1Department of Kinesiology, University of Toledo, and 2Department of Pathology, Medical College of Ohio, Toledo, Ohio
Submitted 12 May 2004 ; accepted in final form 11 November 2004
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ABSTRACT |
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inflammation; cytokines; exercise; free radicals
Skeletal muscle contains several cell types (e.g., skeletal muscle cells, endothelial cells, fibroblasts, and resident macrophages) that can produce factors that influence neutrophil chemotaxis and reactive oxygen species (ROS) production (22, 28, 32). Because of this complexity, the cellular source of factors that influence neutrophil responses cannot be identified with in vivo mechanical loading and/or injury models. Previous investigators, however, demonstrated that cultured skeletal muscle cells can produce numerous factors that are known to influence neutrophils (13, 27, 32, 33, 45). Thus mechanical loading of and traumatic injury to cultured skeletal muscle serve as an ideal paradigm for determining the contribution of skeletal muscle cells to neutrophil chemotaxis and ROS production after exercise and muscle trauma.
Although neutrophil-derived ROS are essential for the phagocytosis of pathogens and injured tissue (15), the release of ROS from neutrophils is known to cause injury to a variety of cell types (16, 53), including skeletal muscle cells (31, 39). Stages of ROS production from neutrophils vary from quiescent to primed to fully activated. Priming refers to a process whereby the response of neutrophils to a physiological agonist [e.g., N-formylmethionyl-leucyl-phenylalanine (fMLP)] is potentiated by prior exposure to a priming agent (11, 47). Increased ROS production, on the other hand, only occurs when unprimed or primed neutrophils become fully activated.
Previous investigators demonstrated that circulating neutrophils are primed for ROS production in vivo after both injurious and noninjurious mechanical loading (37, 40, 46) and during the reperfusion of ischemic skeletal muscle (6, 1820). Conflicting results have been reported on whether skeletal muscle injured in vivo by mechanical loading or by reperfusion increases ROS production from blood neutrophils in vitro (6, 7, 37). Whether skeletal muscle cells are the source of primers and/or activators for neutrophil-derived ROS production after mechanical loading and/or injury, however, is unknown.
The primary purpose of the present study was to develop a cell culture model that determines the contribution of differentiated skeletal muscle cells (myotubes) to neutrophil responses after mechanical loading and injury. A secondary purpose was to determine whether mechanical loading and/or injury causes myotubes to release cytokines [tumor necrosis factor- (TNF-
), IL-8, and transforming growth factor-
1 (TGF-
1)] that are known to influence neutrophil chemotaxis and ROS production (8, 12, 24, 42). We hypothesized that myotubes release factors after mechanical loading that cause neutrophil chemotaxis and that prime neutrophils for ROS production in a manner that is dependent on the degree of strain and independent from muscle injury. The release of factors that fully activate neutrophils for ROS production, we hypothesized, would occur only after traumatic and strain-induced myotube injury. Support for our hypotheses would lend credence to our working model, in which the local environment dictates the concentration and the functional outcome of neutrophils in injured and noninjured skeletal muscle after exercise.
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MATERIALS AND METHODS |
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Treatment of myotubes. Myotubes were washed twice with HBSS followed by the addition of 3 ml of DMEM supplemented with 50 µg/ml gentamicin and 50 µg/ml amphotericin-B (basal medium). Myotubes were then exposed to mechanical strain, traumatic injury, or a control condition.
Myotubes were strained for 2 h in a humidified 5% CO2 atmosphere with a vacuum-based system (Flexercell Strain Unit FX 4000; Flexcell International). Specifically, the application of cyclic (0.25 Hz) negative pressure caused the membrane of the tissue culture plate to undergo 5, 10, 20, or 30% maximal elongation. A rubber stopper was applied to control wells to prevent strain of myotubes. Five hours after the protocol was initiated, media were collected, pooled, and stored at 80°C (conditioned media).
Traumatic injury to myotubes was accomplished by tracing a grid that was placed under the tissue culture plate with an 18-gauge sterile needle (scrape injury). The grid consisted of 13 horizontal and 13 vertical lines, which spanned the entire well surface (9.6 cm2) and created squares with 2.5-mm sides. Five hours after the scrape injury protocol was initiated, conditioned media were collected, pooled, and stored at 80°C.
Myotube injury. Myotube injury was quantified by measuring lactate dehydrogenase (LDH) in conditioned media according to the manufacturer's instructions (Promega, Madison, WI). Incubating myotubes with 0.5% Triton X-100 solution for 45 min induced total LDH release. An injury index was calculated using the following equation: [(e b)/(t b)], where e is LDH release from myotubes exposed to strain or scrape injury, b is LDH release from control myotubes, and t is total release from Triton X-100-treated myotubes.
