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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Post-workout MPS rates peak within three hours and remain elevated for an additional 24-72 h.
“post workout MPS rates peak within three hours and remain elevated for an additional 24–72 h [50, 70].”
From International Society of Sports Nutrition Position Stand: protein and exercise (2017) · cites this paper as [70]
SarcPS remains elevated for 48 h following endurance exercise.
“Indeed, previous reports indicate that SarcPS remains elevated for 48 h following endurance exercise [58], and these increases are likely reflected in the integrative measure of protein synthesis used in this study, which represents a summation of SarcPS throughout the entire intervention.”
From Exercise mitigates sleep-loss-induced changes in glucose tolerance, mitochondrial function, sarcoplasmic protein synthesis, and diurnal rhythms (2021) · cites this paper as [58]
Cites
Calcium's Role in Mechanotransduction during Muscle Development
Damm, T. B., & Egli, M. (2014) · Cellular Physiology and Biochemistry · doi:10.1159/000356667 · Cited by 14,548 · see citing works
Molecular Mechanisms of Stress-Responsive Changes in Collagen and Elastin Networks in Skin
Aziz, J., Shezali, H., Radzi, Z., Yahya, N. A., Abu Kassim, N. H., Czernuszka, J., & Rahman, M. T. (2016) · Skin Pharmacology and Physiology · doi:10.1159/000447017 · Cited by 7,323 · see citing works
Maniotis, A. J., Chen, C. S., & Ingber, D. E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.3.849 · Cited by 1,606 · see citing works
Role of Extracellular Matrix in Adaptation of Tendon and Skeletal Muscle to Mechanical Loading
Kjær, M. (2004) · Physiological Reviews · doi:10.1152/physrev.00031.2003 · Cited by 1,596 · see citing works
Balagopal, P., Rooyackers, O., Adey, D., Ades, P. A., & Nair, K. S. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.4.e790 · Cited by 541 · see citing works
Effect of strength training on human patella tendon mechanical properties of older individuals
Reeves, N. D., Maganaris, C. N., & Narici, M. V. (2003) · The Journal of Physiology · doi:10.1111/j..2003.t01-1-00971.x · Cited by 484 · see citing works
Effect of strength training on human patella tendon mechanical properties of older individuals
Reeves, N. D., Maganaris, C. N., & Narici, M. V. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.035576 · Cited by 484 · see citing works
Atherton, P. J., Babraj, J. A., Smith, K., Singh, J., Rennie, M. J., & Wackerhage, H. (2005) · The FASEB Journal · doi:10.1096/fj.04-2179fje · Cited by 475 · see citing works
Self-citationAge and aerobic exercise training effects on whole body and muscle protein metabolism
Short, K. R., Vittone, J. L., Bigelow, M. L., Proctor, D. N., & Nair, K. S. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00366.2003 · Cited by 470 · cited 4× · see citing works
“Recently it has become clear that modes of muscle contraction other than resistance exercise can result in increases in muscle protein synthesis, with increases being reported in endurance type activities (Carraro et al. 1990; Sheffield-Moore et al. 2004; Short et al. 2004).”
BackgroundInfluentialRennie, M. J., Edwards, R. H. T., Halliday, D., Matthews, D. E., Wolman, S. L., & Millward, D. J. (1982) · Clinical Science · doi:10.1042/cs0630519 · Cited by 455 · see citing works
Self-citationIngber, D. E., Dike, L. E., Hansen, L. K., Karp, S. J., Liley, H. G., Maniotis, A. J., McNamee, H., Mooney, D. J., Plopper, G. E., Sims, J., et al. (1994) · International review of cytology · doi:10.1016/s0074-7696(08)61542-9 · Cited by 430 · see citing works
Regulation of extracellular matrix gene expression by mechanical stress
Chiquet, M. (1999) · Matrix Biology · doi:10.1016/s0945-053x(99)00039-6 · Cited by 428 · see citing works
Applied gas chromatography coupled to isotope ratio mass spectrometry
Meier‐Augenstein, W. (1999) · Journal of Chromatography A · doi:10.1016/s0021-9673(98)01057-7 · Cited by 426 · see citing works
Bohé (2001) · doi:10.1111/j.1469-7793.2001.0575f.x · Cited by 406 · see citing works
Self-citationHow do fibroblasts translate mechanical signals into changes in extracellular matrix production?
