Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle

Haus, Jacob M.; Carrithers, John A.; Trappe, Scott; Trappe, Todd A.

doi:10.1152/japplphysiol.00670.2007

Cited by 335 publications

(295 citation statements)

References 50 publications

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“…Transverse aponeurosis modulus increased from 188.5± 24.2 MPa (N=5) in young rats to 328.0±48.3 MPa (N=5) in old rats (Table 1). The observed change in transverse aponeurosis stiffness is likely to be a result of increases in the amount and cross-linking of collagen with age (Alnaqeeb et al, 1984;Bailey, 2001;Haus et al, 2007).…”

Section: Connective Tissue Propertiesmentioning

confidence: 99%

Stuck in gear: age-related loss of variable gearing in skeletal muscle

Holt

Danos

Roberts

et al. 2016

Journal of Experimental Biology

101

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Skeletal muscles power a broad diversity of animal movements, despite only being able to produce high forces over a limited range of velocities. Pennate muscles use a range of gear ratios, the ratio of muscle shortening velocity to fiber shortening velocity, to partially circumvent these force-velocity constraints. Muscles operate with a high gear ratio at low forces; fibers rotate to greater angles of pennation, enhancing velocity but compromising force. At higher forces, muscles operate with a lower gear ratio; fibers rotate little so limiting muscle shortening velocity, but helping to preserve force. This ability to shift gears is thought to be due to the interplay of contractile force and connective tissue constraints. In order to test this hypothesis, gear ratios were determined in the medial gastrocnemius muscles of both healthy young rats, and old rats where the interaction between contractile and connective tissue properties was assumed to be disrupted. Muscle fiber and aponeurosis stiffness increased with age (P<0.05) from 19.1± 5.0 kPa and 188.5±24.2 MPa, respectively, in young rats to 39.1± 4.2 kPa and 328.0±48.3 MPa in old rats, indicating a mechanical change in the interaction between contractile and connective tissues. Gear ratio decreased with increasing force in young (P<0.001) but not old (P=0.72) muscles, indicating that variable gearing is lost in old muscle. These findings support the hypothesis that variable gearing results from the interaction between contractile and connective tissues and suggest novel explanations for the decline in muscle performance with age.

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Section: Connective Tissue Propertiesmentioning

confidence: 99%

Stuck in gear: age-related loss of variable gearing in skeletal muscle

Holt

Danos

Roberts

et al. 2016

Journal of Experimental Biology

101

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“…We also determined the AGE accumulation in skin using a noninvasive method based on autofluorescence (AGE reader; Meerwaldt et al 2004). It has been shown that the difference between young and older individuals in AGE cross-link density in collagen is twofold in skin (Verzijl et al 2000) and skeletal muscle (Haus et al 2007), fivefold in bone (Saito et al 1997), sevenfold in tendon (Couppe et al 2009), ninefold in ligaments (Chen et al 2000), and 33-fold in cartilage (Verzijl et al 2000) demonstrating marked age-related differences in tissue-specific turnover. The present data showed 45 % higher values in skin with aging, but also 11 % lower values by training, indicating that routinerunning reduced the age-related AGE accumulation in skin.…”

Section: Youngmentioning

confidence: 99%

“…AGE cross-links accumulate with age in long-lived proteins, such as collagen, resulting in markedly higher concentrations in older than in younger individuals (Chen et al 2000;DeGroot et al 2001;Haus et al 2007;Bank et al 1999;Suzuki et al 2008). The accumulation appears to be accelerated with age-related chronic diseases such as diabetes (Dyer et al 1993;Vogt et al 1982) and is believed to influence the function of several tissues.…”

Section: Introductionmentioning

confidence: 99%

Life-long endurance running is associated with reduced glycation and mechanical stress in connective tissue

Couppé

Svensson

Grosset

et al. 2014

AGE

109

103

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Life-long regular endurance exercise is known to counteract the deterioration of cardiovascular and metabolic function and overall mortality. Yet it remains unknown if life-long regular endurance exercise can influence the connective tissue accumulation of advanced glycation endproducts (AGEs) that is associated with aging and lifestyle-related diseases. We therefore examined two groups of healthy elderly men: 15 master athletes (64±4 years) who had been engaged in life-long endurance running and 12 old untrained (66±4 years) together with two groups of healthy young men; ten young athletes matched for running distance (26±4 years), and 12 young untrained (24±3 years). AGE cross-links (pentosidine) of the patellar tendon AGE (2014) were measured biochemically, and in the skin, it was assessed by a fluorometric method. In addition, we determined mechanical properties and microstructure of the patellar tendon. Life-long regular endurance runners (master athletes) had a 21 % lower AGE cross-link density compared to old untrained. Furthermore, both master athletes and young athletes displayed a thicker patellar tendon. These cross-sectional data suggest that life-long regular endurance running can partly counteract the aging process in connective tissue by reducing age-related accumulation of AGEs. This may not only benefit skin and tendon but also other long-lived protein tissues in the body. Furthermore, it appears that endurance running yields tendon tissue hypertrophy that may serve to lower the stress on the tendon and thereby reduce the risk of injury.

