[Frontiers in Bioscience S1, 23-32, June 1, 2009]
Tendon tissue engineering with mesenchymal stem cells and biografts: an option for large tendon defects?
Xiao Chen1,4, Xiao Hui Zou 3, Guo Li Yin 1,4, Hong Wei Ouyang 1, 2,4
1
TABLE OF CONTENTS
1. ABSTRACT
The most important factors in the tissue engineering approach to tissue repair and regeneration are the use of appropriate cells and scaffolds. Mesenchymal stem cells (MSCs) are one of the most promising seed cells, which can be easily derived and have the potential to differentiate into various mesenchymal cell types as well as tenocytes in vitro and in vivo. Biological tendon grafts are the most common choice in current clinical practice, as they possess physical structure, strength and biocompatibility. We review the latest research findings on MSC-based tendon tissue engineering and recent advances in biological graft research.
2. INTRODUCTION
It is difficult for tendon to regenerate after injury. This limited capability of tendons to regenerate poses a challenge to tendon tissue engineering, and emphasizes the importance of developing a procedure to do so.
So far, fewer studies have been performed on tendon tissue engineering when compared to the extensive work on bone and cartilage tissue engineering. Moreover, tendon tissue engineering research has not yet undergone translation from the bench to the bedside. The continued development of tendon tissue engineering will depend on the identification and characterization of appropriate sources of cells as well as the development of practical scaffolds. The identification of an optimal cell source for a particular tissue engineering application will depend on rigorous characterization with regards to plasticity, propagation, and control of differentiation. To guide the organization, growth, and differentiation of cells in tissue engineered constructs, appropriate scaffolds are needed to provide mechanical support and physical, chemical, and mechanical cues in forming functional tissues. Based on the above criteria and the current state of the art, mesenchymal stem cells (MSCs) seem to be the optimal seed cells, and decellularized tendon grafts the most practical scaffolds at present.
3. MSC AS SEED CELLS FOR TENDON REPAIR
Multiple cell types have been seeded within different scaffolds for tendon tissue engineering. As tenocytes are the predominant cell type in tissues, they have been a frequent cell source for active repair (1-17). However, tenocytes are fully differentiated cells with limited lifespan. Moreover, the limitation of donor tissue and morbidity in the donor site prohibit the clinical application of autologous tenocytes (6).
With the rapid development of stem cell biology and technology, clinicians and researchers used stem cells for tendon repair and regeneration. Compared to embryonic stem cells (ESCs), adult stem cells, especially MSCs, have been much more extensively investigated for tissue engineering. MSCs were efficiently expanded and differentiated into cells of a variety of specialized mesenchymal tissues including bone, cartilage, fat, muscle, tendon/ligament and marrow stroma following appropriate stimulation (18-20). They exhibited the potential for a wide range of therapeutic applications through autologous and allogeneic stem cell transplantation (18-20). Moreover, MSCs have been easily harvested and cultured from various types of connective tissue, such as bone marrow (20), periosteum (21), synovium (22), muscle (23), adipose tissue (24), umbilical cord (25), articular cartilage (26), tendon (27, 28) and periodontal ligament (29), amongst others.
Among those sources of MSCs, bone marrow derived MSCs seem to be most appropriate as seed cells for tendon repair. Participatation of MSCs was demonstrated in the long-term remodeling of degradable small intestine submucosa-extracellular matrix scaffold when used as a repair device in the murine model of Achilles tendon repair (30). Furthermore, circulation-derived MSCs where shown to contribute to the rat tendon healing (31). These studies suggest that MSCs from bone marrow source may participate in the natural process of tendon repair. Moreover, bone marrow derived MSCs produced more extracellular matrix with much faster cell proliferation than either anterior cruciate ligament (ACL) cells or dermal fibroblasts. (32)
On the other hand, human bone marrow derived MSCs express low class I human leukocyte antigen (HLA) and do not express class II HLA, which may limit immune recognition (18). In addition to the absence of antigen, MSCs have been shown to exert in vitro immunosuppressive activities on activated T cells (33) and inhibition of most B-cell effector functions (34). Also, MSCs were able to secret a variety of cytokines and growth factors with both paracrine and autocrine activities, which could suppress the local immune system, inhibit fibrosis (scar formation) and apoptosis, enhance angiogenesis, and stimulate mitosis and differentiation of tissue-intrinsic reparative procedure (35).
