Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly

Denisa Máderová, Patrik Krumpolec, Lucia Slobodová, Martin Schön, Veronika Tirpáková, Zuzana Kovaničová, Radka Klepochová, Matej Vajda, Stanislav Šutovský, Ján Cvečka, Ladislav Valkovič, Peter Turčáni, Martin Krššák, Milan Sedliak, Chia Liang Tsai, Barbara Ukropcová, Jozef Ukropec

Research output: Contribution to journalArticle

Abstract

Brain-derived neurotrophic factor (BDNF) participates in orchestrating the adaptive response to exercise. However, the importance of transient changes in circulating BDNF for eliciting whole-body and skeletal muscle exercise benefits in humans remains relatively unexplored. Here, we investigated effects of acute aerobic exercise and 3-month aerobic-strength training on serum, plasma and skeletal muscle BDNF in twenty-two sedentary older individuals (69.0 ± 8.0 yrs., 9 M/13F). BDNF response to acute exercise was additionally evaluated in young trained individuals (25.1 ± 2.1 yrs., 3 M/5F). Acute aerobic exercise transiently increased serum BDNF in sedentary (16%, p = .007) but not in trained elderly or young individuals. Resting serum or plasma BDNF was not regulated by exercise training in the elderly. However, subtle training-related changes of serum BDNF positively correlated with improvements in walking speed (R = 0.59, p = .005), muscle mass (R = 0.43, p = .04) and cognitive performance (R = 0.41, p = .05) and negatively with changes in body fat (R = -0.43, p = .04) and triglyceridemia (R = -0.53, p = .01). Individuals who increased muscle BDNF protein in response to 3-month training (responders) displayed stronger acute exercise-induced increase in serum BDNF than non-responders (p = .006). In addition, muscle BDNF protein content positively correlated with type II-to-type I muscle fiber ratio (R = 0.587, p = .008) and with the rate of post-exercise muscle ATP re-synthesis (R = 0.703, p = .005). Contrary to serum, acute aerobic exercise resulted in a decline of plasma BDNF 1 h post-exercise in both elderly-trained (−34%, p = .002) and young-trained individuals (−48%, p = .034). Acute circulating BDNF regulation by exercise was dependent on the level of physical fitness and correlated with training-induced improvements in metabolic and cognitive functions. Our observations provide an indirect evidence that distinct exercise-induced changes in serum and plasma BDNF as well as training-related increase in muscle BDNF protein, paralleled by improvements in muscle and whole-body clinical phenotypes, are involved in the coordinated adaptive response to exercise in humans.

Original languageEnglish
Article number101961
JournalNeuropeptides
Volume78
DOIs
Publication statusPublished - 2019 Dec

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Brain-Derived Neurotrophic Factor
Skeletal Muscle
Exercise
Serum
Muscles
Nerve Growth Factors
Slow-Twitch Muscle Fibers
Physical Fitness
Resistance Training
Cognition

All Science Journal Classification (ASJC) codes

  • Endocrinology
  • Neurology
  • Endocrine and Autonomic Systems
  • Cellular and Molecular Neuroscience

