Human skeletal muscle macrophages increase following cycle training and are associated with adaptations that may facilitate growth
Open accessAbstract
Skeletal muscle macrophages participate in repair and regeneration following injury. However, their role in physiological adaptations to exercise is unexplored. We determined whether endurance exercise training (EET) alters macrophage content and characteristics in response to resistance exercise (RE), and whether macrophages are associated with other exercise adaptations. Subjects provided vastus lateralis biopsies before and after one bout of RE, after 12 weeks of EET (cycling), and after a final bout of RE. M2 macrophages (CD11b+/CD206+) did not increase with RE, but increased in response to EET (P < 0.01). Increases in M2 macrophages were positively correlated with fiber hypertrophy (r = 0.49) and satellite cells (r = 0.47). M2c macrophages (CD206+/CD163+) also increased following EET (P < 0.001), and were associated with fiber hypertrophy (r = 0.64). Gene expression was quantified using NanoString. Following EET, the change in M2 macrophages was positively associated with changes in HGF, IGF1, and extracellular matrix genes. EET decreased expression of IL6 (P < 0.05), C/EBPβ (P < 0.01), and MuRF (P < 0.05), and increased expression of IL-4 (P < 0.01), TNFα (P < 0.01) and the TWEAK receptor FN14 (P < 0.05). The change in FN14 gene expression was inversely associated with changes in C/EBPβ (r = -0.58) and MuRF (r = -0.46) following EET. In cultured human myotubes, siRNA inhibition of FN14 increased expression of C/EBPβ (P < 0.05) and MuRF (P < 0.05). Our data suggest that macrophages contribute to the muscle response to EET, potentially including modulation of TWEAK-FN14 signaling.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Twelve weeks of endurance exercise training composed of cycling 3 d·wk−1 at a target intensity corresponding to 65% V O2max increased M2 macrophage abundance in human skeletal muscle.
“Twelve weeks of endurance exercise training composed of cycling 3 d·wk−1 at a target intensity corresponding to 65% V O2max increased M2 macrophage abundance in human skeletal muscle, suggesting that adaptive changes to training may reduce local inflammation (40).”
From Exercise Counters the Age-Related Accumulation of Senescent Cells (2022) · cites this paper as [40]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The M1 and M2 paradigm of macrophage activation: Time for reassessment
Martinez, F. O., & Gordon, S. (2014) · F1000Prime Reports · doi:10.12703/p6-13 · Cited by 4,689 · see citing works
Macrophages in Tissue Repair, Regeneration, and Fibrosis
Wynn, T. A., & Vannella, K. M. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.015 · Cited by 4,481 · see citing works
Direct multiplexed measurement of gene expression with color-coded probe pairs
Geiss, G. K., Bumgarner, R. E., Birditt, B., Dahl, T., Dowidar, N., Dunaway, D. L., Fell, H. P., Ferree, S., George, R. D., Grogan, T., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1385 · Cited by 2,066 · see citing works
Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K., & Chazaud, B. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070075 · Cited by 2,002 · see citing works
Understanding the Mysterious M2 Macrophage through Activation Markers and Effector Mechanisms
Rőszer, T. (2015) · Mediators of Inflammation · doi:10.1155/2015/816460 · Cited by 1,762 · see citing works
Signaling in innate immunity and inflammation
Newton, K., & Dixit, V. M. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a006049 · Cited by 1,513 · see citing works
