Sports Medicine

, Volume 47, Issue 9, pp 1709–1720

Endocrinological Roles for Testosterone in Resistance Exercise Responses and Adaptations

  • David R. Hooper
  • William J. Kraemer
  • Brian C. Focht
  • Jeff S. Volek
  • William H. DuPont
  • Lydia K. Caldwell
  • Carl M. Maresh
Review Article

Abstract

Chronic increases in testosterone levels can significantly increase hypertrophy and strength, as has been demonstrated by pharmacological intervention. However, decreases in basal testosterone levels can have the opposite result, as has been seen in hypogonadal populations. Because of these profound effects on hypertrophy and strength, testosterone has often been studied in conjunction with resistance exercise to examine whether the endocrine system plays a role in adaptations to the stimulus. Whereas some studies have demonstrated a chronic increase in basal testosterone, others have failed to find an adaptation to regular resistance exercise. However, improvements in strength and hypertrophy appear to be possible regardless of the presence of this adaptation. Testosterone has also been shown to acutely rise immediately following an acute resistance exercise bout. While this substantial mobilization of testosterone is brief, its effects are seen for several hours through the upregulation of the androgen receptor. The role of this acute response at present is unknown, but further study of the non-genomic action and possible intracrinological processes is warranted. This response does not seem to be necessary for resistance training adaptations to occur either, but whether this response optimizes such adaptations has not yet been determined.

