Development of Method for Three-Dimensional Cultivation of Human Mesenchymal Stem/Stromal Cells Using Cellulose Scaffolds

I. K. Kuneev; Кунеев И. К.; J. S. Ivanova; Иванова Ю. С.; Y. A. Nashchekina; Нащекина Ю. А.; E. K. Patronova; Патронова Е. К.; A. V. Sokolova; Соколова А. В.; A. P. Domnina; Домнина А. П.

doi:10.31857/S0041377123020037

Development of Method for Three-Dimensional Cultivation of Human Mesenchymal Stem/Stromal Cells Using Cellulose Scaffolds

Authors: Kuneev I.K.¹, Ivanova J.S.¹, Nashchekina Y.A.¹, Patronova E.K.¹, Sokolova A.V.¹, Domnina A.P.¹
Affiliations:
1. Institute of Cytology, Russian Academy of Sciences
Issue: Vol 65, No 2 (2023)
Pages: 170-180
Section: Articles
URL: https://journals.rcsi.science/0041-3771/article/view/140100
DOI: https://doi.org/10.31857/S0041377123020037
EDN: https://elibrary.ru/LWOREJ
ID: 140100

Cite item

Full Text

Open Access
Restricted Access

Access granted
Restricted Access

Subscription Access

Abstract
About the authors
References
Supplementary files
Statistics

Abstract

The development of methods for culturing cells in three-dimensional systems is an urgent focus of modern cell biology. When cultured in the 3D system, a tissue-specific architecture is reproduced and the real microenvironment and cell behavior in vivo are more precisely recreated. Human mesenchymal stem/stromal cells (MSCs) are typically isolated and cultured as a monolayer 2D culture. In this work, we developed a method for three-dimensional cultivation and tissue-specific decidual differentiation of MSCs isolated from human endometrial tissue using a matrix derived from decellularized apple. Decellularized apple matrices have sufficient mechanical strength, are biocompatible, accessible, easy to use, and have ample scope for surface modification. This cell culture system is suitable for both confocal microscopy and flow cytometry studies. The model we developed can become the basis for the creation of new cell products and tissue-engineering structures in the field of regenerative biomedicine.

Keywords

3D cultivation, decellularized plants, endometrial mesenchymal stem/stromal cells, decidual differentiation

