Comparison of current biomimetic skeletal muscle models of
The aim of this book chapter is to highlight the fact that regenerative medicine and tissue engineering have important consequences for animal research and can be exploited to develop powerful animal sparing
2. Biomimetic models
Tissue engineering is an interdisciplinary field that applies the principles of biology and engineering to the development of functional substitutes for damaged tissue . The loss or failure of an organ or tissue is one of the most frequent, devastating, and costly problems in human health care. By applying the basic principles of engineering and cell biology tissue engineering is helping us to move toward the development of biological substitutes that restore, maintain, or improve tissue function or a whole organ . The new tissues can be used as test beds in basic research and development and have potential for future use in transplantation and reconstructive surgery .
Biomimetics is defined as the study of the structure and function of biological systems as models for the design and engineering of biomaterials. The term biomimetics was coined by Otto Schmitt in the 1950s for the transfer of ideas and analogues from biology to technology . It generally refers to human-made and engineered processes, substances, devices, or systems that imitate and therefore
Organ, tissue and cell culture have been used for decades as biomimetic models of cells, tissues and organs. The pioneering work of eminent scientists such as Sydney Ringer, Wilhelm Roux and Ross Harrison from 1880 to the early 1900s helped to establish the principles and methodology of tissue culture. Ringer developed salt solutions containing the chlorides of sodium, potassium, calcium and magnesium suitable for developing organ culture. He used this model to maintain the beating of an isolated animal heart outside of the body. Roux maintained a portion of the medullary plate of an embryonic chicken in a warm saline solution for several days, establishing the principle of tissue culture. Harrison published the first paper that successfully introduced tissue culture to settle the argument of how nerve fibres originated . Although other scientists had examined cells
Organ, tissue and cell culture are powerful reductionist techniques that have allowed us to study the function of biological systems. However, they are not suitable models for every type of biological question. For example results from cell culture are often not comparable to those derived from
3. Biomimetic models and their potential for replacing, refining and reducing laboratory animal models in research
The National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs) based in London, UK recently carried out some research to demonstrate that poor or incomplete reporting of studies that use animals have made it difficult to derive the maximum scientific knowledge from animal research. In addition, over the last few decades many research laboratories in academia and industry have used laboratory animals unnecessarily. A survey published by the National Institutes of Health (NIH) Office of Laboratory Animal Welfare (OLAW) http://grants.nih.gov/grants/olaw/ http://www.nc3rs.org.uk/ http://www.defra.gov.uk/ http://www.nerc.ac.uk/ http://erc.europa.eu/ http://www.wellcome.ac.uk/
Although the ARRIVE guidelines are primarily aimed at scientists writing up their research for publication and for those who are involved in peer review and intended to improve standards of reporting data from animal experiments, they have also highlighted the potential of biomimetic and tissue engineered
4. Biomimetic models of muscle
A subset of Pax 7/3+ cells have been identified in the limb buds and myotome in development, but fail to differentiate to form myotubes . These proliferating precursor cells can adopt a position between the developed myofibre and the basal lamina during later muscle development [17, 18], which strongly indicates that this subset of progenitors form the satellite cells of post-natal skeletal muscle.
Satellite cells are the resident stem cells of skeletal muscle tissue, which provide additional nuclei to a muscle fibre during regeneration, such as may occur following muscle injury, damage or overload. Myonuclear addition is important in order for the muscle to effectively synthesise new proteins and thus adapt to specific stimuli, as well as generally maintain and increase its mass. Satellite cells are so called due to their anatomical location between the sarcolemma and basal lamina of a muscle fibre , and this parameter was for some time the only true 'marker' of these cells, achievable via electron microscopy. More recently however, a host of proteins which are expressed by satellite cells have been identified, including Pax 7 , Caveolin-1  and myf-5 , and thus a molecular signature of these cells is being derived.
