ARTICLE |
Correspondence to: Mar Royuela, Dept. of Cell Biology and Genetics, Univ. of Alcalá de Henares (Madrid), Spain. E-mail: ricardo.paniagua@uah.es
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Summary |
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We present an up-to-date study on the nature, at the protein level, of various members of the dystrophin complex at the muscle cell membrane by comparing red and white caudal muscles from Torpedo marmorata. Our investigations involved immunodetection approaches and Western blotting analysis. We determined the presence or absence of different molecules belonging to the dystrophin family complex by analyzing their localization and molecular weight. Specific antibodies directed against dystrophin, i.e., DRP2 -dystrobrevin, ß-dystroglycan,
-syntrophin,
-, ß-,
-, and
-sarcoglycan, and sarcospan, were used. The immunofluorescence study (confocal microscopy) showed differences in positive immunoreactions at the sarcolemmal membrane in these slow-type and fast-type skeletal muscle fibers. Protein extracts from T. marmorata red and white muscles were analyzed by Western blotting and confirmed the presence of dystrophin and associated proteins at the expected molecular weights. Differences were confirmed by comparative immunoprecipitation analysis of enriched membrane preparations with anti-ß-dystroglycan polyclonal antibody. These experiments revealed clear complex or non-complex formation between members of the dystrophin system, depending on the muscle type analyzed. Differences in the potential function of these various dystrophin complexes in fast or slow muscle fibers are discussed in relation to previous data obtained in corresponding mammalian tissues. (J Histochem Cytochem 49:857865, 2001)
Key Words: dystrophin family, associated proteins, striated muscles
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Introduction |
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MOST BEHAVIORAL OR PHYSIOLOGICAL RESPONSES of animals to any environmental situation involve participation of muscle cells specialized in contraction processes. In all organs in which tissue contraction occurs, there is a relationship between muscle activity and movement. Molecular mechanisms are not always the same because there are a wide variety of muscle cells well adapted to specific functions in each organ. Fast muscle fibers, which are involved in rapid contraction, very quickly give rise to maximal tension but are rapidly fatigable. Slow muscle fibers, which are involved in slow contraction, give rise to less tension but are resistant to fatigability. We carried out a close comparative analysis of these two kinds of skeletal muscles, i.e., red and white muscles, which are also found in the caudal region of fish. The red muscle has short, pen-shaped slow-type fibers. The white muscle has large, long fast-type fibers. Because of this clear difference in size and function, we assessed this material to establish the nature of the dystrophin protein complex in both fiber types. Torpedo marmorata was the first fish described as containing dystrophin, particularly in its electric organ (
Since 1987, dystrophin has been known (- and ß-) (
-, ß-,
-,
-, and
) that are complexed with sarcospan (
-, ß1-, ß2-) in muscle tissues (
1- and
2-) have also been reported and were found expressed as brain-specific protein (
In muscles, dystrophin expression is believed to provide resistance of muscle membrane during contraction processes (
This work investigated the possible presence and distribution of dystrophin family products and some dystrophin-associated-like proteins in red and white muscles from T. marmorata. This approach was possible using a large battery of specific monoclonal and polyclonal antibodies produced by us that were authenticated in previous studies as specific for dystrophin, utrophin, or associated proteins (
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Materials and Methods |
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Tissues
Transversely striated muscles (red or white) from live T. marmorata fish were dissected and quickly frozen for indirect cytochemical fluorescence labeling or were treated for crude protein extraction.
Antibodies
We used various antibodies specific for various proteins of the dystrophin family. In detail, monoclonal (5G5, 3E7, 5A3, 4A1,) and polyclonal (C) antibodies were directed against dystrophin and/or utrophin molecules. The specificities of all monoclonal and polyclonal antibodies were previously confirmed in muscle and nerve tissues of rabbit (-dystrobrevin, and sarcospan that were obtained by injecting their specific C-terminal synthetic peptides (ANTLLAS), (GVSYVPYCRS), and (SLTAESEGPQQKI) as antigens, respectively, according to a previously described protocol (
, residues PLILDQH; ß, residues AGYIPIDEDRL;
, residues VREQYTTAT;
, recombinant protein residues 84290) and ß-dystroglycan (residues PPPYVPP). All antibodies were previously characterized in adult bovine heart (
-syntrophin (antigenic residues 191206) was recently detected in Torpedo (
-, ß-,
-, and
-sarcoglycans were obtained from Novocastra (Sigma; St Louis, MO).
