Analyze Diet
International journal of molecular sciences2019; 20(21); 5474; doi: 10.3390/ijms20215474

Transforming Growth Factor Beta 3-Loaded Decellularized Equine Tendon Matrix for Orthopedic Tissue Engineering.

Abstract: Transforming growth factor beta 3 (TGFβ3) promotes tenogenic differentiation and may enhance tendon regeneration in vivo. This study aimed to apply TGFβ3 absorbed in decellularized equine superficial digital flexor tendon scaffolds, and to investigate the bioactivity of scaffold-associated TGFβ3 in an in vitro model. TGFβ3 could effectively be loaded onto tendon scaffolds so that at least 88% of the applied TGFβ3 were not detected in the rinsing fluid of the TGFβ3-loaded scaffolds. Equine adipose tissue-derived multipotent mesenchymal stromal cells (MSC) were then seeded on scaffolds loaded with 300 ng TGFβ3 to assess its bioactivity. Both scaffold-associated TGFβ3 and TGFβ3 dissolved in the cell culture medium, the latter serving as control group, promoted elongation of cell shapes and scaffold contraction ( < 0.05). Furthermore, scaffold-associated and dissolved TGFβ3 affected MSC musculoskeletal gene expression in a similar manner, with an upregulation of tenascin c and downregulation of other matrix molecules, most markedly decorin ( < 0.05). These results demonstrate that the bioactivity of scaffold-associated TGFβ3 is preserved, thus TGFβ3 application via absorption in decellularized tendon scaffolds is a feasible approach.
Publication Date: 2019-11-03 PubMed ID: 31684150PubMed Central: PMC6862173DOI: 10.3390/ijms20215474Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates the application of Transforming Growth Factor Beta 3 (TGFβ3) into a decellularized equine tendon scaffold, to stimulate tenogenic differentiation which could enhance tendon regeneration in vivo. The study confirms that the bioactivity of this growth factor is maintained, providing a promising approach for orthopedic tissue engineering.

Objective and Methodology

  • The aim of the study was to use TGFβ3, absorbed in decellularized scaffolds from equine superficial digital flexor tendons, and investigate its bioactivity in an in vitro model.
  • TGFβ3 is known to promote tenogenic differentiation, which enhances tendon regeneration in vivo. The scaffolds provided a platform to verify if the bioactivity of TGFβ3 is maintained in such settings.
  • A significant portion, at least 88%, of TGFβ3 applied could be effectively loaded onto tendon scaffolds and was not detected in the rinsing fluid of these scaffolds, affirming effective absorption.

Findings

  • The researchers tested the bioactivity of TGFβ3 by seeding equine adipose tissue-derived multipotent mesenchymal stromal cells (MSC) on scaffolds loaded with 300 ng TGFβ3.
  • Observations were that both scaffold-associated TGFβ3 and TGFβ3 dissolved in the cell culture medium promoted cell elongation and scaffold contraction.
  • Examination of gene expression showed that both scaffold-associated and dissolved TGFβ3 affected MSC musculoskeletal gene expression, triggering an upregulation of tenascin c and downregulation of other matrix molecules, particularly decorin.

Implications

  • These results demonstrate that the bioactivity of scaffold-associated TGFβ3 is preserved, pointing to a feasible method for TGFβ3 application.
  • This finding is valuable in the context of orthopedic tissue engineering, as it could be a significant approach for tendon regeneration.
  • Furthermore, the study presents potential opportunities for developing more advanced treatment styles based on the application of bioactive growth factor to tendon matrices.

Cite This Article

APA
Roth SP, Brehm W, Groß C, Scheibe P, Schubert S, Burk J. (2019). Transforming Growth Factor Beta 3-Loaded Decellularized Equine Tendon Matrix for Orthopedic Tissue Engineering. Int J Mol Sci, 20(21), 5474. https://doi.org/10.3390/ijms20215474

Publication

ISSN: 1422-0067
NlmUniqueID: 101092791
Country: Switzerland
Language: English
Volume: 20
Issue: 21
PII: 5474

