Investigation of the Interaction of Adipose-Derived Mesenchymal Stem Cells with ε-Polycaprolactone and Egg White Scaffolds

Year 2023, , 1434 - 1447, 01.12.2023

Olga Nehir Öztel , Hilal Yılmaz , İsmail Alper İşoğlu , Adil Allahverdiyev

https://doi.org/10.35378/gujs.1037746

Cited By: 1

Abstract

The development of three-dimensional (3D) cell culture models is becoming increasingly important due to their numerous advantages over conventional monolayer culture. This study aimed to examine the interaction of adipose tissue-derived mesenchymal stem cells (AD-MSCs) with scaffolds composed of ε-polycaprolactone (ε-PCL) and egg white. In our study, ε-PCL and egg white scaffolds were produced from their monomers by tin octoate catalyzed and heat polymerization, respectively. Characterization of ε-PCL was carried out by Gel Permeation Chromatography (GPC), Fourier Transform Infrared Spectrophotometry (FTIR), Proton Nuclear Magnetic Resonance (H-NMR), Differential Scanning Calorimetry (DSC) and Scanning Electron Microscopy (SEM). AD-MSCs labeled with red fluorescent CellTracker CM-DiI were cultured on egg white and ε-PCL scaffolds for 12 days. Cell viability was determined using 3-(4.5-Dimethylthiazol-2yl)-2.5-diphenyltetrazolium bromide (MTT) and nitric oxide (NO) level was evaluated for toxicity. The results showed that the number of AD-MSCs in the egg white scaffold increased periodically for 12 days compared to the other groups. Although the number of AD-MSCs in the ε-PCL scaffold increased until day 6 of the culture, the number of cells started to decrease after day 6. These results were associated with the toxic effect of lactic acid release on cells resulting from the decomposition of ε-PCL scaffolds through catabolic reactions. Therefore, these results indicated that the egg white scaffold enhanced and maintained cell adhesion and cell viability more than the ε-Polycaprolactone scaffold and could be used as a scaffold in tissue engineering studies involving stem cells.

Keywords

Adipose-derived mesenchymal stem cells, 3D cell culture, ε-Polycaprolactone, Egg white

