| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1August Krogh Institute and 2Rigshospitalet, Copenhagen Muscle Research Centre, DK-2100 Copenhagen, Denmark
Submitted 30 September 2002 ; accepted in final form 23 April 2003
 |
ABSTRACT |
|---|
 TOP ABSTRACT METHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
44% after 1 and 6 h of recovery. The IGF-IEbc mRNA level was
unaffected. The present study shows that myogenin, MyoD, and MRF4 mRNA levels
are transiently elevated in human skeletal muscle after a single bout of
heavy-resistance training, supporting the idea that the MRFs may be involved
in regulating hypertrophy and/or fiber-type transitions. The results also
suggest that IGF-IEa expression may be downregulated at the mRNA level during
the initial part of recovery from resistance exercise. hypertrophy; myogenin; mechanical load; satellite cells
The signaling pathways leading to transcriptional and translational changes in skeletal muscle in response to resistance exercise are still not fully understood. Baar and colleagues (6) suggest four potential stimuli that may regulate these processes: mechanical load or stress, intracellular calcium, hypoxia, and redox state. These are thought to be first messengers in a signaling cascade in which various transcription factors, hormones, and other regulatory proteins are activated. These proteins, in turn, contribute in controlling the qualitative and quantitative changes occurring in the muscle by regulating gene expression. The MRFs and IGF-I might be such regulatory proteins, because previous studies have reported exercise-induced changes in MRFs and IGF-I expression, at both the mRNA and protein level (1, 7, 9, 15, 16, 23, 29).
The MRFs are a family of skeletal muscle-specific transcription factors that regulate the expression of several skeletal muscle genes (31). The family is composed of four members: myogenin, MRF4, MyoD and Myf5. These proteins belong to a larger basic helix-loop-helix class of transcription factors that, after dimerization with a ubiquitous E protein, bind to an E-box domain and transactivate downstream muscle genes, such as desmin, troponin I, and myosin light chain (MLC) (21, 22, 38). Because these genes are involved in qualitative and quantitative changes occurring in the muscle after resistance exercise, there might be an increased expression of the MRFs in response to overload. Studies using stretch overload on animals support this theory (9, 23, 24). So far, there has only been one published study examining the effects of resistance exercise on MRF gene expression in humans, showing increased mRNA levels of myogenin and MyoD, but these increases were much lower than the ones observed in the animal studies (39). The mRNA response of the myogenic transcription factor MRF4 to resistance exercise has, to our knowledge, never been reported in human muscle.
The hormone IGF-I has, in recent years, received increased attention in studies examining exercise-induced muscle hypertrophy. IGF-I increases muscular protein synthesis and stimulates satellite cell proliferation and differentiation in vitro (2, 13). Two isoforms of IGF-I that are expressed and released from skeletal muscle cells have recently been identified (16, 28, 40). One of them, IGF-IEa, is very similar to the isoform produced by the liver and has probably an endocrine function. This isoform is expressed both in working and nonworking muscle (28). The other isoform, mechano-growth factor (MGF) (also called IGF-IEc in humans) has a 49 (52 in animals) base long DNA fragment inserted in the E-domain of IGF-IEa and is mainly expressed in working muscle. This isoform is thought to have an autocrine and paracrine function, stimulating myofibrillar protein synthesis and satellite cell activation (1, 15). Increased MGF (2-864%) and IGF-I (62%) mRNA content has been observed 2.5 and 48 h, respectively, after an acute bout of mechanical loading in humans (7, 16), but a more detailed time course (several time points) of IGF-I mRNA expression during recovery from resistance exercise in humans has never been reported.
The aim of the present study was to test the hypothesis that MRF and IGF-I gene expression is increased in response to resistance exercise. These genes were studied because both IGF-I and the MRFs have been linked to satellite cell activation and because they are potentially important genes in the regulation of hypertrophy. MRF4, myogenin, MyoD, IGF-IEabc (isoforms a, b, and c), and IGF-IEbc (isoform b and c) mRNA contents were determined in muscle biopsies obtained from the vastus lateralis muscle before, immediately after, and during recovery from a single bout of heavy-resistance training.
|
METHODS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
Dietary intake. An individual food plan was constructed for each subject on the basis of body mass and age (World Health Organization Technical Report Series 724 1985). The subjects received three meals per day plus one evening snack.