Mechanisms regulating skeletal muscle growth and atrophy
Schiaffino, S., Dyar, K. A., Ciciliot, S., Blaauw, B., & Sandri, M. (2013) · The FEBS Journal · doi:10.1111/febs.12253 · Cited by 1,492 · see citing works
Modulation of macrophage phenotype by cell shape
McWhorter, F. Y., Wang, T., Nguyen, P., Chung, T., & Liu, W. F. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308887110 · Cited by 1,482 · see citing works
Liver Macrophages in Tissue Homeostasis and Disease
Krenkel, O., & Tacke, F. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.11 · Cited by 1,424 · see citing works
IKKβ/NF-κB Activation Causes Severe Muscle Wasting in Mice
Cai, D., Frantz, J. D., Tawa, N. E., Melendez, P. A., Oh, B.-C., Lidov, H. G. W., Hasselgren, P.-O., Frontera, W. R., Lee, J., Glass, D. J., et al. (2004) · Cell · doi:10.1016/j.cell.2004.09.027 · Cited by 1,367 · see citing works
Regulatory interactions between muscle and the immune system during muscle regeneration
Tidball, J. G., & Villalta, S. A. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00735.2009 · Cited by 1,105 · see citing works
Host Responses in Tissue Repair and Fibrosis
Duffield, J. S., Lupher, M., Thannickal, V. J., & Wynn, T. A. (2012) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-020712-163930 · Cited by 624 · see citing works
Stein, B., Cogswell, P. C., & Baldwin, A. S. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.7.3964 · Cited by 516 · see citing works
Comparison of polarization properties of human adult microglia and blood‐derived macrophages
Durafourt, B. A., Moore, C. S., Zammit, D., Johnson, T., Zaguia, F., Guiot, M., Bar‐Or, A., & Antel, J. P. (2012) · Glia · doi:10.1002/glia.22298 · Cited by 470 · see citing works
Chazaud, B., Sonnet, C., Lafuste, P., Bassez, G., Rimaniol, A., Poron, F., Authier, F., Dreyfus, P. A., & Gherardi, R. K. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212046 · Cited by 452 · see citing works
Nuclear factor-kappa B signaling in skeletal muscle atrophy
Li, H., Malhotra, S., & Kumar, A. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0373-8 · Cited by 442 · see citing works
Saclier, M., Yacoub‐Youssef, H., Mackey, A. L., Arnold, L., Ardjoune, H., Magnan, M., Sailhan, F., Chelly, J., Pavlath, G. K., Mounier, R., et al. (2012) · Stem Cells · doi:10.1002/stem.1288 · Cited by 421 · see citing works
Rapid, reliable, and reproducible molecular sub-grouping of clinical medulloblastoma samples
Northcott, P. A., Shih, D. J. H., Remke, M., Cho, Y., Kool, M., Hawkins, C. E., Eberhart, C. G., Dubuc, A. M., Guettouche, T., Cardentey, Y., et al. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0899-7 · Cited by 382 · see citing works
Macrophages in Renal Injury and Repair
Huen, S. C., & Cantley, L. G. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034219 · Cited by 377 · see citing works
CD163: A Specific Marker of Macrophages in Paraffin-Embedded Tissue Samples
Lau, S. K., Chu, P. G., & Weiss, L. M. (2004) · American Journal of Clinical Pathology · doi:10.1309/qhd6-yfn8-1kqx-uuh6 · Cited by 326 · see citing works
The Eukaryotic Promoter Database: expansion of EPDnew and new promoter analysis tools
Dreos, R., Ambrosini, G., Périer, R. C., & Bücher, P. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1111 · Cited by 325 · see citing works
Tonkin, J. N., Temmerman, L., Sampson, R. D., Gallego-Colón, E., Barberi, L., Bilbao, D., Schneider, M. D., Musarò, A., & Rosenthal, N. A. (2015) · Molecular Therapy · doi:10.1038/mt.2015.66 · Cited by 320 · see citing works