Chiquet, M., Sarasa‐Renedo, A., Huber, F., & Flück, M. (2003) · Matrix Biology · doi:10.1016/s0945-053x(03)00004-0 · Cited by 392 · see citing works
The effect of starvation on the rate of protein synthesis in rat liver and small intestine
McNurlan, M. A., Tomkins, A. M., & Garlick, P. J. (1979) · Biochemical Journal · doi:10.1042/bj1780373 · Cited by 387 · see citing works
Langberg, H., Skovgaard, D. C., Petersen, L. J., Bülow, J., & Kjær, M. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00299.x · Cited by 350 · see citing works
Self-citationP ROTEIN AND A MINO A CID M ETABOLISM D URING AND A FTER E XERCISE AND THE E FFECTS OF N UTRITION
Rennie, M. J., & Tipton, K. D. (2000) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.20.1.457 · Cited by 321 · see citing works
Self-citationRosager, S., Aagaard, P., Dyhre‐Poulsen, P., Neergaard, K., Kjær, M., & Magnusson, S. P. (2002) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1034/j.1600-0838.2002.120205.x · Cited by 317 · see citing works
Cellular adaptation to repeated eccentric exercise-induced muscle damage
Stupka, N., Tarnopolsky, M. A., Yardley, N. J., & Phillips, S. M. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.4.1669 · Cited by 279 · see citing works
Langberg, H., Rosendal, L., & Kjær, M. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00297.x · Cited by 273 · see citing works
Self-citationFrystyk, J., Dinesen, B., & Ørskov, H. (1995) · PubMed · Cited by 272 · see citing works
Scheller, D., & Kolb, J. (1991) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(91)90114-f · Cited by 272 · see citing works
Moore, D. R., Phillips, S. M., Babraj, J. A., Smith, K., & Rennie, M. J. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00387.2004 · Cited by 268 · see citing works
Self-citationThe structure and functional significance of variations in the connective tissue within muscle
Purslow, P. P. (2002) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(02)00141-1 · Cited by 259 · see citing works
Bolster, D. R., Kubica, N., Crozier, S. J., Williamson, D. L., Farrell, P. A., Kimball, S. R., & Jefferson, L. S. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.047019 · Cited by 251 · see citing works
Effect of exercise and recovery on muscle protein synthesis in human subjects
Carraro, F., Stuart, C. A., Hartl, W. H., Rosenblatt, J., & Wolfe, R. R. (1990) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1990.259.4.e470 · Cited by 247 · see citing works
Schwenk, W. F., Berg, P. J., Beaufrère, B., Miles, J. M., & Haymond, M. W. (1984) · Analytical Biochemistry · doi:10.1016/0003-2697(84)90431-7 · Cited by 231 · see citing works
Sheffield-Moore, M., Yeckel, C. W., Volpi, E., Wolf, S. E., Morio, B., Chinkes, D. L., Paddon-Jones, D., & Wolfe, R. R. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00334.2003 · Cited by 197 · see citing works
Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein
Smith, K., Reynolds, N., Downie, S., Patel, A. A., & Rennie, M. J. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.275.1.e73 · Cited by 197 · see citing works
Self-citationIntegrins: Redundant or Important Players in Skeletal Muscle?
Mayer, U. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.r200022200 · Cited by 196 · see citing works
Langberg, H., Olesen, J. L., Gemmer, C., & Kjær, M. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.019141 · Cited by 186 · see citing works
Self-citationCollagen synthesis in human musculoskeletal tissues and skin
Babraj, J., Cuthbertson, D. J., Smith, K., Langberg, H., Miller, B. F., Krogsgaard, M. R., Kjær, M., & Rennie, M. J. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00243.2005 · Cited by 177 · see citing works
Self-citationTendon properties in relation to muscular activity and physical training
Magnusson, S. P., Hansen, P., & Kjær, M. (2003) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1034/j.1600-0838.2003.00308.x · Cited by 166 · see citing works
Watt, P., Lindsay, Y. E., Scrimgeour, C. M., Chien, P., Gibson, J. N. A., Taylor, D. J., & Rennie, M. J. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.13.5892 · Cited by 165 · see citing works
Self-citationRole of TGF-β1 in relation to exercise-induced type I collagen synthesis in human tendinous tissue
Heinemeier, K. M., Langberg, H., Olesen, J. L., & Kjær, M. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00403.2003 · Cited by 137 · see citing works
Self-citationCollagen of slow twitch and fast twitch muscle fibres in different types of rat skeletal muscle
Kovanen, V., Suominen, H., & Heikkinen, E. M. (1984) · European Journal of Applied Physiology · doi:10.1007/bf00433399 · Cited by 119 · see citing works
Mittendorfer, B., Andersen, J. L., Plomgaard, P., Saltin, B., Babraj, J., Smith, K., & Rennie, M. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.077180 · Cited by 117 · see citing works
Self-citationLangberg, H., Skovgaard, D. C., Asp, S., & Kjær, M. (2000) · Calcified Tissue International · doi:10.1007/s00223001094 · Cited by 117 · see citing works
Self-citationLaurent, G. J. (1982) · Biochemical Journal · doi:10.1042/bj2060535 · Cited by 114 · see citing works
