Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise

Benjamin F. Miller, Jens L. Olesen, Mette Hansen, Simon Dossing, Regina M. Crameri, Rasmus J. Welling, Henning Langberg, Allan Flyvbjerg, Michael Kjaer*, John A. Babraj, Kenneth Smith, Michael J. Rennie

*Corresponding author for this work

Research output: Contribution to journalArticle

345 Citations (Scopus)

Abstract

We hypothesized that an acute bout of strenuous, non-damaging exercise would increase rates of protein synthesis of collagen in tendon and skeletal muscle but these would be less than those of muscle myofibrillar and sarcoplasmic proteins. Two groups (n = 8 and 6) of healthy young men were studied over 72 h after 1 h of one-legged kicking exercise at 67% of maximum workload (Wmax). To label tissue proteins in muscle and tendon primed, constant infusions of [1-13C]leucine or [1-13C]valine and flooding doses of [15N] or [13C]proline were given intravenously, with estimation of labelling in target proteins by gas chromatography-mass spectrometry. Patellar tendon and quadriceps biopsies were taken in exercised and rested legs at 6, 24, 42 or 48 and 72 h after exercise. The fractional synthetic rates of all proteins were elevated at 6 h and rose rapidly to peak at 24 h post exercise (tendon collagen (0.077% h-1), muscle collagen (0.054% h-1), myofibrillar protein (0.121% h-1), and sarcoplasmic protein (0.134% h-1)). The rates decreased toward basal values by 72 h although rates of tendon collagen and myofibrillar protein synthesis remained elevated. There was no tissue damage of muscle visible on histological evaluation. Neither tissue microdialysate nor serum concentrations of IGF-I and IGF binding proteins (IGFBP-3 and IGFBP-4) or procollagen type I N-terminal propeptide changed from resting values. Thus, there is a rapid increase in collagen synthesis after strenuous exercise in human tendon and muscle. The similar time course of changes of protein synthetic rates in different cell types supports the idea of coordinated musculotendinous adaptation.
Original languageEnglish
Pages (from-to)1021-1033
Number of pages13
JournalJournal of Physiology
Volume567
Issue number3
DOIs
Publication statusPublished - 12 Sep 2005
Externally publishedYes

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Patellar Ligament
Muscle Proteins
Quadriceps Muscle
Collagen
Exercise
Tendons
Proteins
Muscles
Insulin-Like Growth Factor Binding Protein 3
Insulin-Like Growth Factor Binding Protein 4
Valine
Collagen Type I
Workload
Insulin-Like Growth Factor I
Proline
Leucine
Gas Chromatography-Mass Spectrometry
Leg
Skeletal Muscle
Biopsy

Cite this

Miller, B. F., Olesen, J. L., Hansen, M., Dossing, S., Crameri, R. M., Welling, R. J., ... Rennie, M. J. (2005). Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. Journal of Physiology, 567(3), 1021-1033. https://doi.org/10.1113/jphysiol.2005.093690
Miller, Benjamin F. ; Olesen, Jens L. ; Hansen, Mette ; Dossing, Simon ; Crameri, Regina M. ; Welling, Rasmus J. ; Langberg, Henning ; Flyvbjerg, Allan ; Kjaer, Michael ; Babraj, John A. ; Smith, Kenneth ; Rennie, Michael J. / Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. In: Journal of Physiology. 2005 ; Vol. 567, No. 3. pp. 1021-1033.
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abstract = "We hypothesized that an acute bout of strenuous, non-damaging exercise would increase rates of protein synthesis of collagen in tendon and skeletal muscle but these would be less than those of muscle myofibrillar and sarcoplasmic proteins. Two groups (n = 8 and 6) of healthy young men were studied over 72 h after 1 h of one-legged kicking exercise at 67{\%} of maximum workload (Wmax). To label tissue proteins in muscle and tendon primed, constant infusions of [1-13C]leucine or [1-13C]valine and flooding doses of [15N] or [13C]proline were given intravenously, with estimation of labelling in target proteins by gas chromatography-mass spectrometry. Patellar tendon and quadriceps biopsies were taken in exercised and rested legs at 6, 24, 42 or 48 and 72 h after exercise. The fractional synthetic rates of all proteins were elevated at 6 h and rose rapidly to peak at 24 h post exercise (tendon collagen (0.077{\%} h-1), muscle collagen (0.054{\%} h-1), myofibrillar protein (0.121{\%} h-1), and sarcoplasmic protein (0.134{\%} h-1)). The rates decreased toward basal values by 72 h although rates of tendon collagen and myofibrillar protein synthesis remained elevated. There was no tissue damage of muscle visible on histological evaluation. Neither tissue microdialysate nor serum concentrations of IGF-I and IGF binding proteins (IGFBP-3 and IGFBP-4) or procollagen type I N-terminal propeptide changed from resting values. Thus, there is a rapid increase in collagen synthesis after strenuous exercise in human tendon and muscle. The similar time course of changes of protein synthetic rates in different cell types supports the idea of coordinated musculotendinous adaptation.",
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Miller, BF, Olesen, JL, Hansen, M, Dossing, S, Crameri, RM, Welling, RJ, Langberg, H, Flyvbjerg, A, Kjaer, M, Babraj, JA, Smith, K & Rennie, MJ 2005, 'Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise', Journal of Physiology, vol. 567, no. 3, pp. 1021-1033. https://doi.org/10.1113/jphysiol.2005.093690

Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. / Miller, Benjamin F.; Olesen, Jens L.; Hansen, Mette; Dossing, Simon; Crameri, Regina M.; Welling, Rasmus J.; Langberg, Henning; Flyvbjerg, Allan; Kjaer, Michael; Babraj, John A.; Smith, Kenneth; Rennie, Michael J.

In: Journal of Physiology, Vol. 567, No. 3, 12.09.2005, p. 1021-1033.

Research output: Contribution to journalArticle

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T1 - Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise

AU - Miller, Benjamin F.

AU - Olesen, Jens L.

AU - Hansen, Mette

AU - Dossing, Simon

AU - Crameri, Regina M.

AU - Welling, Rasmus J.

AU - Langberg, Henning

AU - Flyvbjerg, Allan

AU - Kjaer, Michael

AU - Babraj, John A.

AU - Smith, Kenneth

AU - Rennie, Michael J.

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N2 - We hypothesized that an acute bout of strenuous, non-damaging exercise would increase rates of protein synthesis of collagen in tendon and skeletal muscle but these would be less than those of muscle myofibrillar and sarcoplasmic proteins. Two groups (n = 8 and 6) of healthy young men were studied over 72 h after 1 h of one-legged kicking exercise at 67% of maximum workload (Wmax). To label tissue proteins in muscle and tendon primed, constant infusions of [1-13C]leucine or [1-13C]valine and flooding doses of [15N] or [13C]proline were given intravenously, with estimation of labelling in target proteins by gas chromatography-mass spectrometry. Patellar tendon and quadriceps biopsies were taken in exercised and rested legs at 6, 24, 42 or 48 and 72 h after exercise. The fractional synthetic rates of all proteins were elevated at 6 h and rose rapidly to peak at 24 h post exercise (tendon collagen (0.077% h-1), muscle collagen (0.054% h-1), myofibrillar protein (0.121% h-1), and sarcoplasmic protein (0.134% h-1)). The rates decreased toward basal values by 72 h although rates of tendon collagen and myofibrillar protein synthesis remained elevated. There was no tissue damage of muscle visible on histological evaluation. Neither tissue microdialysate nor serum concentrations of IGF-I and IGF binding proteins (IGFBP-3 and IGFBP-4) or procollagen type I N-terminal propeptide changed from resting values. Thus, there is a rapid increase in collagen synthesis after strenuous exercise in human tendon and muscle. The similar time course of changes of protein synthetic rates in different cell types supports the idea of coordinated musculotendinous adaptation.

AB - We hypothesized that an acute bout of strenuous, non-damaging exercise would increase rates of protein synthesis of collagen in tendon and skeletal muscle but these would be less than those of muscle myofibrillar and sarcoplasmic proteins. Two groups (n = 8 and 6) of healthy young men were studied over 72 h after 1 h of one-legged kicking exercise at 67% of maximum workload (Wmax). To label tissue proteins in muscle and tendon primed, constant infusions of [1-13C]leucine or [1-13C]valine and flooding doses of [15N] or [13C]proline were given intravenously, with estimation of labelling in target proteins by gas chromatography-mass spectrometry. Patellar tendon and quadriceps biopsies were taken in exercised and rested legs at 6, 24, 42 or 48 and 72 h after exercise. The fractional synthetic rates of all proteins were elevated at 6 h and rose rapidly to peak at 24 h post exercise (tendon collagen (0.077% h-1), muscle collagen (0.054% h-1), myofibrillar protein (0.121% h-1), and sarcoplasmic protein (0.134% h-1)). The rates decreased toward basal values by 72 h although rates of tendon collagen and myofibrillar protein synthesis remained elevated. There was no tissue damage of muscle visible on histological evaluation. Neither tissue microdialysate nor serum concentrations of IGF-I and IGF binding proteins (IGFBP-3 and IGFBP-4) or procollagen type I N-terminal propeptide changed from resting values. Thus, there is a rapid increase in collagen synthesis after strenuous exercise in human tendon and muscle. The similar time course of changes of protein synthetic rates in different cell types supports the idea of coordinated musculotendinous adaptation.

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JO - Journal of Physiology

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