References

Домнина А.П., Новикова П.В., Фридлянская И.И., Шилина М.А., Зенин В.В. Никольский Н.Н. 2015. Индукция децидуальной дифференцировки в эндометриальных мезенхимных стволовых клетках. Цитология. Т. 57. № 12. С. 880. (Domnina A.P., Novikova P.V., Fridlyanskaya I.I., Shilina M.A., Zenin V.V., Nikolsky N.N. 2016. Induction of decidual differentiation of endometrial mesenchymal stem cells. Tsitologiya. V. 57. № 12. P. 880.)
Земелько В.И., Гринчук Т.М., Домнина А.П., Арцыбашева И.В., Зенин В.В., Кирсанов А.А., Бичевая Н.К., Корсак В.С., Никольский Н.Н. 2011. Мультипотентные мезенхимные стволовые клетки десквамированного эндометрия. Выделение, характеристика и использование в качестве фидерного слоя для культивирования эмбриональных стволовых линий человека. Цитология. Т. 53. № 12. С. 919. (Zemelko V.I., Grinchuk T.M., Domnina A.P., Artzibasheva I.V., Zenin V.V., Kirsanov A.A., Bichevaia N.K., Korsak V.S., Nikolsky N.N. 2012. Multipotent mesenchymal stem cells of desquamated endometrium: isolation, characterization and use as feeder layer for maintenance of human embryonic stem cell lines. Cell Tiss. B-iol. (Tsitologiya). V. 6. P. 1.)
Мусина Р.А., Белявский А.В., Тарусова О.В., Соловьева Е.В., Сухих Г.Т. 2008. Мезенхимные стволовые клетки эндометрия, полученные из менструальной крови. Кл. техн. биол. мед. Т. 2. С. 110. (Musina R.A., Tarusova O.V., Solovyova E.V., Sukhikh G.T., Belyavski A.V. 2008. Endometrial mesenchymal stem cells isolated from the menstrual blood. V. 145. P. 539)
Bartosh T.J., Ylostalo J.H. 2019. Efficacy of 3D culture priming is maintained in human mesenchymal stem cells after extensive expansion of the cells. Cells. V. 8. P. 1031. https://doi.org/10.3390/cells8091031
Baruffaldi D., Palmara G., Pirri C., Frascella F. 2021. 3D cell culture: recent development in materials with tunable stiffness. ACS Applied Bio Materials. V. 4. P. 2233. https://doi.org/10.1021/acsabm.0c01472
Bilirgen A.C., Toker M., Odabas S., Yetisen A. K., Garipcan B., Tasoglu S. 2021. Plant-based scaffolds in tissue engineering. ACS Biomat. Sci. Eng. V. 7. P. 926. https://doi.org/10.1021/acsbiomaterials.0c01527
Bou-Ghannam S., Kim K., Grainger D.W. 2021. 3D cell sheet structure augments mesenchymal stem cell cytokine production. Sci Rep. V. 11. P. 8170. https://doi.org/10.1038/s41598-021-87571-7
Chen G., Qi Y., Niu L., Di T., Zhong J., Fang T., Yan W. 2015. Application of the cell sheet technique in tissue engineering. Biomed. Rep. V. 3. P. 749. https://doi.org/10.3892/br.2015.522
Cherng J.-H., Chou S.-C., Chen C.-L., Wang Y.-W., Chang S.-J., Fan G.-Y., Leung F.-S., Meng E. 2021. Bacterial cellulose as a potential bio-scaffold for effective re-epithelialization. Therapy Pharmaceutics. V. 13. P. 1592. https://doi.org/10.3390/pharmaceutics13101592
Domnina A.P., Ivanova J.V., Alekseenko L.L., Kozhukharova I.V., Borodkina A.V., Pugovkina N.A., Smirnova I.S., Lyublinskaya O.G., Fridlyanskaya I.I., Nikolsky N.N. 2020. Three-dimensional compaction switches stress response programs and enhances therapeutic efficacy of endometrial mesenchymal stem/stromal cells. Front. Cell Devel. B-iol. V. 8. P. 473. https://doi.org/10.3389/fcell.2020.00473
Domnina A.P., Novikova P.V., Obidina J.I., Fridlyanskaya I.I, Alekseenko L.L., Kozhukharova I.V., Lyublinskaya O.G., Zenin V.V., Nikolsky N.N. 2018. Human mesenchymal stem cells in spheroids improve fertility in model animals with damaged endometrium. Stem Cell Res. Ther. V. 9. P. 1. https://doi.org/10.1186/s13287-018-0801-9
Gargett C.E., Masuda H. 2010. Adult stem cells in the endometrium. Mol. Hum. Reprod. V. 16. P. 818. https://doi.org/10.1093/molehr/gaq061
Gorgieva S., Trček J. 2019. Bacterial cellulose: production, modification and perspectives in biomedical applications. Nanomaterials. V. 9. P. 1352. https://doi.org/10.3390/nano9101352
Guruswamy Damodaran R., Vermette P. 2018. Tissue and organ decellularization in regenerative medicine. Biotech. Progress. V. 34. P. 1494. https://doi.org/10.1002/btpr.2699
Haycock J.W. 2011. 3D cell culture: a review of current approaches and techniques. Methods Mol. Biol. V. 695. P. 1. https://doi.org/10.1007/978-1-60761-984-0_1
Husein K.S., Thiemermann C. 2010. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. V. 28. P. 585. https://doi.org/10.1002/stem.269
Jauković A., Abadjieva D., Trivanović D. 2020. Specificity of 3D msc spheroids microenvironment: impact on msc behavior and properties. Stem Cell Rev. Rep. V. 16. P. 853. https://doi.org/10.1007/s12015-020-10006-9
Jensen C., Teng Y. 2020. Is it time to start transitioning from 2d to 3d cell culture? Front. Mol. Biosci. V. 7. P. 33. https://doi.org/10.3389/fmolb.2020.00033
Kouroupis D., Correa D. 2021. Increased mesenchymal stem cell functionalization in three-dimensional manufacturing settings for enhanced therapeutic applications. Front. Bioeng. Biotechnol. V. 9. P. 621748. https://doi.org/10.3389/fbioe.2021.621748
Langhans S.A. 2018. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front. Pharmacol. V. 9. P. 6. https://doi.org/10.3389/fphar.2018.00006
Lee J., Jung H., Park N. 2019. Induced osteogenesis in plants decellularized scaffolds. Sci. Rep. V. 9. P. 20194. https://doi.org/10.1038/s41598-019-56651-0
Lyublinskaya O.G., Ivanova J.S., Pugovkina N.A., Kozhukharova I.V., Kovaleva Z.V., Shatrova A.N., Aksenov N.D., Zenin V.V., Kaulin Y.A., Gamaley I.A., Nikolsky N.N. 2017. Redox environment in stem and differentiated cells: a quantitative approach. Redox Biol. V. 12. P. 758. https://doi.org/10.1016/j.redox.2017.04.016
Meng X., Ichim T.E., Zhong J., Rogers A., Yin Z., Jackson J., Wang H., Ge W., Bogin V., Chan K.W., Thébaud B., Riordan N.H. 2007. Endometrial regenerative cells: a novel stem cell population. J. Transl. Med. V. 5. P. 57. https://doi.org/10.1186/1479-5876-5-57
Modulevsky D.J., Cuerrier C.M., Pelling A.E. 2016. Biocompatibility of subcutaneously implanted plant-derived cellulose biomaterials. PLoS One. V. 11. P. e0157894. https://doi.org/10.1371/journal.pone.0157894
Modulevsky D.J., Lefebvre C., Haase K., Al-Rekabi Z., Pelling A.E. 2014. Apple derived cellulose scaffolds for 3D mammalian cell culture. PLos One. V. 9. P. e97835. https://doi.org/10.1371/journal.pone.0097835
Patel A.N., Park E., Kuzman M., Benetti F., Silva F.J., Allickson J.G. 2008. Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant. V. 17. P. 303. https://doi.org/10.3727/096368908784153922
Phan N.V., Wright T., Rahman M.M., Xu J., Coburn J.M. 2020. In vitro biocompatibility of decellularized cultured plant cell derived matrices. ACS Biomater. Sci. Eng. V. 6. P. 822. https://doi.org/10.1021/acsbiomaterials.9b00870
Svensson A., Nicklasson E., Harrah T., Panilaitis B., Kaplan D.L., Brittberg M., Gatenholm P. 2005. Bacterial cellulose as a potential scaffold for tissue engineering of cartilage. Biomaterials. V. 26. P. 419. https://doi.org/10.1016/j.biomaterials.2004.02.049
Hu Xinqiang, Xia Zengzilu, Cai Kaiyong. 2022. Recent advances in 3D hydrogel culture systems for mesenchymal stem cell-based therapy and cell behavior regulation. J. Mater. Chem. B. V. 10. P. 1486. https://doi.org/10.1039/D1TB02537F
Zack G.W., Rogers W.E., Latt S.A. 1977. Automatic measurement of sister chromatid exchange frequency. J. Histochem. Cytochem. V. 25. P. 741. https://doi.org/10.1177/25.7.70454