The eukaryotic promoter database in its 30th year: focus on non-vertebrate organisms
Dreos, R., Ambrosini, G., Groux, R., Périer, R. C., & Bücher, P. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1069 · Cited by 275 · see citing works
Pelosi, L., Giacinti, C., Nardis, C., Borsellino, G., Rizzuto, E., Nicoletti, C., Wannenes, F., Battistini, L., Rosenthal, N. A., Molinaro, M., et al. (2007) · The FASEB Journal · doi:10.1096/fj.06-7690com · Cited by 268 · see citing works
Lu, H., Huang, D., Ransohoff, R. M., & Zhou, L. (2011) · The FASEB Journal · doi:10.1096/fj.10-178939 · Cited by 255 · see citing works
TNF-α is a mitogen in skeletal muscle
Li, Y.-P. (2003) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00453.2002 · Cited by 249 · see citing works
Way, K. L., Hackett, D. A., Baker, M. K., & Johnson, N. A. (2016) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2016.40.4.253 · Cited by 245 · see citing works
TNF‐related weak inducer of apoptosis (TWEAK) is a potent skeletal muscle‐wasting cytokine
Dogra, C., Changoua, H., Wedhas, N., Qin, X., Wergedal, J. E., & Kumar, A. (2007) · The FASEB Journal · doi:10.1096/fj.06-7537com · Cited by 244 · see citing works
TWEAK Attenuates the Transition from Innate to Adaptive Immunity
Maecker, H. L., Varfolomeev, E. E., Kischkel, F. C., Lawrence, D. A., LeBlanc, H. N., Lee, W. P., Hurst, S. D., Danilenko, D. M., Li, J., Filvaroff, E. H., et al. (2005) · Cell · doi:10.1016/j.cell.2005.09.022 · Cited by 240 · see citing works
Dual and Beneficial Roles of Macrophages During Skeletal Muscle Regeneration
Chazaud, B., Brigitte, M., Yacoub-Youssef, H., Arnold, L., Gherardi, R., Sonnet, C., Lafuste, P., & Chrétien, F. (2009) · Exercise and sport sciences reviews · doi:10.1097/jes.0b013e318190ebdb · Cited by 238 · see citing works
Varma, V., Yao-Borengasser, A., Rasouli, N., Nolen, G. T., Phanavanh, B., Starks, T., Gurley, C., Simpson, P., McGehee, R. E., Kern, P. A., et al. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90885.2008 · Cited by 229 · see citing works
Self-citationBover, L. C., Cardó‐Vila, M., Kuniyasu, A., Sun, J. D., Rangel, R., Takeya, M., Aggarwal, B. B., Arap, W., & Pasqualini, R. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.12.8183 · Cited by 216 · see citing works
Girgenrath, M., Weng, S., Kostek, C. A., Browning, B., Wang, M., Brown, S. A. N., Winkles, J. A., Michaelson, J. S., Allaire, N., Schneider, P., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601441 · Cited by 213 · see citing works
Bakkar, N., Wang, J., Ladner, K. J., Wang, H., Dahlman, J. M., Carathers, M., Acharyya, S., Rudnicki, M. A., Hollenbach, A. D., & D, D. C. G. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200707179 · Cited by 208 · see citing works
Transcriptome analysis of IL-10-stimulated (M2c) macrophages by next-generation sequencing
Lurier, E., Dalton, D., Dampier, W., Raman, P., Nassiri, S., Ferraro, N., Rajagopalan, R., Sarmady, M., & Spiller, K. (2017) · Immunobiology · doi:10.1016/j.imbio.2017.02.006 · Cited by 204 · see citing works
Bakkar, N., Wang, J., Ladner, K. J., Wang, H., Dahlman, J. M., Carathers, M., Acharyya, S., Rudnicki, M. A., Hollenbach, A. D., & D, D. C. G. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.20070717908082013c · Cited by 174 · see citing works
Grace, A., Chan, E., Giallauria, F., Graham, P. L., & Smart, N. A. (2017) · Cardiovascular Diabetology · doi:10.1186/s12933-017-0518-6 · Cited by 174 · see citing works
ED2+ macrophages increase selectively myoblast proliferation in muscle cultures.
