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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION |
* Department of Animal Sciences, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster 44691; and Department of Animal and Range Sciences, South Dakota State University, Brookings 57007
2 Corresponding author: velleman.1{at}osu.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: glypican • glycosaminoglycan • satellite cell • muscle • turkey
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The ECM was classically described as a structural scaffold in which cells were embedded, but in recent years the ECM has been shown to interact with growth factors and regulate cellular signal transduction pathways involved in tissue growth including skeletal muscle (Velleman, 1999). The ECM is composed of collagenous protein, noncollagenous glycoproteins, and proteoglycans. Proteoglycans are a group of macromolecules, which consist of a core protein attached covalently by one or more carbohydrate chains, called glycosaminoglycans (GAG). Glycosaminoglycans can be classified into heparan sulfate (HS), chondroitin sulfate, dermatan sulfate, and keratan sulfate based on their structure and sequence.
Heparan sulfate proteoglycans (HSPG) are present on the cell surface or in the ECM and can interact with many compounds, including ECM constituents, adhesion molecules, and growth factors (Brandan and Larraín, 1998). They exist in both membrane-associated forms (e.g., syndecans and glypicans) and secreted forms (e.g., perlecan and agrin). Membrane-associated HSPG are attached to the cell membrane by a transmembrane core protein or a glycosylphosphatidylinositol anchor. Two major groups of membrane-associated HSPG, syndecans and glypican-1, are found in skeletal muscle and are likely to be associated with the proliferation and differentiation of muscle cells. Heparan sulfate is posttranslationally added to the proteoglycan core protein at specific serine residues (Bourdon et al., 1987) containing Ser-Gly repeats, and amino acid clusters favoring glycosylation (Zhang et al., 1995).
The presence of HS is required for stable binding of FGF2 to its tyrosine kinase receptor (Rapraeger et al., 1991). The participation of HS in the ternary FGF-receptor signaling complex is facilitated through HS-binding motifs on the FGF2 ligand and the tyrosine kinase receptor (Schlessinger et al., 2000). Fibroblast growth factor 2 is a known stimulator of muscle cell proliferation and an inhibitor of differentiation (Dollenmeier et al., 1981). The syndecan and glypican family proteoglycans have been shown to mediate FGF2 binding to fibroblast growth factor receptors (Steinfeld et al., 1996). Chu et al. (2005) demonstrated that FGF2 binding to HS involves multiple binding sites of variable affinity.
Not only are the HS chains important for FGF2 signal transduction, but it also appears that the proteoglycan core protein may also play a role in the biological function of the membrane-associated HSPG. Cornelison et al. (2004) reported that syndecan-4–/– satellite cell proliferation and differentiation could not be rescued by the addition of exogenous soluble heparin containing all the sequences found in HS. These data suggest that the HS chains and the proteoglycan central core protein are necessary for biological activity during skeletal myogenesis.
Although significant evidence exists for the importance of the proteoglycan HS chains in mediating FGF2 signal transduction, there is a lack of direct evidence for the functional contribution of each HS chain attached to the core protein. Glypican-1 is thought to play a role in muscle differentiation due to its elevated expression at this developmental stage (Brandan and Larraín, 1998; Liu et al., 2006). The turkey glypican-1 core protein has 3 potential sites for the attachment of GAG at serine residues 483, 485, and 487. To investigate the functional contribution of each of these sites in the proliferation, differentiation, and FGF2 responsiveness of turkey myogenic satellite cells, a series of site-directed mutants were produced at 2 or all 3 potential GAG attachment sites at Ser483, Ser485, and Ser487 to obtain 1-chain and no-chain mutants, respectively. These mutants and the intact glypican-1 were then transfected into turkey satellite cells to assay proliferation, differentiation, and FGF2 responsiveness. The results from the current study will provide new information concerning the functional roles of each of the glypican-1 GAG attachment sites in turkey satellite cell myogenesis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Construction of Turkey Glypican-1 Glycosaminoglycan Site-Directed Mutant Expression Vectors and Transient Transfection Procedure
The construction of the turkey glypican-1 expression vector in the pCMS-EGFP vector (BD Biosciences Clontech, Palo Alto, CA) was previously reported by Velleman et al. (2006). The glypican-1 expression vector construct was used as the template for site-directed mutagenesis using the QuickChange Multi Site-Directed Mutagenesis kit (Stratagene Corporation, La Jolla, CA). Turkey glypican-1 contains 3 potential GAG attachment sites at Ser483, Ser485, and Ser487 resulting in a repeat sequence of SerGlySerGlySerGly. The Ser at sites 483, 485, and 487 was converted to threonine to generate all possible 2-chain, 1-chain, and no-chain mutants. Figure 1A
illustrates the site-directed mutagenesis strategy used for generation of site-directed mutants of glypican-1. The glypi-can-1 mutations were confirmed by DNA sequencing.
