Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling

Journal of Physiology

Volumn 545, Issue 1, 2002, Pages 27-41

  Chen, Yi Wen ^a   Nader, Gustavo A ^b   Baar, Keith R ^b   Fedele, Mark J ^b   Hoffman, Eric P ^a   Esser, Karyn A ^b  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; ELONGATION FACTOR 1ALPHA; MESSENGER RNA; PROTEIN P53; RIBOSOME RNA; PROTEIN C FOS; FIBROBLAST GROWTH FACTOR 2; RNA;

ANIMAL TISSUE; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GENETIC REGULATION; GENETIC TRANSCRIPTION; MECHANICAL STRESS; MOLECULAR DYNAMICS; MUSCLE CONTRACTILITY; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE EXERCISE; MUSCLE HYPERTROPHY; MUSCLE LEVEL; NONHUMAN; POLYSOME; PRIORITY JOURNAL; RAT; REVIEW; RNA TRANSLATION; SERUM; SKELETAL MUSCLE; TIME; TUMOR SUPPRESSOR GENE; ANIMAL; ARTICLE; ELECTROSTIMULATION; FEMALE; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS; TISSUE DISTRIBUTION; WISTAR RAT; ANIMAL EXPERIMENT; DISEASE COURSE; GENE CONTROL; GENE EXPRESSION; MOLECULAR MECHANICS; RESISTANCE TRAINING; STEADY STATE; TRANSLATION REGULATION;

ANIMALS; ELECTRIC STIMULATION; FEMALE; GENE EXPRESSION PROFILING; MUSCLE CONTRACTION; MUSCLE, SKELETAL; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RNA, MESSENGER; TISSUE DISTRIBUTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0037112473     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.021220     Document Type: Review

References (57)

