Aging of the skeletal muscle extracellular matrix drives a stem cell fibrogenic conversion
Open accessAbstract
Age-related declines in skeletal muscle regeneration have been attributed to muscle stem cell (MuSC) dysfunction. Aged MuSCs display a fibrogenic conversion, leading to fibrosis and impaired recovery after injury. Although studies have demonstrated the influence of in vitro substrate characteristics on stem cell fate, whether and how aging of the extracellular matrix (ECM) affects stem cell behavior has not been investigated. Here, we investigated the direct effect of the aged muscle ECM on MuSC lineage specification. Quantification of ECM topology and muscle mechanical properties reveals decreased collagen tortuosity and muscle stiffening with increasing age. Age-related ECM alterations directly disrupt MuSC responses, and MuSCs seeded ex vivo onto decellularized ECM constructs derived from aged muscle display increased expression of fibrogenic markers and decreased myogenicity, compared to MuSCs seeded onto young ECM. This fibrogenic conversion is recapitulated in vitro when MuSCs are seeded directly onto matrices elaborated by aged fibroblasts. When compared to young fibroblasts, fibroblasts isolated from aged muscle display increased nuclear levels of the mechanosensors, Yes-associated protein (YAP)/transcriptional coactivator with PDZ-binding motif (TAZ), consistent with exposure to a stiff microenvironment in vivo. Accordingly, preconditioning of young fibroblasts by seeding them onto a substrate engineered to mimic the stiffness of aged muscle increases YAP/TAZ nuclear translocation and promotes secretion of a matrix that favors MuSC fibrogenesis. The findings here suggest that an age-related increase in muscle stiffness drives YAP/TAZ-mediated pathogenic expression of matricellular proteins by fibroblasts, ultimately disrupting MuSC fate.
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?
Decreased collagen tortuosity and increased stiffness in the muscle niche are associated with aberrant MuSC differentiation.
“Decreased collagen tortuosity and increased stiffness in the muscle niche are associated with aberrant MuSC differentiation82.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [82]
In muscle, quantitative proteomic studies reveal striking remodelling in ECM during ageing, and those changes can influence MuSC function.
“In muscle, quantitative proteomic studies also reveal striking remodelling in ECM during ageing66,82, and those changes can influence MuSC function.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [82]
In muscle, ECM stiffness also increases with age and is associated with decreased collagen tortuosity; these ECM changes induce MuSCs to adopt a more fibrogenic fate, thereby diminishing their myogenic potential.
“In muscle, ECM stiffness also increases with age and is associated with decreased collagen tortuosity82. These ECM changes induce MuSCs to adopt a more fibrogenic fate, thereby diminishing their myogenic potential.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [82]
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
Matrix elasticity directs stem cell lineage specification
Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006) · Cell · doi:10.1016/j.cell.2006.06.044 · Cited by 13,915 · see citing works
Role of YAP/TAZ in mechanotransduction
Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., et al. (2011) · Nature · doi:10.1038/nature10137 · Cited by 5,979 · see citing works
SATELLITE CELL OF SKELETAL MUSCLE FIBERS
Mauro, A. (1961) · The Journal of Cell Biology · doi:10.1083/jcb.9.2.493 · Cited by 3,683 · see citing works
Rejuvenation of aged progenitor cells by exposure to a young systemic environment
Conboy, I. M., Conboy, M. J., Wagers, A. J., Girma, E. R., Weissman, I. L., & Rando, T. A. (2005) · Nature · doi:10.1038/nature03260 · Cited by 2,287 · see citing works
Self-citationMyotubes differentiate optimally on substrates with tissue-like stiffness
Engler, A. J., Griffin, M. A., Sen, S., Bönnemann, C. G., Sweeney, H. L., & Discher, D. E. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200405004 · Cited by 1,743 · see citing works
Aragona, M., Panciera, T., Manfrin, A., Giulitti, S., Michielin, F., Elvassore, N., Dupont, S., & Piccolo, S. (2013) · Cell · doi:10.1016/j.cell.2013.07.042 · Cited by 1,651 · see citing works
Cellular mechanotransduction: putting all the pieces together again
Ingber, D. E. (2006) · The FASEB Journal · doi:10.1096/fj.05-5424rev · Cited by 1,627 · see citing works
Substrate Elasticity Regulates Skeletal Muscle Stem Cell Self-Renewal in Culture
