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Drying of graphene oxide: effects on red blood cells and protein corona formation

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Abstract

In this work, we performed an integrated study on the physicochemical changes of graphene oxide (GO) during the drying process in terms of their biological effects on red blood cells (hemolysis) and interactions with human plasma (protein corona formation). GO in aqueous dispersion (GO-Disp) was dried exploring two procedures: using a vacuum system at room temperature (GO-VD) and lyophilization (GO-LP). The nanomaterials were well characterized by microscopic (TEM, SEM, and AFM), spectroscopic (FTIR, UV–Vis, Raman, and 13C NMR), and XRD techniques. The lyophilization process produced a nanomaterial with a three-dimensional porous macrostructure and the lowest oxidation degree. In contrast, the vacuum-drying process at room temperature provided a nanomaterial with a film-like macrostructure, presenting a higher oxidation degree as well as physicochemical properties more similar to those of GO-Disp. All of the nanomaterials adsorbed human plasma proteins; however, the protein adsorption was more selective for GO-Disp. GO-VD induced hemolysis of red blood cells in a lower concentration than GO-Disp and GO-LP, but the protein corona formation suppressed the hemolytic effect for all nanomaterials. Finally, our results indicate that the method applied to dry GO nanomaterials has a critical influence on their nanobiointeractions with cells and proteins, suggesting that more attention should be paid to biomedical applications and toxicological evaluations associated with these promising nanomaterials.

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Acknowledgements

This work is “in memoriam” of Professor Oswaldo Luiz Alves and Dr Douglas Soares da Silva. The authors acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Instituto Nacional de Ciência e Tecnologia em Materiais Complexos Funcionais (INCT-Inomat) and NanoBioss/SisNANO/MCTI for financial support. The authors acknowledge the Open facilities: Nanotoxicology and Nanosafety (NANOTOX) and Biophysics of Macromolecules (BFM) at CNPEM. The authors further acknowledge the Hemocenter of the School of Medicine at the UNICAMP for providing the plasma and red cells from human blood for the experiments.

Funding

Financial support was received by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) with a research grant (process number 88882.329207/2019-01).

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Authors and Affiliations

  1. NanoBioss Laboratory and Solid State Chemistry Laboratory (LQES), Institute of Chemistry, Universidade Estadual de Campinas (UNICAMP), Campinas, SP, Brazil

    Djalma Lucas de Sousa Maia, Carlos Henrique Zanini Martins, Leandro Carneiro Fonseca, Douglas Soares da Silva, Diego Stéfani Teodoro Martinez & Oswaldo Luiz Alves

  2. Center for Agricultural, Environmental and Biological Sciences–Federal University of Reconcavo of Bahia (CCAAB–UFRB), Cruz das Almas, BA, 44380-000, Brazil

    Djalma Lucas de Sousa Maia

  3. Agricultural Technological Center of the State of Bahia (CETAB), Salvador, BA, 40296-710, Brazil

    Djalma Lucas de Sousa Maia & Kelly Barbosa da Silva

  4. Brazilian Nanotechnology National Laboratory (LNNano), Brazilian Center for Research in Energy and Materials (CNPEM), Campinas, SP, 13083-970, Brazil

    Francine Côa, Lidiane Silva Franqui, Fabrício de Souza Delite & Diego Stéfani Teodoro Martinez

  5. Center of Nuclear Energy in Agriculture (CENA), University of São Paulo (USP), Piracicaba, SP, 13400-970, Brazil

    Francine Côa & Diego Stéfani Teodoro Martinez

  6. School of Technology, Universidade Estadual de Campinas (UNICAMP), Limeira, SP, 13484-332, Brazil

    Lidiane Silva Franqui & Diego Stéfani Teodoro Martinez

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  1. Djalma Lucas de Sousa Maia
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Contributions

DLSM did conceptualization, methodology, experiments, investigation, data curation, writing—original draft. FC did experiments, data curation and analysis, writing—original draft, review and editing. LSF, LCF, DSS performed data analysis, conduction of experiments, writing—initial draft. KBS and CHZM contributed to conceptualization, review of data, writing—initial draft. FSD was involved in methodology, conduction of experiments and data curation. DSTM and OLA done project administration, supervision, validation, writing—review and editing.

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Correspondence to Djalma Lucas de Sousa Maia or Diego Stéfani Teodoro Martinez.

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This work was approved by the Research Ethical Committee (No. 5.719.081) from the University of Campinas linked to the Plataforma Brasil system at the Ministry of Health/Brazil.

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Supplementary file1 (DOCX 494 KB)

The online version contains supplementary material available. Table S1 presented the chemical composition results of GO samples analyzed by energy-dispersive spectroscopy (EDS). Table S2 presented the total protein quantification in the human plasma measured by Braford assay. And the total protein profile of human plasma applied in this study was demonstrated by SDS-PAGE in supplementary material (Figure S1).

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de Sousa Maia, D.L., Côa, F., da Silva, K.B. et al. Drying of graphene oxide: effects on red blood cells and protein corona formation. J Mater Sci 59, 577–592 (2024). https://doi.org/10.1007/s10853-023-09163-2

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