REVIEW |
Correspondence to: Miranda D. Grounds, Dept. of Anatomy & Human Biology, University of Western Australia, Nedlands, Western Australia 6907, Australia. E-mail: mgrounds@anhb.uwa.edu.au
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Summary |
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In postnatal muscle, skeletal muscle precursors (myoblasts) can be derived from satellite cells (reserve cells located on the surface of mature myofibers) or from cells lying beyond the myofiber, e.g., interstitial connective tissue or bone marrow. Both of these classes of cells may have stem cell properties. In addition, the heretical idea that post-mitotic myonuclei lying within mature myofibers might be able to re-form myoblasts or stem cells is examined and related to recent observations for similar post-mitotic cardiomyocytes. In adult hearts (which previously were not considered capable of repair), the role of replicating endogenous cardiomyocytes and the recruitment of other (stem) cells into cardiomyocytes for new cardiac muscle formation has recently attracted much attention. The relative contribution of these various sources of precursor cells in postnatal muscles and the factors that may enhance stem cell participation in the formation of new skeletal and cardiac muscle in vivo are the focus of this review. We concluded that, although many endogenous cell types can be converted to skeletal muscle, the contribution of non-myogenic cells to the formation of new postnatal skeletal muscle in vivo appears to be negligible. Whether the recruitment of such cells to the myogenic lineage can be significantly enhanced by specific inducers and the appropriate microenvironment is a current topic of intense interest. However, dermal fibroblasts appear promising as a realistic alternative source of exogenous myoblasts for transplantation purposes. For heart muscle, experiments showing the participation of bone marrow-derived stem cells and endothelial cells in the repair of damaged cardiac muscle are encouraging. (J Histochem Cytochem 50:589610, 2002)
Key Words: myoblasts, skeletal muscle, stem cells, cardiomyocytes, cardiac muscle, fibroblasts, transplantation
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Skeletal Muscle |
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Skeletal Muscle Precursor Cells and Regeneration
There is considerable interest in skeletal muscle regeneration for increased efficiency of repair in sports medicine, after severe injury or muscle transplantation, in muscular dystrophies, for possible ablation of mitochondrial myopathies, and for recovery of strength in disuse atrophy or space flight (reviewed in
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Clinical Applications of Myoblast Transplantation
Beyond their role in regeneration, normal skeletal myoblasts have been isolated, cultured, and then transplanted in vivo to replace defective genes in myopathies [e.g., dystrophin in Duchenne muscular dystrophy (DMD);
Transplantation of cultured myoblasts has also been used to replace defective muscles, e.g., for urinary incontinence (
The focus of this review is the source of skeletal muscle precursor cells, and three candidate sources are considered: (a) the satellite cells of myofibers, (b) various types of cells originating outside the myofiber, and (c) "post-mitotic" myonuclei within the sarcoplasm of damaged myofibers that might re-enter the cell cycle (summarized in Fig 1). The reader is also directed to additional recent reviews of developmental relationships, therapeutic possibilities, and other aspects of skeletal muscle satellite and stem cells (
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Satellite Cells |
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Markers For Identification of Satellite Cells
Myoblasts in postnatal muscle are classically considered to be derived from cells located on the surface of the myofiber and lying beneath the basement membrane. These were originally defined on the basis of their geography and were therefore termed satellite cells. The satellite cells appear to be reserve muscle precursor cells. In mature skeletal muscles (e.g., of the limbs) they are normally quiescent and are activated only in response to growth or muscle damage. The most reliable way to identify satellite cells is on the basis of their position using electron microscopy, although this method is not particularly convenient. Therefore, much interest has focused on good antibodies to identify specific proteins in quiescent (and activated) satellite cells in vivo at the light microscopic level (
Cell Surface Proteins.