Preparatory test. The pretest was completed 2 wk before the study to determine the workload to be used during the first set in the experiment. The test was performed on a leg press and a knee extensor machine, and the load was gradually increased until the subjects could only just complete between six and eight repetitions. The subjects were allowed to rest as much as they wanted between the sets to avoid muscle fatigue.
Exercise protocol. A heavy-resistance training protocol that
stimulated the vastus lateralis muscle was used. The exercise protocol
contained four sets of 6-8, 6-8, 10-14, and 10-14 repetitions and was first
carried out on a leg press machine and then on a knee extensor machine. The
intention was to reach total exhaustion in each set. The training started with
a 40-kg warm-up on the leg press machine, after which the load from the
preparatory test was put on. The load was adjusted during the training so that
the predetermined repetitions could be completed. Subjects were encouraged to
lower the weights slowly (the eccentric phase) and to push them up as fast as
possible (the concentric phase). There was a 90-s rest period between each set
and a 3-min rest period between the two machines. The complete exercise
routine (a total of eight sets) was completed in 20 min.
Muscle biopsies. Muscle biopsies were obtained from the middle portion of the vastus lateralis muscle under local anesthesia by using the percutaneous needle biopsy technique with suction. The samples were quickly dipped on a gauze swab to remove superficial blood and frozen in liquid N2. Samples were stored at -80°C until analyzed. Biopsies were taken 1.5 h before the exercise started (Pre), immediately after the last set of knee extension (0 h), and at 1, 2, 6, 24, and 48 h postexercise. Incisions were made, at minimum, 3 cm apart, and only one biopsy was obtained from each incision site. Attempts were made to extract tissue from approximately the same depth in the muscle each time by using the depth markings on the needle. The Pre, 0-h, and 1-h biopsies were obtained from the left leg, and the 2-, 6-, 24-, and 48-h biopsies were obtained from the right leg. From three of the subjects, an additional muscle biopsy was obtained from the right leg 1 h postexercise. The purpose of this biopsy was to examine if prior biopsies would affect the expression of the genes investigated in the present study.
RNA extraction. Total RNA was isolated from 25 mg of muscle
tissue by a modified guanidinium thiocyanate-phenol-chloroform extraction
method, adapted from Chomczynski and Sacchi
(12), as previously described
(34).
RT. RT of the RNA samples was performed by using the Superscript II RNase H system (Invitrogen, Carlsbad, CA), according to the manufacturer's instructions, as previously described (32). Eleven microliters of total RNA were reverse transcribed, and the RT product was diluted to a total of 200 µl. The samples were stored in -20°C for later PCR analysis.
Real-time PCR. The probes and primers used
(Table 1) were constructed from
human-specific sequence databases [Entrez-NIH and Ensemble, Sanger Institute,
using gene bank numbers NM 000618 (IGF-IEa), HUMGFIB (IGF-IEbc), XM001688
(Myogenin), XM 006691 (MRF4), XM 036341 (MyoD)], and applying DNA analysis
computer software (Primer Express, Applied Biosystems). All self-designed
probes were 5'-FAM and 3'-TAMRA labeled. For each of the genes, a
Blast Search revealed that sequence homology was obtained only for the target
gene. The primers and probes were optimized to determine optimal primer
concentration, probe concentration, and efficiency of amplification. The
expected sizes of the PCR products were initially verified by separation on an
agarose gel by electrophoresis. The primers and probes for IGF-IEabc were
designed to detect and amplify the IGF-I isoforms IGF-IEa, IGF-IEb, and
IGF-IEc, whereas the primers and probe for IGF-IEbc were designed to amplify
only the b and c isoforms. GAPDH was used as endogenous control to normalize
the mRNA content of the target genes in each sample. GAPDH was amplified by
using a predeveloped assay reagent (Applied Biosystems). The mRNA content of
the selected genes was determined by fluorescence-based real-time PCR
technology (ABI PRISM Sequence Detection System, Applied Biosystems). Two and
one-half microliters of the diluted RT product (template) were mixed with
2x TaqMan Universal Master Mix, forward primer, reverse primer, probe,
and nuclease free water to a final volume of 25 µl. The Master Mix (Applied
Biosystems) contained AmpliTaq Gold DNA polymerase, AmpErase UNG, dNTPs with
dUTP, ROX as passive reference, and optimized buffer components. The final mix
was added to the PCR plate, and each sample was analyzed in triplicate. The
triplicates had a threshold cycle SD ranging from 0.001 to 0.2. An identical
PCR cycle profile was used for all genes: 50°C for 2 min + 95°C for 10
min + (95°C for 15 s + 60°C for 1 min) x 40 cycles. Data were
analyzed by using a comparative critical threshold (Ct) method, where the
amount of target normalized to the amount of endogenous control and relative
to the control sample is given by 2-
Ct
(Applied Biosystems). For each subject, all samples were run together,
allowing relative comparison of the samples from a given subject.