Gilbert, P. M., Havenstrite, K. L., Magnusson, K. E. G., Sacco, A., Leonardi, N. A., Kraft, P., Nguyen, N. K., Thrun, S., Lutolf, M. P., & Blau, H. M. (2010) · Science · doi:10.1126/science.1191035 · Cited by 1,587 · see citing works
Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis
Brack, A. S., Conboy, M. J., Roy, S., Lee, M., Kuo, C. J., Keller, C., & Rando, T. A. (2007) · Science · doi:10.1126/science.1144090 · Cited by 1,564 · see citing works
Self-citationBrew, K., & Nagase, H. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.01.003 · Cited by 1,384 · see citing works
Notch-Mediated Restoration of Regenerative Potential to Aged Muscle
Conboy, I. M., Conboy, M. J., Smythe, G. M., & Rando, T. A. (2003) · Science · doi:10.1126/science.1087573 · Cited by 1,121 · see citing works
Self-citationMechanosignaling through YAP and TAZ drives fibroblast activation and fibrosis
Liu, F., Lagares, D., Choi, K. M., Stopfer, L., Marinković, A., Vrbanac, V., Probst, C. K., Hiemer, S. E., Sisson, T. H., Horowitz, J. C., et al. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00300.2014 · Cited by 874 · see citing works
Duchenne muscular dystrophy: Deficiency of dystrophin at the muscle cell surface
Bonilla, E., Samitt, C. E., Miranda, A. F., Hays, A. P., Salviati, G., DiMauro, S., Kunkel, L. M., Hoffman, E. P., & Rowland, L. P. (1988) · Cell · doi:10.1016/0092-8674(88)90065-7 · Cited by 626 · see citing works
Collagen VI regulates satellite cell self-renewal and muscle regeneration
Urciuolo, A., Quarta, M., Morbidoni, V., Gattazzo, F., Molon, S., Grumati, P., Montemurro, F., Tedesco, F. S., Blaauw, B., Cossu, G., et al. (2013) · Nature Communications · doi:10.1038/ncomms2964 · Cited by 511 · see citing works
Self-citationEngineering gene expression and protein synthesis by modulation of nuclear shape
Thomas, C. H., Collier, J. H., Sfeir, C. S., & Healy, K. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.032668799 · Cited by 483 · see citing works
Matrix metalloproteinase interactions with collagen and elastin
Doren, S. R. V. (2015) · Matrix Biology · doi:10.1016/j.matbio.2015.01.005 · Cited by 463 · see citing works
Signaling in Fibrosis: TGF-β, WNT, and YAP/TAZ Converge
Piersma, B., Bank, R. A., & Boersema, M. (2015) · Frontiers in Medicine · doi:10.3389/fmed.2015.00059 · Cited by 456 · see citing works
The regeneration of skeletal muscle fibers following injury
Carlson, B. M., & Faulkner, J. A. (1983) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198315030-00003 · Cited by 420 · see citing works
Design and analysis of tissue engineering scaffolds that mimic soft tissue mechanical anisotropy
Courtney, T. D., Sacks, M. S., Stankus, J. J., Guan, J., & Wagner, W. R. (2006) · Biomaterials · doi:10.1016/j.biomaterials.2006.02.024 · Cited by 414 · see citing works
Self-citationFactors Associated with Recurrent Hamstring Injuries
Croisier, J. (2004) · Sports Medicine · doi:10.2165/00007256-200434100-00005 · Cited by 379 · see citing works
Connective tissue fibroblasts and Tcf4 regulate myogenesis
Mathew, S. J., Hansen, J. M., Merrell, A. J., Murphy, M. M., Lawson, J. A., Hutcheson, D. A., Hansen, M. S. T., Angus-Hill, M. L., & Kardon, G. (2010) · Development · doi:10.1242/dev.057463 · Cited by 309 · see citing works
Multiaxial Mechanical Behavior of Biological Materials
Sacks, M. S., & Sun, W. (2003) · Annual Review of Biomedical Engineering · doi:10.1146/annurev.bioeng.5.011303.120714 · Cited by 304 · see citing works
Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing
Gupta, M., Sarangi, B. R., Deschamps, J. R., Nematbakhsh, Y., Callan-Jones, A., Margadant, F., Mège, R., Lim, C. T., Voituriez, R., & Ladoux, B. (2015) · Nature Communications · doi:10.1038/ncomms8525 · Cited by 294 · see citing works
Connective tissue changes and physical properties of developing and ageing skeletal muscle.
Alnaqeeb, M. A., Zaid, N. S. A., & Goldspink, G. (1984) · PubMed · Cited by 275 · see citing works
Age‐associated Changes in the Response of Skeletal Muscle Cells to Exercise and Regenerationa
Grounds, M. D. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09894.x · Cited by 264 · 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
Intrinsic stiffness of extracellular matrix increases with age in skeletal muscles of mice
Wood, L. K., Kayupov, E., Gumucio, J. P., Mendias, C. L., Claflin, D. R., & Brooks, S. V. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00256.2014 · Cited by 216 · see citing works
Role of basal lamina in neoplastic disorganization of tissue architecture.