Researcher Affiliations

Roth, Susanne Pauline
  • Faculty of Veterinary Medicine, Veterinary Teaching Hospital, Department for Horses, University of Leipzig, D 04103 Leipzig, Germany. Susanne.roth@uni-leipzig.de.
  • Saxonian Incubator for Clinical Translation, University of Leipzig, D-04103 Leipzig, Germany. Susanne.roth@uni-leipzig.de.
Brehm, Walter
  • Faculty of Veterinary Medicine, Veterinary Teaching Hospital, Department for Horses, University of Leipzig, D 04103 Leipzig, Germany. brehm@vetmed.uni-leipzig.de.
Groß, Claudia
  • Saxonian Incubator for Clinical Translation, University of Leipzig, D-04103 Leipzig, Germany. claudia.gross@sikt.uni-leipzig.de.
Scheibe, Patrick
  • Saxonian Incubator for Clinical Translation, University of Leipzig, D-04103 Leipzig, Germany. pscheibe@sikt.uni-leipzig.de.
Schubert, Susanna
  • Saxonian Incubator for Clinical Translation, University of Leipzig, D-04103 Leipzig, Germany. susanna.schubert@sikt.uni-leipzig.de.
Burk, Janina
  • Saxonian Incubator for Clinical Translation, University of Leipzig, D-04103 Leipzig, Germany. Janina.Burk@vetmed.uni-giessen.de.
  • Faculty of Veterinary Medicine, Equine Clinic-Surgery, Justus-Liebig-University Giessen, D-35392 Giessen, Germany. Janina.Burk@vetmed.uni-giessen.de.

MeSH Terms

  • Animals
  • Cell Differentiation
  • Cells, Cultured
  • Decorin / genetics
  • Decorin / metabolism
  • Extracellular Matrix / metabolism
  • Gene Expression Regulation
  • Horses
  • Humans
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / metabolism
  • Musculoskeletal System / metabolism
  • Tenascin / genetics
  • Tenascin / metabolism
  • Tendons / cytology
  • Tendons / physiology
  • Tissue Engineering / methods
  • Tissue Scaffolds
  • Transforming Growth Factor beta3 / metabolism

Grant Funding

  • BMBF 1315883 / Bundesministerium fu00fcr Bildung und Forschung
  • DFG BU3110/1-1 / Deutsche Forschungsgemeinschaft

