Collagen VI regulates satellite cell self-renewal and muscle regeneration
Open accessAbstract
Adult muscle stem cells, or satellite cells have essential roles in homeostasis and regeneration of skeletal muscles. Satellite cells are located within a niche that includes myofibers and extracellular matrix. The function of specific extracellular matrix molecules in regulating SCs is poorly understood. Here, we show that the extracellular matrix protein collagen VI is a key component of the satellite cell niche. Lack of collagen VI in Col6a1(-/-) mice causes impaired muscle regeneration and reduced satellite cell self-renewal capability after injury. Collagen VI null muscles display significant decrease of stiffness, which is able to compromise the in vitro and in vivo activity of wild-type satellite cells. When collagen VI is reinstated in vivo by grafting wild-type fibroblasts, the biomechanical properties of Col6a1(-/-) muscles are ameliorated and satellite cell defects rescued. Our findings establish a critical role for an extracellular matrix molecule in satellite cell self-renewal and open new venues for therapies of collagen VI-related muscle diseases.
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Deletion of collagen VI or laminin-α1 (ECM components) or myofiber-specific deletion of O-fucosyltransferase 1 gene (Pofut1) impairs the self-renewal of SCs, leading to the shrinkage of the SC pool after multiple muscle injuries.
“Deletion of collagen VI or laminin-α1 (ECM components) or myofiber-specific deletion of O-fucosyltransferase 1 gene (Pofut1) impairs the self-renewal of SCs36–38, leading to the shrinkage of the SC pool after multiple muscle injuries.”
From In vivo partial reprogramming of myofibers promotes muscle regeneration by remodeling the stem cell niche (2021) · cites this paper as [37]
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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
Molecular Mechanisms of Stress-Responsive Changes in Collagen and Elastin Networks in Skin
Aziz, J., Shezali, H., Radzi, Z., Yahya, N. A., Abu Kassim, N. H., Czernuszka, J., & Rahman, M. T. (2016) · Skin Pharmacology and Physiology · doi:10.1159/000447017 · Cited by 7,323 · see citing works
Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling
Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F. T., Csiszar, K., Giaccia, A., Weninger, W., et al. (2009) · Cell · doi:10.1016/j.cell.2009.10.027 · Cited by 4,101 · 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
Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., & Ohsumi, Y. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0704 · Cited by 2,323 · see citing works
Control of Stem Cell Fate by Physical Interactions with the Extracellular Matrix
Guilak, F., Cohen, D. M., Estes, B. T., Gimble, J. M., Liedtke, W., & Chen, C. S. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.06.016 · Cited by 1,837 · 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
Lepper, C., Partridge, T. A., & Fan, C.-M. (2011) · Development · doi:10.1242/dev.067595 · Cited by 1,105 · see citing works
Structure and function of the skeletal muscle extracellular matrix
Gillies, A. R., & Lieber, R. L. (2011) · Muscle & Nerve · doi:10.1002/mus.22094 · Cited by 1,023 · see citing works
Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration
Sambasivan, R., Yao, R., Kissenpfennig, A., Van Wittenberghe, L., Paldi, A., Gayraud-Morel, B., Guenou, H., Malissen, B., Tajbakhsh, S., & Galy, A. (2011) · Development · doi:10.1242/dev.067587 · Cited by 939 · see citing works
Muscle satellite cells adopt divergent fates
Zammit, P. S., Golding, J. P., Nagata, Y., Hudon, V., Partridge, T. A., & Beauchamp, J. R. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200312007 · Cited by 924 · see citing works
Conboy, I. M., & Rando, T. A. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00254-x · Cited by 905 · see citing works
Self-citationAberrant repair and fibrosis development in skeletal muscle
Mann, C. J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A. L., & Muñoz-Cánoves, P. (2011) · Skeletal Muscle · doi:10.1186/2044-5040-1-21 · Cited by 853 · cited 1× · see citing works
“Muscle substitution by fibrotic connective tissue is a common feature of several conditions, such as aging and Duchenne muscular dystrophy, pointing at a negative effect for excessive production of fibrillar collagens and interstitial ECM components 32 .”
The Skeletal Muscle Satellite Cell: The Stem Cell That Came in From the Cold
Zammit, P. S., Partridge, T. A., & Yablonka‐Reuveni, Z. (2006) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.6r6995.2006 · Cited by 684 · see citing works
Brack, A. S., Conboy, I. M., Conboy, M. J., Shen, J., & Rando, T. A. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2007.10.006 · Cited by 682 · see citing works
Self-citationRepairing skeletal muscle: regenerative potential of skeletal muscle stem cells.
