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1 Laboratoire d'étude de la croissance cellulaire, régénération et réparation tissulaires, FRE 2412 CNRS, Université Paris 12, Créteil, France 2 Université Paris 5, Paris, France
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Abstract |
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(Received 6 January 2005;
accepted after revision 21 February 2005; first published online 22 February 2005)
Corresponding author A. Ferry: Laboratoire d'étude de la croissance cellulaire, régénération et réparation tissulaires, UMR 7149 CNRS, Université Paris 12, Créteil, France. Email: ferry{at}univ-paris12.fr
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Introduction |
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B, is thought to orchestrate the gene expression programmes promoting inflammation and leading to leucocyte adhesion, cytokine and chemokine production, and induction of nitric oxide synthase (Lille et al. 2001). NF-B can be activated by free radicals, especially reactive oxygen species, which are likely to be produced during muscle injury (Zerba et al. 1990; Lille et al. 2001; Brickson et al. 2003; Kumar et al. 2003; Nguyen & Tidball, 2003). It has been proposed that some components of the inflammatory response to injury are responsible for the increase in muscle function deficit (Hirose et al. 2001; Lapointe et al. 2002; Brickson et al. 2003). It was reported that some inflammatory cells, i.e. neutrophils, in vitro injure myotubes, especially through the production of free radical/oxidant (McLoughlin et al. 2003; Nguyen & Tidball, 2003). Early treatments of muscle injury have therefore been aimed at inhibiting the inflammatory response to alleviate the signs of inflammation and provide pain relief (reviewed by Almekinders, 1993). A recent review (Connolly et al. 2003) concludes that non-steroidal anti-inflammatory drugs have a role in the short-term treatment of muscle injury in humans. Experiments in animal models also provided evidence that administration of anti-inflammatory and antioxidant drugs (NSAIAODs; diclofenac, flurbiprofen, piroxicam and EPC-K1 (a combination of vitamins C and E)) decrease the muscle function deficit that is observed a few days after injury (Zerba et al. 1990; Obremsky et al. 1994; Mishra et al. 1995; Hirose et al. 2001; Lapointe et al. 2002, 2003).
In contrast, it is widely accepted, that inflammatory cells play an important role in muscle fibre repair (Lescaudron et al. 1999; Teixeira et al. 2003). Macrophages, in particular, not only remove cellular debris (Tidball, 1995) but also produce cytokines and chemokines, which act on various cells such as inflammatory cells and satellite cells, the muscular progenitor cells (Merly et al. 1999; Warren et al. 2004). Therefore, one could expect that long-term NSAIAOD administration might have detrimental effects by reducing the inflammatory response required for efficient muscle healing. However, scarce information exists on the long-term effects of NSAIAOD treatment on the recovery of muscle function in animals and the few published studies have focused on only one type of injury, i.e. exercise-induced injury (Mishra et al. 1995; Lapointe et al. 2002, 2003).
We report here the results of experiments in the mouse aimed at assessing the outcome of NSAIAOD treatment on long-term recovery after severe muscle injury leading to significant cell death. In order to have a wider insight on the potential effects of these drugs, the experimental conditions were varied. We used different NSAIAODs (diclofenac, diferuloylmethane, dimethylthiourea, dimethyl sulphoxide, indomethacin and pyrrolidine dithiocarbamate) exhibiting various anti-inflammatory and antioxidant properties (Table 1). For example, they may inhibit cyclo-oxygenases which are responsible for prostaglandin production, have antioxidant properties, and/or block the activation of NF-B (Jacob & Herschler, 1986; Thaloor et al. 1999; Kinugawa et al. 2000; Lille et al. 2001; Surh et al. 2001; Tegeder et al. 2001; Lapointe et al. 2002). Since the inflammatory response may vary with the type of lesion (see Discussion; Lefaucheur & Sebille, 1995), the drugs were tested in two different models of severe muscle injury, i.e. myotoxic treatment or crush. To our knowledge, no studies have analysed the effect of NSAIAOD administration on functional muscle recovery after severe muscle injury. For each type of muscle injury, animals were treated with diclofenac or indomethacin (cyclo-oxygenase inhibitors), dimethylthiourea or dimethyl sulphoxide (antioxidants), or diferuloylmethane (cyclo-oxygenase inhibitor, antioxidant and NF-B inhibitor). In addition, myotoxic injured muscles were also treated by pyrrolidine dithiocarbamate (antioxidant and NF-B inhibitor). The long-term recovery of regenerating muscles was evaluated several weeks after injury by examining histological and biochemical parameters and muscle function. Our findings do not support the hypothesis that NSAIAOD administration influences muscle recovery in a detrimental way.