Conflict of Interest Statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

This article includes 60 references
  1. Yang G, Rothrauff BB, Tuan RS. Tendon and ligament regeneration and repair: clinical relevance and developmental paradigm.. Birth Defects Res C Embryo Today 2013 Sep;99(3):203-222.
    doi: 10.1002/bdrc.21041pmc: PMC4041869pubmed: 24078497google scholar: lookup
  2. Verdiyeva G, Koshy K, Glibbery N, Mann H, Seifalian AM. Tendon Reconstruction with Tissue Engineering Approach--A Review.. J Biomed Nanotechnol 2015 Sep;11(9):1495-523.
    doi: 10.1166/jbn.2015.2121pubmed: 26485923google scholar: lookup
  3. Siegel L, Vandenakker-Albanese C, Siegel D. Anterior cruciate ligament injuries: anatomy, physiology, biomechanics, and management.. Clin J Sport Med 2012 Jul;22(4):349-55.
    doi: 10.1097/JSM.0b013e3182580cd0pubmed: 22695402google scholar: lookup
  4. Schulze-Tanzil G, Al-Sadi O, Ertel W, Lohan A. Decellularized tendon extracellular matrix-a valuable approach for tendon reconstruction?. Cells 2012 Nov 5;1(4):1010-28.
    doi: 10.3390/cells1041010pmc: PMC3901141pubmed: 24710540google scholar: lookup
  5. Longo UG, Lamberti A, Maffulli N, Denaro V. Tissue engineered biological augmentation for tendon healing: a systematic review.. Br Med Bull 2011;98:31-59.
    doi: 10.1093/bmb/ldq030pubmed: 20851817google scholar: lookup
  6. Ladewig K. Drug delivery in soft tissue engineering.. Expert Opin Drug Deliv 2011 Sep;8(9):1175-88.
    doi: 10.1517/17425247.2011.588698pubmed: 21679089google scholar: lookup
  7. Tessmar JK, Göpferich AM. Matrices and scaffolds for protein delivery in tissue engineering.. Adv Drug Deliv Rev 2007 May 30;59(4-5):274-91.
    doi: 10.1016/j.addr.2007.03.020pubmed: 17544542google scholar: lookup
  8. Han P, Cui Q, Yang S, Wang H, Gao P, Li Z. Tumor necrosis factor-α and transforming growth factor-β1 facilitate differentiation and proliferation of tendon-derived stem cells in vitro.. Biotechnol Lett 2017 May;39(5):711-719.
    doi: 10.1007/s10529-017-2296-3pubmed: 28155178google scholar: lookup
  9. Wang Z, Wang Z, Lu W.W, Zhen W, Yang D, Peng S. Novel biomaterial strategies for controlled growth factor delivery for biomedical applications.. NPG Asia Mater 2017;9:e435.
    doi: 10.1038/am.2017.171google scholar: lookup
  10. Liu Y, Ramanath HS, Wang DA. Tendon tissue engineering using scaffold enhancing strategies.. Trends Biotechnol 2008 Apr;26(4):201-9.
    doi: 10.1016/j.tibtech.2008.01.003pubmed: 18295915google scholar: lookup
  11. Chung HJ, Park TG. Surface engineered and drug releasing pre-fabricated scaffolds for tissue engineering.. Adv Drug Deliv Rev 2007 May 30;59(4-5):249-62.
    doi: 10.1016/j.addr.2007.03.015pubmed: 17482310google scholar: lookup
  12. Docheva D, Müller SA, Majewski M, Evans CH. Biologics for tendon repair.. Adv Drug Deliv Rev 2015 Apr;84:222-39.
    doi: 10.1016/j.addr.2014.11.015pmc: PMC4519231pubmed: 25446135google scholar: lookup
  13. Yan Z, Yin H, Nerlich M, Pfeifer CG, Docheva D. Boosting tendon repair: interplay of cells, growth factors and scaffold-free and gel-based carriers.. J Exp Orthop 2018 Jan 5;5(1):1.
    doi: 10.1186/s40634-017-0117-1pmc: PMC5768579pubmed: 29330711google scholar: lookup
