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MUSCLE CELL BIOLOGY AND CELL MOTILITY
Department of Kinesiology, The University of Toledo, Toledo, Ohio
Submitted 17 April 2008 ; accepted in final form 21 August 2008
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ABSTRACT |
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skeletal muscle growth; neutrophils; macrophages; compensatory hypertrophy
In compensatory hypertrophy models, neutrophils and macrophages accumulate in skeletal muscle (3, 10, 46) when signs of satellite cell proliferation (1, 31, 41) and signaling for protein synthesis (52) are also evident. This temporal association may indicate that neutrophils and/or macrophages contribute to muscle hypertrophy. Neutrophils and macrophages could influence hypertrophy by producing factors (e.g., cytokines and reactive oxygen species; ROS) that influence satellite cells and/or protein balance in skeletal muscle (14, 17). Indeed, macrophages and/or their derived products promote proliferation of cultured myoblasts (7, 8), aid regrowth of injured skeletal muscle (7, 44), and appear to be required for compensatory hypertrophy (10).
A potential mechanism by which neutrophils and/or macrophages could influence hypertrophy is via activation of β2-integrins (CD11/CD18), which are heterodimers exclusively expressed by cells of the hematopoietic lineage (23). β2-Integrins are important to the inflammatory response because they control the entry of neutrophils into tissues and the ability of neutrophils and monocytes/macrophages to produce ROS and cytokines (9, 22, 27, 29, 30, 37, 48, 49). Several cytokines that appear to be controlled by β2-integrins [e.g., tumor necrosis factor-
(TNF-) interleukin (IL)-6, IL-1β, and transforming growth factor β1 (TGF-β1)] (9, 29, 30, 49) have been reported to be elevated in hypertrophying skeletal muscle (16, 46) and to influence satellite cells, protein synthesis, and/or protein degradation (14, 17). A role of β2-integrins in controlling cytokine production in skeletal muscle is indicated by Hamada et al. (13), who reported significant correlations between transcript levels of CD18 and TNF-, IL-6, IL-1β, and TGF-β1 in human skeletal muscle after exercise. Thus, β2-integrin signaling in neutrophils and/or macrophages could influence hypertrophy induced by mechanical loading.
In the present study, we used the synergist ablation model to test the hypothesis that β2-integrins are necessary for muscle hypertrophy. In support of our hypothesis, we found greater myofiber size, dry muscle mass, and total protein content in overloaded plantaris muscles of wild-type mice compared with mice deficient in CD18 (CD18–/–). We then tested the contribution of β2-integrins to overload-induced changes in neutrophil and macrophage accumulation, satellite cell/myoblast proliferation, muscle differentiation, and cell signaling for protein synthesis and protein degradation.
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METHODS |
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- subunits (e.g., CD11b) of β2-integrins and thus significantly compromise the function of all β2-integrins (43). Mice were fed standard laboratory chow and water ad libitum. Experimental procedures were approved by the University of Toledo Institutional Animal Care and Use Committee and were performed on mice of 3–4 mo of age. Surgical procedures. Mice were anesthetized with an intraperitoneal injection of 2% tribromoethanol (0.015 ml/g body mass), and supplemental doses were given as needed. Chronic overload of the plantaris was achieved by surgical, bilateral removal of the gastrocnemius and soleus muscles using aseptic techniques. The plantaris muscle was left intact to function as the primary plantar flexor during normal cage ambulation. A sham operation was performed on a different set of mice by exposing, but not surgically removing, the soleus and gastrocnemius muscles. Mice were permitted to ambulate for 3, 7, or 14 days following surgical procedures. An additional set of mice who had normal cage activity and who did not undergo surgery were used as controls.
Mice were killed by cervical dislocation under anesthesia. Plantaris muscles were dissected out, blotted dry, and weighed. Muscles used for histological analyses were frozen as previously described (33), whereas other muscles were frozen in liquid nitrogen and analyzed for dry muscle mass, total protein content, or protein or gene expression. Muscles analyzed for gene expression were treated with RNALater (Qiagen) and subsequently stored in liquid nitrogen.
