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Tendon/Ligament Reconstruction by Tissue Engineering

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Materials Science".

Deadline for manuscript submissions: closed (31 August 2020) | Viewed by 39572

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Prof. Dr. Gundula Schulze-Tanzil

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Institute of Anatomy and Cell Biology, Paracelsus Medical University, Nuremberg and Salzburg, 90419 Nuremberg, Germany
Interests: ligament/tendon; cartilage; tissue engineering and reconstruction
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Special Issue Information

Dear Colleagues,

This Special Issue “Tendon/Ligament Reconstruction by Tissue Engineering” will cover a selection of recent research topics and current review articles related to novel approaches in tendon/ligament tissue engineering. Up-to-date review articles, commentaries and experimental manuscripts are all welcome.

This Special Issue “Tendon/Ligament Reconstruction by Tissue Engineering” should present insights into novel approaches for tendon and ligament reconstruction based on tissue engineering or cell-free strategies using natural or synthetic biomaterials. As natural biomaterials for tendon/ligament reconstruction collagen-based scaffolds, decellularized tendons/ligaments or other dense connective tissue-derived extracellular matrices are of high interest. Valuable three-dimensional in vitro models including the application of bioreactors and versatile mechano-stimulatory devices which are known to promote in vitro teno-/ligamentogenesis should be presented for initial testing of implants but also preclinical in vivo implantation models are welcome which allow monitoring of the complex healing process. In addition to reconstruction of the midsubstance of tendons/ligaments, the neoformation of an enthesis-like interface between tendon/ligament and bone is an important prerequisite for stable reconstruction, hence, this unique transition tissue could also be addressed. A particular challenge presents the reconstruction of the anterior cruciate ligament (ACL) as an intraarticular ligament prone to the inflammatory milieu of the injured joint. For this reason, the influence of inflammation on the healing response could be analyzed in more detail.

Prof. Dr. Gundula Gesine Schulze-Tanzil
Guest Editor

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Keywords

tendon tissue engineering
tendon reconstruction
tendon/ligament healing
ligamentogenesis
decellularized tendon
mechanostimulation
anterior cruciate ligament
inflammation
enthesis

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Published Papers (10 papers)

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Research

23 pages, 29944 KiB

Open AccessArticle

3D Bioprinting of Human Adipose-Derived Stem Cells and Their Tenogenic Differentiation in Clinical-Grade Medium

by Deborah Stanco, Monica Boffito, Alessia Bogni, Luca Puricelli, Josefa Barrero, Gianni Soldati and Gianluca Ciardelli

Int. J. Mol. Sci. 2020, 21(22), 8694; https://doi.org/10.3390/ijms21228694 - 18 Nov 2020

Cited by 23 | Viewed by 3780

Abstract

Defining the best combination of cells and biomaterials is a key challenge for the development of tendon tissue engineering (TE) strategies. Adipose-derived stem cells (ASCs) are ideal candidates for this purpose. In addition, controlled cell-based products adherent to good manufacturing practice (GMP) are required for their clinical scale-up. With this aim, in this study, ASC 3D bioprinting and GMP-compliant tenogenic differentiation were investigated. In detail, primary human ASCs were embedded within a nanofibrillar-cellulose/alginate bioink and 3D-bioprinted into multi-layered square-grid matrices. Bioink viscoelastic properties and scaffold ultrastructural morphology were analyzed by rheology and scanning electron microscopy (SEM). The optimal cell concentration for printing among 3, 6 and 9 × 10⁶ ASC/mL was evaluated in terms of cell viability. ASC morphology was characterized by SEM and F-actin immunostaining. Tenogenic differentiation ability was then evaluated in terms of cell viability, morphology and expression of scleraxis and collagen type III by biochemical induction using BMP-12, TGF-β3, CTGF and ascorbic acid supplementation (TENO). Pro-inflammatory cytokine release was also assessed. Bioprinted ASCs showed high viability and survival and exhibited a tenocyte-like phenotype after biochemical induction, with no inflammatory response to the bioink. In conclusion, we report a first proof of concept for the clinical scale-up of ASC 3D bioprinting for tendon TE. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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19 pages, 3296 KiB

