Power training and postmenopausal hormone therapy affect transcriptional control of specific co-regulated gene clusters in skeletal muscle

Age

Volumn 32, Issue 3, 2010, Pages 347-363

  Pöllänen, Eija ^a   Fey, Vidal ^b   Törmäkangas, Timo ^a   Ronkainen, Paula H A ^a   Taaffe, Dennis R ^c   Takala, Timo ^d   Koskinen, Satu ^e   Cheng, Sulin ^a   Puolakka, Jukka ^f   Kujala, Urho M ^a,g   Suominen, Harri ^a   Sipilä, Sarianna ^a   Kovanen, Vuokko ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF OULU   (Finland)

^e NORWEGIAN SCHOOL OF SPORT SCIENCES   (Norway)

^f Central Finland Central Hospital   (Finland)

^g ORTON ORTHOPAEDIC HOSPITAL   (Finland)

Author keywords

Estrogen deprivation; Hormone replacement therapy; Menopause; Plyometric training; Power training; Skeletal muscle characteristics; Transcriptome wide study

Indexed keywords

AGED; ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; ENERGY METABOLISM; EXERCISE INTENSITY; FEMALE; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; HORMONAL THERAPY; HORMONE SUBSTITUTION; HUMAN; HUMAN TISSUE; INTERMETHOD COMPARISON; MICROARRAY ANALYSIS; MUSCLE BIOPSY; MUSCLE CONTRACTION; MUSCLE FUNCTION; MUSCLE STRENGTH; PHYSICAL ACTIVITY; POSTMENOPAUSE; RANDOMIZED CONTROLLED TRIAL; TRANSCRIPTION REGULATION; VASTUS LATERALIS MUSCLE;

ESTROGEN REPLACEMENT THERAPY; EXERCISE; FEMALE; HUMANS; MIDDLE AGED; MUSCLE, SKELETAL; POSTMENOPAUSE; TRANSCRIPTION, GENETIC;

EID: 77956188890     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-010-9140-1     Document Type: Article

References (74)