Tedesco, F. S., Dellavalle, A., Díaz-Manera, J., Messina, G., & Cossu, G. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40373 · Cited by 667 · see citing works
Self-citationGrumati, P., Coletto, L., Sabatelli, P., Cescon, M., Angelin, A., Bertaggia, E., Blaauw, B., Urciuolo, A., Tiepolo, T., Merlini, L., et al. (2010) · Nature Medicine · doi:10.1038/nm.2247 · Cited by 540 · see citing works
Self-citationGrand, F. L., Jones, A., Seale, V., Scimè, A., & Rudnicki, M. A. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.03.013 · Cited by 531 · see citing works
Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency
Irwin, W., Bergamin, N., Sabatelli, P., Reggiani, C., Megighian, A., Merlini, L., Braghetta, P., Columbaro, M., Volpin, D., Bressan, G. M., et al. (2003) · Nature Genetics · doi:10.1038/ng1270 · Cited by 509 · see citing works
Self-citationNiche Regulation of Muscle Satellite Cell Self-Renewal and Differentiation
Kuang, S., Gillespie, M. A., & Rudnicki, M. A. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2007.12.012 · Cited by 507 · see citing works
Iyengar, P., Espina, V. A., Williams, T. W., Lin, Y., Berry, D. C., Jelicks, L. A., Lee, H., Temple, K. A., Graves, R., Pollard, J. W., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23424 · Cited by 429 · see citing works
Self-citationCollagen VI related muscle disorders
Lampe, A., & Bushby, K. M. D. (2005) · Journal of Medical Genetics · doi:10.1136/jmg.2002.002311 · Cited by 395 · see citing works
Fibronectin Regulates Wnt7a Signaling and Satellite Cell Expansion
Bentzinger, C. F., Wang, Y. X., von Maltzahn, J., Soleimani, V. D., Yin, H., & Rudnicki, M. A. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2012.09.015 · Cited by 386 · see citing works
Shea, K. L., Xiang, W., LaPorta, V. S., Licht, J. D., Keller, C., Basson, M. A., & Brack, A. S. (2010) · Cell stem cell · doi:10.1016/j.stem.2009.12.015 · Cited by 351 · see citing works
Type VI Collagen Anchors Endothelial Basement Membranes by Interacting with Type IV Collagen
Kuo, H., Maslen, C. L., Keene, D. R., & Glanville, R. W. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.42.26522 · Cited by 334 · see citing works
The collagen VI-related myopathies: muscle meets its matrix
Bönnemann, C. G. (2011) · Nature Reviews Neurology · doi:10.1038/nrneurol.2011.81 · Cited by 326 · see citing works
Cornelison, D. D. W., Wilcox-Adelman, S. A., Goetinck, P. F., Rauvala, H., Rapraeger, A. C., & Olwin, B. B. (2004) · Genes & Development · doi:10.1101/gad.1214204 · Cited by 317 · see citing works
Bonaldo, P. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.13.2135 · Cited by 306 · see citing works
Self-citationIn situforce mapping of mammary gland transformation
Lopez, J. I., Kang, I., You, W., McDonald, D. M., & Weaver, V. M. (2011) · Integrative Biology · doi:10.1039/c1ib00043h · Cited by 284 · see citing works
A transitional extracellular matrix instructs cell behavior during muscle regeneration
Calve, S., Odelberg, S. J., & Simon, H. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.05.007 · Cited by 234 · see citing works
Bröhl, D., Vasyutina, E. L., Czajkowski, M. T., Griger, J., Raßek, C., Rahn, H.-P., Purfürst, B., Wende, H., & Birchmeier, C. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.07.014 · Cited by 214 · see citing works
Alexopoulos, L. G., Youn, I., Bonaldo, P., & Guilak, F. (2009) · Arthritis & Rheumatism · doi:10.1002/art.24293 · Cited by 200 · see citing works
Self-citationOno, Y., Calhabeu, F., Morgan, J. E., Katagiri, T., Amthor, H., & Zammit, P. S. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.95 · Cited by 198 · see citing works
Fukada, S., Higuchi, S., Segawa, M., Koda, K.-I., Yamamoto, Y., Tsujikawa, K., Kohama, Y., Uezumi, A., Imamura, M., Miyagoe‐Suzuki, Y., et al. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.02.018 · Cited by 190 · see citing works
Zou, Y., Zhang, R.-Z., Sabatelli, P., Chu, M.-L., & Bönnemann, C. G. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181634ef7 · Cited by 155 · see citing works