  14. Zhang YJ, Chen X, Li G, Chan KM, Heng BC, Yin Z, Ouyang HW. Concise Review: Stem Cell Fate Guided By Bioactive Molecules for Tendon Regeneration.. Stem Cells Transl Med 2018 May;7(5):404-414.
    doi: 10.1002/sctm.17-0206pmc: PMC5905226pubmed: 29573225google scholar: lookup
  15. Kuo CK, Petersen BC, Tuan RS. Spatiotemporal protein distribution of TGF-betas, their receptors, and extracellular matrix molecules during embryonic tendon development.. Dev Dyn 2008 May;237(5):1477-89.
    doi: 10.1002/dvdy.21547pmc: PMC3612428pubmed: 18425852google scholar: lookup
  16. Chan KM, Fu SC, Wong YP, Hui WC, Cheuk YC, Wong MW. Expression of transforming growth factor beta isoforms and their roles in tendon healing.. Wound Repair Regen 2008 May-Jun;16(3):399-407.
  17. Berthet E, Chen C, Butcher K, Schneider RA, Alliston T, Amirtharajah M. Smad3 binds Scleraxis and Mohawk and regulates tendon matrix organization.. J Orthop Res 2013 Sep;31(9):1475-83.
    doi: 10.1002/jor.22382pmc: PMC3960924pubmed: 23653374google scholar: lookup
  18. Havis E, Bonnin MA, Olivera-Martinez I, Nazaret N, Ruggiu M, Weibel J, Durand C, Guerquin MJ, Bonod-Bidaud C, Ruggiero F, Schweitzer R, Duprez D. Transcriptomic analysis of mouse limb tendon cells during development.. Development 2014 Oct;141(19):3683-96.
    doi: 10.1242/dev.108654pubmed: 25249460google scholar: lookup
  19. Pryce BA, Watson SS, Murchison ND, Staverosky JA, Dünker N, Schweitzer R. Recruitment and maintenance of tendon progenitors by TGFbeta signaling are essential for tendon formation.. Development 2009 Apr;136(8):1351-61.
    doi: 10.1242/dev.027342pmc: PMC2687466pubmed: 19304887google scholar: lookup
  20. Barsby T, Guest D. Transforming growth factor beta3 promotes tendon differentiation of equine embryo-derived stem cells.. Tissue Eng Part A 2013 Oct;19(19-20):2156-65.
    doi: 10.1089/ten.tea.2012.0372pubmed: 23611525google scholar: lookup
  21. Kapacee Z, Yeung CY, Lu Y, Crabtree D, Holmes DF, Kadler KE. Synthesis of embryonic tendon-like tissue by human marrow stromal/mesenchymal stem cells requires a three-dimensional environment and transforming growth factor β3.. Matrix Biol 2010 Oct;29(8):668-77.
  22. Macri L, Silverstein D, Clark RA. Growth factor binding to the pericellular matrix and its importance in tissue engineering.. Adv Drug Deliv Rev 2007 Nov 10;59(13):1366-81.
    doi: 10.1016/j.addr.2007.08.015pubmed: 17916397google scholar: lookup
  23. Parkinson J, Samiric T, Ilic MZ, Cook J, Handley CJ. Involvement of proteoglycans in tendinopathy.. J Musculoskelet Neuronal Interact 2011 Jun;11(2):86-93.
    pubmed: 21625045
  24. Prabhath A, Vernekar VN, Sanchez E, Laurencin CT. Growth factor delivery strategies for rotator cuff repair and regeneration.. Int J Pharm 2018 Jun 15;544(2):358-371.
    doi: 10.1016/j.ijpharm.2018.01.006pubmed: 29317260google scholar: lookup
  25. Moshaverinia A, Xu X, Chen C, Ansari S, Zadeh HH, Snead ML, Shi S. Application of stem cells derived from the periodontal ligament or gingival tissue sources for tendon tissue regeneration.. Biomaterials 2014 Mar;35(9):2642-50.
