Skip to main content
SpringerLink
Log in

Enhancing the function of PLGA-collagen scaffold by incorporating TGF-β1-loaded PLGA-PEG-PLGA nanoparticles for cartilage tissue engineering using human dental pulp stem cells

  • Original Article
  • Published:
Drug Delivery and Translational Research Aims and scope Submit manuscript

Abstract

Since cartilage has a limited capacity for self-regeneration, treating cartilage degenerative disorders is a long-standing difficulty in orthopedic medicine. Researchers have scrutinized cartilage tissue regeneration to handle the deficiency of cartilage restoration capacity. This investigation proposed to compose an innovative nanocomposite biomaterial that enhances growth factor delivery to the injured cartilage site. Here, we describe the design and development of the biocompatible poly(lactide-co-glycolide) acid-collagen/poly(lactide-co-glycolide)-poly(ethylene glycol)-poly(lactide-co-glycolide) (PLGA-collagen/PLGA-PEG-PLGA) nanocomposite hydrogel containing transforming growth factor-β1 (TGF-β1). PLGA-PEG-PLGA nanoparticles were employed as a delivery system embedding TGF-β1 as an articular cartilage repair therapeutic agent. This study evaluates various physicochemical aspects of fabricated scaffolds by 1HNMR, FT-IR, SEM, BET, and DLS methods. The physicochemical features of the developed scaffolds, including porosity, density, degradation, swelling ratio, mechanical properties, morphologies, BET, ELISA, and cytotoxicity were assessed. The cell viability was investigated with the MTT test. Chondrogenic differentiation was assessed via Alcian blue staining and RT-PCR. In real-time PCR testing, the expression of Sox-9, collagen type II, and aggrecan genes was monitored. According to the results, human dental pulp stem cells (hDPSCs) exhibited high adhesion, proliferation, and differentiation on PLGA-collagen/PLGA-PEG-PLGA-TGFβ1 nanocomposite scaffolds compared to the control groups. SEM images displayed suitable cell adhesion and distribution of hDPSCs throughout the scaffolds. RT-PCR assay data displayed that TGF-β1 loaded PLGA-PEG-PLGA nanoparticles puts forward chondroblast differentiation in hDPSCs through the expression of chondrogenic genes. The findings revealed that PLGA-collagen/PLGA-PEG-PLGA-TGF-β1 nanocomposite hydrogel can be utilized as a supportive platform to support hDPSCs differentiation by implementing specific physio-chemical features.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Availability of data and materials

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

PBS:

Phosphate-buffered saline

FBS:

Fetal bovine serum

DMEM:

Dulbecco modified Eagle’s medium

h-DPSCs:

Human dental pulp-derived mesenchymal stem cells

ELISA:

Enzyme-linked immunosorbent assay

PLGA-PEG-PLGA:

Poly D, L (lactide-co-glycolide)-b-poly (ethylene glycol)-b-poly D, L (lactide-co-glycolide

MTT:

3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide

References

  1. Elisseeff J. Injectable cartilage tissue engineering. Expert Opin Biol Ther. 2004;4(12):1849–59.

    Article  CAS  PubMed  Google Scholar 

  2. Kalamegam G, et al. A comprehensive review of stem cells for cartilage regeneration in osteoarthritis. 2018.

  3. Iturriaga L, et al. Advances in stem cell therapy for cartilage regeneration in osteoarthritis. Expert Opin Biol Ther. 2018;18(8):883–96.

    Article  CAS  PubMed  Google Scholar 

  4. Amini AA, Nair LS. Injectable hydrogels for bone and cartilage repair. Biomed Mater. 2012;7(2): p. 024105.

  5. Munir N, Callanan A. Novel phase separated polycaprolactone/collagen scaffolds for cartilage tissue engineering. Biomed Mater. 2018;13(5): p. 051001.

  6. Mistry H, et al. Autologous chondrocyte implantation in the knee: systematic review and economic evaluation. 2017.

  7. Demoor M, et al. Cartilage tissue engineering: molecular control of chondrocyte differentiation for proper cartilage matrix reconstruction. Biochimica et Biophysica Acta (BBA) - General Subjects. 2014;1840(8): p. 2414–2440.

  8. Mansour JM. Biomechanics of cartilage. Kinesiology: the mechanics and pathomechanics of human movement. 2003;p. 66–79.

  9. Sophia Fox AJ, Bedi A, Rodeo SA. The basic science of articular cartilage: structure, composition, and function. Sports Health. 2009;1(6): p. 461–468.