Massimino, M., Rapizzi, E., Cantini, M., Libera, L., Mazzoleni, F., Arslan, P., & Carraro, U. (1997) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1006/bbrc.1997.6823 · Cited by 162 · see citing works
Przybyla, B., Gurley, C., Harvey, J. F., Bearden, E., Kortebein, P., Evans, W., Sullivan, D., Peterson, C. A., & Dennis, R. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2005.12.007 · Cited by 158 · see citing works
Self-citationDogra, C., Changotra, H., Mohan, S., & Kumar, A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m511131200 · Cited by 158 · see citing works
Effects of endurance training on satellite cell frequency in skeletal muscle of old men.
Charifi, N., Kadi, F., Féasson, L., & Denis, C. (2003) · Muscle & Nerve · doi:10.1002/mus.10394 · Cited by 154 · see citing works
Molecular mechanism of sarcopenia and cachexia: recent research advances
Sakuma, K., Aoi, W., & Yamaguchi, A. (2017) · Pflügers Archiv: European Journal of Physiology · doi:10.1007/s00424-016-1933-3 · Cited by 144 · see citing works
The CD163-expressing macrophages recognize and internalize TWEAK
Moreno, J. A., Muñoz‐García, B., Martı́n-Ventura, J. L., Madrigal‐Matute, J., Orbe, J., Páramo, J. A., Ortega, L. M., Egido, J., & Blanco‐Colio, L. M. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.04.033 · Cited by 141 · see citing works
Fibre type‐specific satellite cell response to aerobic training in sedentary adults
Fry, C. S., Noehren, B. W., Mula, J., Ubele, M. F., Westgate, P. M., Kern, P. A., & Peterson, C. A. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.271288 · Cited by 132 · see citing works
Self-citationCurrent understanding of sarcopenia: possible candidates modulating muscle mass
Sakuma, K., Aoi, W., & Yamaguchi, A. (2014) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-014-1527-x · Cited by 128 · see citing works
Macrophage-released ADAMTS1 promotes muscle stem cell activation
Du, H., Shih, C., Wosczyna, M. N., Mueller, A. A., Cho, J., Aggarwal, A., Rando, T. A., & Feldman, B. J. (2017) · Nature Communications · doi:10.1038/s41467-017-00522-7 · Cited by 128 · see citing works
Cantini, M., Giurisato, E., Radu, C. M., Tiozzo, S., Pampinella, F., Senigaglia, D., Zaniolo, G., Mazzoleni, F., & Vitiello, L. (2002) · Neurological Sciences · doi:10.1007/s100720200060 · Cited by 127 · see citing works
Stein, B., Cogswell, P. C., & Baldwin, A. S. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.7.3964-3974.1993 · Cited by 120 · see citing works
NF-κB Signaling in Skeletal Muscle Health and Disease
Peterson, J. M., Bakkar, N., & D, D. C. G. (2011) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-385940-2.00004-8 · Cited by 118 · see citing works
The breaking and making of healthy adult human skeletal muscle in vivo
Mackey, A. L., & Kjær, M. (2017) · Skeletal Muscle · doi:10.1186/s13395-017-0142-x · Cited by 116 · see citing works
Macrophages Protect against Muscle Atrophy and Promote Muscle Recovery in Vivo and in Vitro
Dumont, N. A., & Frenette, J. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090884 · Cited by 109 · see citing works
CD163 interacts with TWEAK to regulate tissue regeneration after ischaemic injury
Akahori, H., Karmali, V., Polavarapu, R., Lyle, A. N., Weiss, D., Shin, E., Husain, A., Naqvi, N., Dam, R. V., Habib, A., et al. (2015) · Nature Communications · doi:10.1038/ncomms8792 · Cited by 102 · see citing works
Skeletal muscle signature of a champion sprint runner
Trappe, S. W., Luden, N. D., Minchev, K., Raue, U., Jemioło, B., & Trappe, T. A. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00037.2015 · Cited by 100 · see citing works