Transmission electron microscopy was performed to assess myotube membrane integrity 5 h after the 10 and 30% strain protocols were initiated. Briefly, myotubes were washed in 0.1 M cacodylate buffer (pH 7.4) and then fixed in 3% glutaraldehyde-1% lanthanum chloride. Primary fixation was performed at room temperature for 2 min, followed by a 2-h incubation at 4°C. After being washed in cacodylate buffer, myotubes were immersed in 2% osmium tetroxide-1% lanthanum chloride at 4°C for 1 h and rinsed with 2,4,6-collidine-1% lanthanum chloride. Dehydration was accomplished by immersing monolayers in a series of increasing-purity ethanol solutions. Acetone was briefly used as the transitional fluid, followed by a 15-min immersion in 50% Spurr's embedding medium and an overnight infiltration in 100% Spurr's resin at 80°C. Monolayers were then removed from the plates and cut into smaller pieces, and thin sections (900 Å) were obtained with a diamond knife. Monolayers were not stained with uranyl acetate and lead citrate to enhance lanthanum visualization. Observations were made with a CM10 transmission electron microscope (Philips) at an accelerating voltage of 80 kV.
Neutrophil isolation. Heparinized venous blood was obtained from healthy volunteers after written informed consent was obtained. Heparinized blood was layered over a density gradient (1-step Polymorphs; Accurate Chemical, Westbury, NY) and centrifuged to isolate neutrophils from mononuclear and red blood cells as previously described (31, 39). Neutrophils were then suspended in either basal medium or conditioned medium. The isolation procedures routinely yielded >97% neutrophils with cell viability >98% as determined by Trypan blue exclusion. After isolation procedures, neutrophils were used immediately for a neutrophil assay. Neutrophils collected from each donor were used only once for a given neutrophil assay.
Neutrophil chemotaxis.
Neutrophil chemotaxis was measured in a 48-well chamber (Neuro Probe, Gaithersburg, MD). The lower wells of the chamber were loaded in quadruplicate with fMLP (107 M; Sigma), basal medium, conditioned medium, recombinant human (rh)IL-8 (BD Biosciences, San Diego, CA), or human (h)TGF-1 (derived from human platelets; R&D Systems). All media were supplemented with 1% bovine serum albumin. A 3-µm-pore polyvinylpyrrolidone-free polycarbonate filter (Neuro Probe) was placed between the upper and lower chambers. Neutrophils, suspended in basal medium (3.2 x 106/ml), were added to the upper wells, and the chamber was placed in a humidified environment (5% CO2 and 37°C) for 30 min. Nonmigrated neutrophils were removed from the top surface of the filter by washing with phosphate-buffered saline and by scraping against a rubber edge. Migrated neutrophils were fixed in absolute methanol and visualized with Wright-Giemsa stain (Fisher Scientific, Pittsburgh, PA). The total number of neutrophils in 20 high-power fields (x1,000) per well was counted and averaged for each subject. Partially migrated neutrophils and contaminating leukocytes were not counted. Neutrophil chemotaxis was expressed as a chemotactic index with the following equation: [(conditioned medium basal medium)/(fMLP basal medium)] x 100. The inclusion of fMLP, a potent chemoattractant for neutrophils, served as a positive control in the equation.
A checkerboard analysis using 30% strain medium was performed to ensure that the observed responses were attributable to neutrophil chemotaxis as opposed to chemokinesis (random migration) (1). Briefly, the upper wells of the chemotaxis chamber were loaded with neutrophils suspended in undiluted 30% strain medium, half-diluted 30% strain medium, or basal medium. Neutrophils were allowed to migrate for 30 min toward undiluted 30% strain medium, half-diluted 30% strain medium, or basal medium, which was loaded into the lower wells of the chamber. Neutrophil chemotaxis was then determined as described above.
Neutrophil-derived O2·. The ability of conditioned media to prime and to activate neutrophils for O2· production was quantified with the cytochrome c assay (2, 29). Neutrophil priming was evaluated by suspending neutrophils (3.5 x 106/ml) in basal medium, conditioned media, or LPS (Escherichia coli 0127:B8, 100 mM) in basal medium for 2 h and then assaying for O2· production in the presence of fMLP (2.5 x 106 M) after a 10-min incubation. Activation of O2· production was assessed by suspending neutrophils (3.7 x 106/ml) in either basal or conditioned medium and then pipetting them into polypropylene tubes or fibronectin-coated wells (2 µg/well).