Dry muscle mass. Plantaris muscles were weighed, freeze dried for 72 h, and reweighed. Percent water content was calculated from the difference between wet and dry mass for individual muscles. The percent change in wet and dry muscle mass (mg/g body mass) relative to control values was calculated and used to calculate the percent contribution of changes in muscle water to changes in wet muscle mass for each individual muscle. Total protein content of dry muscles was not determined.
Immunohistochemistry. Neutrophils, macrophages, and CD18+ cells in transverse sections (10 µm) were quantified as previously described (33). Neutrophils were identified using an anti-mouse Ly6G antibody [clone RB6-8C5; 1:100 in phosphate-buffered saline (PBS); BD Pharmingen], whereas macrophages were recognized using an anti-mouse F4/80 antibody (clone CI:A3-1; 1:100 in PBS; Serotec). CD18+ cells were labeled with an anti-mouse CD18 antibody (clone M18/2; 1:75 in PBS; BD Pharmingen). Labeled cells in two entire sections for each muscle were manually counted, and the total number of cells was expressed relative to the volume of the section area (Ly6G+, F4/80+, or CD18+/mm3) (33).
Histology. Transverse sections (10 µm) were stained with hematoxylin and eosin and examined for signs of both injury and regeneration. Myofibers that showed a pale or discontinuous cytoplasmic staining, were substantially swollen in appearance, or were invaded by cells were classified as injured. The number of central nucleated myofibers in two entire sections for each muscle was counted and then expressed as a percentage of the total number of myofibers within each section. The cross-sectional area (CSA) of central nucleated and normal myofibers was determined using digital image analysis software (Image Pro Plus). Normal myofibers were defined as those that did not show signs of injury nor central nucleation.
Satellite cell/myoblast proliferation.
Mice were implanted subcutaneously at the time of surgery with a continuous release pellet of 5'-bromo-2'-deoxyuridine (BrdU; Innovative Research America), a thymidine analog. The pellet was intended to deliver 
0.025 mg BrdU·g body mass–1·day–1. Incorporation of BrdU into the DNA of mitotically active cells was determined via immunofluorescence. Transverse sections (10 µm) of muscles were fixed with 4% formaldehyde and microwaved for 5 min at 225 W in 50 ml of 10 mM citrate buffer (pH 6.0) (24). Sections were allowed to cool in citrate buffer for 5 min and were microwaved again in fresh buffer for 5 min. Pilot experiments revealed that this protocol was superior to others tested (e.g., acid treatment) for preparing sections for double labeling. Sections were then blocked [3% bovine serum albumin (BSA), 0.05% Tween 20, and 0.2% gelatin in PBS] for 30 min. Mouse anti-BrdU (catalog no. RPN202, GE Healthcare Life Sciences) and rabbit anti-desmin (catalog no. D8281, Sigma-Aldrich) were diluted 1:50 in a solution containing nuclease (GE Healthcare Life Sciences). Slides were then incubated overnight at 4°C, washed in PBS, and incubated with anti-mouse fluorescein isothiocyanate-conjugated and anti-rabbit Cy-3-conjugated secondary antibodies (1:100; Jackson ImmunoResearch Laboratories). The sections were mounted with Vectashield containing 4',6-diamidino-2-phenylindole. Proliferation of presumptive satellite cells/myoblasts was determined by manually counting the number of desmin-positive (desmin+) cells that incorporated BrdU into their nuclei (desmin+BrdU+ cells). Counting was performed by someone who was blind to the treatment of the muscle sections during analysis. The number of double-positive cells in each muscle section was then expressed relative to muscle area (desmin+BrdU+ cells/mm2).
Protein content. Wet muscles were homogenized in reducing sample buffer (2% sodium dodecyl sulphate, 1.5% dithiothreitol, 1 M Tris·HCl, and 10% glycerol) containing protease inhibitors [1 mM EDTA, 5 µg/ml leupeptin, 5 µg/ml aprotinin, 11 mM 4-(2-aminoethyl) benzenesulfonyl fluoride, and 5 µg/ml sodium orthovanadate]. Homogenates were centrifuged (5,000 g, 4°C, 10 min), and the amount of protein in supernatants was determined (25).
