Electrospun Propolis-coated PLGA Scaffold Enhances the Osteoinduction of Mesenchymal Stem Cells


Cite item

Full Text

Abstract

Background:Major injuries that are caused by trauma and cancer can not be repaired through bone remodeling. The goal of bone regeneration by tissue engineering approaches is to fabricate bone implants in order to restore bone structure and functions. The use of stem cells and polymer scaffolds provides the conditions for tissue regeneration based on tissue engineering.

Objective:This study aimed to fabricate a combined matrix of poly(lactide-co-glycolide) (PLGA) and propolis extract, which is a mixture of pollen and beeswax collected by bees from certain plants and has long been used in traditional herbal medicine, to promote the osteogenic differentiation of human adipose- derived mesenchymal stem cells (AD-MSCs).

Methods:The scaffold was fabricated through electrospinning and was immersed in a propolis extract solution. Then, AD-MSCs were cultured and differentiated into the osteogenic lineage. The cell viability on the scaffold was evaluated by MTT assay. Osteogenic differentiation of the seeded stem cells was detected by evaluating calcium content, alkaline phosphatase (ALP) activity, and the expression of bonespecific genes.

Results:The viability of cells was not affected by propolis-coated and uncoated fabricated scaffolds, while higher calcium content, ALP activity, and expression of RUNX-2, type I collagen, osteocalcin, and osteonectin were observed in cells differentiated on propolis-coated PLGA scaffold on days 7, 14, and 21 of differentiation compared to PLGA scaffold.

Conclusion:The results of this study showed that the presence of propolis in the scaffold could lead to better cell attachment and strengthen the osteoinduction process in stem cells.

About the authors

Mohammad Askari

Applied Biotechnology Research Center, Baqiyatallah University of Medical Sciences

Email: info@benthamscience.net

Maryam Jadid Tavaf

Department of Hematology, Tarbiat Modares University

Email: info@benthamscience.net

Masoud Ghorbani

Applied Biotechnology Research Center, Baqiyatallah University of Medical Sciences

Email: info@benthamscience.net

Mohsen Yazdanian

Research Center for Prevention of Oral and Dental Diseases, Baqiyatallah University of Medical Sciences

Email: info@benthamscience.net

Mehrdad Moghaddam

Applied Biotechnology Research Center, Baqiyatallah University of Medical Sciences

