. H.; Li, Y. F.; Chen, K. C.; Zhao, H. L.; Lan, M. B. Carbon-mediated synthesis of shape-controllable manganese phosphate as nanozymes for modulation of superoxide anions in HeLa cells. J. Mater. Chem. B 2019, 7, 401–407.

    CAS  Google Scholar 

  27. Gao, J. J.; Liu, H.; Tong, C.; Pang, L. Y.; Feng, Y. Q.; Zuo, M. G.; Wei, Z. Q.; Li, J. Q. Hemoglobin-Mn3(PO4)2 hybrid nanoflower with opulent electroactive centers for high-performance hydrogen peroxide electrochemical biosensor. Sens. Actuators B Chem. 2020, 307, 127628.

    Google Scholar 

  28. Naguib, M.; Kurtoglu, M.; Presser, V.; Lu, J.; Niu, J. J.; Heon, M.; Hultman, L.; Gogotsi, Y.; Barsoum, M. W. Two-dimensional nanocrystals produced by exfoliation of Ti3AlC2. Adv. Mater. 2011, 23, 4248–4253.

    CAS  Google Scholar 

  29. Xie, X. H.; Chen, S. G.; Ding, W.; Nie, Y.; Wei, Z. D. An extraordinarily stable catalyst: Pt NPs supported on two-dimensional Ti3C2X2 (X = OH, F) nanosheets for oxygen reduction reaction. Chem. Commun. 2013, 49, 10112–10114.

    CAS  Google Scholar 

  30. Gao, G. P.; O’Mullane, A. P.; Du, A. J. 2D MXenes: A new family of promising catalysts for the hydrogen evolution reaction. ACS Catal. 2017, 7, 494–500.

    CAS  Google Scholar 

  31. Wu, Q.; Li, N. B.; Wang, Y.; Xu, Y. C.; Wu, J. D.; Jia, G. R.; Ji, F. J.; Fang, X. D.; Chen, F. F.; Cui, X. Q. Ultrasensitive and selective determination of carcinoembryonic antigen using multifunctional ultrathin amino-functionalized Ti3C2-MXene nanosheets. Anal. Chem. 2020, 92, 3354–3360.

    CAS  Google Scholar 

  32. Liu, H.; Duan, C. Y.; Yang, C. H.; Shen, W. Q.; Wang, F.; Zhu, Z. F. A novel nitrite biosensor based on the direct electrochemistry of hemoglobin immobilized on MXene-Ti3C2. Sens. Actuators B Chem. 2015, 218, 60–66.

    CAS  Google Scholar 

  33. Yu, M. Z.; Zhou, S.; Wang, Z. Y.; Zhao, J. J.; Qiu, J. S. Boosting electrocatalytic oxygen evolution by synergistically coupling layered double hydroxide with MXene. Nano Energy 2018, 44, 181–190.

    CAS  Google Scholar 

  34. Zheng, J. S.; Wang, B.; Jin, Y. Z.; Weng, B.; Chen, J. C. Nanostructured MXene-based biomimetic enzymes for amperometric detection of superoxide anions from HepG2 cells. Microchim. Acta 2019, 186, 95.

    Google Scholar 

  35. Mohammadniaei, M.; Koyappayil, A.; Sun, Y.; Min, J. H.; Lee, M. H. Gold nanoparticle/MXene for multiple and sensitive detection of oncomiRs based on synergetic signal amplification. Biosens. Bioelectron. 2020, 159, 112208.

    CAS  Google Scholar 

  36. Wang, H.; Li, H.; Huang, Y.; Xiong, M. H.; Wang, F.; Li, C. A label-free electrochemical biosensor for highly sensitive detection of gliotoxin based on DNA nanostructure/MXene nanocomplexes. Biosens. Bioelectron. 2019, 142, 111531.

    CAS  Google Scholar 

  37. Hu, F. X.; Kang, Y. J.; Du, F.; Zhu, L.; Xue, Y. H.; Chen, T.; Dai, L. M.; Li, C. M. Living cells directly growing on a DNA/Mn3(PO4)2-immobilized and vertically aligned CNT array as a free-standing hybrid film for highly sensitive in situ detection of released superoxide anions. Adv. Funct. Mater. 2015, 25, 5924–5932.

    CAS  Google Scholar 

  38. Neher, G.; Salguero, T. T. δ-polymorph of manganese phosphate. Cryst. Growth Des. 2017, 17, 4864–4872.

    CAS  Google Scholar 

  39. Mashtalir, O.; Naguib, M.; Mochalin, V. N.; Dall’Agnese, Y.; Heon, M.; Barsoum, M. W.; Gogotsi, Y. Intercalation and delamination of layered carbides and carbonitrides. Nat. Commun. 2013, 4, 1716.

    Google Scholar 

  40. Xue, Q.; Zhang, H. J.; Zhu, M. S.; Pei, Z. X.; Li, H. F.; Wang, Z. F.; Huang, Y.; Huang, Y.; Deng, Q. H.; Zhou, J. et al. Photoluminescent Ti3C2 MXene quantum dots for multicolor cellular imaging. Adv. Mater. 2017, 29, 1604847.

    Google Scholar 

  41. Wang, F.; Yang, C. H.; Duan, M.; Tang, Y.; Zhu, J. F. TiO2 nanoparticle modified organ-like Ti3C2 MXene nanocomposite encapsulating hemoglobin for a mediator-free biosensor with excellent performances. Biosens. Bioelectron. 2015, 74, 1022–1028.

