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Effect of space flight on the behavior of human retinal pigment epithelial ARPE-19 cells and evaluation of coenzyme Q10 treatment

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Abstract

Astronauts on board the International Space Station (ISS) are exposed to the damaging effects of microgravity and cosmic radiation. One of the most critical and sensitive districts of an organism is the eye, particularly the retina, and > 50% of astronauts develop a complex of alterations designated as spaceflight-associated neuro-ocular syndrome. However, the pathogenesis of this condition is not clearly understood. In the current study, we aimed to explore the cellular and molecular effects induced in the human retinal pigment ARPE-19 cell line by their transfer to and 3-day stay on board the ISS in the context of an experiment funded by the Agenzia Spaziale Italiana. Treatment of cells on board the ISS with the well-known bioenergetic, antioxidant, and antiapoptotic coenzyme Q10 was also evaluated. In the ground control experiment, the cells were exposed to the same conditions as on the ISS, with the exception of microgravity and radiation. The transfer of ARPE-19 retinal cells to the ISS and their living on board for 3 days did not affect cell viability or apoptosis but induced cytoskeleton remodeling consisting of vimentin redistribution from the cellular boundaries to the perinuclear area, underlining the collapse of the network of intermediate vimentin filaments under unloading conditions. The morphological changes endured by ARPE-19 cells grown on board the ISS were associated with changes in the transcriptomic profile related to the cellular response to the space environment and were consistent with cell dysfunction adaptations. In addition, the results obtained from ARPE-19 cells treated with coenzyme Q10 indicated its potential to increase cell resistance to damage.

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Funding

This project was coordinated and funded by the Italian Space Agency (ASI, grant 2016–6-U0 to M.L.) for space s tation experimentation within the national ISS utilization rights. The authors thank Fondazione Cassa di Risparmio Di Firenze (Italy) for financial support.

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Author notes

  1. Sergio Capaccioli and Matteo Lulli contributed equally to this study.

Authors and Affiliations

  1. ASAcampus Joint Laboratory, ASA Res. Div., Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, Università Degli Studi Di Firenze, Firenze, Italy

    Francesca Cialdai, Leonardo Vignali & Monica Monici

  2. Department of Experimental and Clinical Medicine, Università Degli Studi Di Firenze, Firenze, Italy

    Davide Bolognini

  3. Department of Life Sciences, Università Degli Studi Di Siena, Siena, Italy

    Nicola Iannotti

  4. Department of Biology and Biotechnology “Charles Darwin”, Università Di Roma “La Sapienza”, Roma, Italy

    Stefano Cacchione

  5. Department of Information Engineering, Università Degli Studi Di Firenze, Firenze, Italy

    Alberto Magi

  6. Kayser Italia S.R.L., Livorno, Italy

    Michele Balsamo, Marco Vukich, Gianluca Neri & Alessandro Donati

  7. Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, Università Degli Studi Di Firenze, viale Morgagni 50, 50134, Firenze, Italy

    Sergio Capaccioli & Matteo Lulli

Authors
  1. Francesca Cialdai
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  2. Davide Bolognini
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  3. Leonardo Vignali
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  4. Nicola Iannotti
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  5. Stefano Cacchione
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  6. Alberto Magi
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  7. Michele Balsamo
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  8. Marco Vukich
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  9. Gianluca Neri
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  10. Alessandro Donati
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  11. Monica Monici
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  12. Sergio Capaccioli
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  13. Matteo Lulli
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Corresponding author

Correspondence to Matteo Lulli.

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Cialdai, F., Bolognini, D., Vignali, L. et al. Effect of space flight on the behavior of human retinal pigment epithelial ARPE-19 cells and evaluation of coenzyme Q10 treatment. Cell. Mol. Life Sci. 78, 7795–7812 (2021). https://doi.org/10.1007/s00018-021-03989-2

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  • DOI: https://doi.org/10.1007/s00018-021-03989-2

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