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Glypican-1 Small Interfering RNA and Transfection
The small interfering RNA (siRNA) sequences targeting turkey glypican-1 were designed using Invitrogen’s BLOCK-iT RNAi designer (https://rnaidesig ner.invitrogen.com/sirna Accessed February 2007). The primer sequences targeting turkey glypican-1 (GenBank accession number AY551002) corresponding to the coding regions 833-851 (5'-CCAACCAAGCTGACCTAAA-3') were 5'-CCAACCAAGCUGACCUAAAdTdT-3' (sense) and 5'-UUUAGGUCAGCUUGGUUGGdTdT-3' (anti-sense). A nonrelated control siRNA that targeted the same region of turkey glypican-1 was used as control. The primer sequences of the control siRNA were 5'-CCAAA-CUCGCAGUCACAAA-3' (sense) and 5'-UUUGUGA-CUGCGAGUUUGG-3' (antisense). Chemically synthesized siRNA were purchased from Invitrogen in the desalted, preannealed duplex form.
The glypican-1 siRNA was transfected into the RBC2 satellite cells using Lipofectamine 2000 (Invitrogen) according to the manufacturer’s recommended conditions. For the proliferation or FGF2 responsiveness assay, 24 h after the plating of the cells, the cultures were transfected with the glypican-1 siRNA or nonrelated control siRNA containing a final concentration of 0.13 µM of each siRNA in 1.5 µL of lipofectamine 2000 contained in 100 µL of Opti-MEM I Reduced Serum medium in a 24-well plate. For the differentiation assay, after 96 h of plating the cultures were transfected with a mixture containing a final concentration of 0.2 µM glypican-1 siRNA or nonrelated control siRNA in 0.3 µL of lipofectamine 2000 contained in 50 µL of Opti-MEM I Reduced Serum medium in a 96-well plate. Cells were incubated in the transfection mixture under antibiotic-free conditions for 6 h at 37°C in a 95% air/5% CO2 incubator. Expression of glypican-1 was determined by quantitative real-time PCR after 48 h of transfection.
Total RNA Extraction, cDNA Synthesis, and Real-Time Quantitative PCR
Forty-eight hours after the transfection with the glypican-1 siRNA, glypican-1 expression vector, and site-directed mutants, total cellular RNA was extracted using TRIzol (Invitrogen) according to the manufacturer’s protocol. The extracted RNA was treated with 1 U of RQ1 RNase-free DNase-I (Promega) per microgram of RNA to remove genomic DNA. The cDNA were synthesized from 1 µg of the DNase-I treated RNA using Moloney murine leukemia virus reverse transcriptase (M-MLV, Promega). In brief, the RNA-primer mix consisting of 1 µL of 50 µM oligo d(T)20 (Operon, Huntsville, AL), 1 µg of total RNA, and nuclease-free water up to 13.5 µL was heated at 70°C for 5 min. The mixture was cooled down on ice for at least 2 min. To the cooled RNA-primer mix 5 µL of 5x first-strand buffer (250 mM Tris-HCl pH 8.3, 375 mM KCl, 15 mM MgCl2, and 50 mM dithiothreitol; Promega), 1 µL 10 mM deoxynucleoside triphosphate mix (Promega), 0.25 µL of RNasin (40 U/µL; Promega), 1 µL of M-MLV (200 U/µL), and nuclease-free water up to 11.5 µL was added. The reaction mixture was incubated at 55°C for 60 min and then heated at 85°C for 5 min to stop the reaction.
