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© The Rockefeller University Press,
0021-9525/1997//1231 $5.00
The Journal of Cell Biology, Volume 139, Number 5,
, 1997 1231-1242
Article |
Accumulation of Muscle Ankyrin Repeat Protein Transcript Reveals Local Activation of Primary Myotube Endcompartments during Muscle Morphogenesis
The characteristic shapes and positions of each individual body muscle are established during the process of muscle morphogenesis in response to patterning information from the surrounding mesenchyme. Throughout muscle morphogenesis, primary myotubes are arranged in small parallel bundles, each myotube spanning the forming muscles from end to end. This unique arrangement potentially assigns a crucial role to primary myotube end regions for muscle morphogenesis.
We have cloned muscle ankyrin repeat protein (MARP) as a gene induced in adult rat skeletal muscle by denervation. MARP is the rodent homologue of human C-193 (Chu, W., D.K. Burns, R.A. Swerick, and D.H. Presky. 1995. J. Biol. Chem. 270:10236–10245) and is identical to rat cardiac ankyrin repeat protein. (Zou, Y., S. Evans, J. Chen, H.-C. Kuo, R.P. Harvey, and K.R. Chien. 1997. Development. 124:793–804). In denervated muscle fibers, MARP transcript accumulated in a unique perisynaptic pattern. MARP was also expressed in large blood vessels and in cardiac muscle, where it was further induced by cardiac hypertrophy. During embryonic development, MARP was expressed in forming skeletal muscle. In situ hybridization analysis in mouse embryos revealed that MARP transcript exclusively accumulates at the end regions of primary myotubes during muscle morphogenesis. This closely coincided with the expression of thrombospondin-4 in adjacent prospective tendon mesenchyme, suggesting that these two compartments may constitute a functional unit involved in muscle morphogenesis. Transfection experiments established that MARP protein accumulates in the nucleus and that the levels of both MARP mRNA and protein are controlled by rapid degradation mechanisms characteristic of regulatory early response genes. The results establish the existence of novel regulatory muscle fiber subcompartments associated with muscle morphogenesis and denervation and suggest that MARP may be a crucial nuclear cofactor in local signaling pathways from prospective tendon mesenchyme to forming muscle and from activated muscle interstitial cells to denervated muscle fibers.
Abbreviations used in this paper: CARP, cardiac ankyrin repeat protein; E, embryonic day; MARP, muscle ankyrin repeat domain; MLP, muscle LIM protein; TSP-4, thrombospondin-4.
IN their physiological context in vivo, cells must integrate multiple signals from their environment to fulfill their specific roles within the organism. This crucial role of integration is particularly evident during development, when cells display coordinate migration, differentiation, and morphogenesis in response to a variety of specific long-range and local signals. The formation of the skeletal musculature is an attractive model system in which to study how patterns of gene expression lead to the formation of a tissue. Due to major breakthroughs such as the establishment of differentiating myogenic cell lines, and the discovery of the converting activity of myogenic determination factors, the early events in myogenesis, from predetermined cells to terminally differentiated myotubes, are particularly well understood at the cellular level (Buckingham, 1992; Olson and Klein, 1994). In contrast, we know very little about the mechanisms that control muscle formation within the context of the developing organism. For example, the morphogenetic events that orchestrate the formation of the definitive muscle pattern are poorly understood. These include specific successive splitting of primordial muscle masses to generate all the different muscles, directed expansion of the newly formed muscles to generate their unique shapes, sizes, and positions, and attachment of the muscles to their specific tendon organs (Lance-Jones, 1979; Schroeter and Tosney, 1991a, b; Hauschka, 1994). In the developing mouse limb, these events begin around embryonic day (E)1 12.5, and the definitive muscle pattern is established by E16 (Lance-Jones, 1979). Throughout muscle morphogenesis, the muscle pattern is reflected in the parallel arrangement of primary myotubes that span the forming muscles from end to end (Fig. 1) (Hilfer et al., 1973; Hauschka, 1974; Ontell and Kozeka, 1984; Duxson and Usson, 1989; Sweeney et al., 1989). After completion of muscle morphogenesis, primary myotubes then serve as scaffolds for secondary muscle fibers, which are generated through the proliferation and differentiation of intramuscular precursor cells (Ross et al., 1987; Condon et al., 1990; Ashby et al., 1993).