1. AGARWAL, M. L., AGARWAL, A., TAYLOR, W. R. & STARK, G. R. (1995). p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proceedings of the National Academy of Sciences of the USA 92, 8493-8497.
2. AIHARA, Y., KURABAYASHI, M., SAITO, Y., OHYAMA, Y., TANAKA, T., TAKEDA, S., TOMARU, K., SEKIGUCHI, K., ARAI, M., NAKAMURA, T. & NAGAI, R. (2000). Cardiac ankyrin repeat protein is a novel marker of cardiac hypertrophy: role of M-CAT element within the promoter. Hypertension 36, 48-53.
3. ALLEN, R. E. & RANKIN, L. L. (1990). Regulation of satellite cells during skeletal muscle growth and development. Proceedings of the Society for Experimental Biology and Medicine 194, 81-86.
4. ANDREASEN, P. A., EGELUND, R. & PETERSEN, H. H. (2000). The plasminogen activation system in tumor growth, invasion, and metastasis. Cellular and Molecular Life Sciences 57, 25-40.
5. BAAR, K. & ESSER, K. (1999). Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. American Journal of Physiology 276, C120-127.
6. BLOUGH, E., DINEEN, B. & ESSER, K. (1999). Extraction of nuclear proteins from striated muscle tissue. Biotechniques 26, 202-204.
7. BODINE, S. C., STITT, T. N., GONZALEZ, M., KLINE, W. O., STOVER, G. L., BAUERLEIN, R., ZLOTCHENKO, E., SCRIMGEOUR, A., LAWRENCE, J. C., GLASS, D. J. & YAUCOPOULOS, G. D. (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nature Cell Biology 3, 1014-1019.
8. BOOTH, F. W. & THOMASON, D. B. (1991). Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiological Reviews 71, 541-585.
9. BRADBURY, A., POSSENTI, R., SHOOTER, E. M. & TIRONE, F. (1991). Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization. Proceedings of the National Academy of Sciences of the USA 88, 3353-3357.
10. CARRIER, F., SMITH, M. L., BAE, I., KILPATRICK, K. E., LANSING, T. J., CHEN, C. Y., ENGELSTEIN, M., FRIEND, S. H., HENNER, W. D., GILMER, T. M. et al. (1994). Characterization of human Gadd45, a p53-regulated protein. Journal of Biological Chemistry 269, 32672-32677.
11. CARSON, J. A., NETTLETON, D. & REECY, J. M. (2002). Differential gene expression in the rat soleus muscle during early work overload-induced hypertrophy. FASEB Journal 16, 207-219.
12. CHEN, Y. W., ZHAO, P., BORUP, R. & HOFFMAN, E. P. (2000). Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. Journal of Cell Biology 151, 1321-1336.
13. DAVIS, L. & ENGEBRECHT, J. (1998). Yeast dom34 mutants are defective in multiple developmental pathways and exhibit decreased levels of polyribosomes. Genetics 149, 45-56.
14. DUNN, S. E., BURNS, J. & MICHEL, R. (1999). Calcineurin is required for skeletal muscle hypertrophy. Journal of Biological Chemistry 274, 21908-21912.
15. ESSIG, D. A., BORGER, D. R. & JACKSON, D. A. (1997). Induction of heme oxygenase-1 (HSP32) mRNA in skeletal muscle following contractions. American Journal of Physiology 272, C59-67.
16. FIBBI, G., BARLETTA, E., DINI, G., DEL ROSSO, A., PUCCI, M., CERLETTI, M. & DEL ROSSO, M. (2001). Cell invasion is affected by differential expression of the urokinase plasminogen activator/urokinase plasminogen activator receptor system in muscle satellite cells from normal and dystrophic patients. Laboratory Investigation 81, 27-39.
17. GOLDBERG, A. L. (1968). Protein synthesis during work-induced growth of skeletal muscle. Journal of Cell Biology 36, 653-658.
18. GUARDAVACCARO, D., CORRENTE, G., COVONE, F., MICHELI, L., D'AGNANO, I., STARACE, G., CARUSO, M. & TIRONE, F. (2000). Arrest of G(1)-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Molecular and Cellular Biology 20, 1797-1815.
19. HAWKE, T. J. & GARRY, D. J. (2001). Myogenic satellite cells: physiology to molecular biology. Journal of Applied Physiology 91, 534-551.
20. IYER, V. R., EISEN, M. B., ROSS, D. T., SCHULER, G., MOORE, T., LEE, J. C., TRENT, J. M., STAUDT, L. M., HUDSON, J. JR, BOGUSKI, M. S., LASHKARI, D., SHALON, D., BOTSTEIN, D. & BROWN, P. O. (1999). The transcriptional program in the response of human fibroblasts to serum. Science 283, 83-87.