The real-time quantitative PCR was performed using the DNA Engine Opticon 2 real-time system (MJ Research, Las Vegas, NV). A non-reverse-transcribed control RNA sample was used with each real-time PCR experiment to check for the absence of genomic or plasmid DNA contamination. Primer sequences for glypican-1 were designed from GenBank accession number AY551002 with a size of 176 bp: forward: 5'-CTTGTCG CTCTGGCAGATCGG-3', reverse: 5'-CTGCTGGAGCC-TTTTGTGCTGA-3'. The primer sequences for glyceraldehyde phosphate dehydrogenase (GAPDH) were designed from GenBank accession number U94327 with a size of 200 bp: forward: 5'-GAGGGTAGTGAAGGCTGC TG-3', reverse: 5'-CCACAACACGGTTGCTGTAT-3' (Operon). The real-time quantitative PCR was performed using DyNAmo Hot Start SYBR Green qPCR kit (Finn-zymes, Ipswich, MA). The PCR reaction consisted of 2 µL of the cDNA, 10 µL of 2x master mix, and 1 µL containing the forward and reverse primers (final concentration 0.25 µM for each primer), and brought to final volume of 20 µL with nuclease-free water. The cycling parameters were denaturation 95°C for 15 min followed by amplification and quantitation (34 cycles of 94°C for 20 s, 60°C for 30 s, and 72°C for 30 s), and final extension of 72°C for 5 min. The melting curve program was 52°C to 95°C, 0.2°C/read, and a 1 s hold. The final PCR products were also analyzed on a 1% agarose gel to check for amplification specificity. Standard curves were performed for every experiment and constructed for glypican-1 and GAPDH with serial dilutions of purified PCR products from each gene. The PCR products were purified by agarose gel electrophoresis using a QIAquick gel extraction kit (Qiagen). The relative concentrations of sample DNA were determined by plotting fluorescence against cycle number of a logarithmic scale. The cycle threshold is the cycle that fluorescence from a sample elevates above the background. The amount of sample cDNA was determined by comparing the results to a standard curve of serial dilutions of purified PCR products of glypican-1. Each gene construct was normalized to the expression of GAPDH and calculated as arbitrary units.
Proliferation Assay
The proliferation assay was performed as previously described by Velleman et al. (2006). In brief, 24 h after plating the cells in 24-well plates, the cells were transfected with glypican-1, 1-chain or no-chain mutants of the glypican-1 expression vector, and the pCMS-EGFP vector as a control. The transfection was performed as described above. After 6 h incubation, transfection solution was removed and replaced with growth medium. Growth medium was McCoy’s 5A (Sigma-Aldrich) containing 10% chicken serum (Invitrogen), 5% horse serum (Invitrogen) with 0.1% antibiotic/antimycotic (Invitrogen). Every 24 h after the transfection for 72 h, plates were removed, wells were rinsed with PBS, and stored at –70°C until assayed. Proliferation was measured by the DNA content in each well as described by McFarland et al. (1995). The DNA concentration was measured by Hoechst 33258 fluorochrome (Sigma-Aldrich) on a Fluoroskan Ascent FL plate reader (ThermoElectron Co., Waltham, MA) using double-stranded calf thymus DNA as the standard.
Responsiveness to Fibroblast Growth Factor 2 Assay
The responsiveness to FGF2 assay was done as previously reported by Velleman et al. (2006). Twenty-four hours after plating the cells in 24-well plates, the cells were transfected with glypican-1, 1-chain or no-chain mutants of the glypican-1 expression vector, and the pCMS-EGFP vector served as a control. After 6 h of incubation, the transfection solution was removed and replaced with serum-free defined media (McFarland et al., 2006) containing 0, 2.5, or 10.0 ng/mL of FGF2 (Pepro Tech, Rocky Hill, NJ). Responsiveness was measured by the DNA content as described in proliferation assay.