Koskinen, S. O. A., Wang, W., Ahtikoski, A. M., Kjær, M., Han, X. Y., Komulainen, J., Kovanen, V., & Takala, T. E. S. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.5.r1292 · Cited by 113 · see citing works
Flyvbjerg, A., Kessler, U., Dorka, B., Funk, B., �rskov, H., & Kiess, W. (1992) · Diabetologia · doi:10.1007/bf00400489 · Cited by 102 · see citing works
Self-citationHellsten, Y., Hansson, H., JOHNSON, L., Frandsen, U., & Sjödin, B. (1996) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1996.492235000.x · Cited by 86 · see citing works
Serum concentrations of collagen degrading enzymes and their inhibitors after downhill running
Koskinen, S. O. A., Höyhtyä, M., Turpeenniemi-Hujanen, T. M., Martikkala, V., Mäkinen, T. T., Oksa, J., Rintamäki, H., Löfberg, M., Somer, H., & Takala, T. E. S. (2001) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1034/j.1600-0838.2001.011001009.x · Cited by 84 · see citing works
Body composition and resting metabolic rate: the myth of feminine metabolism
Cunningham, J. (1982) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/36.4.721 · Cited by 82 · see citing works
Human Bone Collagen Synthesis Is a Rapid, Nutritionally Modulated Process
Babraj, J., Smith, K., Cuthbertson, D. J., Rickhuss, P. K., Dorling, J. S., & Rennie, M. J. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.050201 · Cited by 76 · see citing works
Self-citationWatt, P., Corbett, M. E., & Rennie, M. J. (1992) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1992.263.3.e453 · Cited by 75 · see citing works
Self-citationHan, X., Wang, W., Koskinen, S. O. A., Kovanen, V., Takala, T., Komulainen, J., Vihko, V., & Trackman, P. C. (1999) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050855 · Cited by 69 · see citing works
Suominen, H., Heikkinen, E. M., & Parkatti, T. (1977) · Journal of Gerontology · doi:10.1093/geronj/32.1.33 · Cited by 69 · see citing works
Louis, M., Poortmans, J. R., Francaux, M., Hultman, E., Berré, J., Boisseau, N., Young, V. R., Smith, K., Meier-Augenstein, W., Babraj, J. A., et al. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00338.2002 · Cited by 61 · see citing works
Self-citationSuominen, H., & Heikkinen, E. M. (1975) · European Journal of Applied Physiology · doi:10.1007/bf00999938 · Cited by 53 · see citing works
Sequential extracts of human bone show differing collagen synthetic rates
Babraj, J., Cuthbertson, D. J., Rickhuss, P. K., Meier‐Augenstein, W., Smith, K., Bohé, J., Wolfe, R. R., Gibson, J. N. A., Adams, C. E., & Rennie, M. J. (2002) · Biochemical Society Transactions · doi:10.1042/bst0300061 · Cited by 52 · see citing works
Self-citationThe measurement of tissue protein turnover
Smith, K., & Rennie, M. J. (1996) · Baillière s Clinical Endocrinology and Metabolism · doi:10.1016/s0950-351x(96)80651-3 · Cited by 52 · see citing works
Self-citationAhtikoski, A. M., Koskinen, S. O. A., Virtanen, P., Kovanen, V., & Takala, T. (2001) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2001.00848.x · Cited by 51 · see citing works
Effects of physical training on metabolism of connective tissues in young mice
Suominen, H., Kiiskinen, A., & Heikkinen, E. M. (1980) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1980.tb06495.x · Cited by 50 · see citing works
Takala, T., Myllyl�, R., Salminen, A., Anttinen, H., & Vihko, V. (1983) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00652751 · Cited by 27 · see citing works
Invited Review: Autocrine/paracrine IGF-I and skeletal muscle adaptation.
Adams, G. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01264.2001 · Cited by 22 · see citing works
Wendel, U., & Langenbeck, U. (1984) · Biochemical Medicine · doi:10.1016/0006-2944(84)90085-1 · Cited by 16 · see citing works
Connecting the Dots for Mechanochemical Transduction in Muscle
Rennie, M. J., & Wackerhage, H. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.054197 · Cited by 9 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Thomas, D. T., Erdman, K. A., & Burke, L. M. (2016) · Journal of the Academy of Nutrition and Dietetics · doi:10.1016/j.jand.2015.12.006 · Cited by 1,359 · see citing works
Nutrition and Athletic Performance
(2016) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000852 · Cited by 1,305 · see citing works
Tang, J. E., Moore, D. R., Kujbida, G. W., Tarnopolsky, M. A., & Phillips, S. M. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00076.2009 · Cited by 998 · see citing works
Wilkinson, D. J., Piasecki, M., & Atherton, P. J. (2018) · Ageing Research Reviews · doi:10.1016/j.arr.2018.07.005 · Cited by 885 · see citing works
International Society of Sports Nutrition Position Stand: protein and exercise
Jäger, R., Kerksick, C. M., Campbell, B. I., Cribb, P. J., Wells, S. D., Skwiat, T. M., Purpura, M., Ziegenfuss, T. N., Ferrando, A. A., Arent, S. M., et al. (2017) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-017-0177-8 · Cited by 873 · see citing works
“These findings and others add to the theoretical basis for consumption of post-protein sooner rather than later after exercise, since post workout MPS rates peak within three hours and remain elevated for an additional 24– 72 h [50, 70].”
