Stength, Endurance or Combined Training Elicit Diverse Skeletal Muscle Myosin Heavy Chain Isoform Proportion but Unaltered Androgen Receptor Concentration in Older Men

Abstract

We investigated whether the myosin heavy chain (MyHC) proportion and androgen receptor (AR) concentration in skeletal muscle differ following 21 weeks of strength, endurance and combined training in untrained older men. Strength (S) and endurance (E) groups trained twice per week and combined (S+E) group trained four times per week (two strength and two endurance). Muscle biopsies were obtained before and after the training period from m. vastus lateralis (VL) and AR mRNA and protein concentration and MyHC proportion were determined. 1RM increased during the training period in S, S+E and E but the changes were greater in S and S+E than in E. Statistically significant increases were observed only in S and S+E in maximal isometric force as well as in VL thickness. VO_2max increased significantly only in E. MyHCIIa proportion increased in S, while MyHCIIa proportion decreased and MyHCI increased (p<0.05) in E. No statistically significant changes were observed in serum testosterone and in AR mRNA or protein concentrations. The present results indicate that 21 weeks of strength, endurance or combined training changed MyHC proportion according to the training method but did not have an effect on AR mRNA or protein expression in skeletal muscle at rest.

Key words

testosterone - hypertrophy - muscle strength - gene and protein expression

References

• 1 Aunola S, Rusko H. Aerobic and anaerobic thresholds determined from venous lactate or from ventilation and gas exchange in relation to muscle fiber composition.  Int J Sports Med. 1986;  7 161-166
• 2 Bell GJ, Syrotuik D, Martin TP, Burnham R, Quinney HA. Effect of concurrent strength and endurance training on skeletal muscle properties and hormone concentrations in humans.  Eur J Appl Physiol. 2000;  81 418-427
• 3 Bottinelli R, Pellegrino MA, Canepari M, Rossi R, Reggiani C. Specific contributions of various muscle fibre types to human muscle performance: an in vitro study.  J Electromyogr Kinesiol. 1999;  9 87-95
• 4 Durnin JV, Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years.  Br J Nutr. 1974;  32 77-97
• 5 Ferrando AA, Sheffield-Moore M, Yeckel CW, Gilkison C, Jiang J, Achacosa A, Lieberman SA, Tipton K, Wolfe RR, Urban RJ. Testosterone administration to older men improves muscle function: molecular and physiological mechanisms.  Am J Physiol. 2002;  282 E601-E607
• 6 Goldspink G. Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload.  J Anat. 1999;  194 323-334
• 7 Hackney AC. Effects of endurance exercise on the reproductive system of men: the “exercise-hypogonadal male condition”.  J Endocrinol Invest. 2008;  31 932-938
• 8 Huang ZQ, Li J, Wong J. AR possesses an intrinsic hormone-independent transcriptional activity.  Mol Endocrinol. 2002;  16 924-937
• 9 Hulmi JJ, Ahtiainen JP, Selänne H, Volek JS, Häkkinen K, Kovanen V, Mero AA. Androgen receptors and testosterone in men – effects of protein ingestion, resistance exercise and fibre type.  J Steroid Biochem Mol Biol. 2008;  110 130-137
• 10 Häkkinen K, Alen M, Kraemer WJ, Gorostiaga E, Izquierdo M, Rusko H, Mikkola J, Häkkinen A, Valkeinen H, Kaarakainen E, Romu S, Erola V, Ahtiainen J, Paavolainen L. Neuromuscular adaptations during concurrent strength and endurance training versus strength training.  Eur J Appl Physiol. 2003;  89 42-52
• 11 Izquierdo M, Häkkinen K, Ibanez J, Kraemer WJ, Gorostiaga EM. Effects of combined resistance and cardiovascular training on strength, power, muscle cross-sectional area, and endurance markers in middle-aged men.  Eur J Appl Physiol. 2005;  94 70-75
• 12 Jemiolo B, Trappe S. Single muscle fiber gene expression in human skeletal muscle: validation of internal control with exercise.  Biochem Biophys Res Commun. 2004;  320 1043-1050
• 13 Kadi F, Bonnerud P, Eriksson A, Thornell LE. The expression of androgen receptors in human neck and limb muscles: effects of training and self-administration of androgenic-anabolic steroids.  Histochem Cell Biol. 2000;  113 25-29
• 14 Karavirta L, Tulppo MP, Laaksonen DE, Nyman K, Laukkanen RT, Kinnunen H, Häkkinen A, Häkkinen K. Heart rate dynamics after combined endurance and strength training in older men.  Med Sci Sports Exerc. 2009;  41 1436-1443
• 15 Korhonen MT, Cristea A, Alén M, Häkkinen K, Sipilä S, Mero A, Viitasalo JT, Larsson L, Suominen H. Aging, muscle fiber type, and contractile function in sprint-trained athletes.  J Appl Physiol. 2006;  101 906-917
