The effect of herbal components, pomegranate and icariin on the chondrogenesis of stem cells in the fibrin- micromass hydrogel system
DOI:
https://doi.org/10.22034/JATE.2023.76Abstract
Abstract
Introduction: Tissue engineering has been employed to encourage cartilage renewal using natural or synthetic scaffolds, stem cells, and growth factors. The present study introduces a novel approach based on the chondrogenesis of human adipose-derived mesenchymal stromal cells (ASC)s in the fibrin hydrogel by applying the micro mass culture, using pomegranate and icariin as the herbal components.
Materials and Methods: To prepare fibrin hydrogel, a thrombin solution was extracted from human fresh-frozen plasma, and the cryoprecipitate was used as the fibrinogen component following thawing. The ASCs were seeded on the fibrin hydrogel via micro mass culture system. To investigate the chondrogenesis of the ASCs, the cell-seeded hydrogels were cultured in the different culture medias containing TGF-β3, pomegranate extract, icariin, and the combined medium containing the Icariin and pomegranate.
Results: Gene expression measurements and histological staining confirmed that the ASC-seeded hydrogels cultured in the chondrogenic media containing the herbal components could express cartilage-specific genes and synthesize the cartilage-related macromolecules. However, in the presence of TGF-β3, the hydrogels exhibited a significant expression of these markers.
Conclusion: These findings suggest that a combination of these two herbal components could significantly stimulate ASCs and increased cellular proliferation, the expression of chondrogenic genes, the enhanced glycosaminoglycan and collagen synthesis, and the reduction of the hypertrophic phenotypes compared to the TGF-β3.
Keywords: Cartilage tissue engineering, Fibrin hydrogel, Herbal components, Micromass culture
References
.Sutherland AJ, Beck EC, Dennis SC, Converse GL, Hopkins RA, Berkland CJ, et al. Decellularized cartilage may be a chondroinductive material for osteochondral tissue engineering. PloS one. 2015;10(5):e0121966.
Athanasiou KA, Darling EM, Hu JC, DuRaine GD, Reddi AH. Articular cartilage: CRC Press; 2013.
Huey DJ, Hu JC, Athanasiou KA. Unlike bone, cartilage regeneration remains elusive. Science. 2012;338(6109):917-21.
Liao I, Moutos FT, Estes BT, Zhao X, Guilak F. Composite three‐dimensional woven scaffolds with interpenetrating network hydrogels to create functional synthetic articular cartilage. Advanced functional materials. 2013;23(47):5833-9.
Blum MM, Ovaert TC. Low friction hydrogel for articular cartilage repair: evaluation of mechanical and tribological properties in comparison with natural cartilage tissue. Materials Science and Engineering: C. 2013;33(7):4377-83.
Setayeshmehr M, Esfandiari E, Rafieinia M, Hashemibeni B, Taheri-Kafrani A, Samadikuchaksaraei A, et al. Hybrid and composite scaffolds based on extracellular matrices for cartilage tissue engineering. Tissue Engineering Part B: Reviews. 2019;25(3):202-24.
Li Y, Meng H, Liu Y, Lee BP. Fibrin gel as an injectable biodegradable scaffold and cell carrier for tissue engineering. The Scientific World Journal. 2015; 2015: 1-10.
Wang W, Li B, Yang J, Xin L, Li Y, Yin H, et al. The restoration of full-thickness cartilage defects with BMSCs and TGF-beta 1 loaded PLGA/fibrin gel constructs. Biomaterials. 2010;31(34):8964-73.
Hashemibeni B, Pourentezari M, Valiani A, Zamani M, Mardani M. Effect of icariin on the chondrogenesis of human adipose derived stem cells on poly (lactic-co-glycolic) acid/fibrin composite scaffold. International Journal of Advanced Biotechnology and Research. 2017;8(2):595-605.
Handschel JG, Depprich RA, Kübler NR, Wiesmann H-P, Ommerborn M, Meyer U. Prospects of micromass culture technology in tissue engineering. Head & face medicine. 2007;3(1):1-4.
Teimouri M, Hashemibeni B, Mardani M. Comparison of aggrecan gene expression in chondrogenesis of adipose-derived stem cells in pellet and micromass culture systems. Tehran University Medical Journal TUMS Publications. 2018;76
. Setayeshmehr M, Esfandiari E, Hashemibeni B, Tavakoli AH, Rafienia M, Samadikuchaksaraei A, et al. Chondrogenesis of human adipose-derived mesenchymal stromal cells on the [devitalized costal cartilage matrix/poly (vinyl alcohol)/fibrin] hybrid scaffolds. European Polymer Journal. 2019;118:528-41.