1. M Ashburner CA Ball JA Blake D Botstein H Butler JM Cherry AP Davis K Dolinski SS Dwight JT Eppig MA Harris DP Hill L Issel-Tarver A Kasarskis S Lewis JC Matese JE Richardson M Ringwald GM Rubin G Sherlock 2000 Gene ontology: tool for the unification of biology. The gene ontology consortium Nat Genet 25 25 29 10.1038/75556 1:CAS:528:DC%2BD3cXjtFSlsbc%3D 10802651
2. YW Chen CM Gregory MT Scarborough R Shi GA Walter K Vandenborne 2007 Transcriptional pathways associated with skeletal muscle disuse atrophy in humans Physiol Genomics 31 510 520 10.1152/physiolgenomics.00115.2006 1:CAS:528:DC%2BD2sXhtl2rt7zK 17804603
3. S Cheng S Sipilä DR Taaffe J Puolakka H Suominen 2002 Change in bone mass distribution induced by hormone replacement therapy and high-impact physical exercise in post-menopausal women Bone 31 126 135 10.1016/S8756- 3282(02)00794-9 1:CAS:528:DC%2BD38XltFWgsro%3D 12110425
4. RJ Copeland JW Bullen GW Hart 2008 Cross-talk between GlcNAcylation and phosphorylation: roles in insulin resistance and glucose toxicity Am J Physiol Endocrinol Metab 295 E17 E28 10.1152/ajpendo.90281.2008 1:CAS:528: DC%2BD1cXoslyhtLY%3D 18445751
5. A d'Albis R Couteaux JC Mira C Janmot A Roulet 1988 Myosin isoforms synthesized during regeneration of fast contraction skeletal muscle regeneration, in the presence of motor nerve and after denervation. Study in adult rats and mice Reprod Nutr Dev 28 753 756 10.1051/rnd:19880508 3187183
6. AS Dobs T Nguyen C Pace CP Roberts 2002 Differential effects of oral estrogen versus oral estrogen-androgen replacement therapy on body composition in postmenopausal women J Clin Endocrinol Metab 87 1509 1516 10.1210/jc.87.4.1509 1:CAS:528:DC%2BD38XivFKltr0%3D 11932273
7. R Edgar M Domrachev AE Lash 2002 Gene expression omnibus: NCBI gene expression and hybridization array data repository Nucleic Acids Res 30 207 210 10.1093/nar/30.1.207 1:CAS:528:DC%2BD38Xht12kurs%3D 11752295
8. L Gautier L Cope BM Bolstad RA Irizarry 2004 Affy-analysis of Affymetrix GeneChip data at the probe level Bioinformatics 20 307 315 10.1093/ bioinformatics/btg405 1:CAS:528:DC%2BD2cXht1Kksr4%3D 14960456
9. PG Giresi EJ Stevenson J Theilhaber A Koncarevic J Parkington RA Fielding SC Kandarian 2005 Identification of a molecular signature of sarcopenia Physiol Genomics 21 253 263 10.1152/physiolgenomics.00249.2004 1:CAS:528: DC%2BD2MXktVCjsL0%3D 15687482
10. E Gonzalez TE McGraw 2009 Insulin-modulated AKT subcellular localization determines AKT isoform-specific signaling Proc Natl Acad Sci USA 106 7004 7009 10.1073/pnas.0901933106 1:CAS:528:DC%2BD1MXlvFSgsbY%3D 19372382
11. BH Goodpaster DE Kelley FL Thaete J He R Ross 2000 Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content J Appl Physiol 89 104 110 1:STN:280:DC%2BD3cvgsVGnuw%3D%3D 10904041
12. LJ Greenlund KS Nair 2003 Sarcopenia-consequences, mechanisms, and potential therapies Mech Ageing Dev 124 287 299 10.1016/S0047-6374(02)00196-3 1:STN:280:DC%2BD3s7kslyqug%3D%3D 12663126
13. K Häkkinen M Alen M Kallinen RU Newton WJ Kraemer 2000 Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people Eur J Appl Physiol 83 51 62 10.1007/s004210000248 11072774
14. T Hazell K Kenno J Jakobi 2007 Functional benefit of power training for older adults J Aging Phys Act 15 349 359 17724399
15. TR Henwood S Riek DR Taaffe 2008 Strength versus muscle power-specific resistance training in community-dwelling older adults J Gerontol A Biol Sci Med Sci 63 83 91 18245765
16. B Holmes GL Dohm 2004 Regulation of GLUT4 gene expression during exercise Med Sci Sports Exerc 36 1202 1206 10.1249/01.MSS.0000132385.34889.FE 1:CAS:528:DC%2BD2cXltlOrtLs%3D 15235326
17. SS Hook AR Means 2001 Ca(2+)/CaM-dependent kinases: from activation to function Annu Rev Pharmacol Toxicol 41 471 505 10.1146/annurev.pharmtox.41.1.471 1:CAS:528:DC%2BD3MXjsVaqt74%3D 11264466
18. H Hoppeler H Howald K Conley SL Lindstedt H Claassen P Vock ER Weibel 1985 Endurance training in humans: aerobic capacity and structure of skeletal muscle J Appl Physiol 59 320 327 1:STN:280:DyaL2M3ovVOrug%3D%3D 4030584