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Methods |
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All procedures were performed in accordance with national and European legislation. Male Swiss mice (15–20 g) were purchased from Janvier (Le Genest Saint l'Isle, France). After at least 7 days of acclimation, the animals were anaesthetized with pentobarbitone (60 mg kg–1, I.P.). The left tibialis anterior (TA) muscle of each mouse was injured by one of two means. Either it was injected with 20 µl of normal saline containing a myotoxic agent (2 µg per muscle of snake venom from Notechis scutatus scutatus, V-0251, Sigma-Aldrich), or it was mildly crushed twice during 5 s with forceps from the distal tendon to the proximal extremity. The contralateral TA muscle was left intact and was used as an uninjured control muscle.
NSAIAOD treatments
Several separate experiments were performed to determine the effect of different drugs which exhibit various anti-inflammatory and antioxidant properties (Table 1). Groups of four to eight mice were injected intraperitoneally daily with 10 ml (kg body weight)–1 of 0.02, 0.2, 2 or 50 mg kg–1 diferuloylmethane (DFM, curcumin), or 30 mg kg–1 pyrrolidine dithiocarbamate (PDTC), or 50 mg kg–1 dimethylthiourea (DMTU), or 0.2 or 2 mg kg–1 indomethacin, or 30 mg kg–1 diclofenac, or 6 ml kg–1 dimethyl sulphoxide (DMSO), or vehicle. Drugs were generally dissolved in normal saline, except indomethacin (vehicle: 0.1 M Na2CO3, pH 7.4). For DFM treatment, DMSO (6.6 µl kg–1) was added to the vehicle. Drug injections generally began on the day of the injury and ended 24 h before the muscle was studied, with the following exception: when muscles were studied 42 days after injury, mice were treated only during the first 2 weeks. Drugs were purchased from Sigma-Aldrich (Lyon, France). Solutions were prepared immediately before being injected.
Contractile measurements
Several days after muscle injury (as specified in the Results), animals were anaesthetized (pentobarbitone, 60 mg kg–1, I.P.). The in situ isometric contractile properties of left (injured) and right (contralateral, uninjured) TA muscles were studied. The distal tendon was attached to an isometric transducer (Harvard Bioscience, Les Ulis, France) using a silk ligature. The body temperature was maintained at about 37°C by means of heating lamps. The muscle nerves (proximally crushed) were stimulated by a bipolar silver electrode using a supramaximal square-wave pulse of 0.1 ms duration. In some instances, muscles were directly stimulated in order to determine whether the induction of muscle injury also led to nerve injury and nerve–muscle transmission failure. Measurements were made at L0 (length at which maximal tension was obtained during the twitch). Submaximal (P50Hz; stimulation frequency of 50 Hz) and maximal (P0; stimulation frequency of 75–143 Hz) isometric forces were successively recorded and analysed on a personal microcomputer, using the PowerLab system and Chart 4 software (AD Instruments, Paris, France). Specific maximal force (sP0) was also calculated (sP0 = P0 (mN)/muscle mass (g)). After contractile measurements, animals were killed with an overdose of pentobarbitone. Muscles were then weighed, precooled in isopentane (for histology) or not (for biochemistry), frozen in liquid nitrogen, and stored at –80°C until histology or biochemical analysis.