BackgroundKumar, V., Selby, A., Rankin, D., Patel, R., Atherton, P., Hildebrandt, W., Williams, J., Smith, K., Seynnes, O., Hiscock, N., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.164483 · Cited by 740 · see citing works
Self-citationInternational Society of Sports Nutrition position stand: protein and exercise
Campbell, B., Kreider, R. B., Ziegenfuss, T., La Bounty, P., Roberts, M., Burke, D., Landis, J., Lopez, H., & Antonio, J. (2007) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-4-8 · Cited by 716 · see citing works
Wilkinson, S. B., Phillips, S. M., Atherton, P. J., Patel, R., Yarasheski, K. E., Tarnopolsky, M. A., & Rennie, M. J. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.153916 · Cited by 628 · see citing works
Self-citationSkeletal Muscle Regulates Metabolism via Interorgan Crosstalk: Roles in Health and Disease
Argilés, J. M., Campos, N., Lopez-Pedrosa, J. M., Rueda, R., & Rodriguez-Mañas, L. (2016) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2016.04.019 · Cited by 581 · see citing works
Wernbom, M., Augustsson, J., & Thome??, R. (2007) · Sports Medicine · doi:10.2165/00007256-200737030-00004 · Cited by 583 · see citing works
Breen, L., & Phillips, S. M. (2011) · Nutrition & Metabolism · doi:10.1186/1743-7075-8-68 · Cited by 576 · see citing works
Burd, N. A., West, D. W. D., Staples, A. W., Atherton, P. J., Baker, J. M., Moore, D. R., Holwerda, A. M., Parise, G., Rennie, M. J., Baker, S. K., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012033 · Cited by 531 · see citing works
Self-citationStructure‐function relationships in tendons: a review
BENJAMIN, M., Kaiser, E., & Milz, S. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00864.x · Cited by 510 · see citing works
The pathogenesis of tendinopathy: balancing the response to loading
Magnusson, S. P., Langberg, H., & Kjær, M. (2010) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2010.43 · Cited by 500 · see citing works
Self-citationEffects of Exercise and Aging on Skeletal MusclePreprint
Distéfano, G., & Goodpaster, B. H. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029785 · Cited by 491 · see citing works
Böhm, S., Mersmann, F., & Arampatzis, A. (2015) · Sports Medicine - Open · doi:10.1186/s40798-015-0009-9 · Cited by 465 · see citing works
Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle
Haus, J. M., Carrithers, J. A., Trappe, S. W., & Trappe, T. A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00670.2007 · Cited by 417 · see citing works
Cook, J. L., Rio, E., Purdam, C. R., & Docking, S. (2016) · British Journal of Sports Medicine · doi:10.1136/bjsports-2015-095422 · Cited by 411 · see citing works
Muscle protein synthesis in response to nutrition and exercise
Atherton, P. J., & Smith, K. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.225003 · Cited by 401 · see citing works
Self-citationBurd, N. A., Tang, J. E., Moore, D. R., & Phillips, S. M. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91351.2008 · Cited by 390 · see citing works
Effect of Estrogen on Musculoskeletal Performance and Injury Risk
Chidi-Ogbolu, N., & Baar, K. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01834 · Cited by 389 · see citing works
Region specific patellar tendon hypertrophy in humans following resistance training
Kongsgaard, M., Reitelseder, S., Pedersen, T. G., Holm, L., Aagaard, P., Kjaer, M., & Magnusson, S. P. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01714.x · Cited by 377 · see citing works
Léger, B., Cartoni, R., Praz, M., Lamon, S., Dériaz, O., Crettenand, A., Gobelet, C., Rohmer, P., Konzelmann, M., Lüthi, F., et al. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.116715 · Cited by 381 · see citing works
Chronic Adaptations to Eccentric Training: A Systematic Review
Douglas, J. M., Pearson, S. N., Ross, A., & McGuigan, M. R. (2016) · Sports Medicine · doi:10.1007/s40279-016-0628-4 · Cited by 385 · see citing works
Stimuli and sensors that initiate skeletal muscle hypertrophy following resistance exercise
Wackerhage, H., Schoenfeld, B. J., Hamilton, D. L., Lehti, M., & Hulmi, J. J. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00685.2018 · Cited by 357 · see citing works
Arampatzis, A., Karamanidis, K., & Albracht, K. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.003814 · Cited by 354 · see citing works
From mechanical loading to collagen synthesis, structural changes and function in human tendon