The specificity of the immunochemical procedures was checked by incubation of sections with non-immune serum instead of primary antibody. As positive controls for this study, skeletal muscle sections of mouse (for polyclonal antibodies) or rabbit (for monoclonal antibodies) were treated simultaneously with the Torpedo muscles.
Western Blotting Analysis
Tissues were homogenized in the extraction buffer (0.05 M Tris-HCl, pH 8) with the addition of a cocktail of protease inhibitors (100 mM iodoacetamide, 0.1 mM phenylmethyl sulfonic fluoride, 0.01 mg/ml soybean trypsin inhibitor, 1 µl/ml leupeptin) in the presence of 1% Triton X-100. Homogenates were centrifuged for 10 min at 10,000 rpm. Supernatants and pellet (resuspended in 50 mM Tris-HCl, pH 8) were mixed with an equivalent volume of SDS buffer (10% SDS in Tris-HCl, pH 8, containing 50% glycerol, 0.1 mM 2-ß-mercaptoetanol, and 0.1% bromophenol blue). The mixture was denatured for 5 min at 100C and 10-µl aliquots of homogenate were separated in SDS-polyacrylamide slab minigels (312% gradient gels). To carefully compare protein extraction, we equilibrated each sample by equilibrating the muscle actin content. Separated proteins were transferred overnight (30 V, 100 mA) in the transfer buffer (25 mM Tris-HCl, 192 mM glycine, 0.1% SDS, and 20% methanol). Nitrocellulose membranes (0.2 µm) were blocked with 3% BSA dissolved in TBST buffer (10 mM Tris-HCl, 150 mM NaCl, 0.05% Tween-20, pH 8) for 1 hr with specific antibodies and then were incubated with a phosphatase-labeled second antibody (1:3000 dilution; Jackson ImmunoResearch Laboratory, West Chester, PA). The protein band was visualized with p-nitroblue tetrazolium, and 5-bromo-4-chloro-3-indoylphosphate substrate, as previously described (
Scanning Densitometry
Western blots were digitized with a 256 gray scale and images were quantitatively analyzed using the NIH 1.62 image program. Each lane was treated independently and corrected by estimation of the relative optical density found in the Coomassie blue gel corresponding to the amount of actin present in the W or R lane. Each blot was obtained in triplicate to avoid errors due to differences in signal intensities. Values were normalized and averages for the three assays were compared between white and red muscles. Their ratio was expressed as a percentage of each component found in red muscle vs white muscle.
Immunoprecipitation
Anti-ß-dystroglycan polyclonal antibody was used as in
Immunofluorescence Light Microscopy
Cryostat sections (10 µm) of unfixed muscle were labeled with different specific antibodies. Immunoreactions were detected with Cy3-conjugated sheep anti-mouse Ig (for monoclonal antibodies) or Cy3-conjugated sheep anti-rabbit IgG (for polyclonal antibodies). For double detection, sections were first labeled with the monoclonal antibody concomitantly with a polyclonal antibody (against dystrophin-related protein or DAP). In a second step, the monoclonal antibody was revealed with Cy3-conjugated sheep anti-mouse IgG (1:500) and fluorescein-conjugated goat anti-rabbit IgG (1:100) for all other polyclonal antibodies (Sigma Bio-Sciences Laboratory; St Louis, MO).