Differentiation Assay
The differentiation assay was adapted from Florini (1989) and Yun et al. (1997) with the following modifications. In brief, 24 h after plating the cells in 96-well plates, the cells were transfected with glypican-1, 1-chain or no-chain mutants of the glypican-1 expression vector, and the pCMS-EGFP vector served as a control. The transfection procedure is described above. After a 6-h incubation, the transfection solution was removed and replaced with growth medium. The medium was changed daily until differentiation was induced at 96 h (when the cells reached 65% confluency) by changing the medium to Dulbecco’s Modified Eagle Medium (Sigma-Aldrich) containing 3% horse serum (Invitrogen), 0.1 mg/mL of porcine gelatin (Sigma-Aldrich), and 1.0 mg/mL bovine serum albumin (Sigma-Aldrich) with 10 µg/mL of gentamicin (Invitrogen), and 0.1% antibiotic/antimycotic (Invitrogen). The differentiation medium was changed daily. Every 24 h during the differentiation period, the plates were removed, washed with PBS, and stored at –70°C until analysis. Differentiation was determined by measuring the muscle specific creatine kinase levels as modified from the method of Yun et al. (1997). At the time of the assay, all plates were thawed at room temperature for 10 min. During this time a standard curve of creatine phosphokinase (Sigma-Aldrich) was prepared in a 96-well plate to use as a standard with a range of 0 to 16 mU brought to a final volume of 200 µL in creatine kinase assay buffer (20 mM glucose (Fisher Scientific, Pittsburgh, PA), 10 mM Mg acetate (Fisher Scientific), 1.0 mM adenosine diphosphate (Sigma-Aldrich), 10 mM adenosine monophosphate (Sigma-Aldrich), 20 mM phosphocreatine (Calbiochem, LaJolla, CA), 0.5 U/mL of hexokinase (Worthington Biochemical, Lakewood, NJ), 1 U/mL of glyceraldehyde-6-phosphodihydrogenase (Worthington Biochemical), 0.4 mM thio-nicotinamide adenine dinucleotide (Sigma-Aldrich), and 1 mg/mL of BSA prepared in 0.1 M glycylglycine (Sigma-Aldrich, pH 7.5). To the experimental plates, 200 µL of creatine kinase assay buffer was added to each sample well, and the plates were wrapped in aluminum foil and incubated at room temperature for 10 min. The rate of thio-nicotinamide adenine dinucleotide reduction was read at 6-min intervals in a Dynex MRX Revelation Microtiter Plate Reader (Dynex Technologies Inc., Chantilly, VA) at 405 nm.
Statistical Analysis
All cell experiments were independently replicated at least 3 times. Within each experiment, 4 to 6 replicates of each treatment were performed. Data were summarized as mean ± SEM. All the statistical analyses were performed using Statistical Analysis System for Windows V.9 (SAS Institute, Cary, NC). The cell proliferation assay, differentiation assay, and real-time quantitative PCR data were analyzed using SAS PROC GLM procedures. For the FGF2 responsiveness experiments, FGF2 treatment and variant gene transfections were considered 2 main factors of variance. The main factors of FGF2 treatment and variant gene transfections and the interaction between 2 factors were analyzed using SAS PROC GLM procedures. Differences among means in each experiment were evaluated using an ANOVA and detected using Fisher’s least significant difference. Two-sided P-values of P < 0.05 were considered statistically significant.
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RESULTS |
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). Figure 1B illustrates the changes in nucleotide and amino acid sequences from the site-directed mutagenesis. The RBC2 line turkey satellite cells were transfected with glypican-1, the 1-chain constructs of glypican-1, no-chain construct, and pCMS-EGFP vector as a control (Figure 2A). The transfected cells were analyzed for the expression of each glypican-1 construct compared with the control 48 h after the transfections. All the constructs had a significant increase in expression compared with the control with a range of a 30- to 70-fold increase. Glypican-1 expression was also reduced using a siRNA against glypican-1. Glypican-1 expression was measured 48 h after the transfection with the glypican-1 siRNA and glypican-1 expression was reduced 50% compared with the control siRNA (Figure 2B).
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). However, when FGF2 responsiveness was measured at 72 h the DNA accretion for cultures transfected with glypican-1 containing 2.5 or 10 ng/mL of FGF2 was increased compared with the control, 1-chain, and no-chain mutants except for the 1-chain mutant G1S2 (Figure 4). No significant interaction between FGF2 and the overexpression of glypican-1 was present.
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). At 72 and 96 h of differentiation, the control and no-chain mutant did not differ from the glypican-1 transfected RBC2 satellite cells. In contrast, the 1-chain mutants had a lower differentiation rate compared with the control, glypican-1, and no-chain transfected cells at 72 and 96 h.