Western blot analysis. Homogenized samples were separated on 7.5% or 10% gels via SDS-PAGE. Proteins were transferred to Immobilon-P (for p70S6k) or PVDF-FL (for Akt) membranes (Millipore), and Ponceau S staining of membranes was done to assess quality of transfer. Membranes were blocked with either 3% BSA/0.05% Tween 20 in Tris-buffered saline (TBS; for p70S6k) or 5% nonfat dry milk in TBS (for Akt). Membranes were washed in TBS/0.05% Tween 20 (TBS-T) and incubated overnight at 4°C with one of the following antibodies (Cell Signaling Technologies) that was diluted in blocking buffer: total p70S6k (1:1,000; catalog no. 9202), phospho-p70S6k Thr389 (1:1,000; catalog no. 9205), total Akt (1:1,000; catalog no. 9272), and phospho-Akt Ser473 (1:1,000; catalog no. 9271). Membranes were washed in TBS-T and incubated with either a peroxidase-conjugated secondary antibody (for p70S6k; 1:10,000; Jackson ImmunoResearch Laboratories) or an Alexa Fluor 680 secondary antibody (for Akt; 1:5,000; Invitrogen). Presence of protein was determined using an amplified opti-4CN detection kit (for p70S6k; Bio-Rad) or using the Odyssey infrared detection system (for Akt).
Real-time PCR.
Plantaris muscles, pretreated with RNALater, were homogenized using a bead homogenizer (Tissue Lyser, Qiagen) and RNA was isolated using a commercial kit for fibrous tissue according to the manufacturer's protocol (Qiagen). Purity and concentration of RNA were determined spectrophotometrically, and reverse transcription was performed using the high-capacity cDNA reverse transcription kit from Applied Biosystems. Real-time PCR was performed for the following using TaqMan PCR master mix and gene expression primers and probes (prelabeled with FAMJ as a reporter dye) that are inventory items of Applied Biosystems: MyoD (assay ID: Mm00440387_m1), myogenin (assay ID: Mm00446194_m1), MAFbx/atrogin-1 (assay ID:Mn00499518_m1), and MuRF1 (assay ID:Mn01188690_m1). Each sample was run in triplicate, and detection was achieved using Applied Biosystems 7500 real-time PCR system. The relative quantification method (
CT, where CT is threshold cycle) was used to document results, and data were normalized to GAPDH (assay ID: Mn99999915_g1).
Statistical analyses. Data sets that included sham-treated mice were initially analyzed using a three-way analysis of variance (ANOVA) using mouse strain (wild type and CD18–/–), surgery (sham and ablated), and time (3, 7, and 14 days) as independent factors. Because only two-way interactions were found in these analyses, data were analyzed again using a two-way ANOVA using mouse strain and time as independent factors. Data sets that did not include sham-treated mice were analyzed using a two-way ANOVA. The Student-Newman-Keuls post hoc test was used to locate the differences between means when the observed F ratio was statistically significant (P < 0.05). Data are reported as means ± SE unless otherwise stated.
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RESULTS |
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β2-Integrins contribute to compensatory hypertrophy. Wet muscle mass was significantly higher in overloaded (3, 7, and 14 d) wild-type and CD18–/– mice relative to their sham-treated counterparts and was higher in wild-type relative to CD18–/– mice at 14 days of overload (Fig. 1A). Overload-induced elevations in wet muscle masses, however, were largely the result of an increase in muscle water content. Muscle water content (see supplemental data Fig. S1 in the online version of this article available at American Journal of Physiology-Cell Physiology website) and its contribution to changes in wet muscle mass (Fig. 1B), however, were not statistically different between wild-type and CD18–/– mice at any overload time point, although the percent contribution of increased water content to changes in muscle mass at 14 days of overload was slightly (P = 0.25) lower for wild-type (51%) compared with CD18–/– mice (62%). Because of the relatively large contribution of muscle water content to increased wet muscle mass, myofiber CSA, dry plantaris mass, and total protein content were used as the primary outcome measures of hypertrophy.
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β2-Integrins influence regenerating myofibers. Muscle sections showed no overt signs of myofiber injury at any time point of muscle overload (Fig. 4A). The most consistent abnormality at 3 days of overload for both wild-type and CD18–/– mice was an increase in the extracellular space between myofibers, a hallmark sign of edema.