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In a search for genes involved in the regulation of muscle gene expression and the formation of neuromuscular synapses, we constructed and screened a cDNA library enriched in messages induced in adult skeletal muscle by denervation. As reported elsewhere, two clones coded for a striated muscle-specific positive regulator of myogenesis: muscle LIM protein (MLP; Arber et al., 1994) and thrombospondin-4 (TSP-4; Arber and Caroni, 1995), whose expression is induced in denervated muscle interstitial cells. We report here that a third clone codes for a nuclear protein with four ankyrin repeats that is expressed in striated muscle and vascular endothelial cells. Due to its predominant expression in striated muscle we have called it MARP (muscle ankyrin repeat protein). During the course of this work, isolation of the homologous human protein (C-139; Chu et al., 1995) and of the identical rat cDNA (cardiac ankyrin repeat protein [CARP]; Zou et al., 1997) were reported. MARP mRNA has degradation-promoting motifs characteristic of regulatory factors. Consistent with a possible role in signaling, MARP protein is rapidly degraded in the cell, and degradation can be substantially delayed by the addition of short carboxyl-terminal extentions. The distribution of MARP mRNA in developing mouse skeletal muscle revealed a unique and highly localized pattern associated with muscle morphogenesis. This was accompanied by a complementary pattern of TSP-4 expression in adjacent mesenchyme. The results establish the existence of novel muscle subcompartments associated with muscle morphogenesis and the perisynaptic region of denervated muscle and suggest that MARP may be a key nuclear cofactor in novel local signaling pathways to muscle.
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and C (kind gift of M.C. Weiss, Institut Pasteur, Paris, France).
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Transfection and Coculture Experiments
All cell lines (mouse 3T3 fibroblasts; mouse C2C12 myoblasts; rat L6 myoblasts; rat 10T1/2 fibroblasts; monkey kidney epithelial cells COS-1) were from American Type Cell Culture Collection (Rockville, MD). Cells were cultured, transfected with the lipofectamine reagent (GIBCO BRL, Gaithersburg, MD), and differentiated as described (Arber et al., 1994). When indicated, cultures were treated for 6 to 8 h with 10–50 µg/ml cycloheximide (Fluka, Buchs, Switzerland). For transfections, a CMV promoter-based eukaryotic expression vector (pcDNA3; Invitrogen, San Diego, CA) was used. To obtain a MARP construct devoid of 3' ATTTA motifs, cDNA sequences downstream of nucleotide 999 (i.e., 37 bp 3' from the MARP stop codon) were deleted, and the deletion construct was subcloned in pcDNA3. Epitope tags were added to MARP cDNA using the PCR, with appropriate primers. The corresponding MARP constructs had the following amino acid sequences: MEQKLISEEDLN-MM . . . (Myc-MARP); ..ATFAAAPMEQKLISEEDLN (MARP-Myc); MEQKLISEEDLNI-MMV. . . .ATFAAAPGLVVMNIT (Myc-MARP-GLVVMNIT). The rabbit antibody against the synthetic carboxyl-terminal peptide VLRVEELVTGKKC of MARP was produced by coupling the peptide to keyhole lympet hemocyanin (Sigma Chemical Co., St. Louis, MO) via a carboxyl-terminal Cys. Further antibodies were from the following sources: rabbit antiserum to carboxyl-terminal peptide GLVVMNIT (kind gift of R. Chiquet-Ehrismann, Friedrich Miescher Institute), monoclonal antibody to Myc epitope (kind gift of A. Matus, Friedrich Miescher Institute), monoclonal antibody to sarcomeric -actinin (Sigma Chemical Co.). For immunoblots, tissues or cells were homogenized in SDS-PAGE sample buffer, homogenates were boiled, and solubilized proteins were fractionated. For immunocytochemistry, cells (usually 24 h after transfection) were fixed for 10 min at room temperature with 4% paraformaldehyde in PBS and then permeabilized for 7 min at room temperature with 0.2% Triton X-100 in PBS. Antibody incubations were carried out in PBS with 5% BSA, and all washes were in PBS. Double-labeling immunocytochemistry was carried out with biotinylated secondary antibodies, followed by lucifer yellow–conjugated streptavidin for the first channel and rhodamine-coupled second antibodies for the second epifluorescence channel. All secondary antibodies were from Molecular Probes Inc. (Eugene, OR).