|
GAPDH as endogenous control. GAPDH is frequently used as an endogenous control in exercise studies and has previously been used in studying gene expression in response to resistance exercise (7, 39). In addition, we tested if GAPDH mRNA was influenced by the protocol used in the present study. This was done on all samples from two of the subjects. Total RNA was measured spectrophotometrically, and the same amount of RNA was added to the RT reaction. The GAPDH cDNA was PCR amplified, showing similar GAPDH mRNA levels in the samples, with no indication that GAPDH was affected by the exercise protocol used.
Statistical analysis. Results are presented as means ± SE. The mRNA contents were normalized to GAPDH, and the samples were expressed relative to the corresponding control (Pre) sample, which was set to 1. A one-way ANOVA for repeated measures was used to determine whether there were any significant differences over time among the samples. If a significant difference was present, a Bonferroni t-test was used to locate the difference. Differences were considered significant at P < 0.05.
|
RESULTS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
|
IGF-I. IGF-IEac mRNA was reduced by 44% (P < 0.05) at 1 and 6 h postexercise compared with the Pre sample (Fig. 2). This decrease was absent when the IGF-IEa isoform was excluded (see IGF-IEc in Fig. 2), indicating that the observed decrease was due to a decrease in IGF-IEa. As expected, the levels measured during the real-time PCR indicated that more IGF-IEa mRNA content was present than IGF-IEbc mRNA, although direct comparisons between the absolute levels of isoform a and isoform c cannot be performed based on the present results.
|
Effects of the repeated biopsies on MRF and IGF-I mRNA content. The prior biopsies in the left leg did not seem to affect the mRNA expression of the MRF and IGF-I genes. The fold change observed for the left leg (where prior biopsies had been taken) was, on average, 1.04 ± 0.25 for MRF4, 1.29 ± 0.21 for myogenin, 1.59 ± 0.58 for MyoD, 1.01 ± 0.17 for IGF-IEbc, and 1.03 ± 0.334 for IGF-IEabc of the value obtained for the right leg (where no biopsies had been taken). This shows that there were no consistent differences between the two legs, indicating that the repeated biopsies were not a source of error that could explain the changes in gene expression observed in the present study.
|
DISCUSSION |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
The MRFs regulate the transcription of several skeletal muscle-specific genes, such as MLC, troponin I, and desmin (21, 22, 38). These proteins are building blocks of larger protein complexes, and it may, therefore, be speculated that one or more of these proteins are rate limiting when muscle fibers synthesize new structural and contractile elements. Skeletal muscle may thus, to some extent, be able to change the synthesis rate of more complex structures by regulating transcription of the building blocks. The MRFs may, therefore, contribute to regulating hypertrophy by controlling transcription of genes such as MLC, troponin, and desmin. In line with such a possibility is a correlation between changes in muscle mass and MRF expression found in three studies (3, 4, 17). Hespel and colleagues (17) showed that the MRF4 protein content in human muscle was closely correlated with the concomitant change in average muscle-fiber size after 10 wk of resistance exercise. In rats, aging was associated with a 50% reduction in muscle to body weight, and this decline was similar to the decline in mRNA levels of the MRF-regulated genes desmin and MLC (4). In addition, hypertrophy was attenuated in old rats compared with young rats, and the hypertrophied muscle from the old rats had significantly lower levels of MRF than the muscle from the young rats (3).