  10. Fernandes TL, et al. Systematic review of human dental pulp stem cells for cartilage regeneration. Tissue Eng Part B Rev. 2020;26(1):1–12.

    Article  PubMed  Google Scholar 

  11. Li P-L, et al. Clinical-grade human dental pulp stem cells suppressed the activation of osteoarthritic macrophages and attenuated cartilaginous damage in a rabbit osteoarthritis model. Stem Cell Res Ther. 2021;12(1):1–15.

    Article  Google Scholar 

  12. Hokmabad VR, et al. A comparison of the effects of silica and hydroxyapatite nanoparticles on poly (ε-caprolactone)-poly (ethylene glycol)-poly (ε-caprolactone)/chitosan nanofibrous scaffolds for bone tissue engineering. Tissue Engineering and Regenerative Medicine. 2018;15(6):735–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Aghazadeh M, et al. The effect of melanocyte stimulating hormone and hydroxyapatite on osteogenesis in pulp stem cells of human teeth transferred into polyester scaffolds. Fibers and Polymers. 2018;19(11):2245–53.

    Article  CAS  Google Scholar 

  14. Cristaldi M, et al. Dental pulp stem cells for bone tissue engineering: a review of the current literature and a look to the future. Regen Med. 2018;13(2):207–18.

    Article  Google Scholar 

  15. Williams DF, et al. Chapter 36 - hydrogels in regenerative medicine. In: Atala A, et al., editors. Principles of Regenerative Medicine (Third Edition). Boston: Academic Press; 2019. p. 627–50.

    Chapter  Google Scholar 

  16. Yegappan R, et al. Injectable angiogenic and osteogenic carrageenan nanocomposite hydrogel for bone tissue engineering. Int J Biol Macromol. 2019;122:320–8.

    Article  CAS  PubMed  Google Scholar 

  17. Vega SL, Kwon MY, Burdick JA. Recent advances in hydrogels for cartilage tissue engineering. Eur Cell Mater. 2017;33:59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bernhard JC, Vunjak-Novakovic G. Should we use cells, biomaterials, or tissue engineering for cartilage regeneration? Stem Cell Res Ther. 2016;7(1):56.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Elango J, et al. Rheological, biocompatibility and osteogenesis assessment of fish collagen scaffold for bone tissue engineering. Int J Biol Macromol. 2016;91:51–9.

    Article  CAS  PubMed  Google Scholar 

  20. Lee HJ. Hybrid hydrogels for tissue engineering. 2015.

  21. Wang J, et al. Silk fibroin/collagen/hyaluronic acid scaffold incorporating pilose antler polypeptides microspheres for cartilage tissue engineering. Mater Sci Eng, C. 2019;94:35–44.

    Article  CAS  Google Scholar 

  22. Chicatun F, et al. Collagen/chitosan composite scaffolds for bone and cartilage tissue engineering. In: Biomedical Composites. Elsevier; 2017. p. 163–98.

    Chapter  Google Scholar 

  23. Quinlan E, et al. Hypoxia-mimicking bioactive glass/collagen glycosaminoglycan composite scaffolds to enhance angiogenesis and bone repair. Biomaterials. 2015;52:358–66.

    Article  CAS  PubMed  Google Scholar 

  24. Raeisdasteh Hokmabad V, et al. Design and fabrication of porous biodegradable scaffolds: a strategy for tissue engineering. J Biomater Sci Polym Ed. 2017;28(16):1797–825.

    Article  CAS  PubMed  Google Scholar 

  25. Khorshid NK, et al. Novel structural changes during temperature-induced self-assembling and gelation of PLGA-PEG-PLGA triblock copolymer in aqueous solutions. Macromol Biosci. 2016;16(12):1838–52.

    Article  CAS  PubMed  Google Scholar 

  26. Chen G, Kawazoe N. Porous scaffolds for regeneration of cartilage, bone and osteochondral tissue. Osteochondral Tissue Engineering: Nanotechnology, Scaffolding-Related Developments and Translation. 2018; p. 171–191.

  27. Witwer KW, Wolfram J. Extracellular vesicles versus synthetic nanoparticles for drug delivery. Nat Rev Mater. 2021;6(2):103–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Herrmann IK, Wood MJA, Fuhrmann G. Extracellular vesicles as a next-generation drug delivery platform. Nat Nanotechnol. 2021;16(7):748–59.