Davis A, Guldberg RE, Samsonraj RM. Osteoimmunological Implications in Regenerative Medicine: Cross-Talk Between Mesenchymal Stem Cells and Immune Cells. Journal of Musculoskeletal Research. 2020.
Hsiao Y-m, Hu C-C, Chang C-H, Chen M-F, Chang Y. Adult mesenchymal stem cell-based approaches for osteoarthritis: current perspectives and challenges. Journal of Musculoskeletal Research. 2020.
Hashemibeni B, Razavi S, Esfandiary E, Karbasi S, Mardani M, Nasresfahani M. Induction of chondrogenic differentiation of human adipose-derived stem cells with TGF-β3 in pellet culture system. Iranian Journal of Basic Medical Sciences. 2008;11(1):10-7.
Hashemibeni B, Valiani A, Esmaeli M, Kazemi M, Aliakbari M, Iranpour FG. Comparison of the efficacy of piascledine and transforming growth factor β1 on chondrogenic differentiation of human adipose-derived stem cells in fibrin and fibrin-alginate scaffolds. Iranian journal of basic medical sciences. 2018;21(2):212.
Valiani A, Izadi M, Bahramian H, Esfandiari E, Hashemibeni B. Comparison between the effect of kartogenin and TGFβ3 on chondrogenesis of human adipose-derived stem cells in fibrin scaffold. Bratislavske lekarske listy. 2017;118(10):591-7.
Esfandiari E, Roshankhah S, Mardani M, Hashemibeni B, Naghsh E, Kazemi M, et al. The effect of high frequency electric field on enhancement of chondrogenesis in human adipose-derived stem cells. Iranian Journal of Basic Medical Sciences. 2014;17(8):571-6.
Kawamura K, Chu CR, Sobajima S, Robbins PD, Fu FH, Izzo NJ, et al. Adenoviral-mediated transfer of TGF-β1 but not IGF-1 induces chondrogenic differentiation of human mesenchymal stem cells in pellet cultures. Experimental hematology. 2005;33(8):865-72.
Newfeld SJ, Wisotzkey RG, Kumar S. Molecular evolution of a developmental pathway: phylogenetic analyses of transforming growth factor-β family ligands, receptors and Smad signal transducers. Genetics. 1999;152(2):783-95.
Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development. 1995;121(6):1845-54.
Buhrmann C, Honarvar A, Setayeshmehr M,
. LIU K-p, WANG L-f, Yang L, Bin Y, Chao D, Yang W. Preparation, pharmacokinetics, and tissue distribution properties of icariin-loaded stealth solid lipid nanoparticles in mice. Chinese Herbal Medicines. 2012;4(2):170-4.
Wang ZC, Sun HJ, Li KH, Fu C, Liu MZ. Icariin promotes directed chondrogenic differentiation of bone marrow mesenchymal stem cells but not hypertrophy in vitro. Experimental and therapeutic medicine. 2014;8(5):1528-34.
Li D, Yuan T, Zhang X, Xiao Y, Wang R, Fan Y. Icariin: a potential promoting compound for cartilage tissue engineering. Osteoarthritis and cartilage. 2012;20(12):1647-56.
Wang Z, Li K, Sun H, Wang J, Fu Z, Liu M. Icariin promotes stable chondrogenic differentiation of bone marrow mesenchymal stem cells in self‑assembling peptide nanofiber hydrogel scaffolds. Molecular medicine reports. 2018;17(6):8237-43.
Li Y, Zhu C-p, Zhai X-c, Zhang Y, Duan Z, Sun J-r. Optimization of enzyme assisted extraction of polysaccharides from pomegranate peel by response surface methodology and their antioxidant potential. Chinese Herbal Medicines. 2018;10(4):416-23.
Gorji M, Zargar A, Setayeshmehr M, Ghasemi N, Soleimani M, Kazemi M, et al. Releasing and structural/mechanical properties of nanoparticle/Punica granatum (Pomegranate) in poly(lactic-co-glycolic) acid/fibrin as nano-composite scaffold. Bratislavske lekarske listy. 2021;122(1):54-64.
Gullon B, Pintado ME, Pérez-Álvarez JA, Viuda-Martos M. Assessment of polyphenolic profile and antibacterial activity of pomegranate peel (Punica granatum) flour obtained from co-product of juice extraction. Food Control. 2016;59:94-8.