19. Y Ikeda T Noguchi 1998 Allosteric regulation of pyruvate kinase M2 isozyme involves a cysteine residue in the intersubunit contact J Biol Chem 273 12227 12233 10.1074/jbc.273.20.12227 1:CAS:528:DyaK1cXjtlSgtrk%3D 9575171
20. M Illario S Monaco AL Cavallo I Esposito P Formisano L D'Andrea E Cipolletta B Trimarco G Fenzi G Rossi M Vitale 2009 Calcium-calmodulin-dependent kinase II (CaMKII) mediates insulin-stimulated proliferation and glucose uptake Cell Signal 21 786 792 10.1016/j.cellsig.2009.01.022 1:CAS:528: DC%2BD1MXisFWjsbo%3D 19171190
21. DA Kallman CC Plato JD Tobin 1990 The role of muscle loss in the age-related decline of grip strength: cross-sectional and longitudinal perspectives J Gerontol 45 M82 M88 1:STN:280:DyaK3c3ksVSksg%3D%3D 2335723
22. M Kanehisa S Goto M Hattori KF Aoki-Kinoshita M Itoh S Kawashima T Katayama M Araki M Hirakawa 2006 From genomics to chemical genomics: new developments in KEGG Nucleic Acids Res 34 D354 D357 10.1093/nar/gkj102 1:CAS:528:DC%2BD28XisFyitw%3D%3D 16381885
23. JA Katula WJ Rejeski AP Marsh 2008 Enhancing quality of life in older adults: a comparison of muscular strength and power training Health Qual Life Outcomes 6 45 10.1186/1477-7525-6-45 18554394
24. AM Kenny A Kleppinger Y Wang KM Prestwood 2005 Effects of ultra-low-dose estrogen therapy on muscle and physical function in older women J Am Geriatr Soc 53 1973 1977 10.1111/j.1532-5415.2005.53567.x 16274381
25. K Kuwahara T Barrientos GC Pipes S Li EN Olson 2005 Muscle-specific signaling mechanism that links actin dynamics to serum response factor Mol Cell Biol 25 3173 3181 10.1128/MCB.25.8.3173-3181.2005 1:CAS:528:DC%2BD2MXjtlSjsrg%3D 15798203
26. Lamon S, Wallace MA, Leger B, Russell AP (2009) Regulation of STARS and its downstream targets suggest a novel pathway involved in human skeletal muscle hypertrophy and atrophy. J Physiol
27. A L'honore V Rana N Arsic C Franckhauser NJ Lamb A Fernandez 2007 Identification of a new hybrid serum response factor and myocyte enhancer factor 2-binding element in MyoD enhancer required for MyoD expression during myogenesis Mol Biol Cell 18 1992 2001 10.1091/mbc.E06-09-0867 17377068
28. DJ Mahoney G Parise S Melov A Safdar MA Tarnopolsky 2005 Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise FASEB J 19 1498 1500 1:CAS:528:DC%2BD2MXpvFKhtbo%3D 15985525
29. S Marshall V Bacote RR Traxinger 1991 Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance J Biol Chem 266 4706 4712 1:CAS:528:DyaK3MXhs1WltL0%3D 2002019
30. S Melov MA Tarnopolsky K Beckman K Felkey A Hubbard 2007 Resistance exercise reverses aging in human skeletal muscle PLoS ONE 2 e465 10.1371/journal.pone.0000465 17520024
31. W Melzer A Herrmann-Frank HC Luttgau 1995 The role of Ca2+ ions in excitation-contraction coupling of skeletal muscle fibres Biochim Biophys Acta 1241 59 116 7742348
32. HD Nelson 2008 Menopause Lancet 371 760 770 10.1016/S0140-6736(08)60346-3 18313505
33. R Orr J Raymond M Fiatarone Singh 2008 Efficacy of progressive resistance training on balance performance in older adults: a systematic review of randomized controlled trials Sports Med 38 317 343 10.2165/00007256-200838040- 00004 18348591
34. FL Orsatti EA Nahas N Maesta J Nahas-Neto RC Burini 2008 Plasma hormones, muscle mass and strength in resistance-trained postmenopausal women Maturitas 59 394 404 10.1016/j.maturitas.2008.04.002 1:CAS:528:DC%2BD1cXmsFKgtLY%3D 18499368
35. DH Paterson GR Jones CL Rice 2007 Ageing and physical activity: evidence to develop exercise recommendations for older adults Can J Public Health 98 Suppl 2 S69 S108 18213941
36. SK Phillips KM Rook NC Siddle SA Bruce RC Woledge 1993 Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy Clin Sci (Lond) 84 95 98 1:STN:280: DyaK3s7mvFyqtA%3D%3D
37. E Pöllänen PH Ronkainen H Suominen T Takala S Koskinen J Puolakka S Sipilä V Kovanen 2007 Muscular transcriptome in postmenopausal women with or without hormone replacement Rejuvenation Res 10 485 500 10.1089/rej.2007.0536 17985945
38. MM Porter 2006 Power training for older adults Appl Physiol Nutr Metab 31 87 94 10.1139/H05-034 16604125