Not only MSCs, but also progenitor cells differentiated from MSC retained their immunoprivilege and immunomodulatory properties in vitro, although the later was lost following transplantation (36). To investigate viability and function, allogeneic bone marrow derived MSCs were implanted into the patellar tendon defect of rabbits. The labeled allogeneic MSCs were viable up to eight weeks after implantation, and differentiated into tenocyte-like spindle shape cells. Allogeneic MSCs may therefore be used as "off -the -shelf" seed cells for tendon repair and tissue engineering.
4. MSC BASED TENDON TISSUE ENGINEERING
Many recent studies used bone marrow derived MSCs (2, 37-60) as candidate seed cells for tendon tissue engineering. Most of them compared MSC seeded scaffolds with scaffolds alone (37-60). Table 1 presents a synopsis of the current tendon tissue engineering experiments with cells in vivo (Table 1). Researchers have applied undifferentiated autologous bone marrow derived MSC to collagen gels (50, 51, 53, 57) and collagen sponges (58, 59) for both patellar tendon (51, 53-59, 61-64) and Achilles tendon repair (50, 52, 57).
MSC with collagen matrix were able to improve the quality of tendon repair: Several studies showed that autologous MSCs have potential for tendon repair (50, 51, 54). Tissues treated with MSC-collagen gel exhibited faster repair rate and were significantly stronger and stiffer than natural healing tissues. Their maximum force and stiffness were, respectively, 174% and 183% greater than those of natural repairs at 26 weeks (54). Although the grafted repairs were still only 17-25% and 10-19% of normal maximum force and stiffness respectively (54), they were higher than the in vivo living peak forces (63, 65, 66) of the tendons measured, suggesting that the MSC repaired tendon were able to fulfill their physical function. Following those experiments, the researchers modified the cell deliver matrix. With the use of collagen-gel-sponge to deliver MSC, the average maximum force and maximum stress of the tendon repairs achieved 50 and 85% of the normal values for the Achilles tendon (57), and 60% and 50% for the patellar tendon (58). Although the failure forces were above the in vivo force, the large additional repair displacement (56-60) and moderate crimp pattern compared to the normal tendon (54, 58) indicated that the repair tendon is still inferior to the normal tendon.
The relationship between cell density and the quality of tendon repair was investigated: Gel contraction was measured to at about 30% of original diameter when seeded with MSCs, producing elongated cells that aligned along the suture axis (50). Increasing the seeding density (below a threshold value 0.5 million cells/mL (60)) accelerated the rate of collagen gel contraction, improved the alignment and appearance of the cell nuclei up to 72 hours in culture (53). Varying cell-seeding density (1, 4, and 8 million cells/mL) (54) and the lower cell-to-collagen ratio (0.1 million and 1 million cell/mL) at two collagen concentrations (1.3 and 2.6 mg/mL)) (56, 58) did not affect the biomechanical properties of the repair tissues.
MSCs might induce ectopic bone formation at tendon repair site: Ectopic bones were found in 28% of MSC-treated rabbit tendons (54, 62). Lowering cell-to-collagen ratios may have reduced, but did not eliminate ectopic ossification (56, 60, 62). This finding warrants further investigation on selecting the optimal subpopulation of MSCs for tendon repair.
The age of MSCs might relate to the quality of tendon repair: An age-related trend of decline in the strength of tendon repair can be as great as 50%, although this study did not achieve statistical significance (61), likely due to the small sample size (n=5). These results implicated that the age of MSCs and tendon might affect the quality of tendon repair. Further studies with larger samples are needed. Authors have performed tendon/ligament repair studies on the use of allogeneic MSCs (40-49) and various kinds of scaffolds, including biodegradable polymers such as PLGA/PLLA scaffold (42, 48, 67, 68), collagen-coated polymer scaffolds (69), silk-based scaffolds (69) and fibrin (40).
Allogeneic MSCs were able to survive at tendon repair: We examined the fate of allogeneic MSCs delivered by fibrin gel and implanted into patellar tendon defects. The implanted MSCs remained viable at least 8 weeks after surgery. Moreover, the morphology of MSCs changed from round shape to tenocyte-like spindle shape at 5 and 8 weeks after implantation (44). These results illustrated that allogeneic MSCs were able to survive at the tendon wound site after local delivery.