Histology
Transverse serial sections of muscles (10 µm) obtained using a cryostat were stained with Gomori trichrome solution (Gabe, 1968). Images of muscle sections were acquired using a video camera mounted on a bright-field microscope and attached to a personal microcomputer.
Electrophoresis and immunoblotting
The expression of fast myosin heavy chain was analysed. Briefly, frozen muscle samples were homogenized in buffer solution (pH 6.5) containing 0.25 mM sucrose, 20 mM Hepes, and a mixture of protease inhibitors (P8340, Sigma) precooled in ice. Aliquots were stored at –20°C until protein content analysis (protein assay system kit 600-0005, Bio-Rad) was performed. Vertical sodium dodecyl sulphate polyacrylamide gel electrophoresis was performed using a mini-protean II electrophoresis apparatus (Bio-Rad). The homogenates were combined with an equal volume of denaturing buffer (2 x Laemmli buffer) and boiled for 3 min. For each sample, 5 µg of protein were loaded per lane. Stacking and separating gels contained 4 and 8% acrylamide, respectively. After electrophoresis, proteins were electroblotted to polyvinylidene fluoride (PVDF) membranes (Millipore). The membranes were probed with the primary monoclonal antibody specific for fast MHC (NCL-MHCf Novocastra, Newcastle upon Tyne, UK). Membranes were then incubated with secondary antibody specific for mouse IgG conjugated with peroxydase. The immunoreactivity was detected by chemiluminescence as indicated by the manufacturer (1500-708, Boehringer Mannheim, Meylan, France). The signal intensity of bands was quantified using densitometry (ChemiGenius, Syngene Cambridge, Ozyme, Montigny le Bretonneux). The data were expressed relative to an internal standard sample.
Statistical analysis
Data were analysed using Statistica 5.5 software (StatSoft, Paris, France). Groups were compared using non-parametric Wilcoxon or Mann–Whitney tests. Values are medians (25–75% centiles). Since there was no effect of the different treatments on contralateral uninjured muscles, some values are only expressed relative to those of uninjured contralateral muscles (% contralateral).
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Results |
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We injected a myotoxic agent into the left TA muscles of mice and the right TA were left uninjured. We found that 5 days after injury, submaximal (P50Hz) and maximal (P0) force production was abolished in injured muscles of vehicle-treated mice (Table 2, P < 0.05). Accordingly, nearly all muscle fibres were destroyed by the myotoxic agent (Fig. 1B). Muscle recovery was not completed at day 10 or 14. Ten or 14 days after injury, muscle mass and force productions (Table 2, and data not shown) and the size of regenerating muscle fibres (Fig. 1D, F and H) of the injured muscles of vehicle-treated mice were still reduced compared to that of uninjured (contralateral) muscles.
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Crush injury
In a further series of experiments, we wanted to test the effect of NSAIAODs using a different model of muscle injury. Left TA muscles were mildly crushed instead of being injected with a myotoxic agent. Five days after injury, force production was reduced in the injured muscles of vehicle-treated mice (Table 3). About 40% of the muscle cross-sectional area exhibited damage (data not shown). Forty-two days after injury P50Hz, but not P0 or sP0, of vehicle-treated mice was still significantly reduced compared to that of the contralateral muscles (Table 3, P < 0.05). The smaller muscle fibres in injured muscle compared to contralateral uninjured muscle of vehicle-injected mice (data not shown) confirmed that muscle recovery was not complete, even 42 days after injury. However, the level of fast MHC expression was fully regained 42 days after injury: for injured muscle of vehicle-treated mice it was 96.7% (87.5–106.9%) of the contralateral muscle (P > 0.05).