Open AccessArticle

Impact of Uniaxial Stretching on Both Gliding and Traction Areas of Tendon Explants in a Novel Bioreactor

by Mersedeh Tohidnezhad, Johanna Zander, Alexander Slowik, Yusuke Kubo, Gözde Dursun, Wolfgang Willenberg, Adib Zendedel, Nisreen Kweider, Marcus Stoffel and Thomas Pufe

Int. J. Mol. Sci. 2020, 21(8), 2925; https://doi.org/10.3390/ijms21082925 - 22 Apr 2020

Cited by 11 | Viewed by 3430

Abstract

The effects of mechanical stress on cells and their extracellular matrix, especially in gliding sections of tendon, are still poorly understood. This study sought to compare the effects of uniaxial stretching on both gliding and traction areas in the same tendon. Flexor digitorum longus muscle tendons explanted from rats were subjected to stretching in a bioreactor for 6, 24, or 48 h, respectively, at 1 Hz and an amplitude of 2.5%. After stimulation, marker expression was quantified by histological and immunohistochemical staining in both gliding and traction areas. We observed a heightened intensity of scleraxis after 6 and 24 h of stimulation in both tendon types, though it had declined again 48 h after stimulation. We observed induced matrix metalloproteinase-1 and -13 protein expression in both tendon types. The bioreactor produced an increase in the mechanical structural strength of the tendon during the first half of the loading time and a decrease during the latter half. Uniaxial stretching of flexor tendon in our set-up can serve as an overloading model. A combination of mechanical and histological data allows us to improve the conditions for cultivating tendon tissues. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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20 pages, 4585 KiB

Open AccessArticle

Effects of SCCO₂, Gamma Irradiation, and Sodium Dodecyl Sulfate Treatments on the Initial Properties of Tendon Allografts

by Yikan Sun, Vedran Lovric, Tian Wang, Rema A. Oliver and William R. Walsh

Int. J. Mol. Sci. 2020, 21(5), 1565; https://doi.org/10.3390/ijms21051565 - 25 Feb 2020

Cited by 17 | Viewed by 4921

Abstract

Sterile and decellularized allograft tendons are viable biomaterials used in reconstructive surgeries for dense connective tissue injuries. Established allograft processing techniques including gamma irradiation and sodium dodecyl sulfate (SDS) can affect tissue integrity. Supercritical carbon dioxide (SCCO₂) represents a novel alternative that has the potential to decellularize and sterilize tendons with minimized exposure to denaturants, shortened treatment time, lack of toxic residues, and superior tissue penetration, and thus efficacy. This study attempted to develop a single-step hybrid decellularization and sterilization protocol for tendons that involved SCCO₂ treatment with various chemical additives. The processed tendons were evaluated with mechanical testing, histology, scanning electron microscopy (SEM), and Fourier-transform infrared (FTIR) spectroscopy. Uniaxial mechanical testing showed that tendons treated with SCCO₂ and additive NovaKill^TM Gen2 and 0.1% SDS had significantly higher (p < 0.05) ultimate tensile stress (UTS) and Young’s modulus compared to gamma-irradiated and standard-SDS-treated tendons. This was corroborated by the ultrastructural intactness of SCCO₂-treated tendons as examined by SEM and FTIR spectroscopy, which was not preserved in gamma-irradiated and standard SDS-treated tendons. However, complete decellularization was not achieved by the experimented SCCO₂-SDS protocols used in this study. The present study therefore serves as a concrete starting point for development of an SCCO₂-based combined sterilization and decellularization protocol for allograft tendons, where additive choice is to be optimized. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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22 pages, 4437 KiB

Open AccessArticle

Enhanced Growth of Lapine Anterior Cruciate Ligament-Derived Fibroblasts on Scaffolds Embroidered from Poly(l-lactide-co-ε-caprolactone) and Polylactic Acid Threads Functionalized by Fluorination and Hexamethylene Diisocyanate Cross-Linked Collagen Foams

by Clemens Gögele, Judith Hahn, Cindy Elschner, Annette Breier, Michaela Schröpfer, Ina Prade, Michael Meyer and Gundula Schulze-Tanzil

Int. J. Mol. Sci. 2020, 21(3), 1132; https://doi.org/10.3390/ijms21031132 - 8 Feb 2020