Ingber, D. E., Madri, J. A., & Jamieson, J. D. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.6.3901 · Cited by 208 · see citing works
Yang, G., Rothrauff, B. B., Lin, H., Gottardi, R., Alexander, P. G., & Tuan, R. S. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.08.054 · Cited by 182 · see citing works
Self-citationCharacterization of the complete fiber network topology of planar fibrous tissues and scaffolds
D’Amore, A., Stella, J. A., Wagner, W. R., & Sacks, M. S. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.03.052 · Cited by 159 · see citing works
Self-citationBone marrow contribution to skeletal muscle: A physiological response to stress
Palermo, A. T., LaBarge, M. A., Doyonnas, R., Pomerantz, J. H., & Blau, H. M. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2004.12.024 · Cited by 145 · see citing works
D’Amore, A., Yoshizumi, T., Luketich, S. K., Wolf, M. T., Gu, X., Cammarata, M., Hoff, R., Badylak, S. F., & Wagner, W. R. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.07.039 · Cited by 144 · see citing works
Self-citationA Wnt-TGFβ2 axis induces a fibrogenic program in muscle stem cells from dystrophic mice
Biressi, S., Miyabara, E. H., Gopinath, S. D., Carlig, P. M. M., & Rando, T. A. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008411 · Cited by 143 · see citing works
Self-citationOn the biomechanical function of scaffolds for engineering load-bearing soft tissues
Stella, J. A., D’Amore, A., Wagner, W. R., & Sacks, M. S. (2010) · Acta Biomaterialia · doi:10.1016/j.actbio.2010.01.001 · Cited by 140 · see citing works
Self-citationGargioli, C., Coletta, M., Grandis, F. D., Cannata, S. M., & Cossu, G. (2008) · Nature Medicine · doi:10.1038/nm.1852 · Cited by 125 · see citing works
The pro-myogenic environment provided by whole organ scale acellular scaffolds from skeletal muscle
Perniconi, B., Costa, A., Aulino, P., Teodori, L., Adamo, S., & Coletti, D. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.07.016 · Cited by 114 · see citing works
Imayama, S., & Braverman, I. M. (1989) · PubMed · Cited by 108 · see citing works
Fibrogenic Cell Plasticity Blunts Tissue Regeneration and Aggravates Muscular Dystrophy
Pessina, P., Kharraz, Y., Jardı́, M., Fukada, S., Serrano, A. L., Perdiguero, E., & Muñoz‐Cánoves, P. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.04.007 · Cited by 101 · see citing works
Holloszy, J. O., & Carlson, B. M. (1995) · The Journals of Gerontology Series A · doi:10.1093/gerona/50a.special_issue.96 · Cited by 92 · see citing works
Ambrosio, F., Ferrari, R., Distéfano, G., Plassmeyer, J. M., Carvell, G. E., Deasy, B. M., Boninger, M. L., Fitzgerald, G. K., & Huard, J. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2009.0113 · Cited by 85 · see citing works
Self-citationHashizume, R., Fujimoto, K. L., Hong, Y., Amoroso, N. J., Tobita, K., Miki, T., Keller, B. B., Sacks, M. S., & Wagner, W. R. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.01.051 · Cited by 84 · see citing works
Self-citationTissue-to-cellular level deformation coupling in cell micro-integrated elastomeric scaffolds
Stella, J. A., Liao, J., Hong, Y., Merryman, W. D., Wagner, W. R., & Sacks, M. S. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.04.029 · Cited by 80 · see citing works
Self-citationThe Difference in Stiffness of the Active Plantarflexors Between Young and Elderly Human Females
BLANPIED, P. R., & Smidt, G. L. (1993) · Journal of Gerontology · doi:10.1093/geronj/48.2.m58 · Cited by 76 · see citing works
D’Amore, A., Amoroso, N. J., Gottardi, R., Hobson, C. M., Carruthers, C. A., Watkins, S. C., Wagner, W. R., & Sacks, M. S. (2014) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2014.07.016 · Cited by 75 · see citing works
Self-citationZordan, P., Rigamonti, E., Freudenberg, K., Conti, V., Azzoni, E., Rovere, P. Q., & Brunelli, S. (2014) · Cell Death and Disease · doi:10.1038/cddis.2013.558 · Cited by 70 · see citing works
Koch, R. G., Tsamis, A., D’Amore, A., Wagner, W. R., Watkins, S. C., Gleason, T. G., & Vorp, D. A. (2014) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2014.01.027 · Cited by 61 · see citing works
Self-citationPassive length-force properties of senescent diaphragm: relationship with collagen characteristics
Gosselin, L. E., Martinez, D. A., VAILAS, A. C., & Sieck, G. C. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.76.6.2680 · Cited by 55 · see citing works
Distéfano, G., Ferrari, R., Weiss, C. M., Deasy, B. M., Boninger, M. L., Fitzgerald, G. K., Huard, J., & Ambrosio, F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054922 · Cited by 49 · see citing works
Self-citationNeoplastic disorganization of pancreatic epithelial cell-cell relations. Role of basement membrane.
