Effects of aging and gender on muscle mass and regulation of Akt-mTOR-p70s6k related signaling in the F344BN rat model

Mechanisms of Ageing and Development

Volumn 131, Issue 3, 2010, Pages 202-209

  Paturi, Satyanarayana ^a   Gutta, Anil K ^a   Katta, Anjaiah ^b   Kakarla, Sunil K ^b   Arvapalli, Ravi K ^a   Gadde, Murali K ^a   Nalabotu, Siva K ^b   Rice, Kevin M ^a   Wu, Miaozong ^a   Blough, Eric ^a,b  

^a MARSHALL UNIVERSITY   (United States)

^b MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Gender; Sarcopenia; Skeletal muscle

Indexed keywords

ADENYLATE KINASE; CALCINEURIN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; S6 KINASE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; EMBRYO; ENZYME REGULATION; EXTENSOR DIGITORUM LONGUS MUSCLE; FEMALE; FISCHER 344 RAT; MALE; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE TWITCH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SOLEUS MUSCLE;

AGING; ANIMALS; CALCINEURIN; FEMALE; MALE; MAMMALS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MUSCULAR DISEASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, INBRED BN; RATS, INBRED F344; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SARCOPENIA; SIGNAL TRANSDUCTION; SIROLIMUS;

ANIMALIA; MAMMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 77950025967     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2010.01.008     Document Type: Article

References (49)