  26. Zhao HY, Wu J, Zhu JJ, Xiao ZC, He CC, Shi HX, Li XK, Yang SL, Xiao J. Research Advances in Tissue Engineering Materials for Sustained Release of Growth Factors.. Biomed Res Int 2015;2015:808202.
    doi: 10.1155/2015/808202pmc: PMC4548067pubmed: 26347885google scholar: lookup
  27. Lomas AJ, Ryan CN, Sorushanova A, Shologu N, Sideri AI, Tsioli V, Fthenakis GC, Tzora A, Skoufos I, Quinlan LR, O'Laighin G, Mullen AM, Kelly JL, Kearns S, Biggs M, Pandit A, Zeugolis DI. The past, present and future in scaffold-based tendon treatments.. Adv Drug Deliv Rev 2015 Apr;84:257-77.
    doi: 10.1016/j.addr.2014.11.022pubmed: 25499820google scholar: lookup
  28. Longo UG, Lamberti A, Petrillo S, Maffulli N, Denaro V. Scaffolds in tendon tissue engineering.. Stem Cells Int 2012;2012:517165.
    doi: 10.1155/2012/517165pmc: PMC3236365pubmed: 22190961google scholar: lookup
  29. Basile P, Dadali T, Jacobson J, Hasslund S, Ulrich-Vinther M, Søballe K, Nishio Y, Drissi MH, Langstein HN, Mitten DJ, O'Keefe RJ, Schwarz EM, Awad HA. Freeze-dried tendon allografts as tissue-engineering scaffolds for Gdf5 gene delivery.. Mol Ther 2008 Mar;16(3):466-73.
    doi: 10.1038/sj.mt.6300395pmc: PMC2705193pubmed: 18180771google scholar: lookup
  30. Abbah SA, Spanoudes K, O'Brien T, Pandit A, Zeugolis DI. Assessment of stem cell carriers for tendon tissue engineering in pre-clinical models.. Stem Cell Res Ther 2014;5(2):38.
    doi: 10.1186/scrt426pmc: PMC4056691pubmed: 25157898google scholar: lookup
  31. Youngstrom DW, Rajpar I, Kaplan DL, Barrett JG. A bioreactor system for in vitro tendon differentiation and tendon tissue engineering.. J Orthop Res 2015 Jun;33(6):911-8.
    doi: 10.1002/jor.22848pmc: PMC5098427pubmed: 25664422google scholar: lookup
  32. Burk J, Plenge A, Brehm W, Heller S, Pfeiffer B, Kasper C. Induction of Tenogenic Differentiation Mediated by Extracellular Tendon Matrix and Short-Term Cyclic Stretching.. Stem Cells Int 2016;2016:7342379.
    doi: 10.1155/2016/7342379pmc: PMC5007347pubmed: 27630718google scholar: lookup
  33. Yin Z, Chen X, Zhu T, Hu JJ, Song HX, Shen WL, Jiang LY, Heng BC, Ji JF, Ouyang HW. The effect of decellularized matrices on human tendon stem/progenitor cell differentiation and tendon repair.. Acta Biomater 2013 Dec;9(12):9317-29.
    doi: 10.1016/j.actbio.2013.07.022pubmed: 23896565google scholar: lookup
  34. Ning LJ, Zhang YJ, Zhang Y, Qing Q, Jiang YL, Yang JL, Luo JC, Qin TW. The utilization of decellularized tendon slices to provide an inductive microenvironment for the proliferation and tenogenic differentiation of stem cells.. Biomaterials 2015 Jun;52:539-50.
  35. Qin TW, Chen Q, Sun YL, Steinmann SP, Amadio PC, An KN, Zhao C. Mechanical characteristics of native tendon slices for tissue engineering scaffold.. J Biomed Mater Res B Appl Biomater 2012 Apr;100(3):752-8.
    doi: 10.1002/jbm.b.32508pmc: PMC3911687pubmed: 22323314google scholar: lookup
  36. Almeida HV, Liu Y, Cunniffe GM, Mulhall KJ, Matsiko A, Buckley CT, O'Brien FJ, Kelly DJ. Controlled release of transforming growth factor-β3 from cartilage-extra-cellular-matrix-derived scaffolds to promote chondrogenesis of human-joint-tissue-derived stem cells.. Acta Biomater 2014 Oct;10(10):4400-9.
    doi: 10.1016/j.actbio.2014.05.030pubmed: 24907658google scholar: lookup