Kjær, M., Langberg, H., Heinemeier, K. M., Bayer, M. L., Hansen, M., Holm, L., Doessing, S., Kongsgaard, M., Krogsgaard, M. R., & Magnusson, S. P. (2009) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2009.00986.x · Cited by 344 · see citing works
Self-citationBoer, M. D. D., Selby, A., Atherton, P. J., Smith, K., Seynnes, O., Maganaris, C. N., Maffulli, N., Movin, T., Narici, M. V., & Rennie, M. J. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.142828 · Cited by 344 · see citing works
Self-citationHuman tendon behaviour and adaptation, <i>in vivo</i>
Magnusson, S. P., Narici, M. V., Maganaris, C. N., & Kjaer, M. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.139105 · Cited by 330 · see citing works
Moore, D. R., Tang, J. E., Burd, N. A., Rerecich, T., Tarnopolsky, M. A., & Phillips, S. M. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.164087 · Cited by 322 · see citing works
Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb 14 C
Heinemeier, K. M., Schjerling, P., Heinemeier, J., Magnusson, S. P., & Kjær, M. (2013) · The FASEB Journal · doi:10.1096/fj.12-225599 · Cited by 324 · see citing works
Drummond, M. J., Dreyer, H. C., Fry, C. S., Glynn, E. L., & Rasmussen, B. B. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91397.2008 · Cited by 322 · see citing works
Skeletal Muscle Hypertrophy After Aerobic Exercise Training
Konopka, A. R., & Harber, M. P. (2014) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000007 · Cited by 320 · see citing works
Crameri, R. M., Aagaard, P., Qvortrup, K., Langberg, H., Olesen, J., & Kjær, M. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.128827 · Cited by 319 · see citing works
Self-citationChurchward‐Venne, T. A., Burd, N. A., Mitchell, C. J., West, D. W. D., Philp, A., Marcotte, G. R., Baker, S. K., Baar, K., & Phillips, S. M. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.228833 · Cited by 314 · see citing works
Human muscle protein synthesis and breakdown during and after exercise
Kumar, V., Atherton, P. J., Smith, K., & Rennie, M. J. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91481.2008 · Cited by 285 · see citing works
Self-citationChurchward-Venne, T. A., Breen, L., Di Donato, D. M., Hector, A. J., Mitchell, C. J., Moore, D. R., Stellingwerff, T., Breuille, D., Offord, E. A., Baker, S. K., et al. (2014) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.068775 · Cited by 290 · see citing works
Habitual loading results in tendon hypertrophy and increased stiffness of the human patellar tendon
Couppé, C., Kongsgaard, M., Aagaard, P., Hansen, P., Bojsen‐Møller, J., Kjær, M., & Magnusson, S. P. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90361.2008 · Cited by 290 · see citing works
Heinemeier, K. M., Olesen, J. L., Haddad, F., Langberg, H., Kjær, M., Baldwin, K. M., & Schjerling, P. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.127639 · Cited by 288 · see citing works
Self-citationA Brief Review of Critical Processes in Exercise-Induced Muscular Hypertrophy
Phillips, S. M. (2014) · Sports Medicine · doi:10.1007/s40279-014-0152-3 · Cited by 281 · see citing works
Seynnes, O., Erskine, R. M., Maganaris, C. N., Longo, S., Simoneau-Buessinger, É., Grosset, J. F., & Narici, M. V. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00213.2009 · Cited by 268 · see citing works
Egan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278 · see citing works
West, D. W., Burd, N. A., Coffey, V. G., Baker, S. K., Burke, L. M., Hawley, J. A., Moore, D. R., Stellingwerff, T., & Phillips, S. M. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.013722 · Cited by 264 · see citing works
Heat shock response and autophagy—cooperation and control
Dokładny, K., Myers, O., & Moseley, P. L. (2015) · Autophagy · doi:10.1080/15548627.2015.1009776 · Cited by 254 · see citing works
Extracellular matrix adaptation of tendon and skeletal muscle to exercise
Kjær, M., Magnusson, S. P., Krogsgaard, M. R., Bojsen‐Møller, J., Olesen, J. L., Heinemeier, K. M., Hansen, M., Haraldsson, B. T., Koskinen, S., Esmarck, B., et al. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00549.x · Cited by 249 · see citing works
Self-citationSchranner, D., Kastenmüller, G., Schönfelder, M., Römisch‐Margl, W., & Wackerhage, H. (2020) · Sports Medicine - Open · doi:10.1186/s40798-020-0238-4 · Cited by 250 · see citing works
Effect of aging and exercise on the tendon