One of the most useful markers appears to be the cell surface protein M-cadherin (M-cad) located at the interface of the satellite cell and underlying myofiber (reviewed in
A wide range of cell surface markers are routinely used for fluorescent activated cell sorting (FACS) analysis of hematopoetic (HSC), mesenchymal, and other stem cells (including a small side population, termed SP cells, that exclude Hoechst stain) (
Transcription Factors.
Expression of specific transcription factors is also a potentially useful marker for satellite cells. Myocyte nuclear factor (MNF) is present in quiescent and proliferating satellite cells and appears to be required for satellite cell function (
The important observation that expression of Pax7 is essential for satellite cell formation (
The skeletal muscle-specific transcription factors MyoD and Myf5 have been intensively studied because these are key factors for acquisition of myogenic identity (
Stem Cell Subpopulation of Satellite Cells?
It has been proposed that satellite cells contain a subpopulation of cells with stem-like characteristics that serve to replenish the satellite cells' compartment, and this is the subject of an excellent recent review (
In support of a myogenic stem cell in muscle, an exceptional capacity for high clonal expansion of a myogenic precursor is evidenced by many dystrophin-positive myofibers generated from a single revertant nucleus in mdx muscle in vivo (Partridge unpublished observations;
The surprising observation that cells extracted from skeletal muscle, using methods used to isolate and culture satellite cells, are remarkably effective at generating cells of the hematopoetic lineages (discussed below) initially suggested a potent multipotential capacity of satellite cells. However, it appeared equally likely that such lineage plasticity could be accounted for by contaminating stem cells in the interstitial connective tissue (of non-muscle origin) extracted by the same procedure. Indeed, there is now strong evidence for (at least) two distinct lines of stem cells extracted from skeletal muscle tissue (
In part this approach has been used to demonstrate that satellite cells on isolated myofibers in culture can also give rise to adipocytes or osteogenic cells (
Problems with Survival of Transplanted Cells and the Host Immune Response
For all cell transplantation therapies the introduced donor cells must be able to survive in their host environment. However, IM injection of cultured isolated (congenic) myoblasts in classical myoblast transfer therapy (MTT) shows that there is a massive and rapid necrosis of donor myoblasts, with over 90% dead within the first hour after injection (reviewed in
Massive death of injected donor cells is also recognized as a major problem with transplanted cardiomyocytes, especially in the inflammatory conditions that follow infarction (
Overall, although it is known that satellite cells give rise to myoblasts and result in formation of new skeletal muscle, the presence of a subpopulation of satellite cells that represents a true stem cell has yet to be demonstrated. While tissue culture studies enforce the idea of plasticity between myogenic, adipogenic, and osteogenic lineages, wider lineage plasticity of a true satellite (stem) cell remains to be proved. Although cells extracted from skeletal muscle clearly show stem cell properties and considerable lineage plasticity (as discussed below), these stem cells may not be derived from satellite cells but from other cells in the tissue.
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Myoblasts Originating from Cells Outside the Myofiber |
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The definition of stem cells is well reviewed elsewhere (
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Resident Cells in Non-muscle Tissues That Give Rise to Myoblasts
Ready Interconversion of Mesenchymal Cells.
Inter-stitial connective tissue contains many cell types. There is a plasticity of mesenchymal cells (in interstitial connective tissue) and interconversion among myoblasts, fibroblasts, adipocytes, chondroblasts, and osteoblasts has long been recognized and can be demonstrated in tissue culture under different conditions, as indicated in Table 2 (see also
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Mesenchymal Stem Cells.
At least two populations of mesenchymal stem cells (MSCs) that can be extracted from connective tissue of many species have been described extensively by Young and colleagues (
Dermal Fibroblasts and Stem Cells.
The ability of dermal fibroblasts to fuse spontaneously with developing myotubes was demonstrated for dysgenic muscle and resulted in genetic and functional rescue of the defective muscle (
There may be several kinds of stem cells resident in the dermis with different lineage capabilities (
Myofibroblasts.