  37. Kim SH, Kim SH, Jung Y. TGF-β3 encapsulated PLCL scaffold by a supercritical CO2-HFIP co-solvent system for cartilage tissue engineering.. J Control Release 2015 May 28;206:101-7.
    doi: 10.1016/j.jconrel.2015.03.026pubmed: 25804870google scholar: lookup
  38. Yang Q, Teng BH, Wang LN, Li K, Xu C, Ma XL, Zhang Y, Kong DL, Wang LY, Zhao YH. Silk fibroin/cartilage extracellular matrix scaffolds with sequential delivery of TGF-β3 for chondrogenic differentiation of adipose-derived stem cells.. Int J Nanomedicine 2017;12:6721-6733.
    doi: 10.2147/IJN.S141888pmc: PMC5600265pubmed: 28932116google scholar: lookup
  39. Roth SP, Schubert S, Scheibe P, Groß C, Brehm W, Burk J. Growth Factor-Mediated Tenogenic Induction of Multipotent Mesenchymal Stromal Cells Is Altered by the Microenvironment of Tendon Matrix.. Cell Transplant 2018 Oct;27(10):1434-1450.
    doi: 10.1177/0963689718792203pmc: PMC6180728pubmed: 30251565google scholar: lookup
  40. King WJ, Krebsbach PH. Growth factor delivery: how surface interactions modulate release in vitro and in vivo.. Adv Drug Deliv Rev 2012 Sep;64(12):1239-56.
    doi: 10.1016/j.addr.2012.03.004pmc: PMC3586795pubmed: 22433783google scholar: lookup
  41. Rifkin DB. Latent transforming growth factor-beta (TGF-beta) binding proteins: orchestrators of TGF-beta availability.. J Biol Chem 2005 Mar 4;280(9):7409-12.
    doi: 10.1074/jbc.R400029200pubmed: 15611103google scholar: lookup
  42. Munger JS, Sheppard D. Cross talk among TGF-β signaling pathways, integrins, and the extracellular matrix.. Cold Spring Harb Perspect Biol 2011 Nov 1;3(11):a005017.
    doi: 10.1101/cshperspect.a005017pmc: PMC3220354pubmed: 21900405google scholar: lookup
  43. Danielpour D, Roberts AB. Specific and sensitive quantitation of transforming growth factor beta 3 by sandwich enzyme-linked immunosorbent assay.. J Immunol Methods 1995 Mar 27;180(2):265-72.
    doi: 10.1016/0022-1759(94)00322-Npubmed: 7714341google scholar: lookup
  44. Taylor SE, Vaughan-Thomas A, Clements DN, Pinchbeck G, Macrory LC, Smith RK, Clegg PD. Gene expression markers of tendon fibroblasts in normal and diseased tissue compared to monolayer and three dimensional culture systems.. BMC Musculoskelet Disord 2009 Feb 26;10:27.
    doi: 10.1186/1471-2474-10-27pmc: PMC2651848pubmed: 19245707google scholar: lookup
  45. Chiquet-Ehrismann R. Tenascins.. Int J Biochem Cell Biol 2004 Jun;36(6):986-90.
    doi: 10.1016/j.biocel.2003.12.002pubmed: 15094113google scholar: lookup
  46. Lu P, Zhang GR, Cai YZ, Heng BC, Ren H, Wang LL, Ji J, Zou XH, Ouyang HW. Lentiviral-encoded shRNA silencing of proteoglycan decorin enhances tendon repair and regeneration within a rat model.. Cell Transplant 2013;22(9):1507-17.
    doi: 10.3727/096368912X661292pubmed: 23295185google scholar: lookup
  47. Nakamura N, Hart DA, Boorman RS, Kaneda Y, Shrive NG, Marchuk LL, Shino K, Ochi T, Frank CB. Decorin antisense gene therapy improves functional healing of early rabbit ligament scar with enhanced collagen fibrillogenesis in vivo.. J Orthop Res 2000 Jul;18(4):517-23.
    doi: 10.1002/jor.1100180402pubmed: 11052486google scholar: lookup