Defining the transcriptional signature of skeletal muscle stem cells1,2
Yablonka‐Reuveni, Z., Day, K. R., Vine, A. L., & Shefer, G. (2007) · Journal of Animal Science · doi:10.2527/jas.2007-0473 · Cited by 141 · see citing works
Cosgrove, B. D., Sacco, A., Gilbert, P. M., & Blau, H. M. (2009) · Differentiation · doi:10.1016/j.diff.2009.08.004 · Cited by 135 · see citing works
Regeneration of muscles after cardiotoxin injury I. Cytological aspects
Couteaux, R., Mira, J. C., & d’Albis, A. (1988) · Biology of the Cell · doi:10.1111/j.1768-322x.1988.tb00719.x · Cited by 130 · see citing works
Syndecan-3 and Notch cooperate in regulating adult myogenesis
Pisconti, A., Cornelison, D., Olguín, H. C., Antwine, T. L., & Olwin, B. B. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201003081 · Cited by 126 · see citing works
Braghetta, P., Ferrari, A., Fabbro, C., Bizzotto, D., Volpin, D., Bonaldo, P., & Bressan, G. M. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.08.006 · Cited by 40 · see citing works
Self-citationAndersson, G., Denaro, M., Johnson, K. B., Morgan, P., Sullivan, A., Houser, S. L., Patience, C., White‐Scharf, M. E., & Down, J. D. (2003) · Molecular Therapy · doi:10.1016/s1525-0016(03)00210-7 · Cited by 33 · see citing works
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Extracellular matrix: A dynamic microenvironment for stem cell niche
Gattazzo, F., Urciuolo, A., & Bonaldo, P. (2014) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2014.01.010 · Cited by 1,304 · see citing works
Self-citationAdvancing biomaterials of human origin for tissue engineering
Chen, F.-M., & Liu, X. (2016) · Progress in Polymer Science · doi:10.1016/j.progpolymsci.2015.02.004 · Cited by 1,158 · see citing works
Advanced Therapeutic Dressings for Effective Wound Healing—A Review
Boateng, J. S., & Catanzano, O. (2015) · Journal of Pharmaceutical Sciences · doi:10.1002/jps.24610 · Cited by 957 · see citing works
Functional and Biomimetic Materials for Engineering of the Three-Dimensional Cell Microenvironment
Huang, G., Li, F., Zhao, X., Ma, Y., Li, Y., Lin, M., Jin, G., Lu, T. J., Genin, G. M., & Xu, F. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00094 · Cited by 825 · see citing works
Pitfalls in the measurement of muscle mass: A need for a reference standard
Buckinx, F., Landi, F., Cesari, M., Fielding, R. A., Visser, M., Engelke, K., Maggi, S., Dennison, E., Al‐Daghri, N. M., Allepaerts, S., et al. (2018) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12268 · Cited by 765 · see citing works
Satellite Cells and Skeletal Muscle Regeneration
Dumont, N. A., Bentzinger, C. F., Sincennes, M., & Rudnicki, M. A. (2015) · Comprehensive Physiology · doi:10.1002/cphy.c140068 · Cited by 719 · see citing works
Mercuri, E. M., Bönnemann, C. G., & Francesco Muntoni, A. (2019) · The Lancet · doi:10.1016/s0140-6736(19)32910-1 · Cited by 555 · see citing works
Intrinsic and extrinsic mechanisms regulating satellite cell function
Dumont, N. A., Wang, Y. X., & Rudnicki, M. A. (2015) · Development · doi:10.1242/dev.114223 · Cited by 491 · see citing works
Control of satellite cell function in muscle regeneration and its disruption in ageing
Sousa-Victor, P., García-Prat, L., & Muñoz-Cánoves, P. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00421-2 · Cited by 476 · see citing works
The central role of muscle stem cells in regenerative failure with aging
Blau, H. M., Cosgrove, B. D., & Ho, A. T. V. (2015) · Nature Medicine · doi:10.1038/nm.3918 · Cited by 437 · see citing works
Qazi, T. H., Mooney, D. J., Pumberger, M., Geißler, S., & Duda, G. N. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.02.110 · Cited by 433 · see citing works
Csapo, R., Gumpenberger, M., & Wessner, B. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00253 · Cited by 435 · see citing works
Crosstalk between mechanotransduction and metabolism
