Intracellular signaling pathways regulating net protein balance following diaphragm muscle denervation

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 2, 2011, Pages

  Argadine, Heather M ^a   Mantilla, Carlos B ^a,b   Zhan, Wen Zhi ^a   Sieck, Gary C ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Innervation; Protein synthesis; Skeletal muscle

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INITIATION FACTOR 4E; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEASOME; TRANSCRIPTION FACTOR FOXO;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIAPHRAGM MUSCLE; ENZYME ACTIVATION; INTRACELLULAR SIGNALING; MALE; MUSCLE DENERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DIAPHRAGM; DOWN-REGULATION; EUKARYOTIC INITIATION FACTOR-4E; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FORKHEAD TRANSCRIPTION FACTORS; GLYCOGEN SYNTHASE KINASE 3; MALE; MUSCLE DENERVATION; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EUKARYOTA; MAMMALIA; RATTUS;

EID: 79251576152     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00172.2010     Document Type: Article

References (76)

1. Akoumianaki T, Kardassis D, Polioudaki H, Georgatos SD, Theodoropoulos PA. Nucleocytoplasmic shuttling of soluble tubulin in mammalian cells. J Cell Sci 122: 1111-1118, 2009.
2. Anthony JC, Yoshizawa F, Anthony TG, Vary TC, Jefferson LS, Kimball SR. Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J Nutr 130: 2413-2419, 2000.
3. Argadine HM, Hellyer NJ, Mantilla CB, Zhan WZ, Sieck GC. The effect of denervation on protein synthesis and degradation in adult rat diaphragm muscle. J Appl Physiol 107: 438-444, 2009.
4. Baar K, Esser K. Phosphorylation of p70S6k correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol Cell Physiol 276: C120-C127, 1999.
5. Bamman MM, Shipp JR, Jiang J, Gower BA, Hunter GR, Goodman A, McLafferty CL Jr, Urban RJ. Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol Endocrinol Metab 280: E383-E390, 2001.
6. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001.
7. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277: 23977-23980, 2002.
8. Bray JJ, Harris AJ. Dissociation between nerve-muscle transmission and nerve trophic effects on rat diaphragm using type D botulinum toxin. J Physiol 253: 53-77, 1975.
9. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868, 1999.
10. Brunn GJ, Hudson CC, Sekulic A, Williams JM, Hosoi H, Houghton PJ, Lawrence JC Jr, Abraham RT. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277: 99-101, 1997.
11. Cao P, Hanai J, Tanksale P, Imamura S, Sukhatme VP, Lecker SH. Statin-induced muscle damage and atrogin-1 induction is the result of a geranylgeranylation defect. FASEB J 23: 2844-2854, 2009.
12. Chen J. Novel regulatory mechanisms of mTOR signaling. Curr Top Microbiol Immunol 279: 245-257, 2004.
13. Cho JE, Fournier M, Da X, Lewis MI. Time course expression of Foxo transcription factors in skeletal muscle following corticosteroid administration. J Appl Physiol 108: 137-145, 2010.
14. Copp J, Manning G, Hunter T. TORC-specific phosphorylation of mammalian target of rapamycin (mTOR): phospho-Ser2481 is a marker for intact mTOR signaling complex 2. Cancer Res 69: 1821-1827, 2009.
15. Corton JM, Gillespie JG, Hawley SA, Hardie DG. 5-Aminoimidazole-4- carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem 229: 558-565, 1995.
16. Eliasson J, Elfegoun T, Nilsson J, Kohnke R, Ekblom B, Blomstrand E. Maximal lengthening contractions increase p70 S6 kinase phosphorylation in human skeletal muscle in the absence of nutritional supply. Am J Physiol Endocrinol Metab 291: E1197-E1205, 2006.
17. Gingras AC, Kennedy SG, O'Leary MA, Sonenberg N, Hay N. 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev 12: 502-513, 1998.
18. Glass DJ. Molecular mechanisms modulating muscle mass. Trends Mol Med 9: 344-350, 2003.
19. Glass DJ. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 5: 87-90, 2003.
20. Gosselin LE, Brice G, Carlson B, Prakash YS, Sieck GC. Changes in satellite cell mitotic activity during acute period of unilateral diaphragm denervation. J Appl Physiol 77: 1128-1134, 1994.
21. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, Brunet A. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17: 1646-1656, 2007.
22. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP, Brunet A. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282: 30107-30119, 2007.
23. Hardie DG, Carling D. The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur J Biochem 246: 259-273, 1997.
24. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 18: 1926-1945, 2004.
25. Hellyer NJ, Mantilla CB, Park EW, Zhan WZ, Sieck GC. Neuregulin-dependent protein synthesis in C2C12 myotubes and rat diaphragm muscle. Am J Physiol Cell Physiol 291: C1056-C1061, 2006.
26. Hoffman EP, Nader GA. Balancing muscle hypertrophy and atrophy. Nat Med 10: 584-585, 2004.
27. Hornberger TA, Chu WK, Mak YW, Hsiung JW, Huang SA, Chien S. The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle. Proc Natl Acad Sci USA 103: 4741-4746, 2006.
28. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, Wang CY, He X, MacDougald OA, You M, Williams BO, Guan KL. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126: 955-968, 2006.
29. Jacinto E, Hall MN. Tor signalling in bugs, brain and brawn. Nat Rev Mol Cell Biol 4: 117-126, 2003.
30. Jefferson LS, Fabian JR, Kimball SR. Glycogen synthase kinase-3 is the predominant insulin-regulated eukaryotic initiation factor 2B kinase in skeletal muscle. Int J Biochem Cell Biol 31: 191-200, 1999.
31. Jorgensen SB, Richter EA, Wojtaszewski JF. Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J Physiol 574: 17-31, 2006.
32. 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.
33. Kim SJ, Roy RR, Kim JA, Zhong H, Haddad F, Baldwin KM, Edgerton VR. Gene expression during inactivity-induced muscle atrophy: effects of brief bouts of a forceful contraction countermeasure. J Appl Physiol 105: 1246-1254, 2008.
34. Kimball SR, Jurasinski CV, Lawrence JC Jr, Jefferson LS. Insulin stimulates protein synthesis in skeletal muscle by enhancing the association of eIF-4E and eIF-4G. Am J Physiol Cell Physiol 272: C754-C759, 1997.
35. King TD, Song L, Jope RS. AMP-activated protein kinase (AMPK) activating agents cause dephosphorylation of Akt and glycogen synthase kinase-3. Biochem Pharmacol 71: 1637-1647, 2006.
36. Kleijn M, Scheper GC, Voorma HO, Thomas AA. Regulation of translation initiation factors by signal transduction. Eur J Biochem 253: 531-544, 1998.
37. Lantier L, Mounier R, Leclerc J, Pende M, Foretz M, Viollet B. Coordinated maintenance of muscle cell size control by AMP-activated protein kinase. FASEB J 24: 3555-3561.
38. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471, 2007.
39. Martelli AM, Tazzari PL, Evangelisti C, Chiarini F, Blalock WL, Billi AM, Manzoli L, McCubrey JA, Cocco L. Targeting the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin module for acute myelogenous leukemia therapy: from bench to bedside. Curr Med Chem 14: 2009-2023, 2007.
40. Mascher H, Andersson H, Nilsson PA, Ekblom B, Blomstrand E. Changes in signalling pathways regulating protein synthesis in human muscle in the recovery period after endurance exercise. Acta Physiol (Oxf) 191: 67-75, 2007.
41. Miyata H, Zhan WZ, Prakash YS, Sieck GC. Myoneural interactions affect diaphragm muscle adaptations to inactivity. J Appl Physiol 79: 1640-1649, 1995.
42. Moylan JS, Smith JD, Chambers MA, McLoughlin TJ, Reid MB. TNF induction of atrogin-1/MAFbx mRNA depends on Foxo4 expression but not AKT-Foxo1/3 signaling. Am J Physiol Cell Physiol 295: C986-C993, 2008.
43. Nakashima K, Yakabe Y. AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 71: 1650-1656, 2007.
44. 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 USA 99: 9213-9218, 2002.
45. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, Lawrence JC Jr, Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5=-cap function. Nature 371: 762-767, 1994.
46. Peterson RT, Beal PA, Comb MJ, Schreiber SL. FKBP12-rapamycin-associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J Biol Chem 275: 7416-7423, 2000.
47. Raught B, Gingras AC. eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31: 43-57, 1999.