    Article  CAS  PubMed  Google Scholar 

  29. Alcaraz MJ, Compañ A, Guillén MI. Extracellular vesicles from mesenchymal stem cells as novel treatments for musculoskeletal diseases. Cells. 2020;9(1):98.

    Article  CAS  Google Scholar 

  30. Jin Q, et al. Extracellular vesicles derived from human dental pulp stem cells promote osteogenesis of adipose-derived stem cells via the MAPK pathway. Journal of tissue engineering. 2020;11:2041731420975569.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Della Porta G, Ciardulli MC, Maffulli N. Microcapsule technology for controlled growth factor release in musculoskeletal tissue engineering. Sports medicine and arthroscopy review. 2018;26(2): p. e2-e9.

  32. Awad HA, et al. Effects of transforming growth factor β 1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng. 2003;9(6):1301–12.

    Article  CAS  PubMed  Google Scholar 

  33. Na K, et al. Delivery of dexamethasone, ascorbate, and growth factor (TGF β-3) in thermo-reversible hydrogel constructs embedded with rabbit chondrocytes. Biomaterials. 2006;27(35):5951–7.

    Article  CAS  PubMed  Google Scholar 

  34. Kowalczewski CJ, Saul JM. Biomaterials for the delivery of growth factors and other therapeutic agents in tissue engineering approaches to bone regeneration. Front Pharmacol. 2018;9:513.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Askari M, et al. Sustained release of TGF-β1 via genetically-modified cells induces the chondrogenic differentiation of mesenchymal stem cells encapsulated in alginate sulfate hydrogels. J Mater Sci - Mater Med. 2019;30(1):7.

    Article  Google Scholar 

  36. Levinson C, et al. An injectable heparin-conjugated hyaluronan scaffold for local delivery of transforming growth factor β1 promotes successful chondrogenesis. Acta Biomater. 2019;99:168–80.

    Article  CAS  PubMed  Google Scholar 

  37. Böck T, et al. TGF-β1-modified hyaluronic acid/poly (glycidol) hydrogels for chondrogenic differentiation of human mesenchymal stromal cells. Macromol Biosci. 2018;18(7):1700390.

    Article  Google Scholar 

  38. Fernandes TL, et al. Macrophage: a potential target on cartilage regeneration. Front Immunol. 2020;11:111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Modaresifar K, Hadjizadeh A, Niknejad H. Design and fabrication of GelMA/chitosan nanoparticles composite hydrogel for angiogenic growth factor delivery. Artificial cells, nanomedicine, and biotechnology. 2018;46(8):1799–808.

    CAS  PubMed  Google Scholar 

  40. Begines B, et al. Polymeric nanoparticles for drug delivery: recent developments and future prospects. Nanomaterials. 2020;10(7):1403.

    Article  CAS  PubMed Central  Google Scholar 

  41. Oliveira ÉR, et al. Advances in growth factor delivery for bone tissue engineering. Int J Mol Sci. 2021;22(2):903.

    Article  CAS  PubMed Central  Google Scholar 

  42. Wang J, et al. Double-layered collagen/silk fibroin composite scaffold that incorporates TGF-β1 nanoparticles for cartilage tissue engineering. J Biomater Tissue Eng. 2015;5(5):357–63.

    Article  Google Scholar 

  43. Li Y, Liu Y, Guo Q. Silk fibroin hydrogel scaffolds incorporated with chitosan nanoparticles repair articular cartilage defects by regulating TGF-β1 and BMP-2. Arthritis Res Ther. 2021;23(1):1–11.

    Article  Google Scholar 

  44. Rong X, et al. Neuroprotective effect of insulin-loaded chitosan nanoparticles/PLGA-PEG-PLGA hydrogel on diabetic retinopathy in rats. Int J Nanomed. 2019;14:45.

    Article  CAS  Google Scholar 

  45. Pan J, et al. Thermosensitive hydrogel delivery of human periodontal stem cells overexpressing platelet-derived growth factor-BB enhances alveolar bone defect repair. Stem cells and development. 2019;28(24):1620–31.

    Article  CAS  PubMed  Google Scholar 

  46. Lamparelli EP, et al. Chondrogenic commitment of human bone marrow mesenchymal stem cells in a perfused collagen hydrogel functionalized with hTGF-β1-releasing PLGA microcarrier. Pharmaceutics. 2021;13(3):399.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kirby GT, et al. Microparticles for sustained growth factor delivery in the regeneration of critically-sized segmental tibial bone defects. Materials. 2016;9(4):259.