21. JEFFERIES, H. B. & THOMAS, G. (1994). Elongation factor-1 alpha mRNA is selectively translated following mitogenic stimulation. Journal of Biological Chemistry 269, 4367-4372.
22. JEYASEELAN, R., POIZAT, C., BAKER, R. K., ABDISHOO, S., ISTERABADI, L. B., LYONS, G. E. & KEDES, L. (1997). A novel cardiac-restricted target for doxorubicin. CARP, a nuclear modulator of gene expression in cardiac progenitor cells and cardiomyocytes. Journal of Biological Chemistry 272, 22800-22808.
23. JIN, S., ANTINORE, M. J., LUNG, F. D., DONG, X., ZHAO, H., FAN, F., COLCHAGIE, A. B., BLANCK, P., ROLLER, P. P., FORNACE, A. J. JR & ZHAN, Q. (2000). The GADD45 inhibition of Cdc2 kinase correlates with GADD45-mediated growth suppression. Journal of Biological Chemistry 275, 16602-16608.
24. JOHNATTY, S. E., DYCK, J. R., MICHAEL, L. H., OLSON, E. N. & ABDELLATIF, M. (2000). Identification of genes regulated during mechanical load-induced cardiac hypertrophy. Journal of Molecular and Cellular Cardiology 32, 805-815.
25. KANAI, H., TANAKA, T., AIHARA, Y., TAKEDA, S., KAWABATA, M., MIYAZONO, K., NAGAI, R. & KURABAYASHI, M. (2001). Transforming growth factor-beta/Smads signaling induces transcription of the cell type-restricted ankyrin repeat protein CARP gene through CAGA motif in vascular smooth muscle cells. Circulation Research (Online) 88, 30-36.
26. KHALYFA, A., BOURBEAU, D., CHEN, E., PETROULAKIS, E., PAN, J., XU, S. & WANG, E. (2001). Characterization of elongation factor-1A (eEF1A-1) and eEF1A-2/S1 protein expression in normal and wasted mice. Journal of Biological Chemistry 276, 22915-22922.
27. KIM, S., LI, Q., DANG, C. V. & LEE, L. A. (2000). Induction of ribosomal genes and hepatocyte hypertrophy by adenovirus-mediated expression of c-Myc in vivo. Proceedings of the National Academy of Sciences of the USA 97, 11198-11202.
28. LAURENT, G. J., SPARROW, M. P. & MILLWARD, D. J. (1978). Turnover of muscle protein in the fowl. Changes in rates of protein synthesis and breakdown during hypertrophy of the anterior and posterior latissimus dorsi muscles. Biochemical Journal 176, 407-417.
29. LIM, D. S., ROBERTS, R. & MARIAN, A. (2001). Expression profiling of cardiac genes in human hypertrophic cardiomyopathy: insight into the pathogenesis of phenotypes. Journal of the American College of Cardiology 38, 1175-1180.
30. LLUIS, F., ROMA, J., SUELVES, M., PARRA, M., ANIORTE, G., GALLARDO, E., ILLA, I., RODRIGUEZ, L., HUGHES, S. M., CARMELIET, P., ROIG, M. & MUNOZ-CANOVES, P. (2001). Urokinase-dependent plasminogen activation is required for efficient skeletal muscle regeneration in vivo. Blood 97, 1703-1711.
31. LOCKE, M. & NOBLE, E. G. (1995). Stress proteins: the exercise response. Canadian Journal of Applied Physiology 20, 155-167.
32. LOCKHART, D. J., DONG, H., BYRNE, M. C., FOLLETTIE, M. T., GALLO, M. V., CHEE, M. S., MITTMANN, M., WANG, C., KOBAYASHI, M., HORTON, H. & BROWN, E. L. (1996). Expression monitoring by hybridization to high-density oligonucleotide arrays. Nature Biotechnology 14, 1675-1680.
33. MACDOUGALL, J. D., GIBALA, M. J., TARNOPOLSKY, M. A., MACDONALD, J. R., INTERISANO, S. A. & YARASHESKI, K. E. (1995). The time course for elevated muscle protein synthesis following heavy resistance exercise. Canadian Journal of Applied Physiology 20, 480-486.
34. MATHEWS, M., SONENBERG, N. & HERSHEY, J. (2000). Origins and Principles of Translational Control. In Translational Control of Gene Expression. ed. SONENBERG, N., HERSHEY, J. & MATHEWS, M., pp. 1-32. Cold Spring Harbor Press, New York.
35. MEYUHAS, O. & HORNSTEIN, E. (2000). Translational control of TOP mRNAs. In Translational Control of Gene Expression. ed. SONENBERG, N., HERSHEY, J. & MATHEWS, M., pp. 671-693. Cold Spring Harbor Press, New York.
36. NEIMAN, P. E., RUDDELL, A., JASONI, C., LORING, G., THOMAS, S. J., BRANDVOLD, K. A., LEE, R., BURNSIDE, J. & DELROW, J. (2001). Analysis of gene expression during myc oncogene-induced lymphomagenesis in the bursa of Fabricius. Proceedings of the National Academy of Sciences of the USA 98, 6378-6383.