Cited by 21 | Viewed by 3945

Abstract

Reconstruction of ruptured anterior cruciate ligaments (ACLs) is limited by the availability and donor site morbidity of autografts. Hence, a tissue engineered graft could present an alternative in the future. This study was undertaken to determine the performance of lapine (L) ACL-derived fibroblasts on embroidered poly(l-lactide-co-ε-caprolactone) (P(LA-CL)) and polylactic acid (PLA) scaffolds in regard to a tissue engineering approach for ACL reconstruction. Surface modifications of P(LA-CL)/PLA by gas-phase fluorination and cross-linking of a collagen foam using either ethylcarbodiimide (EDC) or hexamethylene diisocyanate (HMDI) were tested regarding their influence on cell adhesion, growth and gene expression. The experiments were performed using embroidered P(LA-CL)/PLA scaffolds that were seeded dynamically or statically with LACL-derived fibroblasts. Scaffold cytocompatibility, cell survival, numbers, metabolic activity, ultrastructure and sulfated glycosaminoglycan (sGAG) synthesis were evaluated. Quantitative real-time polymerase chain reaction (QPCR) revealed gene expression of collagen type I (COL1A1), decorin (DCN), tenascin C (TNC), Mohawk (MKX) and tenomodulin (TNMD). All tested scaffolds were highly cytocompatible. A significantly higher cellularity and larger scaffold surface areas colonized by cells were detected in HMDI cross-linked and fluorinated scaffolds compared to those cross-linked with EDC or without any functionalization. By contrast, sGAG synthesis was higher in controls. Despite the fact that the significance level was not reached, gene expressions of ligament extracellular matrix components and differentiation markers were generally higher in fluorinated scaffolds with cross-linked collagen foams. LACL-derived fibroblasts maintained their differentiated phenotype on fluorinated scaffolds supplemented with a HMDI cross-linked collagen foam, making them a promising tool for ACL tissue engineering. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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14 pages, 3478 KiB

Open AccessArticle

Different Frequency of Cyclic Tensile Strain Relates to Anabolic/Catabolic Conditions Consistent with Immunohistochemical Staining Intensity in Tenocytes

by Yusuke Kubo, Bernd Hoffmann, Katja Goltz, Uwe Schnakenberg, Holger Jahr, Rudolf Merkel, Gundula Schulze-Tanzil, Thomas Pufe and Mersedeh Tohidnezhad

Int. J. Mol. Sci. 2020, 21(3), 1082; https://doi.org/10.3390/ijms21031082 - 6 Feb 2020

Cited by 22 | Viewed by 3363

Abstract

Tenocytes are mechanosensitive cells intimately adapting their expression profile and hence, their phenotype to their respective mechanomilieu. The immunolocalization and expression intensity of tenogenic, anabolic and catabolic markers in tenocytes in response to in vitro mechanical loading have not been monitored by immunohistochemical staining (IHC). Thus, we investigated the association between IHC intensities, different stimulation frequencies, and tenogenic metabolism using a versatile mechanical stretcher. Primary tenocytes obtained from murine Achilles tendons were transferred to poly(dimethylsiloxane) (PDMS) elastomeric chamber. Chambers were cyclically stretched by 5% in uniaxial direction at a variation of tensile frequency (1 or 2 Hz) for 3 h. After stretching, cell physiology, IHC intensities of tendon-related markers, and protein level of the angiogenesis marker vascular endothelial growth factor (VEGF) were evaluated. Cell proliferation in tenocytes stimulated with 1 Hz stretch was significantly higher than with 2 Hz or without stretch, while 2 Hz stretch induced significantly reduced cell viability and proliferation with microscopically detectable apoptotic cell changes. The amount of scleraxis translocated into the nuclei and tenomodulin immunoreactivity of tenocytes treated with stretch were significantly higher than of non-stretched cells. The collagen type-1 expression level in tenocytes stretched at 1 Hz was significantly higher than in those cultivated with 2 Hz or without stretching, whereas the matrix metalloproteinase (MMP)-1 and MMP-13 immunoreactivities of cells stretched at 2 Hz were significantly higher than in those stimulated with 1 Hz or without stretching. The secreted VEGF-protein level of tenocytes stretched at 2 Hz was significantly higher than without stretching. Our IHC findings consistent with cell physiology suggest that appropriate stretching can reproduce in vitro short-term tenogenic anabolic/catabolic conditions and allow us to identify an anabolic stretching profile. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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16 pages, 13648 KiB

