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RESEARCH COMMUNICATION
1 Department of Molecular, Cellular, and Developmental Biology, University of Colorado at Boulder, Boulder, Colorado 80309, USA; 2 Cutaneous Biology Research Center, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts 02129, USA; 3 Neuroscience Center, Department of Biosciences, and Institute of Biotechnology, University of Helsinki, Helsinki FIN-00014, Finland; 4 Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA
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[Keywords: Muscle regeneration; satellite cell; stem cell; myogenesis]
Received April 23, 2004; revised version accepted July 15, 2004.
; Hawke and Garry 2001). The molecular mechanisms controlling this process are not understood, particularly the signaling pathways operating early in regeneration that lead to the initial activation and proliferation of the satellite cells and later to their induction of the myogenic program.
The receptor tyrosine kinase c-met and/or fibroblast growth factor (FGF)-dependent receptor tyrosine kinases are currently the best candidates for transducing these early satellite cell signaling events (Allen et al. 1995; Cornelison and Wold 1997; Tatsumi et al. 1998). Both receptors are absolutely dependent on heparan sulfate to form a high affinity ternary complex capable of transducing intracellular signaling events (Carey 1997; Ornitz 2000; Rapraeger 2000) and thus, it is significant that quiescent satellite cells also express the transmembrane heparin sulfate proteoglycans (HSPGs) syndecan-3 and syndecan-4 (Cornelison et al. 2001). There are four related members of the syndecan family, which are highly similar at the protein level through the transmembrane and intracellular domains but divergent in their extracellular domains (for review, see Zimmermann and David 1999). Although skeletal muscle cell lines express all four syndecan family members (Larrain et al. 1997; Olguin and Brandan 2001), developing myoblasts in the embryo express syndecan-1, syndecan-3, and syndecan-4 (Cornelison et al. 2001; Olguin and Brandan 2001), and adult satellite cells express only syndecan-3 and syndecan-4 (Cornelison et al. 2001). Previously, we have shown that disruption of heparan sulfate in cultured primary satellite cells results in delayed activation and delayed initiation of myogenesis (Cornelison et al. 2001). However, this effect could not be definitively attributed to the inactivation of any specific HSPG. Therefore, we examined the skeletal muscle and satellite cell behavior from mice carrying homozygous deletions of either syndecan-3 or syndecan-4. Unexpectedly, we found skeletal muscle and satellite cell defects that are unique to the loss of each syndecan, suggesting that they function to perform distinct yet essential roles in both skeletal muscle development and skeletal muscle regeneration.
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Results and Discussion |
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TopAbstractResults and DiscussionMaterials and methodsAcknowledgmentsReferences |
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) and learning and memory abnormalities (Kaksonen et al. 2002); additionally, their hindlimb locomotion is impaired in our colony. Adult muscle in wild-type mice is characterized by uniformly packed myofibers of consistent caliber, a smooth and regular basal lamina, and the presence of sublaminar quiescent satellite cells identified by c-met staining (Fig. 1A-C). In contrast, syndecan-3-/- adult muscle possesses extensive fatty infiltrates (fibrosis) both between and within muscle fibers (Fig. 1D). This phenotype resembles that common in other dystrophic muscle (Watchko et al. 2002). Innervation, as determined by the presence of neurofilament-labeled peripheral nerve bundles (Fig. 1E) and 
-bungarotoxin labeling of motor endplates (Supplementary Fig. 1), is qualitatively and quantitatively similar to wild type (Fig. 1B; Supplementary Fig. 1). Sublaminar (quiescent) satellite cells (Fig. 1F) appear morphologically similar to wild type from their size, position, and marker gene expression. A striking difference from wild type is the >15-fold increase in the number of regenerating myofibers indicated by centrally located myonuclei (Fig. 1J) in the syndecan-3-/- muscle, suggesting that regeneration is ongoing in the absence of experimental damage. This is consistent with the locomotion defects we observe in syndecan-3-/- mice and suggests that deletion of syndecan-3 may be implicated in a novel form of muscular dystrophy.
