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Effects of upper-body, lower-body, or combined resistance training on the ratio of follistatin and myostatin in middle-aged men

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Abstract

Purpose

Due to the mechanistic role of myostatin and follistatin in modulating muscle mass, shifts in the follistatin to myostatin ratio (F:M) may help explain changes in muscular size in response to resistance training (RT). The present study examined whether differential responses in follistatin and myostatin occur based on the amount of active musculature in a RT program in middle-aged men.

Methods

Forty middle-aged men (age = 46.5 ± 3.1 years) were randomly assigned to 1 of 4 groups, upper-body RT (UB; n = 10), lower-body RT (LB; n = 10), combined RT (UB + LB; n = 10) or control (C; n = 10). The training protocol consisted of three exercise sessions per week for 8 weeks. Blood samples were obtained at baseline and 48 h after the final session of the training program.

Results

Muscle mass significantly increased (p < 0.05) following UB = 0.76 ± 0.46 kg, LB = 0.90 ± 0.29 kg, UB + LB = 1.38 ± 0.70 kg, compared to no changes after control. Serum follistatin increased in the LB = 0.24 ± 0.06 ng mL−1, UB = 0.27 ± 0.17 ng mL−1, UB + LB = 0.50 ± 0.18 ng mL−1, while serum myostatin decreased in the LB = − 0.11 ± 0.08 ng mL−1 and UB + LB = − 0.34 ± 0.23 ng mL−1, but not UB = 0.07 ± 0.16 ng mL−1. Further, change in concentration following training was larger between UB + LB and either LB or UB alone for both follistatin and myostatin.

Conclusions

Both UB and LB increase muscle mass and alter the F: M ratio; however, the change in these endocrine markers is approximately twice as large if UB and LB is combined. The endocrine response to RT of myostatin and follistatin may depend on the volume of muscle mass activated during training.

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Abbreviations

RT:

Resistance training

F:M:

Follistatin to myostatin ratio

SkMM:

Skeletal muscle mass

PBF:

Percent body fat

BMI:

Body mass index

LBM:

Lean body mass

FM:

Fat mass

1RM:

One repetition maximum

ng mL−1 :

Nanograms per milliliter

UB:

Upper body

LB:

Lower body

UB + LB:

Upper body + lower body

mL:

Milliliter

ANOVA:

Analysis of variance

vs:

Versus

IGF-1:

Insulin-like growth factor 1

References

  • Allen DL, Hittel DS, McPherron AC (2011) Expression and function of myostatin in obesity, diabetes, and exercise adaptation. Med Sci Sports Exerc 43:1828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, Patel K (2004) Follistatin complexes myostatin and antagonises myostatin-mediated inhibition of myogenesis. Dev Biol 270:19–30

    Article  CAS  PubMed  Google Scholar 

  • Attarzadeh Hosseini SR, Moeinnia N, Motahari Rad M (2017) The effect of two intensities resistance training on muscle growth regulatory myokines in sedentary young women. Obes Med 2:25–28

    Article  Google Scholar 

  • Barrios-Silva LV et al (2018) Activin subfamily peptides predict chronological age in humans. Physiol Rep 6:e13823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burd NA et al (2010) Resistance exercise volume affects myofibrillar protein synthesis and anabolic signalling molecule phosphorylation in young men. J Physiol 588:3119–3130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Church DD et al (2016) Comparison of high-intensity vs. high-volume resistance training on the BDNF response to exercise. J Appl Physiol 121:123–128

    Article  PubMed  Google Scholar 

  • de Souza EO et al (2014) Effects of concurrent strength and endurance training on genes related to myostatin signaling pathway and muscle fiber responses. J Strength Cond Res 28:3215–3223

    Article  PubMed  Google Scholar 

  • Deng B et al (2017) The function of myostatin in the regulation of fat mass in mammals. Nutr Metab 14:29

    Article  Google Scholar 

  • Elliott B, Renshaw D, Getting S, Mackenzie R (2012) The central role of myostatin in skeletal muscle and whole body homeostasis. Acta Physiol 205:324–340

    Article  CAS  Google Scholar 

  • Elliott BT, Herbert P, Sculthorpe N, Grace FM, Stratton D, Hayes LD (2017) Lifelong exercise, but not short-term high-intensity interval training, increases GDF11, a marker of successful aging: a preliminary investigation. Physiol Rep 5:e13343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frontera WR, Meredith CN, O’Reilly KP, Knuttgen HG, Evans WJ (1988) Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 64:1038–1044

    Article  CAS  PubMed  Google Scholar 

  • Gilson H, Schakman O, Kalista S, Lause P, Tsuchida K, Thissen J-P (2009) Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin. Am J Physiol Endocrinol Metab 297:E157–E164

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Cadavid NF et al (1998) Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting. Proc Natl Acad Sci 95:14938–14943

    Article  CAS  PubMed  Google Scholar 

  • Görgens SW, Raschke S, Holven KB, Jensen J, Eckardt K, Eckel J (2013) Regulation of follistatin-like protein 1 expression and secretion in primary human skeletal muscle cells. Arch Physiol Biochem 119:75–80