The MRFs are known to be of importance when myoblasts proliferate and differentiate (30). This implies that these transcription factors are involved in the stretch-induced activation and subsequent differentiation of satellite cells, and it has been speculated that myogenin regulates the expression of a protein that is required for satellite cell fusion (23). Satellite cell proliferation, differentiation, and fusion with muscle fibers are necessary if the hypertrophy response is to continue during longer periods of mechanical overload (23, 34), and the MRFs might, therefore, be involved in regulating prolonged muscle growth. Several studies have shown that muscle injury induces satellite cell activation and MRF expression (20, 26, 33). Although recent studies examining human muscle after high-force eccentric muscle contractions do not show any signs of muscle injury, even though delayed onset of muscle soreness was observed (25, 42), it cannot be ruled out that the training protocol used in the present study may have resulted in muscle injury because it contained a high number of eccentric muscle contractions (14). The possibility, therefore, exists that the changes observed in MRF mRNA in the present study may originate from activated satellite cells regenerating damaged muscle fibers.
Several studies have shown that the MRFs are upregulated, not only during hypertrophy but also during atrophy (5, 36). Why are the MRFs induced during both atrophy and hypertrophy? There are two possibilities that might explain this paradox. First, if the MRFs do not regulate muscle mass, the reason for the observed upregulation during hypertrophy and atrophy could be that they regulate other processes coinciding with changes in muscle mass. One such process is fiber-type transition. MyoD and myogenin have been suggested to be implicated in regulating muscle-fiber type, as myogenin has been found to accumulate in slow-twitch fibers and MyoD in fast-twitch fibers (18, 36). Moreover, a study conducted by Mozdziak et al. (29) indicates that myogenin and MyoD mRNA levels are associated more with alterations in MHC isoform composition than changes in muscle mass. Second, the increase in MRF during unloading might be an attempt from the muscle to offset muscle wasting. This possibility is supported by the findings that aged rats have a higher rate of atrophy and a lower increase in MRF mRNA and protein levels during unloading than young rats (5). The authors of the latter study suggest that this failure to accumulate adequate amounts of MRF protein may play a role in the accelerated muscle loss seen in senescent rats during unloading.
IGF-I. The present study shows a 44% decrease in IGF-IEabc mRNA levels after resistance exercise. This is in contrast to the recent findings, with no change in IGF-IEa 2.5 h after mechanical loading (16) and a 62% increase in IGF-I 48 h after resistance exercise (7). However, it is important to note that the increase in the latter study (7) was observed much later in recovery than the decline found in the present study: 1 and 6 h postexercise. Bamman et al. (7) did not separate the different IGF-I isoforms. This was completed to some extent in the present study in which the mRNA content of IGF-IEabc and IGF-IEbc was examined. Thus IGF-IEabc includes the IGF-I isoforms, IGF-IEa (exons 1, 3, 4, and 6), IGF-IEb (exons 1, 3, 4, 5), and IGF-IEc (exons 1, 3, 4, a small part of 5 and 6), whereas IGF-IEbc includes the b and c isoforms. IGF-IEa is the most abundant isoform in both liver and muscle, whereas IGF-IEc is expressed at a much lower level (11, 16, 35, 40). Several animal studies have examined the impact of muscle overload on IGF-I isoform expression (15, 28, 40), but there has, to our knowledge, only been one human study in which this has been examined (16). That study examined the expression of the MGF (IGF-IEc) and IGF-IEa isoforms before and 2.5 h after a single bout of high-resistance weight-lifting exercise, with MGF being upregulated by 2-865% and the IGF-IEa isoform remaining unchanged. This is in contrast to the present findings in which a decrease in IGF-IEabc mRNA levels and no change in IGF-IEbc levels were observed. The fact that IGF-IEbc remained unchanged indicates that the decrease in IGF-IEabc was caused by a decrease in IGF-IEa. These different results might be due to individual responses (see paragraph below), the use of different training protocols, and/or differences in sampling time points (2.5 h vs. 0, 1, 2, 6, 24, and 48 h). In addition, the expression pattern of the IGF-IEb isoform in human muscle is still unclear.