Myofibroblasts are classically considered to be intermediate between fibroblasts and smooth muscle cells (reviewed in -actin, but they do not express cardiac or skeletal
-actin (
Vascular Tissue.
Similarly, lines of vascular smooth muscle cells in culture have been shown to express MyoD, myogenin, and several skeletal muscle-specific structural genes, but it should be noted that they do not express Myf5 and only some cell lines could fuse to form myotubes (
There is now strong in vivo evidence that skeletal muscle precursors can arise from cells in the vasculature (reviewed
Neural Tissue.
That neural tissue can give rise to skeletal muscle cells (including myotubes) has long been recognized (Table 1; and
Mysterious Myoid Cells in the Thymus and Other Ectopic Myogenic Cells.
It seems pertinent to examine the well-documented existence of skeletal muscle precursor cells in tissues (considered to be of neuroectodermal origin) such as the thymus and pineal. Although it has been known for over 30 years that skeletal myocytes are readily grown from such tissues in vitro, striated skeletal muscle cells are also formed in thymus tissue in vivo, especially in birds and reptiles and sometimes in humans (reviewed in
A recent report (
Circulating Bone Marrow-Derived Stem Cells
Bone marrow contains many cell types, including hematopoetic stem cells (HSCs), mesenchymal stem cells (MSCs), and endothelial stem cells (
To detect the contribution of circulating (donor) bone marrow cells to skeletal muscle formation in vivo, donor cells are now often identified in transplantation studies using a Y-chromosome (male)-specific probe to track donor male cells in female host tissues (
The recent demonstration that muscle nuclei can arise from bone marrow-derived precursor cells in vivo (
Of particular interest was the demonstration of hematopoietic lineages arising from stem cells extracted from skeletal muscle (
Bone marrow-derived stem cells can give rise to many other cell types apart from skeletal muscle, including cardiac muscle (
It is possible that circulating stem cells during development might give rise to many of the stem cells ascribed to specific tissues. In postnatal tissues, it is not clear whether bone marrow-derived stem cells contribute to cells in the vasculature or become resident in interstitial connective tissue. However, from studies of clearance of GFP-labeled lineage-negative blood cells, it has been calculated that 20,000100,000 HSCs/progenitors enter the blood every day, and these are rapidly sequestered (within minutes) into tissues (I. Weissman 2001, personal communication). These observations on circulating bone marrow-derived stem cells have attracted great interest because delivery of muscle precursors through the bloodstream represents an ideal route for distribution to all skeletal muscles. It should be considered that the use of umbilical cord blood may be an alternative and possibly superior source of multipotential stem cells (
Inducers to Enhance Recruitment of "Stem" Cells into the Myogenic Lineage
It has long been recognized that the immediate environment can radically alter the phenotype of a cell and re-direct its gene program. Complex interactions between cells and their extracellular matrix environment clearly play a central role in determining cell fate (
Such studies have understandably often been carried out in the artificial environment of tissue culture. The particular tissue culture conditions used can dictate the cell response and the lineage pathway. This is well illustrated by changes in oxygen levels. The proliferation of old (
One powerful inductive stimulus to convert pluripotent cells into a committed lineage is dexamethasone, whereas insulin (or insulin-like growth factors-I and -II) is required to induce myogenic expression in progenitor cells. It is interesting to note that many weeks are required for this conversion in vitro (
A particularly interesting factor is galectin-1, which induces conversion of primary cultures of mouse (
Overall, it appears that the wide range of non-myogenic sources of myoblasts (Table 1) fall broadly into four classes, as outlined in Table 3. Many of these are present in skeletal muscle tissue as potential alternative sources of myoblasts, while others (e.g., dermal fibroblasts) are not. Normally there appears to be a very low contribution of these alternative myogenic precursors to muscle formation in vivo. Much work remains to be done to clarify the relationship between these various myogenic precursor cell types. The identification of inductive agents to increase recruitment of non-myogenic (stem) cells into the skeletal muscle lineage (ideally in vivo), and factors that can increase the numbers of such cells in situ are two main challenges to overcome before potential clinical application can realistically be considered.