    Article  CAS  PubMed  Google Scholar 

  • Goto K, Nagasawa M, Yanagisawa O, Kizuka T, Ishii N, Takamatsu K (2004) Muscular adaptations to combinations of high-and low-intensity resistance exercises. J Strength Cond Res 18:730–737

    PubMed  Google Scholar 

  • Gotshalk LA et al (1997) Hormonal responses of multiset versus single-set heavy-resistance exercise protocols. Can J Appl Physiol 22:244–255

    Article  CAS  PubMed  Google Scholar 

  • Grgic J, Mcllvenna LC, Fyfe JJ, Sabol F, Bishop DJ, Schoenfeld BJ, Pedisic Z (2018) Does aerobic training promote the same skeletal muscle hypertrophy as resistance training? A systematic review and meta-analysis. Sports Med 49:1–22

    Google Scholar 

  • Guo T, Jou W, Chanturiya T, Portas J, Gavrilova O, McPherron AC (2009) Myostatin inhibition in muscle, but not adipose tissue, decreases fat mass and improves insulin sensitivity. PLoS One 4:e4937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haff GG, Triplett NT (2015) Essentials of strength training and conditioning, 4th edn. Human kinetics

  • Hakkinen K, Pakarinen A, Kraemer WJ, Newton RU, Alen M (2000) Basal concentrations and acute responses of serum hormones and strength development during heavy resistance training in middle-aged and elderly men and women. J Gerontol Biol Sci Med Sci 55:B95

    Article  CAS  Google Scholar 

  • Hofmann M et al (2016) Effects of elastic band resistance training and nutritional supplementation on muscle quality and circulating muscle growth and degradation factors of institutionalized elderly women: the Vienna Active Ageing Study (VAAS). Eur J Appl Physiol 116:885–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hulmi JJ et al (2007) Postexercise myostatin and activin IIb mRNA levels: effects of strength training. Med Sci Sports Exerc 39:289–297

    Article  CAS  PubMed  Google Scholar 

  • Jang KS, Kang S, Woo SH, Bae JY, Shin KO (2016) Effects of combined open kinetic chain and closed kinetic chain training using pulley exercise machines on muscle strength and angiogenesis factors. J Phys Ther Sci 28:960–966

    Article  PubMed  PubMed Central  Google Scholar 

  • Krieger JW (2010) Single vs. multiple sets of resistance exercise for muscle hypertrophy: a meta-analysis. J Strength Cond Res 24:1150–1159

    Article  PubMed  Google Scholar 

  • Laurentino GC et al (2012) Strength training with blood flow restriction diminishes myostatin gene expression. Med Sci Sports Exerc 44:406–412

    Article  CAS  PubMed  Google Scholar 

  • Law TD, Clark LA, Clark BC (2016) Resistance exercise to prevent and manage sarcopenia and dynapenia. Ann Rev Gerontol Geriatr 36:205

    Article  Google Scholar 

  • Medicine ACoS (2009) American College of Sports Medicine position stand Progression models in resistance training for healthy adults. Med Sci Sports Exerc 41:687

    Article  Google Scholar 

  • Motevalli MS, Dalbo VJ, Attarzadeh RS, Rashidlamir A, Tucker PS, Scanlan AT (2015) The effect of rate of weight reduction on serum myostatin and follistatin concentrations in competitive wrestlers. Int J Sports Physiol Perform 10:139–146

    Article  PubMed  Google Scholar 

  • Murach KA, Bagley JR (2016) Skeletal muscle hypertrophy with concurrent exercise training: contrary evidence for an interference effect. Sports Med 46:1029–1039

    Article  PubMed  Google Scholar 

  • Negaresh R, Ranjbar R, Habibi A, Mokhtarzade M, Fokin A, Gharibvand M (2017) The effect of resistance training on quadriceps muscle volume and some growth factors in elderly and young men. Adv Gerontol Uspekhi Gerontol 30:880–887

    CAS  Google Scholar 

  • Ratkevicius A et al (2011) Serum concentrations of myostatin and myostatin-interacting proteins do not differ between young and sarcopenic elderly men. J Gerontol Ser A Biomed Sci Med Sci 66:620–626

    Article  CAS  Google Scholar 

  • Roberts HC, Denison HJ, Martin HJ, Patel HP, Syddall H, Cooper C, Sayer AA (2011) A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing 40:423–429

    Article  PubMed  Google Scholar 

  • Rodgers BD, Garikipati DK (2008) Clinical, agricultural, and evolutionary biology of myostatin: a comparative review. Endocr Rev 29:513–534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodino-Klapac LR, Haidet AM, Kota J, Handy C, Kaspar BK, Mendell JR (2009) Inhibition of myostatin with emphasis on follistatin as a therapy for muscle disease. Muscle Nerve 39:283–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roth SM, Martel GF, Ferrell RE, Metter EJ, Hurley BF, Rogers MA (2003) Myostatin gene expression is reduced in humans with heavy-resistance strength training: a brief communication. Exp Biol Med 228:706–709