Satellite cells lie quiescent on the muscle periphery until becoming activated upon muscle damage/overload. The precise cause of satellite cell activation remain elusive Neil R.W. Martin and Mark P. Lewis.Satellite cell activation and number following acute and chronic exercise: A mini review. Cellular and Molecular Exercise Physiology 1: e3. doi:10.7457/cmep.v1i1.e3
Neil R.W. Martin and Mark P. Lewis.Satellite cell activation and number following acute and chronic exercise: A mini review. Cellular and Molecular Exercise Physiology 1: e3. doi:10.7457/cmep.v1i1.e3
Isolation and subsequent culture of MPCs (satellite cells when in their anatomical niche) can be conducted either by explant culture, whereby muscle tissue is minced and maintained in culture until MPCs migrate from the tissue [42, 43], or via enzymatic digestion, whereby the tissue is broken down completely to release all of the resident mononuclear cells [44, 45]. Following isolation, careful consideration of the culture techniques should be taken in order to standardise/optimise the desired experiments. Indeed, MPCs are sensitive to the media composition, and will either proliferate or exit the cell cycle and differentiate when exposed to various media compositions . Furthermore, MPCs are sensitive to environmental factors, and will proliferate and fail to differentiate when exposed to low oxygen levels [47, 48] and similarly, serial passaging of MPCs also appears to negatively effect their ability to differentiate . Finally, as the population of cells released from skeletal muscle tissue tends to be mixed in nature (e.g. MPCs, fibroblasts, pericytes, endothelial cells etc.), it is often favourable to further purify the MPCs prior to experimentation either via differential adhesion methods or magnetic separation, a methodology optimise in our laboratory , however these cells may contribute to the development of more biomimetic tissue (detailed in Figure 1 below).
The isolation and characterisation of cells for utilisation in the development of
Particularly, integrins and proteins of the Dystrophin Associated Protein (DAP) complex have been demonstrated to play significant roles in MPC-ECM interaction
The primary function of skeletal muscle Alec S.T. Smith, Rishma Shah, Nigel P. Hunt, Mark P. Lewis. The Role of Connective Tissue and Extracellular Matrix Signaling in Controlling Muscle Development, Function, and Response to Mechanical Forces. Seminars in orthodontics 1 June 2010 (volume 16 issue 2 Pages 135-142 DOI: 10.1053/j.sodo.2010.02.005)
Alec S.T. Smith, Rishma Shah, Nigel P. Hunt, Mark P. Lewis. The Role of Connective Tissue and Extracellular Matrix Signaling in Controlling Muscle Development, Function, and Response to Mechanical Forces. Seminars in orthodontics 1 June 2010 (volume 16 issue 2 Pages 135-142 DOI: 10.1053/j.sodo.2010.02.005)
The provision of mechanical signals for the alignment and fusion of MPCs is an essential criterion for developing biomimetic constructs
A further advantage of using naturally derived polymers is the ability to easily stimulate, both mechanically and electrically, due to the innate mechanical compliance of the polymerised tissue. To this end, numerous investigations have employed such techniques to promote myogenesis and maturation of seeded MPCs [65, 68, 69]. In contrast, the effect of a combined mechanical stimulation protocol, contributed to a reduction in maturation of 3-D seeded myogenic cells compared to monolayer controls . Nevertheless, the effect of increased mechanical signals for the promotion of MPC alignment and fusion, satisfies the desire for a biomimetic.
Consideration of the body of data discussed above, indicates that an argument can be made that the ideal solution for a tissue engineered skeletal muscle construct would embrace the following:
Appropriate matrix signals.
Induction of alignment.
Presence of other cell types.
Provision of all of the cues simultaneously requires an approach that moves beyond conventional monolayer models. The structure defines function in skeletal muscle
|Passive longitudinal tension generated by anchor points||Myotendinous junctions||Collagen [43, 45, 53, 67, 68, 71]; Fibrin [53, 60, 65, 66]|
|ECM||ECM protein composition||Collagen [43, 45, 53, 67, 68, 71]; Fibrin |
|Morphology of cells||Alignment and fusion of seeded cells in a single plane||Collagen [45, 53]; Fibrin [53, 66]|
|Active contractile phenotype (vector force)||Excitability and contractility profile||Fibrin [60, 62, 65];|
|Passive contractile phenotype (vector force)||Cell-matrix passive contractile interaction||Collagen [43, 45]|
|Myosin Heavy Chain (MYH) expression||Increase in MYH-7 mRNA (slow genotype)||Collagen |
|Responses to stimulation (mechanical and electrical)||Increases in gene and protein expression similar to that with exercise||Collagen [68, 71]
There can now be a high degree of confidence that the aforementioned systems do recreate a significant aspect of
5. Animal models of cartilage for arthritis research
Experimental models of degenerative joint diseases such as osteoarthritis (OA) and rheumatoid arthritis (RA) have been in existence for several decades . Animal models of arthritis have been used to understand elements of the arthritic disease process in human patients . They are powerful tools for studying pathologic changes in articular cartilage and bone in great detail, and can be used to evaluate mechanisms of erosive processes . Animal models of arthritis are also used to evaluate potential anti-arthritic drugs for clinical use in human patients [74-76]. The capacity for predicting efficacy in human disease is one of the most important criteria in the selection of animal models . The use of animals has been indispensable to the investigation of the aetiology, pathophysiology, and treatment of various forms of juvenile arthritis . Animal models of rheumatoid arthritis (RA) are also well established and have a proven track record of predictability [74, 78]. These include rat adjuvant arthritis , rat and mouse type II collagen arthritis [80-82], and antigen-induced arthritis in several species. Many animal species are currently used in OA research . Figure 3 summarises the main procedures and disadvantages of animal models of OA.
