Apoptosis in capillary endothelial cells in ageing skeletal muscle
Open accessAbstract
The age-related loss of skeletal muscle mass and function (sarcopenia) is a consistent hallmark of ageing. Apoptosis plays an important role in muscle atrophy, and the intent of this study was to specify whether apoptosis is restricted to myofibre nuclei (myonuclei) or occurs in satellite cells or stromal cells of extracellular matrix (ECM). Sarcopenia in mouse gastrocnemius muscle was characterized by myofibre atrophy, oxidative type grouping, delocalization of myonuclei and ECM fibrosis. Terminal deoxynucleotidyl transferase-mediated dUTP nick end-labelling (TUNEL) indicated a sharp rise in apoptosis during ageing. TUNEL coupled with immunostaining for dystrophin, paired box protein-7 (Pax7) or laminin-2α, respectively, was used to identify apoptosis in myonuclei, satellite cells and stromal cells. In adult muscle, apoptosis was not detected in myofibres, but was restricted to stromal cells. Moreover, the age-related rise in apoptotic nuclei was essentially due to stromal cells. Myofibre-associated apoptosis nevertheless occurred in old muscle, but represented < 20% of the total muscle apoptosis. Specifically, apoptosis in old muscle affected a small proportion (0.8%) of the myonuclei, but a large part (46%) of the Pax7(+) satellite cells. TUNEL coupled with CD31 immunostaining further attributed stromal apoptosis to capillary endothelial cells. Age-dependent rise in apoptotic capillary endothelial cells was concomitant with altered levels of key angiogenic regulators, perlecan and a perlecan domain V (endorepellin) proteolytic product. Collectively, our results indicate that sarcopenia is associated with apoptosis of satellite cells and impairment of capillary functions, which is likely to contribute to the decline in muscle mass and functionality during ageing.
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?
Key angiogenic regulators and endothelial cell content in skeletal muscle are reduced during aging.
“Key angiogenic regulators and endothelial cell content in skeletal muscle are reduced during aging.”
From Skeletal muscle aging, cellular senescence, and senotherapeutics: current knowledge and future directions (2021) · cites this paper as Wang et al., 2014
Declines in skeletal muscle perfusion may directly influence anabolic resistance and contribute to sarcopenia.
“Corresponding declines in skeletal muscle perfusion may directly influence anabolic resistance and contribute to sarcopenia”
From Skeletal muscle aging, cellular senescence, and senotherapeutics: current knowledge and future directions (2021) · cites this paper as Wang et al., 2014
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
Woessner, J. F. (1961) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(61)90291-0 · Cited by 3,851 · see citing works
Lamberts, S. W. J., van den Beld, A. W., & van der Lely, A.-J. (1997) · Science · doi:10.1126/science.278.5337.419 · Cited by 980 · see citing works
Muscle Satellite Cells and Endothelial Cells: Close Neighbors and Privileged Partners
Christov, C., Chrétien, F. C., Abou-Khalil, R., Bassez, G., Vallet, G., Authier, F., Bassaglia, Y., Shinin, V., Tajbakhsh, S., Chazaud, B., et al. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-08-0693 · Cited by 702 · see citing works
Stem and Progenitor Cells in Skeletal Muscle Development, Maintenance, and Therapy
Péault, B., Rudnicki, M. A., Torrente, Y., Cossu, G., Tremblay, J. P., Partridge, T. A., Gussoni, E., Kunkel, L. M., & Huard, J. (2007) · Molecular Therapy · doi:10.1038/mt.sj.6300145 · Cited by 572 · see citing works
Satellite-cell pool size does matter: Defining the myogenic potency of aging skeletal muscle
Shefer, G., de Mark, D. P. V., Richardson, J. B., & Yablonka‐Reuveni, Z. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.02.022 · Cited by 506 · see citing works
Valdez, G., Tapia, J. C., Kang, H., Clemenson, G. D., Gage, F. H., Lichtman, J. W., & Sanes, J. R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002220107 · Cited by 502 · see citing works
Morgan, J. E., & Partridge, T. A. (2003) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(03)00042-6 · Cited by 438 · see citing works
Allen, D. L., Linderman, J. K., Roy, R. R., Bigbee, A. J., Grindeland, R. E., Mukku, V. R., & Edgerton, V. R. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.273.2.c579 · Cited by 364 · see citing works
Tullberg-Reinert, H., & Jundt, G. (1999) · Histochemistry and Cell Biology · doi:10.1007/s004180050447 · Cited by 330 · see citing works
Endothelial dysfunction and aging: An update
Herrera, M. D., Mingorance, C., Rodríguez‐Rodríguez, R., & de Sotomayor, M. Á. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2009.07.002 · Cited by 322 · see citing works