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“…Following freeze drying, each sample was homogenized in 40 volumes of cold homogenizing buffer (250 mM sucrose, 100 mM potassium chloride, 20 mM imidazole, and 5 mM EDTA; pH 6.8) in a ground-glass homogenizer (Radnoti Glass Technology, Monrovia, CA) (10). An aliquot of each homogenate was measured for protein concentration using the bicinchoninic acid assay (Sigma) with bovine serum albumin used as the protein standard (20,44). The amount of protein and water in each sample was normalized to muscle wet weight.…”

Section: Muscle Protein and Water Quantificationmentioning

confidence: 99%

Influence of acetaminophen and ibuprofen on skeletal muscle adaptations to resistance exercise in older adults

Trappe

Carroll

Dickinson

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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157

215

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Trappe TA, Carroll CC, Dickinson JM, LeMoine JK, Haus JM, Sullivan BE, Lee JD, Jemiolo B, Weinheimer EM, Hollon CJ. Influence of acetaminophen and ibuprofen on skeletal muscle adaptations to resistance exercise in older adults. Am J Physiol Regul Integr Comp Physiol 300: R655-R662, 2011. First published December 15, 2010; doi:10.1152/ajpregu.00611.2010.-Evidence suggests that consumption of over-the-counter cyclooxygenase (COX) inhibitors may interfere with the positive effects that resistance exercise training has on reversing sarcopenia in older adults. This study examined the influence of acetaminophen or ibuprofen consumption on muscle mass and strength during 12 wk of knee extensor progressive resistance exercise training in older adults. Thirty-six individuals were randomly assigned to one of three groups and consumed the COX-inhibiting drugs in double-blind placebo-controlled fashion: placebo (67 Ϯ 2 yr; n ϭ 12), acetaminophen (64 Ϯ 1 yr; n ϭ 11; 4 g/day), and ibuprofen (64 Ϯ 1 yr; n ϭ 13; 1.2 g/day). Compliance with the resistance training program (100%) and drug consumption (via digital video observation, 94%), and resistance training intensity were similar (P Ͼ 0.05) for all three groups. Drug consumption unexpectedly increased muscle volume (acetaminophen: 109 Ϯ 14 cm 3 , 12.5%; ibuprofen: 84 Ϯ 10 cm 3 , 10.9%) and muscle strength (acetaminophen: 19 Ϯ 2 kg; ibuprofen: 19 Ϯ 2 kg) to a greater extent (P Ͻ 0.05) than placebo (muscle volume: 69 Ϯ 12 cm 3 , 8.6%; muscle strength: 15 Ϯ 2 kg), when controlling for initial muscle size and strength. Follow-up analysis of muscle biopsies taken from the vastus lateralis before and after training showed muscle protein content, muscle water content, and myosin heavy chain distribution were not influenced (P Ͼ 0.05) by drug consumption. Similarly, muscle content of the two known enzymes potentially targeted by the drugs, COX-1 and -2, was not influenced (P Ͼ 0.05) by drug consumption, although resistance training did result in a drug-independent increase in COX-1 (32 Ϯ 8%; P Ͻ 0.05). Drug consumption did not influence the size of the nonresistance-trained hamstring muscles (P Ͼ 0.05). Over-thecounter doses of acetaminophen or ibuprofen, when consumed in combination with resistance training, do not inhibit and appear to enhance muscle hypertrophy and strength gains in older adults. The present findings coupled with previous short-term exercise studies provide convincing evidence that the COX pathway(s) are involved in the regulation of muscle protein turnover and muscle mass in humans.cyclooxygenase; prostaglandin; sarcopenia SARCOPENIA, DEFINED AS THE loss of skeletal muscle mass, is a debilitating clinical condition associated with old age (13,40). This age-related loss of muscle mass is associated with a loss of muscle strength and function, a reduced functional independence, and a financial burden to the US healthcare system estimated at $20 billion per year (19,23,24,51). One of the most proven treatments for sarcopenia is resistance exercise training, which in...

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Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle

Cited by 335 publications

References 50 publications

Stuck in gear: age-related loss of variable gearing in skeletal muscle

Stuck in gear: age-related loss of variable gearing in skeletal muscle

Life-long endurance running is associated with reduced glycation and mechanical stress in connective tissue

Influence of acetaminophen and ibuprofen on skeletal muscle adaptations to resistance exercise in older adults

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