Romani, P., Valcárcel-Jiménez, L., Frezza, C., & Dupont, S. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00306-w · Cited by 409 · see citing works
Cellular dynamics in the muscle satellite cell niche
Bentzinger, C. F., Wang, Y. X., Dumont, N. A., & Rudnicki, M. A. (2013) · The EMBO Reports · doi:10.1038/embor.2013.182 · Cited by 398 · see citing works
Fry, C. S., Kirby, T. J., Kosmac, K., McCarthy, J. J., & Peterson, C. A. (2017) · Cell stem cell · doi:10.1016/j.stem.2016.09.010 · Cited by 372 · see citing works
Cescon, M., Gattazzo, F., Chen, P., & Bonaldo, P. (2015) · Journal of Cell Science · doi:10.1242/jcs.169748 · Cited by 366 · see citing works
Self-citationSkeletal 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
The role of matrix metalloproteinases in aging: Tissue remodeling and beyond
Freitas‐Rodríguez, S., Folgueras, A. R., & López-Otı́n, C. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2017.05.007 · Cited by 367 · see citing works
Verma, M., Asakura, Y., Murakonda, B. S. R., Pengo, T., Latroche, C., Chazaud, B., McLoon, L. K., & Asakura, A. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.09.007 · Cited by 349 · see citing works
The Role of the Extracellular Matrix in Cancer Stemness
Nallanthighal, S., Heiserman, J. P., & Cheon, D.-J. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00086 · Cited by 344 · see citing works
Lukjanenko, L., Jung, M. J., Hegde, N., Perruisseau-Carrier, C., Migliavacca, E., Rozo, M., Karaz, S., Jacot, G. E., Schmidt, M., Li, L., et al. (2016) · Nature Medicine · doi:10.1038/nm.4126 · Cited by 337 · see citing works
Tissue Stem Cells: Architects of Their Niches
Fuchs, E., & Blau, H. M. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.09.011 · Cited by 332 · see citing works
Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease
Almada, A. E., & Wagers, A. J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.7 · Cited by 315 · see citing works
Stem Cell Quiescence: Dynamism, Restraint, and Cellular Idling
van Velthoven, C. T. J., & Rando, T. A. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.01.001 · Cited by 313 · see citing works
Self-citationExtracellular 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
Regulation of the muscle fiber micro environment by activated satellite cells during hypertrophy
Fry, C. S., Lee, J. D., Jackson, J. R., Kirby, T. J., Stasko, S. A., Liu, H., Dupont‐Versteegden, E. E., McCarthy, J. J., & Peterson, C. A. (2014) · The FASEB Journal · doi:10.1096/fj.13-239426 · Cited by 273 · see citing works
Aging of the skeletal muscle extracellular matrix drives a stem cell fibrogenic conversion
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., et al. (2017) · Aging Cell · doi:10.1111/acel.12578 · Cited by 265 · see citing works
Self-citationMuscle satellite cell heterogeneity and self-renewal
Motohashi, N., & Asakura, A. (2014) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2014.00001 · Cited by 251 · see citing works
Mechanical regulation of chromatin and transcription
Dupont, S., & Wickström, S. A. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00493-6 · Cited by 240 · see citing works
Naturally derived and synthetic scaffolds for skeletal muscle reconstruction
Wolf, M. T., Dearth, C. L., Sonnenberg, S. B., Loboa, E. G., & Badylak, S. F. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.08.011 · Cited by 231 · see citing works
Intravital three-dimensional bioprinting
Urciuolo, A., Poli, I., Brandolino, L., Raffa, P., Scattolini, V., Laterza, C., Giobbe, G. G., Zambaiti, E., Selmin, G., Magnussen, M., et al. (2020) · Nature Biomedical Engineering · doi:10.1038/s41551-020-0568-z · Cited by 224 · see citing works
Self-citationBasal lamina remodeling at the skeletal muscle stem cell niche mediates stem cell self-renewal
Rayagiri, S. S., Ranaldi, D., Raven, A., Mohamad Azhar, N. I. F., Lefebvre, O., Zammit, P. S., & Borycki, A.-G. (2018) · Nature Communications · doi:10.1038/s41467-018-03425-3 · Cited by 218 · see citing works
