Aging Affects the Transcriptional Regulation of Human Skeletal Muscle Disuse Atrophy

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Suetta, Charlotte ^a,d   Frandsen, Ulrik ^b   Jensen, Line ^a,b   Jensen, Mette Munk ^b   Jespersen, Jakob G ^a   Hvid, Lars G ^b   Bayer, Monika ^a   Petersson, Stine J ^c   Schrøder, Henrik D ^c   Andersen, Jesper L ^a   Heinemeier, Katja M ^a   Aagaard, Per ^b   Schjerling, Peter ^a   Kjaer, Michael ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; MESSENGER RNA; MUSCLE RING FINGER 1 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PROTEIN KINASE B; PROTEIN S6; TRANSCRIPTION FACTOR;

ADULT; AGED; AGING; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL SIZE; DISEASE COURSE; DOWN REGULATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMOBILIZATION; MALE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE MASS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION;

ADULT; AGED; AGING; APOPTOSIS; AUTOPHAGY; CYTOKINES; FORKHEAD TRANSCRIPTION FACTORS; HEAT-SHOCK PROTEINS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MALE; MIDDLE AGED; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DISORDERS, ATROPHIC; NF-KAPPA B; ORGAN SIZE; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; UBIQUITIN-PROTEIN LIGASES; YOUNG ADULT;

ANIMALIA;

EID: 84871274897     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051238     Document Type: Article

References (68)