References

• [1] Rinoldi, C., Kijeńska‐Gawrońska, E., Khademhosseini, A., Tamayol, A., and Swieszkowski, W., "Fibrous Systems as Potential Solutions for Tendon and Ligament Repair, Healing, and Regeneration", Advanced Healthcare Materials, 10(7): 2001305, (2021).
• [2] Naureen, B., Haseeb, A. S. M. A., Basirun, W. J., and Muhamad, F., "Recent advances in tissue engineering scaffolds based on polyurethane and modified polyurethane", Materials Science and Engineering: C, 118: 111228, (2021).
• [3] Janagama, D., and Hui, S. K., "3-D Cell Culture Systems in Bone Marrow Tissue and Organoid Engineering, and BM Phantoms as In Vitro Models of Hematological Cancer Therapeutics—A Review", Materials, 13(24): 5609, (2020).
• [4] Kapałczyńska, M., Kolenda, T., Przybyła, W., Zajączkowska, M., Teresiak, A., Filas, V., Ibbs, M., Bliźniak, R., Łuczewski, Ł., and Lamperska, K., "2D and 3D cell cultures–a comparison of different types of cancer cell cultures", Archives of Medical Science: AMS, 14(4): 910, (2018).
• [5] Shkarina, S., Shkarin, R., Weinhardt, V., Melnik, E., Vacun, G., Kluger, P. J., Loza, K., Epple, M., Ivlev, S. I., Baumbach, T., Surmeneva, M. A., and Surmenev, R. A., "Author Correction: 3D biodegradable scaffolds of polycaprolactone with silicate-containing hydroxyapatite microparticles for bone tissue engineering: High-resolution tomography and in vitro study", Scientific Reports, 8(1): 1-13, (2018).
• [6] Yousefi, A. M., Powers, J., Sampson, K., Wood, K., Gadola, C., Zhang, J., and James, P. F., "In vitro characterization of hierarchical 3D scaffolds produced by combining additive manufacturing and thermally induced phase separation", Journal of Biomaterials Science, Polymer Edition, 32(4): 454-476, (2020).
• [7] Wang, Z., Zuo, F., Liu, Q., Wu, X., Du, Q., Lei, Y., Wu, Z., and Lin, H., "Comparative Study of Human Pluripotent Stem Cell-Derived Endothelial Cells in Hydrogel-Based Culture Systems", ACS Omega, 6(10): 6942-6952, (2021).
• [8] Huang, Y., Fitzpatrick, V., Zheng, N., Cheng, R., Huang, H., Ghezzi, C., Ghezzi, C., Kaplan, D. L., and Yang, C., "Self‐Folding 3D Silk Biomaterial Rolls to Facilitate Axon and Bone Regeneration", Advanced Healthcare Materials, 9(18): 2000530, (2020).
• [9] Huang, T. Y., Wang, G. S., Ko, C. S., Chen, X. W., and Su, W. T., "A study of the differentiation of stem cells from human exfoliated deciduous teeth on 3D silk fibroin scaffolds using static and dynamic culture paradigms", Materials Science and Engineering: C, 109: 110563, (2020).
• [10] Le, M. C. N., Xu, K., Wang, Z., Beverung, S., Steward, R. L., and Florczyk, S. J., "Evaluation of the effect of 3D porous Chitosan‐alginate scaffold stiffness on breast cancer proliferation and migration", Journal of Biomedical Materials Research Part A, 109(10): 1990-2000, (2021).
• [11] Houdellier, F., Masseboeuf, A., Monthioux, M., and Hÿtch, M. J., "New carbon cone nanotip for use in a highly coherent cold field emission electron microscope", Carbon 50(5): 2037-2044, (2012).
• [12] Sukul, M., Sahariah, P., Lauzon, H. L., Borges, J., Másson, M., Mano, J. F., Haugen, H. J., and Reseland, J. E., "In vitro biological response of human osteoblasts in 3D chitosan sponges with controlled degree of deacetylation and molecular weight", Carbohydrate Polymers, 254: 117434, (2021).
• [13] Gentile, P., Chiono, V., Carmagnola, I., and Hatton, P. V., "An overview of poly (lactic-co-glycolic) acid (PLGA)-based biomaterials for bone tissue engineering", International Journal of Molecular Sciences, 15(3): 3640-3659, (2014).
• [14] Lai, G. J., Shalumon, K. T., Chen, S. H., and Chen, J. P., "Composite chitosan/silk fibroin nanofibers for modulation of osteogenic differentiation and proliferation of human mesenchymal stem cells", Carbohydrate Polymers, 111: 288-297, (2014).
• [15] Johnstone, B., Alini, M., Cucchiarini, M., Dodge, G. R., Eglin, D., Guilak, F., Madry, H., Mata, A., Mauck, R. L., Semino, C. E., and Stoddart, M. J., "Tissue engineering for articular cartilage repair—the state of the art", Eur Cell Mater, 25(248): e67, (2013).