A Population of Myogenic Stem Cells That Survives Skeletal Muscle Aging
Collins, C. A., Zammit, P. S., Ruiz, A. P., Morgan, J. E., & Partridge, T. A. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0372 · Cited by 320 · see citing works
Regenerative potential of human skeletal muscle during aging
Renault, V. M., Thorne, L., Eriksson, P., Butler-Browne, G. S., & Mouly, V. (2002) · Aging Cell · doi:10.1046/j.1474-9728.2002.00017.x · Cited by 318 · see citing works
Muscle fibre type adaptation in the elderly human muscle
Andersen, J. L. (2003) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1034/j.1600-0838.2003.00299.x · Cited by 316 · see citing works
Diverse Cell Signaling Events Modulated by Perlecan
Whitelock, J. M., Melrose, J., & Iozzo, R. V. (2008) · Biochemistry · doi:10.1021/bi8013938 · Cited by 270 · see citing works
Ibebunjo, C., Chick, J. M., Kendall, T., Eash, J. K., Li, C., Zhang, Y., Vickers, C., Wu, Z., Clarke, B. A., Shi, J., et al. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01036-12 · Cited by 267 · see citing works
Caspase 3/caspase-activated DNase promote cell differentiation by inducing DNA strand breaks
Larsen, B. D., Rampalli, S., Burns, L. E., Brunette, S., Dilworth, F. J., & Megeney, L. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913089107 · Cited by 242 · see citing works
Kragstrup, T. W., Kjær, M., & Mackey, A. L. (2011) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2011.01377.x · Cited by 241 · see citing works
The number of nuclei in adult rat muscles with special reference to satellite cells
Schmalbruch, H., & Hellhammer, U. (1977) · The Anatomical Record · doi:10.1002/ar.1091890204 · Cited by 234 · see citing works
Basement Membrane Proteoglycans: Modulators Par Excellence of Cancer Growth and Angiogenesis
Iozzo, R. V., Zoeller, J. J., & Nyström, A. (2009) · Molecules and Cells · doi:10.1007/s10059-009-0069-0 · Cited by 221 · see citing works
PECAM-1: Conflicts of interest in inflammation
Privratsky, J. R., Newman, D. K., & Newman, P. J. (2010) · Life Sciences · doi:10.1016/j.lfs.2010.06.001 · Cited by 205 · see citing works
Evidence for Nervous System Degeneration with Advancing Age
Lexell, J. E. (1997) · Journal of Nutrition · doi:10.1093/jn/127.5.1011s · Cited by 199 · see citing works
Peripheral Vascular Endothelial Dysfunction and Apoptosis in Old Monkeys
Asai, K., Kudej, R. K., Shen, Y.-T., Yang, G.-P., Takagi, G., Kudej, A. B., Geng, Y., Sato, N., Nazareno, J. B., Vatner, D. E., et al. (2000) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.20.6.1493 · Cited by 189 · see citing works
Differential proteome analysis of aging in rat skeletal muscle
Piec, I., Listrat, A., Alliot, J., Chambon, C., Taylor, R. G., & Béchet, D. (2005) · The FASEB Journal · doi:10.1096/fj.04-3084fje · Cited by 181 · see citing works
The muscle satellite cell at 50: the formative years
Scharner, J., & Zammit, P. S. (2011) · Skeletal Muscle · doi:10.1186/2044-5040-1-28 · Cited by 180 · see citing works
In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy
Bruusgaard, J. C., & Gundersen, K. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34022 · Cited by 162 · see citing works
Skeletal muscle proteolysis in aging
Combaret, L., Dardevet, D. P., Béchet, D., Taillandier, D., Mosoni, L., & Attaix, D. (2008) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32831b9c31 · Cited by 152 · see citing works
Distribution of myonuclei and microtubules in live muscle fibers of young, middle-aged, and old mice
Bruusgaard, J. C., Liestøl, K., & Gundersen, K. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00913.2005 · Cited by 144 · see citing works
Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice
Shavlakadze, T., McGeachie, J. K., & Grounds, M. D. (2009) · Biogerontology · doi:10.1007/s10522-009-9260-0 · Cited by 135 · see citing works
Aging increases the susceptibility of skeletal muscle derived satellite cells to apoptosis
Jejurikar, S. S., Henkelman, E., Cederna, P. S., Marcelo, C. L., Urbanchek, M. G., & Kuzon, W. M. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.06.053 · Cited by 133 · see citing works
Apoptosis of Skeletal Muscle Myofibers and Interstitial Cells in Experimental Heart Failure
Vescovo, G., Zennaro, R., Sandri, M., Carraro, U., Leprotti, C., Ceconi, C., Ambrosio, G. B., & Libera, L. D. (1998) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1998.0807 · Cited by 127 · see citing works
Yablonka‐Reuveni, Z., & Anderson, J. E. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20602 · Cited by 123 · see citing works
Apoptotic myonuclei in human Duchenne muscular dystrophy.