37. OHNISHI, T., WANG, X, FUKUDA, S, TAKAHASHI, A, OHNISHI, K & S., N. (2000). Accumulation of tumor suppressor p53 in rat muscle after a space flight. Advances in Space Research 25, 2119-2122.
38. PILEGAARD, H., ORDWAY, G. A., SALTIN, B. & NEUFER, P. D. (2000). Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. American Journal of Physiology - Endocrinology and Metabolism 279, E806-814.
39. PLAFKER, S. M. & MACARA, I. G. (2002). Ribosomal protein L12 uses a distinct nuclear import pathway mediated by importin 11. Molecular and Cellular Biology 22, 1266-1275.
40. PRADET-BALADE, B. (2001). Translation control: bridging the gap between genomics and proteomics? Trends in Biochemical Sciences 26, 225-229.
41. PUNTSCHART, A.., WEY, E., JOSTARNDT, K., VOGT, M., WITTWER, M., WIDMER, H. R., HOPPELER, H. & BILLETER, R. (1998). Expression of fos and jun genes in human skeletal muscle after exercise. American Journal of Physiology 274, C129-137.
42. PUTMAN, C. T., DUSTERHOFT, S. & PETTE, D. (2000). Satellite cell proliferation in low frequency-stimulated fast muscle of hypothyroid rat. American Journal of Physiology - Cell Physiology 279, C682-690.
43. PYRONNET, S. & SONENBERG, N. (2001). Cell-cycle-dependent translational control. Current Opinion in Genetics and Development 11, 13-18.
44. SCHMALBRUCH, H. & HELLHAMMER, U. (1977). The number of nuclei in adult rat muscles with special reference to satellite cells. Anatomical Record 189, 169-175.
45. SCHULTZ, E. (1989). Satellite cell behavior during skeletal muscle growth and regeneration. Medicine and Science in Sports and Exercise 21, S181-186.
46. SHEIKH, M. S., HOLLANDER, M. C. & FORNANCE, A. J., JR (2000). Role of Gadd45 in apoptosis. Biochemical Pharmacology 59, 43-45.
47. SMITH, C. W., KLAASMEYER, J. G., WOODS, T. L. & JONES, S. J. (1999). Effects of IGF-I, IGF-II, bFGF and PDGF on the initiation of mRNA translation in C2C12 myoblasts and differentiating myoblasts. Tissue and Cell 31, 403-412.
48. SMITH, R. H., PALMER, R. M. & P. J. REED, P. J. (1983). Protein synthesis in isolated rabbit forelimb muscles. The possible role of metabolites of arachidonic acid in the response to intermittent stretching. Biochemical Journal 214, 153-161.
49. SRIVASTAVA, P., RUSSO, J., MGBONYEBI, O. & I. RUSSO, (1998). Growth inhibition and activation of apoptotic gene expression by human chorionic gonadotropin in human breast epithelial cells. Anticancer Research 18, 4003-4010.
50. TAYLOR, A., K., OBHOLZ, K., LINDEN, G., SADIEV, S. KLAUS, S. & CARLSON, K. O. (1998). DNA sequence and muscle-specific expression of human sarcosin transcripts. Molecular and Cellular Biochemistry 183, 105-112.
51. TAYLOR, W. R. & STARK, G. R. (2001). Regulation of the G2/M transition by p53. Oncogene 20, 1803-1815.
52. TERADA, K. & MORI, M. (2000). Human DnaJ homologs dj2 and dj3, and bag-1 are positive cochaperones of hsc70. Journal of Biological Chemistry 275, 24728-24734.
53. TIAINEN, M., PAJALUNGA, D., FERRANTELLI, F., SODDU, S., SALVATORI, G., SACCHI, A. & CRESCENZI, M. (1996). Terminally differentiated skeletal myotubes are not confined to G0 but can enter G1 upon growth factor stimulation. Cell Growth and Differentiation 7, 1039-1050.
54. WANG, X., LI, W., WILLIAMS, M., TERADA, N., ALESSI, D. R. & PROUD, C. G. (2001). Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO Journal 20, 4370-4379.
55. ZHAN, Q., CHEN, I. T., ANTINORE, M. J. & FORNACE, A. J. JR (1998). Tumor suppressor p53 can participate in transcriptional induction of the GADD45 promoter in the absence of direct DNA binding. (erratum appears in Molecular and Cellular Biology 18, 5620). Molecular and Cellular Biology 18, 2768-2778.
56. ZONG, Q., SCHUMMER, M., HOOD, L. & MORRIS, D. R. (1999). Messenger RNA translation state: the second dimension of high-throughput expression screening. Proceedings of the National Academy of Sciences of the USA 96, 10632-10636.
57. ZOU, Y., EVANS, S., CHEN, J., KUO, H., HARVEY, R. & CHIEN, K. (1997). CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development 124, 793-804.