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In subsequent experiments, mice were treated with high doses of DFM (50 mg kg–1), indomethacin (20 mg kg–1) or DMSO (6.6 ml kg–1). These treatments had no effect on the contralateral uninjured muscles (data not shown). We also observed that treatment with DMSO had no effect on the recovery of injured muscles, 14 days after crush injury (Fig. 2A). In contrast, five out of eight and six out of seven mice treated, respectively, with 50 mg kg–1 DFM or 20 mg kg–1 indomethacin died, whereas no deaths occurred before the end of the experiment (14 days after crush injury) in the groups of mice treated with 6.6 ml kg–1 DMSO or vehicle. The body weight of the mice treated with DFM and DMSO was decreased compared to mice treated with vehicle (data not shown, P < 0.05). In the three mice surviving the treatment with 50 mg kg–1 DFM, the force recovery of crushed muscles 14 days after injury was lower compared to the other groups of mice (Fig. 2A, P < 0.05). Moreover, in these DFM-treated mice, the regenerating muscle fibres were scarce and of decreased size compared to those of mice treated with DMSO or vehicle (data not shown). Expression of fast MHC (Fig. 2B and C) in injured muscles was also reduced in the DFM-treated mice compared to mice treated with DMSO or vehicle (P < 0.05).
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Discussion |
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In the case of steroid anti-inflammatory drugs, it has been clearly shown that high doses severely decrease muscle regeneration after injury (Noirez et al. 1999), whereas low doses of glucocorticoids do not markedly affect regeneration (Mitchell et al. 1991). In addition to their anti-inflammatory action, it is well known that glucocorticoids alter muscle growth and induce atrophy (Almon & Dubois, 1990). In the present study, we tested several types of non-steroidal drugs exhibiting different anti-inflammatory and antioxidant properties (Table 1). DFM, diclofenac and indomethacin reduce the synthesis of prostaglandins by inhibiting the two isoforms of cyclo-oxygenases (COX-1 and COX-2; Surh et al. 2001; Tegeder et al. 2001; Lapointe et al. 2002). DMTU, PDTC and DMSO are antioxidant drugs, as is DFM; for example they may have free-radical scavenging properties (Jacob & Herschler, 1986; Kinugawa et al. 2000; Lille et al. 2001; Surh et al. 2001). In addition, DFM and PDTC block the activation of NF-B (Thaloor et al. 1999; Lille et al. 2001; Surh et al. 2001), which is not the case for indomethacin and diclofenac (Tegeder et al. 2001).
The number of accumulated cells in the damaged muscle reaches a maximum a few hours (neutrophils) or days (macrophages) after myotoxic or crush injuries (Lefaucheur & Sebille, 1995; Pimorady-Esfahani et al. 1997; Teixeira et al. 2003). In the present study, it was expected that treatment with NSAIAODs would diminish this accumulation of inflammatory cells into the damaged muscle and reduce the production of free radicals/oxidants, prostaglandins, cytokines and chemokines in the first few days following injury. Since the inflammatory response is thought to play a role not only in degeneration but also in muscle repair (Tidball, 1995; Lescaudron et al. 1999; Merly et al. 1999; Teixeira et al. 2003; Warren et al. 2004), we therefore hypothesized that long-term NSAIAOD treatment would markedly reduce the subsequent muscle recovery after severe injury. We report here for the first time that there is no evidence of any detrimental effect of these drugs on long-term functional muscle recovery (maximal and submaximal force production) after myotoxic or crush injuries in mice, except when using NSAIAODs at lethal doses (see below). Histological and biochemical muscle parameters confirmed this lack of detrimental effect on force recovery. The present study extends previous results showing that ibuprofen treatment did not inhibit the long-term muscle growth and maturation after myotoxic injury in the rat (Noirez et al. 2000). In keeping with our observations, two recent studies reported that diclofenac treatment did not blunt complete force recovery 4 weeks after exercise-induced injury in the rat (Lapointe et al. 2002, 2003). In contrast, Mishra et al. (1995) found a slight deficit in muscle force 4 weeks after exercise-induced injury in rabbits treated with flurbiprofen. The discrepancies between these studies are not yet explained but may be due to species differences.