4–5 h before the addition of muscle-derived cells, COS or COS-TSP-4 cells (Arber and Caroni, 1997) were plated at densities of 40,000–80,000 cells on laminin-coated 35-mm culture dishes in the presence of DME with 10% horse serum and 5% chick embryo extract. Muscle-derived cells consisted mainly of myoblasts and fibroblasts and were obtained and cultured according to standard procedures. Briefly, muscle from the hind limbs of P0-P1 mice was minced, trypsinised for 45 min at 37°C, and triturated with a pasteur pipette in the presence of DNaseI. Cells were then filtered through a cell strainer (70 µm) and preplated for 1.5 h in DME with 10% horse serum and 5% chick embryo extract. Nonadherent cells were counted, and 500,000 cells were plated onto the laminin/COS or laminin/ COS-TSP-4 dishes. After 2 d of coculture the medium was changed to DME with 2% horse serum (differentiation medium), and myotube formation was scored 1 and 2 d later.
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Fig. 3 A shows that no MARP transcript was detectable in adult medial gastrocnemius muscle, where strong expression in the vicinity of acetylcholine esterase–positive neuromuscular synapses was induced by denervation. At closer inspection, the MARP signal frequently highlighted striations and accumulated in a longitudinal pattern along the inner face of muscle fibers, indicating that it was localized inside skeletal muscle fibers (Fig. 3 B). This dramatic accumulation pattern in denervated muscle had features unique to MARP. Thus: (a) MyoD and MLP transcripts accumulated throughout denervated muscle fibers, and the signal for clone-16 mRNA only showed partial synaptic enrichment (data not shown); (b) although the subunit of the acetylcholine receptor displays some synaptic enrichment, it is largely due to its synaptic expression in innervated muscle, and synaptic accumulation is in fact reduced in denervated muscle (Fontaine and Changeux, 1989; Witzemann et al., 1991); (c) while typical synapse- associated transcripts such as the subunit of the acetylcholine receptor or the regulatory subunit RI of protein kinase A display local accumulation restricted to the subsynaptic region (i.e., coincident with acetylcholine esterase reaction product; data not shown; see Witzemann et al., 1991; Imaizumi-Scherrer et al., 1996), MARP transcript accumulated in a much broader perisynaptic pattern, suggesting local regulation by signals in the vicinity of denervated synapses. Unlike these muscle fiber transcripts, and as reported previously, TSP-4 mRNA accumulated in muscle interstitial cells (Fig. 3 B; see also Arber and Caroni, 1995). In innervated muscle it was restricted to epimysium, whereas denervation induced expression in the endomysium (Arber and Caroni, 1995). Interestingly, induction was distinctly more pronounced in perisynaptic regions, providing a first example of spatial correlation between the accumulation of MARP mRNA in muscle fibers and that of TSP-4 in adjacent cells (see below). The dramatic perisynaptic accumulation of MARP transcript in denervated muscle is highly unusual. It suggests that this transcript is subject to local regulatory mechanisms and that even several days after removal of the motor nerve the perisynaptic region of muscle is under the influence of distinct local signals.
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MARP Is a Nuclear and Cytosolic Protein Subject to Tight Posttranscriptional Regulation
To investigate the cellular regulation of MARP mRNA we analyzed its levels in non- and myogenic cell lines. As shown in Fig. 4 A, the transcript could be detected in the myogenic cell line C2C12, in 10T1/2 fibroblasts, but not in 3T3 fibroblasts. Significantly, when C2C12 cells were transferred to differentiation medium, MARP transcript levels were selectively upregulated in myotubes (Fig. 4 B). Myogenic cell lines exhibited varying degrees of coupling between MARP transcript levels and differentiation. Thus, while one batch of C2C12 cells displayed detectable expression only upon differentiation (see Arber et al., 1994), a second C2C12 batch (Fig. 4 A) and L6 cells (data not shown) already expressed significant levels under nondifferentiating conditions. In 10T1/2 cells, but much less so in C2C12 cells MARP mRNA levels were elevated in the presence of the protein synthesis inhibitor cycloheximide (Fig. 4 A). This is reminiscent of human vascular endothelial cells, where C-193 transcript has early response properties in small vessel cells and is expressed at much higher levels in large vessel cells (Chu et al., 1995).
