Regeneration of dystrophin-expressing myocytes in the mdx heart by skeletal muscle stem cells

Payne, Thomas R.; Oshima, Hideki; Sakai, Tetsuro; Ling, Yibei; Gharaibeh, Burhan; Cummins, James; Huard, Johnny

doi:10.1038/sj.gt.3302521

Cited by 69 publications

(58 citation statements)

References 53 publications

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“…Previously, we found only low levels of in vivo MDSC differentiation toward a cardiac phenotype 13,14 that was confirmed in the current study, with less than 1 out of 100 injected cells coexpressing cTnI and fsMHC at 6 or 12 weeks after injection (data not shown). There were no differences observed between the MS and NS cells (6 weeks: n = 3 per treatment, p = 0.72; 12 weeks: n = 5 per treatment, p = 0.95; data not shown).…”

Section: Mechanical Stimulation Does Not Affect Cell Survival and Carsupporting

confidence: 61%

“…[9][10][11][12][13] MDSCs have been shown to regenerate cardiac and skeletal muscle in a more effective manner than myoblasts. 13,14 While stem cell transplantation has produced promising initial results, many of the stem cell-mediated improvements in cardiac function are only transient. One main barrier to successful cardiac cell therapy is low cell survival due to initial cell death postimplantation, subsequent biological cell death, 15 and immune-mediated cell destruction.…”

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confidence: 99%

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Mechanical Loading of Stem Cells for Improvement of Transplantation Outcome in a Model of Acute Myocardial Infarction: The Role of Loading History

Cassino

Drowley

Okada

et al. 2012

Tissue Engineering Part A

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Stem cell therapy for tissue repair is a rapidly evolving field and the factors that dictate the physiological responsiveness of stem cells remain under intense investigation. In this study we hypothesized that the mechanical loading history of muscle-derived stem cells (MDSCs) would significantly impact MDSC survival, host tissue angiogenesis, and myocardial function after MDSC transplantation into acutely infarcted myocardium. Mice with acute myocardial infarction by permanent left coronary artery ligation were injected with either nonstimulated (NS) or mechanically stimulated (MS) MDSCs. Mechanical stimulation consisted of stretching the cells with equibiaxial stretch with a magnitude of 10% and frequency of 0.5 Hz. MS cell-transplanted hearts showed improved cardiac contractility, increased numbers of host CD31 + cells, and decreased fibrosis, in the peri-infarct region, compared to the hearts treated with NS MDSCs. MS MDSCs displayed higher vascular endothelial growth factor expression than NS cells in vitro. These findings highlight an important role for cyclic mechanical loading preconditioning of donor MDSCs in optimizing MDSC transplantation for myocardial repair.

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Section: Mechanical Stimulation Does Not Affect Cell Survival and Carsupporting

confidence: 61%

mentioning

confidence: 99%

Mechanical Loading of Stem Cells for Improvement of Transplantation Outcome in a Model of Acute Myocardial Infarction: The Role of Loading History

Cassino

Drowley

Okada

et al. 2012

Tissue Engineering Part A

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“…M-mode tracings were used to measure the EDD and ESD as previously described ( Figure 7A; Oshima et al, 2005;Payne et al, 2007). No differences in left ventricular cavity size as measured by the area of the myocardium during diastole were observed among all three groups as assessed by EDA ( Figure 7B), a result commonly observed in this type of experiments Payne et al, 2005). As assessed by FS and FAC, infarcted hearts injected with MDSCs had significantly better systolic function relative to the infarcted hearts injected with both MDSCs treated with DEM and PBS (p Ͻ 0.05).…”

Section: Decreasing the Gsh Levels Of Mdscs Decreases The Regeneratiomentioning

confidence: 89%

Antioxidant Levels Represent a Major Determinant in the Regenerative Capacity of Muscle Stem Cells

Urish

Vella

Okada³

et al. 2009

MBoC

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Stem cells are classically defined by their multipotent, long-term proliferation, and self-renewal capabilities. Here, we show that increased antioxidant capacity represents an additional functional characteristic of muscle-derived stem cells (MDSCs). Seeking to understand the superior regenerative capacity of MDSCs compared with myoblasts in cardiac and skeletal muscle transplantation, our group hypothesized that survival of the oxidative and inflammatory stress inherent to transplantation may play an important role. Evidence of increased enzymatic and nonenzymatic antioxidant capacity of MDSCs were observed in terms of higher levels of superoxide dismutase and glutathione, which appears to confer a differentiation and survival advantage. Further when glutathione levels of the MDSCs are lowered to that of myoblasts, the transplantation advantage of MDSCs over myoblasts is lost when transplanted into both skeletal and cardiac muscles. These findings elucidate an important cause for the superior regenerative capacity of MDSCs, and provide functional evidence for the emerging role of antioxidant capacity as a critical property for MDSC survival post-transplantation. INTRODUCTIONMyogenic cell transplantation has been proposed as a promising therapeutic approach in the treatment of skeletal and cardiac muscle injury. Early studies of myoblast transplantation into dystrophic skeletal muscle yielded limited regeneration of dystrophin-expressing muscle fibers (Beauchamp et al., 1994;Gussoni et al., 1997;Qu-Petersen et al., 2002). Similarly, given the limited regenerative ability of cardiac muscle, cell transplantation has been proposed as an alternative to heart transplantation (Assmus et al., 2006;Lunde et al., 2006;Schachinger et al., 2006).A major obstacle in both cardiac and skeletal myogenic therapies is the poor rate of engraftment of myogenic cells after transplantation (Taylor et al., 1998;Oshima et al., 2005). In skeletal muscle, numerous groups have observed a rapid inflammatory response that appears to contribute to rapid cell loss and limit therapeutic success (Beauchamp et al., 1994;Gussoni et al., 1997;Beauchamp et al., 1999). Multiple groups have postulated that the small number of injected cells that survive transplantation in both cardiac and skeletal muscle may represent a special subpopulation of stem-like cells (Qu et al., 1998;Beauchamp et al., 1999;Qu-Petersen et al., 2002).For these reasons, our group attempted to isolate this putative subpopulation of cells using a modified preplate technique. This procedure was initially developed to purify myoblasts from nonmyogenic cells, including fibroblasts, of whole tissue preparations based on the differential adhesion characteristics of the cells to a collagen coated flask (Rando and Blau, 1994). Our group modified this technique to isolate various populations of myogenic cells, including a population of early adhering preplate (EP) cells and a late adhering preplate (LP) cell population from which a subpopulation of long-term proliferating (LTP) cells,...