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) and defects in fibroblast adhesion and migration (Wilcox-Adelman et al. 2002), have a normal gait and do not display signs of chronic muscle regeneration. Examination of the tissue shows adipose infiltrates between but not within muscle fibers (Fig. 1G), as well as the presence of normal peripheral nerve bundles (Fig. 1H) and normal motor endplate morphology (Supplementary Fig. 1). Although sublaminar satellite cells are present, they apparently display reduced levels of c-met (Fig. 1I) and syndecan-3 staining (data not shown). We also observe a reduction in thickness as well as an apparent disorganization of the myofiber basal laminae (Fig. 1, cf. C,F and I). Additionally, unlike syndecan-3-/- muscle, syndecan-4-/- muscle exhibits only a slight increase in centrally located nuclei (Fig. 1J), suggesting that regeneration is not ongoing. Thus, our initial phenotypic characterization suggests that syndecan-3 and syndecan-4, surprisingly, appear to perform quite distinct functions in skeletal muscle development. When single fibers from syndecan-3-/- muscle are examined, both differentiated myonuclei and satellite cell nuclei are present in great excess over wild-type counts (Fig. 1K,L), although neither fiber number per muscle nor average fiber diameter changes significantly (data not shown). When satellite cells (c-met-positive, myofiber-associated cells) and DAPI-stained myofiber nuclei are counted at 24 h postharvest (prior to the first satellite cell division) and the number of satellite cells per 100 myofiber nuclei is determined, a 6.7-fold increase over wild type is observed (Fig. 1K). When satellite cells and myonuclei are counted per millimeter myofiber length to control for the increase in myonuclear number, syndecan-3-/- satellite cells exceed wild-type cells by greater than fivefold (Fig. 1K) and syndecan-3-/- myonuclei exceed wild-type by at least twofold (Fig. 1L). This increase in both myonuclear and satellite cell numbers is particularly intriguing because it may indicate a possible inhibitory role for syndecan-3 signaling in myogenic precursors contributing to both the differentiated muscle and satellite cell. In contrast, the number of syndecan-4-/- satellite cells (Fig. 1K) and myonuclei (Fig. 1L) is indistinguishable from wild type, suggesting that such a putative role in developmental control of cell number is unique to syndecan-3. To determine if loss of one satellite cell-specific syndecan affected expression of the other syndecan, we examined expression of each syndecan in the opposite null phenotype. Expression of syndecan-4 in syndecan-3-/- fiber-associated satellite cells was comparable to syndecan-4 expression in wild type (Supplementary Fig. 2), whereas syndecan-3 expression in syndecan-4-/- satellite cells was, as seen in section stains, slightly reduced compared with wild type (Supplementary Fig. 2).
When examined in myofiber culture, wild-type and syndecan-3-/- satellite cells are activated by 24 h postharvest, on the basis of emergence from beneath the basal lamina and expansion of their cytoplasm (Fig. 2A,D). Wild-type (Fig. 2B,C) and syndecan-3-null cells (Fig. 2E,F) both proliferate and express myogenic regulatory factors with normal timing. However, quantitative analysis of the satellite cells depicted in Figure 2 reveals that significantly fewer syndecan-3-/- satellite cells express MyoD than do equivalent wild-type cells (Fig. 3). The reduction in MyoD protein is frequently accompanied by mislocalization of MyoD to the cytoplasm of the satellite cell (Fig. 2, cf. C and F) that appears to be exacerbated over time (Fig. 3). Both the cause and the potential effects of this mislocalization of a transcription factor essential for appropriate satellite cell myogenesis (Cornelison et al. 2000) are unknown at this point.
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). The failure of syndecan-3-/- and syndecan-4-/- satellite cells to express nuclear MyoD appropriately could be expected to result in defects in differentiation. We found that when deprived of association with the host myofiber, more extensive defects in satellite cell function emerge. Although wild-type satellite cell colonies widely express nuclear MyoD and fuse to form elongated, multinucleate myotubes (Fig. 4A and insets) that express terminal differentiation markers such as myosin heavy chain (Fig. 4B), both syndecan-null mutants display defects in gene expression and subsequent differentiation. Syndecan-3-/- cells proliferate extensively in mass culture but form large, irregular syncytia when attempting to differentiate (Fig. 4C). Furthermore, these cells fail to express MyoD protein either in the nucleus or in the cytoplasm (Fig. 4C and insets) or myosin heavy chain (Fig. 4D), demonstrating a more severe phenotype than that seen on intact myofibers and a general failure to differentiate appropriately in culture. In mass culture, syndecan-4-/- satellite cells fail at all aspects of the satellite cell program. Compared with wild-type and syndecan-3-/- cultures, syndecan-4-/- satellite cells are delayed by an additional 48-96 h before adherent colonies become visible on the culture dish, consistent with the activation and migration defects observed in fiber culture. These cells will continue to express the satellite cell marker c-met, but their myogenic progression is severely impaired: Like syndecan-3-/- cells, they fail to express MyoD (Fig. 4E and insets) or myosin heavy chain (Fig. 4F) and they also fail to fuse with one another (Fig. 4E,F).