Ingber, D. E., Madri, J. A., & Jamieson, J. D. (1985) · PubMed · Cited by 39 · see citing works
Scale‐dependent fiber kinematics of elastomeric electrospun scaffolds for soft tissue engineering
Stella, J. A., Wagner, W. R., & Sacks, M. S. (2009) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.32593 · Cited by 38 · see citing works
Self-citationTakanari, K., Hong, Y., Hashizume, R., Huber, A., Amoroso, N. J., D'Amore, A., Badylak, S. F., & Wagner, W. R. (2016) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.1834 · Cited by 35 · see citing works
Self-citationAmbrosio, F., Ferrari, R., Fitzgerald, G. K., Carvell, G. E., Boninger, M. L., & Huard, J. (2009) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2008.06.035 · Cited by 23 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Skeletal muscle: A review of molecular structure and function, in health and disease
Mukund, K., & Subramaniam, S. (2019) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1462 · Cited by 680 · see citing works
Lin, H., Sohn, J., Shen, H., Langhans, M. T., & Tuan, R. S. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.06.026 · Cited by 448 · see citing works
Self-citationAgeing and rejuvenation of tissue stem cells and their niches
Brunet, A., Goodell, M. A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00510-w · Cited by 407 · see citing works
Self-citationChemical strategies to engineer hydrogels for cell culture
Lou, J., & Mooney, D. J. (2022) · Nature Reviews Chemistry · doi:10.1038/s41570-022-00420-7 · Cited by 400 · see citing works
Bao, H., Cao, J., Chen, M., Min, C., Chen, W., Chen, X., Chen, Y., Chen, Y., Chen, Y., Chen, Z., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2305-0 · Cited by 389 · see citing works
Skeletal muscle fibrosis: an overview
Mahdy, M. A. A. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2955-2 · Cited by 365 · see citing works
Mechanoregulation of YAP and TAZ in Cellular Homeostasis and Disease Progression
Cai, X., Wang, K.-C., & Meng, Z. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.673599 · Cited by 311 · see citing works
Extracellular matrix: an important regulator of cell functions and skeletal muscle development
Zhang, W., Liu, Y., & Zhang, H. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00579-4 · Cited by 289 · see citing works
Mesenchymal Stem/Stromal Cell Senescence: Hallmarks, Mechanisms, and Combating Strategies
Weng, Z., Wang, Y., Ouchi, T., Liu, H., Qiao, X., Wu, C., Zhao, Z., Li, L., & Li, B. (2022) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szac004 · Cited by 291 · see citing works
Cellular and epigenetic drivers of stem cell ageing
Ermolaeva, M., Neri, F., Ori, A., & Rudolph, K. L. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0020-3 · Cited by 272 · see citing works
Identity Noise and Adipogenic Traits Characterize Dermal Fibroblast Aging
Salzer, M. C., Lafzi, A., Berenguer, A., Youssif, C., Castellanos‐Martín, A., Solanas, G., Peixoto, F. O., Attolini, C. S., Prats, N., Aguilera, M., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.012 · Cited by 241 · see citing works
Mechanisms of Arterial Stiffening
Lacolley, P. J., Regnault, V., & Laurent, S. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.313129 · Cited by 203 · see citing works
Perandini, L. A., Chimin, P., Lutkemeyer, D. D. S., & Câmara, N. O. S. (2018) · FEBS Journal · doi:10.1111/febs.14417 · Cited by 160 · see citing works
Vitamin D Promotes Skeletal Muscle Regeneration and Mitochondrial Health
Latham, C. M., Brightwell, C. R., Keeble, A. R., Munson, B. D., Thomas, N. T., Zagzoog, A. M., Fry, C. S., & Fry, J. L. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.660498 · Cited by 163 · see citing works
Inflammaging: The ground for sarcopenia?
Liang, Z., Zhang, T., Liu, H., Li, Z., Peng, L., Wang, C., & Wang, T. (2022) · Experimental Gerontology · doi:10.1016/j.exger.2022.111931 · Cited by 147 · see citing works
The Muscle Stem Cell Niche in Health and Disease
Mashinchian, O., Pisconti, A., Moal, E. L., & Bentzinger, C. F. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.08.003 · Cited by 127 · see citing works
In Vitro Tissue‐Engineered Skeletal Muscle Models for Studying Muscle Physiology and Disease
Khodabukus, A., Prabhu, N. K., Wang, J., & Bursac, N. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201701498 · Cited by 128 · see citing works
Role of YAP/TAZ in Cell Lineage Fate Determination and Related Signaling Pathways
Heng, B. C., Zhang, X., Aubel, D., Bai, Y., Li, X., Yan, W., Fussenegger, M., & Deng, X. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00735 · Cited by 128 · see citing works