Confocal Laser Microscopy
Confocal laser microscopy analyses were performed as described in previous studies (
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Results |
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Immunofluorescence Analyses
Immunofluorescence reactions were studied through two concomitant investigations and are presented comparatively in two figures, i.e., Fig 1A1J (white muscle) and Fig 2A2J (red muscle). It was always clear that the large fibers corresponded to white muscle (fast-type), whereas small fibers were found only in red muscle (slow-type) (see Fig 1 and Fig 2). For these experiments, as later in Western blotting assays, components such as dystrophin and 90-kD protein were viewed with monoclonal antibodies 5A3 and 13E2, respectively, while all other proteins were identified with polyclonal antibodies that we produced. Torpedo dystrophin detection was found (as expected) at the muscle cell membrane with each of the specific antibodies used in this study (Fig 1A and Fig 2A, left panels) and this presentation is repeated in each following image (left panel), excluding Fig 1E and Fig 2E, left panels. The two other dystrophin family proteins studied, i.e., DRP2 and -dystrobrevin, are presented in Fig 1A, Fig 1B, Fig 2A, and Fig 2B, middle panels, and were not found at the muscle cell periphery of fast-type fibers (Fig 1) but rather at the membrane of slow-type fibers (Fig 2). ß-Dystroglycan, which is presented in Fig 1C, Fig 1E, Fig 2C, and Fig 2E, middle panels, was detected in both fast- and slow-type fibers.
-syntrophin Fig 1D and Fig 2D, central portion, was located in fast-type fibers (Fig 1) but was absent in cell membranes of slow-type fibers (Fig 2). Similarly, in Fig 1E and Fig 2E, left panels, a specific monoclonal antibody against a 90-kD protein (as described in Materials and Methods) was clearly detected in the membrane of fast-type fibers (Fig 1) co-localized with ß-dystroglycan but was not present in cell membrane structures of slow-type fibers (Fig 2). In the following set of experiments, we analyzed polyclonal antibodies that we had developed and characterized as specific for sarcoglycan family products. We also obtained a good correlation between results with polyclonal antibodies and similar commercially available specific monoclonal antibodies, in their capacity to detect, at the membrane or not, one of these sarcoglycans. However, only a commercial monoclonal antibody against
-sarcoglycan was undetectable in both fiber types, in contrast to our polyclonal antibody produced against this protein, which was efficient. In fast fibers (Fig 1), the following differences appeared in the middle panel:
-sarcoglycan (Fig 1F),
-sarcoglycan (Fig 1H), and sarcospan (Fig 1J) were all present at the white muscle membrane. In contrast, ß-sarcoglycan (Fig 1G) and
-sarcoglycan (Fig 1I) were not detected at the membrane of these fast-type fibers (Fig 1). In slow fibers (Fig 2), all proteins detected Fig 2F2J (middle panels, corresponding respectively to
-, ß-,
-,
-sarcoglycan, and sarcospan) were found at the cell membrane.
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These confocal microscopic observations are illustrated in the right panel of each set, corresponding to the superimposed images, which gave a clear yellow color when there was co-localization but only a pale orange color when the associated protein was not found at the muscle cell membrane. These results are summarized in Table 1, in which we comparatively present the membrane distribution in white muscle (fast type) and red muscle (slow type) for each member of the dystrophin complex.
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To obtain more information in these comparative immunodetections, we confirmed the presence of the molecule analyzed in crude white (W) and red (R) muscle extracts.
Western Blotting Analyses
Crude protein extracts from T. marmorata slow-type and fast-type fibers were transferred to nitrocellulose sheets and incubated respectively with each antibody reported above. Whereas no clear result was obtained with -dystrobrevin,
-sarcoglycan, and sarcospan, the specific antibodies presented in Fig 3 showed that (as expected) dystrophin (400-kD protein band), ß-dystroglycan (43-kD protein band), and
-sarcoglycan (50-kD protein band) were detectable in both fast (W) and slow (R) muscles.
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Fast muscle fibers from Torpedo contained -syntrophin (59-kD) but appeared to be depleted of DRP2 and both ß- and
-sarcoglycan. There was also a 90-kD protein (called 90k) in crude protein extracts from white muscles, i.e., detected with monoclonal antibody 13E2 that we produced and which is assumed to correspond to the Ao protein reported by
Slow muscle fibers from Torpedo were found to contain DRP2 (120-kD) and ß-sarcoglycan (43 kD). -sarcoglycan appeared to be present but with an apparent migration of about 37 kD, as compared to 3531 kD in mammalian muscles. No
-syntrophin or 90-kD protein was detected in Western blots.
In addition to these positive or negative detections, it was also possible to estimate the relative amount of proteins present in both muscle types. We have presented here a preliminary attempt at Western blotting quantification. The densitometric measurements enabled us to estimate that the relative OD levels were different in red (slow) and white (fast) Torpedo muscle. This corresponded to the presence of dystrophin (125%), ß-dystroglycan (110%), and -sarcoglycan (160%) at higher levels in Torpedo slow-type fibers.