References

  1. 1.
    American College of Sports Medicine Position Stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2009;41(3):687–708. doi:10.1249/MSS.0b013e3181915670.CrossRefGoogle Scholar
  2. 2.
    Bhasin S, Woodhouse L, Casaburi R, et al. Testosterone dose-response relationships in healthy young men. Am J Physiol Endocrinol Metab. 2001;281(6):E1172–81.PubMedGoogle Scholar
  3. 3.
    Bhasin S, Woodhouse L, Casaburi R, et al. Older men are as responsive as young men to the anabolic effects of graded doses of testosterone on the skeletal muscle. J Clin Endocrinol Metab. 2005;90(2):678–88. doi:10.1210/jc.2004-1184.CrossRefPubMedGoogle Scholar
  4. 4.
    Katagiri M, Kagawa N, Waterman MR. The role of cytochrome b5 in the biosynthesis of androgens by human P450c17. Arch Biochem Biophys. 1995;317(2):343–7. doi:10.1006/abbi.1995.1173.CrossRefPubMedGoogle Scholar
  5. 5.
    Luu-The V, Dufort I, Pelletier G, et al. Type 5 17beta-hydroxysteroid dehydrogenase: its role in the formation of androgens in women. Mol Cell Endocrinol. 2001;171(1–2):77–82 (pii: S0303-7207(00)00425-1).CrossRefPubMedGoogle Scholar
  6. 6.
    Pelletier G, Luu-The V, El-Alfy M, et al. Immunoelectron microscopic localization of 3beta-hydroxysteroid dehydrogenase and type 5 17beta-hydroxysteroid dehydrogenase in the human prostate and mammary gland. J Mol Endocrinol. 2001;26(1):11–9 (pii: JME00950).CrossRefPubMedGoogle Scholar
  7. 7.
    Labrie F. Adrenal androgens and intracrinology. Semin Reprod Med. 2004;22(4):299–309. doi:10.1055/s-2004-861547.CrossRefPubMedGoogle Scholar
  8. 8.
    Marouliss GB, Triantafillidis IK. Polycystic ovarian disease: the adrenal connection. Pediatr Endocrinol Rev. 2006;3(Suppl. 1):205–7.PubMedGoogle Scholar
  9. 9.
    Roa J, Navarro VM, Tena-Sempere M. Kisspeptins in reproductive biology: consensus knowledge and recent developments. Biol Reprod. 2011;85(4):650–60. doi:10.1095/biolreprod.111.091538.CrossRefPubMedGoogle Scholar
  10. 10.
    Garcia-Galiano D, Pinilla L, Tena-Sempere M. Sex steroids and the control of the Kiss1 system: developmental roles and major regulatory actions. J Neuroendocrinol. 2012;24(1):22–33. doi:10.1111/j.1365-2826.2011.02230.x.CrossRefPubMedGoogle Scholar
  11. 11.
    Smith JT. Sex steroid regulation of kisspeptin circuits. Adv Exp Med Biol. 2013;784:275–95. doi:10.1007/978-1-4614-6199-9_13.CrossRefPubMedGoogle Scholar
  12. 12.
    Volek JS, Gomez AL, Love DM, et al. Effects of a high-fat diet on postabsorptive and postprandial testosterone responses to a fat-rich meal. Metabolism. 2001;50(11):1351–5 (pii: S0026049501565464).CrossRefPubMedGoogle Scholar
  13. 13.
    Hjalmarsen A, Aasebo U, Aakvaag A, et al. Sex hormone responses in healthy men and male patients with chronic obstructive pulmonary disease during an oral glucose load. Scand J Clin Lab Investig. 1996;56(7):635–40.CrossRefGoogle Scholar
  14. 14.
    Kraemer WJ, Spiering BA, Volek JS, et al. Androgenic responses to resistance exercise: effects of feeding and l-carnitine. Med Sci Sports Exerc. 2006;38(7):1288–96. doi:10.1249/01.mss.0000227314.85728.35.CrossRefPubMedGoogle Scholar
  15. 15.
    Hackney AC. Effects of endurance exercise on the reproductive system of men: the “exercise-hypogonadal male condition”. J Endocrinol Invest. 2008;31(10):932–8 (pii: 5022).CrossRefPubMedGoogle Scholar
  16. 16.
    Arver S, Lehtihet M. Current guidelines for the diagnosis of testosterone deficiency. Front Horm Res. 2009;37:5–20. doi:10.1159/000175839175839.CrossRefPubMedGoogle Scholar
  17. 17.
    American College of Sports Medicine. Position statement on the use and abuse of anabolic-androgenic steroids in sports. Med Sci Sports. 1977;9(4):xi–xii.Google Scholar
  18. 18.
    American College of Sports Medicine. Position stand on the use of anabolic-androgenic steroids in sports. Med Sci Sports Exerc. 1987;19(5):534–9.Google Scholar
  19. 19.
    Hoffman JR, Kraemer WJ, Bhasin S, et al. Position stand on androgen and human growth hormone use. J Strength Cond Res. 2009;23(5 Suppl):S1–59. doi:10.1519/JSC.0b013e31819df2e6.CrossRefPubMedGoogle Scholar
  20. 20.
    Kvorning T, Andersen M, Brixen K, et al. 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(6):E1325–32. doi:10.1152/ajpendo.00143.2006.CrossRefPubMedGoogle Scholar
  21. 21.
    Kvorning T, Kadi F, Schjerling P, et al. The activity of satellite cells and myonuclei following 8 weeks of strength training in young men with suppressed testosterone levels. Acta Physiol Scand. 2015;213(3):676–87. doi:10.1111/apha.12404.CrossRefGoogle Scholar
  22. 22.
    Harman SM, Metter EJ, Tobin JD, et al. Longitudinal effects of aging on serum total and free testosterone levels in healthy men: Baltimore longitudinal study of aging. J Clin Endocrinol Metab. 2001;86(2):724–31. doi:10.1210/jcem.86.2.7219.CrossRefPubMedGoogle Scholar