Open AccessArticle

TGF–β3 Loaded Electrospun Polycaprolacton Fibre Scaffolds for Rotator Cuff Tear Repair: An in Vivo Study in Rats

by Janin Reifenrath, Mathias Wellmann, Merle Kempfert, Nina Angrisani, Bastian Welke, Sarah Gniesmer, Andreas Kampmann, Henning Menzel and Elmar Willbold

Int. J. Mol. Sci. 2020, 21(3), 1046; https://doi.org/10.3390/ijms21031046 - 5 Feb 2020

Cited by 28 | Viewed by 4447

Abstract

Biological factors such as TGF–β3 are possible supporters of the healing process in chronic rotator cuff tears. In the present study, electrospun chitosan coated polycaprolacton (CS–g–PCL) fibre scaffolds were loaded with TGF–β3 and their effect on tendon healing was compared biomechanically and histologically to unloaded fibre scaffolds in a chronic tendon defect rat model. The biomechanical analysis revealed that tendon–bone constructs with unloaded scaffolds had significantly lower values for maximum force compared to native tendons. Tendon-bone constructs with TGF–β3-loaded fibre scaffolds showed only slightly lower values. In histological evaluation minor differences could be observed. Both groups showed advanced fibre scaffold degradation driven partly by foreign body giant cell accumulation and high cellular numbers in the reconstructed area. Normal levels of neutrophils indicate that present mast cells mediated rather phagocytosis than inflammation. Fibrosis as sign of foreign body encapsulation and scar formation was only minorly present. In conclusion, TGF–β3-loading of electrospun PCL fibre scaffolds resulted in more robust constructs without causing significant advantages on a cellular level. A deeper investigation with special focus on macrophages and foreign body giant cells interactions is one of the major foci in further investigations. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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19 pages, 7759 KiB

Open AccessArticle

SV40 Transfected Human Anterior Cruciate Ligament Derived Ligamentocytes—Suitable as a Human in Vitro Model for Ligament Reconstruction?

by Gundula Schulze-Tanzil, Philipp Arnold, Clemens Gögele, Judith Hahn, Annette Breier, Michael Meyer, Benjamin Kohl, Michaela Schröpfer and Silke Schwarz

Int. J. Mol. Sci. 2020, 21(2), 593; https://doi.org/10.3390/ijms21020593 - 16 Jan 2020

Cited by 9 | Viewed by 3682

Abstract

Cultured human primary cells have a limited lifespan undergoing dedifferentiation or senescence. Anterior cruciate ligaments (ACL) are hypocellular but tissue engineering (TE) requires high cell numbers. Simian virus (SV) 40 tumor (T) antigen expression could extend the lifespan of cells. This study aimed to identify cellular changes induced by SV40 expression in human ACL ligamentocytes by comparing them with non-transfected ligamentocytes and tissue of the same donor to assess their applicability as TE model. Human ACL ligamentocytes (40-year-old female donor after ACL rupture) were either transfected with a SV40 plasmid or remained non-transfected (control) before monitored for SV40 expression, survival, and DNA content. Protein expression of cultured ligamentocytes was compared with the donor tissue. Ligamentocyte spheroids were seeded on scaffolds embroidered either from polylactic acid (PLA) threads solely or combined PLA and poly (L-lactide-co-ε-caprolactone) (P(LA-CL)) threads. These scaffolds were further functionalized with fluorination and fibrillated collagen foam. Cell distribution and survival were monitored for up to five weeks. The transfected cells expressed the SV40 antigen throughout the entire observation time, but often exhibited random and incomplete cell divisions with significantly more dying cells, significantly more DNA and more numerous nucleoli than controls. The expression profile of non-transfected and SV40-positive ligamentocytes was similar. In contrast to controls, SV40-positive cells formed larger spheroids, produced less vimentin and focal adhesions and died on the scaffolds after 21 d. Functionalized scaffolds supported human ligamentocyte growth. SV40 antigen expressing ligamentocytes share many properties with their non-transfected counterparts suggesting them as a model, however, applicability for TE is limited. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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20 pages, 3622 KiB