The O2· assay consisted of running two sets of triplicate polypropylene tubes or fibronectin-coated wells. SOD (90 µg/ml, bovine erythrocytes; Sigma) was added to one set of tubes or wells, and an equal volume of HBSS was added to the other set. Ferricytochrome c (80 µM, horse heart; Sigma) was added to all tubes or wells, and the samples were then incubated at 37°C in a shaking water bath or a plate reader (SpectraMAX 190; Molecular Devices). For evaluation of the ability of conditioned media to increase O2· production for neutrophils in suspension, catalase (1,000 U/ml; Sigma) and S-ethylisothiourea (a nitric oxide synthase inhibitor, 1,000 µM; Sigma) were added to all tubes to prevent the reoxidation of ferrocytochrome c by hydrogen peroxide and nitric oxide, respectively (48, 51). Catalase and S-ethylisothiourea were not added to fibronectin-coated wells because 1) we recently reported (31) that human neutrophils do not produce nitric oxide via nitric oxide synthase and 2) pilot experiments revealed that the inclusion of catalase in conditioned media did not improve our detection of O2· when neutrophils were adherent to fibronectin, an observation that was in contrast to pilot experiments using neutrophil suspensions. The optical density of the supernatant or well was read spectrophotometrically at 550 nm. The quantity of O2· produced was calculated from the difference in the mean absorbance of tubes or wells that were without SOD from those with SOD and by using the extinction coefficient for ferrocytochrome c (29.5 mM/cm). A neutrophil count was performed on the final cell preparation, and O2· production was expressed as nanomoles of O2· per 5 x 105 neutrophils.
Cytokines.
IL-8 (BD Biosciences), TGF-1 (Promega), and TNF-
(BD Biosciences) concentrations in conditioned media were quantified with ELISA kits according to the manufacturer's instructions (n = 56 wells/condition). The concentration of active TGF-
1 was determined by omitting the acidification and neutralization steps as recommended by the manufacturer.
Statistics.
Separate analysis of variance was used to evaluate the influence of mechanical strain and traumatic injury on neutrophil chemotaxis, ROS production, and cytokine concentrations in conditioned media. Neuman-Keuls post hoc test was used when a significant F ratio was observed (P 0.05). Data are reported as means ± SE.
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RESULTS |
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We next tested whether neutrophil priming is a prerequisite for 30% strain medium to increase O2· production from neutrophils in suspension. For these experiments, neutrophils were primed with unconcentrated 30% strain medium for 2 h and then assayed for their ability to produce O2· after a 10-min exposure to either concentrated control or concentrated 30% strain medium. These experiments (n = 6) also failed to demonstrate an activating effect for 30% strain medium (data not reported).
Because previous investigators reported that the kinetics and the magnitude of ROS production elicited by some cytokines [e.g., TNF- and granulocyte-macrophage colony-stimulating factor (GM-CSF)] is enhanced when neutrophils are adherent to the extracellular matrix protein fibronectin (12, 3436), we also assessed the ability of conditioned media from strained myotubes to increase O2· from neutrophils adherent to fibronectin. Conditioned media from myotubes exposed to 5, 10, 20, and 30% strain failed to increase O2· from neutrophils adherent to fibronectin relative to control medium (Fig. 9).
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DISCUSSION |
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Neutrophil chemotaxis was sensitive to the magnitude of strain and occurred in the absence of muscle injury. This finding is in agreement with our previous in vivo observations. Specifically, we reported (30, 38) that passive stretching, isometric contractions, and concentric contractions, which do not cause overt injury, elevated neutrophils in skeletal muscle in the hours to days after the activity. The blunted neutrophil chemotaxis elicited by noninjurious relative to injurious strain in the present study is also consistent with the lower concentration of neutrophils after passive stretching and isometric contractions relative to injurious lengthening contractions (38). Thus both mechanical loading and loading-induced injury are potent stimuli for the release of one or more factors from skeletal muscle cells that cause neutrophil chemotaxis.
While migrating to sites of inflammation, human neutrophils can be primed in vivo for ROS production in vitro after injurious and noninjurious exercise (37, 40, 46). In the present study, neutrophil priming for O2· production occurred after noninjurious strains (10 and 20%) and was not elevated further by a higher, injurious, strain magnitude (30%). These observations suggest that beyond a threshold of mechanical strain, myotube-induced neutrophil priming is not sensitive to the magnitude of strain or the presence of muscle injury. The lack of specificity and sensitivity for muscle injury may indicate that neutrophil priming merely serves as a preparative stage for ROS production while neutrophils are in transit to their final destination within skeletal muscle. At their final destination, neutrophils may, in the case of overtly injured muscle, encounter soluble agonists and/or immobilized ligands that increase their production of ROS. Interestingly, priming for neutrophil-derived ROS production has been reported to be a reversible event (25). The reversal of priming, in the absence of factors that increase ROS production from neutrophils, may serve as a protective mechanism to prevent neutrophils from injuring cells via the release of ROS (11, 25).