Iijima, H., Gilmer, G. G., Wang, K., Bean, A., He, Y., Lin, H., Tang, W., Lamont, D. N., Tai, C., Ito, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-022-35359-2 · Cited by 117 · see citing works
Self-citationPavan, P. G., Monti, E., Bondı̀, M., Fan, C., Stecco, C., Narici, M. V., Reggiani, C., & Marcucci, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113992 · Cited by 106 · see citing works
Shang, G., Han, L., Wang, Z., Liu, Y., Yan, S., Sai, W.-W., Wang, D., Li, Y., Zhang, W., & Zhong, M. (2020) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12560 · Cited by 104 · see citing works
Loreti, M., & Sacco, A. (2022) · npj Regenerative Medicine · doi:10.1038/s41536-022-00204-z · Cited by 101 · see citing works
Decellularized tissues as platforms for in vitro modeling of healthy and diseased tissues
McCrary, M. W., Bousalis, D., Mobini, S., Song, Y. H., & Schmidt, C. E. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.05.031 · Cited by 96 · see citing works
Ala, M., & Ala, M. (2021) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.1c00167 · Cited by 96 · see citing works
Kramerova, I. A., Kumagai-Cresse, C., Ermolova, N. V., Mokhonova, E. I., Marinov, M., Capote, J. C., Becerra, D., Quattrocelli, M., Crosbie, R. H., Welch, E. M., et al. (2019) · Human Molecular Genetics · doi:10.1093/hmg/ddz181 · Cited by 94 · see citing works
Epigenetic regulation of satellite cell fate during skeletal muscle regeneration
Massenet, J., Gardner, E., Chazaud, B., & Dilworth, F. J. (2021) · Skeletal Muscle · doi:10.1186/s13395-020-00259-w · Cited by 94 · see citing works
Opportunities for organoids as new models of aging
Hu, J. L., Todhunter, M. E., LaBarge, M. A., & Gartner, Z. J. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201709054 · Cited by 88 · see citing works
Stochastic non-enzymatic modification of long-lived macromolecules - A missing hallmark of aging
Fedintsev, A., & Moskalev, A. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101097 · Cited by 81 · see citing works
Tissue-Engineered Skeletal Muscle Models to Study Muscle Function, Plasticity, and Disease
Khodabukus, A. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.619710 · Cited by 82 · see citing works
Passive stiffness of fibrotic skeletal muscle in mdx mice relates to collagen architecture
Brashear, S. E., Wohlgemuth, R. P., Gonzalez, G., & Smith, L. (2020) · The Journal of Physiology · doi:10.1113/jp280656 · Cited by 78 · see citing works
Extracellular matrix: Brick and mortar in the skeletal muscle stem cell niche
Schüler, S. C., Liu, Y., Dumontier, S., Grandbois, M., Moal, E. L., Cornelison, D., & Bentzinger, C. F. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1056523 · Cited by 82 · see citing works
Wohlgemuth, R. P., Brashear, S. E., & Smith, L. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00287.2023 · Cited by 82 · see citing works
Tissue-specific parameters for the design of ECM-mimetic biomaterials
Tonti, O. R., Larson, H., Lipp, S. N., Luetkemeyer, C. M., Makam, M., Vargas, D., Wilcox, S. M., & Calve, S. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.04.017 · Cited by 81 · see citing works
Forcina, L., Miano, C., Scicchitano, B. M., & Musarò, A. (2019) · Cells · doi:10.3390/cells8030232 · Cited by 79 · see citing works
Mitochondrial Dysfunction in Cancer Cachexia: Impact on Muscle Health and Regeneration
Beltrà, M., Pin, F., Ballarò, R., Costelli, P., & Penna, F. (2021) · Cells · doi:10.3390/cells10113150 · Cited by 76 · see citing works
Giroud, J., Bouriez, I., Paulus, H., Pourtier, A., Debacq‐Chainiaux, F., & Pluquet, O. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310788 · Cited by 77 · see citing works
Wang, D. M., Zhang, X., Huang, S., Liu, Y., Fu, S., Mak, K. K., Blocki, A. M., Yung, P. S., Tuan, R. S., & Ker, D. F. E. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120789 · Cited by 71 · see citing works
Self-citationGhosh, D., Peña, C. M., Quach, N. D., Xuan, B., Lee, A. H., & Dawson, M. (2020) · Journal of Cell Science · doi:10.1242/jcs.232470 · Cited by 67 · see citing works
Liu, X., Gao, Y., Long, X., Hayashi, T., Mizuno, K., Hattori, S., Fujisaki, H., Ogura, T., Wang, D. O., & Ikejima, T. (2019) · Food & Function · doi:10.1039/c9fo01346f · Cited by 68 · see citing works
Zullo, A., Fleckenstein, J., Schleip, R., Hoppe, K., Wearing, S. C., & Klingler, W. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00592 · Cited by 70 · see citing works
The cellular mechanobiology of aging: from biology to mechanics
Bajpai, A., Li, R., & Chen, W. (2020) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14529 · Cited by 67 · see citing works
Lipotoxicity, aging, and muscle contractility: does fiber type matter?