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“…The strategy is to deliver the protein missing from DMD muscle through the fusion of dystrophin-expressing myogenic cells with dystrophic myofibres. There is growing success in testing this modality of treatment (Chretien et al, 2005;Cossu and Mavilio, 2000;Cousins et al, 2004;Gussoni et al, 1999;Huard et al, 1994;Ikezawa et al, 2003;Jankowski and Huard, 2004;Li et al, 2005b;Liu et al, 2005;Partridge et al, 1989;Payne et al, 2005;Qu-Petersen et al, 2002).…”

Section: (2) Satellite Cells As a Conveyance In Skeletal Muscle Plastmentioning

confidence: 99%

The satellite cell as a companion in skeletal muscle plasticity:currency, conveyance, clue, connector and colander

Anderson

2006

Journal of Experimental Biology

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THE JOURNAL OF EXPERIMENTAL BIOLOGY 2277 Satellite cells in muscle plasticity formed cells fusing to form myoblasts and finally multinucleated muscle fibres.'That conference was a landmark in studies of the satellite cell and muscle regeneration, and was attended by many of the notable and pioneering contributors to the field of muscle development and muscle regeneration. Muir summarized the debate on a working definition of the satellite cell, as follows (Muir, 1970):'The satellite cell of striated muscle can be defined as a mononucleated cell, whose cytoplasm does not contain myofilaments, and which is enclosed by or lies within the basement membrane component of the sarcolemma of the striated muscle fibre. This definition does not exclude cells which are partially or completely separated from the muscle fibre plasma membrane by extensions of the basement membrane, providing that the basement membrane forms a complete investment of their outer surfaces. ' Although there were presentations detailing the observed uptake of 3 H-thymidine into nuclei of satellite cells (Hay, 1970), the role of satellite cells as precursors was not fully established in 1969. In fact there was still very strong debate that a muscle fibre could fragment into blastema cells that led to new formation of muscle. Even at this time, there was more than one paper on the appearance of osteogenic and chondrogenic tissues from minces of muscle replaced under the skin, and a report of muscle fibre nuclei contributed by a labelled connective tissue grafted into a salamander limb during regeneration (Steen, 1970).It wasn't until two seminal reports from the laboratory of Dr Charles Leblond at McGill University (Moss and Leblond, 1970;Moss and Leblond, 1971) that skeletal muscle satellite cells were convincingly identified as the source of precursor cells that proliferate and fuse to form new skeletal muscle fibres. Time-course studies of labelled nuclei in growing muscle showed that satellite cells were the only muscle cells that had incorporated 3 H-thymidine. The report followed work on colchicine-treated rats (MacConnachie et al., 1964) that showed mitotic figures only in the peripheral 'satellite' position on muscle fibres. The idea that muscle fibre nuclei give rise to the increasing number of myonuclei during the growth was convincingly ruled out (Enesco and Puddy, 1964). The notion that satellite cells contribute these domains to a growing or regenerating fibre, one at a time, is daunting in light of the expenditure of proliferative energy and fusion events. However, it speaks strongly to one of the major roles of satellite cells as a currency of muscle (see below). Satellite cells were also observed on intrafusal fibres (Katz, 1961). Two types of satellite cells were identified on these socalled muscle spindle fibres and were distinguished from those on extrafusal fibres (Maynard and Cooper, 1973), although at least one would now be called a myoblast.Although typically quiescent in normal adult muscle, satellite cells are generally con...

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Regeneration of dystrophin-expressing myocytes in the mdx heart by skeletal muscle stem cells

Cited by 69 publications

References 53 publications

Mechanical Loading of Stem Cells for Improvement of Transplantation Outcome in a Model of Acute Myocardial Infarction: The Role of Loading History

Mechanical Loading of Stem Cells for Improvement of Transplantation Outcome in a Model of Acute Myocardial Infarction: The Role of Loading History

Antioxidant Levels Represent a Major Determinant in the Regenerative Capacity of Muscle Stem Cells

The satellite cell as a companion in skeletal muscle plasticity:currency, conveyance, clue, connector and colander

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