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Can Myonuclei Give Rise to Skeletal Myoblasts? |
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Traditionally, the answer to this question for mammalian muscle has been an unequivocal "NO." However, this idea is rather attractive because efficient salvage of myonuclei from damaged myofibers could provide a large pool of new myoblasts for muscle repair: There are two aspects to such "recycling" of myonuclei. One is the formation of new membranes around myonuclei and fragmentation of the myotube/myofiber to form individual mononucleated cells, and the second is re-initiation of DNA synthesis in "post-mitotic" nuclei. Exciting new developments from studies of amphibian myotubes in vivo and in vitro and from tissue culture experiments with mamalian myotubes unequivocally show that reversal of myonuclear fate is possible in some situations. However, little is really known about local conditions/inducers in damaged mammalian muscle regenerating in vivo that might facilitate such events.
Amphibians
It has long been recognized that adult urodele amphibians such as the newt, have a remarkable regenerative ability for many tissues, including whole limbs (
Mammals
Tantalizing EM observations of vesicles accumulating around myonuclei in damaged mouse myofibers (Fig 2) support the possibility of sequestration of myonuclei by newly formed membranes to form myoblasts, but this is only suggestive and certainly is not strong evidence because there are many alternative interpretations of such static images. These images correspond to sequestration of myonuclei demonstrated in the blastema of regenerating salamander muscles (
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In mouse myotubes in culture, re-initiation of DNA synthesis can occur by overexpression of the oncogenic SV40 big-T-antigen that inactivates tumor suppressor Rb and re-activates Cdc2-cyclin B, and this can lead to mitosis and cytokinesis (
Factors Involved in De-differentiation of Myonuclei
The intriguing question is, what are the in vivo factors that stimulate the de-differentiation of nuclei within myofibers and do such conditions occur in damaged mammalian skeletal muscle? Recently, information gleaned from studies of newt myogenesis has been applied to mammalian myotubes, and it appears that the two processes of DNA synthesis and fragmentation of the myotube/myofiber can operate independently (reviewed in
Disassembly of myotubes also results from ectopic expression of the transciptional repressor protein msx1, which is implicated in de-differentiation: msx-induced cleavage of C2C12 myotubes (seen initially in about 9% of treated myotubes) resulted in the formation of either smaller myotubes or myoblasts (5.4%) capable of replication (
These fascinating observations show that the muscle nuclei in mature mammalian myotubes (like their amphibian counterparts) are capable of de-differentiating to form cells that are like myoblasts or multipotential cells, when exposed to appropriate signals. The extent to which this might normally occur in damaged skeletal muscle remains an open question. Such reversal of the post-mitotic status of myonuclei (in the highly differentiated muscle fiber) also has implications for cardiac myocytes.
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Cardiac Muscle |
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Growth, Damage, and Repair
Hypertrophy, Polyploidy, and Multinucleation.
Cardiac and skeletal muscles have a similar sophisticated organization of contractile proteins into sarcomeres and are collectively referred to as striated muscles. Growth of the heart is generally characterized by division of muscle cells during the embryonic stages of life, followed after birth by entry into a post-mitotic state. Therefore, growth of the heart during normal development and in cases of cardiac disease requires enlargement of individual cardiomyocytes (hypertrophy) rather than proliferation of post-mitotic cardiac myocytes. The average size of mature cardiomyocytes in a wide range of species appears to be 1118 µm (
Lack of Regeneration of Cardiac Muscle. In a normal situation, this hypertrophic growth is sufficient to maintain adequate cardiac myocyte function, but significant problems arise when the myocytes are damaged in conditions such as cardiac infarction. The postnatal capacity for cell replication during growth and regeneration of cardiac and skeletal muscle is markedly different. As outlined above, skeletal muscle cells are multinucleated and can readily regenerate from precursor cells (satellite cells/myoblasts), whereas until very recently it was established dogma that postnatal cardiac muscle was incapable of tissue repair. This was because (like skeletal myofibers) the mature cardiac cells were post-mitotic and incapable of replication (either in vivo or in vitro) but (in marked contrast to skeletal muscle) there appeared to be no reserve precursor cells. Therefore, damaged heart muscle was replaced by scar tissue, presenting a major clinical problem (Fig 3B). However, this dogma is now being replaced by the idea that there is some in vivo proliferation of cardiomyocytes after damage (see below): whether this occurs from pre-existing mature cardiomyocytes or from local stem cells is now an area of intense research.
