Electrostimulation during hindlimb unloading modulates PI3K-AKT downstream targets without preventing soleus atrophy and restores slow phenotype through ERK

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 2, 2011, Pages

  Dupont, Erwan ^a   Cieniewski Bernard, Caroline ^a   Bastide, Bruno ^a   Stevens, Laurence ^a  

^a UNIVERSITÉ D'ARTOIS   (France)

Author keywords

Glycolytic metabolism; Low frequency stimulation; Mitogen activated protein kinase pathway; Myosin heavy chain isoform

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MUSCLE RING FINGER 1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; S6 KINASE; TRANSCRIPTION FACTOR FOXO;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DOWN REGULATION; ELECTROSTIMULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HEAVY CHAIN; HINDLIMB; MALE; MUSCLE ATROPHY; MUSCLE MASS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SOLEUS MUSCLE; UPREGULATION;

ANIMALS; DOWN-REGULATION; ELECTRIC STIMULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FORKHEAD TRANSCRIPTION FACTORS; GLYCOLYSIS; HINDLIMB SUSPENSION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOSIN HEAVY CHAINS; NERVE TISSUE PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TIBIAL NERVE; TOR SERINE-THREONINE KINASES; UP-REGULATION;

EID: 79551538314     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00793.2009     Document Type: Article

References (46)