  48. Hoffmann A, Pelled G, Turgeman G, Eberle P, Zilberman Y, Shinar H, Keinan-Adamsky K, Winkel A, Shahab S, Navon G, Gross G, Gazit D. Neotendon formation induced by manipulation of the Smad8 signalling pathway in mesenchymal stem cells.. J Clin Invest 2006 Apr;116(4):940-52.
    doi: 10.1172/JCI22689pmc: PMC1421340pubmed: 16585960google scholar: lookup
  49. Shahab-Osterloh S, Witte F, Hoffmann A, Winkel A, Laggies S, Neumann B, Seiffart V, Lindenmaier W, Gruber AD, Ringe J, Häupl T, Thorey F, Willbold E, Corbeau P, Gross G. Mesenchymal stem cell-dependent formation of heterotopic tendon-bone insertions (osteotendinous junctions).. Stem Cells 2010 Sep;28(9):1590-601.
    doi: 10.1002/stem.487pubmed: 20882636google scholar: lookup
  50. Pelled G, Snedeker JG, Ben-Arav A, Rigozzi S, Zilberman Y, Kimelman-Bleich N, Gazit Z, Müller R, Gazit D. Smad8/BMP2-engineered mesenchymal stem cells induce accelerated recovery of the biomechanical properties of the Achilles tendon.. J Orthop Res 2012 Dec;30(12):1932-9.
    doi: 10.1002/jor.22167pmc: PMC3479351pubmed: 22696396google scholar: lookup
  51. Morikawa M, Derynck R, Miyazono K. TGF-β and the TGF-β Family: Context-Dependent Roles in Cell and Tissue Physiology.. Cold Spring Harb Perspect Biol 2016 May 2;8(5).
    doi: 10.1101/cshperspect.a021873pmc: PMC4852809pubmed: 27141051google scholar: lookup
  52. Ivaska J, Heino J. Cooperation between integrins and growth factor receptors in signaling and endocytosis.. Annu Rev Cell Dev Biol 2011;27:291-320.
  53. Lovati AB, Bottagisio M, Moretti M. Decellularized and Engineered Tendons as Biological Substitutes: A Critical Review.. Stem Cells Int 2016;2016:7276150.
    doi: 10.1155/2016/7276150pmc: PMC4736572pubmed: 26880985google scholar: lookup
  54. Patterson-Kane JC, Rich T. Achilles tendon injuries in elite athletes: lessons in pathophysiology from their equine counterparts.. ILAR J 2014;55(1):86-99.
    doi: 10.1093/ilar/ilu004pubmed: 24936032google scholar: lookup
  55. Wu F, Nerlich M, Docheva D. Tendon injuries: Basic science and new repair proposals.. EFORT Open Rev 2017 Jul;2(7):332-342.
    doi: 10.1302/2058-5241.2.160075pmc: PMC5549180pubmed: 28828182google scholar: lookup
  56. Rodrigues MT, Reis RL, Gomes ME. Engineering tendon and ligament tissues: present developments towards successful clinical products.. J Tissue Eng Regen Med 2013 Sep;7(9):673-86.
    doi: 10.1002/term.1459pubmed: 22499564google scholar: lookup
  57. Roth SP, Erbe I, Burk J. Decellularization of Large Tendon Specimens: Combination of Manually Performed Freeze-Thaw Cycles and Detergent Treatment.. Methods Mol Biol 2018;1577:227-237.
    doi: 10.1007/7651_2017_49pubmed: 28702884google scholar: lookup
  58. Burk J, Erbe I, Berner D, Kacza J, Kasper C, Pfeiffer B, Winter K, Brehm W. Freeze-thaw cycles enhance decellularization of large tendons.. Tissue Eng Part C Methods 2014 Apr;20(4):276-84.
    doi: 10.1089/ten.tec.2012.0760pmc: PMC3968887pubmed: 23879725google scholar: lookup
  59. Ryan J.A. Evolution of Cell Culture Surfaces. .
  60. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR.. Nucleic Acids Res 2001 May 1;29(9):e45.
    doi: 10.1093/nar/29.9.e45pmc: PMC55695pubmed: 11328886google scholar: lookup

