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

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 (W(max)). To label tissue proteins in muscle and tendon primed, constant infusions of [1-(13)C]leucine or [1-(13)C]valine and flooding doses of [(15)N] or [(13)C]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.

Figure 1. Schedule of application of stable isotope infusions and biopsy sampling in Group I (n = 8) for the examination of the time course in change of muscle contractile and collagen and tendon collagen protein

Time scale is in hours with the initiation of tracer infusion at time 0. Not shown in the figure is the skin biopsy obtained prior to isotope infusion.

Figure 2. Schedule of application of stable isotope infusions and biopsy sampling in Group II (n = 6) for determination of the time course in change of muscle contractile and collagen and tendon collagen protein

Time scale is replicated from Group I. Not shown in the figure is the skin biopsy obtained prior to isotope infusion. Please note that the 42 h protocol was only performed on 3 subjects for the purposes of obtaining 42 h measurements and to ascertain the feasibility of performing repeated tendon biopsies. Although the 42 h measurements fall in line with the time course, the reader is encouraged to use discretion in their interpretation.

Figure 3. No difference (P≥ 0.05) between FSR of proteins in repeated rested muscle biopsies on three different days (top) or between 24 h values in two groups (bottom)

Values are the same regardless of tracer used. Values are means ±s.d.

Figure 4. Fractional rates of synthesis of: tendon collagen protein (row 1), muscle collagen protein (row 2), myofibrillar protein (row 3), and sarcoplasmic protein (row 4) at rest and after exercise

Values are means ±s.d.*Significantly different compared with rested leg (P < 0.05). Tendon biopsy electron micrograph (top right) illustrates that the biopsy procedure was sampling tendon tissue as denoted by striated pattern of collagen fibres. Tissue staining of muscle samples at 6 and 24 h with: fibronectin (row 2 right), desmin (row 3 right), and dystrophin (row 4 right). There was no tissue damage as evident by membrane integrity (fibronectin and desmin) and lack of ghost fibres (dystrophin).