  23. 23.
    Katznelson L, Rosenthal DI, Rosol MS, et al. Using quantitative CT to assess adipose distribution in adult men with acquired hypogonadism. AJR Am J Roentgenol. 1998;170(2):423–7. doi:10.2214/ajr.170.2.9456958.CrossRefPubMedGoogle Scholar
  24. 24.
    Staron RS, Karapondo DL, Kraemer WJ, et al. Skeletal muscle adaptations during early phase of heavy-resistance training in men and women. J Appl Physiol (1985). 1994;76(3):1247–55.Google Scholar
  25. 25.
    Hakkinen K, Pakarinen A, Alen M, et al. Neuromuscular and hormonal adaptations in athletes to strength training in two years. J Appl Physiol (1985). 1988;65(6):2406–12.Google Scholar
  26. 26.
    Kraemer WJ, Patton JF, Gordon SE, et al. Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J Appl Physiol. 1995;78(3):976–89.PubMedGoogle Scholar
  27. 27.
    Ahtiainen JP, Nyman K, Huhtaniemi I, et al. Effects of resistance training on testosterone metabolism in younger and older men. Exp Gerontol. 2015;69:148–58. doi:10.1016/j.exger.2015.06.010.CrossRefPubMedGoogle Scholar
  28. 28.
    Fahey TD, Rolph R, Moungmee P, et al. Serum testosterone, body composition, and strength of young adults. Med Sci Sports. 1976;8(1):31–4.PubMedGoogle Scholar
  29. 29.
    Kraemer WJ, Fry AC, Warren BJ, et al. Acute hormonal responses in elite junior weightlifters. Int J Sports Med. 1992;13(2):103–9. doi:10.1055/s-2007-1021240.CrossRefPubMedGoogle Scholar
  30. 30.
    Vingren JL, Kraemer WJ, Ratamess NA, et al. Testosterone physiology in resistance exercise and training: the up-stream regulatory elements. Sports Med. 2010;40(12):1037–53. doi:10.2165/11536910-000000000-000004.CrossRefPubMedGoogle Scholar
  31. 31.
    Goto K, Ishii N, Kizuka T, et al. Hormonal and metabolic responses to slow movement resistance exercise with different durations of concentric and eccentric actions. Eur J Appl Physiol. 2009;106(5):731–9. doi:10.1007/s00421-009-1075-9.CrossRefPubMedGoogle Scholar
  32. 32.
    Linnamo V, Pakarinen A, Komi PV, et al. Acute hormonal responses to submaximal and maximal heavy resistance and explosive exercises in men and women. J Strength Cond Res. 2005;19(3):566–71. doi:10.1519/R-15404.1.PubMedGoogle Scholar
  33. 33.
    West DW, Burd NA, Churchward-Venne TA, et al. Sex-based comparisons of myofibrillar protein synthesis after resistance exercise in the fed state. J Appl Physiol (1985). 2012;112(11):1805–13. doi:10.1152/japplphysiol.00170.2012.CrossRefGoogle Scholar
  34. 34.
    Kraemer WJ, Hakkinen K, Newton RU, et al. Acute hormonal responses to heavy resistance exercise in younger and older men. Eur J Appl Physiol Occup Physiol. 1998;77(3):206–11.CrossRefPubMedGoogle Scholar
  35. 35.
    Evans NA. Gym and tonic: a profile of 100 male steroid users. Br J Sports Med. 1997;31(1):54–8.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Kraemer WJ, Gordon SE, Fleck SJ, et al. Endogenous anabolic hormonal and growth factor responses to heavy resistance exercise in males and females. Int J Sports Med. 1991;12(2):228–35. doi:10.1055/s-2007-1024673.CrossRefPubMedGoogle Scholar
  37. 37.
    Spiering BA, Kraemer WJ, Vingren JL, et al. Elevated endogenous testosterone concentrations potentiate muscle androgen receptor responses to resistance exercise. J Steroid Biochem Mol Biol. 2009;114(3–5):195–9. doi:10.1016/j.jsbmb.2009.02.005.CrossRefPubMedGoogle Scholar
  38. 38.
    Ratamess NA, Kraemer WJ, Volek JS, et al. Androgen receptor content following heavy resistance exercise in men. J Steroid Biochem Mol Biol. 2005;93(1):35–42. doi:10.1016/j.jsbmb.2004.10.019.CrossRefPubMedGoogle Scholar
  39. 39.
    Biolo G, Maggi SP, Williams BD, et al. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol. 1995;268(3 Pt 1):E514–20.PubMedGoogle Scholar
  40. 40.
    Schoenfeld BJ. Postexercise hypertrophic adaptations: a reexamination of the hormone hypothesis and its applicability to resistance training program design. J Strength Cond Res. 2013;27(6):1720–30. doi:10.1519/JSC.0b013e31828ddd53.CrossRefPubMedGoogle Scholar
  41. 41.
    Smilios I, Pilianidis T, Karamouzis M, et al. Hormonal responses after various resistance exercise protocols. Med Sci Sports Exerc. 2003;35(4):644–54. doi:10.1249/01.MSS.0000058366.04460.5F.CrossRefPubMedGoogle Scholar
  42. 42.
    Mitchell CJ, Churchward-Venne TA, West DW, et al. Resistance exercise load does not determine training-mediated hypertrophic gains in young men. J Appl Physiol (1985). 2012;113(1):71–7. doi:10.1152/japplphysiol.00307.2012.CrossRefPubMedCentralGoogle Scholar
  43. 43.
    Campos GE, Luecke TJ, Wendeln HK, et al. Muscular adaptations in response to three different resistance-training regimens: specificity of repetition maximum training zones. Eur J Appl Physiol. 2002;88(1–2):50–60. doi:10.1007/s00421-002-0681-6.CrossRefPubMedGoogle Scholar