Author for correspondence.
Email: info@benthamscience.net

References

  1. Florencio-Silva R, Rodrigues da Silva Sasso G, Sasso-Cerri E, Jesus Simões M, Sérgio Cerri P. Biology of bone tissue: Structure, function, and factors that influence bone cells. BioMed research international 2015; 2015. doi: 10.1155/2015/421746
  2. Morgan EF, Gerstenfeld LC. The bone organ system: Form and function Marcus and Feldman’s Osteoporosis. Elsevier 2021; pp. 15-35. doi: 10.1016/B978-0-12-813073-5.00002-2
  3. Fratzl P, Gupta HS, Roschger P, Klaushofer K. Bone nanostructure and its relevance for mechanical performance, disease and treatment. Nanotechnology. Online 2010; 9: 345-60. doi: 10.1002/9783527628155.nanotech060
  4. Fratzl P, Gupta HS, Paschalis EP, Roschger P. Structure and mechanical quality of the collagen–mineral nano-composite in bone. J Mater Chem 2004; 14(14): 2115-23. doi: 10.1039/B402005G
  5. Alford AI, Kozloff KM, Hankenson KD. Extracellular matrix networks in bone remodeling. Int J Biochem Cell Biol 2015; 65: 20-31. doi: 10.1016/j.biocel.2015.05.008 PMID: 25997875
  6. Parkinson IH, Fazzalari NL. Characterisation of trabecular bone structure Skeletal aging and osteoporosis. Springer 2013; pp. 31-51. doi: 10.1007/8415_2011_113
  7. STEIN GS. LIAN JB Molecular mechanisms mediating developmental and hormone-regulated expression of genes in osteoblasts: an inte-grated relationship of cell growth and differentiation Cellular and molecular biology of bone. Elsevier 1993; pp. 47-95.
  8. Davies J, Ottensmeyer P, Shen X, Hashimoto M, Peel S. 20 Early ace. University of Toronto Press 2016; pp. 214-28.
  9. Abdulahy SB, Esmaeili Bidhendi M, Vaezi MR, Moosazadeh Moghaddam M. Osteogenesis improvement of gelatin-based nanocomposite scaffold by loading zoledronic acid. Front Bioeng Biotechnol 2022; 10: 890583. doi: 10.3389/fbioe.2022.890583 PMID: 35547164
  10. Schindeler A, McDonald MM, Bokko P, Little DG, Eds. Bone remodeling during fracture repair: The cellular picture Seminars in cell & developmental biology. Elsevier 2008.
  11. Perry CR. Bone repair techniques, bone graft, and bone graft substitutes. Clin Orthop Relat Res 1999; 360(360): 71-86. doi: 10.1097/00003086-199903000-00010 PMID: 10101312
  12. Murphy CM, O’Brien FJ, Little DG, Schindeler A. Cell-scaffold interactions in the bone tissue engineering triad. Eur Cell Mater 2013; 26: 120-32. doi: 10.22203/eCM.v026a09
  13. Storti G, Scioli MG, Kim B-S, Orlandi A, Cervelli V. Adipose-derived stem cells in bone tissue engineering: Useful tools with new applica-tions. Stem Cells Int 2019; 2019: 3673857. doi: 10.1155/2019/3673857
  14. Abazari MF, Hosseini Z, Zare Karizi S, et al. Different osteogenic differentiation potential of mesenchymal stem cells on three different polymeric substrates. Gene 2020; 740: 144534. doi: 10.1016/j.gene.2020.144534 PMID: 32145328
  15. Sabouri E, Rezaie Z, Enderami SE, Mirahmadi M, Askari M. Different osteoconductivity of PLLA/PHB composite nanofibers prepared by one‐ and two‐nozzle electrospinning. Polym Adv Technol 2021; 32(4): 1783-92. doi: 10.1002/pat.5215
  16. Abazari MF, Nejati F, Nasiri N, et al. Platelet-rich plasma incorporated electrospun PVA-chitosan-HA nanofibers accelerates osteogenic differentiation and bone reconstruction. Gene 2019; 720: 144096. doi: 10.1016/j.gene.2019.144096 PMID: 31476405
  17. Hosseini FS, Soleimanifar F, Ardeshirylajimi A, et al. In vitro osteogenic differentiation of stem cells with different sources on composite scaffold containing natural bioceramic and polycaprolactone. Artif Cells Nanomed Biotechnol 2019; 47(1): 300-7. doi: 10.1080/21691401.2018.1553785 PMID: 30688102
  18. Moosazadeh Moghaddam M, Bonakdar S, Shokrgozar MA, Faghihi S. Repair of spinal cord injury; mesenchymal stem cells as an alterna-tive for Schwann cells. Journal of Applied Biotechnology Reports 2018; 5(1): 42-7. doi: 10.29252/JABR.05.02.01