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β2-Integrins influence satellite cell/myoblast proliferation. We assessed satellite cell/myoblast proliferation by quantifying the incorporation of BrdU into the nuclei of desmin+ cells (Fig. 5A). A limitation of using desmin as a marker of skeletal muscle cells, however, is that it is also expressed by smooth muscle cells, myofibroblasts, and a very small fraction of fibroblasts. Whether these cells proliferate and contribute to hypertrophy after mechanical loading, however, remains to be determined.
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β2-Integrins contribute to the regulation of the myogenic program. Gene expression of MyoD1, which is highly expressed in proliferating satellite cells/myoblasts and during the early stages of muscle differentiation (14, 39), was higher in wild-type compared with CD18–/– mice after overload (Fig. 6A). Gene expression of myogenin, which is required for muscle differentiation (14, 39), was also substantially higher in wild-type compared with CD18–/– mice (Fig. 6B). Interestingly, gene expression of MyoD1 and myogenin was higher in wild-type mice at 3 days of overload, whereas the number of BrdU+desmin+ cells was lower in wild-type mice at 3 days of overload. These observations are likely attributable to the fact that gene expression of MyoD1 and myogenin would precede BrdU incorporation and the formation of regenerating myofibers, a morphological sign of muscle differentiation.
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DISCUSSION |
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Previous investigators have demonstrated that the synergist ablation model of hypertrophy causes neutrophils and macrophages to accumulate in skeletal muscle (3, 10, 46). Similar to DiPasquale et al. (10), neutrophils and macrophages in the present study were elevated in overloaded muscles in the absence of histological signs of muscle cell injury. Others have also noted the absence of overt injury in overloaded muscles (10, 18, 20, 41), whereas Snow (41) reported ultrastructural abnormalities (e.g., Z-line disruptions) in overloaded muscles despite no signs of injury at the light microscopy level. Regenerating myofibers, commonly interpreted to indicate prior injury, have also been reported in overloaded muscles (18, 41, 51). Thus, neutrophil and macrophage accumulation in the present study could have been initiated by mechanical loading and/or loading-induced muscle injury that occurred at some level (e.g., ultrastructural) before 7 days of overload.
The mechanisms by which skeletal muscle attracts neutrophils and allows them to enter skeletal muscle after mechanical loading are not well understood (32, 47). We previously demonstrated that β2-integrins were required for neutrophil accumulation after lengthening contractions (33). Thus we were surprised to find that neutrophil concentrations at 3 days of overload were similar between wild-type and CD18–/– mice. Higher neutrophils at 7 days of overload in wild-type relative to CD18–/– mice, however, were anticipated given our prior observations (33). We interpret these findings to indicate that neutrophil accumulation in the synergistic ablation model occurs via both a β2-integrin-independent (3 days of overload) and a β2-integrin-dependent (7 days of overload) mechanism. The substantial edema observed at 3 days of overload, and a resulting widening of intercellular junctions between endothelial cells, could have allowed neutrophils to enter skeletal muscle via a mechanism that is not dependent on β2-integrins. Neutrophil binding to junctional adhesion molecules (JAMs) on endothelial cells, which normally follows β2-integrin-mediated firm adhesion, is the final adhesion event of neutrophil diapedesis (26). Previous investigators have demonstrated that neutrophil binding to JAMs occurs predominantly via β1- and β3-integrins (26, 40). Thus, neutrophils in CD18–/– mice may have entered skeletal muscle at 3 days of overload by bypassing β2-integrin-mediated firm adhesion and by adhering directly to JAMs via β1- and/or β3-integrins.
Macrophage accumulation after mechanical loading is thought to be largely attributable to the diapedesis of monocytes. Because macrophage concentrations in overloaded muscles were not reduced in CD18–/– mice, the mechanism for macrophage accumulation in overloaded muscle does not appear to be the result of β2-integrin-mediated diapedesis of monocytes. Similar to our previous report (33), macrophage concentrations were slightly higher in CD18–/– mice at 7 days of muscle overload compared with wild-type mice. This finding could be the result of a compensatory mechanism for reduced neutrophil accumulation and/or impaired function of CD18–/– inflammatory cells that were found in overloaded muscles.
