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Analysis of nanomaterial biocoronas in biological and environmental surroundings

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Abstract

A biomolecular coating, or biocorona, forms on the surface of engineered nanomaterials (ENMs) immediately as they enter biological or environmental systems, defining their biological and environmental identity and influencing their fate and performance. This biomolecular layer includes proteins (the protein corona) and other biomolecules, such as nucleic acids and metabolites. To ensure a meaningful and reproducible analysis of the ENMs-associated biocorona, it is essential to streamline procedures for its preparation, separation, identification and characterization, so that studies in different labs can be easily compared, and the information collected can be used to predict the composition, dynamics and properties of biocoronas acquired by other ENMs. Most studies focus on the protein corona as proteins are easier to monitor and characterize than other biomolecules and play crucial roles in receptor engagement and signaling; however, metabolites play equally critical roles in signaling. Here we describe how to reproducibly prepare and characterize biomolecule-coated ENMs, noting especially the steps that need optimization for different types of ENMs. The structure and composition of the biocoronas are characterized using general methods (transmission electron microscopy, dynamic light scattering, capillary electrophoresis–mass spectrometry and liquid chromatography–mass spectrometry) as well as advanced techniques, such as transmission electron cryomicroscopy, synchrotron-based X-ray absorption near edge structure and circular dichroism. We also discuss how to use molecular dynamic simulation to study and predict the interaction between ENMs and biomolecules and the resulting biocorona composition. The application of this protocol can provide mechanistic insights into the formation, composition and evolution of the ENM biocorona, ultimately facilitating the biomedical and agricultural application of ENMs and a better understanding of their impact in the environment.

Key points

  • The authors provide a detailed workflow for the isolation and biophysical characterization of biomolecule corona (biocorona) components (proteins and metabolites) through mass spectrometry, advanced structural techniques (for example, transmission electron cryomicroscopy and synchrotron-based X-ray absorption near edge structure) and molecular dynamic simulations to model ENM–biocorona interactions.

  • The designed pipeline normalizes the acquisition of data in different labs, increases their reproducibility, and facilitates their use for the prediction of the biocoronas acquired by less characterized ENMs.

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Fig. 1: Overview of the five main parts in the biocorona determination protocol.
Fig. 2
Fig. 3: Flowchart of the two ENM corona characterization assays using QCM-D.
Fig. 4: Flowchart of the BLI assay.
Fig. 5: General characterization of the biocorona on SWCNTs and Au ENMs.
Fig. 6: Structural characterization of the ENM protein corona.
Fig. 7: Identification and quantification of biocorona using CE–MS/MS.
Fig. 8: Identification and quantification of biocorona using nanoLC–MS/MS.
Fig. 9: Analysis of the protein corona from D. magna.
Fig. 10: QCM-D analysis of the interaction between ENMs and biocorona.
Fig. 11: Interaction dynamics between GDY, GDYO or MoS2 NMs and proteins determined with MD simulations.

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Data availability

Datasets for this protocol are based on the published research articles18,22,24,31,35,43,54,55,56,57,58. Other data related to this paper can be requested from the authors. Source data are provided with this paper.

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Acknowledgements

This research project was supported by the Engineering and Physical Sciences Research Council Impact Acceleration Accounts Developing Leaders (grant no. 1001634) and EU H2020 projects NanoSolveIT (grant agreement 814572), RiskGone (grant agreement 814425), NanoCommons (grant agreement 731032) and CompSafeNano (grant agreement 101008099), the National Key Research and Development Program of China (2023YFC3711500, 2021YFA1200900, 2022YFA1603700 and 2021YFE0112600), the Major Instrument Project of National Natural Science Foundation of China (22027810 and 32071402), the National Natural Science Foundation of China (22027810 and U2032107), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB36000000), the New Cornerstone Science Foundation (NCI202318), the National Postdoctoral Program for Innovative Talents (BX2021088), Project funded by China Postdoctoral Science Foundation (2021M700977) and the Special Research Assistant Funding Project of the Chinese Academy of Sciences (E37751R1 to M.C.). Royal Society International Exchange Programs (1853690 and 2122860) and the CAS PIFI award to I.L. (2020VBA0012) are also acknowledged. We acknowledge the University of Eastern Finland water program funded by the Saastamoinen foundation, the Wihuri foundation and the Olvi foundation. The authors acknowledge Milena L. Brito and Luelc S. Costa (LNNano/CNPEM) for discussions to elaborate the cryo-TEM protocol for characterization of ENM biocoronas.