    CAS  Google Scholar 

  42. Zhu, J. F.; Tang, Y.; Yang, C. H.; Wang, F.; Cao, M. J. Composites of TiO2 nanoparticles deposited on Ti3C2 MXene nanosheets with enhanced electrochemical performance. J. Electrochem. Soc. 2016, 163, A785–A791.

    CAS  Google Scholar 

  43. Green, M. A.; Pillai, S. Harnessing plasmonics for solar cells. Nat. Photonics 2012, 6, 130–132.

    CAS  Google Scholar 

  44. Guo, C. X.; Xie, J. L.; Yang, H. B.; Li, C. M. Au@CdS core-shell nanoparticles-modified ZnO nanowires photoanode for efficient photoelectrochemical water splitting. Adv. Sci. 2015, 2, 1500135.

    Google Scholar 

  45. Xu, M.; Obodo, D.; Yadavalli, V. K. The design, fabrication, and applications of flexible biosensing devices. Biosens. Bioelectron. 2019, 124–125, 96–114.

    Google Scholar 

  46. Guo, C. X.; Zheng, Y.; Ran, J. R.; Xie, F. X.; Jaroniec, M.; Qiao, S. Z. Engineering high-energy interfacial structures for high-performance oxygen-involving electrocatalysis. Angew. Chem., Int. Ed. 2017, 56, 8539–8543.

    CAS  Google Scholar 

  47. Guo, C. X.; Li, C. M. Room temperature-formed iron-doped nickel hydroxide on nickel foam as a 3D electrode for low polarized and high-current-density oxygen evolution. Chem. Commun. 2018, 54, 3262–3265.

    CAS  Google Scholar 

  48. Jin, K.; Park, J.; Lee, J.; Yang, K. D.; Pradhan, G. K.; Sim, U.; Jeong, D.; Jang, H. L.; Park, S.; Kim, D. et al. Hydrated manganese(II) phosphate (Mn3(PO4)2-3H2O) as a water oxidation catalyst. J. Am. Chem. Soc. 2014, 136, 7435–7443.

    CAS  Google Scholar 

  49. Yang, C.; Dong, L.; Chen, Z. X.; Lu, H. B. High-performance all-solid-state supercapacitor based on the assembly of graphene and manganese(II) phosphate nanosheets. J. Phys. Chem. C 2014, 118, 18884–18891.

    CAS  Google Scholar 

  50. Wang, J. T.; Chen, P. P.; Shi, B. B.; Guo, W. W.; Jaroniec, M.; Qiao, S. Z. A regularly channeled lamellar membrane for unparalleled water and organics permeation. Angew. Chem., Int. Ed. 2018, 57, 6814–6818.

    CAS  Google Scholar 

  51. Peng, J. H.; Chen, X. Z.; Ong, W. J.; Zhao, X. J.; Li, N. Surface and heterointerface engineering of 2D MXenes and their nanocomposites: Insights into electro- and photocatalysis. Chem 2019, 5, 18–50.

    CAS  Google Scholar 

  52. Zhong, R. B.; Tang, Q.; Wang, S. P.; Zhang, H. B.; Zhang, F.; Xiao, M. S.; Man, T. T.; Qu, X. M.; Li, L.; Zhang, W. J. et al. Self-assembly of enzyme-like nanofibrous G-molecular hydrogel for printed flexible electrochemical sensors. Adv. Mater. 2018, 30, 1706887.

    Google Scholar 

  53. Chung, S.; Cho, K.; Lee, T. Recent progress in inkjet-printed thin-film transistors. Adv. Sci. 2019, 6, 1801445.

    Google Scholar 

Download references

Acknowledgements

We greatly thank financial support from the National Natural Science Foundation of China (Nos. 21972102, 21705115 and 21605110), the Natural Science Foundation of Jiangsu Province of China (No. BK20170378), the Natural Science Research Foundation of Jiangsu Higher Education Institutions (No. 17KJB150036), Jiangsu Laboratory of Biological and Chemical Sensing and Biochip, Jiangsu Key Laboratory of Micro/Nano Thermo Fluidics and Green Energy, Jiangsu Innovation and Entrepreneurship Plan.

Author information

Author notes

  1. Shen Fei Zhao and Fang Xin Hu contributed equally to this work.

Authors and Affiliations

  1. Institute of Materials Science and Devices, Suzhou University of Science and Technology, Suzhou, 215009, China

    Shen Fei Zhao, Fang Xin Hu, Zhuan Zhuan Shi, Chun Xian Guo & Chang Ming Li

  2. Institute for Clean Energy and Advanced Materials, Southwest University, Chongqing, 400715, China

    Jing Jing Fu, Yue Chen & Chang Ming Li

  3. State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing, 400715, China

    Fang Yin Dai

  4. Institute for Advanced Cross-field Science & College of Life Science, Qingdao University, Qingdao, 200671, China

    Chang Ming Li

Authors
  1. Shen Fei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fang Xin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhuan Zhuan Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Jing Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yue Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fang Yin Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chun Xian Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chang Ming Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Chun Xian Guo or Chang Ming Li.

Electronic Supplementary Material

12274_2020_3130_MOESM1_ESM.pdf

2-D/2-D heterostructured biomimetic enzyme by interfacial assembling Mn3(PO4)2 and MXene as a flexible platform for realtime sensitive sensing cell superoxide

Supplementary material, approximately 10.0 MB.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, S.F., Hu, F.X., Shi, Z.Z. et al. 2-D/2-D heterostructured biomimetic enzyme by interfacial assembling Mn3(PO4)2 and MXene as a flexible platform for realtime sensitive sensing cell superoxide. Nano Res. 14, 879–886 (2021). https://doi.org/10.1007/s12274-020-3130-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-020-3130-0

Keywords

Search

Navigation