Allogeneic MSCs accelerated and improved tendon repair: Animal studies of tendon defect repair showed that at as early as 4 weeks post-implantation the regenerated tissue comprised bundles of collagen fibers with an apparently mature crimp pattern. The tensile stiffness of allogeneic MSC-knitted PLGA scaffolds treated group reached 87% of normal value, 30% higher than that of natural healing group. As tendon is a structure that transmits force from muscle to bone, the near normal stiffness of MSC treated tendon repair could ensure the restoration of the physical function of the regenerated tendon (46, 48). Also, in the study of primary tendon repair without defect (40), the intratendinous cell therapy with bone marrow-derived mesenchymal stem cells could improve several histological and biomechanical variables in the early stages of tendon-healing.
Knitted scaffold possessed internal connective space and allowed the formation of functional connective collagen fibrous tissues inside the scaffold: PLGA has greater internal connective space as compared to a braided structure, especially when it is under tension. The internal connective space allows enough cells to be seeded initially, and allows bundles of connective tissue to form during the repair process. This was clearly observed from the histology of knitted PLGA scaffold treated tendon repair. Large amounts of cell in-growth and matrix regeneration were observed in the scaffold as early as two weeks post operation. At 4 weeks after implantation, bundles of collagen fibers with proper orientation and crimp pattern were formed. The potential of knitted structure for tendon tissue ingrowths was well illustrated by those findings (46, 48).
MSCs could restore the fibrocartilage zone at tendon-to-bone insertion: The flexor hallucis longus tendon was transferred through a 2.5 mm diameter tunnel in the calcaneum. The tendon-to-bone insertion was treated with or without MSCs. In the MSCs treated group, the application of a large number of MSCs had the potential to accelerate tissue remodeling, with more perpendicular collagen fibers at the insertion, and promote fibro-cartilage-like tissue formation, confirmed by collagen type II immunostaining. These findings illustrate the added value of MSCs as compared to other cell sources for tendon regeneration (45).
MSCs cell sheet technology could improve the efficiency of cell seeding onto scaffolds with bigger pores or less pores: Porous scaffolds usually have the drawback of poor cell-seeding efficiency, and require a vehicle for cell-delivery. Our in vitro study fabricated three-dimensional cell sheets (41, 42) before attaching them to scaffolds. With MSCs sheet techniques, cells were connected by their synthesized matrixes, which avoided the issue of failure of attachment of cells on scaffolds. Fibroblasts and bone marrow cells (41, 42) have been grown into three -dimensional cell sheets, and the combination of cell sheet/PLLA scaffold constructs had transformed into tissue like ligament analogs which consist primarily of collagen type I and small amount of collagen type III and tenascin (42).
Current tendon tissue engineering research proved the efficiency of autologous and allogenic MSCs for tendon repair. However, the scaffolds used are still not practical which impeded the translation of tendon tissue engineering research from the laboratory benches to patients. The collagen gel/sponge is weak, whereas synthetic polymers have several inherent disadvantages, such as acidic degradation products and inferior biocompatibility. Thus, current scaffolds for MSC delivery have not yet fulfilled the requirements of human application. Allogeneic tendon grafts are still the common choice in current clinical practices.
5. ACELLULAR GRAFTS FOR TENDON REPAIR
5.1. Grafts accepted in current clinical practice
Non-degradable synthetic materials used for ligament and tendon repair include carbon fibers, polyethylene terephthalate (Leeds-Keio ligament), polypropylene (Kennedy Ligament Augmentation Device), and polytetrafuoroethylene (Gore-Tex) (70-73). Although these synthetic grafts exhibit excellent short-term results, the long-term clinical outcome is poor, with a failure rate of 40% to 78% from fragmentation, stress shielding of new tissue, fatigue, creep, and wear debris, which can eventually lead to arthritis and synovitis (71, 73, 74, 75). The permanent polymeric prosthesis developed in the 1970s have not gained wide acceptance. Hence, biological grafts are still the main material used in daily clinical practice to repair tendon defects (50, 76, 77).
Biological substitutes include autograft, allograft, and xenograft (71, 76, 78-82). Autologous grafts of patellar tendon and hamstring tendons are considered the "gold standard" in tissue repair (71) and usually preferred to avoid rejection. Both autografts and allografts possess good initial mechanical strength, and promote cell proliferation and new tissue growth, although fresh autologous grafts may be superior to allogeneic grafts in tissue repair and remodeling (41). However, they suffer from a number of disadvantages. For example, autografts inherently require additional surgery which may cause donor site morbidity, increased recovery time, and possible pain at the harvesting site, such as harvest site infection, nerve injury, and patellar fracture.
