Folia Biologica
Journal of Cellular and Molecular Biology, Charles University 

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Fol. Biol. 2024, 70, 209-218

https://doi.org/10.14712/fb2024070040209

Effect of Cryoprotectants on Long-Term Storage of Oral Mucosal Epithelial Cells: Implications for Stem Cell Preservation and Proliferation Status

Joao Victor Cabral1, Natálie Smorodinová1,2, Eleni Voukali1, Lukáš Balogh1, Tomáš Kučera2, Vojtěch Kolín3, Pavel Studený4, Tomáš Vacík1, Kateřina Jirsová1

1Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic
2Institute of Histology and Embryology, First Faculty of Medicine, Charles University, Prague, Czech Republic
3Department of Pathology, Third Faculty of Medicine, Charles University and University Hospital Kralovske Vinohrady, Prague, Czech Republic
4Department of Ophthalmology, Third Faculty of Medicine, Charles University and University Hospital Kralovske Vinohrady, Prague, Czech Republic

Received July 2024
Accepted October 2024

References

1. Attico, E., Galaverni, G., Bianchi, E. et al. (2022) SOX2 is a univocal marker for human oral mucosa epithelium useful in post-COMET patient characterization. Int. J. Mol. Sci. 23, 5785. <https://doi.org/10.3390/ijms23105785>
2. Best, B. P. (2015) Cryoprotectant toxicity: facts, issues, and questions. Rejuvenation Res. 18, 422-436. <https://doi.org/10.1089/rej.2014.1656>
3. Booranapong, W., Kosrirukvongs, P., Duangsa-Ard, S. et al. (2022) Transplantation of autologous cultivated oral mucosal epithelial sheets for limbal stem cell deficiency at Siriraj hospital: a case series. J. Med. Case Rep. 16, 298. <https://doi.org/10.1186/s13256-022-03502-8>
4. Brejchova, K., Trosan, P., Studeny, P. et al. (2018) Characterization and comparison of human limbal explant cultures grown under defined and xeno-free conditions. Exp. Eye Res. 176, 20-28. <https://doi.org/10.1016/j.exer.2018.06.019>
5. Cabral, J. V., Jackson, C. J., Utheim, T. P. et al. (2020) Ex vivo cultivated oral mucosal epithelial cell transplantation for limbal stem cell deficiency: a review. Stem Cell Res. Ther. 11, 301. <https://doi.org/10.1186/s13287-020-01783-8>
6. Cabral, J. V., Voukali, E., Smorodinova, N. et al. (2024) Cultivation and characterization of oral mucosal epithelial cells on fibrin gel in a xenobiotic-free medium for the treatment of limbal stem cell deficiency. Exp. Eye Res. (Under review)
7. Cordeiro, R. M., Stirling, S., Fahy, G. M. et al. (2015) Insights on cryoprotectant toxicity from gene expression profiling of endothelial cells exposed to ethylene glycol. Cryobiology 71, 405-412. <https://doi.org/10.1016/j.cryobiol.2015.10.142>
8. Czysz, K., Minger, S., Thomas, N. (2015) DMSO efficiently down regulates pluripotency genes in human embryonic stem cells during definitive endoderm derivation and increases the proficiency of hepatic differentiation. PLoS One 10, e0117689. <https://doi.org/10.1371/journal.pone.0117689>
9. Hibino, Y., Hata, K., Horie, K. et al. (1996) Structural changes and cell viability of cultured epithelium after freezing storage. J. Craniomaxillofac. Surg. 24, 346-351. <https://doi.org/10.1016/S1010-5182(96)80035-7>
10. Hirayama, M., Satake, Y., Higa, K. et al. (2012) Transplantation of cultivated oral mucosal epithelium prepared in fibrin-coated culture dishes. Invest. Ophthalmol. Vis. Sci. 53, 1602-1609. <https://doi.org/10.1167/iovs.11-7847>
11. Ibars, E. P., Cortes, M., Tolosa, L. et al. (2016) Hepatocyte transplantation program: lessons learned and future strategies. World J. Gastroenterol. 22, 874-886. <https://doi.org/10.3748/wjg.v22.i2.874>
12. Jaiswal, A. N., Vagga, A. (2022) Cryopreservation: a review article. Cureus 14, e31564.