  44. 44.
    Camera DM, Edge J, Short MJ, et al. Early time course of Akt phosphorylation after endurance and resistance exercise. Med Sci Sports Exerc. 2010;42(10):1843–52. doi:10.1249/MSS.0b013e3181d964e4.CrossRefPubMedGoogle Scholar
  45. 45.
    Vissing K, McGee S, Farup J, et al. Differentiated mTOR but not AMPK signaling after strength vs endurance exercise in training-accustomed individuals. Scand J Med Sci Sports. 2013;23(3):355–66.CrossRefPubMedGoogle Scholar
  46. 46.
    Fry AC. The role of resistance exercise intensity on muscle fibre adaptations. Sports Med. 2004;34(10):663–79.CrossRefPubMedGoogle Scholar
  47. 47.
    Morton RW, Oikawa SY, Wavell CG, et al. Neither load nor systemic hormones determine resistance training-mediated hypertrophy or strength gains in resistance-trained young men. J Appl Physiol (1985). 2016;121(1):129–38. doi:10.1152/japplphysiol.00154.2016.CrossRefGoogle Scholar
  48. 48.
    Smith GI, Reeds DN, Hall AM, et al. Sexually dimorphic effect of aging on skeletal muscle protein synthesis. Biol Sex Differ. 2012;3(1):11. doi:10.1186/2042-6410-3-11.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Coffey VG, Shield A, Canny BJ, et al. Interaction of contractile activity and training history on mRNA abundance in skeletal muscle from trained athletes. J Clin Endocrinol Metab. 2006;290(5):E849–55. doi:10.1152/ajpendo.00299.2005.Google Scholar
  50. 50.
    Timmons JA. Variability in training-induced skeletal muscle adaptation. J Appl Physiol (1985). 2011;110(3):846–53. doi:10.1152/japplphysiol.00934.2010.CrossRefGoogle Scholar
  51. 51.
    Mitchell CJ, Churchward-Venne TA, Parise G, et al. Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PLoS One. 2014;9(2):e89431. doi:10.1371/journal.pone.0089431.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Diver MJ. Laboratory measurement of testosterone. Front Horm Res. 2009;37:21–31. doi:10.1159/000175841175841.CrossRefPubMedGoogle Scholar
  53. 53.
    Mendel CM. The free hormone hypothesis: a physiologically based mathematical model. Endocr Rev. 1989;10(3):232–74.CrossRefPubMedGoogle Scholar
  54. 54.
    Beato M, Klug J. Steroid hormone receptors: an update. Hum Reprod Update. 2000;6(3):225–36.CrossRefPubMedGoogle Scholar
  55. 55.
    Pratt WB, Toft DO. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev. 1997;18(3):306–60.PubMedGoogle Scholar
  56. 56.
    Grino PB, Griffin JE, Wilson JD. Testosterone at high concentrations interacts with the human androgen receptor similarly to dihydrotestosterone. Endocrinology. 1990;126(2):1165–72.CrossRefPubMedGoogle Scholar
  57. 57.
    Brinkmann AO. Molecular mechanisms of androgen action: a historical perspective. Methods Mol Biol. 2011;776:3–24. doi:10.1007/978-1-61779-243-4_1.CrossRefPubMedGoogle Scholar
  58. 58.
    Michels G, Hoppe UC. Rapid actions of androgens. Front Neuroendocrinol. 2008;29(2):182–98. doi:10.1016/j.yfrne.2007.08.004.CrossRefPubMedGoogle Scholar
  59. 59.
    Norman AW, Mizwicki MT, Norman DP. Steroid-hormone rapid actions, membrane receptors and a conformational ensemble model. Nat Rev Drug Discov. 2004;3(1):27–41. doi:10.1038/nrd1283nrd1283.CrossRefPubMedGoogle Scholar
  60. 60.
    Gottlicher M, Heck S, Herrlich P. Transcriptional cross-talk, the second mode of steroid hormone receptor action. J Mol Med (Berl). 1998;76(7):480–9.CrossRefGoogle Scholar
  61. 61.
    Estrada M, Espinosa A, Muller M, et al. Testosterone stimulates intracellular calcium release and mitogen-activated protein kinases via a G protein-coupled receptor in skeletal muscle cells. Endocrinology. 2003;144(8):3586–97.CrossRefPubMedGoogle Scholar
  62. 62.
    Labrie F. Intracrinology. Mol Cell Endocrinol. 1991;78(3):C113–8 (pii: 0303-7207(91)90116-A).CrossRefPubMedGoogle Scholar
  63. 63.
    Luu-The V, Labrie F. The intracrine sex steroid biosynthesis pathways. Prog Brain Res. 2010;181:177–92. doi:10.1016/S0079-6123(08)81010-2.CrossRefPubMedGoogle Scholar
  64. 64.
    Vingren JL, Kraemer WJ, Hatfield DL, et al. Effect of resistance exercise on muscle steroidogenesis. J Appl Physiol (1985). 2008;105(6):1754–60. doi:10.1152/japplphysiol.91235.2008.CrossRefGoogle Scholar
  65. 65.
    Biolo G, Tipton KD, Klein S, et al. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol. 1997;273(1 Pt 1):E122–9.PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • David R. Hooper
    • 1
    • 2
  • William J. Kraemer
    • 1
  • Brian C. Focht
    • 1
  • Jeff S. Volek
    • 1
  • William H. DuPont
    • 1
  • Lydia K. Caldwell
    • 1
  • Carl M. Maresh
    • 1
  1. 1.Department of Human SciencesThe Ohio State UniversityColumbusUSA
  2. 2.Department of Health SciencesArmstrong State UniversitySavannahUSA

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