Allografts include tendon graft, dermal graft and other connect tissue grafts (79). Xenografts are harvested from animal tendons, small intestine submucosa (30, 83), dermis and skin, and pericardium (84). Allografts and xenografts are primarily composed of type I collagen with similar structure and mechanical properties of human tendons. However, allo- and xeno-grafts could potentially transmit disease or infection, and may elicit an unfavorable immunogenic response from the host (70, 71, 85, 86). Therefore, graft processing is most important for safe clinical application of allo- and xeno-grafting (79).
5.2. Current research on the decelullar technology and immunogenicity of biografts
To decrease the bio-burden and the risk of inflammatory or foreign body reactions, all biografts, regardless of their origin, have to be extensively purified to remove proteins, cells, and lipids. The major source of antigenicity in musculoskeletal transplants is the surface histocompatibility complex markers on donor (graft) cells. Removing these intrinsic cells or damaging the histocompatibility markers results in a significant reduction in antigenicity in vivo. Common processing techniques such as fresh-freezing or freeze-drying of allografts may also decrease graft antigenicity, but do not remove cells (86). Frozen allografts of tendons/ligaments frequently result in an immunological foreign-body response that hinders tissue remodeling (87). There is no widely used method for removing cells from tendon allografts while maintaining tissue structure, nativity, and mechanical properties (Table 2) (88-92). SDS, TBP and Triton-X treatments are effective at removing most midsubstance cells from tendon tissue while maintaining mechanical properties, crimp characteristics, and glycosaminoglycan content (86, 88).
In addition to cells, alpha-1,3-Gal epitopes can cause major immunogenicity and acute vascular rejection of pig-to-human xenotransplantation (84, 93, 94). To reduce the immunogenicity of xenografts, many studies had investigated to eliminate alpha-1,3-Gal epitopes, producing alpha-gal deficient pigs (94). Pretreatment with anti-Gal antibodies and complement can reduce the immunogenicity of porcine tissue, may be a valuable alternative or supplement to immunosuppression in xenotransplantation (95). Recently recombinant alpha-galactosidase was used to remove alpha-1,3-Gal epitopes successfully. The enzymatic treated porcine patellar tendon graft was appropriate for replacing ruptured human ACL (84). Within two years posttransplantation, the pig tissue was replaced by repopulating recipient's fibroblasts which secreted matrix in the process of ligamentization, although low-level inflammation persisted as long as there are pig xenoantigens in xenograft recipients (84).
Porcine small intestine submucosa extracellular matrix xenografts are currently used in clinical practice for tendon repair. They contain a number of growth factor and are rapidly absorbed, with approximately 40-60% of the ECM degenerated within the first 4 weeks, and complete absorption by 3 months after surgery (30, 96). However, xenograft SIS has no recognizable benefit in the repair of large rotator cuff defect (97). In 30 patients, porcine intestinal submucosa patches caused long term severe inflammatory reactions, and did not improve the rate of tendon-healing or clinical outcome scores (98).
Although frozen allografts are already accepted in clinical practice, absence of viable cells in cryopreserved allografts compromises the clinical outcome of tissue repair and regeneration. With the recent development of tissue engineering and stem cell research, decellularized allografts and xenograft serve as high-strength delivery vehicles for a variety of cell types, including differentiated or pluripotential MSCs.
6. MSCS REVITALIZED DECELLULAR GRAFTS
6.1. Current researches on the repopulation of tendon grafts
To be clinically useful, cell-extracted allo- or xeno-grafts of tendons must be recellularized, possibly seeding cells in vitro and ingrowing host cells in vivo prior to implantation. Current cell-seeding techniques include: 1) delivering cell-gel composites into the scaffold and 2) delivering cell suspension into scaffolds in a static or dynamic situation. However, there are some disadvantages in the above current techniques, such as the low efficiency of cell attachment to dense fibrous matrix or scaffolds and the weak mechanical strength of gel systems. These disadvantages make it very difficult to seed a large number of cells on dense tissue grafts. The limitations of current technology prohibited the use of stem cells to improve the efficiency of large tissue grafts for tissue repair.