Sandri, M., Minetti, C., Pedemonte, M., & Carraro, U. (1998) · PubMed · Cited by 112 · see citing works
Laplante, P., Raymond, M., Gagnon, G., Vigneault, N., Sasseville, A. M.-J., Langelier, Y., Bernard, M., Raymond, Y., & Hébert, M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.9.5740 · Cited by 109 · see citing works
Apoptosis of myofibres and satellite cells: exercise‐induced damage in skeletal muscle of the mouse
Podhorska‐Okolow, Sandri, Zampieri, Brun, Rossini, & Carraro, U. (1998) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.1998.00149.x · Cited by 103 · see citing works
Apoptosis Occurs in Endothelial Cells during Hypertension-Induced Microvascular Rarefaction
Gobe, G. C., Browning, J., Howard, T., Hogg, N., Winterford, C. M., & Cross, R. B. (1997) · Journal of Structural Biology · doi:10.1006/jsbi.1996.3835 · Cited by 89 · see citing works
Clinical and molecular overlap between myopathies and inherited connective tissue diseases
Voermans, N. C., Bönnemann, C. G., Huijing, P. A., Hamel, B. C. J., Kuppevelt, T. H. V., HAAN, A. D., Schalkwijk, J., van Engelen, B. G. M., & Jenniskens, G. J. (2008) · Neuromuscular Disorders · doi:10.1016/j.nmd.2008.05.017 · Cited by 89 · see citing works
Alsharidah, M. S., Lazarus, N. R., George, T., Agley, C. C., Velloso, C. P., & Harridge, S. D. R. (2013) · Aging Cell · doi:10.1111/acel.12051 · Cited by 85 · see citing works
Endothelial dysfunction and vascular disease in later life
Virdis, A., Ghiadoni, L., Giannarelli, C., & Taddei, S. (2010) · Maturitas · doi:10.1016/j.maturitas.2010.04.006 · Cited by 79 · see citing works
Multiple Pathways to the Same End: Mechanisms of Myonuclear Apoptosis in Sarcopenia of Aging
Marzetti, E., Privitera, G., Simili, V., Wohlgemuth, S. E., Aulisa, L., Pahor, M., & Leeuwenburgh, C. (2010) · The Scientific World JOURNAL · doi:10.1100/tsw.2010.27 · Cited by 74 · see citing works
Cell proliferation in denervated muscle: Time course, distribution and relation to disuse
Murray, M. A., & Robbins, N. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90039-2 · Cited by 73 · see citing works
Rees, M. D., Whitelock, J. M., Malle, E., Chuang, C. Y., Iozzo, R. V., Nilasaroya, A., & Davies, M. J. (2009) · Matrix Biology · doi:10.1016/j.matbio.2009.09.005 · Cited by 64 · see citing works
Expression and modification proteomics during skeletal muscle ageing
Baraibar, M. A., Gueugneau, M., Duguez, S., Butler-Browne, G. S., Béchet, D., & Friguet, B. (2013) · Biogerontology · doi:10.1007/s10522-013-9426-7 · Cited by 49 · see citing works
Tenascin-X increases the stiffness of collagen gels without affecting fibrillogenesis
Margaron, Y., Bostan, L. E., Exposito, J., Malbouyres, M., Trunfio-Sfarghiu, A.-M., Berthier, Y., & Lethias, C. (2010) · Biophysical Chemistry · doi:10.1016/j.bpc.2009.12.011 · Cited by 46 · see citing works
Malmgren, L. T., Jones, C. E., & Bookman, L. M. (2001) · Otolaryngology · doi:10.1067/mhn.2001.116449 · Cited by 39 · see citing works
Yarovaya, N., Kramarova, L., Borg, J., Kovalenko, S. A., Caragounis, A., & Linnane, A. W. (2002) · Biogerontology · doi:10.1023/a:1015295011131 · Cited by 20 · see citing works
Resende, M., Amaral, S. L., Munzenmaier, D. H., & Greene, A. S. (2006) · Physiological Genomics · doi:10.1152/physiolgenomics.00253.2005 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sarcopenia: Aging-Related Loss of Muscle Mass and Function
Larsson, L., Degens, H., Li, M., Salviati, L., Lee, Y. I., Thompson, W., Kirkland, J. L., & Sandri, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00061.2017 · Cited by 1,797 · see citing works
Impairment of an endothelial NAD(+)-H2S signaling network is a reversible cause of vascular aging
Das, A., Huang, G. X., Bonkowski, M. S., Longchamp, A., Li, C., Schultz, M. B., Kim, L.-J., Osborne, B., Joshi, S., Lu, Y., et al. (2018) · Cell · doi:10.1016/j.cell.2018.02.008 · Cited by 496 · see citing works
“For reasons that are unclear, as we age there is an increase in muscle EC apoptosis, decreased neovascularization, and blood vessel loss (Groen et al., 2014; Wang et al., 2014), resulting in reduced muscle mass (sarcopenia) and a decline in strength and endurance in the later decades of life, even with exercise (Denis…”
Age-related Impairment of Vascular Structure and Functions