Carter, C. S., Justice, J. N., & Thompson, L. (2019) · GeroScience · doi:10.1007/s11357-019-00077-z · Cited by 66 · see citing works
Dysregulation of the Hippo pathway signaling in aging and cancer
Yeung, Y. T., Guerrero‐Castilla, A., Cano, M., Muñoz, M. F., Ayala, A., & Argüelles, S. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.03.018 · Cited by 62 · see citing works
The Effects of Aging on the Intramuscular Connective Tissue
Fede, C., Fan, C., Pirri, C., Petrelli, L., Biz, C., Porzionato, A., Macchi, V., De, R., & Stecco, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911061 · Cited by 64 · see citing works
Advanced Glycation End-Products in Skeletal Muscle Aging
Olson, L. C., Redden, J. T., Schwartz, Z., Cohen, D. J., & McClure, M. J. (2021) · Bioengineering · doi:10.3390/bioengineering8110168 · Cited by 63 · see citing works
Rando, T. A., Brunet, A., & Goodell, M. A. (2025) · Cell stem cell · doi:10.1016/j.stem.2025.06.004 · Cited by 66 · see citing works
Self-citationAgeing of skeletal muscle extracellular matrix and mitochondria: finding a potential link
Cai, L., Shi, L., Peng, Z., Sun, Y., & Chen, J. (2023) · Annals of Medicine · doi:10.1080/07853890.2023.2240707 · Cited by 60 · see citing works
Mechanisms of muscle cells alterations and regeneration decline during aging
Chinvattanachot, G., Rivas, D., & Duque, G. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102589 · Cited by 59 · see citing works
Stem Cell Aging in Lifespan and Disease: A State-of-the-Art Review
Sameri, S., Samadi, P., Dehghan, R., Salem, E., Hosseini, N. F., & Amini, R. (2020) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x15666200213105155 · Cited by 55 · see citing works
Rahman, F. A., Angus, S. A., Stokes, K., Karpowicz, P. A., & Krause, M. P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134575 · Cited by 55 · see citing works
Obstacles and challenges for tissue engineering and regenerative medicine: Australian nuances
Grounds, M. D. (2017) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12899 · Cited by 54 · see citing works
Dietary epicatechin improves survival and delays skeletal muscle degeneration in aged mice
Si, H., Wang, X., Zhang, L., Parnell, L. D., Ahmed, B., LeRoith, T., Ansah, T.-A., Zhang, L., Li, J., Ordovás, J. M., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201800554rr · Cited by 54 · see citing works
Abbott, C. B., Lawrence, M. M., Kobak, K. A., Lopes, E. B. P., Peelor, F. F., Donald, E. J., Remmen, H. V., Griffin, T. M., & Miller, B. F. (2021) · Function · doi:10.1093/function/zqab028 · Cited by 54 · see citing works
Sassoli, C., Pierucci, F., Zecchi‐Orlandini, S., & Meacci, E. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225545 · Cited by 53 · see citing works
Brightwell, C. R., Latham, C. M., Thomas, N. T., Keeble, A. R., Murach, K. A., & Fry, C. S. (2022) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00200.2022 · Cited by 52 · see citing works
Careccia, G., Mangiavini, L., & Cirillo, F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms25010512 · Cited by 59 · see citing works
Zhou, J., So, K. K. H., Li, Y., Li, Y., Yuan, J., Ding, Y., Chen, F., Huang, Y., Liu, J., Lee, W., et al. (2019) · Aging Cell · doi:10.1111/acel.12996 · Cited by 51 · see citing works
Targeting the stem cell niche micro-environment as therapeutic strategies in aging
Farahzadi, R., Valipour, B., Montazersaheb, S., & Fathi, E. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1162136 · Cited by 49 · see citing works
Anoikis in cell fate, physiopathology, and therapeutic interventions
Mei, J., Jiang, X., Tian, H., Rong, D., Song, J., Wang, L., Chen, Y., Wong, R. C. B., Guo, C., Wang, L., et al. (2024) · MedComm · doi:10.1002/mco2.718 · Cited by 52 · see citing works
Cellular Biomechanics in Skeletal Muscle Regeneration
Li, E. W., McKee-Muir, O. C., & Gilbert, P. M. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.08.007 · Cited by 49 · see citing works
Fuqua, J. D., Lawrence, M. M., Hettinger, Z. R., Borowik, A., Brecheen, P., Szczygiel, M. M., Abbott, C. B., Peelor, F. F., Confides, A. L., Kinter, M. T., et al. (2023) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13285 · Cited by 45 · see citing works
Hsp90β interacts with MDM2 to suppress p53‐dependent senescence during skeletal muscle regeneration
He, M. Y., Xu, S. B., Qu, Z., Guo, Y. M., Liu, X. C., Cong, X. X., Wang, J. F., Low, B. C., Li, L., Wu, Q., et al. (2019) · Aging Cell · doi:10.1111/acel.13003 · Cited by 46 · see citing works
Skeletal muscle as an experimental model of choice to study tissue aging and rejuvenation
Etienne, J., Liu, C., Skinner, C. M., Conboy, M. J., & Conboy, I. M. (2020) · Skeletal Muscle · doi:10.1186/s13395-020-0222-1 · Cited by 48 · see citing works
Liu, Y., Li, M., Lv, X., Bao, K., Tian, X. Y., He, L., Shi, L., Zhu, Y., & Ai, D. (2022) · Circulation Research · doi:10.1161/circresaha.121.320464 · Cited by 45 · see citing works