Global mRNA sequencing of human skeletal muscle: Search for novel exercise-regulated myokines
Pourteymour, S., Eckardt, K., Holen, T., Langleite, T. M., Lee-Ødegård, S., Jensen, J., Birkeland, K. I., Drevon, C. A., & Hjorth, M. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.01.007 · Cited by 99 · see citing works
Resistance exercise training influences skeletal muscle immune activation: a microarray analysis
Gordon, P. M., Liu, D., Sartor, M. A., IglayReger, H. B., Pistilli, E. E., Gutmann, L., Nader, G. A., & Hoffman, E. P. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00860.2011 · Cited by 98 · see citing works
Dogra, C., Hall, S. L., Wedhas, N., Linkhart, T. A., & Kumar, A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m608668200 · Cited by 94 · see citing works
Roos, C., Wicovsky, A., Müller, N., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903555 · Cited by 93 · see citing works
Low-Frequency Electrical Stimulation Attenuates Muscle Atrophy in CKD—A Potential Treatment Strategy
Hu, L., Klein, J. D., Hassounah, F., Cai, H., Zhang, C., Xu, P., & Wang, X. H. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2014020144 · Cited by 90 · see citing works
Wu, C., Kandarian, S. C., & Jackman, R. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016171 · Cited by 82 · see citing works
Joanisse, S., Gillen, J. B., Bellamy, L. M., McKay, B. R., Tarnopolsky, M. A., Gibala, M. J., & Parise, G. (2013) · The FASEB Journal · doi:10.1096/fj.13-229799 · Cited by 82 · see citing works
DiPasquale, D. M., Cheng, M., Billich, W., Huang, S. A., van Rooijen, N., Hornberger, T. A., & Koh, T. J. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00201.2007 · Cited by 79 · see citing works
Immunohistochemical Identification of Human Skeletal Muscle Macrophages
Kosmac, K., Peck, B. D., Walton, R., Mula, J., Kern, P. A., Bamman, M. M., Dennis, R. A., Jacobs, C. A., Lattermann, C. M., Johnson, D. L., et al. (2018) · BIO-PROTOCOL · doi:10.21769/bioprotoc.2883 · Cited by 79 · see citing works
Self-citationTranscriptome response of human skeletal muscle to divergent exercise stimuli
Dickinson, J. M., D’Lugos, A. C., Naymik, M., Siniard, A. L., Wolfe, A. J., Curtis, D. R., Huentelman, M. J., & Carroll, C. C. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00014.2018 · Cited by 76 · see citing works
Veldman-Jones, M. H., Lai, Z., Wappett, M., Harbron, C. G., Barrett, J. C., Harrington, E. A., & Thress, K. S. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-0357 · Cited by 75 · see citing works
Liu, X., Liu, Y., Zhao, L., Zeng, Z., Xiao, W., & Chen, P. (2016) · Cell Biology International · doi:10.1002/cbin.10705 · Cited by 73 · see citing works
TWEAK/Fn14 Signaling Axis Mediates Skeletal Muscle Atrophy and Metabolic Dysfunction
Sato, S., Ogura, Y., & Kumar, A. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00018 · Cited by 72 · see citing works
IKKα and alternative NF-κB regulate PGC-1β to promote oxidative muscle metabolism
Bakkar, N., Ladner, K. J., Canan, B. D., Liyanarachchi, S., Bal, N. C., Pant, M., Periasamy, M., Li, Q., Janssen, P. M. L., & D, D. C. G. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201108118 · Cited by 69 · see citing works
The TWEAK-Fn14 pathway: A potent regulator of skeletal muscle biology in health and disease
Tajrishi, M. M., Zheng, T. S., Burkly, L. C., & Kumar, A. (2013) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2013.12.004 · Cited by 68 · see citing works
Optimizing IGF-I for skeletal muscle therapeutics