39. EL Ribom K Piehl-Aulin S Ljunghall O Ljunggren T Naessen 2002 Six months of hormone replacement therapy does not influence muscle strength in postmenopausal women Maturitas 42 225 231 10.1016/S0378-5122(02)00079-8 1:CAS:528:DC%2BD38XlvVWju7g%3D 12161047
40. S Rome K Clement R Rabasa-Lhoret E Loizon C Poitou GS Barsh JP Riou M Laville H Vidal 2003 Microarray profiling of human skeletal muscle reveals that insulin regulates approximately 800 genes during a hyperinsulinemic clamp J Biol Chem 278 18063 18068 10.1074/jbc.M300293200 1:CAS:528:DC%2BD3sXjs1Kiu74%3D 12621037
41. Ronkainen PH, Kovanen V, Alen M, Pöllänen E, Palonen EM, Ankarberg-Lindgren C, Hämäläinen E, Turpeinen U, Kujala UM, Puolakka J, Kaprio J, Sipilä S (2009) Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol
42. AJ Rose C Broholm K Kiillerich SG Finn CG Proud MH Rider EA Richter B Kiens 2005 Exercise rapidly increases eukaryotic elongation factor 2 phosphorylation in skeletal muscle of men J Physiol 569 223 228 10.1113/jphysiol.2005.097154 1:CAS:528:DC%2BD2MXhtlSmsrvO 16210351
43. Rose AJ, Richter EA (2008) Regulatory mechanisms of skeletal muscle protein turnover during exercise. J Appl Physiol
44. AJ Rose TJ Alsted TE Jensen JB Kobbero SJ Maarbjerg J Jensen EA Richter 2009 A Ca(2+)-calmodulin-eEF2K-eEF2 signalling cascade, but not AMPK, contributes to the suppression of skeletal muscle protein synthesis during contractions J Physiol 587 1547 1563 10.1113/jphysiol.2008.167528 1:CAS:528:DC%2BD1MXos1GjtL0%3D 19188248
45. SM Roth FM Ivey GF Martel JT Lemmer DE Hurlbut EL Siegel EJ Metter JL Fleg JL Fozard MC Kostek DM Wernick BF Hurley 2001 Muscle size responses to strength training in young and older men and women J Am Geriatr Soc 49 1428 1433 10.1046/j.1532-5415.2001.4911233.x 1:STN:280:DC%2BD387lslOgsw%3D%3D 11890579
46. SM Roth RE Ferrell DG Peters EJ Metter BF Hurley MA Rogers 2002 Influence of age, sex, and strength training on human muscle gene expression determined by microarray Physiol Genomics 10 181 190 1:CAS:528:DC%2BD38XnvV2mtLo%3D 12209020
47. MM Samson IB Meeuwsen A Crowe JA Dessens SA Duursma HJ Verhaar 2000 Relationships between physical performance measures, age, height and body weight in healthy adults Age Ageing 29 235 242 10.1093/ageing/29.3.235 1:STN:280:DC%2BD3M%2FhtF2gsQ%3D%3D 10855906
48. S Schmutz C Dapp M Wittwer M Vogt H Hoppeler M Fluck 2006 Endurance training modulates the muscular transcriptome response to acute exercise Pflugers Arch 451 678 687 10.1007/s00424-005-1497-0 1:CAS:528:DC%2BD28Xms1Gg 16362354
49. S Sipilä DR Taaffe S Cheng J Puolakka J Toivanen H Suominen 2001 Effects of hormone replacement therapy and high-impact physical exercise on skeletal muscle in post-menopausal women: a randomized placebo-controlled study Clin Sci (Lond) 101 147 157 10.1042/CS20000271
50. K Sjogren KC Leung W Kaplan M Gardiner-Garden J Gibney KK Ho 2007 Growth hormone regulation of metabolic gene expression in muscle: a microarray study in hypopituitary men Am J Physiol Endocrinol Metab 293 E364 E371 10.1152/ajpendo.00054.2007 1:CAS:528:DC%2BD2sXosV2mt7s%3D 17456639
51. DA Skelton SK Phillips SA Bruce CH Naylor RC Woledge 1999 Hormone replacement therapy increases isometric muscle strength of adductor pollicis in post-menopausal women Clin Sci (Lond) 96 357 364 10.1042/CS19980318 1:CAS:528:DyaK1MXislKrsr4%3D
52. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3
53. NK Stepto VG Coffey AL Carey AP Ponnampalam BJ Canny D Powell JA Hawley 2009 Global gene expression in skeletal muscle from well-trained strength and endurance athletes Med Sci Sports Exerc 41 546 565 1:CAS:528: DC%2BD1MXitFSqs74%3D 19204596
54. DR Taaffe 2006 Sarcopenia-exercise as a treatment strategy Aust Fam Physician 35 130 134 16525526
55. DR Taaffe S Sipilä S Cheng J Puolakka J Toivanen H Suominen 2005 The effect of hormone replacement therapy and/or exercise on skeletal muscle attenuation in postmenopausal women: a yearlong intervention Clin Physiol Funct Imaging 25 297 304 10.1111/j.1475-097X.2005.00628.x 1:CAS:528:DC%2BD2MXhtVGgsL3J 16117734