Because the various IGF-I isoforms originate from the same gene, the possibility exists that the ratio between the isoforms depends on how the IGF-I mRNA precursor is spliced. Certain kinds of signals might alter the splicing, reducing the production of one isoform while increasing the formation of another. If resistance exercise induces such signals, this might, for example, lead to a decreased production of IGF-IEa and an increased production of IGF-IEc. Thus changes in the individual IGF-I mRNA isoforms may occur without changes in transcription of the IGF-I gene.
Individual response. The mRNA content measured during recovery from exercise was highly variable among subjects, with some subjects showing a marked increase and some showing no change. This might indicate individual variations in gene response to a given resistance exercise protocol, which is supported by the results obtained in the study by Hameed et al. (16). In addition, the mean increase in muscle-fiber area has been shown to differ among subjects after 12 wk of heavy-resistance training (27). The explanation for these individual responses could be individual differences in the gene expression pattern, depending on the inherited organization of the genome, so that resistance exercise induces a more marked expression of genes important for hypertrophy in some individuals than in others.
In conclusion, the present study shows that resistance exercise induces a transient increase in mRNA levels of myogenin, MyoD, and MRF4 in human skeletal muscle. This implies that these transcription factors are regulated at the transcriptional level and that they might be involved in the regulation of fiber-type transitions and/or hypertrophy. In addition, the present data suggest that one bout of heavy-resistance training reduces the mRNA content of the IGF-IEa isoform during the initial part of recovery.
|
DISCLOSURES |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
|
ACKNOWLEDGMENTS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
|
FOOTNOTES |
|---|
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.
|
REFERENCES |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
This article has been cited by other articles:
|
|
 |
|
  D. J. Kosek and M. M. Bamman Modulation of the dystrophin-associated protein complex in response to resistance training in young and older men J Appl Physiol, May 1, 2008; 104(5): 1476 - 1484. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Lundby, Y. Hellsten, M. B. F. Jensen, A. S. Munch, and H. Pilegaard Erythropoietin receptor in human skeletal muscle and the effects of acute and long-term injections with recombinant human erythropoietin on the skeletal muscle J Appl Physiol, April 1, 2008; 104(4): 1154 - 1160. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Deldicque, P. Atherton, R. Patel, D. Theisen, H. Nielens, M. J. Rennie, and M. Francaux Effects of resistance exercise with and without creatine supplementation on gene expression and cell signaling in human skeletal muscle J Appl Physiol, February 1, 2008; 104(2): 371 - 378. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-s. Kim, J. K. Petrella, J. M. Cross, and M. M. Bamman Load-mediated downregulation of myostatin mRNA is not sufficient to promote myofiber hypertrophy in humans: a cluster analysis J Appl Physiol, November 1, 2007; 103(5): 1488 - 1495. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. Vogiatzis, G. Stratakos, D. C M Simoes, G. Terzis, O. Georgiadou, C. Roussos, and S. Zakynthinos Effects of rehabilitative exercise on peripheral muscle TNF{alpha}, IL-6, IGF-I and MyoD expression in patients with COPD Thorax, November 1, 2007; 62(11): 950 - 956. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. I. Lewis, M. Fournier, T. W. Storer, S. Bhasin, J. Porszasz, S.-G. Ren, X. Da, and R. Casaburi Skeletal muscle adaptations to testosterone and resistance training in men with COPD J Appl Physiol, October 1, 2007; 103(4): 1299 - 1310. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. R. Nielsen, R. Mounier, P. Plomgaard, O. H. Mortensen, M. Penkowa, T. Speerschneider, H. Pilegaard, and B. K. Pedersen Expression of interleukin-15 in human skeletal muscle effect of exercise and muscle fibre type composition J. Physiol., October 1, 2007; 584(1): 305 - 312. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. D. R. Harridge Plasticity of human skeletal muscle: gene expression to in vivo function Exp Physiol, September 1, 2007; 92(5): 783 - 797. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Bamman, J. K. Petrella, J.-s. Kim, D. L. Mayhew, and J. M. Cross Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans J Appl Physiol, June 1, 2007; 102(6): 2232 - 2239. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. G. Churchley, V. G. Coffey, D. J. Pedersen, A. Shield, K. A. Carey, D. Cameron-Smith, and J. A. Hawley Influence of preexercise muscle glycogen content on transcriptional activity of metabolic and myogenic genes in well-trained humans J Appl Physiol, April 1, 2007; 102(4): 1604 - 1611. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Kvorning, M. Andersen, K. Brixen, P. Schjerling, C. Suetta, and K. Madsen Suppression of testosterone does not blunt mRNA expression of myoD, myogenin, IGF, myostatin or androgen receptor post strength training in humans J. Physiol., January 15, 2007; 578(2): 579 - 593. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Kvorning, M. Andersen, K. Brixen, and K. Madsen Suppression of endogenous testosterone production attenuates the response to strength training: a randomized, placebo-controlled, and blinded intervention study Am J Physiol Endocrinol Metab, December 1, 2006; 291(6): E1325 - E1332. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. K. Petrella, J.-s. Kim, J. M. Cross, D. J. Kosek, and M. M. Bamman Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women Am J Physiol Endocrinol Metab, November 1, 2006; 291(5): E937 - E946. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Kosek, J.-s. Kim, J. K. Petrella, J. M. Cross, and M. M. Bamman Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults J Appl Physiol, August 1, 2006; 101(2): 531 - 544. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Raue, D. Slivka, B. Jemiolo, C. Hollon, and S. Trappe Myogenic gene expression at rest and after a bout of resistance exercise in young (18-30 yr) and old (80-89 yr) women J Appl Physiol, July 1, 2006; 101(1): 53 - 59. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. G. Coffey, A. Shield, B. J. Canny, K. A. Carey, D. Cameron-Smith, and J. A. Hawley Interaction of contractile activity and training history on mRNA abundance in skeletal muscle from trained athletes Am J Physiol Endocrinol Metab, May 1, 2006; 290(5): E849 - E855. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-s. Kim, D. J. Kosek, J. K. Petrella, J. M. Cross, and M. M. Bamman Resting and load-induced levels of myogenic gene transcripts differ between older adults with demonstrable sarcopenia and young men and women J Appl Physiol, December 1, 2005; 99(6): 2149 - 2158. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Nordsborg, M. Thomassen, C. Lundby, H. Pilegaard, and J. Bangsbo Contraction-induced increases in Na+-K+-ATPase mRNA levels in human skeletal muscle are not amplified by activation of additional muscle mass Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2005; 289(1): R84 - R91. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-s. Kim, J. M. Cross, and M. M. Bamman Impact of resistance loading on myostatin expression and cell cycle regulation in young and older men and women Am J Physiol Endocrinol Metab, June 1, 2005; 288(6): E1110 - E1119. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Yang, A. Creer, B. Jemiolo, and S. Trappe Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle J Appl Physiol, May 1, 2005; 98(5): 1745 - 1752. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Bickel, J. Slade, E. Mahoney, F. Haddad, G. A. Dudley, and G. R. Adams Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise J Appl Physiol, February 1, 2005; 98(2): 482 - 488. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. P. Fischer, P. Plomgaard, A. K. Hansen, H. Pilegaard, B. Saltin, and B. K. Pedersen Endurance training reduces the contraction-induced interleukin-6 mRNA expression in human skeletal muscle Am J Physiol Endocrinol Metab, December 1, 2004; 287(6): E1189 - E1194. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Bamman, R. C. Ragan, J.-s. Kim, J. M. Cross, V. J. Hill, S. C. Tuggle, and R. M. Allman Myogenic protein expression before and after resistance loading in 26- and 64-yr-old men and women J Appl |