So, partial thickness incisions (86) and ultrasonication (92) were developed to allow the seeded cells infiltrate the tendon in culture prior to implantation. Without incisions or ultrasonication, extrinsic cells which were seeded onto the tendon surface have difficulty infiltrating into the tendon. But, with incision and ultrasonication, the grafts decrease their mechanical strength, a priority in clinical applications. Hence, the tissue grafts have to be preserved intact, while cell delivery is limited by the difficulty of cell seeding.
6.2. MSCs cell sheet repopulated tendon allograft
Encouraged by the previous studies of MSC sheet, some authors (41) used MSC sheet to seed cells into cryopreserved Achilles tendon graft (Figure 1), and found that MSCs differentiated into spindle-like cells (Figure 2). MSCs proliferated fast, and formed coherent cellular sheets within 2 weeks after attaining confluence. After the cell sheets were formed, these could be detached from the culture substratum, thus yielding a sheet of living cells in a collagen matrix of endogenous origin. When cell sheets were formed, the preserved tendon grafts were put on the cell sheet and rolled up. With this technique, 2.0x107 MSCs were completely and successfully incorporated into the 2.5 cm Achilles tendon graft. This technique overcomes the inherent disadvantages of current tissue engineering techniques of cell seeding. By assembling MSC sheet with dense allogeneic grafts, the advantages of both the cell sheet technique and dense tissue grafts were better utilized. With the MSCs sheet technique, cells were connected by their synthesized matrixes which eased the assembly of cells within dense grafts. Large numbers of MSCs were efficiently seeded onto tendon grafts and MSCs were differentiated into tenocyte-like cells. This novel strategy engineers strong and living tissue grafts to repair large tendon defect, with the possibility of using decellularized grafts as scaffold to deliver large numbers of MSCs. This may revolutionize current technology of tendon tissue engineering and clinical tendon repair and reconstruction (41).
However, the time of MSC culture and MSC cell sheet formation, the immunogenicity of MSC sheets, and the survival of MSC sheets after implantation are still to be optimized (41).
7. FUTURE DIRECTIONS
Cell-based tissue engineering for tendon repair and regeneration hold great promise for future clinical application. Defining the cellular component and appropriate scaffold to generate the tissue engineering paradigm is a complex task. MSC populations may be well suited for this task. Allografts may be the most practical scaffolds to MSCs for tendon repair at present. However, many issues have yet to be investigated.
Future research should be directed toward better characterization of MSCs population, including identifying unique markers and mapping out lineage development. It is hard to fully regenerate tendon. This may due to two reasons. One is that the regeneration ability of tendon tissue is limited. Unlike bone, which can heal by regenerating normal bone in most cases, injured tendon often heals with scar tissue formation. The other is the lack of knowledge about the tissue specific differentiation factors for tendons, with similar function to BMP-2 for bone regeneration. Further studies need to be conducted. Perhaps it may be helpful to obtain some clues from the study of embryonic tendon development.
Allografts and xenograft for tendon reconstruction may be still used. The understanding of biological processes relating allograft and xenograft antigenicity, cellular ingrowth, and tendonization should be investigated to improve the efficacy of tendon grafts. Further studies need to improve the technology of cell extraction and repopulation to reduce the failure of tendon reconstruction with acellular grafts.
With the development of stem cell biology and graft processing technology, the synergic effect of using MSCs and allografts for tendon repair will likely favour the transition from bench top to clinical reality in the next several years.
8. ACKNOWLEDGMENT
This work was supported by National Natural Science Foundation of China (30600301, 30600670, U0672001) and Zhejiang Province grants (R206016, 2006C14024).
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Abbreviations: MSCs: mesenchymal stem cells, PLGA: poly(dl-lactide-co-glycolide), PLLA: poly-L-lactic acid, SDS: sodium dodecyl sulfate, TnBP: tri(n-butyl)phosphate, TritonX-100: t-octyl-phenoxypolyethoxyethanol, PT: Patellar tendon, ACL: anterior cruciate ligament, HLA: human leukocyte antigen, ECM: extracellular matrix, BMP: bone morphogenetic protein, ESCs: embryonic stem cells
Key Words: Tendon Defect, Mesenchymal Stem Cells, Allogeneic Graft, Tissue Engineering, Review
Send orrespondence to: Hong Wei Ouyang, Box 39 , Center for stem cell and tissue engineering, School of Medicine, Zhejiang University, 388 YuHangTang Road, Hangzhou, P.R.China, 310058, Tel: 86-571-88208262, Fax: 86-571-88208262, E-mail:hwoy@zju.edu.cn