We hypothesized that the microenvironment of skeletal muscle injured by strain and trauma contains one or more soluble factors that increase O2· production from neutrophils. Our results partially support this hypothesis by demonstrating that scrape injury, but not injurious nor noninjurious strain, caused myotubes to release factors that increased O2· production from neutrophils. The inability of conditioned medium from strain-injured myotubes to increase O2· production from neutrophils was not attributable to a suboptimal concentration of potential agonists or to neutrophil priming, because concentrated media failed to increase O2· production from unprimed and primed neutrophils. Although previous investigators reported that the potency of TNF- and GM-CSF is enhanced when neutrophils are adherent to fibronectin (12, 3436), we also failed to observe a significant influence of strain media on O2· production from neutrophils adherent to fibronectin. Together, the ability of injured myotubes to release one or more factors that increase O2· production from neutrophils appears to be dependent on the nature of the injury (strain vs. trauma) and/or the magnitude of the injury.
Functional activities of neutrophils are controlled by cytokines, ELR+ CXC chemokines, complement proteins, lipid derivatives, extracellular matrix proteins, and adhesion molecules (8, 15). Interestingly, cultured skeletal muscle has been reported to produce several neutrophil chemoattractants and/or modulators of neutrophil-derived ROS production from each of these categories. For example, protein levels of IL-1, IL-6, IL-8, IL-15, GM-CSF, TGF-, monocyte chemoattractant protein-1, and fibroblast growth factor have all been reported to be released from cultured skeletal muscle (myoblasts and/or myotubes) under control conditions, after treatment with inflammatory cytokines (e.g., IL-1
and TNF-
) (9, 13, 33, 45), or after mechanical strain (10). Furthermore, cultured myoblasts and/or myotubes express various components of the complement pathway (27) and produce lipid derivatives (e.g., prostaglandins) (52) with chemotactic and ROS-inducing potential. Thus there is compelling evidence that skeletal muscle cells produce an array of factors that are capable of influencing neutrophil responses after mechanical loading and/or injury.
Our initial approach to identifying candidates for the observed responses was to quantify selected factors in conditioned media. To our surprise, IL-8, a potent chemoattractant and primer for ROS production from neutrophils (8), was reduced by mechanical loading and traumatic injury. In addition, rhIL-8 at concentrations of IL-8 observed in conditioned media failed to elicit neutrophil chemotaxis. These later observations are consistent with previous investigators who demonstrated that rhIL-8 causes neutrophil chemotaxis at much higher concentrations (10 ng/ml80 µg/ml) than concentrations of IL-8 observed in our conditioned media (1070 pg/ml) (23, 24). Because TGF-
1, a potent neutrophil chemoattractant and a modest activator of ROS production from adherent neutrophils (3, 42), has been reported to inhibit the synthesis of IL-8 (44), we then measured TGF-
1. The concentration of total TGF-
1 in conditioned media was also reduced by mechanical loading, whereas the active form remained unchanged. Furthermore, hTGF-
1 at concentrations of TGF-
1 observed in conditioned media failed to significantly increase neutrophil chemotaxis. These observations are in agreement with previous investigators who demonstrated that neutrophil chemotaxis in vitro reaches maximal levels at
1 pg/ml TGF-
1 and declines rapidly with higher concentrations (5, 17, 42). The concentration of TNF-
, which can increase ROS production from adherent, but not suspended, neutrophils (12, 35, 43), was not influenced by mechanical loading or injury. The concentrations of TNF-
observed in conditioned media (<20 pg/ml) were much lower than concentrations (0.1100 ng/ml) that have been reported to increase ROS production from neutrophils (12, 35, 43). Together, our observations suggest that factors other than IL-8, TGF-
1, and TNF-
are probably orchestrating the observed neutrophil responses after mechanical strain and/or injury to myotubes.
The present study demonstrates that mechanical loading and/or injury influences the immunobiology of skeletal muscle cells in a manner that differentially influences neutrophil chemotaxis and the stages of neutrophil-derived ROS production. This sophisticated level of interplay may serve as a mechanism by which the microenvironment of skeletal muscle dictates the concentration and the functional outcome of neutrophils in injured and noninjured skeletal muscle after exercise. Further work is needed to identify the skeletal muscle-derived factors that orchestrate neutrophil chemotaxis, priming, and ROS production after mechanical loading and traumatic injury. Once the skeletal muscle-derived factors have been identified, therapeutic and/or pharmacological strategies could be developed to manipulate the immunobiology of skeletal muscle to minimize any negative consequences of neutrophils in skeletal muscle.
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GRANTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
* S. K. Tsivitse and E. Mylona contributed equally to this work.
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