    Article  PubMed Central  Google Scholar 

  48. Ghandforoushan P, et al. Novel nanocomposite scaffold based on Gelatin/PLGA-PEG-PLGA hydrogels embedded with TGF-β1 for chondrogenic differentiation of human dental pulp stem cells in vitro. Int J Biol Macromol. 2022.

  49. Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. In: Williams DF, editor. The Biomaterials: Silver Jubilee Compendium. Oxford: Elsevier Science; 2000. p. 175–89.

    Chapter  Google Scholar 

  50. Lee DH, et al. Enhanced osteogenesis of β-tricalcium phosphate reinforced silk fibroin scaffold for bone tissue biofabrication. Int J Biol Macromol. 2017;95:14–23.

    Article  CAS  PubMed  Google Scholar 

  51. Zijah V, et al. Towards optimization of odonto/osteogenic bioengineering: in vitro comparison of simvastatin, sodium fluoride, melanocyte-stimulating hormone. In Vitro Cellular & Developmental Biology-Animal. 2017;53(6):502–12.

    Article  CAS  Google Scholar 

  52. Sun X, et al. Collagen-based porous scaffolds containing PLGA microspheres for controlled kartogenin release in cartilage tissue engineering. Artificial cells, nanomedicine, and biotechnology. 2018;46(8):1957–66.

    CAS  PubMed  Google Scholar 

  53. Valipour F, et al. Novel hybrid polyester-polyacrylate hydrogels enriched with platelet-derived growth factor for chondrogenic differentiation of adipose-derived mesenchymal stem cells in vitro. J Biol Eng. 2021;15(1):1–14.

    Article  Google Scholar 

  54. Riaz T, et al. FTIR analysis of natural and synthetic collagen. Appl Spectrosc Rev. 2018;53(9):703–46.

    Article  CAS  Google Scholar 

  55. Bhardwaj N, et al. Potential of 3-D tissue constructs engineered from bovine chondrocytes/silk fibroin-chitosan for in vitro cartilage tissue engineering. Biomaterials. 2011;32(25):5773–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Khajavi M, et al. Fish cartilage: a promising source of biomaterial for biological scaffold fabrication in cartilage tissue engineering. J Biomed Mater Res Part A. 2021.

  57. Song JE, et al. Evaluation of silymarin/duck’s feet-derived collagen/hydroxyapatite sponges for bone tissue regeneration. Mater Sci Eng, C. 2019;97:347–55.

    Article  CAS  Google Scholar 

  58. Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26(27):5474–91.

    Article  CAS  PubMed  Google Scholar 

  59. Wang Y-F, et al. Systematic characterization of porosity and mass transport and mechanical properties of porous polyurethane scaffolds. J Mech Behav Biomed Mater. 2017;65:657–64.

    Article  CAS  PubMed  Google Scholar 

  60. Velasco-Rodriguez B, et al. Hybrid methacrylated gelatin and hyaluronic acid hydrogel scaffolds. preparation and systematic characterization for prospective tissue engineering applications. Int J Mol Sci. 2021;22(13): p. 6758.

  61. Toledo L, et al. Physical nanocomposite hydrogels filled with low concentrations of TiO2 nanoparticles: swelling, networks parameters and cell retention studies. Mater Sci Eng, C. 2018;92:769–78.

    Article  CAS  Google Scholar 

  62. Raschip IE, et al. Development of antioxidant and antimicrobial xanthan-based cryogels with tuned porous morphology and controlled swelling features. Int J Biol Macromol. 2020;156:608–20.

    Article  CAS  PubMed  Google Scholar 

  63. Jiang Y, et al. Nanoparticle–hydrogel superstructures for biomedical applications. J Control Release. 2020;324:505–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Ren L, et al. Surface modification of bundle-type polyamide fiber nonwoven with collagen to improve its hydrophilicity. J Ind Eng Chem. 2020;89:392–9.

    Article  CAS  Google Scholar 

  65. Nandagiri VK, et al. Incorporation of PLGA nanoparticles into porous chitosan–gelatin scaffolds: influence on the physical properties and cell behavior. J Mech Behav Biomed Mater. 2011;4(7):1318–27.

    Article  CAS  PubMed  Google Scholar 

  66. Nistor MT, Vasile C, Chiriac AP. Hybrid collagen-based hydrogels with embedded montmorillonite nanoparticles. Mater Sci Eng, C. 2015;53:212–21.