We did not study the reasons why the long-term effect of non-toxic doses of NSAIAODs was negligible. It is unlikely that effective effects would require higher NSAIAODs doses. For DFM and indomethacin, mice were treated with such high doses that several animals died before the end of the study. A need of a longer period of treatment is not pertinent since NSAIAODs were administrated for 2 weeks and by this time muscle inflammation had very probably resolved (Lefaucheur & Sebille, 1995; Pimorady-Esfahani et al. 1997; Teixeira et al. 2003). Despite the fact that administration of one NSAIAOD alone had no effect, it is possible that a combination of different NSAIAODs would be more potent. For example, hydrophilic and lipophilic antioxidants, such as vitamins C and E, showed an enhanced effect when coadministrated (Chaudiere & Ferrari-Iliou, 1999; Hirose et al. 2001; Gao et al. 2002).
The possibility that NSAIAODs decrease both muscle degeneration and subsequent repair cannot be excluded. There is evidence that NSAIAODs may reduce muscle damage in the case of exercise-induced damage or ischaemia–reperfusion injury (Zerba et al. 1990; Obremsky et al. 1994; Mishra et al. 1995; Hirose et al. 2001; Lille et al. 2001; Lapointe et al. 2002, 2003). However, this explanation is only partly relevant to the lack of effect of NSAIAODs after crush injury but not after myotoxic treatment, since diclofenac has previously been reported not to reduce myonecrosis after myotoxic injury (Miyabara et al. 2004). It is also possible that the drugs used here did not effectively decrease the inflammatory response in the damaged muscle (Almekinders, 1993). According to recent studies, it is not clear whether NSAIAOD treatments genuinely have anti-inflammatory and antioxidant effects after muscle injury. NSAIAODs neither reduced accumulation of neutrophils (Mishra et al. 1995) and macrophages (Mishra et al. 1995; Cheung & Tidball, 2003) nor lowered prostaglandin E2 levels in injured muscle (Trappe et al. 2001). One explanation may be that these drugs do not efficiently inhibit COX-2, which plays a crucial role in the accumulation of inflammatory cells after muscle injury (Bondesen et al. 2004). Finally, besides their effects on inflammation, NSAIAODs might interfere with muscle biology through quite different mechanisms. For instance, NF-B, which can be inhibited by several NSAIAODs (Thaloor et al. 1999; Lille et al. 2001; Surh et al. 2001), plays a role in myogenesis and muscle growth/atrophy (Thaloor et al. 1999; Guttridge et al. 2000). It is also known that DMSO (Blau & Epstein, 1979) and prostaglandins, which are inhibited by indomethacin, may affect myogenesis and protein turnover in muscle (Rodemann & Goldberg, 1982; Horsley & Pavlath, 2003).
In contrast, we observed marked effects when high doses of DFM (50 mg kg–1) or indomethacin (20 mg kg–1), which proved to be lethal for most of the animals, were administrated. Moreover, muscle function, muscle histology and fast MHC expression were altered by high doses of DFM. We noted that mice treated with high doses of DFM or 6.6 ml kg–1 DMSO (the vehicle of 50 mg kg–1 DFM) had decreased body weight. It is known that DMSO alone can have behavioural, neurotoxic and myotoxic effects (Kranz et al. 2001). However, a high dose of DFM had deleterious effects that were not observed with 6.6 ml kg–1 DMSO alone. This toxic effect could be related to the fact that DFM reduces serum and liver lipid (Asai & Miyazawa, 2001). Lipid-lowering agents, e.g. fibrates and statins, have previously been implicated in rhabdomyolysis and myopathy (reviewed by Hodel, 2002).
Conclusion
Non-steroidal anti-inflammatory drugs are frequently prescribed after skeletal muscle injury. We demonstrate for the first time that NSAIAOD administration (at non-lethal doses) does not affect the long-term muscle repair after myotoxic or crush injuries in mice, although the inflammatory response is thought to play an important role in this process. In future studies it will be interesting to clarify the precise role of the inflammatory response in muscle degenerative and regenerative phases.
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