Scott, R. W., Arostegui, M., Schweitzer, R., Rossi, F. M. V., & Underhill, T. M. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.11.004 · Cited by 214 · see citing works
Akhmanova, M., Osidak, E. O., Domogatsky, S. P., Rodin, S., & Domogatskaya, A. (2015) · Stem Cells International · doi:10.1155/2015/167025 · Cited by 200 · see citing works
Quarta, M., Brett, J. O., DiMarco, R. L., de Morrée, A., Boutet, S. C., Chacon, R., Gibbons, M. C., Garcia, V. A., Su, J., Shrager, J. B., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3576 · Cited by 196 · see citing works
Self-citationBiomaterials for skeletal muscle tissue engineering
Kwee, B. J., & Mooney, D. J. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.05.003 · Cited by 196 · see citing works
Extracellular matrix regulation in the muscle satellite cell niche
Thomas, K. A., Engler, A. J., & Meyer, G. A. (2014) · Connective Tissue Research · doi:10.3109/03008207.2014.947369 · Cited by 194 · see citing works
Fibro-adipogenic progenitors in skeletal muscle homeostasis, regeneration and diseases
Molina, T., Fabre, P., & Dumont, N. A. (2021) · Open Biology · doi:10.1098/rsob.210110 · Cited by 191 · see citing works
Regulation and phylogeny of skeletal muscle regeneration
Baghdadi, M. B., & Tajbakhsh, S. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.07.026 · Cited by 186 · see citing works
Collagen VI disorders: Insights on form and function in the extracellular matrix and beyond
Lamandé, S. R., & Bateman, J. F. (2017) · Matrix Biology · doi:10.1016/j.matbio.2017.12.008 · Cited by 185 · see citing works
Type-1 pericytes participate in fibrous tissue deposition in aged skeletal muscle
Birbrair, A., Zhang, T., Wang, Z.-M., Messi, M. L., Mintz, A., & Delbono, O. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00171.2013 · Cited by 177 · see citing works
Maintaining bovine satellite cells stemness through p38 pathway
Ding, S., Swennen, G., Meßmer, T., Gagliardi, M., Molin, D. G. M., Li, C., Zhou, G., & Post, M. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-28746-7 · Cited by 176 · see citing works
Chen, P., Cescon, M., Zuccolotto, G., Nobbio, L., Colombelli, C., Filaferro, M., Vitale, G., Feltri, M. L., & Bonaldo, P. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1369-9 · Cited by 171 · see citing works
Self-citationRoles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle
Uezumi, A., Ikemoto‐Uezumi, M., & Tsuchida, K. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00068 · Cited by 163 · see citing works
Electrical Stimulation Counteracts Muscle Decline in Seniors
Kern, H., Barberi, L., Löfler, S., Sbardella, S., Burggraf, S., Fruhmann, H., Carraro, U., Mosole, S., Šarabon, N., Vogelauer, M., et al. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00189 · Cited by 163 · see citing works
Cell therapy to improve regeneration of skeletal muscle injuries
Qazi, T. H., Duda, G. N., Ort, M., Perka, C., Geißler, S., & Winkler, T. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12416 · Cited by 160 · see citing works
Insights into the key roles of proteoglycans in breast cancer biology and translational medicine
Theocharis, A. D., Skandalis, S. S., Neill, T., Multhaupt, H. A. B., Hubo, M., Frey, H., Gopal, S., Gomes, A. M., Afratis, N. A., Lim, H. C., et al. (2015) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2015.03.006 · Cited by 157 · see citing works
An Overview About the Biology of Skeletal Muscle Satellite Cells
Forcina, L., Miano, C., Pelosi, L., & Musarò, A. (2019) · Current Genomics · doi:10.2174/1389202920666190116094736 · Cited by 151 · see citing works
Muscle stem cell isolation and in vitro culture for meat production: A methodological review
Choi, K., Yoon, J. W., Kim, M., Lee, H. J., Jeong, J., Ryu, M., Jo, C., & Lee, C. (2020) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12661 · Cited by 146 · see citing works
Biomaterial-based delivery for skeletal muscle repair