The animal models of OA include laboratory animals: mice, rats, guinea pigs, rabbits; farm animals: sheep, goats; and companion animals: dogs, cats, horses. Animal models of OA roughly fall into five categories; firstly, spontaneous OA, which naturally occurs in the knee joints of animals, such as guinea pigs and dogs, and has a similar pathogenesis to human OA [84, 85]. Secondly, the surgical creation of joint instability, for example anterior cruciate ligament transection (ACLT) in dogs , meniscal tear model in rats , and collateral ligament transection in horses . Thirdly, the surgical replication of joint trauma, for example the canine groove model , and carpal chip fragmentation in horses . Fourthly, injection into the joint, for example papain , sodium mono-iodoacetate  and collagenase . The final category is the knockout model, which deletes certain genes in mice resulting in the development of OA-like degenerative joint disease. For example the deletion of genes that code for type IX collagen , or the double deletion of biglycan and fibromodulin .
6. Biomimetic models of cartilage
Biomimetic models of articular cartilage were developed specifically for use in preclinical and clinical research long before the advent of tissue engineering and regenerative medicine, and the realisation that the development of these models is an elementary form of tissue engineering. One of the major advantages of articular cartilage is the fact that it is a relatively simple tissue consisting of a fairly homogeneous extracellular matrix and a single cell type. Also, cartilage is avascular, aneural and alymphatic [96, 97], a fact that was disputed for centuries until modern histological techniques were applied to study the tissue . This unique property overcomes many of the obstacles that are involved in culturing other vascularised and innervated tissues. The following sections will discuss the most popular 2- and 3-dimensional models of cartilage.
6.1. 2-Dimensional monolayer models of chondrocyes
Although chondrocyte survival and phenotype are regulated by culture conditions, the expression of the chondrogenic transcription factor Sox9 is of crucial importance . The unique phenotype of the chondrocyte requires sustained expression of Sox9. This transcription factor plays an important role in the normal skeletal development and regulate the expression of other genes involved in chondrogenesis [114, 115].
6.2. 3-Dimensional cartilage culture systems — Alginate beads
Alginic acid, also called algin or alginate, is an anionic polysaccharide that is widely distributed in the cell walls of brown algae. When extracted in granular or powdered forms, alginate is capable of absorbing 200-300 times its own weight in water. Due to its biocompatibility and simple gelation with divalent cations such as Ca2+, alginate is widely used for cell immobilization and encapsulation. Therefore, alginate beads offer an ideal substrate for developing support matrices for 3-dimensional chondrocyte culture (see Figure 5). Immobilization of cells along with macromolecules and biomaterials in alginate gels has become a well-established technology. Alginate beads are used in many biomedical and industrial applications. Cells immobilized in alginate gels maintain their differentiated phenotype during long-term culture due to the 3-dimensional environment of the gel network. In tissue engineering applications immobilized cells or tissue explants can be used as bioartificial organs as the alginate gel may function as a protective barrier towards physical stress and to avoid immunological reactions with the host. Chondrocytes can be encapsulated and maintained in calcium alginate beads or gels in 3-dimensional culture . Avian and mammalian chondrocytes cultured in "semi-solid" and "hollow" alginate beads exhibit a spherical shape as opposed to the fibroblastic morphology that is observed in monolayer culture . The encapsulation methodology is suitable for the culture of chondrocytes in single beads, in multiwell dishes, or mass culture. Human and bovine adult articular chondrocytes have also been cultured in alginate beads