13. Jang, T. H., Park, S. C., Yang, J. H. et al. (2017) Cryopreservation and its clinical applications. Integr. Med. Res. 6, 12-18. <https://doi.org/10.1016/j.imr.2016.12.001>
14. Jones, K. B., Klein, O. D. (2013) Oral epithelial stem cells in tissue maintenance and disease: the first steps in a long journey. Int. J. Oral Sci. 5, 121-129. <https://doi.org/10.1038/ijos.2013.46>
15. Kaufman, S. C., Suri, K., Twite, M. et al. (2014) Recent advance in the cryopreservation of corneal limbal stem cells. Int. J. Eye Bank. 2, 1-7.
16. Leelahavanichkul, K., Gutkind, J. S. (2013) Oral and pharyngeal epithelial keratinocyte culture. Methods Mol. Biol. 945, 67-79. <https://doi.org/10.1007/978-1-62703-125-7_5>
17. Liu, J., Sheha, H., Fu, Y. et al. (2011) Oral mucosal graft with amniotic membrane transplantation for total limbal stem cell deficiency. Am. J. Ophthalmol. 152, 739-747.e1. <https://doi.org/10.1016/j.ajo.2011.03.037>
18. Lužnik, Z., Bertolin, M., Breda, C. et al. (2016) Preservation of ocular epithelial limbal stem cells: the new frontier in regenerative medicine. Adv. Exp. Med. Biol. 951, 179-189. <https://doi.org/10.1007/978-3-319-45457-3_15>
19. Lysak, D., Brychtova, M., Leba, M. et al. (2021) Long-term cryopreservation does not affect quality of peripheral blood stem cell grafts: a comparative study of native, short-term and long-term cryopreserved haematopoietic stem cells. Cell Transplant. 30, <https://doi.org/10.1177/9636897211-036004>
20. Ma, D. H., Hsueh, Y. J., Ma, K. S. et al. (2021) Long-term survival of cultivated oral mucosal epithelial cells in human cornea: generating cell sheets using an animal product-free culture protocol. Stem Cell Res. Ther. 12, 524. <https://doi.org/10.1186/s13287-021-02564-7>
21. Martin-Lopez, M., Rosell-Valle, C., Arribas-Arribas, B. et al. (2023) Bioengineered tissue and cell therapy products are efficiently cryopreserved with pathogen-inactivated human platelet lysate-based solutions. Stem Cell Res. Ther. 14, 69. <https://doi.org/10.1186/s13287-023-03300-z>
22. Mazur, P. (1970) Cryobiology: the freezing of biological systems. Science 168, 939-949. <https://doi.org/10.1126/science.168.3934.939>
23. Miyamoto, Y. (2023) Cryopreservation of cell sheets for regenerative therapy: application of vitrified hydrogel membranes. Gels 9, 321. <https://doi.org/10.3390/gels9040321>
24. Mohamed-Noriega, K., Toh, K. P., Poh, R. et al. (2011) Cornea lenticule viability and structural integrity after refractive lenticule extraction (ReLEx) and cryopreservation. Mol. Vis. 17, 3437-3449.
25. Morino, T., Takagi, R., Yamamoto, K. et al. (2019) Explant culture of oral mucosal epithelial cells for fabricating transplantable epithelial cell sheet. Regen. Ther. 10, 36-45. <https://doi.org/10.1016/j.reth.2018.10.006>
26. Murray, K. A., Gibson, M. I. (2022) Chemical approaches to cryopreservation. Nat. Rev. Chem. 6, 579-593. <https://doi.org/10.1038/s41570-022-00407-4>
27. Nakamura, T., Inatomi, T., Sotozono, C. et al. (2004) Transplantation of cultivated autologous oral mucosal epithelial cells in patients with severe ocular surface disorders. Br. J. Ophthalmol. 88, 1280-1284. <https://doi.org/10.1136/bjo.2003.038497>
28. Nishida, K., Yamato, M., Hayashida, Y. et al. (2004) Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. N. Engl. J. Med. 351, 1187-1196. <https://doi.org/10.1056/NEJMoa040455>
29. Oliva, J., Florentino, A., Bardag-Gorce, F. et al. (2019) Vitrification and storage of oral mucosa epithelial cell sheets. J. Tissue Eng. Regen. Med. 13, 1153-1163. <https://doi.org/10.1002/term.2864>