Author information

Author notes

  1. These authors contributed equally: Peng Zhang, Mingjing Cao.

Authors and Affiliations

  1. School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, UK

    Peng Zhang & Zhiling Guo

  2. Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, China

    Peng Zhang, Laura-Jayne A. Ellis, Hossein Hayat Davoudi, Katie Reilly & Iseult Lynch

  3. CAS Center for Excellence in Nanoscience and CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, New Cornerstone Science Laboratory, National Center for Nanoscience and Technology of China, Beijing, China

    Mingjing Cao, Rong Cai & Chunying Chen

  4. Department of Women’s and Children’s Health, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool, UK

    Andrew J. Chetwynd

  5. Centre for Proteome Research, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK

    Andrew J. Chetwynd

  6. Institute of Medical Biochemistry, Medical University of Innsbruck, Innsbruck, Austria

    Klaus Faserl

  7. Department of Chemical Sciences, University of Padua, Padova, Italy

    Fazel Abdolahpur Monikh

  8. Institute for Nanomaterials, Advanced Technologies, and Innovation, Technical University of Liberec, Liberec, Czech Republic

    Fazel Abdolahpur Monikh

  9. Metabolomics and Analytics Centre, Leiden Academic Centre for Drug Research, Leiden University, Leiden, the Netherlands

    Wei Zhang & Rawi Ramautar

  10. Department of Chemistry and Biochemistry, Santa Clara University, Santa Clara, CA, USA

    Korin E. Wheeler

  11. Brazilian Nanotechnology National Laboratory (LNNano), Brazilian Centre for Research in Energy and Materials (CNPEM), Campinas, Brazil

    Diego Stéfani Teodoro Martinez

  12. Research Unit of Nanoscience and Technology, Chinese Academy of Medical Sciences, Beijing, China

    Chunying Chen

  13. GBA National Institute for Nanotechnology Innovation, Guangzhou, China

    Chunying Chen

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  1. Peng Zhang
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Contributions

P.Z., M.C., A.J.C., F.A.M., K.F., W.Z., R.R., L.-J.A.E., H.H.D., K.R., R.C., K.E.W., D.S.T.M., Z.G., C.C. and I.L. cowrote the manuscript. Z.G., P.Z., C.C., M.C. and I.L. oversaw the manuscript preparation and revised the manuscript.

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Correspondence to Zhiling Guo, Chunying Chen or Iseult Lynch.

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Key references using this protocol.

Cai, R. et al. Proc. Natl Acad. Sci. USA 119, e2200363119 (2022): https://doi.org/10.1073/pnas.2200363119

Ellis, L.-J. A. & Lynch, I. Environ. Sci. Nano 7, 3343–3359 (2020): https://doi.org/10.1039/D0EN00625D

Chetwynd, A. J. et al. Small 16, 2000295 (2020): https://doi.org/10.1002/smll.202000295

Guo, M. et al. Nano Lett. 21, 6005–6013 (2021): https://doi.org/10.1021/acs.nanolett.1c01048

Supplementary information

Supplementary Information

Supplementary Methods, Tables 1–8 and Figs. 1 and 2.

Source data

Source Data Figs. 5, 8, 10

Fig. 5: hydrodynamic radius and protein density values; Fig. 8: raw data of protein counts associated with the specific NMs; Fig. 10: frequency variation.

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Zhang, P., Cao, M., Chetwynd, A.J. et al. Analysis of nanomaterial biocoronas in biological and environmental surroundings. Nat Protoc (2024). https://doi.org/10.1038/s41596-024-01009-8

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