Xu, X., Wang, B. Z., Ren, C., Hu, J., Greenberg, D. A., Chen, T., Xie, L., & Jin, K. (2017) · Aging and Disease · doi:10.14336/ad.2017.0430 · Cited by 351 · see citing works
Fan, J., Yang, X., Li, J., Shu, Z., Dai, J., Liu, X., Li, B., Jia, S., Kou, X., Yang, Y., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.15728 · Cited by 179 · see citing works
Hong, W., Mo, F., Zhang, Z., Huang, M., & Wei, X. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00246 · Cited by 179 · see citing works
Prior, S. J., Ryan, A. S., Blumenthal, J. B., Watson, J. M., Katzel, L. I., & Goldberg, A. P. (2016) · The Journals of Gerontology Series A · doi:10.1093/gerona/glw017 · Cited by 140 · see citing works
The role of the microcirculation in muscle function and plasticity
Hendrickse, P. W., & Degens, H. (2019) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-019-09520-2 · Cited by 137 · see citing works
Skeletal Muscle Microvasculature: A Highly Dynamic Lifeline
Latroche, C., Gitiaux, C., Chrétien, F., Desguerre, I., Mounier, R., & Chazaud, B. (2015) · Physiology · doi:10.1152/physiol.00026.2015 · Cited by 134 · see citing works
Endostatin and endorepellin: A common route of action for similar angiostatic cancer avengers
Poluzzi, C., Iozzo, R. V., & Schaefer, L. (2015) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.10.012 · Cited by 133 · see citing works
Decoding the Matrix: Instructive Roles of Proteoglycan Receptors
Neill, T., Schaefer, L., & Iozzo, R. V. (2015) · Biochemistry · doi:10.1021/acs.biochem.5b00653 · Cited by 130 · see citing works
Treatment of hind limb ischemia using angiogenic peptide nanofibers
Kumar, V., Liu, Q., Wickremasinghe, N. C., Shi, S., Cornwright, T. T., Deng, Y., Azares, A. R., Moore, A. N., Acevedo‐Jake, A. M., Agudo, N. R., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.04.032 · Cited by 106 · see citing works
Englund, D. A., Zhang, X., Aversa, Z., & LeBrasseur, N. K. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111595 · Cited by 94 · see citing works
Hierarchical Mechanics of Connective Tissues: Integrating Insights from Nano to Macroscopic Studies
Goh, K. L., Listrat, A., & Béchet, D. (2014) · Journal of Biomedical Nanotechnology · doi:10.1166/jbn.2014.1960 · Cited by 88 · see citing works
Proteomics of muscle chronological ageing in post-menopausal women
Gueugneau, M., Coudy‐Gandilhon, C., Gourbeyre, O., Chambon, C., Combaret, L., Polge, C., Taillandier, D., Attaix, D., Friguet, B., Maier, A. B., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1165 · Cited by 82 · see citing works
Douglass, S. M., Goyal, A. K., & Iozzo, R. V. (2015) · Connective Tissue Research · doi:10.3109/03008207.2015.1045297 · Cited by 68 · see citing works
Catechins enhance skeletal muscle performance
Li, P., Liu, A., Xiong, W., Lin, H., Xiao, W., Huang, J., Zhang, S., & Liu, Z. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1549534 · Cited by 67 · see citing works
Endothelial Piezo1 sustains muscle capillary density and contributes to physical activity
Bartoli, F., Debant, M., Chuntharpursat‐Bon, E., Evans, E. L., Musialowski, K. E., Parsonage, G., Morley, L. C., Futers, T. S., Sukumar, P., Bowen, T. S., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci141775 · Cited by 65 · see citing works
Vascular Ageing and Exercise: Focus on Cellular Reparative Processes
Ross, M., Malone, E. M., & Florida-James, G. D. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/3583956 · Cited by 56 · see citing works
Goh, K. L., & Holmes, D. F. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18050901 · Cited by 56 · see citing works
Metabolic Regulation of Angiogenesis in Diabetes and Aging
Sawada, N., & Arany, Z. P. (2017) · Physiology · doi:10.1152/physiol.00039.2016 · Cited by 52 · see citing works
Moore, D. R., Kelly, R. P., Devries, M. C., Churchward‐Venne, T. A., Phillips, S. M., Parise, G., & Johnston, A. P. (2018) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12306 · Cited by 50 · see citing works
Molecular mechanisms and therapeutic interventions in sarcopenia
Park, S. S., Kwon, E., & Kwon, K. (2017) · Osteoporosis and Sarcopenia · doi:10.1016/j.afos.2017.08.098 · Cited by 51 · see citing works
Giacomello, E., Crea, E., Torelli, L., Bergamo, A., Reggiani, C., Sava, G., & Toniolo, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113923 · Cited by 48 · see citing works