Changes in cardiac resident fibroblast physiology and phenotype in aging
Trial, J., & Cieslik, K. A. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00237.2018 · Cited by 45 · see citing works
Insight into muscle stem cell regeneration and mechanobiology
Pang, K. T., Loo, L. S. W., Chia, S., Ong, F. Y. T., Yu, H., & Walsh, I. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03363-y · Cited by 43 · see citing works
Differentiation reveals latent features of aging and an energy barrier in murine myogenesis
Kimmel, J. C., Yi, N., Roy, M., Hendrickson, D. G., & Kelley, D. R. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109046 · Cited by 42 · see citing works
Age-associated changes in the mechanical properties of human cadaveric pelvic floor muscles
Burnett, L. A., Cook, M. S., Shah, S. B., Wong, M., Kado, D. M., & Alperin, M. (2019) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2019.109436 · Cited by 42 · see citing works
Available In Vitro Models for Human Satellite Cells from Skeletal Muscle
Romagnoli, C., Iantomasi, T., & Brandi, M. L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413221 · Cited by 42 · see citing works
Age-Associated Differences in Recovery from Exercise-Induced Muscle Damage
Li, D. C. W., Rudloff, S., Langer, H. T., Norman, K., & Herpich, C. (2024) · Cells · doi:10.3390/cells13030255 · Cited by 41 · see citing works
Lyu, A., Zhu, S., Chen, J., Zhao, Y., Pu, D., Luo, C., Lyu, Q., Fan, Z., Sun, Y., Wu, J., et al. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.04.008 · Cited by 40 · see citing works
Xu, J., Fu, S. N., & Hug, F. (2021) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-021-04519-8 · Cited by 41 · see citing works
Age-Related Changes in the Matrisome of the Mouse Skeletal Muscle
Lofaro, F. D., Cisterna, B., Lacavalla, M. A., Boschi, F., Malatesta, M., Quaglino, D., Zancanaro, C., & Boraldi, F. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910564 · Cited by 40 · see citing works
Taetzsch, T., Brayman, V. L., & Valdez, G. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.06.009 · Cited by 39 · see citing works
Thrown for a loop: fibro-adipogenic progenitors in skeletal muscle fibrosis
Loomis, T., & Smith, L. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00245.2023 · Cited by 39 · see citing works
Acun, A., Oganesyan, R., Uygun, K., Yeh, H., Yarmush, M. L., & Uygun, B. E. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120689 · Cited by 39 · see citing works
Myoblast mechanotransduction and myotube morphology is dependent on BAG3 regulation of YAP and TAZ
Günay, K. A., Silver, J. S., Chang, T.-L., Bednarski, O. J., Bannister, K. L., Rogowski, C. J., Olwin, B. B., & Anseth, K. S. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.121097 · Cited by 38 · see citing works
Caloric restriction maintains stem cells through niche and regulates stem cell aging
Maharajan, N., Vijayakumar, K. A., Jang, C. H., & Cho, G. (2019) · Journal of Molecular Medicine · doi:10.1007/s00109-019-01846-1 · Cited by 38 · see citing works
Sosa, P., Alcalde‐Estévez, E., Asenjo‐Bueno, A., Plaza, P., Carrillo‐López, N., Olmos, G., López‐Ongil, S., & Ruiz‐Torres, M. P. (2021) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12750 · Cited by 39 · see citing works
Giha, H. A., Sater, M. S., & Alamin, O. A. O. (2022) · Acta Diabetologica · doi:10.1007/s00592-022-01860-9 · Cited by 39 · see citing works
Alcalde-Estévez, E., Asenjo-Bueno, A., Sosa, P., Olmos, G., Plaza, P., Caballero-Mora, M. Á., Rodríguez-Puyol, D., Ruíz-Torres, M. P., & López-Ongil, S. (2020) · Aging · doi:10.18632/aging.103450 · Cited by 35 · see citing works
Extracellular matrix/mitochondria pathway: A novel potential target for sarcopenia
Melouane, A., Yoshioka, M., & St‐Amand, J. (2019) · Mitochondrion · doi:10.1016/j.mito.2019.10.007 · Cited by 35 · see citing works
Natural products and skeletal muscle health
Qu, Z., Zhou, S., Li, P., Liu, C., Yuan, B., Zhang, S., & Liu, A. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2021.108619 · Cited by 35 · see citing works
Xiong, X., Li, W., Nam, J., Qu, M., Kay, S. A., & Ma, K. (2022) · Journal of Cell Science · doi:10.1242/jcs.260094 · Cited by 34 · see citing works
Age-Related Changes in Extracellular Matrix
Guvatova, Z. G., Borisov, P. V., Alekseev, A. A., & Moskalev, A. (2022) · Biochemistry (Moscow) · doi:10.1134/s0006297922120112 · Cited by 34 · see citing works
Decellularized Cell‐Secreted Extracellular Matrices as Biomaterials for Tissue Engineering
Ramos‐Rodriguez, D. H., & Leach, J. K. (2024) · Small Science · doi:10.1002/smsc.202400335 · Cited by 33 · see citing works
Narayanan, N., & Calve, S. (2020) · Connective Tissue Research · doi:10.1080/03008207.2020.1814263 · Cited by 33 · see citing works
Cellular enlargement - A new hallmark of aging?