1. Alessi D.R., Pearce L.R., Garcia-Martinez J.M. New insights into mTOR signaling: mTORC2 and beyond. Sci. Signal. 2009, 2:pe27.
2. Baar K., Esser K. Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am. J. Physiol. 1999, 276:C120-C127.
3. 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., Yancopoulos G.D. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 2001, 3:1014-1019.
4. Brown E.J., Albers M.W., Shin T.B., Ichikawa K., Keith C.T., Lane W.S., Schreiber S.L. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 1994, 369:756-758.
5. Caccia M.R., Harris J.B., Johnson M.A. Morphology and physiology of skeletal muscle in aging rodents. Muscle Nerve 1979, 2:202-212.
6. Chale-Rush A., Morris E.P., Kendall T.L., Brooks N.E., Fielding R.A. Effects of chronic overload on muscle hypertrophy and mTOR signaling in young adult and aged rats. J. Gerontol. A: Biol. Sci. Med. Sci. 2009, 64:1232-1239.
7. Chou M.M., Blenis J. The 70kDa S6 kinase: regulation of a kinase with multiple roles in mitogenic signalling. Curr. Opin. Cell Biol. 1995, 7:806-814.
8. Davies C.T., Rutherford I.C., Thomas D.O. Electrically evoked contractions of the triceps surae during and following 21 days of voluntary leg immobilization. Eur. J. Appl. Physiol. Occup. Physiol. 1987, 56:306-312.
9. Dorn G.W., Force T. Protein kinase cascades in the regulation of cardiac hypertrophy. J. Clin. Invest. 2005, 115:527-537.
10. Drummond M.J., Dreyer H.C., Pennings B., Fry C.S., Dhanani S., Dillon E.L., Sheffield-Moore M., Volpi E., Rasmussen B.B. Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. J. Appl. Physiol. 2008, 104:1452-1461.
11. Fang Y., Vilella-Bach M., Bachmann R., Flanigan A., Chen J. Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 2001, 294:1942-1945.
12. Franke T.F., Kaplan D.R., Cantley L.C. PI3K: downstream AKTion blocks apoptosis. Cell 1997, 88:435-437.
13. Gingras A.C., Raught B., Sonenberg N. Control of translation by the target of rapamycin proteins. Prog. Mol. Subcell. Biol. 2001, 27:143-174.
14. Gingras A.C., Raught B., Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 2001, 15:807-826.
15. Gupte A.A., Bomhoff G.L., Geiger P.C. Age-related differences in skeletal muscle insulin signaling: the role of stress kinases and heat shock proteins. J. Appl. Physiol. 2008, 105:839-848.
16. Haddad F., Adams G.R. Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J. Appl. Physiol. 2006, 100:1188-1203.
17. Hardie D.G. The AMP-activated protein kinase pathway-new players upstream and downstream. J. Cell Sci. 2004, 117:5479-5487.
18. Hornberger T.A., Sukhija K.B., Wang X.R., Chien S. mTOR is the rapamycin-sensitive kinase that confers mechanically-induced phosphorylation of the hydrophobic motif site Thr(389) in p70(S6k). FEBS Lett. 2007, 581:4562-4566.
19. Horsley V., Pavlath G.K. NFAT: ubiquitous regulator of cell differentiation and adaptation. J. Cell Biol. 2002, 156:771-774.
20. Iannuzzi-Sucich M., Prestwood K.M., Kenny A.M. Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy, older men and women. J. Gerontol. A: Biol. Sci. Med. Sci. 2002, 57:M772-M777.
21. Janssen I., Shepard D.S., Katzmarzyk P.T., Roubenoff R. The healthcare costs of sarcopenia in the United States. J. Am. Geriatr. Soc. 2004, 52:80-85.
22. Karlsson J. Metabolic adaptations to exercise: a review of potential beta-adrenoceptor antagonist effects. Am. J. Cardiol. 1985, 55:48D-58D.
23. Kinnard R.S., Mylabathula D.B., Uddemarri S., Rice K.M., Wright G.L., Blough E.R. Regulation of p70S6k, GSK-3beta, and calcineurin in rat striated muscle during aging. Biogerontology 2005, 6:173-184.
24. Klee C.B., Ren H., Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J. Biol. Chem. 1998, 273:13367-13370.
25. Klitgaard H., Brunet A., Maton B., Lamaziere C., Lesty C., Monod H. Morphological and biochemical changes in old rat muscles: effect of increased use. J. Appl. Physiol. 1989, 67:1409-1417.
26. Lauretani F., Russo C.R., Bandinelli S., Bartali B., Cavazzini C., Di Iorio A., Corsi A.M., Rantanen T., Guralnik J.M., Ferrucci L. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J. Appl. Physiol. 2003, 95:1851-1860.
27. Marzetti E., Wohlgemuth S.E., Lees H.A., Chung H.Y., Giovannini S., Leeuwenburgh C. Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech. Ageing Dev. 2008.
28. McCullagh K.J., Calabria E., Pallafacchina G., Ciciliot S., Serrano A.L., Argentini C., Kalhovde J.M., Lomo T., Schiaffino S. NFAT is a nerve activity sensor in skeletal muscle and controls activity-dependent myosin switching. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:10590-10595.
29. Mitchell P.O., Mills S.T., Pavlath G.K. Calcineurin differentially regulates maintenance and growth of phenotypically distinct muscles. Am. J. Physiol. Cell Physiol. 2002, 282:C984-C992.
30. Mitchell P.O., Pavlath G.K. Multiple roles of calcineurin in skeletal muscle growth. Clin. Orthop. Relat. Res. 2002, S197-202.
31. Pansarasa O., Flati V., Corsetti G., Brocca L., Pasini E., D'Antona G. Oral amino acid supplementation counteracts age-induced sarcopenia in elderly rats. Am. J. Cardiol. 2008, 101:35E-41E.
32. Paturi S., Gutta A.K., Kakarla S.K., Katta A., Arnold E.C., Wu M., Rice K.M., Blough E.R. Impaired overload-induced hypertrophy in obese Zucker rat slow-twitch skeletal muscle. J. Appl. Physiol. 2010, 108(1):7-13.
33. Pause A., Belsham G.J., Gingras A.C., Donze O., Lin T.A., Lawrence J.C., Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 1994, 371:762-767.
34. Peterson R.T., Beal P.A., Comb M.J., Schreiber S.L. FKBP12-rapamycin-associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J. Biol. Chem. 2000, 275:7416-7423.
35. Rantanen T. Muscle strength, disability and mortality. Scand. J. Med. Sci. Sports 2003, 13:3-8.
36. Rao A., Luo C., Hogan P.G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 1997, 15:707-747.
37. Rice K.M., Wu M., Blough E.R. Aortic aging in the Fischer 344/NNiaHSd x Brown Norway/BiNia Rat. J. Pharmacol. Sci. 2008, 108(4):393-398. 10.1254/jphs.08R02CP.
38. Richmond S.R., Touchberry C.D., Gallagher P.M. Forskolin attenuates the action of insulin on the Akt-mTOR pathway in human skeletal muscle. Appl. Physiol. Nutr. Metab. 2009, 34:916-925.
39. Sabatini D.M., Erdjument-Bromage H., Lui M., Tempst P., Snyder S.H. RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 1994, 78:35-43.
40. Sato T., Akatsuka H., Kito K., Tokoro Y., Tauchi H., Kato K. Age changes in size and number of muscle fibers in human minor pectoral muscle. Mech. Ageing Dev. 1984, 28:99-109.
41. Serrano A.L., Murgia M., Pallafacchina G., Calabria E., Coniglio P., Lomo T., Schiaffino S. Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:13108-13113.
42. Spangenburg E.E. Changes in muscle mass with mechanical load: possible cellular mechanisms. Appl. Physiol. Nutr. Metab. 2009, 34:328-335.
43. Syrovy I., Gutmann E. Changes in speed of contraction and ATPase activity in striated muscle during old age. Exp. Gerontol. 1970, 5:31-35.
44. Thomson D.M., Fick C.A., Gordon S.E. AMPK activation attenuates S6K1, 4EBP1, and eEF2 signaling responses to high-frequency electrically stimulated skeletal muscle contractions. J. Appl. Physiol. 2008, 104:625-632.
45. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications, 1979. Biotechnology 1992, 24:145-149.
46. Wiederrecht G.J., Sabers C.J., Brunn G.J., Martin M.M., Dumont F.J., Abraham R.T. Mechanism of action of rapamycin: new insights into the regulation of G1-phase progression in eukaryotic cells. Prog. Cell Cycle Res. 1995, 1:53-71.
47. Wu, M., Fannin, J., Rice, K.M., Wang, B., Blough, E.R., 2009a. Effect of aging on cellular mechanotransduction. Ageing Res. Rev. PMid: 19932197. doi:10.1016/j.arr.2009.11.002.
48. Wu M., Desai D.H., Kakarla S.K., Katta A., Paturi S., Gutta A.K., Rice K.M., Walker E.M., Blough E.R. Acetaminophen prevents aging-associated hyperglycemia in aged rats: effect of aging-associated hyperactivation of p38-MAPK and ERK1/2. Diabetes Metab. Res. Rev. 2009, 25(3):279-286. 10.1002/dmrr.932.
49. Wu M., Katta A., Gadde M.K., Liu H., Kakarla S.K., Fannin J., Paturi S., Arvapalli R.K., Rice K.M., Wang Y., Blough E.R. Aging-associated dysfunction of akt/protein kinase B: s-nitrosylation and acetaminophen intervention. PLoS One 2009, 4(7):e6430. 10.1371/journal.pone.0006430.