Svensson, R. B., Heinemeier, K. M., Couppé, C., Kjær, M., & Magnusson, S. P. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00328.2016 · Cited by 231 · see citing works
The adaptability of tendon to loading differs in men and women
Magnusson, S. P., Hansen, M., Langberg, H., Miller, B. F., Haraldsson, B. T., Westh, E. K., Koskinen, S., Aagaard, P., & Kjær, M. (2007) · International Journal of Experimental Pathology · doi:10.1111/j.1365-2613.2007.00551.x · Cited by 226 · see citing works
Self-citationHarber, M. P., Konopka, A. R., Undem, M. K., Hinkley, J. M., Minchev, K., Kaminsky, L. A., Trappe, T. A., & Trappe, S. W. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00786.2012 · Cited by 218 · see citing works
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Szewczyk, N. J., Greenhaff, P. L., Smith, K., & Atherton, P. J. (2015) · The FASEB Journal · doi:10.1096/fj.15-273755 · Cited by 206 · see citing works
Self-citationThe impact of loading, unloading, ageing and injury on the human tendon
Magnusson, S. P., & Kjær, M. (2018) · The Journal of Physiology · doi:10.1113/jp275450 · Cited by 208 · see citing works
Doessing, S., Heinemeier, K. M., Holm, L., Mackey, A. L., Schjerling, P., Rennie, M. J., Smith, K., Reitelseder, S., Kappelgaard, A., Rasmussen, M. H., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.179325 · Cited by 207 · see citing works
Self-citationNutritional modulation of training-induced skeletal muscle adaptations
Hawley, J. A., Burke, L. M., Phillips, S. M., & Spriet, L. L. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00949.2010 · Cited by 205 · see citing works
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Phillips, B. E., Szewczyk, N. J., Greenhaff, P. L., Smith, K., & Atherton, P. J. (2016) · The Journal of Physiology · doi:10.1113/jp272857 · Cited by 204 · see citing works
Self-citationEffect of range of motion in heavy load squatting on muscle and tendon adaptations
Bloomquist, K., Langberg, H., Karlsen, S. F., Madsgaard, S., Boesen, M., & Raastad, T. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-013-2642-7 · Cited by 204 · see citing works
Self-citationDamas, F., Phillips, S., Vechin, F. C., & Ugrinowitsch, C. (2015) · Sports Medicine · doi:10.1007/s40279-015-0320-0 · Cited by 225 · see citing works
Dietary protein requirements and adaptive advantages in athletes
Phillips, S. M. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114512002516 · Cited by 199 · see citing works
Thorpe, C. T., Streeter, I., Pinchbeck, G. L., Goodship, A. E., Clegg, P., & Birch, H. L. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.077503 · Cited by 199 · see citing works
Wilkinson, D. J., Franchi, M. V., Brook, M. S., Narici, M. V., Williams, J. P., Mitchell, W. K., Szewczyk, N. J., Greenhaff, P. L., Atherton, P. J., & Smith, K. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00650.2013 · Cited by 195 · see citing works
Self-citationCancer cachexia prevention via physical exercise: molecular mechanisms
Gould, D. W., Lahart, I. M., Carmichael, A. R., Koutedakis, Y., & Metsios, G. S. (2012) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-012-0096-0 · Cited by 195 · see citing works
Skeletal muscle homeostasis and plasticity in youth and ageing: impact of nutrition and exercise
Brook, M. S., Wilkinson, D. J., Phillips, B. E., Pérez‐Schindler, J., Philp, A., Smith, K., & Atherton, P. J. (2015) · Acta Physiologica · doi:10.1111/apha.12532 · Cited by 193 · see citing works
Self-citationHeinemeier, K. M., Olesen, J. L., Schjerling, P., Haddad, F., Langberg, H., Baldwin, K. M., & Kjær, M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00866.2006 · Cited by 189 · see citing works
Self-citationTendon collagen synthesis at rest and after exercise in women
Miller, B. F., Hansen, M., Olesen, J. L., Schwarz, P., Babraj, J., Smith, K., Rennie, M. J., & Kjær, M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00797.2006 · Cited by 189 · see citing works
Self-citationInfluence of aging on the in vivo properties of human patellar tendon
Carroll, C. C., Dickinson, J. M., Haus, J. M., Lee, G. A., Hollon, C. J., Aagaard, P., Magnusson, S. P., & Trappe, T. A. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00059.2008 · Cited by 186 · see citing works
Norheim, F., Raastad, T., Thiede, B., Rustan, A. C., Drevon, C. A., & Haugen, F. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00326.2011 · Cited by 180 · see citing works
In vivo investigation of tendon responses to mechanical loading.