Cezar, C. A., & Mooney, D. J. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.09.008 · Cited by 142 · see citing works
Satellite Cells and Skeletal Muscle Regeneration
Dumont, N. A., Bentzinger, C. F., Sincennes, M., & Rudnicki, M. A. (2015) · Comprehensive physiology · doi:10.1002/j.2040-4603.2015.tb00646.x · Cited by 143 · see citing works
Théret, M., Rossi, F. M. V., & Contreras, O. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.673404 · Cited by 144 · see citing works
Starring or supporting role? Satellite cells and skeletal muscle fiber size regulation
Murach, K. A., Fry, C. S., Kirby, T. J., Jackson, J. R., Lee, J. D., White, S. H., Dupont-Versteegden, E. E., McCarthy, J. J., & Peterson, C. A. (2018) · Physiology · doi:10.1152/physiol.00019.2017 · Cited by 137 · see citing works
Hyldahl, R. D., Nelson, B., Xin, L., Welling, T., Groscost, L., Hubal, M. J., Chipkin, S. R., Clarkson, P. M., & Parcell, A. C. (2015) · The FASEB Journal · doi:10.1096/fj.14-266668 · Cited by 135 · see citing works
Gutiérrez, J. M., Escalante, T., Rucavado, A., Herrera, C., & Fox, J. W. (2016) · Toxins · doi:10.3390/toxins8100304 · Cited by 138 · 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
Bachman, J. F., Klose, A. M., Liu, W., Paris, N. D., Blanc, R. S., Schmalz, M., Knapp, E. K., & Chakkalakal, J. V. (2018) · Development · doi:10.1242/dev.167197 · Cited by 133 · see citing works
Collagen Type III and VI Turnover in Response to Long-Term Immobilization
Sun, S., Henriksen, K., Karsdal, M. A., Byrjalsen, I., Rittweger, J., Armbrecht, G., Belavý, D. L., Felsenberg, D., & Nedergaard, A. F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144525 · Cited by 132 · see citing works
Wang, Y. X., Dumont, N. A., & Rudnicki, M. A. (2014) · Journal of Cell Science · doi:10.1242/jcs.151209 · Cited by 125 · see citing works
Basement membrane collagens and disease mechanisms
Gatseva, A., Sin, Y. Y., Brezzo, G., & Agtmael, T. V. (2019) · Essays in Biochemistry · doi:10.1042/ebc20180071 · Cited by 125 · see citing works
Collagens in Cancer: Structural Regulators and Guardians of Cancer Progression
Martino, D. D., & Bravo‐Cordero, J. J. (2023) · Cancer Research · doi:10.1158/0008-5472.can-22-2034 · Cited by 127 · see citing works
Wang, C., Rabadan Ros, R., Martinez-Redondo, P., Ma, Z., Shi, L., Xue, Y., Guillen-Guillen, I., Huang, L., Hishida, T., Liao, H.-K., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23353-z · Cited by 119 · see citing works
Bidirectional roles of skeletal muscle fibro-adipogenic progenitors in homeostasis and disease
Chen, W., You, W., Valencak, T. G., & Shan, T. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101682 · Cited by 118 · see citing works
Ayoglu, B., Chaouch, A., Lochmüller, H., Politano, L., Bertini, E., Spitali, P., Hiller, M., Niks, E. H., Gualandi, F., Pontén, F., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201303724 · Cited by 116 · see citing works
Judge, S. M., Wu, C.-L., Beharry, A. W., Roberts, B. M., Ferreira, L. F., Kandarian, S. C., & Judge, A. R. (2014) · BMC Cancer · doi:10.1186/1471-2407-14-997 · Cited by 111 · see citing works
Instructive Roles of Extracellular Matrix on Autophagy
Neill, T., Schaefer, L., & Iozzo, R. V. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2014.05.010 · Cited by 112 · see citing works
Non-myogenic Contribution to Muscle Development and Homeostasis: The Role of Connective Tissues
Nassari, S., Duprez, D., & Fournier‐Thibault, C. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2017.00022 · Cited by 111 · see citing works
Collagen VI as a driver and disease biomarker in human fibrosis
Williams, L. M., Layton, T., Yang, N., Feldmann, M., & Nanchahal, J. (2021) · FEBS Journal · doi:10.1111/febs.16039 · Cited by 108 · see citing works
Estrogen Receptor β Controls Muscle Growth and Regeneration in Young Female Mice
Seko, D., Fujita, R., Kitajima, Y., Nakamura, K., Imai, Y., & Ono, Y. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.07.017 · Cited by 104 · see citing works