  19. Hedelin H, Larnert P, Hebelka H, Brisby H, Lagerstrand K, Laine T. Innominate Salter osteotomy using resorbable screws: A retrospective case series and presentation of a new concept for fixation. J Child Orthop 2019; 13(3): 310-7. doi: 10.1302/1863-2548.13.180195 PMID: 31312271
  20. Araujo-Pires AC, Mendes VC, Ferreira-Junior O, Carvalho PSP, Guan L, Davies JE. Investigation of a Novel PLGA/CaP scaffold in the healing of tooth extraction sockets to alveolar bone preservation in humans. Clin Implant Dent Relat Res 2016; 18(3): 559-70. doi: 10.1111/cid.12326 PMID: 25819474
  21. Koons GL, Diba M, Mikos AG. Materials design for bone-tissue engineering. Nat Rev Mater 2020; 5(8): 584-603. doi: 10.1038/s41578-020-0204-2
  22. Zheng Y, Han Q, Wang J, Li D, Song Z, Yu J. Promotion of osseointegration between implant and bone interface by titanium alloy porous scaffolds prepared by 3D printing. ACS Biomater Sci Eng 2020; 6(9): 5181-90. doi: 10.1021/acsbiomaterials.0c00662 PMID: 33455268
  23. Przybyłek I, Karpiński TM. Antibacterial properties of propolis. Molecules 2019; 24(11): 2047. doi: 10.3390/molecules24112047 PMID: 31146392
  24. Anjum SI, Ullah A, Khan KA, et al. Composition and functional properties of propolis (bee glue): A review. Saudi J Biol Sci 2019; 26(7): 1695-703. doi: 10.1016/j.sjbs.2018.08.013 PMID: 31762646
  25. Santos LM, Fonseca MS, Sokolonski AR, et al. Propolis: types, composition, biological activities, and veterinary product patent prospect-ing. J Sci Food Agric 2020; 100(4): 1369-82. doi: 10.1002/jsfa.10024 PMID: 31487405
  26. Ciuffreda MC, Malpasso G, Musarò P, Turco V, Gnecchi M. Protocols for in vitro differentiation of human mesenchymal stem cells into osteogenic, chondrogenic and adipogenic lineages Mesenchymal Stem Cells. Springer 2016; pp. 149-58.
  27. Bankova V, Trusheva B, Popova M. Propolis extraction methods: A review. J Apic Res 2021; 60(5): 734-43. doi: 10.1080/00218839.2021.1901426
  28. Shin HJ, Lee CH, Cho IH, et al. Electrospun PLGA nanofiber scaffolds for articular cartilage reconstruction: mechanical stability, degrada-tion and cellular responses under mechanical stimulation in vitro. J Biomater Sci Polym Ed 2006; 17(1-2): 103-19. doi: 10.1163/156856206774879126 PMID: 16411602
  29. Daliri Shadmehri F, Karimi E, Saburi E. Electrospun PCL/fibrin scaffold as a bone implant improved the differentiation of human adipose-derived mesenchymal stem cells into osteo-like cells. International Journal of Polymeric Materials and Polymeric Biomaterials 2022; 71: 1-8. doi: 10.1080/00914037.2022.2124253
  30. Langenbach F, Handschel J. Effects of dexamethasone, ascorbic acid and β-glycerophosphate on the osteogenic differentiation of stem cells in vitro. Stem Cell Res Ther 2013; 4(5): 117. doi: 10.1186/scrt328 PMID: 24073831
  31. Porter RM, Huckle WR, Goldstein AS. Effect of dexamethasone withdrawal on osteoblastic differentiation of bone marrow stromal cells. J Cell Biochem 2003; 90(1): 13-22. doi: 10.1002/jcb.10592 PMID: 12938152
  32. Tahmasebi A, Enderami SE, Saburi E, et al. Micro‐RNA‐incorporated electrospun nanofibers improve osteogenic differentiation of hu-man‐induced pluripotent stem cells. J Biomed Mater Res A 2020; 108(2): 377-86. doi: 10.1002/jbm.a.36824 PMID: 31654461
  33. Abazari MF, Soleimanifar F, Amini Faskhodi M, et al. Improved osteogenic differentiation of human induced pluripotent stem cells cul-tured on polyvinylidene fluoride/collagen/platelet‐rich plasma composite nanofibers. J Cell Physiol 2020; 235(2): 1155-64. doi: 10.1002/jcp.29029 PMID: 31250436
  34. Mirzaei A, Saburi E, Enderami SE, et al. Synergistic effects of polyaniline and pulsed electromagnetic field to stem cells osteogenic differ-entiation on polyvinylidene fluoride scaffold. Artif Cells Nanomed Biotechnol 2019; 47(1): 3058-66. doi: 10.1080/21691401.2019.1645154 PMID: 31339375