Heinemeier, K. M., & Kjær, M. (2011) · PubMed · Cited by 180 · see citing works
Role and potential mechanisms of anabolic resistance in sarcopenia
Haran, P. H., Rivas, D. A., & Fielding, R. A. (2012) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-012-0068-4 · Cited by 172 · see citing works
Mackey, A. L., Brandstetter, S., Schjerling, P., Bojsen‐Møller, J., Qvortrup, K., Pedersen, M. M., Doessing, S., Kjær, M., Magnusson, S. P., & Langberg, H. (2011) · The FASEB Journal · doi:10.1096/fj.10-176487 · Cited by 171 · see citing works
Self-citationUse it or lose it: multiscale skeletal muscle adaptation to mechanical stimuli
Wisdom, K. M., Delp, S. L., & Ellen Kuhl, A. (2014) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-014-0607-3 · Cited by 168 · see citing works
Scalzo, R. L., Peltonen, G. L., Binns, S. E., Shankaran, M., Giordano, G. R., Hartley, D. A., Klochak, A. L., Lonac, M. C., Paris, H. L. R., Szallar, S. E., et al. (2014) · The FASEB Journal · doi:10.1096/fj.13-246595 · Cited by 167 · see citing works
Self-citationCuthbertson, D. J., Babraj, J., Smith, K., Wilkes, E., Fedele, M. J., Esser, K., & Rennie, M. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00415.2005 · Cited by 166 · see citing works
Self-citationHansen, M., Kongsgaard, M., Holm, L., Skovgaard, D. C., Magnusson, S. P., Qvortrup, K., Larsen, J. O., Aagaard, P., Dahl, M., Serup, A. K., et al. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90935.2008 · Cited by 166 · see citing works
Self-citationResistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men
Hulmi, J. J., Tannerstedt, J., Selänne, H., Kainulainen, H., Kovanen, V., & Mero, A. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00087.2009 · Cited by 163 · see citing works
Effects of Increased Loading on In Vivo Tendon Properties: A Systematic Review
WIESINGER, H.-P., KÖSTERS, A., MÜLLER, E., & SEYNNES, O. R. (2015) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000603 · Cited by 158 · see citing works
Therapeutic strategies for preventing skeletal muscle fibrosis after injury
Garg, K., Corona, B. T., & Walters, J. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00087 · Cited by 158 · see citing works
Time Course of Changes in Muscle and Tendon Properties During Strength Training and Detraining
Kubo, K., Ikebukuro, T., Yata, H., Tsunoda, N., & Kanehisa, H. (2010) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e3181c865e2 · Cited by 157 · see citing works
Meléndez‐Hevia, E., de Paz-Lugo, P., Cornish-Bowden, A. J., & Cárdenas, M. L. (2009) · Journal of Biosciences · doi:10.1007/s12038-009-0100-9 · Cited by 147 · see citing works
Hansen, M., Miller, B. F., Holm, L., Doessing, S., Petersen, S. G., Skovgaard, D. C., Frystyk, J., Flyvbjerg, A., Koskinen, S., Pingel, J., et al. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90933.2008 · Cited by 146 · see citing works
Self-citationResistance exercise increases leg muscle protein synthesis and mTOR signalling independent of sex
Dreyer, H. C., Fujita, S., Glynn, E. L., Drummond, M. J., Volpi, E., & Rasmussen, B. B. (2010) · Acta Physiologica · doi:10.1111/j.1748-1716.2010.02074.x · Cited by 141 · see citing works
Deldicque, L., Atherton, P. J., Patel, R. S., Theisen, D., Nielens, H., Rennie, M. J., & Francaux, M. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00873.2007 · Cited by 141 · see citing works
Self-citationDonato, D. M. D., West, D. W. D., Churchward‐Venne, T. A., Breen, L., Baker, S. K., & Phillips, S. M. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00487.2013 · Cited by 141 · see citing works
Silbernagel, K. G., & Crossley, K. M. (2015) · Journal of Orthopaedic and Sports Physical Therapy · doi:10.2519/jospt.2015.5885 · Cited by 141 · see citing works
Villareal, D. T., Smith, G. I., Sinacore, D. R., Shah, K., & Mittendorfer, B. (2011) · Obesity · doi:10.1038/oby.2010.110 · Cited by 140 · see citing works
“, every 24–72 h), and (iii) it has been shown that although that the acute effect of resistance exercise lasts for 48–72 h in untrained subjects (50,51) an increase in the rate of muscle protein synthesis in healthy young trained subjects is evident for only ~24–30 h after the last bout of exercise (56).”