Immunoprecipitation
Comparative analyses of proteins specifically immunoprecipitated with anti-ß-dystroglycan polyclonal antibody and then retained on a protein ASepharose column are presented in Fig 4. The use of anti-ß-dystroglycan revealed in both enriched membrane-eluted fractions from white and red Torpedo muscles the presence of the expected proteins, such as ß-dystroglycan, but also dystrophin. Similarly, -sarcoglycan was detected in both membrane fractions, whereas DRP2 and
-sarcoglycan proteins were found only in red muscle extracts. In contrast, only the white muscle-eluted fraction contained
-syntrophin.
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Discussion |
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We comparatively investigated the composition of dystrophin-associated proteins from red and white caudal muscles in Torpedo marmorata. This was undertaken first to visualize the presence of this protein system at the fish muscle membrane and then to compare the expression pattern according to the muscle fiber type analyzed. We intended to establish, in the light of increasing knowledge on the number of molecules constituting dystrophin-associated protein complex, a catalogue of dystrophin family proteins that exist in slow- and fast-type muscle fibers from fish (which are similar in terms of myosin presence as tested with a monoclonal antibody directed specifically against slow fiber type muscles from mammals and which gave cytoplasmic staining only in red Torpedo muscle; not shown).
With the monoclonal and polyclonal antibodies against dystrophin and/or utrophin used in this study, we identified two proteins in white and red muscles of Torpedo: a 400-kD protein band corresponding to Torpedo dystrophin and utrophin proteins and a 116-kD protein band that corresponded to a short Torpedo dystrophin/utrophin family product (referred to as DRP2). These proteins have already been described in the T. marmorata electric organ (-syntrophin (
-syntrophin only in Torpedo white muscle. Dystroglycan in Torpedo electric organ consists of 190-kD and 43-kD proteins (
-sarcoglycan (
-sarcoglycan was detected in both muscles studied, but ß- and
-sarcoglycan appeared only in red muscle. Finally, the 90-kD protein that was present in electric organ, in accordance with
These differences between Torpedo electric organ and two kinds of Torpedo muscles might be explained by the fact that Torpedo electric organ is embryonically derived from immature striated muscle (-sarcoglycan, increased by about 130%, 110%, and 120% in rat soleus muscle (
-Sarcoglycan was not quantified in this work, but we observed significant overexpression (160%) for
-sarcoglycan in slow-type muscles. Recently,
-sarcoglycan might replace
-sarcoglycan in smooth muscle but participate in the skeletal muscle dystrophin complex, as reported recently by
-sarcoglycan abundance in slow-type fibers.
-sarcoglycan complex, including DRP2, ß-sarcoglycan,
-sarcoglycan,
-sarcoglycan with sarcospan and
-dystrobrevin, might be related to the high-strength capacity of this muscle and the absent
-syntrophin might be replaced by other proteins of the syntrophin family (ß or
isoform). In white muscle,
-syntrophin in complex with dystrophin/utrophin,
-sarcoglycan, and
-sarcoglycan might be important for the fish undulatory movement, while the absence of DRP2, ß-sarcoglycan,
-sarcoglycan, and
-dystrobrevin might be compensated for the presence of a 90-kD protein and/or other proteins from the dystrobrevin family. Then, in reference to the work cited above (
To our knowledge, the present study is a rather broad investigation on dystrophin family products present in two different muscle types from the Torpedo caudal region. Due to the loss of the vasoconstrictor response regulation and eventual muscle damage that now appears to be correlated with dystrophin deficiency (
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Acknowledgments |
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Supported in part by grants from INSERM and the Association Française contre les Myopathies (AFM). RM was a Consejo Social University of Alcalá and INSERM postdoctoral fellow over the course of this work.
We are very grateful to Nicole LautrédouAudouy for granting access to the confocal microscope at the Centre de Recherche en Imagerie Cellulaire (CRIC, Montpellier, France). We are also grateful to the fisherman Jacques Lapeyre, who provided us with the live fish.
Received for publication November 9, 2000; accepted February 12, 2001.
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