Philippou, Α., & Barton, E. R. (2014) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2014.06.003 · Cited by 67 · see citing works
Alvarez, B., Quinn, L. S., Busquets, S., Quiles, M., López-Soriano, F. J., & Argilés, J. M. A. (2002) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(01)00167-7 · Cited by 66 · see citing works
Villena, J., & Brandan, E. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10422 · Cited by 63 · see citing works
Enwere, E. K., LaCasse, E. C., Adam, N., & Korneluk, R. G. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00034 · Cited by 62 · see citing works
Single Muscle Fiber Gene Expression with Run Taper
Murach, K. A., Raue, U., Wilkerson, B. S., Minchev, K., Jemioło, B., Bagley, J. R., Luden, N. D., & Trappe, S. W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108547 · Cited by 61 · see citing works
Molecular mechanisms of hepatic apoptosis regulated by nuclear factors
Wang, K. (2014) · Cellular Signalling · doi:10.1016/j.cellsig.2014.11.038 · Cited by 56 · see citing works
Kurosaka, M., Naıto, H., Ogura, Y., Machida, S., & Katamoto, S. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02381.x · Cited by 54 · see citing works
Brown, S. A. N., Cheng, E., Williams, M. S., & Winkles, J. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065248 · Cited by 48 · see citing works
Skeletal muscle regeneration involves macrophage-myoblast bonding
Ceafalan, L. C., Fertig, T. E., Popescu, A. C., Popescu, B. O., Hinescu, M. E., & Gherghiceanu, M. (2017) · Cell Adhesion & Migration · doi:10.1080/19336918.2017.1346774 · Cited by 46 · see citing works
Raue, U., Jemioło, B., Yang, Y., & Trappe, S. W. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00759.2014 · Cited by 44 · see citing works
Ogura, Y., Mishra, V. K., Hindi, S. M., Kuang, S., & Kumar, A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.517300 · Cited by 43 · see citing works
Glucocorticoids increase skeletal muscle NF ‐κB inducing kinase ( NIK ): links to muscle atrophy
Fry, C. S., Nayeem, S. Z., Dillon, E. L., Sarkar, P. S., Tumurbaatar, B., Urban, R. J., Wright, T. J., Sheffield‐Moore, M., Tilton, R. G., & Choudhary, S. (2016) · Physiological Reports · doi:10.14814/phy2.13014 · Cited by 42 · see citing works
Self-citationSamaan, M. C., Marcinko, K., Sikkema, S. R., Fullerton, M. D., Ziafazeli, T., Khan, M. I., & Steinberg, G. R. (2014) · Physiological Reports · doi:10.14814/phy2.12012 · Cited by 41 · see citing works
Walton, R. G., Finlin, B. S., Mula, J., Long, D. E., Zhu, B., Fry, C. S., Westgate, P. M., Lee, J. D., Bennett, T., Kern, P. A., et al. (2015) · Physiological Reports · doi:10.14814/phy2.12415 · Cited by 33 · see citing works
Self-citationMurach, K. A., Walton, R. G., Fry, C. S., Michaelis, S. L., Groshong, J. S., Finlin, B. S., Kern, P. A., & Peterson, C. A. (2016) · Physiological Reports · doi:10.14814/phy2.12973 · Cited by 30 · see citing works
Self-citationYamaguchi, A., Ishii, H., Morita, I., Oota, I., & Takeda, H. (2004) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-004-1282-5 · Cited by 29 · see citing works
Satellite cell response to erythropoietin treatment and endurance training in healthy young men
Hoedt, A., Christensen, B., Nellemann, B., Mikkelsen, U. R., Hansen, M., Schjerling, P., & Farup, J. (2015) · The Journal of Physiology · doi:10.1113/jp271333 · Cited by 25 · see citing works
Tanaka, Y., Yamaguchi, A., Fujikawa, T., et al. (2008) · Acta Physiologica · doi:10.1111/j.1748-1716.2008.01866.x · Cited by 22 · see citing works
Sawano, S., Suzuki, T., Do, M. Q., Ohtsubo, H., Mizunoya, W., Ikeuchi, Y., & Tatsumi, R. (2014) · Animal Science Journal · doi:10.1111/asj.12264 · Cited by 20 · see citing works