• 16 Kraemer WJ, Patton JF, Gordon SE, Harman EA, Deschenes MR, Reynolds K, Newton RU, Triplett NT, Dziados JE. Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations.  J Appl Physiol. 1995;  78 976-989
• 17 Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training.  Sports Med. 2005;  35 339-361
• 18 Kraemer WJ, Spiering BA, Volek JS, Ratamess NA, Sharman MJ, Rubin MR, French DN, Silvestre R, Hatfield DL, Van Heest JL, Vingren JL, Judelson DA, Deschenes MR, Maresh CM. Androgenic responses to resistance exercise: effects of feeding and L-carnitine.  Med Sci Sports Exerc. 2006;  38 1288-1296
• 19 Kvorning T, Andersen M, Brixen K, Madsen K. Suppression of endogenous testosterone production attenuates the response to strength training: a randomized, placebo-controlled, and blinded intervention study.  Am J Physiol Endocrinol Metab. 2006;  291 E1325-1332
• 20 Lee WJ, McClung J, Hand GA, Carson JA. Overload-induced androgen receptor expression in the aged rat hindlimb receiving nandrolone decanoate.  J Appl Physiol. 2003;  94 1153-1161
• 21 Lee WJ, Thompson RW, McClung JM, Carson JA. Regulation of androgen receptor expression at the onset of functional overload in rat plantaris muscle.  Am J Physiol. 2003;  285 R1076-1085
• 22 Mahoney DJ, Carey K, Fu MH, Snow R, Cameron-Smith D, Parise G, Tarnopolsky MA. Real-time RT-PCR analysis of housekeeping genes in human skeletal muscle following acute exercise.  Physiol Genomics. 2004;  18 226-231
• 23 Marcell TJ, Harman SM, Urban RJ, Metz DD, Rodgers BD, Blackman MR. Comparison of GH, IGF-I, and testosterone with mRNA of receptors and myostatin in skeletal muscle in older men.  Am J Physiol Endocrinol Metab. 2001;  281 1159-1164
• 24 Martins KJ, Murdoch GK, Shu Y, Harris RL, Gallo M, Dixon WT, Foxcroft GR, Gordon T, Putman CT. Satellite cell ablation attenuates short-term fast-to-slow fibre type transformations in rat fast-twitch skeletal muscle.  Pflugers Arch. 2009;  458 325-335
• 25 Matsakas A, Nikolaidis MG, Kokalas N, Mougios V, Diel P. Effect of voluntary exercise on the expression of IGF-I and androgen receptor in three rat skeletal muscles and on serum IGF-I and testosterone levels.  Int J Sports Med. 2004;  25 502-508
• 26 McGuigan MR, Kraemer WJ, Deschenes MR, Gordon SE, Kitaura T, Scheett TP, Sharman MJ, Staron RS. Statistical analysis of fiber area in human skeletal muscle.  Can J Appl Physiol. 2002;  27 415-422
• 27 Nazareth LV, Weigel NL. Activation of the human androgen receptor through a protein kinase A signalling pathway.  J Biol Chem. 1996;  271 19900-19907
• 28 Putman CT, Xu X, Gillies E, MacLean IM, Bell GJ. Effects of strength, endurance and combined training on myosin heavy chain content and fibre-type distribution in humans.  Eur J Appl Physiol. 2004;  92 376-384
• 29 Rahman F, Christian HC. Non-classical actions of testosterone: an update.  Trends Endocrinol Metab. 2007;  18 371-378
• 30 Rance NE, Max SR. Modulation of the cytosolic androgen receptor in striated muscle by sex steroids.  Endocrinology. 1984;  115 862-866
• 31 Ratamess NA, Kraemer WJ, Volek JS, Maresh CM, Vanheest JL, Sharman MJ, Rubin MR, French DN, Vescovi JD, Silvestre R, Hatfield DL, Fleck SJ, Deschenes MR. Androgen receptor content following heavy resistance exercise in men.  J Steroid Biochem Mol Biol. 2005;  93 35-42
• 32 Sillanpää E, Häkkinen A, Nyman K, Mattila M, Cheng S, Karavirta L, Laaksonen DE, Huuhka N, Kraemer WJ, Häkkinen K. Body composition and fitness during strength and/or endurance training in older men.  Med Sci Sports Exerc. 2008;  40 950-958
• 33 Sillanpää E, Laaksonen DE, Häkkinen A, Karavirta L, Jensen B, Kraemer WJ, Nyman K, Häkkinen K. Body composition, fitness, and metabolic health during strength and endurance training and their combination in middle-aged and older women.  Eur J Appl Physiol. 2009;  106 285-296
• 34 Spiering BA, Kraemer WJ, Vingren JL, Ratamess NA, Anderson JM, Armstrong LE, Nindl BC, Volek JS, Häkkinen K, Maresh CM. Elevated endogenous testosterone concentrations potentiate muscle androgen receptor responses to resistance exercise.  J Steroid Biochem Mol Biol. 2009;  114 195-199
• 35 Tenover JS. Declining testicular function in aging men.  Int J Impot Res. 2003;  4 S3 S8
• 36 Vermeulen A. Andropause.  Maturitas. 2000;  34 5-15
• 37 Wheeler GD, Wall SR, Belcastro AN, Cumming DC. Reduced serum testosterone and prolactin levels in male distance runners.  JAMA. 1984;  252 514-516
• 38 Yeap BB. Testosterone and ill-health in aging men.  Nat Clin Pract Endocrinol Metab. 2009;  5 113-121

Correspondence