BackgroundAckermann, P. W., & Renström, P. A. F. H. (2012) · Sports Health A Multidisciplinary Approach · doi:10.1177/1941738112440957 · Cited by 143 · see citing works
Westh, E. K., Kongsgaard, M., Bojsen‐Møller, J., Aagaard, P., Hansen, M., Kjær, M., & Magnusson, S. P. (2007) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2007.00638.x · Cited by 140 · see citing works
Self-citationExercise, Amino Acids, and Aging in the Control of Human Muscle Protein Synthesis
Walker, D. K., Dickinson, J. M., Timmerman, K. L., Drummond, M. J., Reidy, P. T., Fry, C. S., Gundermann, D. M., & Rasmussen, B. B. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318223b037 · Cited by 137 · see citing works
Beyond muscle hypertrophy: why dietary protein is important for endurance athletes
Moore, D. R., Camera, D. M., Areta, J. L., & Hawley, J. A. (2014) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2013-0591 · Cited by 138 · see citing works
Goodman, C. A. (2013) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/112_2013_17 · Cited by 139 · see citing works
Human Achilles tendon plasticity in response to cyclic strain: effect of rate and duration
Böhm, S., Mersmann, F., Tettke, M., Kraft, M., & Arampatzis, A. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.112268 · Cited by 136 · see citing works
Hyldahl, R. D., Nelson, B., Xin, L., Welling, T., Groscost, L., Hubal, M. J., Chipkin, S. R., Clarkson, P. M., & Parcell, A. C. (2015) · The FASEB Journal · doi:10.1096/fj.14-266668 · Cited by 135 · see citing works
Dudhia, J., Scott, C. M., Draper, E. R. C., Heinegård, D. K., Pitsillides, A. A., & Smith, R. K. W. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00307.x · Cited by 134 · see citing works
Heinemeier, K. M., Olesen, J. L., Haddad, F., Schjerling, P., Baldwin, K. M., & Kjær, M. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91092.2008 · Cited by 134 · see citing works
Self-citationHolm, L., van Hall, G., Rose, A. J., Miller, B. F., Doessing, S., Richter, E. A., & Kjaer, M. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00609.2009 · Cited by 132 · see citing works
Self-citationCollagen Type III and VI Turnover in Response to Long-Term Immobilization
Sun, S., Henriksen, K., Karsdal, M. A., Byrjalsen, I., Rittweger, J., Armbrecht, G., Belavý, D. L., Felsenberg, D., & Nedergaard, A. F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144525 · Cited by 132 · see citing works
Tang, J. E., Manolakos, J. J., Kujbida, G. W., Lysecki, P. J., Moore, D. R., & Phillips, S. M. (2007) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h07-076 · Cited by 130 · see citing works
Robinson, M. M., Turner, S., Hellerstein, M. K., Hamilton, K. L., & Miller, B. F. (2011) · The FASEB Journal · doi:10.1096/fj.11-186437 · Cited by 128 · see citing works
Self-citationWilkinson, D. J., Bukhari, S. S. I., Phillips, B. E., Limb, M. C., Cegielski, J., Brook, M. S., Rankin, D., Mitchell, W. K., Kobayashi, H., Williams, J. P., et al. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2017.09.008 · Cited by 128 · see citing works
Self-citationEffects of and Response to Mechanical Loading on the Knee
Logerstedt, D. S., Ebert, J. R., MacLeod, T. D., Heiderscheit, B. C., Gabbett, T. J., & Eckenrode, B. J. (2021) · Sports Medicine · doi:10.1007/s40279-021-01579-7 · Cited by 127 · see citing works
Eccentric Training for the Treatment of Tendinopathies
Murtaugh, B., & Ihm, J. M. (2013) · Current Sports Medicine Reports · doi:10.1249/jsr.0b013e3182933761 · Cited by 127 · see citing works
Erskine, R. M., Jones, D. A., Williams, A. G., Stewart, C. E., & Degens, H. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1601-9 · Cited by 124 · see citing works
- Authors
- Miller, B. F., Olesen, J. L., Hansen, M., Døssing, S., Crameri, R. M., Welling, R. J., Langberg, H., Flyvbjerg, A., Kjaer, M., Babraj, J. A., Smith, K., & Rennie, M. J.
- Affiliations
- Bispebjerg Hospital (DK)
- Aarhus University Hospital (DK)
- University of Dundee (GB)
- University of Nottingham (GB)
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2005-09
- Volume
- 567
- Issue
- 3
- Pages
- 1021-1033
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- OpenAlex
- W2123852369
- Cited by
- 610
- References
- 58
- Citations by year
- 2026: 25 · 2025: 30 · 2024: 30 · 2023: 26 · 2022: 27 · 2021: 40 · 2020: 27 · 2019: 27 · 2018: 36 · 2017: 26 · 2016: 34 · 2015: 37 · 2014: 20 · 2013: 29 · 2012: 35
- FWCI
- 9.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Tendon Structure and Treatment
- Keywords
- collagen synthesis, muscle protein synthesis, patellar tendon, quadriceps, physical activity, myofibrillar proteins, sarcoplasmic proteins, insulin-like growth factor I, IGF binding proteins, P1NP, post-exercise recovery
- MeSH terms
- Adult, Carbon Radioisotopes, Collagen, Humans, Keto Acids, Leucine, Male, Muscle Proteins, Myofibrils, Nitrogen Radioisotopes, Patella, Proline, Sarcoplasmic Reticulum, Tendons, Thigh, Valine, Exercise, Muscle, Skeletal, Hemiterpenes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