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Strategies for Repair.
When confronted with the problem of heart damage after infarction, replacement of myocytes is the ideal scenario. There is increasing interest in cell transplantation as a potential therapy for cardiovascular disease (
It should be emphasized that, to be clinically effective, the enhancement of cardiomyocyte proliferation after damage must be rapid if the animal is to survive any acute insult that disrupts heart function through damage to the individual cardiac myocytes. In cases in which there is chronic damage to the heart muscle, the proliferation might need to be sustained to slowly but continually replace myocytes as necessary during the course of the disease. Whatever the source of the cells and the use to which they are put, a concurrent revascularization must also keep pace with repopulation of the infarct to ensure viability of the repaired region and prevent further scar tissue formation. Finally, the newly formed myocardium must integrate into the existing myocardial wall if it is to assume the function of the tissue it replaces. All of this must occur while the heart continues to beat and perform the essential work of supplying blood throughout the organism. Furthermore, even small areas of imperfectly integrated tissues are likely to severely alter electrical conduction and syncytial contraction of the heart, with long-term life-threatening consequences. This is in marked contrast to the situation in skeletal muscle where the tissue can rest during repair. Here we discuss the historical use of transplanted skeletal muscle cells and fetal cardiomyocytes to replace damaged myocardium, re-initiation of mitosis in mature "post-mitotic" cardiomyocytes, and formation of cardiomyocytes from stem cells (endogenous and exogenous).
Transplantation of Skeletal or Fetal Cardiac Muscle Cells into Hearts
Skeletal Muscle.
Attempts to use autologous skeletal muscle to repair damaged hearts has been attempted by relocating (from their normal position) wraps of whole sheets of the latissimus dorsi muscle to supplement myocardial function (
Alternatively, transplantation of isolated cultured myoblasts has been used to try to restore muscle function in hearts (
Cardiomyocytes.
Attention has recently shifted from such studies using skeletal muscle to the use of cardiomyocytes, and especially stem cells, as a source of replacement muscle. Because traditionally mature cardiomyocytes are considered to be incapable of cell replication, the donor cardiomyocytes to date have largely been of embryonic/fetal origin. Although some experiments in animal models report successful engraftment and maturation of embryonic cardiomyocytes in normal and injured hearts (
The use of skeletal muscle cells to repair damaged heart muscle has had some success, and experiments are ongoing. A more attractive approach is the use of donor cardiomyocytes, but mixed results have been obtained with donor fetal/embryonic/neonatal cardiomyocytes and the use of such donor cells in humans raises major ethical issues.
Proliferation of Mature Cardiomyocytes
As outlined above, in contrast to the well-documented capacity for regeneration of (post-mitotic) skeletal muscle from muscle precursor (satellite) cells, it has long been considered that proliferation of cardiac myocytes ceases permanently soon after birth and that there is no replacement with new cardiomyocytes after damage. Although binucleated cardiomyocytes apparently arise by nuclear division, cytokinesis is also required to generate new cardiomyocytes. It now appears that there is a low level of myocyte proliferation (accompanied by cytokinesis) in the postnatal heart (
Many studies have investigated the molecular basis of the "block" to proliferation that occurs in most cardiomyocytes shortly after birth. Increased cardiomyocyte replication is reported after increasing IGF-I levels (
Beyond nuclear replication is the necessity for generation of daughter nuclei (rather than increased ploidy of the original nucleus) and cytokinesis to generate new cardiomyocytes. Therefore, factors that stimulate both of these events need to be investigated. It is not clear whether reversal of the apparently post-mitotic state of cardiomyocytes and cleavage of this highly organized muscle cell may have parallels with the reversal of the post-mitotic status of myonuclei in the sarcoplasm of myotubes/myofibers (as discussed above).