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MARP contains a classical nuclear localization sequence, suggesting that it may be a nuclear protein. Detection with MARP-specific antiserum revealed accumulation in the nucleus and in the cytosol of transfected cells (Chu et al., 1995; Zou et al., 1997). About two thirds of the labeled cells showed an exclusively nuclear pattern, whereas the rest of the cells also displayed cytosolic signal (Fig. 4 D). Cytosolic MARP frequently accumulated in clump-like structures, suggesting aggregation and/or degradation. To determine whether the entire MARP protein translocates to the nucleus and whether stabilization against proteolytic degradation may reveal selective accumulation in a cellular compartment, we analyzed the subcellular localization of epitope-tagged MARP constructs. When amino and carboxyl-terminus-tagged protein was double labeled for both epitopes, a majority of the labeled cells displayed comparable distribution of the two epitopes (Fig. 4 D). These results indicate that a substantial proportion of apparently intact MARP accumulates in the nucleus (Chu et al., 1995; Zou et al., 1997). It is therefore likely that this highly regulated early response protein exerts its function in this compartment. In addition, the experiments revealed that besides greatly elevating the number of cells with detectable MARP signals (
20-fold increase), carboxyl-terminal tags also led to a substantially higher proportion of cytosolic MARP in the transfected cells (Fig. 4 D). A possible interpretation of these findings is that carboxyl-terminal epitope tags protect MARP from degradation in the cytosol.
The Spatial and Temporal Distribution of MARP mRNA in Embryonic Mouse Skeletal Muscle Coincides with Muscle Morphogenesis
In mouse embryos before E11.5, MARP mRNA was only detectable in the heart and in large blood vessels. Both tissues expressed high levels of MARP transcript at all later stages of embryogenesis. Prominent expression in the developing and adult heart is consistent with the findings of Zou et al. (1997), and selective accumulation of MARP mRNA in large blood vessels is consistent with the constitutive expression of the human homologue of MARP (C-193) in endothelial cell lines derived from large, but not small blood vessels (Chu et al., 1995). Based on the tissue culture results with myogenic cell lines, the absence of MARP mRNA in myogenic regions of E10.5 embryos was unexpected, since in these embryos, determined myogenic cells already express MyoD, which in mouse skeletal muscle cells is the latest of the myogenic determination factors (Buckingham, 1992). At E11.5, MARP mRNA was detectable in the myotome region (Fig. 5 A). Comparison with the somitic expression patterns of MyoD, and of MLP, which is only expressed in terminally differentiated skeletal muscle cells (Arber et al., 1994), revealed the presence of MARP transcript in a subset of cells within MLP-positive territories (Fig. 5 A). In contrast, no MARP expression was detected in E11.5 forelimb, which contained MyoD-positive, but MLP-negative cells (Fig. 5 A). This coincidence between MLP- and MARP-positive areas was consistently observed between E11.5 and 16.5. The observation that within MLP-expressing areas MARP-positive cells were consistently less numerous than those expressing MLP prompted us to analyze these cells in E14.5 embryos, where myotubes are easier to identify. As shown in Fig. 5 B, MLP-positive myotubes were arranged in small clusters of primary myotubes. These clusters were oriented parallel to each other and spanned the muscle from end to end (Fig. 5 B; see Fig. 7, left, for E12.5 data and Fig. 1 for a schematic representation of myotube arrangement during muscle morphogenesis). In contrast, MyoD-positive cells, which included myotubes and muscle precursor cells, displayed a more homogeneous distribution. Hybridization for MARP mRNA revealed a striking pattern specifically associated with the end regions of primary myotube clusters (Figs. 5 B, 6, and 7). The higher magnification photographs show that MARP mRNA accumulated inside multinucleated striated muscle fibers (Fig. 6). Systematic analysis revealed that all MLP-positive muscles in these embryos contained MARP-positive muscle fibers.