  35. Osteogenesis and mineralization of mesenchymal stem cells in collagen type I-based recombinant peptide scaffolds. Journal of Biomedical Materials Research Part A 2017; 105(7): 1856-66. doi: 10.1002/jbm.a.36049 doi: 10.1242/bio.053280 PMID: 32973080
  36. Bruderer M, Richards RG, Alini M, Stoddart MJ. Role and regulation of RUNX2 in osteogenesis. Eur Cell Mater 2014; 28(28): 269-86. doi: 10.22203/eCM.v028a19 PMID: 25340806
  37. Kannan S, Ghosh J, Dhara SK. Osteogenic differentiation potential and marker gene expression of different porcine bone marrow mesenchymal stem cell subpopulations selected in different basal media. bioRxiv. Biology Open 2020; 9(10): bio053280. 10.1242/bio.053280 doi: 10.1101/2020.04.27.063230
  38. Lin X, Patil S, Gao YG, Qian A. The bone extracellular matrix in bone formation and regeneration. Front Pharmacol 2020; 11: 757. doi: 10.3389/fphar.2020.00757 PMID: 32528290
  39. Xin X, Hussain M, Mao JJ. Continuing differentiation of human mesenchymal stem cells and induced chondrogenic and osteogenic line-ages in electrospun PLGA nanofiber scaffold. Biomaterials 2007; 28(2): 316-25. doi: 10.1016/j.biomaterials.2006.08.042 PMID: 17010425
  40. Thomas M, Arora A, Katti DS. Surface hydrophilicity of PLGA fibers governs in vitro mineralization and osteogenic differentiation. Mater Sci Eng C 2014; 45: 320-32. doi: 10.1016/j.msec.2014.08.074 PMID: 25491835
  41. Elkhenany H, El-Badri N, Dhar M. Green propolis extract promotes in vitro proliferation, differentiation, and migration of bone marrow stromal cells. Biomed Pharmacother 2019; 115: 108861. doi: 10.1016/j.biopha.2019.108861 PMID: 31005795
  42. Elgendy A, Fayyad D. Cell viability and apoptotic changes of dental pulp stem cells treated with propolis, chitosan, and their nano coun-terparts. Tanta Dental J 2017; 14(4): 198-207. doi: 10.4103/tdj.tdj_27_17
  43. Chahal S, Kumar A, Hussian FSJ. Development of biomimetic electrospun polymeric biomaterials for bone tissue engineering. A review. J Biomater Sci Polym Ed 2019; 30(14): 1308-55. doi: 10.1080/09205063.2019.1630699 PMID: 31181982
  44. Wang S, Hu F, Li J, et al. Design of electrospun nanofibrous mats for osteogenic differentiation of mesenchymal stem cells. Nanomedicine 2018; 14(7): 2505-20. doi: 10.1016/j.nano.2016.12.024 PMID: 28554595
  45. Jin S, Xia X, Huang J, et al. Recent advances in PLGA-based biomaterials for bone tissue regeneration. Acta Biomater 2021; 127: 56-79. doi: 10.1016/j.actbio.2021.03.067 PMID: 33831569
  46. Gentile P, Chiono V, Carmagnola I, Hatton P. An overview of poly(lactic-co-glycolic) acid (PLGA)-based biomaterials for bone tissue engineering. Int J Mol Sci 2014; 15(3): 3640-59. doi: 10.3390/ijms15033640 PMID: 24590126
  47. Yang X, Li Y, Liu X, Huang Q, Zhang R, Feng Q. Incorporation of silica nanoparticles to PLGA electrospun fibers for osteogenic differen-tiation of human osteoblast-like cells. Regen Biomater 2018; 5(4): 229-38. doi: 10.1093/rb/rby014 PMID: 30094062
  48. Yang X, Li Y, He W, Huang Q, Zhang R, Feng Q. Hydroxyapatite/collagen coating on PLGA electrospun fibers for osteogenic differentia-tion of bone marrow mesenchymal stem cells. J Biomed Mater Res A 2018; 106(11): 2863-70. doi: 10.1002/jbm.a.36475 PMID: 30289593
  49. Abazari MF, Zare Karizi S, Kohandani M, et al. MicroRNA ‐2861 and nanofibrous scaffold synergistically promote human inducedpluripotent stem cells osteogenic differentiation. Polym Adv Technol 2020; 31(10): pat.4946. doi: 10.1002/pat.4946
  50. Kresnoadi U, Lunardhi L, Agustono B. Propolis extract and bovine bone graft combination in the expression of VEGF and FGF2 on the preservation of post extraction socket. J Indian Prosthodont Soc 2020; 20(4): 417-23. doi: 10.4103/jips.jips_106_20 PMID: 33487970
  51. Somsanith N, Kim YK, Jang YS, et al. Enhancing of osseointegration with propolis-loaded TiO2 nanotubes in rat mandible for dental implants. Materials 2018; 11(1): 61. doi: 10.3390/ma11010061 PMID: 29301269

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers