Muscle tissue engineering

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Muscle tissue engineering is a subset of the general field of tissue engineering, which studies the combined use of cells and scaffolds to design therapeutic tissue implants. Within the clinical setting, muscle tissue engineering involves the culturing of cells from the patient's own body or from a donor, development of muscle tissue with or without the use of scaffolds, then the insertion of functional muscle tissue into the patient's body. Ideally, this implantation results in full regeneration of function and aesthetic within the patient's body. Outside the clinical setting, muscle tissue engineering is involved in drug screening, hybrid mechanical muscle actuators, robotic devices, and the development of engineered meat as a new food source. [1]

Contents

Innovations within the field of muscle tissue engineering seek to repair and replace defective muscle tissue, thus returning normal function.The practice begins by harvesting and isolating muscle cells from a donor site, then culturing those cells in media. The cultured cells form cell sheets and finally muscle bundles which are implanted into the patient.

Overview

Muscle is a naturally aligned organ, with individual muscle fibers packed together into larger units called muscle fascicles. [2] The uniaxial alignment of muscle fibers allows them to simultaneously contract in the same direction and properly propagate force on the bones via the tendons. Approximately 45% of the human body is composed of muscle tissue, and this tissue can be classified into three different groups: skeletal muscle, cardiac muscle, and smooth muscle. Muscle plays a role in structure, stability, and movement in mammalian bodies. The basic unit for a muscle is a muscle fiber, which is made up of myofilaments actin and myosin. This muscle fiber contains sarcomeres which generate the force required for contraction.

A major focus of muscle tissue engineering is to create constructs with the functionality of native muscle and ability to contract. To this end, alignment of the tissue engineered construct is extremely important. It has been shown that cells grown on substrates with alignment cues form more robust muscle fibers. [3] Several other design criteria considered in muscle tissue engineering include the scaffold porosity, stiffness, biocompatibility, and degradation timeline. Substrate stiffness should ideally be in the myogenic range, which has been shown to be 10-15 kPa. [4]

The purpose of muscle tissue engineering is to reconstruct functional muscular tissue which has been lost via traumatic injury, tumor ablation, or functional damage caused by myopathies. Until now, the only method used to restore muscular tissue function and aesthetic was free tissue transfer. Full function is typically not restored, however, which results in donor site morbidity and volume deficiency. The success of tissue engineering as it pertains to the regeneration of skin, cartilage, and bone indicates that the same success will be found in engineering muscular tissue. [5] Early innovations in the field yielded in vitro cell culturing and regeneration of muscle tissue which would be implanted in the body, but advances in recent years have shown that there may be potential for in vivo muscle tissue engineering using scaffolding.

Etymology

The term muscle tissue engineering, while it is a subset of the much larger discipline, tissue engineering, was first coined in 1988 when Herman Vandenburgh, a surgeon, cultured avian myotubes in collagen-coated culture plates. [6] This started a new era of in vitro tissue engineering. The ideal was officially adopted in 1988 in Vandenburgh's publication titled Maintenance of Highly Contractile Tissue-Cultured Avian Skeletal Myotubes in Collagen Gel. [7] In 1989, the same group determined that mechanical stimulation of myoblasts in vitro facilitates engineered skeletal muscle growth. [8]

History

19th Century

A rudimentary understanding of muscle tissue began to develop as early as 1835, when embryonic myogenesis was first described. In the 1860s, it was shown that muscle is capable of regeneration and an experimental regeneration was conducted to better understand the specific method by which this was done in vivo. Following this discovery, muscle generation and degeneration in man were described for the first time. Researchers consequently assessed several aspects of muscle regeneration in vivo, including "the continuous or discontinuous regeneration depending on tissue type" to increase functional understanding of the phenomena. [9] It was not until the 1960s, however, that researchers determined what components were required for muscle regeneration. [9]

20th Century

In 1957, it was determined via DNA content that myoblasts proliferate, but myonuclei do not. Following this discovery, the satellite cell was experimentally uncovered by Mauro and Katz [10] as stem cells which sit on the surface of the myofibre and have the capability to differentiate into muscle cells. Satellite cells provide myoblasts for growth, differentiation, and repair of muscle tissue. Muscle tissue engineering officially began as a discipline in 1988 when Herman Vandenburgh cultured avian myotubes in collagen-coated culture plates. Following this development, it was found in 1989 that mechanical stimulation of myoblasts in vitro facilitates engineered skeletal muscle growth. Most of the modern innovations in the field of muscle tissue engineering are found in the 21st century.

21st Century

Between 2000 and 2010, the effects of volumetric muscle loss (VML) were assessed as it pertains to muscle tissue engineering. VML can be caused by a variety of injuries or diseases, including general trauma, postoperative damage, cancer ablation, congenital defects, and degenerative myopathy. Although muscle contains a stem cell population called satellite cells that are capable of regenerating small muscle injuries, muscle damage in VML is so extensive that it overwhelms muscle's natural regenerative capabilities. Currently VML is treated through an autologous muscle flap or graft but there are various problems associated with this procedure. Donor site morbidity, lack of donor tissue, and inadequate vascularization all limit the ability of doctors to adequately treat VML. [11] The field of muscle tissue engineering attempts to address this problem through the design of a functional muscle construct that can be used to treat the damaged muscle instead of harvesting an autologous muscle flap from elsewhere on the patient's body.

Research conducted between 2000 and 2010 informed the conclusion that functional analysis of a tissue engineered muscle construct is important to illustrate its potential to help regenerate muscle. A variety of assays are generally used to evaluate a tissue engineered muscle construct including immunohistochemistry, RT-PCR, electrical stimulation and resulting peak-to-peak voltage, scanning electron microscope imaging, and in vivo response.

The most recent advances in the field include cultured meat, biorobotic systems, and biohybrid impants in regenerative medicine or disease modeling. [12]

Examples

The majority of current advancements in muscle tissue engineering reside in the skeletal muscle category, so the majority of these examples will have to do with skeletal muscle engineering and regeneration. We will review a couple of examples of smooth muscle tissue engineering and cardiac muscle tissue engineering in this section as well.

Skeletal Muscle Tissue Engineering (SMTE)

Smooth Muscle Tissue Engineering

Cardiac Muscle Tissue Engineering

Methods

Muscle tissue engineering methods are consistently categorized across literature into three groups: in situ, in vivo, and in vitro muscle tissue engineering. We will assess each of these categories and detail specific practices used in each one.

In Situ

In situ” is a latin phrase whose literal translation is “on site.” It is a term that has been used in the English language since the mid-eighteenth century to describe something that is in its original place or position. In the context of muscle tissue engineering, in situ tissue engineering involves the introduction and implantation of an acellular scaffold into the site of injury or degenerated tissue. The goal of in situ muscle tissue engineering is to encourage host cell recruitment, natural scaffold formation, and proliferation and differentiation of host cells. The main idea which in situ muscle tissue engineering is based on is the self-healing, regenerative properties of the mammalian body. [26] The primary method for in situ muscle tissue engineering is described in the following section:

As described in Biomaterials for In Situ Tissue Regeneration: A Review (Abdulghani & Mitchell, 2019) [27] , in situ muscle tissue engineering requires very specific biomaterials which have the capability to recruit stem cells or progenitor cells to the site of the muscle defect, thus allowing regeneration of tissue without implantation of seed cells. The key to a successful scaffold is the appropriate properties (i.e. biocompatibility, mechanical strength, elasticity, biodegradability) and the correct shape and volume for the specific muscle defect in which they are implanted. This scaffold should effectively mimic the cellular response of the host tissue, and Mann et al. have found that Polyethylene glycol-based hydrogels are very successful as in situ biomaterial scaffolds because they are chemically modified to be degraded by biological enzymes, thus encouraging cell migration and proliferation. [28] Beyond Polyethylene glycol-based hydrogels, synthetic biomaterials such as PLA and PCL are successful in situ scaffolds as they can be fully customized to each specific patient. These materials' stiffness, degradation, and porosity properties are tailored to the degenerated tissue's topology, volume, and cell type so as to provide the optimal environment for host cell migration and proliferation.

In situ engineering promotes natural regeneration of damaged tissue by effectively mimicking the mammalian body's own wound healing response. The use of both biological and synthetic biomaterials as scaffolds promotes host cell migration and proliferation directly to the defect site, thus decreasing the amount of time required for muscle tissue regeneration. Furthermore, in situ engineering effectively bypasses the risk of implant rejection by the immune system due to the biodegradable qualities in each scaffold.

In Vivo

"In vivo" is a latin phrase whose literal translation is "in a living thing." This term is used in the English language to describe a process which occurs inside of a living organism. In the realm of muscle tissue engineering, this term applies to the seeding of cells into a biomaterial scaffold immediately prior to implantation. The goal of in vivo muscle tissue engineering is to create a cell-seeded scaffold that once implanted into the wound site will preserve cell efficacy. In vivo methods provide a greater amount of control over cell phenotype, mechanical properties, and functionality of the tissue construct. [26]

As described in Skeletal Muscle Tissue Engineering: Biomaterials-Based Strategies for the Treatment of Volumetric Muscle Loss (Carnes & Pins, 2020) [26] , in vivo muscle tissue engineering builds on the concept of in situ engineering by not only implanting a biomaterial scaffold with specific mechanical and chemical properties, but also seeding the scaffold with the specific cell type needed for regeneration of the tissue. Reid et al. [29] describe common scaffolds utilized in the in vivo muscle tissue engineering process. These scaffolds include hydrogels infused with hyaluronic acid (HA), gelatin silk fibroin, and chitosan as these materials promote muscle cell migration and proliferation. For example, a biodegradable and renewable material derived from chitin known as chitosan, has unique mechanical properties which support smooth muscle cell differentiation and retention in the tissue regeneration site. When this scaffold is further functionalized with Arginine-Glycine-Aspartic Acid (RGD), it provides a better growth environment for smooth muscle cells. Another scaffold commonly used is decellularized extracellular matrix (ECM) tissue as it is fully biocompatible, biodegradable, and contains all of the necessary protein binding sites for full functional recovery and integration of muscle tissue. Once seeded with cells, this material becomes an optimal environment for cell proliferation and integration with existing tissue as it effectively mimics the environment in which tissue naturally regenerates in the mammalian body.

The in vivo muscle tissue engineering technique provides the wound healing process with a "head start" in development, as the body no longer needs to recruit host cells to begin regeneration. This approach also bypasses the need for cell manipulation prior to implantation, thus ensuring that they maintain all of their mechanical and functional properties. [30]

In Vitro

"In vitro" is a latin phrase whose literal translation is "within the glass." This term is used in the English language to describe a process which occurs outside of a living organism. Within the context of muscle tissue engineering, the term "in vitro" applies to the seeding of cells into a biomaterial scaffold with growth factors and nutrients, then culturing these constructs until a functional construct, such as myofibres, is developed. These developed constructs are then implanted into the wound site with the expectation that they will continue to proliferate and integrate into host muscle tissue. The goal of in vitro muscle tissue engineering is to increase the functionality of the tissue before it is ever implanted into the body, thus increasing mechanical properties and potential to thrive in the host body.

Abdulghani & Mitchell [27] describe in vitro muscle tissue engineering as a concept with utilizes the same basic strategies of in vivo tissue engineering. The difference between the two methods, however, is the development of a fully functional tissue engineered muscle graft (TEMG) that occurs in the in vitro technique. In vitro muscle tissue engineering includes the seeding of cells onto a biomaterial scaffold, but goes a step further by adding growth factors and biochemical and biophysical cues to promote cell growth, proliferation, differentiation, and finally regeneration into a functional muscle tissue construct. Typically, in vitro scaffolds contain specific surface features which guide the direction of cell proliferation. They are usually fibrous with aligned pores as these features encourage cell adhesion during regeneration. Beyond the types of scaffolds used in this technique, a largely important aspect of this technique is the electrical and mechanical stimulation which mimic the natural regeneration environment and encourage the expansion of intracellular communication pathways. Before TEMGs are introduced into the wound defect, they musts be vascularized to promote proper integration with the host tissue. To achieve vascularization, researchers typically seed a scaffold with multiple cell types in order to develop both muscle tissue and vascular pathways. This process prevents rejection of the TEMG upon implantation as it is able to effectively thrive in the host tissue environment. There is always a risk of immune rejection when implanting fully developed tissue, though, so this method tissue regeneration is the most closely monitored post-implantation. [26]

The in vitro muscle tissue engineering technique is used to create muscle tissue with more successful functional and mechanical properties. According to Carnes & Pins in Skeletal Muscle Tissue Engineering: Biomaterials-Based Strategies for the Treatment of Volumetric Muscle Loss [26] , this approach develops a microenvironment that is more conducive to enhancing tissue regeneration upon implantation, thus restoring full functionality to patients.

Future Work

Current muscle tissue engineering trends lead towards the development of skeletal muscle regeneration techniques over smooth muscle or cardiac muscle regeneration. A current trend found throughout literature is the treatment of Volumetric Muscle Loss (VML) using muscle tissue engineering techniques. VML is the result of abrupt loss of skeletal muscle due to surgical resection, trauma, or combat injuries. [29] It has been observed that tissue grafts, the current treatment plan, do not restore full functionality or aesthetic integrity to the site of injury. Muscle tissue engineering offers an optimistic possibility for patients, as in situ, in vivo, and in vitro techniques have been proven to restore functionality to muscle tissue in the wound site. Methods being explored include acellular scaffold implantation, cell-seeded scaffold implantation, and in vitro fabrication of muscle grafts. Preliminary data from each of these methods promises a solution for patients suffering from VML.

Beyond specific technological advances in the field of muscle tissue engineering, researchers are working to establish a connection with the larger umbrella that is tissue engineering.

Related Research Articles

<span class="mw-page-title-main">Tissue engineering</span> Biomedical engineering discipline

Tissue engineering is a biomedical engineering discipline that uses a combination of cells, engineering, materials methods, and suitable biochemical and physicochemical factors to restore, maintain, improve, or replace different types of biological tissues. Tissue engineering often involves the use of cells placed on tissue scaffolds in the formation of new viable tissue for a medical purpose, but is not limited to applications involving cells and tissue scaffolds. While it was once categorized as a sub-field of biomaterials, having grown in scope and importance, it can is considered as a field of its own.

Myosatellite cells, also known as satellite cells, muscle stem cells or MuSCs, are small multipotent cells with very little cytoplasm found in mature muscle. Satellite cells are precursors to skeletal muscle cells, able to give rise to satellite cells or differentiated skeletal muscle cells. They have the potential to provide additional myonuclei to their parent muscle fiber, or return to a quiescent state. More specifically, upon activation, satellite cells can re-enter the cell cycle to proliferate and differentiate into myoblasts.

<span class="mw-page-title-main">Organoid</span> Miniaturized and simplified version of an organ

An organoid is a miniaturised and simplified version of an organ produced in vitro in three dimensions that mimics the key functional, structural and biological complexity of that organ. They are derived from one or a few cells from a tissue, embryonic stem cells or induced pluripotent stem cells, which can self-organize in three-dimensional culture owing to their self-renewal and differentiation capacities. The technique for growing organoids has rapidly improved since the early 2010s, and The Scientist names it as one of the biggest scientific advancements of 2013. Scientists and engineers use organoids to study development and disease in the laboratory, drug discovery and development in industry, personalized diagnostics and medicine, gene and cell therapies, tissue engineering and regenerative medicine.

Articular cartilage, most notably that which is found in the knee joint, is generally characterized by very low friction, high wear resistance, and poor regenerative qualities. It is responsible for much of the compressive resistance and load bearing qualities of the knee joint and, without it, walking is painful to impossible. Osteoarthritis is a common condition of cartilage failure that can lead to limited range of motion, bone damage and invariably, pain. Due to a combination of acute stress and chronic fatigue, osteoarthritis directly manifests itself in a wearing away of the articular surface and, in extreme cases, bone can be exposed in the joint. Some additional examples of cartilage failure mechanisms include cellular matrix linkage rupture, chondrocyte protein synthesis inhibition, and chondrocyte apoptosis. There are several different repair options available for cartilage damage or failure.

<span class="mw-page-title-main">Myogenesis</span> Formation of muscular tissue, particularly during embryonic development

Myogenesis is the formation of skeletal muscular tissue, particularly during embryonic development.

Cardiomyoplasty is a surgical procedure in which healthy muscle from another part of the body is wrapped around the heart to provide support for the failing heart. Most often the latissimus dorsi muscle is used for this purpose. A special pacemaker is implanted to make the skeletal muscle contract. If cardiomyoplasty is successful and increased cardiac output is achieved, it usually acts as a bridging therapy, giving time for damaged myocardium to be treated in other ways, such as remodeling by cellular therapies.

<span class="mw-page-title-main">Mesoangioblast</span>

A mesoangioblast is a type of progenitor cell that is associated with vasculature walls. Mesoangioblasts exhibit many similarities to pericytes, which are found in the small vessels. Mesoangioblasts are multipotent stem cells with the potential to progress down the endothelial or mesodermal lineages. Mesoangioblasts express the critical marker of angiopoietic progenitors, KDR (FLK1). Because of these properties, mesoangioblasts are a precursor of skeletal, smooth, and cardiac muscle cells along with endothelial cells. Research has suggested their application for stem cell therapies for muscular dystrophy and cardiovascular disease.

Neural tissue engineering is a specific sub-field of tissue engineering. Neural tissue engineering is primarily a search for strategies to eliminate inflammation and fibrosis upon implantation of foreign substances. Often foreign substances in the form of grafts and scaffolds are implanted to promote nerve regeneration and to repair damage caused to nerves of both the central nervous system (CNS) and peripheral nervous system (PNS) by an injury.

A nerve guidance conduit is an artificial means of guiding axonal regrowth to facilitate nerve regeneration and is one of several clinical treatments for nerve injuries. When direct suturing of the two stumps of a severed nerve cannot be accomplished without tension, the standard clinical treatment for peripheral nerve injuries is autologous nerve grafting. Due to the limited availability of donor tissue and functional recovery in autologous nerve grafting, neural tissue engineering research has focused on the development of bioartificial nerve guidance conduits as an alternative treatment, especially for large defects. Similar techniques are also being explored for nerve repair in the spinal cord but nerve regeneration in the central nervous system poses a greater challenge because its axons do not regenerate appreciably in their native environment.

<span class="mw-page-title-main">Clemens van Blitterswijk</span>

Clemens A. van Blitterswijk is a Dutch tissue engineer who contributed to the use of biomaterials to heal bone injuries, especially using osteoinductive ceramics. In collaboration with Jan de Boer and others, he has contributed to screening microtextures to study cell-biomaterial interactions, an approach termed materiomics.

Nano-scaffolding or nanoscaffolding is a medical process used to regrow tissue and bone, including limbs and organs. The nano-scaffold is a three-dimensional structure composed of polymer fibers very small that are scaled from a Nanometer scale. Developed by the American military, the medical technology uses a microscopic apparatus made of fine polymer fibers called a scaffold. Damaged cells grip to the scaffold and begin to rebuild missing bone and tissue through tiny holes in the scaffold. As tissue grows, the scaffold is absorbed into the body and disappears completely.

<span class="mw-page-title-main">C2C12</span> Mouse myoblast cell line

C2C12 is an immortalized mouse myoblast cell line. The C2C12 cell line is a subclone of myoblasts that were originally obtained by Yaffe and Saxel at the Weizmann Institute of Science in Israel in 1977. Developed for in vitro studies of myoblasts isolated from the complex interactions of in vivo conditions, C2C12 cells are useful in biomedical research. These cells are capable of rapid proliferation under high serum conditions and differentiation into myotubes under low serum conditions. Mononucleated myoblasts can later fuse to form multinucleated myotubes under low serum conditions or starvation, leading to the precursors of contractile skeletal muscle cells in the process of myogenesis. C2C12 cells are used to study the differentiation of myoblasts, osteoblasts, and myogenesis, to express various target proteins, and to explore mechanistic biochemical pathways.

<span class="mw-page-title-main">Decellularization</span>

Decellularization is the process used in biomedical engineering to isolate the extracellular matrix (ECM) of a tissue from its inhabiting cells, leaving an ECM scaffold of the original tissue, which can be used in artificial organ and tissue regeneration. Organ and tissue transplantation treat a variety of medical problems, ranging from end organ failure to cosmetic surgery. One of the greatest limitations to organ transplantation derives from organ rejection caused by antibodies of the transplant recipient reacting to donor antigens on cell surfaces within the donor organ. Because of unfavorable immune responses, transplant patients suffer a lifetime taking immunosuppressing medication. Stephen F. Badylak pioneered the process of decellularization at the McGowan Institute for Regenerative Medicine at the University of Pittsburgh. This process creates a natural biomaterial to act as a scaffold for cell growth, differentiation and tissue development. By recellularizing an ECM scaffold with a patient’s own cells, the adverse immune response is eliminated. Nowadays, commercially available ECM scaffolds are available for a wide variety of tissue engineering. Using peracetic acid to decellularize ECM scaffolds have been found to be false and only disinfects the tissue.

A 3D cell culture is an artificially created environment in which biological cells are permitted to grow or interact with their surroundings in all three dimensions. Unlike 2D environments, a 3D cell culture allows cells in vitro to grow in all directions, similar to how they would in vivo. These three-dimensional cultures are usually grown in bioreactors, small capsules in which the cells can grow into spheroids, or 3D cell colonies. Approximately 300 spheroids are usually cultured per bioreactor.

The in vivo bioreactor is a tissue engineering paradigm that uses bioreactor methodology to grow neotissue in vivo that augments or replaces malfunctioning native tissue. Tissue engineering principles are used to construct a confined, artificial bioreactor space in vivo that hosts a tissue scaffold and key biomolecules necessary for neotissue growth. Said space often requires inoculation with pluripotent or specific stem cells to encourage initial growth, and access to a blood source. A blood source allows for recruitment of stem cells from the body alongside nutrient delivery for continual growth. This delivery of cells and nutrients to the bioreactor eventually results in the formation of a neotissue product. 

Human engineered cardiac tissues (hECTs) are derived by experimental manipulation of pluripotent stem cells, such as human embryonic stem cells (hESCs) and, more recently, human induced pluripotent stem cells (hiPSCs) to differentiate into human cardiomyocytes. Interest in these bioengineered cardiac tissues has risen due to their potential use in cardiovascular research and clinical therapies. These tissues provide a unique in vitro model to study cardiac physiology with a species-specific advantage over cultured animal cells in experimental studies. hECTs also have therapeutic potential for in vivo regeneration of heart muscle. hECTs provide a valuable resource to reproduce the normal development of human heart tissue, understand the development of human cardiovascular disease (CVD), and may lead to engineered tissue-based therapies for CVD patients.

<span class="mw-page-title-main">Antonios Mikos</span> Greek-American biomedical engineer

Antonios Georgios Mikos is a Greek-American biomedical engineer who is the Louis Calder Professor of Bioengineering and Chemical and Biomolecular Engineering at Rice University. He specialises in biomaterials, drug delivery, and tissue engineering.

Tissue engineered heart valves (TEHV) offer a new and advancing proposed treatment of creating a living heart valve for people who are in need of either a full or partial heart valve replacement. Currently, there are over a quarter of a million prosthetic heart valves implanted annually, and the number of patients requiring replacement surgeries is only suspected to rise and even triple over the next fifty years. While current treatments offered such as mechanical valves or biological valves are not deleterious to one's health, they both have their own limitations in that mechanical valves necessitate the lifelong use of anticoagulants while biological valves are susceptible to structural degradation and reoperation. Thus, in situ (in its original position or place) tissue engineering of heart valves serves as a novel approach that explores the use creating a living heart valve composed of the host's own cells that is capable of growing, adapting, and interacting within the human body's biological system.

Matthias Lutolf is a bio-engineer and a professor at EPFL where he leads the Laboratory of Stem Cell Bioengineering. He is specialised in biomaterials, and in combining stem cell biology and engineering to develop improved organoid models. In 2021, he became the scientific director for Roche's Institute for Translation Bioengineering in Basel.

Bioinstructive materials provide instruction to biological cells or tissue, for example immune instruction when monocytes are cultured on certain polymers they polarise to pro- or anti-inflammatory macrophages with potential applications in implanted devices, or materials for the repair of musculoskeletal tissues. Due to the paucity of information on the mechanism of materials control of cells, beyond the general recognition of the important role of adsorbed biomolecules, high throughput screening of large libraries of materials, topographies, and shapes are often used to identify cell instructive material systems. Applications of bioinstructive materials as substrates for stem cell production, cell delivery and reduction of foreign body reaction and coatings to reduce infections on medical devices. This non-leaching approach is distinct from strategies of infection control relying on antibiotic release, cytokine delivery or guidance of cells by surface located epitopes inspired by nature.

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