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During Muscle Morphogenesis Expression of TSP-4 in Prospective Tendon Mesenchyme Is Adjacent to that of MARP-positive Skeletal Muscle Fibers
What signals are responsible for the striking accumulation of MARP transcript at the end regions of primary myotubes in forming muscles? Because of the role of mesenchyme in muscle morphogenesis, we searched for transcripts expressed in regions adjacent to MARP-positive muscle. Due to its association with tendon regions (Tucker et al., 1994) and its upregulation in interstitial cells of denervated muscle (Arber and Caroni, 1995), TSP-4 was one potential candidate. Before E12.5, TSP-4 mRNA was detected in the developing heart (data not shown). In addition, like in the chick (Tucker et al., 1995), TSP-4 mRNA accumulated in chondrogenic regions of the mouse embryo. Close examination of the TSP-4 signal in the vicinity of developing cartilage revealed a striking complementarity to the localization of MARP mRNA (Fig. 8). The high-magnification photographs (Fig. 9 B) show that the MARP and TSP-4 signals precisely apposed each other, and that TSP-4 expressing tissue was coextensive to muscle tissue. Exclusion of muscle transcripts from TSP-4–expressing end regions was also observed for MLP (Fig. 9) and MyoD mRNA. Comparable relative localizations of MARP and TSP-4 transcripts were detected from E13.5 to 17.5 (Figs. 8 and 9). As shown in Fig. 9 B, spatial coincidence was not restricted to regions adjacent to developing bone. The characteristic arrangement of the TSP-4 signal with respect to forming muscle suggested that it was associated with prospective tendon mesenchyme. This conclusion was supported by the fact that TSP-4–expressing tissue also accumulated tenascin-C transcript (data not shown; Chiquet and Fambrough, 1984).
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What types of functional responses may be induced at muscle end regions by prospective tendon mesenchyme? As mentioned above, one possibility is local induction of muscle growth, including proliferation and fusion of myoblasts to primary myotubes, myogenic differentiation, and myotube extension. A previous in vitro study demonstrated that myoblasts adhere to a peptide corresponding to the cell-binding carboxyl-terminal end of TSP-4 (Adams and Lawler, 1994). Accordingly, to determine whether TSP-4 can promote myogenic differentiation we carried out coculture experiments with primary myoblasts from newborn mice and TSP-4–expressing COS cells (COS-TSP-4; Arber and Caroni, 1995). The latter secrete substantial amounts of TSP-4, which was shown in a previous study to efficiently promote neurite outgrowth (Arber and Caroni, 1995). COS-TSP-4 or naive COS cells were plated at low density on laminin-coated culture dishes, and hind limb muscle-derived cells were added 4–5 h later. After 2 d in growth-promoting medium the cultures were switched to differentiation medium, and myotube formation was scored 1 and 2 d later. As shown in Fig. 10, under these experimental conditions, myogenic differentiation and myotube formation were markedly potentiated in the presence of the COS-TSP-4 cells. Muscle-derived cells, which were noticably smaller and thus easily distinguishable from cocultured COS cells, could be detected in comparable amounts in the two types of cultures. However, in the absence of TSP-4 these cells only expressed low levels of muscle-specific actinin and only rarely fused to myotubes (Fig. 10). The finding that TSP-4 can promote myogenic differentiation under these in vitro conditions is consistent with the possibility that secretion of this extracellular matrix protein by prospective tendon mesenchyme cells is part of a local signaling process to couple muscle formation to tendon morphogenesis.
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Regulation of MARP levels has cell type- and signal-specific features. Thus a human cell line with properties of large vessel vascular endothelial cells expresses comparatively high levels of MARP mRNA, whereas corresponding small vessel cells require activation with IL1, lysophosphatidic acid, or cycloheximide for detectable MARP expression (Chu et al., 1995). Regulation of MARP mRNA levels in vascular endothelial cells may have similar properties in vivo, since in mouse embryos, corresponding in situ hybridization signals were only detected along subdomains of large blood vessels (not shown). Similar cell-type specific regulation was detected in myogenic and fibroblastic cell lines. In addition, cell type- and signal-specific regulation was detected in developing and adult mouse muscle in vivo, where MARP expression was restricted to subtypes and subdomains of striated muscle cells under defined reactive conditions. The unique temporal and spatial patterns of MARP transcript accumulation suggest that MARP levels may control specific signaling pathways to the nucleus. The observation that certain cell lines can contain unexpectedly high levels of MARP mRNA may reflect the absence or attenuation of physiological inhibitory mechanisms under tissue culture conditions. Similar considerations probably apply to primary myotubes from newborn hindlimb myoblasts, which expressed substantial levels of MARP mRNA, although the corresponding muscle cells in vivo contained no detectable MARP transcript (not shown).