• [16] Alaribe, F. N., Manoto, S. L., and Motaung, S. C., "Scaffolds from biomaterials: advantages and limitations in bone and tissue engineering", Biologia, 71(4): 353-366, (2016).
• [17] Boni, R., Ali, A., Shavandi, A., and Clarkson, A. N., "Current and novel polymeric biomaterials for neural tissue engineering", Journal of Biomedical Science, 25(1): 1-21, (2018).
• [18] Mamsen, F. P., Munthe-Fog, L., Kring, M. K. M., Duscher, D., Taudorf, M., Katz, A. J., and Kølle, S. F. T., "Differences of embedding adipose-derived stromal cells in natural and synthetic scaffolds for dermal and subcutaneous delivery", Stem Cell Research & Therapy, 12(1): 1-12, (2021).
• [19] Mine, Y., "Egg proteins and peptides in human health-chemistry, bioactivity and production", Current Pharmaceutical Design, 13(9): 875-884, (2007).
• [20] Kovacs-Nolan, J., Phillips, M., and Mine, Y., "Advances in the value of eggs and egg components for human health", Journal of Agricultural and Food Chemistry, 53(22): 8421-8431, (2005).
• [21] Dong, X., and Zhang, Y. Q., "An insight on egg white: From most common functional food to biomaterial application", Journal of Biomedical Materials Research Part B: Applied Biomaterials, 109(7): 1045-1058, (2021).
• [22] Mobarra, N., Soleimani, M., Pakzad, R., Enderami, S. E., and Pasalar, P., "Three-dimensional nanofiberous PLLA/PCL scaffold improved biochemical and molecular markers hiPS cell-derived insulin-producing islet-like cells", Artificial Cells, Nanomedicine, and Biotechnology, 46(sup3): S685-S692, (2018).
• [23] Pandey, S., Rathore, K., Johnson, J., and Cekanova, M., "Aligned nanofiber material supports cell growth and increases osteogenesis in canine adipose‐derived mesenchymal stem cells in vitro", Journal of Biomedical Materials Research Part A, 106(7): 1780-1788, (2018).
• [24] Allahverdiyev, A. M., Bagirova, M., Elcicek, S., Koc, R. C., Baydar, S. Y., Findikli, N., and Oztel, O. N., "Adipose tissue-derived mesenchymal stem cells as a new host cell in latent leishmaniasis", The American Journal of Tropical Medicine and Hygiene, 85(3): 535, (2011).
• [25] Kaipparettu, B. A., Kuiatse, I., Tak-Yee Chan, B., Benny Kaipparettu, M., Lee, A. V., and Oesterreich, S., "Novel egg white–based 3-D cell culture system", Biotechniques, 45(2): 165-171, (2008).
• [26] Sönmezer, D., Lati̇foğlu, F., Toprak, G., Düzler, A., and İşoğlu, İ. A., "Pericardial fluid and vascular tissue engineering: A preliminary study", Bio-Medical Materials and Engineering, 32(2): 101-113, (2021).
• [27] Pişkin, E., İşoğlu, İ. A., Bölgen, N., Vargel, I., Griffiths, S., Çavuşoğlu, T., Korkusuz, P., Güzel, E., and Cartmell, S., "In vivo performance of simvastatin‐loaded electrospun spiral‐wound polycaprolactone scaffolds in reconstruction of cranial bone defects in the rat model", Journal of Biomedical Materials Research Part A: An Official Journal of the Society for Biomaterials, The Japanese Society for Biomaterials, and The Australian Society for Biomaterials and the Korean Society for Biomaterials, 90(4): 1137-1151, (2009).
• [28] Siddiqui, N., Asawa, S., Birru, B., Baadhe, R., and Rao, S., "PCL-based composite scaffold matrices for tissue engineering applications", Molecular Biotechnology, 60(7): 506-532, (2018).
• [29] Kim, Hye‐Joung, Jin‐Ho Lee, and Gun‐Il Im., "Chondrogenesis using mesenchymal stem cells and PCL scaffolds", Journal of Biomedical Materials Research Part A: An Official Journal of The Society for Biomaterials, The Japanese Society for Biomaterials, and The Australian Society for Biomaterials and the Korean Society for Biomaterials, 92(2): 659-666, (2010).
• [30] Caetano, G. F., Bártolo, P. J., Domingos, M., Oliveira, C. C., Leite, M. N., and Frade, M. A. C., "Osteogenic differentiation of adipose-derived mesenchymal stem cells into Polycaprolactone (PCL) scaffold", Procedia Engineering, 110: 59-66, (2015).