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An appealing hypothesis to explain the differences in phenotype between syndecan-3-/- and syndecan-4-/- satellite cells would be that the individual syndecans are differentially required for binding and signal transduction of different growth factors. The most probable candidates for such signals, based on their known roles in satellite cell biology and the observed results when syndecan-null satellite cells are treated with heparin, are members of the FGF family and hepatocyte growth factor (HGF). Surprisingly, when satellite cells cultured from wild-type, syndecan-3-/-, and syndecan-4-/- mice are starved, then stimulated with FGF-2 or HGF, either alone or preincubated with soluble heparin, differences in signaling specific to FGF or HGF were not observed. Instead, signaling for both FGF and HGF was similarly affected and dependent on the genotype of the cells. Although wild-type and syndecan-3-/- cells respond to both FGF-2 and HGF by rapid phosphorylation of the ERK1/2 MAP (mitogen-activated protein) kinases, syndecan-3-/- cells exhibit a greater than twofold increase in levels of ERK phosphorylation over wild type (Supplementary Fig. 3A). In contrast to wild-type and syndecan-3-/- cells, syndecan-4-/- cells show almost undetectable ERK phosphorylation in response to either FGF or HGF (Supplementary Fig. 3A), indicating a severe impairment of both FGF- and HGF-mediated activation of ERK1/2. When global levels of tyrosine phosphorylation in growing cells of each genotype are examined, syndecan-3-/- cells remarkably display an overall increase in phosphorylation (Supplementary Fig. 3B), whereas syndecan-4-/- cells are similar to wild type. Thus, it appears that syndecan-3-null cells may be missing a key inhibitory signal resulting in a general overstimulation of tyrosine phosphorylation, consistent with the satellite cell and myonuclear hyperplasia. Syndecan-4-/- cells appear incompetent for ERK activation through either FGF or HGF receptor tyrosine kinases, yet the global pattern of tyrosine phosphorylation is similar to wild type. This is consistent with the inability of syndecan-4-/- satellite cells to initially activate and proliferate on myofiber harvest.
These results suggest both the presence of unique defects in syndecan-3-/- and syndecan-4-/- satellite cells, and a requirement for matrix factors not present in ex vivo culture for successful satellite cell function in these cells. Thus, to extend the characterization of the mutant phenotypes and to test this requirement in an in vivo setting, we have analyzed syndecan-3-/- and syndecan-4-/- tibialis anterior (TA) muscle following barium chloride-induced myonecrosis (Caldwell et al. 1990). Although saline injections failed to induce damage or subsequent regeneration in any genotype (Fig. 5A-C), injection of 1.2% barium chloride into the TA muscle rapidly induced myonecrosis. At 5 d postinjury in wild-type TA muscle, we consistently observe multiple regenerated myofibers (small-caliber fibers with centrally located nuclei) that appear well organized (Fig. 5D). Syndecan-3-/- TA muscle, after 5 d, appears comparable to wild type (Fig. 5E), whereas syndecan-4-/- TA muscle 5 d postinjury is characterized by poorly organized, irregularly shaped and sized syncytia with highly variable nucleation (Fig. 5F). After 12 d of regeneration, wild-type TA muscle has continued to regenerate, producing closely packed nascent myofibers (Fig. 5G), as has syndecan-3-/- TA muscle (Fig. 5H); however, syndecan-3-/--regenerated TA muscle is also characterized by extensive myonuclear and satellite cell hyperplasia that appears similar to all limb muscle formed during development (data not shown). In marked contrast, after 12 d of regeneration, syndecan-4-/- TA muscle has not regenerated and is composed primarily of disorganized, nonfunctional myofibers and nonmuscle scar tissue (Fig. 5I). Note that some fibers that appear are so disorganized that they do not align with the axis of the former myofibers (asterisks, Fig. 5I). Unlike wild-type and syndecan-3-/- mice, which will begin to bear weight on the injured leg within 2-3 d after injury, injured syndecan-4-/- animals continue to favor the injured leg for at least 4 wk postinjury (data not shown). Interestingly, the expression patterns of syndecan-3 and syndecan-4 diverge during regeneration in wild-type muscle, the first such instance we have observed. During acute regeneration, syndecan-4 immunoreactivity is increased in the activated satellite cells, whereas syndecan-3 immunoreactivity becomes preferentially localized to the nascent myofibers (data not shown). Following regeneration, the normal pattern of coexpression on quiescent satellite cells is reestablished.