    Article  CAS  Google Scholar 

  • Saremi A, Gharakhanloo R, Sharghi S, Gharaati M, Larijani B, Omidfar K (2010) Effects of oral creatine and resistance training on serum myostatin and GASP-1. Mol Cell Endocrinol 317:25–30

    Article  CAS  PubMed  Google Scholar 

  • Schiffer T, Geisler S, Sperlich B, Strüder H (2011) MSTN mRNA after varying exercise modalities in humans. Int J Sports Med 32:683–687

    Article  CAS  PubMed  Google Scholar 

  • Schoenfeld BJ, Ogborn D, Krieger JW (2016) Effects of resistance training frequency on measures of muscle hypertrophy: a systematic review and meta-analysis. Sports Med 46:1689–1697

    Article  PubMed  Google Scholar 

  • Simão R et al (2013) Influence of upper-body exercise order on hormonal responses in trained men. Appl Physiol Nutr Metab 38:177–181

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi Y (1997) Lateral specificity in resistance training: the effect of bilateral and unilateral training. Eur J Appl Physiol 75:144–150

    Article  CAS  Google Scholar 

  • Taniguchi Y (1998) Relationship between the modifications of bilateral deficit in upper and lower limbs by resistance training in humans. Eur J Appl Physiol 78:226–230

    Article  CAS  Google Scholar 

  • Terzis G, Spengos K, Mascher H, Georgiadis G, Manta P, Blomstrand E (2010) The degree of p70S6 k and S6 phosphorylation in human skeletal muscle in response to resistance exercise depends on the training volume. Eur J Appl Physiol 110:835–843

    Article  CAS  PubMed  Google Scholar 

  • Thomas DT, Erdman KA, Burke LM (2016) Position of the Academy of Nutrition and Dietetics, Dietitians of Canada, and the American College of Sports Medicine: nutrition and athletic performance. J Acad Nutr Diet 116:501–528

    Article  PubMed  Google Scholar 

  • Tortoriello DV, Sidis Y, Holtzman DA, Holmes WE, Schneyer AL (2001) Human follistatin-related protein: a structural homologue of follistatin with nuclear localization. Endocrinology 142:3426–3434

    Article  CAS  PubMed  Google Scholar 

  • Viitasalo J, Era P, Leskinen A-L, Heikkinen E (1985) Muscular strength profiles and anthropometry in random samples of men aged 31–35, 51–55 and 71–75 years. Ergonomics 28:1563–1574

    Article  Google Scholar 

  • Walker KS, Kambadur R, Sharma M, Smith HK (2004) Resistance training alters plasma myostatin but not IGF-1 in healthy men. Med Sci Sports Exerc 36:787–793

    Article  CAS  PubMed  Google Scholar 

  • Willoughby DS (2004) Effects of an alleged myostatin-binding supplement and heavy resistance training on serum myostatin, muscle strength and mass, and body composition. Int J Sport Nutr Exerc Metab 14:461–472

    Article  CAS  PubMed  Google Scholar 

  • Yarasheski K, Bhasin S, Sinha-Hikim I, Pak-Loduca J, Gonzalez-Cadavid N (2002) Serum myostatin-immunoreactive protein is increased in 60–92 year old women and men with muscle wasting. J Nutr Health Ageing 6:343–348

    CAS  Google Scholar 

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Acknowledgements

The authors wish to thank all the participants in this research project.

Author information

Authors and Affiliations

  1. Department of Exercise Physiology, Ferdowsi University of Mashhad, Mashhad, Iran

    Reza Bagheri, Amir Rashidlamir & Mohamad S. Motevalli

  2. Translational Physiology Research Group, School of Life Sciences, University of Westminster, London, UK

    Bradley T. Elliott

  3. Deparment of Exercise Physiology, University of Guilan, Rasht, Iran

    Javad Mehrabani

  4. Department of Health and Human Performance, Marymount University, Arlington, VA, USA

    Alexei Wong

Authors
  1. Reza Bagheri
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  2. Amir Rashidlamir
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  3. Mohamad S. Motevalli
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  4. Bradley T. Elliott
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  5. Javad Mehrabani
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  6. Alexei Wong
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Contributions

AR conceived and designed research. RB conducted the experiments and wrote the paper. AW and JM fixed grammatical mistakes. In addition, AW analyzed data, contributed in writing the paper and preparing revisions. MSM analyzed the nutrition data. BTE analyzed the other data, wrote the result sections and fixed all the section of the paper academically. Finally, all the authors read and approved the manuscript.

Corresponding author

Correspondence to Amir Rashidlamir.

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The authors declare no conflict of interest.

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Communicated by William J. Kraemer.

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Bagheri, R., Rashidlamir, A., Motevalli, M.S. et al. Effects of upper-body, lower-body, or combined resistance training on the ratio of follistatin and myostatin in middle-aged men. Eur J Appl Physiol 119, 1921–1931 (2019). https://doi.org/10.1007/s00421-019-04180-z

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