Kargl, C. K., Nie, Y., Evans, S., Stout, J., Shannahan, J. H., Kuang, S., & Gavin, T. P. (2019) · The Journal of Physiology · doi:10.1113/jp278165 · Cited by 37 · see citing works
Muscle Proteomic and Transcriptomic Profiling of Healthy Aging and Metabolic Syndrome in Men
Gueugneau, M., Coudy‐Gandilhon, C., Chambon, C., Verney, J., Taillandier, D., Combaret, L., Polge, C., Walrand, S., Roche, F., Barthélemy, J., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084205 · Cited by 37 · see citing works
Lower skeletal muscle capillarization in hypertensive elderly men
Gueugneau, M., Coudy‐Gandilhon, C., Meunier, B., Combaret, L., Taillandier, D., Polge, C., Attaix, D., Roche, F., Féasson, L., Barthélemy, J., et al. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.01.013 · Cited by 36 · see citing works
Endothelial Regenerative Capacity and Aging: Influence of Diet, Exercise and Obesity
Ross, M. (2018) · Current Cardiology Reviews · doi:10.2174/1573403x14666180726112303 · Cited by 33 · see citing works
Engineering complex muscle-tissue interfaces through microfabrication
Arrigoni, C., Petta, D., Bersini, S., Mironov, V., Candrian, C., & Moretti, M. (2019) · Biofabrication · doi:10.1088/1758-5090/ab1e7c · Cited by 33 · see citing works
MW Laschke, C. G., Laschke, M. W., Gräßer, C., Kleer, S., Scheuer, C., Eglin, D., Alini, M., & Menger, M. (2014) · European Cells and Materials · doi:10.22203/ecm.v028a20 · Cited by 33 · see citing works
The Importance of Muscle Capillarization for Optimizing Satellite Cell Plasticity
Nederveen, J. P., Betz, M. W., Snijders, T., & Parise, G. (2021) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000270 · Cited by 32 · see citing works
Betz, M. W., Aussieker, T., Kruger, C. Q., Gorissen, S. H. M., van Loon, L. J. C., & Snijders, T. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111161 · Cited by 29 · see citing works
Bigler, M. R., Koutsantonis, D., Odriozola, A., Halm, S., Tschanz, S. A., Zakrzewicz, A., Weichert, A., & Baum, O. (2016) · Acta Physiologica · doi:10.1111/apha.12709 · Cited by 30 · see citing works
Shimizu, Y., Sato, S., Koyamatsu, J., Yamanashi, H., Nagayoshi, M., Kadota, K., Kawashiri, S., Inoue, K., Nagata, Y., & Maeda, T. (2017) · Oncotarget · doi:10.18632/oncotarget.20618 · Cited by 28 · see citing works
Differential gene expression analysis in ageing muscle and drug discovery perspectives
Melouane, A., Ghanemi, A., Aubé, S., Yoshioka, M., & St‐Amand, J. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.10.006 · Cited by 27 · see citing works
Bagley, J. R., & Galpin, A. J. (2015) · Biochemistry and Molecular Biology Education · doi:10.1002/bmb.20891 · Cited by 26 · see citing works
Valencia, Á., & Torres, F. (2016) · Journal of Mechanics in Medicine and Biology · doi:10.1142/s021951941750018x · Cited by 26 · see citing works
Possible-sarcopenic screening with disturbed plasma amino acid profile in the elderly
Duan, Y., Tao, K., Fang, Z., & Lu, Y. (2023) · BMC Geriatrics · doi:10.1186/s12877-023-04137-0 · Cited by 26 · see citing works
Ginkgolide B increases healthspan and lifespan of female mice
Lee, C., Wang, B. Y., Wong, S. H., Chen, Y., Cao, Q., Hsiao, A. W., Fung, S.-H., Chen, Y.-F., Wu, H.-H., Cheng, P.-Y., et al. (2025) · Nature Aging · doi:10.1038/s43587-024-00802-0 · Cited by 24 · see citing works
Lopes, K. G., Farinatti, P., Bottino, D. A., de Souza, M. D. G. C., Maranhao, P. A., Bouskela, E., Lourenço, R. A., & Oliveira, R. B. (2021) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-211202 · Cited by 24 · see citing works
Castillo-Mariqueo, L., Pérez‐García, M. J., & Giménez‐Llort, L. (2021) · Biomedicines · doi:10.3390/biomedicines9101365 · Cited by 23 · see citing works
Madsen, A. B., Knudsen, J. R., Henríquez‐Olguín, C., Angın, Y., Zaal, K. J. M., Sylow, L., Schjerling, P., Ralston, E., & Jensen, T. E. (2018) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00392.2017 · Cited by 22 · see citing works
Single‐cell RNA‐seq reveals interferon‐induced guanylate‐binding proteins are linked with sarcopenia
Peng, Z. Y., Zhang, R., Kuang, X., Chen, Y., Niu, S., Du, Y., Lu, D., Li, S., Teng, Z., & Lu, S. (2022) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13091 · Cited by 21 · see citing works
Effect of the Lipoxygenase Inhibitor Baicalein on Muscles in Ovariectomized Rats