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). Because the satellite cells and myonuclei exhibit a similar hyperplasia, our data would support the hypothesis that differentiated muscle precursors and satellite cell precursors share common regulatory mechanisms and may either share a common progenitor or may occupy a common niche during development. The disparities observed between the myogenic capacity of syndecan-3-/- satellite cells in vivo (as demonstrated by the high percentage of regenerating myofibers in uninjured muscle and after induced regeneration), in fiber culture, and in adherent culture suggest a requirement for additional matrix factors to achieve appropriate myogenesis in syndecan-3-/- satellite cells. This is likely to include heparan sulfate provided by other HSPGs such as perlecan, which is expressed at higher levels in the matrix of syndecan-3-/- muscle (data not shown). This conclusion is consistent with the rescue of differentiated morphology and gene expression in syndecan-3-/- satellite cells by addition of exogenous heparin. In contrast, whereas syndecan-4-/- muscle tissue is significantly less affected than syndecan-3-/- muscle, syndecan-4-/- satellite cells are much more severely impaired than syndecan-3-/- cells, as they both fail to behave normally in culture and fail to regenerate functional muscle in vivo. Rescue of the syndecan-4-/- cells in mass culture by exogenous heparin is also less efficient than in syndecan-3-/- satellite cells.
Our data demonstrate that the surrounding environment is critical for satellite cell proliferation and differentiation. These experiments have demonstrated that syndecan-3 and syndecan-4 play distinct roles in muscle development as well as in satellite cell physiology and that the molecular and cellular consequences of deleting either syndecan are both complex and context dependent. We have initiated mRNA analysis of quiescent and activated satellite cells directly harvested from intact or injured hindlimb muscle of wild-type and syndecan-null mice. Preliminary analysis of these data suggests that syndecan-3-/- and syndecan-4-/- satellite cells differ significantly from each other as well as from wild-type satellite cells. Syndecan-3-/- cells most resemble wild-type cells (D. Cornelison, T. Cheung, X. Liu, and B. Olwin, in prep.), as might be expected from their cellular phenotype. Further analysis of the gene expression profiles between the syndecan-3-null and syndecan-4-null satellite cells, coupled with biochemical characterization of affected signaling pathways, is expected to identify molecular differences between these genotypes critical for satellite cell function.
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Materials and methods |
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TopAbstractResults and DiscussionMaterials and methodsAcknowledgmentsReferences |
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All genotypes of mice used were housed in the same pathogen-free facility at the University of Colorado; all mice used were females between 80 and 160 d of age. Wild-type mice were C57Bl/6xDBA2 (B6D2F1; Jackson Labs); syndecan-3-/- mice carry the homozygous deletion of syndecan-3 on a C57Bl/6 background (Kaksonen et al. 2002), and syndecan-4-/- mice carry the homozygous deletion of syndecan-4 on a C57Bl/6 background (Echtermeyer et al. 2001).
Sectioning and immunostaining of fixed frozen sections
For Oil Red O staining, sections were equilibrated into propylene glycol, stained with 0.7% Oil Red O in propylene glycol, destained in 85% propylene glycol, and extensively washed with water. For fluorescent staining, sections were blocked in 10% BlokHen (Aves) if chicken anti-syndecan-4 was to be used, and/or 10% normal goat serum in phosphate-buffered saline. Primary antibodies used were rabbit anti-laminin (Sigma) at 1:200, mouse anti-neurofilament (Sigma) at 1:100, rabbit anti-syndecan-3 at 1:100, chicken anti-syndecan-4 at 1:1500, rabbit anti-c-met (Santa Cruz) at 1:100, mouse anti-MyoD (Novocastra) at 1:10, and mouse anti-myosin heavy chain (MF20) neat. Secondary antibodies conjugated to Alexa 488 or Alexa 594 (Molecular Probes) were used at 1:500.
Myofiber preparation and staining
Single myofibers were isolated, cultured, and stained as described previously (Cornelison et al. 2001), except that the culture medium used was Ham's F-12 supplemented with 15% horse serum and 0.5 nM FGF-2. Fibers at designated times after harvest were fixed and stained with antibodies as described earlier.
Adherent culture
Single myofibers 24 h after isolation were plated in growth medium in tissue culture dishes containing gelatin-coated glass coverslips and left undisturbed for 6 d. Soluble heparin (Sigma) was added as indicated from a 50 mg/mL stock. The colonies formed by emigrating satellite cells on the coverslips were fixed and stained as described earlier.
In vivo regeneration
Mice were anesthetized with 5% Avertin (175 µL/mouse). Left TA muscles were injected with 50 µL sterile saline and the contralateral TA muscles were injected with 50 µL 1.2% BaCl2 in sterile saline. Mice were allowed to recover for 5 or 12 d, then injected muscles were harvested for sectioning and staining as described earlier.
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Footnotes |
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Article and publication are at http://www.genesdev.org/cgi/doi/10.1101/gad.1214204.
5 Corresponding author.
E-MAIL bradley.olwin{at}colorado.edu; FAX (303) 492-1587. 
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