Tierney, M. T., Gromova, A., Sesillo, F. B., Sala, D., Spenlé, C., Orend, G., & Sacco, A. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.072 · Cited by 98 · see citing works
Loreti, M., & Sacco, A. (2022) · npj Regenerative Medicine · doi:10.1038/s41536-022-00204-z · Cited by 101 · see citing works
Towards stem cell therapies for skeletal muscle repair
Judson, R. N., & Rossi, F. M. V. (2020) · npj Regenerative Medicine · doi:10.1038/s41536-020-0094-3 · Cited by 102 · see citing works
Urbani, L., Camilli, C., Phylactopoulos, D.-E., Crowley, C., Natarajan, D., Scottoni, F., Maghsoudlou, P., McCann, C. J., Pellegata, A. F., Urciuolo, A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06385-w · Cited by 101 · see citing works
Self-citationNorris, S. C. P., Kawecki, N. S., Davis, A. R., Chen, K. K., & Rowat, A. C. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121669 · Cited by 102 · see citing works
CMG2/ANTXR2 regulates extracellular collagen VI which accumulates in hyaline fibromatosis syndrome
Bürgi, J., Kunz, B., Abrami, L., Deuquet, J., Piersigilli, A., Scholl‐Bürgi, S., Lausch, E. U., Unger, S., Superti‐Furga, A., Bonaldo, P., et al. (2017) · Nature Communications · doi:10.1038/ncomms15861 · Cited by 98 · see citing works
Self-citationSkeletal muscle in health and disease
Morgan, J. E., & Partridge, T. A. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.042192 · Cited by 95 · see citing works
Urciuolo, A., Urbani, L., Perin, S., Maghsoudlou, P., Scottoni, F., Gjinovci, A., Collins‐Hooper, H., Loukogeorgakis, S., Tyraskis, A., Torelli, S., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-26371-y · Cited by 98 · see citing works
Self-citationSteering cell behavior through mechanobiology in 3D: A regenerative medicine perspective
Zonderland, J., & Moroni, L. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120572 · Cited by 96 · see citing works
Rezza, A., Sennett, R., & Rendl, M. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00012-3 · Cited by 95 · see citing works
Muscle wasting in myotonic dystrophies: a model of premature aging
Mateos-Aierdi, A. J., Goicoechea, M., Aiastui, A., Fernández‐Torrón, R., García-Puga, M., Matheu, A., & de Munaín, A. L. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00125 · Cited by 92 · see citing works
One size does not fit all: developing a cell-specific niche for in vitro study of cell behavior
Marinkovic, M., Block, T. J., Rakian, R., Li, Q., Wang, E., Reilly, M. A., Dean, D. D., & Chen, X. (2016) · Matrix Biology · doi:10.1016/j.matbio.2016.01.004 · Cited by 95 · see citing works
Chaturvedi, V., Dye, D. E., Kinnear, B. F., Kuppevelt, T. H. V., Grounds, M. D., & Coombe, D. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127675 · Cited by 95 · see citing works
Programming hydrogels to probe spatiotemporal cell biology
Qazi, T. H., Blatchley, M. R., Davidson, M. D., Yavitt, F. M., Cooke, M. E., Anseth, K. S., & Burdick, J. A. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.03.013 · Cited by 96 · see citing works
Fibrosis development in early-onset muscular dystrophies: Mechanisms and translational implications
Serrano, A. L., & Muñoz‐Cánoves, P. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.09.013 · Cited by 94 · see citing works
Noehren, B. W., Kosmac, K., Walton, R. G., Murach, K. A., Lyles, M. F., Loeser, R. F., Peterson, C. A., & Messier, S. P. (2018) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2018.05.011 · Cited by 93 · see citing works
Chellini, F., Tani, A., Zecchi‐Orlandini, S., & Sassoli, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030683 · Cited by 87 · see citing works
The Many Roles of Macrophages in Skeletal Muscle Injury and Repair
Wang, X., & Zhou, L. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.952249 · Cited by 92 · see citing works
Decellularized Tissue for Muscle Regeneration
Urciuolo, A., & Coppi, P. D. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082392 · Cited by 86 · see citing works
