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Marine Polysaccharides Carrageenans Enhance Eryptosis and Alter Lipid Order of Cell Membranes in Erythrocytes

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Abstract

Aim In the current study, hemocompatibility of three major commercially available types of carrageenans (ι, κ and λ) was investigated focusing on eryptosis. Materials and methods: Carrageenans of ι-, κ- and λ-types were incubated with washed erythrocytes (hematocrit 0.4%) at 0–1–5–10 g/L for either 24 h or 48 h. Incubation was followed by flow cytometry-based quantitative analysis of eryptosis parameters, including cell volume, cell membrane scrambling and reactive oxygen species (ROS) production, lipid peroxidation markers and confocal microscopy-based evaluation of intracellular Ca2+ levels, assessment of lipid order in cell membranes and the glutathione antioxidant system. Confocal microscopy was used to assess carrageenan cellular internalization using rhodamine B isothiocyanate-conjugated carrageenans. Results: All three types of carrageenans were found to trigger eryptosis. Pro-eryptotic properties were type-dependent and λ-carrageenan had the strongest impact inducing phosphatidylserine membrane asymmetry, changes in cell volume, Ca2+ signaling and oxidative stress characterized by ROS overproduction, activation of lipid peroxidation and severe glutathione system depletion. Eryptosis induction by carrageenans does not require their uptake by erythrocytes. Changes in physicochemical properties of cell membrane were also type-dependent. No carrageenan-induced generation of superoxide and hydroxyl radicals was observed in cell-free milieu. Conclusions: Our findings suggest that ι-, κ- and λ-types trigger eryptosis in a type-dependent manner and indicate that carrageenans can be further investigated as potential eryptosis-regulating therapeutic agents.

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Data availability

The data that support the findings of this study are available from the corresponding author Anton Tkachenko upon reasonable request.

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Funding

The study was supported by the Ministry of Health of Ukraine as a fragment of the research project entitled “Research on the Safety and Effectiveness of Food Additives Carrageenans (E407/E407a) and Their Oligosaccharide Fragments as Therapeutic Agents Capable of Modulating Programmed Cell Death, Namely Eryptosis, Necroptosis, Ferroptosis and Autophagy-Related Cell Death” (state registration number 0123U100179). The study of cell membranes using the fluorescent probe and flow cytometry was supported by the National Research Foundation of Ukraine under project No. 2021.01/0414.

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Authors and Affiliations

  1. Research Institute of Experimental and Clinical Medicine, Kharkiv National Medical University, 4 Nauky ave, 61022, Kharkiv, Ukraine

    Volodymyr Prokopiuk, Anatolii Onishchenko, Yevgen Posokhov & Anton Tkachenko

  2. Department of Cryobiochemistry, Institute for Problems of Cryobiology and Cryomedicine of the National Academy of Sciences of Ukraine, Kharkiv, 61015, Ukraine

    Volodymyr Prokopiuk

  3. Institute of Health, National University of Water and Environmental Engineering, 11 Soborna st, 33000, Rivne, Ukraine

    Liliya Tryfonyuk

  4. Department of Organic Chemistry, Biochemistry, Paints and Coatings, The National Technical University “Kharkiv Polytechnic Institute”, 2 Kyrpychova st, 61000, Kharkiv, Ukraine

    Yevgen Posokhov

  5. Department of Biochemistry, Kharkiv National Medical University, 4 Nauky ave., 61022, Kharkiv, Ukraine

    Tetyana Gorbach & Oksana Nakonechna

  6. Department of Biochemistry, V. N. Karazin Kharkiv National University, 4 Svobody sq., 61022, Kharkiv, Ukraine

    Yurii Kot & Kateryna Kot

  7. Institute for Scintillation Materials, National Academy of Sciences of Ukraine, 60 Nauky ave, 61072, Kharkiv, Ukraine

    Pavel Maksimchuk

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  1. Volodymyr Prokopiuk
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Contributions

Conceptualization – A.T., methodology – A.T., A.O. V.P., Ye.P., L.T., T.G., O.N., Yu. K., K.K. P.M., data analysis – A.T., A.O., V.P., L.T., Ye.P., P.M., Yu. K., K.K. Investigation – A.O. V.P., T.G., P.M., Ye.P., Yu. K., K.K., L.T. resources – A.T., V.P., Writing - Original Draft – A.T., Ye.P., Yu.K., Writing - Review & Editing – A.T, A.O., Ye.P, O.N., visualization – A.O., Ye.P., Yu. K., A.T., funding – A.T., V.P., project administration – A.T.

Corresponding author

Correspondence to Anton Tkachenko.

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Conflict of Interest

The authors declare no competing interests.

Ethics Approval

All experiments with laboratory animals involved were carried out following the legislative requirements and ethical standards in agreement with the EU Directive 2010/63/EU on the protection of animals used for scientific purposes, which is based on the Council of Europe Convention for the Protection of Vertebrate Animals used for Experimental and other Scientific Purposes (ETS123). The experimental design was approved by the Commission on Ethics and Bioethics at Kharkiv National Medical University, Kharkiv, Ukraine (minutes No 5 dated September 17, 2019).

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Prokopiuk, V., Onishchenko, A., Tryfonyuk, L. et al. Marine Polysaccharides Carrageenans Enhance Eryptosis and Alter Lipid Order of Cell Membranes in Erythrocytes. Cell Biochem Biophys (2024). https://doi.org/10.1007/s12013-024-01225-9

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