and studies have shown that they retain their spherical shape and typical chondrocyte-like appearance for at least 5 weeks . Alginate culture has also been used for cultivating intervertebral disc cells , nucleus pulposus and annulus fibrosus cells  and chondrocyte cell lines . Aggrecan appears to be a major ECM molecule produced by alginate cultured chondrocytes. Sensitive assays have been developed for the quantification of glycosaminoglycans (GAGs) and nitric oxide (NO) produced by alginate cultures [121, 122]. Decorin is also synthesized in small amounts but it is rapidly lost from the agarose or alginate gel . Alginate culture can be used to induce the re-expression of cartilage-specific genes (aggrecan and collagen II) by dedifferentiated human articular chondrocytes cultured in alginate beads. However, alginate is unable to restore the chondrocyte phenotype in SV-40 transformed cells . Thus, articular chondrocytes embedded in alginate gel can produce
6.3. 3–Dimensional cartilage culture systems — Agarose gels
Agar is a gelatinous substance derived from algae. It is a mixture of two components: the linear polysaccharide agarose, and a heterogeneous mixture of smaller molecules called agaropectin. Agar and agarose have been used extensively for cell culture. Agar gels are have been used throughout the world to provide a solid surface containing medium for the growth of bacteria and fungi. As a gel, an agarose medium is porous and therefore can be used to re-create the 3-dimensional environment that chondrocytes are accustomed to in articular cartilage. Culturing chondrocytes in agarose gels is actually very similar to alginate beads. Agarose gels proved to be particularly useful for studies on proteoglycans produced by avian , porcine  and bovine  chondrocytes. Agarose gels re-create a biomimetic 3-dimensional environment and stimulate ECM production by chondrocytes . One of the most important studies on chondrocyte differentiation and redifferentiation was done using agarose gels by Benya and Shaffer . As described earlier serial monolayer culture results in chondrocyte dedifferentiation and loss of phenotype. When chondrocytes dedifferentiate in monolayer culture they stop producing proteoglycans and type II collagen and instead secrete a different ECM consisting predominately of type I collagen and a low level of proteoglycan synthesis. Benya and Shaffer used agarose gels to demonstrate that dedifferentiated chondrocytes re-express the differentiated phenotype, producing proteoglycans and cartilage specific collagens . The same outcome was achieved years later using alginate beads . The original work of Benya and Shaffer demonstrated that a complete return to the differentiated collagen and proteoglycan producing chondrocyte phenotype is possible in agarose gels. Their results also emphasized the essential role of the spherical cell shape in the modulation of the chondrocyte phenotype and demonstrate a reversible system for the study of gene expression .
It is important to bear in mind that articular cartilage is subjected to dynamic compressive loading during normal activity and this influences chondrocyte metabolism. Mechanical forces are key determinants of connective tissue differentiation. Agarose gels, alginate beads and other 3-D gel systems are well established for studying the effects of dynamic compression on chondrocytes [132, 133]. These techniques have gained significant popularity over the last two decades  and are still in use today to study patterns of gene expression in response to dynamic compression  and chondrocyte mechanotransduction pathways . The preservation of the chondrocyte phenotype and the gradually increasing proteoglycan synthesis in agarose and alginate gels are promising methods for creating and engineering tissue implants for cartilage repair. These techniques can also be used to create new cartilage tissue from the joints of food producing animals (i.e. cattle, sheep, pigs) without having to sacrifice many smaller laboratory animals. This is an important area of cartilage tissue engineering with important consequences for animal research.