Satellite cells, which normally reside in a quiescent state between the basal lamina and the sarcolemma of myofibers, are thought to contribute to muscle hypertrophy through their ability to proliferate, migrate, differentiate, and fuse with existing myofibers (14). Prior work using 
-irradiation to inhibit cellular proliferation indicates that satellite cell proliferation is a prerequisite for compensatory hypertrophy (1, 31, 38).
We found evidence suggesting that β2-integrins influence the kinetics of satellite cell/myoblast proliferation as indicated by a delayed rise in BrdU+desmin+ cells in overloaded muscles of wild-type compared with CD18–/– mice. It is unknown whether the persistent elevation in the number of BrdU+desmin+ cells in overloaded CD18–/– mice represents continuous proliferation of desmin+ cells or simply the detection of desmin+ cells that incorporated BrdU before the 3-day overload time point. We favor the latter interpretation, particularly for the 14-day time point, because MyoD1 gene transcripts, which normally are elevated in proliferating satellite cells/myoblasts, were near control levels at 14 days of overload for CD18–/– mice. In wild-type mice, the temporal response in the number of BrdU+desmin+ cells preceded measurable hypertrophy, whereas, CD18–/– mice showed little to no signs of hypertrophy despite an earlier increase in the number of BrdU+desmin+ cells. These findings may indicate that β2-integrin signaling in neutrophils and/or macrophages contributes to the temporal regulation of satellite cell/myoblast proliferation and that this regulation may be important in linking satellite cell/myoblast proliferation to hypertrophy. Given the time course of neutrophil and macrophage accumulation at 3 and 7 days of overload, it is conceivable that β2-integrin signaling in neutrophils suppresses satellite cell/myoblast proliferation and that this suppressive effect is augmented by β2-integrin signaling in macrophages.
Because of the observed uncoupling between BrdU+desmin+ cells and hypertrophy in CD18–/– mice, we hypothesized that β2-integrins influence the expression profile of MyoD1 and myogenin, muscle-specific basic helix-loop-helix transcription factors. Although MyoD1 is expressed in proliferating satellite cells/myoblasts, its expression promotes differentiation by inducing the expression of myogenin, which is required for terminal differentiation (39, 45). The increased gene expression of MyoD1 and myogenin at 3 days of overload and its pattern of expression over the course of 14 days of overload in wild-type mice is in agreement with findings of Adams and colleagues (1, 2). Importantly, transcript levels of MyoD1 and myogenin in overloaded muscles were on average two- to threefold higher for wild-type compared with CD18–/– mice. We also found that regenerating myofibers, a global marker of muscle differentiation, were threefold higher in wild-type compared with CD18–/– mice. These findings may indicate that β2-integrin signaling in neutrophils and/or macrophages aids muscle differentiation, possibly by enhancing the transition of proliferating satellite cells/myoblasts to a state of differentiation.
Skeletal muscle hypertrophy has been reported to be dependent on Akt, mTOR, and p70S6k signaling (52). Activation of mTOR in skeletal muscle cells can occur via phosphorylation by Akt or via Akt-independent mechanisms such as mechanical loading, amino acid availability, and insulin (15, 35). Activation of mTOR increases the activity of downstream targets such as p70S6k and 4E binding protein-1, which are thought to promote hypertrophy by increasing the translational capacity of skeletal muscle cells. Evidence of a role of p70S6k in muscle hypertrophy after mechanical loading was provided by Baar and Esser (4), who reported that an acute rise in p70S6k (Thr389) levels statistically correlated with an increase in muscle mass after training with electrically stimulated muscle contractions.
In agreement with prior work, the relative abundance of Akt (Ser473) and p70S6k (Thr389) was elevated in overloaded muscles of wild-type mice (1, 5, 10). Higher levels of p70S6k (Thr389) observed in wild-type mice could be the result of increased signaling in skeletal muscle cells and/or other cell types (e.g., neutrophils and macrophages) that reside in overloaded muscles. Because p70S6k signaling in neutrophils occurs during their migration (12), observed differences in p70S6k (Thr389) levels could be attributable to the higher concentration of neutrophils that we found in overloaded muscles of wild-type compared with CD18–/– mice. DiPasquale et al. (10) reported that overload-induced elevations in p70S6k (Thr389) levels were not influenced by reductions in macrophage accumulation. Clearly, further work is needed to determine cell type-specific changes in Akt and p70S6k signaling in hypertrophying muscles and if β2-integrins influence these kinases in a cell type-specific manner.