56. LB Tanko L Movsesyan OL Svendsen C Christiansen 2002 The effect of hormone replacement therapy on appendicular lean tissue mass in early postmenopausal women Menopause 9 117 121 10.1097/00042192-200203000-00006 11875330
57. M Teran-Garcia T Rankinen RA Koza DC Rao C Bouchard 2005 Endurance training-induced changes in insulin sensitivity and gene expression Am J Physiol Endocrinol Metab 288 E1168 E1178 10.1152/ajpendo.00467.2004 1:CAS:528:DC%2BD2MXlsVylsL8%3D 15687108
58. AE Thalacker-Mercer JC Fleet BA Craig NS Carnell WW Campbell 2007 Inadequate protein intake affects skeletal muscle transcript profiles in older humans Am J Clin Nutr 85 1344 1352 1:CAS:528:DC%2BD2sXls1Khs74%3D 17490972
59. JA Timmons O Larsson E Jansson H Fischer T Gustafsson PL Greenhaff J Ridden J Rachman M Peyrard-Janvid C Wahlestedt CJ Sundberg 2005 Human muscle gene expression responses to endurance training provide a novel perspective on Duchenne muscular dystrophy FASEB J 19 750 760 10.1096/fj.04-1980com 1:CAS:528:DC%2BD2MXktV2rtb8%3D 15857889
60. MP Walsh 1983 Calmodulin and its roles in skeletal muscle function Can Anaesth Soc J 30 390 398 10.1007/BF03007862 1:CAS:528:DyaL3sXkvVGmtrs%3D 6307499
61. A Weiss S Schiaffino LA Leinwand 1999 Comparative sequence analysis of the complete human sarcomeric myosin heavy chain family: implications for functional diversity J Mol Biol 290 61 75 10.1006/jmbi.1999.2865 1:CAS:528:DyaK1MXktV2ktb4%3D 10388558
62. S Welle AI Brooks JM Delehanty N Needler CA Thornton 2003 Gene expression profile of aging in human muscle Physiol. Genomics 14 149 159 1:CAS:528:DC%2BD3sXotFSitLk%3D 12783983
63. S Welle AI Brooks JM Delehanty N Needler K Bhatt B Shah CA Thornton 2004 Skeletal muscle gene expression profiles in 20-29 year old and 65-71 year old women Exp Gerontol 39 369 377 10.1016/j.exger.2003.11.011 1:CAS:528: DC%2BD2cXhsVOksLY%3D 15036396
64. S Welle R Tawil CA Thornton 2008 Sex-related differences in gene expression in human skeletal muscle PLoS ONE 3 e1385 10.1371/journal.pone. 0001385 18167544
65. L Wells SA Whelan GW Hart 2003 O-GlcNAc: a regulatory post-translational modification Biochem Biophys Res Commun 302 435 441 10.1016/S0006-291X(03)00175- X 1:CAS:528:DC%2BD3sXhs1Khuro%3D 12615051
66. M Wittwer R Billeter H Hoppeler M Fluck 2004 Regulatory gene expression in skeletal muscle of highly endurance-trained humans Acta Physiol Scand 180 217 227 10.1046/j.0001-6772.2003.01242.x 1:CAS:528:DC%2BD2cXhsFKqtb8%3D 14738480
67. 48th WMA General Assembly (1996) Nurenberg doctors' trial: declaration of Helsinki (1964). BMJ 313:1448-1449
68. DC Wright 2007 Mechanisms of calcium-induced mitochondrial biogenesis and GLUT4 synthesis Appl Physiol Nutr Metab 32 840 845 10.1139/H07-062 1:CAS:528:DC%2BD2sXhsVagtbnL 18059607
69. H Wu SB Kanatous FA Thurmond T Gallardo E Isotani R Bassel-Duby RS Williams 2002 Regulation of mitochondrial biogenesis in skeletal muscle by CaMK Science 296 349 352 10.1126/science.1071163 1:CAS:528:DC%2BD38XjtVWhs7w%3D 11951046
70. Z Yablonka-Reuveni AJ Rivera 1994 Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers Dev Biol 164 588 603 10.1006/dbio.1994.1226 1:CAS:528:DyaK2cXmsFagtr4%3D 7913900
71. Z Yablonka-Reuveni MA Rudnicki AJ Rivera M Primig JE Anderson P Natanson 1999 The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD Dev Biol 210 440 455 10.1006/dbio.1999. 9284 1:CAS:528:DyaK1MXjsFWnsLg%3D 10357902
72. X Yang PP Ongusaha PD Miles JC Havstad F Zhang WV So JE Kudlow RH Michell JM Olefsky SJ Field RM Evans 2008 Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance Nature 451 964 969 10.1038/nature06668 1:CAS:528:DC%2BD1cXit1yns74%3D 18288188
73. JM Zahn R Sonu H Vogel E Crane K Mazan-Mamczarz R Rabkin RW Davis KG Becker AB Owen SK Kim 2006 Transcriptional profiling of aging in human muscle reveals a common aging signature PLoS Genet 2 e115 10.1371/journal.pgen.0020115 16789832
74. AC Zambon EL McDearmon N Salomonis KM Vranizan KL Johansen D Adey JS Takahashi M Schambelan BR Conklin 2003 Time-and exercise-dependent gene regulation in human skeletal muscle Genome Biol 4 R61 10.1186/gb-2003-4-10-r61 14519196