Response of macrophages in rat skeletal muscle after eccentric exercise
Zuo, Q., Wang, S., Yu, X., & Chao, W. (2018) · Chinese journal of traumatology = Zhonghua chuang shang za zhi · doi:10.1016/j.cjtee.2017.12.001 · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Roberts, M. D., McCarthy, J. J., Hornberger, T. A., Phillips, S. M., Mackey, A. L., Nader, G. A., Boppart, M. D., Kavazis, A. N., Reidy, P. T., Ogasawara, R., et al. (2023) · Physiological Reviews · doi:10.1152/physrev.00039.2022 · Cited by 214 · see citing works
Walton, R. G., Dungan, C. M., Long, D. E., Tuggle, S. C., Kosmac, K., Peck, B. D., Bush, H. M., Villasante Tezanos, A. G., McGwin, G., Windham, S. T., et al. (2019) · Aging Cell · doi:10.1111/acel.13039 · Cited by 210 · see citing works
Self-citationFusion and beyond: Satellite cell contributions to loading-induced skeletal muscle adaptation
Murach, K. A., Fry, C. S., Dupont‐Versteegden, E. E., McCarthy, J. J., & Peterson, C. A. (2021) · The FASEB Journal · doi:10.1096/fj.202101096r · Cited by 120 · see citing works
Self-citationExercise Counters the Age-Related Accumulation of Senescent Cells
Zhang, X., Englund, D. A., Aversa, Z., Jachim, S. K., White, T. A., & LeBrasseur, N. K. (2022) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000302 · Cited by 63 · see citing works
Glucagon-like peptide-1 receptor agonists and muscle mass effects
Ceasovschih, A., Asaftei, A., Lupo, M. G., Kotlyarov, S., Bartušková, H., Balta, A., Sorodoc, V., Sorodoc, L., & Banach, M. (2025) · Pharmacological Research · doi:10.1016/j.phrs.2025.107927 · Cited by 64 · see citing works
Age-associated inflammation and implications for skeletal muscle responses to exercise
Kunz, H. E., & Lanza, I. R. (2023) · Experimental Gerontology · doi:10.1016/j.exger.2023.112177 · Cited by 56 · see citing works
- Authors
- Walton, R. G., Kosmac, K., Mula, J., Fry, C. S., Peck, B. D., Groshong, J. S., Finlin, B. S., Zhu, B., Kern, P. A., & Peterson, C. A.
- Affiliations
- University of Kentucky (US)
- The University of Texas Medical Branch at Galveston (US)
- University of Central Florida (US)
- Corresponding author
- Walton, R. Grace
- ORCID
- Venue
- Scientific Reports
- Published
- 2019-01-30
- Volume
- 9
- Issue
- 1
- Pages
- 969-969
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC6353900
- OpenAlex
- W2911336809
- Cited by
- 97
- References
- 88
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 17 · 2023: 7 · 2022: 13 · 2021: 16 · 2020: 13 · 2019: 9
- FWCI
- 8.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UKnowledge (University of Kentucky) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (071349)
- U.S. Department of Health & Human Services | NIH | National Center for Advancing Translational Sciences (UL1TR001998)
- U.S. Department of Health & Human Services | NIH | National Institute on Aging (046920)
- Topics
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- endurance training, resistance training, M2 macrophages, M2c macrophages, muscle fiber hypertrophy, satellite cells, Fn14, C/EBPβ, MurF, interleukin-6, insulin-like growth factor I, extracellular matrix, muscle growth, vastus lateralis
- MeSH terms
- Adaptation, Physiological, Adult, Aged, Female, Fibronectins, Gene Expression Regulation, Humans, Inflammation, Macrophages, Male, Middle Aged, Muscle Proteins, Physical Endurance, Muscle, Skeletal, Muscle Fibers, Skeletal, CCAAT-Enhancer-Binding Protein-beta, Satellite Cells, Skeletal Muscle, Resistance Training
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