Although increased activity of MAFbx/atrogin-1 and MuRF1 can cause muscle atrophy (19), little is known about their contribution to compensatory hypertrophy. In the present study, β2-integrins diminished overload-induced reductions in gene expression of MAFbx/atrogin-1. These data indicate that β2-integrins may contribute to signaling for protein degradation in overloaded muscles by increasing the activity of MAFbx/atrogin-1, but not MuRF1. More importantly, the mechanism by which β2-integrins influenced compensatory hypertrophy does not appear to be attributable to reduced signaling for protein degradation.
We suspect that the underlying mechanism for how β2-integrins influence the hypertrophic response is related to their ability to control cytokine production from neutrophils and macrophages. Previous investigators have reported that β2-integrins activate nuclear transcription factor-
B in human neutrophils (22) and monocytes (37) and cause them to produce several cytokines [IL-8, IL-1β, TNF-, and macrophage inflammatory protein (MIP)-1 and -1β] (22, 36, 37, 49). Peters and colleagues (29, 30) reported that β2-integrins stimulate MIP-2 and TGF-β1 and inhibit IL-1, IL-1β, and IL-6 production from mouse macrophages. β2-Integrins have also been reported to be associated with reduced serum TNF- and IL-6 concentrations in mice after an injection of lipopolysaccharide (9, 29). Because some of these cytokines (e.g., TNF-, IL-6, IL-1β, and TGF-β1) are elevated in hypertrophying muscle (16, 46) and are known to influence skeletal muscle cells (14, 17), β2-integrin-mediated release of cytokines from neutrophils and/or macrophages may be necessary for hypertrophy after mechanical loading. Preliminary ongoing studies support this contention by revealing that β2-integrin-mediated production of soluble factors in hypertrophying muscle directly affects skeletal muscle cells.
β2-Integrin-mediated hypertrophy is not likely the result of β2-integrins controlling the production of proangiogenic cytokines. This interpretation is based on our findings that the numbers of CD31+ endothelial cells, expressed relative to either muscle area or number of myofibers, were not different between wild-type and CD18–/– mice at 14 days of overload (data not reported). Furthermore, angiogenesis is not prevalent until after weeks of chronic muscle overload (34). Thus it seems unlikely that β2-integrin signaling for angiogenesis would account for differences in hypertrophy that were observed between wild-type and CD18–/– mice.
An alternative mechanism for the β2-integrin-mediated hypertrophy involves hematopoietic stem cells, which have been reported to contribute nuclei to myofibers after injury and during hypertrophy (6, 11, 28). Although controversial, these cells are believed to be derived from non- or pre-myeloid cell lineage. Myeloid cells, however, are known to express β2-integrins only during the later stages of their maturation (21, 42). Furthermore, Doyonnas et al. (11) demonstrated that CD11b+ cells (neutrophils and macrophages) and Gr1+ cells (Ly6G+; neutrophils) do not contribute nuclei to myofibers. Thus, differences in hypertrophy between wild-type and CD18–/– mice are not likely attributable to the expression of β2-integrins on hematopoietic stem cells that may become incorporated into myofibers.
The present study provides novel evidence that β2-integrins, which control functional activities of neutrophils and macrophages, contribute to skeletal muscle hypertrophy after mechanical loading. β2-Integrins appear to influence the hypertrophic response by temporally regulating satellite cell/myoblast proliferation, enhancing muscle differentiation, and/or by augmenting signaling for protein synthesis. Further work is needed to determine how β2-integrin signaling in neutrophils and macrophages communicates with skeletal muscle cells to regulate cellular and molecular events associated with hypertrophy, including rates of muscle protein synthesis and degradation. This information would aid the development of translational strategies (e.g., pharmaceuticals) to promote muscle growth in inflammatory muscle diseases and other conditions with an inflammatory component, such as aging, cancer, and several cardiovascular and metabolic diseases.
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ACKNOWLEDGMENTS |
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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.
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