What cellular processes may be affected by MARP? Although it accumulates in the nucleus, MARP does not appear to bind DNA with high affinity (Chou et al., 1995). A recent independent study focusing on the possible role of CARP/MARP in heart-specific gene expression provided evidence that this protein is a nuclear cofactor that promotes the expression of certain muscle-specific genes in cardiomyocytes (Zou et al., 1997). In that study CARP/ MARP was isolated by a two-hybrid approach as a nuclear cofactor that interacts with the ubiquitous transcription factor YB-1. Negative regulation of a YB-1–responsive minimal promoter construct suggested that CARP/MARP may specifically regulate HF-1–dependent pathways for ventricular muscle gene expression (Zou et al., 1997). Possibly due to technical reasons, although a weak CARP/ MARP signal was detected in that study on a Northern blot of adult skeletal muscle, no in situ hybridization signal was detected in skeletal muscle at any stage of mouse embryogenesis (hence the name CARP; Zou et al., 1997). Assuming that the findings on YB-1 regulation can be extended to skeletal muscle genes, then MARP may be a nuclear cofactor in a signal transduction pathway for local cell activation in forming and denervated muscle.
Besides a classical bipartite nuclear localization sequence and the PEST motif mentioned above, MARP has a cluster of four ankyrin repeats near its carboxyl-terminal end. Clusters containing different numbers of this 30-amino acid motif have been found in a variety of apparently unrelated proteins, where they are thought to mediate protein–protein interactions (Blank et al., 1992). The molecular size of MARP, the arrangement and number of its ankyrin repeats, and the fact that it is subject to degradative regulation in the cell are most reminiscent of I
B proteins. These are negative regulators of NF-B proteins, a family of transcription factors mediating acute cellular responses. To explore the possibility that MARP may function as an IB we carried out cotransfection experiments with various NF-B constructs, assaying for protein stability in the presence and absence of phorbol ester and for transcriptional activation. So far, however, these experiments provided no positive indications (data not shown). Therefore, while it is tempting to speculate that MARP may be involved in novel signal transduction pathways mediating local alterations in gene expression, elucidation of the actual nature of the processes affected by MARP will require further experimentation.
Primary Myotube Endcompartments and Adjacent Prospective Tendon Mesenchyme May Constitute a Functional Unit Involved in Muscle Morphogenesis
A main finding of this study is that the accumulation of MARP transcript visualizes a novel muscle subcompartment associated with muscle morphogenesis. MARP mRNA accumulated at the ends of MLP-positive primary myotubes from about E12 to 16. Later in development, MARP skeletal muscle signal was restricted to the tongue, where it could still be detected during the first postnatal week. In addition, denervation rapidly induced skeletal muscle MARP mRNA in the vicinity of vacated neuromuscular synapses. Therefore, in developing and adult skeletal muscle, MARP transcript is under tight spatial and temporal regulation. Due to the unique size and shape of myotubes and skeletal muscle fibers, this narrow regulation of MARP mRNA reveals regulatory subcompartments within muscle fibers. The perisynaptic compartment of functionally denervated skeletal muscle fibers may reflect signaling from activated muscle interstitial cells (Fig. 11; Connor and McMahan, 1987; Gatchalian et al., 1989). The unique properties of primary myotube end regions during muscle morphogenesis have not been detected before, and the possible implications of these observations are discussed below.
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In conclusion, this study has revealed the existence of a novel muscle subcompartment at the ends of primary myotubes and has provided molecular markers for that subcompartment and prospective tendon mesenchyme during muscle morphogenesis. The spatial and temporal relation between the compartments defined by the expression of MARP and TSP-4 suggests that they may define a functional unit involved in muscle morphogenesis. These findings should provide a molecular basis to elucidate novel local signaling pathways leading to the specification and shaping of defined skeletal muscles. Likewise, the visualization of a perisynaptic subcompartment in denervated skeletal muscle may provide a starting point to define novel signaling pathways at denervated neuromuscular junctions.
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Acknowledgments |
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B proteins, M.C. Weiss for specific protein kinase A cDNA probes (RI and C), and D. Birnbaum for a specific FGF6 cDNA probe. We are particularly grateful to G. Kardon (Duke University, Durham, NC) and C. Lance-Jones (University of Pittsburgh, Pittsburgh, PA) for precious information and insight about muscle morphogenesis.
Submitted: 28 February 1997
Revised: 20 August 1997
Address all correspondence to Pico Caroni, Friederich Miescher Institute, P.O. Box 2543, CH-4002 Basel, Switzerland. Tel.: (41) 61-6973727. Fax: (41) 61-6973976. E-mail: caroni{at}fmi.ch
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