Open AccessArticle

Supporting Cell-Based Tendon Therapy: Effect of PDGF-BB and Ascorbic Acid on Rabbit Achilles Tenocytes In Vitro

by Olivera Evrova, Damian Kellenberger, Maurizio Calcagni, Viola Vogel and Johanna Buschmann

Int. J. Mol. Sci. 2020, 21(2), 458; https://doi.org/10.3390/ijms21020458 - 10 Jan 2020

Cited by 25 | Viewed by 3720

Abstract

Cell-based tendon therapies with tenocytes as a cell source need effective tenocyte in vitro expansion before application for tendinopathies and tendon injuries. Supplementation of tenocyte culture with biomolecules that can boost proliferation and matrix synthesis is one viable option for supporting cell expansion. In this in vitro study, the impacts of ascorbic acid or PDGF-BB supplementation on rabbit Achilles tenocyte culture were studied. Namely, cell proliferation, changes in gene expression of several ECM and tendon markers (collagen I, collagen III, fibronectin, aggrecan, biglycan, decorin, ki67, tenascin-C, tenomodulin, Mohawk, α-SMA, MMP-2, MMP-9, TIMP1, and TIMP2) and ECM deposition (collagen I and fibronectin) were assessed. Ascorbic acid and PDGF-BB enhanced tenocyte proliferation, while ascorbic acid significantly accelerated the deposition of collagen I. Both biomolecules led to different changes in the gene expression profile of the cultured tenocytes, where upregulation of collagen I, Mohawk, decorin, MMP-2, and TIMP-2 was observed with ascorbic acid, while these markers were downregulated by PDGF-BB supplementation. Vice versa, there was an upregulation of fibronectin, biglycan and tenascin-C by PDGF-BB supplementation, while ascorbic acid led to a downregulation of these markers. However, both biomolecules are promising candidates for improving and accelerating the in vitro expansion of tenocytes, which is vital for various tendon tissue engineering approaches or cell-based tendon therapy. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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16 pages, 1940 KiB

Open AccessArticle

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

by Susanne Pauline Roth, Walter Brehm, Claudia Groß, Patrick Scheibe, Susanna Schubert and Janina Burk

Int. J. Mol. Sci. 2019, 20(21), 5474; https://doi.org/10.3390/ijms20215474 - 3 Nov 2019

Cited by 21 | Viewed by 3319

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 (p < 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 (p < 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. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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18 pages, 6915 KiB

Open AccessArticle

Viscoelastic Behavior of Embroidered Scaffolds for ACL Tissue Engineering Made of PLA and P(LA-CL) After In Vitro Degradation

by Judith Hahn, Gundula Schulze-Tanzil, Michaela Schröpfer, Michael Meyer, Clemens Gögele, Mariann Hoyer, Axel Spickenheuer, Gert Heinrich and Annette Breier

Int. J. Mol. Sci. 2019, 20(18), 4655; https://doi.org/10.3390/ijms20184655 - 19 Sep 2019

Cited by 20 | Viewed by 4123

Abstract

A rupture of the anterior cruciate ligament (ACL) is the most common knee ligament injury. Current applied reconstruction methods have limitations in terms of graft availability and mechanical properties. A new approach could be the use of a tissue engineering construct that temporarily reflects the mechanical properties of native ligament tissues and acts as a carrier structure for cell seeding. In this study, embroidered scaffolds composed of polylactic acid (PLA) and poly(lactic-co-ε-caprolactone) (P(LA-CL)) threads were tested mechanically for their viscoelastic behavior under in vitro degradation. The relaxation behavior of both scaffold types (moco: mono-component scaffold made of PLA threads, bico: bi-component scaffold made of PLA and P(LA-CL) threads) was comparable to native lapine ACL. Most of the lapine ACL cells survived 32 days of cell culture and grew along the fibers. Cell vitality was comparable for moco and bico scaffolds. Lapine ACL cells were able to adhere to the polymer surfaces and spread along the threads throughout the scaffold. The mechanical behavior of degrading matrices with and without cells showed no significant differences. These results demonstrate the potential of embroidered scaffolds as an ACL tissue engineering approach. Full article

(This article belongs to the Special Issue Tendon/Ligament Reconstruction by Tissue Engineering)

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