Saul, D., Kling, J. H., Kosinsky, R. L., Hoffmann, D. B., Komrakova, M., Wicke, M., Menger, B., & Sehmisch, S. (2016) · Journal of Nutrition and Metabolism · doi:10.1155/2016/3703216 · Cited by 21 · see citing works
NAD+: An old but promising therapeutic agent for skeletal muscle ageing
Xu, Y., & Xiao, W. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102106 · Cited by 19 · see citing works
A high-resolution view of the heterogeneous aging endothelium
Dobner, S., Tóth, F., & de Rooij, L. P. M. H. (2024) · Angiogenesis · doi:10.1007/s10456-023-09904-6 · Cited by 21 · see citing works
Dalle, C., Ostermann, A. I., Konrad, T., Coudy‐Gandilhon, C., Decourt, A., Barthélemy, J., Roche, F., Féasson, L., Mazur, A., Béchet, D., et al. (2018) · The Journals of Gerontology Series A · doi:10.1093/gerona/gly187 · Cited by 18 · see citing works
Dong, L., Gan, L., Wang, H., & Cai, W. (2019) · Medical Science Monitor · doi:10.12659/msm.916287 · Cited by 17 · see citing works
Ghanemi, A., Yoshioka, M., & St‐Amand, J. (2023) · Diseases · doi:10.3390/diseases11010033 · Cited by 17 · see citing works
Cardiovascular Disease and Aging
Chiao, Y. A., Lakatta, E. G., Ungvari, Z. I., Dai, D., & Rabinovitch, P. S. (2015) · Springer eBooks · doi:10.1007/978-3-319-23246-1_5 · Cited by 15 · see citing works
The Effect of Metabolites on Mitochondrial Functions in the Pathogenesis of Skeletal Muscle Aging
Gu, X., Wang, W., Yang, Y., Lei, Y., Liu, D., Wang, X., & Wu, T. (2022) · Clinical Interventions in Aging · doi:10.2147/cia.s376668 · Cited by 14 · see citing works
Link between blood flow and muscle protein metabolism in elderly adults
Zempo, H., Isobe, M., & Naito, H. (2017) · The Journal of Physical Fitness and Sports Medicine · doi:10.7600/jpfsm.6.25 · Cited by 14 · see citing works
AXIN1 knockout does not alter AMPK/mTORC1 regulation and glucose metabolism in mouse skeletal muscle
Li, J., Knudsen, J. R., Henríquez‐Olguín, C., Li, Z., Birk, J. B., Persson, K. W., Hellsten, Y., Offergeld, A., Jarassier, W., Grand, F. L., et al. (2021) · The Journal of Physiology · doi:10.1113/jp281187 · Cited by 14 · see citing works
Lal, N. N., Cornwall, J., & Sheard, P. W. (2021) · Experimental Gerontology · doi:10.1016/j.exger.2021.111618 · Cited by 14 · see citing works
Shimizu, Y., Sato, S., Noguchi, Y., Koyamatsu, J., Yamanashi, H., Higashi, M., Nagayoshi, M., Kawashiri, S., Nagata, Y., Takamura, N., et al. (2018) · Environmental Health and Preventive Medicine · doi:10.1186/s12199-018-0720-5 · Cited by 14 · see citing works
Thermal injury initiates pervasive fibrogenesis in skeletal muscle
Brightwell, C. R., Hanson, M. E., Ayadi, A. E., Prasai, A., Wang, Y., Finnerty, C. C., & Fry, C. S. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00337.2019 · Cited by 13 · see citing works
Perlecan: a review of its role in neurologic and musculoskeletal disease
Lavorgna, T., Gressett, T., Chastain, W., & Bix, G. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1189731 · Cited by 13 · see citing works
Spangenberg, A., Maghsoodi, N., Dulnoan, D., Moore, A. E. B., Edwards, S. F., Frost, M. L., & Hampson, G. (2016) · Calcified Tissue International · doi:10.1007/s00223-016-0186-7 · Cited by 13 · see citing works
Organotypic cultures as aging associated disease models
Sanchez, M. M., Bagdasarian, I. A., Darch, W., & Morgan, J. T. (2022) · Aging · doi:10.18632/aging.204361 · Cited by 12 · see citing works
SIMULATION OF MUSCLE ACTIVATION WITH COUPLED NONLINEAR FE MODELS
Li, F., Li, H., HU, W., Su, S., & Wang, B. (2016) · Journal of Mechanics in Medicine and Biology · doi:10.1142/s0219519416500822 · Cited by 11 · see citing works
Knudsen, J. R., Madsen, A. B., Li, Z., Andersen, N. R., Schjerling, P., & Jensen, T. E. (2022) · Physiological Reports · doi:10.14814/phy2.15183 · Cited by 10 · see citing works
Nyúl‐Tóth, Á., Shanmugarama, S., Patai, R., Gulej, R., Faakye, J., Nagy, D., Nagykaldi, M., Kiss, T., Csípő, T., Milan, M., et al. (2025) · GeroScience · doi:10.1007/s11357-025-01653-2 · Cited by 10 · see citing works
Wang, N., Zheng, A., Yan, Y., He, T., Wu, X., Xian, M., Luo, J., Li, C., Wei, J., Wang, Y., et al. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.07.004 · Cited by 10 · see citing works