Davies, D., van den Handel, K., Bharadwaj, S., & Lengefeld, J. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1036602 · Cited by 35 · see citing works
Liao, J., Zheng, Y., Hu, M., Xu, P., Lin, L., Liu, X., Wu, Y., Huang, B., Ye, X., Li, S., et al. (2021) · Hypertension · doi:10.1161/hypertensionaha.121.18363 · Cited by 32 · see citing works
Odd skipped-related 1 controls the pro-regenerative response of fibro-adipogenic progenitors
Kotsaris, G., Qazi, T. H., Bucher, C. H., Zahid, H., Pöhle‐Kronawitter, S., Ugorets, V., Jarassier, W., Börno, S. T., Timmermann, B., Giesecke‐Thiel, C., et al. (2023) · npj Regenerative Medicine · doi:10.1038/s41536-023-00291-6 · Cited by 31 · see citing works
Kobak, K. A., Lawrence, M. M., Pharaoh, G. A., Borowik, A., Peelor, F. F., Shipman, P. D., Griffin, T. M., Remmen, H. V., & Miller, B. F. (2021) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12772 · Cited by 31 · see citing works
Chen, S., Huang, L., Liu, B., Duan, H., Li, Z., Liu, Y., Li, H., Fu, X., Lin, J., Xu, Y., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2400-3 · Cited by 31 · see citing works
Bechshøft, C. J. L., Jensen, S. M., Schjerling, P., Andersen, J. L., Svensson, R. B., Eriksen, C. S., Mkumbuzi, N. S., Kjær, M., & Mackey, A. L. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00049.2019 · Cited by 30 · see citing works
Skeletal muscle aging – Stem cells in the spotlight
Henze, H., Jung, M. J., Ahrens, H. E., Steiner, S., & von Maltzahn, J. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111283 · Cited by 28 · see citing works
RhoA within myofibers controls satellite cell microenvironment to allow hypertrophic growth
Noviello, C., Kobon, K., Delivry, L., Guilbert, T., Britto, F. A., Julienne, F., Maire, P., Randrianarison-Huetz, V., & Sotiropoulos, A. (2021) · iScience · doi:10.1016/j.isci.2021.103616 · Cited by 29 · see citing works
Mechanical control of the mammalian circadian clock via YAP/TAZ and TEAD
Abenza, J. F., Rossetti, L., Mouelhi, M., Burgués, J., Andreu, I., Kennedy, K., Roca‐Cusachs, P., Marco, S., García‐Ojalvo, J., & Trepat, X. (2023) · The Journal of Cell Biology · doi:10.1083/jcb.202209120 · Cited by 28 · see citing works
Fischer, A. G., Elliott, E. M., Brittian, K. R., Garrett, L. T., Sadri, G., Aebersold, J., Singhal, R. A., Nong, Y., Leask, A., Jones, S. P., et al. (2024) · Matrix Biology · doi:10.1016/j.matbio.2024.08.001 · Cited by 28 · see citing works
Hunt, E. R., Confides, A. L., Abshire, S. M., Dupont‐Versteegden, E. E., & Butterfield, T. A. (2019) · Physiological Reports · doi:10.14814/phy2.14200 · Cited by 26 · see citing works
Sinha, U. S., Malis, V., Chen, J., Csapo, R., Kinugasa, R., Narici, M. V., & Sinha, S. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00626 · Cited by 27 · see citing works
Aparicio, P., Navarrete‐Villanueva, D., Gómez‐Cabello, A., López‐Royo, T., Santamaría, E., Fernández‐Irigoyen, J., Ausín, K., Arruebo, M., Sebastián, V., Vicente‐Rodríguez, G., et al. (2024) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13539 · Cited by 26 · see citing works
- Authors
- Stearns-Reider, K. M., D'Amore, A., Beezhold, K., Rothrauff, B., Cavalli, L., Wagner, W. R., Vorp, D. A., Tsamis, A., Shinde, S., Zhang, C., Barchowsky, A., Rando, T. A., Tuan, R. S., & Ambrosio, F.
- Affiliations
- University of Pittsburgh (US)
- Department of Surgery; University of Pittsburgh; 450 Technology Drive, Suite 300 Pittsburgh PA 15219 USA
- University of Leicester (GB)
- VA Palo Alto Health Care System (US)
- Corresponding author
- Ambrosio, Fabrisia
- ORCID
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2017-03-30
- Volume
- 16
- Issue
- 3
- Pages
- 518-528
- ISSN
- 1474-9718 (ISSN-L)
- PMC
- PMC5418187
- OpenAlex
- W2601343417
- Cited by
- 265
- References
- 52
- Citations by year
- 2026: 41 · 2025: 30 · 2024: 31 · 2023: 31 · 2022: 25 · 2021: 38 · 2020: 29 · 2019: 22 · 2018: 13 · 2017: 5
- FWCI
- 7.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Aging Cell (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- Leicester Research Archive (University of Leicester) (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute on Aging (K01AG039477)
- National Institute of Environmental Health Sciences (F32ES022134, R01ES023696, R01ES025529)
- University of Pittsburgh Medical Center Rehabilitation Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hippo pathway signaling and YAP/TAZ
- Keywords
- skeletal muscle aging, muscle stem cells, extracellular matrix, muscle fibrosis, muscle stiffness, matricellular proteins, muscle regeneration
- MeSH terms
- YAP-Signaling Proteins, Acyltransferases, Aging, Animals, Biomechanical Phenomena, Cell Differentiation, Extracellular Matrix, Fibroblasts, Fibrosis, Gene Expression Regulation, Male, Mice, Inbred C57BL, Phosphoproteins, Stem Cells, Transcription Factors, Muscle, Skeletal, Cell Cycle Proteins, Muscle Development, Myoblasts, Adaptor Proteins, Signal Transducing, Mice, Torsion, Mechanical, Primary Cell Culture
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