• [31] Topuzogullari, M., Cakir Koc, R., Dincer Isoglu, S., Bagirova, M., Akdeste, Z., Elcicek, S., Oztel, O. N., Yeşilkır Baydar, S., Canim Ates, S., and Allahverdiyev, A. M., "Conjugation, characterization, and toxicity of lipophosphoglycan-polyacrylic acid conjugate for vaccination against leishmaniasis", Journal of Biomedical Science, 20(1): 1-8, (2013).
• [32] Xu, D., Yang, M., Capitano, M., Guo, B., Liu, S., Wan, J., Broxmeyer, H., and Huang, X., "Pharmacological activation of nitric oxide signaling promotes human hematopoietic stem cell homing and engraftment", Leukemia 35(1): 229-234, (2021).
• [33] Bassaneze, V., Barauna, V. G., Lavini-Ramos, C., Kalil, J., Schettert, I. T., Miyakawa, A. A., and Krieger, J. E., "Shear stress induces nitric oxide–mediated vascular endothelial growth factor production in human adipose tissue mesenchymal stem cells", Stem Cells and Development, 19(3): 371-378, (2010).
• [34] Gao, M., Zhang, H., Dong, W., Bai, J., Gao, B., Xia, D., Feng, B., Chen, M., He, X., Yin, M., Xu, Z., Witman, N., Fu, W., and Zheng, J., "Tissue-engineered trachea from a 3D-printed scaffold enhances whole-segment tracheal repair", Scientific Reports, 7(1): 1-12, (2017).
• [35] Srouji, S., Kizhner, T., Suss-Tobi, E., Livne, E., and Zussman, E., "3-D Nanofibrous electrospun multilayered construct is an alternative ECM mimicking scaffold", Journal of Materials Science: Materials in Medicine, 19(3): 1249-1255, (2008).
• [36] Huang, K., Li, Q., Li, Y., Yao, Z., Luo, D., Rao, P., and Xiao, J., "Cartilage tissue regeneration: the roles of cells, stimulating factors and scaffolds", Current Stem Cell Research & Therapy, 13(7): 547-567, (2018).
• [37] Woodruff, M. A., and Hutmacher, D. W., "The return of a forgotten polymer—Polycaprolactone in the 21st century", Progress in Polymer Science, 35(10): 1217-1256, (2010).
• [38] Dalton, P. D., Woodfield, T., and Hutmacher, D. W., "Snapshot: Polymer scaffolds for tissue engineering", Biomaterials, 30(4): 701-702, (2009).
• [39] Jalili-Firoozinezhad, S., Filippi, M., Mohabatpour, F., Letourneur, D., and Scherberich, A., "Chicken egg white: Hatching of a new old biomaterial", Materials Today, 40: 193-214, (2020).
• [40] Duval, K., Grover, H., Han, L. H., Mou, Y., Pegoraro, A. F., Fredberg, J., and Chen, Z., “Modeling physiological events in 2D vs. 3D cell culture", Physiology, 32(4): 266-277, (2017).
• [41] Lee, S. H., Lee, J. H., and Cho, Y. S. Lee, Se-Hwan, Jun Hee Lee, and Young-Sam Cho., "Analysis of degradation rate for dimensionless surface area of well-interconnected PCL scaffold via in-vitro accelerated degradation experiment", Tissue Engineering and Regenerative Medicine, 11(6): 446-452, (2014).
• [42] Gaudiello, E., Melly, L., Cerino, G., Boccardo, S., Jalili‐Firoozinezhad, S., Xu, L., Eckstein, F., Martin, I., Kaufmann, B. A., Banfi, A., and Marsano, A., "Scaffold Composition Determines the Angiogenic Outcome of Cell‐Based Vascular Endothelial Growth Factor Expression by Modulating Its Microenvironmental Distribution", Advanced Healthcare Materials, 6(24): 1700600, (2017).
• [43] Edlund, U., and Albertsson, A. C., "Degradable polymer microspheres for controlled drug delivery", Degradable Aliphatic Polyesters, 67-112, (2002).
• [44] Malikmammadov, E., Tanir, T. E., Kiziltay, A., Hasirci, V., and Hasirci, N., "PCL and PCL-based materials in biomedical applications", Journal of Biomaterials science, Polymer edition, 29(7-9): 863-893, (2018).
• [45] Shin, S. W., Jang, Y. D., Ko, K. W., Kang, E. Y., Han, J. H., Bedair, T. M., Kim, I.H., Son, T. I., Park, W., and Han, D. K., "PCL microspheres containing magnesium hydroxide for dermal filler with enhanced physicochemical and biological performances", Journal of Industrial and Engineering Chemistry, 80: 854-861, (2019).
• [46] Michurina, T., Krasnov, P., Balazs, A., Nakaya, N., Vasilieva, T., Kuzin, B., Khrushchov, N., Mulligan, R. C., and Enikolopov, G., "Nitric oxide is a regulator of hematopoietic stem cell activity", Molecular Therapy, 10(2): 241-248, (2004).