Overall, in contrast to long-standing dogma, there is now evidence to support some proliferation of postnatal mammalian cardiomyocytes in vivo, especially after heart damage. It remains a major challenge to achieve significant proliferation of such postnatal mammalian heart cells. Under the circumstances, an attractive alternative is the use of stem cells to generate new cardiomyocytes.
Cardiomyocytes from Stem Cells
Bone Marrow-Derived Stem Cells.
Since the 1999 demonstration of cardiac muscle formation from circulating bone-marrow cells (
In experimental infarcted hearts in adult mice, cardiomyocytes and vascular cells can be formed in vivo from circulating mouse bone marrow stem cells (
Although the formation of vascular cells such as endothelial cells may not appear directly relevant to the attempts to repair damaged hearts, it should be noted that an adequate blood and oxygen supply for newly seeded cardiomyocytes is critical for their survival. Therefore, the ability of transplanted bone marrow stem cells to form the cells of the vasculature is another important advantage to the use of a totipotent cell type (
Female hearts transplanted into male recipients provide the opportunity to assess the contribution of host male (Y-chromosome-positive) cells to undamaged myocardium of the donor heart in a clinical context. In contrast with earlier studies,
Endothelial Cells.
The interesting demonstration of good conversion (trans-differentiation) of mouse and human endothelial cells into cardiomyocytes in tissue co-culture and in vivo (
Embryonic Stem Cells.
It is well established that murine embryonic stem (ES) cells can give rise to cardiomyocytes in vitro and in vivo (
Neural and Hepatocyte Stem Cells.
Other studies have shown that a clonal hepatocyte stem cell line WB-F344, when transplanted into the hearts of mice in vivo was able to differentiate into cardiac myocytes (
In summary, given the time constraints for repair after acute myocardial infarction, delivery of pre-differentiated cells (cardiomyocyte and vascular cells possibly derived from stem cells) appears desirable. Local delivery of these cells results in direct seeding of the damaged zone, but we need to understand more about how the microenvironment promotes cell differentiation so that this can be exploited. Local delivery might be improved if such cells were engineered into 3D grafts on appropriate matrix/biomaterials.
Systemic delivery of stem cells is relatively non-invasive and remains an attractive option. This relies heavily on the ability of cells to home to damaged tissue. However, little is known yet about the factors responsible for such specific tissue targeting. Furthermore, expansion of the stem cell population in the damaged heart and differentiation into functional cardiomyocytes are required, and the local conditions that dictate this need to be elucidated.
For heart tissue there have been some rather promising results in the past 3 years with bone marrow and endothelial stem cell replacement of cardiomyocytes and vascular cells. These studies need to be firmly substantiated in vivo and carefully evaluated for humans. It is early days and, in the absence of solid in vivo data, it seems premature to extend such studies to the clinical situation.
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Acknowledgments |
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The research on myoblast transfer therapy and stem cells was made possible by grants from the Association Francaise Contre les Myopathies (MDG), the International Duchenne Parent Project (MDG), and the Muscular Dystrophy Association of America (MDG and NR). Recent funding from the Heart Foundation of Australia (MDG, MB, and NR) is also acknowledged.
The generous comments and unpublished data of colleagues are gratefully acknowledged. We are particular grateful to Zipora YablonkaReuveni for helpful criticism.
Received for publication December 19, 2000; accepted January 15, 2002.
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