1. Allen DL, Leinwand LA. Intracellular calcium and myosin isoform transitions. Calcineurin and calcium-calmodulin kinase pathways regulate preferential activation of the IIa myosin heavy chain promoter. J Biol Chem 277: 45323-45330, 2002.
2. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, Wackerhage H. Selective activation of AMPK-PGC-1α or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19: 786-788, 2005.
3. Baldwin KM, Haddad F. Skeletal muscle plasticity: cellular and molecular responses to altered physical activity paradigms. Am J Phys Med Rehabil 81: S40-S51, 2002.
4. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
5. Boonyarom O, Inui K. Atrophy and hypertrophy of skeletal muscles: structural and functional aspects. Acta Physiol (Oxf) 188: 77-89, 2006.
6. Buonanno A, Fields RD. Gene regulation by patterned electrical activity during neural and skeletal muscle development. Curr Opin Neurobiol 9: 110-120, 1999.
7. Carlson CJ, Fan Z, Gordon SE, Booth FW. Time course of the MAPK and PI3-kinase response within 24 h of skeletal muscle overload. J Appl Physiol 91: 2079-2087, 2001.
8. Chen Z, Gibson TB, Robinson F, Silvestro L, Pearson G, Xu B, Wright A, Vanderbilt C, Cobb MH. MAP kinases. Chem Rev 101: 2449-2476, 2001.
9. Childs TE, Spangenburg EE, Vyas DR, Booth FW. Temporal alterations in protein signaling cascades during recovery from muscle atrophy. Am J Physiol Cell Physiol 285: C391-C398, 2003.
10. Fitts RH, Riley DR, Widrick JJ. Physiology of a microgravity environment invited review: microgravity and skeletal muscle. J Appl Physiol 89: 823-839, 2000.
11. Fluck M, Hoppeler H. Molecular basis of skeletal muscle plasticity-from gene to form and function. Rev Physiol Biochem Pharmacol 146: 159-216, 2003.
12. Glass DJ. Molecular mechanisms modulating muscle mass. Trends Mol Med 9: 344-350, 2003.
13. Han B, Zhu MJ, Ma C, Du M. Rat hindlimb unloading down-regulates insulin like growth factor-1 signaling and AMP-activated protein kinase, and leads to severe atrophy of the soleus muscle. Appl Physiol Nutr Metab 32: 1115-1123, 2007.
14. Higginson J, Wackerhage H, Woods N, Schjerling P, Ratkevicius A, Grunnet N, Quistorff B. Blockades of mitogen-activated protein kinase and calcineurin both change fibre-type markers in skeletal muscle culture. Pflügers Arch 445: 437-443, 2002.
15. Hilder TL, Tou JC, Grindeland RE, Wade CE, Graves LM. Phosphorylation of insulin receptor substrate-1 serine 307 correlates with JNK activity in atrophic skeletal muscle. FEBS Lett 553: 63-67, 2003.
16. Hirose T, Nakazato K, Song H, Ishii N. TGF-beta1 and TNF-alpha are involved in the transcription of type I collagen α2 gene in soleus muscle atrophied by mechanical unloading. J Appl Physiol 104: 170-177, 2008.
17. Hornberger TA, Hunter RB, Kandarian SC, Esser KA. Regulation of translation factors during hindlimb unloading and denervation of skeletal muscle in rats. Am J Physiol Cell Physiol 281: C179-C187, 2001.
18. Isfort RJ, Wang F, Greis KD, Sun Y, Keough TW, Farrar RP, Bodine SC, Anderson NL. Proteomic analysis of rat soleus muscle undergoing hindlimb suspension-induced atrophy and reweighting hypertrophy. Proteomics 2: 543-550, 2002.
19. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, Nishino I, Ezaki O. Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279: 41114-41123, 2004.
20. Kandarian SC, Jackman RW. Intracellular signaling during skeletal muscle atrophy. Muscle Nerve 33: 155-165, 2006.
21. Lee YH, Giraud J, Davis RJ, White MF. c-Jun N-terminal kinase (JNK) mediates feedback inhibition of the insulin signaling cascade. J Biol Chem 278: 2896-2902, 2003.
22. Leterme D, Falempin M. Compensatory effects of chronic electrostimulation on unweighted rat soleus muscle. Pflügers Arch 426: 155-160, 1994.
23. Li YP, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J 19: 362-370, 2005.
24. Meissner JD, Chang KC, Kubis HP, Nebreda AR, Gros G, Scheibe RJ. The p38alpha/beta mitogen-activated protein kinases mediate recruitment of CREB-binding protein to preserve fast myosin heavy chain IId/x gene activity in myotubes. J Biol Chem 282: 7265-7275, 2007.
25. Morey ER, Sabelman EE, Turner RT, Baylink DJ. A new rat model simulating some aspects of space flight. Physiologist 22: S23-S24, 1979.
26. Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects. J Appl Physiol 92: 1367-1377, 2002.
27. 2+ activation properties in human muscle fibers: effects of a 60-day bed rest and countermeasures. J Appl Physiol 106: 1086-1099, 2009.
28. Murgia M, Serrano AL, Calabria E, Pallafacchina G, Lomo T, Schiaffino S. Ras is involved in nerve-activity-dependent regulation of muscle genes. Nat Cell Biol 2: 142-147, 2000.
29. Pallafacchina G, Calabria E, Serrano AL, Kalhovde JM, Schiaffino S. A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc Natl Acad Sci U S A 99: 9213-9218, 2002.
30. Parkington JD, Siebert AP, LeBrasseur NK, Fielding RA. Differential activation of mTOR signaling by contractile activity in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 285: R1086-R1090, 2003.
31. Pette D, Staron RS. Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 170: 143-223, 1997.
32. Russo TL, Peviani SM, Durigan JL, Gigo-Benato D, Delfino GB, Salvini TF. Stretching and electrical stimulation reduce the accumulation of MyoD, myostatin and atrogin-1 in denervated rat skeletal muscle. J Muscle Res Cell Motil 31:45-57, 2010.
33. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23: 160-170, 2008.
34. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412, 2004.
35. Schiaffino S, Sandri M, Murgia M. Activity-dependent signaling pathways controlling muscle diversity and plasticity. Physiology (Bethesda) 22: 269-278, 2007.
36. Shi H, Scheffler JM, Zeng C, Pleitner JM, Hannon KM, Grant AL, Gerrard DE. Mitogen-activated protein kinase signaling is necessary for the maintenance of skeletal muscle mass. Am J Physiol Cell Physiol 296: C1040-C1048, 2009.
37. Stein TP, Wade CE. Metabolic consequences of muscle disuse atrophy. J Nutr 135: 1824S-1828S, 2005.
38. Stevens L, Sultan KR, Peuker H, Gohlsch B, Mounier Y, Pette D. Time-dependent changes in myosin heavy chain mRNA and protein isoforms in unloaded soleus muscle of rat. Am J Physiol Cell Physiol 277: C1044-C1049, 1999.
39. Sugiura T, Abe N, Nagano M, Goto K, Sakuma K, Naito H, Yoshioka T, Powers SK. Changes in PKB/Akt and calcineurin signaling during recovery in atrophied soleus muscle induced by unloading. Am J Physiol Regul Integr Comp Physiol 288: R1273-R1278, 2005.
40. Thomason DB, Booth FW. Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68: 1-12, 1990.
41. Thomson DM, Fick CA, Gordon SE. AMPK activation attenuates S6K1, 4E-BP1, and eEF2 signaling responses to high-frequency electrically stimulated skeletal muscle contractions. J Appl Physiol 104: 625-632, 2008.
42. Tidball JG. Mechanical signal transduction in skeletal muscle growth and adaptation. J Appl Physiol 98: 1900-1908, 2005.
43. Toursel T, Stevens L, Mounier Y. Evolution of contractile and elastic properties of rat soleus muscle fibres under unloading conditions. Exp Physiol 84: 93-107, 1999.
44. Westgaard RH, Lomo T. Control of contractile properties within adaptive ranges by patterns of impulse activity in the rat. J Neurosci 8: 4415-4426, 1988.
45. Zanchi NE, Lancha AH Jr. Mechanical stimuli of skeletal muscle: implications on mTOR/p70s6k and protein synthesis. Eur J Appl Physiol 102: 253-263, 2008.
46. Zhang P, Chen X, Fan M. Signaling mechanisms involved in disuse muscle atrophy. Med Hypotheses 69: 310-321, 2007.