6.4. 3-Dimensional cartilage explant culture
Explant culture is a technique used for the isolation of cells from a piece of tissue. Tissue harvested in this manner is called an explant. The tissue is harvested under sterile conditions and explants are placed in a cell culture dish containing growth media. In some explant cultures (i.e. skeletal muscle) progenitor cells migrate out of the tissue and grow on the surface of the dish. These primary cells can then be further expanded and exploited. In cartilage explant culture cells remain in their surrounding extracellular matrix and this accurately mimics the
6.4.1. 3-Dimensional High-Density and Pellet Cultures of Chondrocytes
High-density culture is a 3-dimensional system that has been in the literature since the early 1970’s. High-density suspension cultures of chondrocytes were initially used to study cartilage matrix protein synthesis by mammalian chondrocytes [144, 145], specifically mucoprotein  and proteoglycan  biosynthesis. In an important study published in 1977 the method was refined by von der Mark and von der Mark who used tissue culture plastic dishes on an agar base to monitor chondrogenesis of stage-24 chick limb mesodermal cells
The high-density model exhibits a number of characteristics that make it particularly suitable for studies on chondrogenesis. In the first 24 hours of the high-density chondrocytes culture, cells form prechondrogenic areas composed of densely packed cells with intercellular interactions (gap junctions); these are surrounded by a perichondrium of flat fibroblast-like cells  resembling the situation during the early stage of chondrogenesis
6.4.2. Co–cultures of chondrocytes and synoviocytes
The synovial joint contains several important tissue components. These are articular cartilage, synovium, subchondral bone and fat pads (adipose tissue). Developing http://www.nc3rs.org.uk/researchportfolio/showcatportfolio.asp?id=254
Cell culture has a bright future. It is a fundamental and core component of tissue engineering and regenerative medicine. In this context the majority of studies carried out to date have used the well-established method of growing cells on 2-D plastic or glass substrates. There is increasing use of 3-D cell cultures in research areas as diverse as drug discovery, cancer biology, regenerative medicine and basic life science research. There are many methods to facilitate the growth of 3-D cellular structures including nanoparticle facilitated magnetic levitation, gels, beads and solid matrices, self-assembling scaffolds and hanging drop plates. The culture of mammalian cells for toxicity testing or drug screening is likely to increase in the future. The biotechnology, pharmaceutical and cosmetic industries urgently need 3-D cell culture models that more accurately mimic living tissues and organs. This kind of technology will gradually increase in importance because of the vast array of natural and combinatorial products that require screening and the increased pressure from regulatory authorities to reduce animal testing. Most importantly, the pressure to reduce animal testing will stimulate scientists to create more robust biomimetic culture models and culture systems that may eventually eliminate the need for using animals for antibody production and vaccine development. There are many exciting and emerging areas that have not been reviewed in this chapter. This chapter has focused on biomimetic models of joint and muscle. Since joint tissues contain a diverse number of cell types, we have focused our efforts on
It is becoming clear that OA is a disease of the entire joint rather than any single component and deterioration of associated skeletal muscle masses around an affected joint is a well-reported phenomena. Changes in the highly adaptive skeletal muscle may precede changes seen in other tissue types so analysis of the transcriptome/metabolome could have great value in prognosis and diagnosis. It is possible to conduct such studies in humans although such experiments are logistically complicated, requiring appropriate subject numbers that adhere to complicated inclusion and exclusion criteria and expensive consumables. It could however be argued that a more beneficial approach would be to utilise a “pre-clinical model” to further refine and develop hypotheses before introduction in the human being. This approach would clearly also decrease the need for animal work.
A number of animal models of arthritis have been developed to study arthritic disease pathogenesis and evaluate the efficacy of candidate anti-inflammatory and anti-arthritic drugs for clinical development [161-167]. These animal models may involve injection of inflammatory agents into the joint, surgical creation of joint instability or surgical replication of joint trauma. Such models not only cause a considerable amount of pain and suffering but also none of them have a proven track record of predictability in human disease. Consequently, there is an acute need for developing novel and alternative
Articular cartilage damage is a persistent and increasing problem as the ageing population expands and treatments to achieve biological repair have been challenging . Cartilage tissue engineering has been around for over 20 years. However, none of the approaches available so far have been able to achieve the consistency, effectiveness and reliability that are required for clinical applications. Tissue engineering of a mechanically resilient cartilage construct that meets the structural and functional criteria for effective functional integration into a defect site in the host is a difficult endeavour . One of the fundamental weaknesses of all the models available to date is that none of them possess the normal zonal organization of chondrocytes that is seen
In summary, it may be difficult to imagine research being done without animal models but it is worth pointing out that
AcknowledgmentsA. Mobasheri acknowledges the financial support of The Wellcome Trust, the National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs) (grant number: Mobasheri.A.28102007), the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BBSRC/S/M/2006/ 13141 and BB/G018030/1), the Engineering and Physical Sciences Research Council (EPSRC), Arthritis Research UK (ARUK) and the European Commission Framework 7 (EU FP7). M. Lewis acknowledges the financial support of the National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs), the Engineering and Physical Sciences Research Council (EPSRC), Arthritis Research UK (ARUK), The Wellcome Trust, the National Centre for Sport and Exercise Medicine (NCSEM).
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