Shimizu, Y., Yamanashi, H., Fukui, S., Kawashiri, S., Nagata, Y., & Maeda, T. (2021) · Scientific Reports · doi:10.1038/s41598-020-80163-x · Cited by 10 · see citing works
Role of Growth Factors in Modulation of the Microvasculature in Adult Skeletal Muscle
Smythe, G. M. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-27511-6_7 · Cited by 10 · see citing works
Rai, J., Pring, E. T., Knight, K. A., Tilney, H. S., Gudgeon, J., Gudgeon, M., Taylor, F., Gould, L. E., Wong, J., Andreani, S. M., et al. (2024) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13536 · Cited by 8 · see citing works
Combined angiogenic and hypertrophic gene therapy enhances skeletal muscle growth
Männistö, A., Tonttila, K., Ortega‐Alonso, A., Nurmi, H. J., Uusitalo‐Kylmälä, L., Hemanthakumar, K. A., Saikkala, E., Myllykangas, S., Vertainen, S., Nissinen, T. A., et al. (2025) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00966.2024 · Cited by 7 · see citing works
Quercetin prevents sarcopenia by reversing oxidative stress and mitochondrial damage
Sun, J., Liu, H., Yan, Y., & Fang, F. (2025) · Journal of Molecular Histology · doi:10.1007/s10735-025-10411-9 · Cited by 7 · see citing works
Potential Compensation among Group I PAK Members in Hindlimb Ischemia and Wound Healing
Elsherif, L., Özler, M., Zayed, M. A., Shen, J. H., Chernoff, J., Faber, J. E., & Parise, L. V. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112239 · Cited by 7 · see citing works
Challenging Sarcopenia: Exploring AdipoRon in Aging Skeletal Muscle as a Healthspan-Extending Shield
Selvais, C. M., de Carrizosa, M. A. D., Versele, R., Dubuisson, N., Noël, L., Brichard, S. M., & Abou‐Samra, M. (2024) · Antioxidants · doi:10.3390/antiox13091073 · Cited by 6 · see citing works
A Single Bout of Ultra-Endurance Exercise Reveals Early Signs of Muscle Aging in Master Athletes
Coudy‐Gandilhon, C., Gueugneau, M., Chambon, C., Taillandier, D., Combaret, L., Polge, C., Millet, G. Y., Féasson, L., & Béchet, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073713 · Cited by 5 · see citing works
Fujita, N., Hatakeyama, S., Momota, M., Tobisawa, Y., Yoneyama, T., Okamoto, T., Yamamoto, H., Yoneyama, T., Hashimoto, Y., Yoshikawa, K., et al. (2021) · The Aging Male · doi:10.1080/13685538.2021.2016690 · Cited by 4 · see citing works
Lacaze, L., Rochdi, S., Couvert, A., Touboulic, S., Guérin, S., Randuineau, G., Martin, D., Rome, V., Malbert, C., Derbré, F., et al. (2022) · Clinical Nutrition · doi:10.1016/j.clnu.2022.08.002 · Cited by 4 · see citing works
Lal, N. N., & Sheard, P. W. (2015) · Biogerontology · doi:10.1007/s10522-015-9565-0 · Cited by 3 · see citing works
A PASSIVE STATE SIMULATION OF AN ANAL SPHINCTER USING SIMMECHANICS
ATAXCA, B. N. R., García‐Beltrán, C. D., Lelis, J. M. R., Olivares-Peregrino, V. H., de la Concha-Bermejillo, F., & Castro, L. (2018) · Journal of Mechanics in Medicine and Biology · doi:10.1142/s0219519418500598 · Cited by 3 · see citing works
Chen, J.-Y., Chen, M., Liu, Y., Yao, M., Wang, X.-R., Chen, J., Zhang, J., Pan, M., Zhou, J., & Bai, Y.-P. (2026) · Acta Pharmacologica Sinica · doi:10.1038/s41401-025-01736-y · Cited by 2 · see citing works
Παπανικολάου, Κ., Yadav, A., Mankowski, R. T., Alexander, M. S., Gamboa, J. L., Thalacker‐Mercer, A. E., Dungan, C. M., & Englund, D. A. (2026) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00876.2025 · Cited by 2 · see citing works
Les effets musculaires de la vitamine D : application à la perte musculaire liée à l’âge
Walrand, S. (2014) · OCL · doi:10.1051/ocl/2014011 · Cited by 2 · see citing works
Huang, T., Shang, S., Wan, Q., Li, Q., Li, Y., Zheng, J.-N., & Chen, F.-X. (2025) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-025-05657-1 · Cited by 2 · see citing works
Shimizu, Y., Yamanashi, H., Noguchi, Y., Koyamatsu, J., Higashi, M., Fukui, S., Kawashiri, S., Arima, K., Takamura, N., & Maeda, T. (2020) · Dysphagia · doi:10.1007/s00455-020-10096-0 · Cited by 2 · see citing works
Molecular and cellular parameters of ageing: an overview
Thukral, H., Soin, S., Rani, R., & Sarkar, A. (2016) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 2 · see citing works
Genes in Skeletal Muscle Remodeling and Impact of Feeding
Chen, Y.-W., Barberio, M. D., & Hubal, M. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802167-5.00023-2 · Cited by 1 · see citing works