48. Reynolds THt Bodine SC, Lawrence JC Jr. Control of Ser2448 phosphorylation in the mammalian target of rapamycin by insulin and skeletal muscle load. J Biol Chem 277: 17657-17662, 2002.
49. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013, 2001.
50. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD, Glass DJ. Differentiation stagespecific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286: 1738-1741, 1999.
51. Rose AJ, Bisiani B, Vistisen B, Kiens B, Richter EA. Skeletal muscle eEF2 and 4EBP1 phosphorylation during endurance exercise is dependent on intensity and muscle fiber type. Am J Physiol Regul Integr Comp Physiol 296: R326-R333, 2009.
52. Saito Y, Vandenheede JR, Cohen P. The mechanism by which epidermal growth factor inhibits glycogen synthase kinase 3 in A431 cells. Biochem J 303: 27-31, 1994.
53. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23: 160-170, 2008.
54. 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.
55. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 14: 1296-1302, 2004.
56. Sarbassov DD, Ali SM, Sabatini DM. Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603, 2005.
57. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101, 2005.
58. Senf SM, Dodd SL, Judge AR. FOXO signaling is required for disuse muscle atrophy and is directly regulated by Hsp70. Am J Physiol Cell Physiol 298: C38-C45, 2010.
59. Shah OJ, Anthony JC, Kimball SR, Jefferson LS. 4E-BP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle. Am J Physiol Endocrinol Metab 279: E715-E729, 2000.
60. Skurk C, Maatz H, Kim HS, Yang J, Abid MR, Aird WC, Walsh K. The Akt-regulated forkhead transcription factor FOXO3a controls endothelial cell viability through modulation of the caspase-8 inhibitor FLIP. J Biol Chem 279: 1513-1525, 2004.
61. Smith JW, Thesleff S. Spontaneous activity in denervated mouse diaphragm muscle. J Physiol 257: 171-186, 1976.
62. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14: 395-403, 2004.
63. Takahashi A, Kureishi Y, Yang J, Luo Z, Guo K, Mukhopadhyay D, Ivashchenko Y, Branellec D, Walsh K. Myogenic Akt signaling regulates blood vessel recruitment during myofiber growth. Mol Cell Biol 22:4803-4814, 2002.
64. Thimmaiah KN, Easton JB, Germain GS, Morton CL, Kamath S, Buolamwini JK, Houghton PJ. Identification of N10-substituted phenoxazines as potent and specific inhibitors of Akt signaling. J Biol Chem 280: 31924-31935, 2005.
65. Vandenburgh HH, Karlisch P, Shansky J, Feldstein R. Insulin and IGF-I induce pronounced hypertrophy of skeletal myofibers in tissue culture. Am J Physiol Cell Physiol 260: C475-C484, 1991.
66. Walss C, Kreisberg JI, Luduena RF. Presence of the betaII isotype of tubulin in the nuclei of cultured mesangial cells from rat kidney. Cell Motil Cytoskeleton 42: 274-284, 1999.
67. Wang X, Proud CG. The mTOR pathway in the control of protein synthesis. Physiology (Bethesda) 21: 362-369, 2006.
68. Waskiewicz AJ, Flynn A, Proud CG, Cooper JA. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J 16: 1909-1920, 1997.
69. Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 19: 1871-1880, 1999.
70. Williamson DL, Bolster DR, Kimball SR, Jefferson LS. Time course changes in signaling pathways and protein synthesis in C2C12 myotubes following AMPK activation by AICAR. Am J Physiol Endocrinol Metab 291: E80-E89, 2006.
71. Xu K, Luduena RF. Characterization of nuclear betaII-tubulin in tumor cells: a possible novel target for taxol. Cell Motil Cytoskeleton 53: 39-52, 2002.
72. 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.
73. Zhan WZ, Farkas GA, Schroeder MA, Gosselin LE, Sieck GC. Regional adaptations of rabbit diaphragm muscle fibers to unilateral denervation. J Appl Physiol 79: 941-950, 1995.
74. Zhan WZ, Miyata H, Prakash YS, Sieck GC. Metabolic and phenotypic adaptations of diaphragm muscle fibers with inactivation. J Appl Physiol 82: 1145-1153, 1997.
75. Zhan WZ, Sieck GC. Adaptations of diaphragm and medial gastrocnemius muscles to inactivity. J Appl Physiol 72: 1445-1453, 1992.
76. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6: 472-483, 2007.