Citations

This article has been cited 18 times.
  1. Santra M, Liu YC, Jhanji V, Yam GH. Human SMILE-Derived Stromal Lenticule Scaffold for Regenerative Therapy: Review and Perspectives. Int J Mol Sci 2022 Jul 19;23(14).
    doi: 10.3390/ijms23147967pubmed: 35887309google scholar: lookup
  2. Jankauskaite L, Malinauskas M, Aukstikalne L, Dabasinskaite L, Rimkunas A, Mickevicius T, Pockevičius A, Krugly E, Martuzevicius D, Ciuzas D, Baniukaitiene O, Usas A. Functionalized Electrospun Scaffold-Human-Muscle-Derived Stem Cell Construct Promotes In Vivo Neocartilage Formation. Polymers (Basel) 2022 Jun 19;14(12).
    doi: 10.3390/polym14122498pubmed: 35746068google scholar: lookup
  3. Melzer M, Schubert S, Müller SF, Geyer J, Hagen A, Niebert S, Burk J. Rho/ROCK Inhibition Promotes TGF-β3-Induced Tenogenic Differentiation in Mesenchymal Stromal Cells. Stem Cells Int 2021;2021:8284690.
    doi: 10.1155/2021/8284690pubmed: 34659420google scholar: lookup
  4. Tao M, Ao T, Mao X, Yan X, Javed R, Hou W, Wang Y, Sun C, Lin S, Yu T, Ao Q. Sterilization and disinfection methods for decellularized matrix materials: Review, consideration and proposal. Bioact Mater 2021 Sep;6(9):2927-2945.
  5. Yang F, Richardson DW. Comparative Analysis of Tenogenic Gene Expression in Tenocyte-Derived Induced Pluripotent Stem Cells and Bone Marrow-Derived Mesenchymal Stem Cells in Response to Biochemical and Biomechanical Stimuli. Stem Cells Int 2021;2021:8835576.
    doi: 10.1155/2021/8835576pubmed: 33510795google scholar: lookup
  6. Reifenrath J, Wellmann M, Kempfert M, Angrisani N, Welke B, Gniesmer S, Kampmann A, Menzel H, Willbold E. TGF-β3 Loaded Electrospun Polycaprolacton Fibre Scaffolds for Rotator Cuff Tear Repair: An in Vivo Study in Rats. Int J Mol Sci 2020 Feb 5;21(3).
    doi: 10.3390/ijms21031046pubmed: 32033294google scholar: lookup
  7. Liang W, Ao R, Xu M, Jin M, Han M, Wang Z, Dang W, Wu H, Lin W, Zhen Y, Xu T, An Y. Bifunctional adECM bioscaffold with STIM1-ASCs and IGF-2 promotes functional masseter VML repair via myogenesis and fibrosis suppression. Bioact Mater 2025 Dec;54:466-491.
  8. Pan JJ, Ye C, Li Q, Chen SS, Ning XP, Yu Q, Li BL, Liu XH, Xu ZY. 75% ethanol disinfection preserves biocompatibility and mechanical properties of swim bladder for cardiovascular applications. Am J Transl Res 2025;17(5):3368-3379.
    doi: 10.62347/OVKI5914pubmed: 40535650google scholar: lookup
  9. Euppayo T, Siengdee P, Limlenglert P, Nganvongpanit K, Watanabe G, Kasashima Y, Arai K. In vitro model of equine cartilage degradation; using cartilage pellets differentiated from bone marrow-derived mesenchymal stem cells. In Vitro Cell Dev Biol Anim 2025 Jun;61(6):694-702.
    doi: 10.1007/s11626-025-01049-8pubmed: 40425901google scholar: lookup
  10. Liu J, Song Q, Yin W, Li C, An N, Le Y, Wang Q, Feng Y, Hu Y, Wang Y. Bioactive scaffolds for tissue engineering: A review of decellularized extracellular matrix applications and innovations. Exploration (Beijing) 2025 Feb;5(1):20230078.
    doi: 10.1002/EXP.20230078pubmed: 40040827google scholar: lookup
  11. Mao Y, Wang Y, Liu S, Liu Z, Yao P, Sun B, Chen C. Decellularized tendon patch enhance biological and mechanical healing of large-to-massive rotator cuff tear in a rat chronic model: a comparison study of patch sterilization and storage methods. J Orthop Surg Res 2025 Mar 1;20(1):218.
    doi: 10.1186/s13018-025-05596-4pubmed: 40022094google scholar: lookup
  12. Zheng Z, Zhou H, Zhang W, Wang T, Swamiappan S, Peng X, Zhou Y. Effects of advanced glycation end products on stem cell. Front Cell Dev Biol 2024;12:1532614.
    doi: 10.3389/fcell.2024.1532614pubmed: 39777263google scholar: lookup
  13. Sueters J, de Boer L, Groenman F, Huirne JAF, Smit TH, Zaat SAJ. A sterilization method for human decellularized vaginal matrices. Sci Rep 2024 Dec 30;14(1):31728.
    doi: 10.1038/s41598-024-82409-4pubmed: 39738284google scholar: lookup
  14. Dehghani S, Aghaee Z, Soleymani S, Tafazoli M, Ghabool Y, Tavassoli A. An overview of the production of tissue extracellular matrix and decellularization process. Cell Tissue Bank 2024 Mar;25(1):369-387.
    doi: 10.1007/s10561-023-10112-1pubmed: 37812368google scholar: lookup
  15. Govindaraju DT, Chen CH, Shalumon KT, Kao HH, Chen JP. Bioactive Nanostructured Scaffold-Based Approach for Tendon and Ligament Tissue Engineering. Nanomaterials (Basel) 2023 Jun 12;13(12).
    doi: 10.3390/nano13121847pubmed: 37368277google scholar: lookup
  16. Pearson JJ, Temenoff JS. Growth Factor Immobilization Strategies for Musculoskeletal Disorders. Curr Osteoporos Rep 2022 Feb;20(1):13-25.
    doi: 10.1007/s11914-022-00718-xpubmed: 35118607google scholar: lookup
  17. Zhang X, Chen X, Hong H, Hu R, Liu J, Liu C. Decellularized extracellular matrix scaffolds: Recent trends and emerging strategies in tissue engineering. Bioact Mater 2022 Apr;10:15-31.
  18. Rinoldi C, Kijeńska-Gawrońska E, Khademhosseini A, Tamayol A, Swieszkowski W. Fibrous Systems as Potential Solutions for Tendon and Ligament Repair, Healing, and Regeneration. Adv Healthc Mater 2021 Apr;10(7):e2001305.
    doi: 10.1002/adhm.202001305pubmed: 33576158google scholar: lookup