    Article  CAS  Google Scholar 

  67. She Z, et al. Preparation and in vitro degradation of porous three-dimensional silk fibroin/chitosan scaffold. Polym Degrad Stab. 2008;93(7):1316–22.

    Article  CAS  Google Scholar 

  68. Rychter P, et al. PLGA–PEG terpolymers as a carriers of bioactive agents, influence of PEG blocks content on degradation and release of herbicides into soil. Polym Degrad Stab. 2019.

  69. Ibrahim TM, El-Megrab NA, El-Nahas HM. An overview of PLGA in-situ forming implants based on solvent exchange technique: effect of formulation components and characterization. Pharm Dev Technol. 2021;26(7):709–28.

    Article  CAS  PubMed  Google Scholar 

  70. Jin S, et al. Recent advances in PLGA-based biomaterials for bone tissue regeneration. Acta Biomater. 2021;127:56–79.

    Article  CAS  PubMed  Google Scholar 

  71. Makadia HK, Siegel SJ. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers. 2011;3(3):1377–97.

    Article  CAS  PubMed  Google Scholar 

  72. Houchin M, Topp E. Physical properties of PLGA films during polymer degradation. J Appl Polym Sci. 2009;114(5):2848–54.

    Article  CAS  Google Scholar 

  73. Li Y, Rodrigues J, Tomas H. Injectable and biodegradable hydrogels: gelation, biodegradation and biomedical applications. Chem Soc Rev. 2012;41(6):2193–221.

    Article  CAS  PubMed  Google Scholar 

  74. Li Y, et al. Immunosuppressive PLGA TGF-β1 microparticles induce polyclonal and antigen-specific regulatory T cells for local immunomodulation of allogeneic islet transplants. Front Immunol. 2021;12:1484.

    Google Scholar 

  75. Chen L, et al. Growth factor and its polymer scaffold-based delivery system for cartilage tissue engineering. Int J Nanomed. 2020;15:6097.

    Article  CAS  Google Scholar 

  76. Lin SJ, et al. Growth factor-loaded microspheres in mPEG-polypeptide hydrogel system for articular cartilage repair. J Biomed Mater Res, Part A. 2021;109(12):2516–26.

    Article  CAS  Google Scholar 

  77. Gan S, et al. Nano-hydroxyapatite enhanced double network hydrogels with excellent mechanical properties for potential application in cartilage repair. Carbohydr Polym. 2020;229, p. 115523.

  78. Ma F, et al. In situ fabrication of a composite hydrogel with tunable mechanical properties for cartilage tissue engineering. J Mater Chem B. 2019;7(15):2463–73.

    Article  CAS  PubMed  Google Scholar 

  79. Mallakpour S, Tukhani M, Hussain CM. Recent advancements in 3D bioprinting technology of carboxymethyl cellulose-based hydrogels: utilization in tissue engineering. Adv Colloid Interface Sci. 2021;292, p. 102415.

  80. Khalesi H, et al. New insights into food hydrogels with reinforced mechanical properties: A review on innovative strategies. Adv Colloid Interface Sci. 2020; p. 102278.

  81. Thomas LV, Rahul V, Nair PD. Effect of stiffness of chitosan-hyaluronic acid dialdehyde hydrogels on the viability and growth of encapsulated chondrocytes. Int J Biol Macromol. 2017;104:1925–35.

    Article  CAS  Google Scholar 

  82. Uzieliene I, et al. Mechanotransducive biomimetic systems for chondrogenic differentiation in vitro. Int J Mol Sci. 2021;22(18):9690.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Gao F, et al. Osteochondral regeneration with 3D-printed biodegradable high-strength supramolecular polymer reinforced-gelatin hydrogel scaffolds. Advanced Science. 2019;6(15):1900867.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Liao I-C, et al. Composite Three-dimensional woven scaffolds with interpenetrating network hydrogels to create functional synthetic articular cartilage. Adv Func Mater. 2013;23(47):5833–9.

    Article  CAS  Google Scholar 

  85. Mondal D, Willett TL. Mechanical properties of nanocomposite biomaterials improved by extrusion during direct ink writing. J Mech Behav Biomed Mater. 2020;104, p. 103653.

  86. Czepirski L, Balys MR, Komorowska-Czepirska E. Some generalization of Langmuir adsorption isotherm. Internet J Chem. 2000;3(14):1099–8292.