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, at 72 h of proliferation, proliferation was decreased in the glypican-1 siRNA transfected cultures. The responsiveness to FGF2 was sensitive to the reduction in glypican-1 expression (Figure 6B). The decrease in glypican-1 expression reduced the proliferation of the RBC2 satellite cells (Figure 6B) as reflected by a decrease in DNA concentration when compared with the control with the addition of FGF2 at 2.5 and 10 ng/mL. Differentiation was reduced by the knock-down in glypican-1 expression beginning at 48 h (Figure 6C).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Turkey glypican-1 contains 3 potential attachment sites for GAG at serine residues 483, 485, and 487. These serine residues are part of an amino acid sequence repeat of SerGlySerGlySerGly. This amino acid sequence has been reported by others to be the preferential acceptor site for xylosyltransferase, the enzyme that initiates the addition of GAG chains (Bourdon et al., 1987; Zhang et al., 1995). The attached GAG chains in the turkey are assumed to be HS similar to other species, but further research addressing the type of GAG chain needs to be done. The potential GAG sites in turkey glypican-1 are located at the C-terminus, which would localize these sites in close proximity to the cell surface. The functional contribution of each of these sites, which may result in the addition of a GAG side chains is not known. For example, do each of these sites for the addition of a GAG chain have an equal functional contribution, or do they have accumulating effects in terms of a cellular response to FGF2?
To study the role of these potential GAG attachment sites, a series of glypican-1 site-directed mutants were produced where the serine amino acids were changed to threonine at amino acid sites 483, 485, and 487. In the current study, glypican-1, the site-directed mutants containing one unaltered GAG attachment site, and the expression construct with all potential GAG sites mutated were overexpressed in RBC2 line turkey satellite cells. The proliferation of RBC2 satellite cells was not affected by the overexpression of glypican-1 or any of the site-directed mutant constructs. However, with increased FGF2 concentration, the glypican-1 transfected cells had enhanced proliferation compared with the control, whereas the mutated constructs of glypican-1, except for the 1-chain mutant G1S2 when stimulated with 2.5 ng/ mL of FGF2, had proliferation levels similar to the control. These results suggest that each of the GAG sites is involved in the cell signaling mediated by glypican-1. The difference in the cell growth characteristics of proliferation and FGF2 responsiveness at 72 h are likely due to the cell culture conditions. The proliferation assay medium contains chicken serum and horse serum. These serums contain a variety of growth factors. In contrast, the FGF2 responsiveness assay is performed in a defined medium in which the only growth factor is FGF2. It is likely that these proliferation changes are due to the addition of exogenous FGF2.
During muscle development the expression of glypican-1 increases during in vitro muscle cell differentiation (Brandan et al., 1996; Liu et al., 2004, 2006) and during the posthatch period of growth up to 12 wk of age in the RBC2 turkey line (Liu et al., 2004). Brandan et al. (1996) also demonstrated that glypican-1 was spontaneously released or shed into the culture medium during the differentiation phase and is maintained on the muscle cell surface. In the present study, at 24 and 48 h of differentiation, the glypican-1 transfection increased differentiation relative to the control and site-directed mutants. Interestingly, by 72 h, the no-chain glypican-1 expression vector construct had a differentiation rate similar to the control and glypican-1. The 1-chain mutants all had lower differentiation rates. These data indicated that the conformation of the glypican-1 molecule may play a significant role in the differentiation process. Fibroblast growth factor 2 is a potent inhibitor of differentiation. The glypican-1 overexpression, as previously shown, results in the early formation of myotubes, which would reduce the available cell number at later stages and decrease the differentiation rate (Velleman et al., 2004, 2006). Because the control and glypican-1 no-chain transfected cells differentiated at a lower rate compared with the glypican-1 overexpressing cultures, it is probable that more cells are available to differentiate and form multinucleated myotubes later in the differentiation process (72 and 96 h). In contrast, differentiation was in general reduced with the 1-chain mutants, suggesting that the GAG chains are important in muscle cell differentiation.
In addition to the data in the present study showing the importance of the GAG attachment sites, the current data also demonstrated that the expression levels of glypican-1 affect muscle proliferation, responsiveness to FGF2, and differentiation. In confirmation of the overexpression studies with glypican-1, the knock-down of glypican-1 showed the reverse effects. In the cultures with reduced glypican-1 expression, proliferation was decreased at 72 h, responsiveness to FGF2 was decreased, and differentiation was decreased. Based on these findings, future studies will need to address the role of the glypican-1 GAG chains and core protein in modulating cell signaling events associated with muscle cell growth and development.
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FOOTNOTES |
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Received for publication April 13, 2007. Accepted for publication May 30, 2007.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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