30. Osei-Bempong, C., Figueiredo, F. C., Lako, M. (2013) The limbal epithelium of the eye – a review of limbal stem cell biology, disease and treatment. Bioessays 35, 211-219. <https://doi.org/10.1002/bies.201200086>
31. Pellegrini, G., Rama, P., Di Rocco, A. et al. (2014) Concise review: hurdles in a successful example of limbal stem cell-based regenerative medicine. Stem Cells 32, 26-34. <https://doi.org/10.1002/stem.1517>
32. Pellegrini, G., Traverso, C. E., Franzi, A. T. et al. (1997) Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet 349, 990-993. <https://doi.org/10.1016/S0140-6736(96)11188-0>
33. Prabhasawat, P., Ekpo, P., Uiprasertkul, M. et al. (2016) Long-term result of autologous cultivated oral mucosal epithelial transplantation for severe ocular surface disease. Cell Tissue Bank. 17, 491-503. <https://doi.org/10.1007/s10561-016-9575-4>
34. Promprasit, D., Bumroongkit, K., Tocharus, C. et al. (2015) Cultivation and phenotypic characterization of rabbit epithelial cells expanded ex vivo from fresh and cryopreserved limbal and oral mucosal explants. Curr. Eye Res. 40, 274-281. <https://doi.org/10.3109/02713683.2014.917191>
35. R Core Team (2024) R: a language and environment for statistical computing. R Foundation for statistical computing. Vienna, Austria, https://www.R-project.org/.
36. Sambu, S. (2015) A Bayesian approach to optimizing cryopreservation protocols. PeerJ 3, e1039. <https://doi.org/10.7717/peerj.1039>
37. Stadnikova, A., Trosan, P., Skalicka, P. et al. (2019) Interleukin-13 maintains the stemness of conjunctival epithelial cell cultures prepared from human limbal explants. PLoS One 14, e0211861. <https://doi.org/10.1371/journal.pone.0211861>
38. Sui, X., Wen, C., Yang, J. et al. (2019) Betaine combined with membrane stabilizers enables solvent-free whole blood cryopreservation and one-step cryoprotectant removal. ACS Biomater. Sci. Eng. 5, 1083-1091. <https://doi.org/10.1021/acsbiomaterials.8b01286>
39. Sumida, K., Igarashi, Y., Toritsuka, N. et al. (2011) Effects of DMSO on gene expression in human and rat hepatocytes. Hum. Exp. Toxicol. 30, 1701-1709. <https://doi.org/10.1177/0960327111399325>
40. Trousil, J., Cabral, J. V., Voukali, E. et al. (2024) Electrospun poly(L-lactide-co-CL-lactide) nanofibrous scaffold as substrate for ex vivo limbal epithelial cell cultivation. Heliyon 10, e30970. <https://doi.org/10.1016/j.heliyon.2024.e30970>
41. Xiong, X., Jia, J., He, S. et al. (2010) Cryopreserved lip mucosa tissue derived keratinocytes can fabricate tissue engineered palatal mucosa equivalent. J. Biomed. Mater. Res. B Appl. Biomater. 94, 165-170. <https://doi.org/10.1002/jbm.b.31637>
42. Yang, J., Cai, N., Zhai, H. et al. (2016) Natural zwitterionic betaine enables cells to survive ultrarapid cryopreservation. Sci. Rep. 6, 37458. <https://doi.org/10.1038/srep37458>
43. Yang, J., Gao, L., Liu, M. et al. (2020) Advanced biotechnology for cell cryopreservation. Trans. Tianjin Univ. 26, 409-423. <https://doi.org/10.1007/s12209-019-00227-6>
44. Yeh, H. J., Yao, C. L., Chen, H. I. et al. (2008) Cryopreservation of human limbal stem cells ex vivo expanded on amniotic membrane. Cornea 27, 327-333. <https://doi.org/10.1097/ICO.0b013e31815dcfaf>
45. Zhao, G., Fu, J. (2017) Microfluidics for cryopreservation. Biotechnol. Adv. 35, 323-336. <https://doi.org/10.1016/j.biotechadv.2017.01.006>
46. Zieske, J. D., Mason, V. S., Wasson, M. E. et al. (1994) Basement membrane assembly and differentiation of cultured corneal cells: importance of culture environment and endothelial cell interaction. Exp. Cell Res. 214, 621-633. <https://doi.org/10.1006/excr.1994.1300>
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