    Google Scholar 

  87. Chi H, et al. 3D-HA scaffold functionalized by extracellular matrix of stem cells promotes bone repair. Int J Nanomed. 2020;15:5825.

    Article  CAS  Google Scholar 

  88. Ying J, et al. Transforming growth factor-beta1 promotes articular cartilage repair through canonical Smad and Hippo pathways in bone mesenchymal stem cells. Life Sci. 2018;192:84–90.

    Article  CAS  PubMed  Google Scholar 

  89. Asen A-K, et al. Sustained spatiotemporal release of TGF-β1 confers enhanced very early chondrogenic differentiation during osteochondral repair in specific topographic patterns. FASEB J. 2018;32(10):5298–311.

    Article  CAS  PubMed  Google Scholar 

  90. Velot É, et al. Efficient TGF-β1 delivery to articular chondrocytes in vitro using agro-based liposomes. Int J Mol Sci. 2022;23(5):2864.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Rey-Rico A, et al. Adapted chondrogenic differentiation of human mesenchymal stem cells via controlled release of TGF-β1 from poly (ethylene oxide)–terephtalate/poly (butylene terepthalate) multiblock scaffolds. J Biomed Mater Res, Part A. 2015;103(1):371–83.

    Article  Google Scholar 

  92. Lim SM, et al. Dual growth factor-releasing nanoparticle/hydrogel system for cartilage tissue engineering. J Mater Sci - Mater Med. 2010;21(9):2593–600.

    Article  CAS  PubMed  Google Scholar 

  93. Soysal A, et al. Preparation and characterization of poly (lactic-co-glycolic acid) nanoparticles containing TGF-beta 1 and evaluation of in vitro wound healing effect. J Res Pharm. 2020;24.

Download references

Acknowledgements

This project was fulfilled at the Stem Cell Research Center, Tabriz, Iran. The authors would like to thank everybody who assisted us in this regard.

Funding

This investigation was funded by a grant from Tabriz University of Medical Sciences, Tabriz, Iran, Grant No: 64103.

Author information

Authors and Affiliations

  1. Stem Cell Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Parisa Ghandforoushan & Soodabeh Davaran

  2. Department of Medicinal Chemistry, Faculty of Pharmacy, Tabriz University of Medical Sciences, Tabriz, Iran

    Parisa Ghandforoushan, Jalal Hanaee & Soodabeh Davaran

  3. Pharmaceutical Analysis Research Center, Tabriz University of Medicinal Science, Tabriz, Iran

    Jalal Hanaee

  4. Stem Cell Research Center, Oral Medicine Department, Tabriz University of Medical Sciences, Tabriz, Iran

    Zahra Aghazadeh

  5. Department of Endodontics, Faculty of Dentistry, Tabriz University of Medical Sciences, Tabriz, Iran

    Mohammad Samiei

  6. Department of Orthopedy, Tabriz University of Medical Sciences, Tabriz, Iran

    Amir Mohammad Navali

  7. Department of Biotechnology, Alzahra University, Tehran, Iran

    Ali Khatibi

  8. Applied Drug Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Soodabeh Davaran

Authors
  1. Parisa Ghandforoushan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jalal Hanaee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zahra Aghazadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohammad Samiei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amir Mohammad Navali
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ali Khatibi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Soodabeh Davaran
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Parisa Ghandforoushan: conceptualization, methodology, software, investigation, and writing - original; Jalal Hanaee: validation and supervision; Zahra Aghazadeh: methodology, validation, and data curation; Shahin Ahmadian: conceptualization and methodology; Mohammad Samiei: data curation and validation; Amir Mohammad Navali: investigation and writing - reviewing and editing; Ali Khatibi: investigation, software, and data curation; Soodabeh Davaran: conceptualization, methodology, validation, and supervision.

Corresponding author

Correspondence to Soodabeh Davaran.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

All authors have been personally and actively involved in substantial work leading to the paper, and will take public responsibility for its content.

Competing interests

The author declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 118 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghandforoushan, P., Hanaee, J., Aghazadeh, Z. et al. Enhancing the function of PLGA-collagen scaffold by incorporating TGF-β1-loaded PLGA-PEG-PLGA nanoparticles for cartilage tissue engineering using human dental pulp stem cells. Drug Deliv. and Transl. Res. 12, 2960–2978 (2022). https://doi.org/10.1007/s13346-022-01161-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13346-022-01161-2

Keywords

Search

Navigation