Cite this

Máderová, D., Krumpolec, P., Slobodová, L., Schön, M., Tirpáková, V., Kovaničová, Z., ... Ukropec, J. (2019). Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly. Neuropeptides, 78, [101961]. https://doi.org/10.1016/j.npep.2019.101961
Máderová, Denisa ; Krumpolec, Patrik ; Slobodová, Lucia ; Schön, Martin ; Tirpáková, Veronika ; Kovaničová, Zuzana ; Klepochová, Radka ; Vajda, Matej ; Šutovský, Stanislav ; Cvečka, Ján ; Valkovič, Ladislav ; Turčáni, Peter ; Krššák, Martin ; Sedliak, Milan ; Tsai, Chia Liang ; Ukropcová, Barbara ; Ukropec, Jozef. / Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly. In: Neuropeptides. 2019 ; Vol. 78.
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abstract = "Brain-derived neurotrophic factor (BDNF) participates in orchestrating the adaptive response to exercise. However, the importance of transient changes in circulating BDNF for eliciting whole-body and skeletal muscle exercise benefits in humans remains relatively unexplored. Here, we investigated effects of acute aerobic exercise and 3-month aerobic-strength training on serum, plasma and skeletal muscle BDNF in twenty-two sedentary older individuals (69.0 ± 8.0 yrs., 9 M/13F). BDNF response to acute exercise was additionally evaluated in young trained individuals (25.1 ± 2.1 yrs., 3 M/5F). Acute aerobic exercise transiently increased serum BDNF in sedentary (16{\%}, p = .007) but not in trained elderly or young individuals. Resting serum or plasma BDNF was not regulated by exercise training in the elderly. However, subtle training-related changes of serum BDNF positively correlated with improvements in walking speed (R = 0.59, p = .005), muscle mass (R = 0.43, p = .04) and cognitive performance (R = 0.41, p = .05) and negatively with changes in body fat (R = -0.43, p = .04) and triglyceridemia (R = -0.53, p = .01). Individuals who increased muscle BDNF protein in response to 3-month training (responders) displayed stronger acute exercise-induced increase in serum BDNF than non-responders (p = .006). In addition, muscle BDNF protein content positively correlated with type II-to-type I muscle fiber ratio (R = 0.587, p = .008) and with the rate of post-exercise muscle ATP re-synthesis (R = 0.703, p = .005). Contrary to serum, acute aerobic exercise resulted in a decline of plasma BDNF 1 h post-exercise in both elderly-trained (−34{\%}, p = .002) and young-trained individuals (−48{\%}, p = .034). Acute circulating BDNF regulation by exercise was dependent on the level of physical fitness and correlated with training-induced improvements in metabolic and cognitive functions. Our observations provide an indirect evidence that distinct exercise-induced changes in serum and plasma BDNF as well as training-related increase in muscle BDNF protein, paralleled by improvements in muscle and whole-body clinical phenotypes, are involved in the coordinated adaptive response to exercise in humans.",
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Máderová, D, Krumpolec, P, Slobodová, L, Schön, M, Tirpáková, V, Kovaničová, Z, Klepochová, R, Vajda, M, Šutovský, S, Cvečka, J, Valkovič, L, Turčáni, P, Krššák, M, Sedliak, M, Tsai, CL, Ukropcová, B & Ukropec, J 2019, 'Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly', Neuropeptides, vol. 78, 101961. https://doi.org/10.1016/j.npep.2019.101961

Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly. / Máderová, Denisa; Krumpolec, Patrik; Slobodová, Lucia; Schön, Martin; Tirpáková, Veronika; Kovaničová, Zuzana; Klepochová, Radka; Vajda, Matej; Šutovský, Stanislav; Cvečka, Ján; Valkovič, Ladislav; Turčáni, Peter; Krššák, Martin; Sedliak, Milan; Tsai, Chia Liang; Ukropcová, Barbara; Ukropec, Jozef.

In: Neuropeptides, Vol. 78, 101961, 12.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly

AU - Máderová, Denisa

AU - Krumpolec, Patrik

AU - Slobodová, Lucia

AU - Schön, Martin

AU - Tirpáková, Veronika

AU - Kovaničová, Zuzana

AU - Klepochová, Radka

AU - Vajda, Matej

AU - Šutovský, Stanislav

AU - Cvečka, Ján

AU - Valkovič, Ladislav

AU - Turčáni, Peter

AU - Krššák, Martin

AU - Sedliak, Milan

AU - Tsai, Chia Liang

AU - Ukropcová, Barbara

AU - Ukropec, Jozef

PY - 2019/12

Y1 - 2019/12

N2 - Brain-derived neurotrophic factor (BDNF) participates in orchestrating the adaptive response to exercise. However, the importance of transient changes in circulating BDNF for eliciting whole-body and skeletal muscle exercise benefits in humans remains relatively unexplored. Here, we investigated effects of acute aerobic exercise and 3-month aerobic-strength training on serum, plasma and skeletal muscle BDNF in twenty-two sedentary older individuals (69.0 ± 8.0 yrs., 9 M/13F). BDNF response to acute exercise was additionally evaluated in young trained individuals (25.1 ± 2.1 yrs., 3 M/5F). Acute aerobic exercise transiently increased serum BDNF in sedentary (16%, p = .007) but not in trained elderly or young individuals. Resting serum or plasma BDNF was not regulated by exercise training in the elderly. However, subtle training-related changes of serum BDNF positively correlated with improvements in walking speed (R = 0.59, p = .005), muscle mass (R = 0.43, p = .04) and cognitive performance (R = 0.41, p = .05) and negatively with changes in body fat (R = -0.43, p = .04) and triglyceridemia (R = -0.53, p = .01). Individuals who increased muscle BDNF protein in response to 3-month training (responders) displayed stronger acute exercise-induced increase in serum BDNF than non-responders (p = .006). In addition, muscle BDNF protein content positively correlated with type II-to-type I muscle fiber ratio (R = 0.587, p = .008) and with the rate of post-exercise muscle ATP re-synthesis (R = 0.703, p = .005). Contrary to serum, acute aerobic exercise resulted in a decline of plasma BDNF 1 h post-exercise in both elderly-trained (−34%, p = .002) and young-trained individuals (−48%, p = .034). Acute circulating BDNF regulation by exercise was dependent on the level of physical fitness and correlated with training-induced improvements in metabolic and cognitive functions. Our observations provide an indirect evidence that distinct exercise-induced changes in serum and plasma BDNF as well as training-related increase in muscle BDNF protein, paralleled by improvements in muscle and whole-body clinical phenotypes, are involved in the coordinated adaptive response to exercise in humans.

AB - Brain-derived neurotrophic factor (BDNF) participates in orchestrating the adaptive response to exercise. However, the importance of transient changes in circulating BDNF for eliciting whole-body and skeletal muscle exercise benefits in humans remains relatively unexplored. Here, we investigated effects of acute aerobic exercise and 3-month aerobic-strength training on serum, plasma and skeletal muscle BDNF in twenty-two sedentary older individuals (69.0 ± 8.0 yrs., 9 M/13F). BDNF response to acute exercise was additionally evaluated in young trained individuals (25.1 ± 2.1 yrs., 3 M/5F). Acute aerobic exercise transiently increased serum BDNF in sedentary (16%, p = .007) but not in trained elderly or young individuals. Resting serum or plasma BDNF was not regulated by exercise training in the elderly. However, subtle training-related changes of serum BDNF positively correlated with improvements in walking speed (R = 0.59, p = .005), muscle mass (R = 0.43, p = .04) and cognitive performance (R = 0.41, p = .05) and negatively with changes in body fat (R = -0.43, p = .04) and triglyceridemia (R = -0.53, p = .01). Individuals who increased muscle BDNF protein in response to 3-month training (responders) displayed stronger acute exercise-induced increase in serum BDNF than non-responders (p = .006). In addition, muscle BDNF protein content positively correlated with type II-to-type I muscle fiber ratio (R = 0.587, p = .008) and with the rate of post-exercise muscle ATP re-synthesis (R = 0.703, p = .005). Contrary to serum, acute aerobic exercise resulted in a decline of plasma BDNF 1 h post-exercise in both elderly-trained (−34%, p = .002) and young-trained individuals (−48%, p = .034). Acute circulating BDNF regulation by exercise was dependent on the level of physical fitness and correlated with training-induced improvements in metabolic and cognitive functions. Our observations provide an indirect evidence that distinct exercise-induced changes in serum and plasma BDNF as well as training-related increase in muscle BDNF protein, paralleled by improvements in muscle and whole-body clinical phenotypes, are involved in the coordinated adaptive response to exercise in humans.

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Máderová D, Krumpolec P, Slobodová L, Schön M, Tirpáková V, Kovaničová Z et al. Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly. Neuropeptides. 2019 Dec;78. 101961. https://doi.org/10.1016/j.npep.2019.101961