1. Bloomfield SA, (1997) Changes in musculoskeletal structure and function with prolonged bed rest. Medicine and Science in Sports and Exercise 29: 197-206.
2. Janssen I, Heymsfield SB, Ross R, (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. Journal of the American Geriatrics Society 50: 889-896.
3. Furuno K, Goodman MN, Goldberg AL, (1990) Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265: 8550-8557.
4. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708.
5. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL, (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98: 14440-14445.
6. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, et al. (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51.
7. Booth FW, Seider MJ, (1979) Early change in skeletal muscle protein synthesis after limb immobilization of rats. J Appl Physiol 47: 974-977.
8. Watson PA, Stein JP, Booth FW, (1984) Changes in actin synthesis and alpha-actin-mRNA content in rat muscle during immobilization. Am J Physiol 247: C39-C44.
9. de Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, et al. (2007) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585: 241-251.
10. Gibson JN, Halliday D, Morrison WL, Stoward PJ, Hornsby GA, et al. (1987) Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 72: 503-509.
11. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, et al. (2008) Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586: 6049-6061.
12. Bruunsgaard H, Andersen-Ranberg K, Hjelmborg JB, Pedersen BK, Jeune B, (2003) Elevated levels of tumor necrosis factor alpha and mortality in centenarians. Am J Med 115: 278-283.
13. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, et al. (2005) Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19: 422-424.
14. Dirks A, Leeuwenburgh C, (2002) Apoptosis in skeletal muscle with aging. Am J Physiol Regul Integr Comp Physiol 282: R519-R527.
15. Dupont-Versteegden EE, (2005) Apoptosis in muscle atrophy: relevance to sarcopenia. Exp Gerontol 40: 473-481.
16. Carlson ME, Suetta C, Conboy MJ, Aagaard P, Mackey A, et al. (2009) Molecular aging and rejuvenation of human muscle stem cells. EMBO Mol Med 1: 381-391.
17. Grounds MD, (1998) Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. Ann N Y Acad Sci 854: 78-91.
18. Marcinek DJ, Schenkman KA, Ciesielski WA, Lee D, Conley KE, (2005) Reduced mitochondrial coupling in vivo alters cellular energetics in aged mouse skeletal muscle. J Physiol 569: 467-473.
19. Alway SE, Lowe DA, Chen KD, (2001) The effects of age and hindlimb supension on the levels of expression of the myogenic regulatory factors MyoD and myogenin in rat fast and slow skeletal muscles. Exp Physiol 86: 509-517.
20. Bar-Shai M, Carmeli E, Reznick AZ, (2005) The role of NF-kappaB in protein breakdown in immobilization, aging, and exercise: from basic processes to promotion of health. Ann N Y Acad Sci 1057: 431-447.
21. Suetta C, Hvid LG, Justesen L, Christensen U, Neergaard K, et al. (2009) Effects of aging on human skeletal muscle after immobilization and retraining. J Appl Physiol 107: 1172-1180.
22. Pistilli EE, Siu PM, Alway SE, (2006) Molecular regulation of apoptosis in fast plantaris muscles of aged rats. J Gerontol A Biol Sci Med Sci 61: 245-255.
23. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, et al. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019.
24. Hunter RB, Stevenson E, Koncarevic A, Mitchell-Felton H, Essig DA, et al. (2002) Activation of an alternative NF-kappaB pathway in skeletal muscle during disuse atrophy. FASEB J 16: 529-538.
25. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, et al. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471.
26. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, et al. (2007) Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21: 140-155.
27. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, et al. (2006) PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci U S A 103: 16260-16265.
28. Calura E, Cagnin S, Raffaello A, Laveder P, Lanfranchi G, et al. (2008) Meta-analysis of expression signatures of muscle atrophy: gene interaction networks in early and late stages. BMC Genomics 9: 630.
29. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC, (2003) Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J Physiol 551: 33-48.
30. Jagoe RT, Goldberg AL, (2001) What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care 4: 183-190.
31. Raffaello A, Laveder P, Romualdi C, Bean C, Toniolo L, et al. (2006) Denervation in murine fast-twitch muscle: short-term physiological changes and temporal expression profiling. Physiol Genomics 25: 60-74.
32. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, et al. (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6: 472-483.
33. Jones SW, Hill RJ, Krasney PA, O'Conner B, Peirce N, et al. (2004) Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18: 1025-1027.
34. Chen YW, Gregory CM, Scarborough MT, Shi R, Walter GA, et al. (2007) Transcriptional pathways associated with skeletal muscle disuse atrophy in humans. Physiol Genomics 31: 510-520.
35. Abadi A, Glover EI, Isfort RJ, Raha S, Safdar A, et al. (2009) Limb immobilization induces a coordinate down-regulation of mitochondrial and other metabolic pathways in men and women. PLoS ONE 4: e6518.
36. Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, et al. (2006) Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 576: 923-933.
37. Leger B, Derave W, De BK, Hespel P, Russell AP, (2008) Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res 11: 163-175B.
38. Zhao J, Brault JJ, Schild A, Goldberg AL, (2008) Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4: 378-380.
39. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, et al. (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412.
40. Senf SM, Dodd SL, Judge AR, (2010) FOXO signaling is required for disuse muscle atrophy and is directly regulated by Hsp70. Am J Physiol Cell Physiol 298: C38-C45.
41. Brault JJ, Jespersen JG, Goldberg AL, (2010) Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem 285: 19460-19471.
42. Marzetti E, Wohlgemuth SE, Lees HA, Chung HY, Giovannini S, et al. (2008) Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech Ageing Dev 129: 542-549.
43. Marzetti E, Carter CS, Wohlgemuth SE, Lees HA, Giovannini S, et al. (2009) Changes in IL-15 expression and death-receptor apoptotic signaling in rat gastrocnemius muscle with aging and life-long calorie restriction. Mech Ageing Dev 130: 272-280.
44. Phillips T, Leeuwenburgh C, (2005) Muscle fiber specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J 19: 668-670.
45. Pistilli EE, Jackson JR, Alway SE, (2006) Death receptor-associated pro-apoptotic signaling in aged skeletal muscle. Apoptosis 11: 2115-2126.
46. Siu PM, Pistilli EE, Butler DC, Alway SE, (2005) Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. Am J Physiol Cell Physiol 288: C338-C349.
47. Bruunsgaard H, Pedersen BK, (2003) Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am 23: 15-39.
48. Hvid L, Aagaard P, Justesen L, Bayer ML, Andersen JL, et al. (2010) Effects of aging on muscle mechanical function and muscle fiber morphology during short-term immobilization and subsequent retraining. J Appl Physiol 109: 1628-1634.
49. Suetta C, Andersen JL, Dalgas U, Berget J, Koskinen S, et al. (2008) Resistance training induces qualitative changes in muscle morphology, muscle architecture, and muscle function in elderly postoperative patients. J Appl Physiol 105: 180-186.
50. Bergström J, (1962) Muscle electrolytes in man. Scand J Clin Lab Invest 68 (suppl):: 1-110.
51. Guerra B, Gomez-Cabrera MC, Ponce-Gonzalez JG, Martinez-Bello VE, Guadalupe-Grau A, et al. (2011) Repeated muscle biopsies through a single skin incision do not elicit muscle signaling, but IL-6 mRNA and STAT3 phosphorylation increase in injured muscle. J Appl Physiol 110: 1708-1715.
52. Brooke MH, Kaiser KK, (1970) Muscle fiber types: How many and what kind? Arch Neurol 23: 369-379.
53. Kadi F, Schjerling P, Andersen LL, Charifi N, Madsen JL, et al. (2004) The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J Physiol 558: 1005-1012.
54. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
55. Thomason DB, Biggs RB, Booth F, (1989) Protein metabolism and beta-myosin heavy-chain mRNA in unweighted soleus muscle. Am J Physiol 257: R300-305.
56. Thomason DB, Booth FW, (1990) Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68: 1-12.
57. Gustafsson T, Osterlund T, Flanagan JN, von WF, Trappe TA, et al. (2010) Effects of 3 days unloading on molecular regulators of muscle size in humans. J Appl Physiol 109: 721-727.
58. Ferrando AA, Lane HW, Stuart CA, vis-Street J, Wolfe RR, (1996) Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 270: E627-E633.
59. Paddon-Jones D, Sheffield-Moore M, Cree MG, Hewlings SJ, Aarsland A, et al. (2006) Atrophy and impaired muscle protein synthesis during prolonged inactivity and stress. J Clin Endocrinol Metab 91: 4836-4841.
60. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, et al. (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14: 395-403.
61. Sacheck JM, Ohtsuka A, McLary SC, Goldberg AL, (2004) IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am J Physiol Endocrinol Metab 287: E591-E601.
62. Kimball SR, O'Malley JP, Anthony JC, Crozier SJ, Jefferson LS, (2004) Assessment of biomarkers of protein anabolism in skeletal muscle during the life span of the rat: sarcopenia despite elevated protein synthesis. Am J Physiol Endocrinol Metab 287: E772-E780.
63. Sandri M, (2008) Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23: 160-170.
64. Malmgren LT, Jones CE, Bookman LM, (2001) Muscle fiber and satellite cell apoptosis in the aging human thyroarytenoid muscle: a stereological study with confocal laser scanning microscopy. Otolaryngol Head Neck Surg 125: 34-39.
65. Strasser H, Tiefenthaler M, Steinlechner M, Eder I, Bartsch G, et al. (2000) Age dependent apoptosis and loss of rhabdosphincter cells. J Urol 164: 1781-1785.
66. Whitman SA, Wacker MJ, Richmond SR, Godard MP, (2009) Contributions of the ubiquitin-proteasome pathway and apoptosis to human skeletal muscle wasting with age. Pflugers Arch 450: 437-446.
67. Dupont-Versteegden EE, Strotman BA, Gurley CM, Gaddy D, Knox M, et al. (2006) Nuclear translocation of EndoG at the initiation of disuse muscle atrophy and apoptosis is specific to myonuclei. Am J Physiol Regul Integr Comp Physiol 291: R1730-R1740.
68. Bruusgaard JC, Gundersen K, (2008) In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy. J Clin Invest 118: 1450-1457.