Self-citationFry, C. S., Johnson, D. L., Ireland, M. L., & Noehren, B. W. (2016) · Journal of Orthopaedic Research® · doi:10.1002/jor.23502 · Cited by 85 · see citing works
Ahmad, K., Shaikh, S., Chun, H. J., Ali, S. M., Lim, J. H., Ahmad, S. S., Lee, E. J., & Choi, I. (2023) · Inflammation and Regeneration · doi:10.1186/s41232-023-00308-z · Cited by 85 · 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
Smith, L., Cho, S., & Discher, D. E. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.05.025 · Cited by 78 · see citing works
Defining and identifying satellite cell-opathies within muscular dystrophies and myopathies
Ganassi, M., Francesco Muntoni, A., & Zammit, P. S. (2021) · Experimental Cell Research · doi:10.1016/j.yexcr.2021.112906 · Cited by 80 · see citing works
Tiskratok, W., Chuinsiri, N., Limraksasin, P., Kyawsoewin, M., & Jitprasertwong, P. (2025) · Polymers · doi:10.3390/polym17060822 · Cited by 88 · see citing works
Combining insoluble and soluble factors to steer stem cell fate
Dingal, P. C. D. P., & Discher, D. E. (2014) · Nature Materials · doi:10.1038/nmat3997 · Cited by 80 · see citing works
Chapman, M., Mukund, K., Subramaniam, S., Brenner, D. A., & Lieber, R. L. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00226.2016 · Cited by 77 · see citing works
The role of satellite cells in muscle hypertrophy
Blaauw, B., & Reggiani, C. (2014) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-014-9376-y · Cited by 78 · see citing works
Self-citationFarup, J., Rahbek, S. K., Knudsen, I. S., de Paoli, F. V., Mackey, A. L., & Vissing, K. (2014) · Amino Acids · doi:10.1007/s00726-014-1810-3 · Cited by 78 · see citing works
Skeletal Muscle Regeneration in Cardiotoxin-Induced Muscle Injury Models
Wang, Y., Lu, J., & Liu, Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113380 · Cited by 77 · see citing works
- Authors
- Urciuolo, A., Quarta, M., Morbidoni, V., Gattazzo, F., Molon, S., Grumati, P., Montemurro, F., Tedesco, F. S., Blaauw, B., Cossu, G., Vozzi, G., Rando, T. A., & Bonaldo, P.
- Affiliations
- University of Padua (IT)
- Stanford Medicine (US)
- University of Pisa (IT)
- University College London (GB)
- Corresponding author
- Rando, Thomas A.
- Bonaldo, Paolo
- ORCID
- Venue
- Nature Communications
- Published
- 2013-06-07
- Volume
- 4
- Issue
- 1
- Pages
- 1964-1964
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC3682802
- OpenAlex
- W2001061424
- Cited by
- 511
- References
- 41
- Citations by year
- 2026: 31 · 2025: 38 · 2024: 42 · 2023: 35 · 2022: 34 · 2021: 53 · 2020: 57 · 2019: 37 · 2018: 37 · 2017: 40 · 2016: 38 · 2015: 35 · 2014: 27 · 2013: 7
- FWCI
- 15.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Funders
- U.S. Department of Veterans Affairs (P01 AG036695)
- Glenn Foundation for Medical Research (P01 AG036695)
- Fondation pour la Recherche Médicale
- Ministero dell’Istruzione, dell’Università e della Ricerca (GGP11082, RBAP11Z3YA_003)
- Università degli Studi di Padova (GGP11082)
- National Institutes of Health (DP1OD000392, AG036695)
- Medical Research Council (MR/K000608/1)
- National Institute on Aging (R37AG023806, R01AG023806, P01AG036695)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01 AR56849, R01AR062185, R01AR056849)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Genetics › Neurogenetic and Muscular Disorders Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- collagen VI, satellite cells, muscle stem cells, self-renewal, muscle regeneration, extracellular matrix, muscle stiffness, muscle mechanics, muscle damage
- MeSH terms
- Animals, Extracellular Space, Fibroblasts, Fluorescent Antibody Technique, Mice, Inbred C57BL, Regeneration, Transcription Factors, Muscle, Skeletal, Microscopy, Confocal, Collagen Type VI, Satellite Cells, Skeletal Muscle, Cell Proliferation, Mice, Elastic Modulus, Stem Cell Niche, In Vitro Techniques
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