Aging in the Skeletal Muscle Revealed by Molecular Immunohistochemical Imaging
Malatesta, M., & Cisterna, B. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26135986 · Cited by 1 · see citing works
Les effets musculaires de la vitamine D : application à la perte musculaire liée à l’âge
Walrand, S. (2014) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2014.09.003 · Cited by 1 · see citing works
Dataset on transcriptome signature of skeletal muscle of young, adult and aged mice
Listrat, A., Goh, K. L., Jousse, C., Tounayre, J., Wang, H., Lee, K., & Béchet, D. (2022) · Data in Brief · doi:10.1016/j.dib.2022.108321 · Cited by 1 · see citing works
Jacques, E., Garcia, P., Mercier, O., Hu, Y., Dégletagne, C., Ravent, J., Fall, S., Almeida, M. P., Wheeler, A. R., Angers, S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.22.604619 · Cited by 1 · see citing works
Role of vascular plasticity in muscle remodeling in the child
Gitiaux, C. (2015) · theses.fr (ABES) · doi:10.70675/6a10c0d4z3afaz49efza017z843ffa5759f2
Rezaei, S., Matinhomaee, H., Azarbayjani, M. A., & Farzanegi, P. (2018) · journal of ilam university of medical sciences · doi:10.29252/sjimu.26.3.27
Viggars, M. R. (2018) · Liverpool John Moores University · doi:10.24377/researchonline.ljmu.ac.uk.00009368
Vitamin D Signaling and Skeletal Muscle Cells
Domingues-Faria, C., & Walrand, S. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-810422-4.00023-3
The Effect of DHT Treatment on Changes in Amino Acid Transport Occurring in Aged Muscle
Wendowski, O. (2018) · UEA Digital Repository (University of East Anglia)
Endorepellin downregulation promotes angiogenesis after experimental traumatic brain injury
Zhang, Q., Yao, J., Gong, Q., Cai, L., Wang, R., Yang, D., Wang, L., Qu, M., Chen, H., Tang, Y., et al. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.382861
Ultrastructural changes in the common carotid artery in terms of age and gender-related in Rat model
Ünlükal, N. (2025) · Revista Científica de la Facultad de Ciencias Veterinarias · doi:10.52973/rcfcv-e35516
Yamashita, Y., & Arikawa‐Hirasawa, E. (2026) · Trends in Glycoscience and Glycotechnology · doi:10.4052/tigg.2416.1e
Yamashita, Y., & Arikawa‐Hirasawa, E. (2026) · Trends in Glycoscience and Glycotechnology · doi:10.4052/tigg.2416.1j
Listrat, A., Jousse, C., Tournayre, J., Boby, C., Lee, K., Béchet, D., Wang, H., & Goh, K. L. (2026) · BMC Genomics · doi:10.1186/s12864-026-12677-z
- Authors
- Wang, H., Listrat, A., Meunier, B., Gueugneau, M., Coudy‐Gandilhon, C., Combaret, L., Taillandier, D., Polge, C., Attaix, D., Lethias, C., Lee, K., Goh, K. L., & Béchet, D.
- Affiliations
- Nanyang Technological University (SG)
- VetAgro Sup (FR)
- Université Clermont Auvergne (FR)
- Centre National de la Recherche Scientifique (FR)
- Newcastle University Singapore (SG)
- Corresponding author
- Taillandier, Daniel
- ORCID
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2013-11-19
- Volume
- 13
- Issue
- 2
- Pages
- 254-262
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC4331780
- OpenAlex
- W2107698649
- Cited by
- 109
- References
- 46
- Citations by year
- 2026: 8 · 2025: 8 · 2024: 4 · 2023: 5 · 2022: 9 · 2021: 9 · 2020: 7 · 2019: 7 · 2018: 12 · 2017: 9 · 2016: 12 · 2015: 11 · 2014: 8
- FWCI
- 4.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Aging Cell (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- DR-NTU (Nanyang Technological University) (submittedVersion)
- Newcastle University ePrints (Newcastle Univesity) (cc-by)
- Funders
- Egide Merlion (2007 n°5.03.07)
- European Commission MyoAge (EC Fp7 CT-223756)
- Fondation Caisse d'Epargne Rhone Alpes (Sarcopenie n°30)
- Fonds Européens de Développement Régional (23000422)
- NTU Academic Research Fund (AcRF) (RG37/07)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- apoptosis, sarcopenia, skeletal muscle aging, capillary endothelial cells, satellite cells, myonuclei, extracellular matrix fibrosis, perlecan, endorepellin, angiogenesis, muscle atrophy, gastrocnemius
- MeSH terms
- Aging, Animals, Cell Nucleus, Extracellular Space, Male, Mice, Inbred C57BL, Stromal Cells, Apoptosis, Muscle, Skeletal, Muscle Fibers, Skeletal, Tenascin, Heparan Sulfate Proteoglycans, Satellite Cells, Skeletal Muscle, Endothelial Cells, Mice, Sarcopenia
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