Mansour E, Ben Khaled A, Lachiheb B, Abid M, Bachar K, Ferchichi A. Phenolic compounds, antioxidant, and antibacterial activities of peel extract from Tunisian pomegranate. J Agr Sci Tech. 2013;15:1393-403.
Sadeghi N, Jannat B, Oveisi M, Hajimahmoodi M, Photovat M. Antioxidant activity of Iranian pomegranate (Punica granatum L.) seed extracts. J Agr Sci Tech. 2009;11:633-8.
Yasoubi P, Barzegar M, Sahari M, Azizi M. Total phenolic contents and antioxidant activity of pomegranate (Punica granatum L.) peel extracts. J Agric Sci Technol. 2007;9:35-42.
Choi B-R, Ku S-K, Kang S-J, Park H-R, Sung M-S, Lee Y-J, et al. Anti-osteoarthritic effects of a combination of pomegranate concentrate powder, Eucommiae cortex and Achyranthis radix in rats. Journal of Korean Medicine. 2018;39(4):86-113.
Qu W, Breksa III AP, Pan Z, Ma H. Quantitative determination of major polyphenol constituents in pomegranate products. Food
Akhavan H, Barzegar M, Weidlich H, Zimmermann BF. Phenolic compounds and antioxidant activity of juices from ten Iranian pomegranate cultivars depend on extraction. Journal of Chemistry. 2015;2015.
Katani M, Zolfaghari B, Soleimani M, Valiani A, Hashemibeni B. The effect of pomegranate extract on producing type ii collagen in differentiation of adipose-derived stem cells into chondrocytes.
Cheng N-C, Estes BT, Young T-H, Guilak F. Genipin-crosslinked cartilage-derived matrix as a scaffold for human adipose-derived stem cell chondrogenesis. Tissue engineering Part A. 2012;19(3-4):484-96.
Kabiri A, Esfandiari E, Hashemibeni B, Kazemi M, Mardani M, Esmaeili A. Effects of FGF-2 on human adipose tissue derived adult stem cells morphology and chondrogenesis enhancement in Transwell culture. Biochemical and biophysical research communications. 2012;424(2):234-8.
Sarveazad A, Babahajian A, Bakhtiari M, Soleimani M, Behnam B, Yari A, et al. The combined application of human adipose derived stem cells and Chondroitinase ABC in treatment of a spinal cord injury model. Neuropeptides. 2017;61:39-47.
Yang SH, Wu CC, Shih TTF, Chen PQ, Lin FH. Three‐dimensional Culture of Human Nucleus Pulposus Cells in Fibrin Clot: Comparisons on Cellular Proliferation and Matrix Synthesis With Cells in Alginate. Artificial organs. 2008;32(1):70-3.
Garrigues NW, Little D, Sanchez‐Adams J, Ruch DS, Guilak F. Electrospun cartilage‐derived matrix scaffolds for cartilage tissue engineering. Journal of biomedical materials research Part A. 2014;102(11):3998-4008.
Gong YY, Xue JX, Zhang WJ, Zhou GD, Liu W, Cao Y. A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes. Biomaterials. 2011;32(9):2265-73.
Gorji M, Ghasemi N, Setayeshmehr M, Zargar A, Kazemi M, Soleimani M, et al. The Effects of Fibrin-icariin Nanoparticle Loaded in Poly (lactic-co-glycolic) Acid Scaffold as a Localized Delivery System on Chondrogenesis of Human Adipose-derived Stem Cells. Adv Biomed Res. 2020;9:6-.
Liu D, Tang W, Zhang H, Huang H, Zhang Z, Tang D, et al. Icariin protects rabbit BMSCs against OGD-induced apoptosis by inhibiting ERs-mediated autophagy via MAPK signaling pathway. Life Sciences. 2020;253:117730.
Wang P, Xiong X, Zhang J, Qin S, Wang W, Liu Z. Icariin increases chondrocyte vitality by promoting hypoxia-inducible factor-1α expression and anaerobic glycolysis. The Knee. 2020;27(1):18-25.
Choi B-R, Kang S-J, Kim J-L, Lee Y-J, Ku S-K. Anti-Osteoarthritic Effects of a Mixture of Dried Pomegranate Concentrate Powder, Eucommiae Cortex, and Achyranthis Radix 5: 4: 1 (g/g) in a Surgically Induced Osteoarthritic Rabbit Model. Nutrients. 2020;12(3):852.
Ng K, DeFrancis J, Kugler L, Kelly T-A, Ho M, O'Conor C, et al. Amino acids supply in culture media is not a limiting factor in the matrix synthesis of engineered cartilage tissue. Amino acids. 2008;35(2):433-8.
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