Self-renewal and expansion of single transplanted muscle stem cells
Open accessAbstract
Adult muscle satellite cells have a principal role in postnatal skeletal muscle growth and regeneration. Satellite cells reside as quiescent cells underneath the basal lamina that surrounds muscle fibres and respond to damage by giving rise to transient amplifying cells (progenitors) and myoblasts that fuse with myofibres. Recent experiments showed that, in contrast to cultured myoblasts, satellite cells freshly isolated or satellite cells derived from the transplantation of one intact myofibre contribute robustly to muscle repair. However, because satellite cells are known to be heterogeneous, clonal analysis is required to demonstrate stem cell function. Here we show that when a single luciferase-expressing muscle stem cell is transplanted into the muscle of mice it is capable of extensive proliferation, contributes to muscle fibres, and Pax7(+)luciferase(+) mononucleated cells can be readily re-isolated, providing evidence of muscle stem cell self-renewal. In addition, we show using in vivo bioluminescence imaging that the dynamics of muscle stem cell behaviour during muscle repair can be followed in a manner not possible using traditional retrospective histological analyses. By imaging luciferase activity, real-time quantitative and kinetic analyses show that donor-derived muscle stem cells proliferate and engraft rapidly after injection until homeostasis is reached. On injury, donor-derived mononucleated cells generate massive waves of cell proliferation. Together, these results show that the progeny of a single luciferase-expressing muscle stem cell can both self-renew and differentiate after transplantation in mice, providing new evidence at the clonal level that self-renewal is an autonomous property of a single adult muscle stem cell.
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?
In mice, transplantation of satellite cells into damaged muscle leads to self-renewal and muscle regeneration.
“In mice, transplantation of satellite cells into damaged muscle leads to self-renewal and muscle regeneration466,467.”
From Sarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies (2018) · cites this paper as [467]
Dedicated muscle stem cells, also called satellite cells, support repair of skeletal muscle.
“Skeletal muscle repair is facilitated by a population of dedicated muscle stem cells (MuSCs), also known as satellite cells, that reside in anatomically defined niches within muscle tissues.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [10]
Multiple rounds of self-renewing divisions by MuSCs are required for their regenerative function, as shown by transplantation, genetic ablation, and lineage tracing.
“Subsequently, MuSCs undergo multiple rounds of self-renewing divisions that are essential to their function in regeneration, as demonstrated by transplantation, genetic ablation, and lineage tracing experiments5–12.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [10]
Single MuSCs can produce thousands of progeny, differentiate into myofibers, and self-renew after re-injury.
“By using BLI, single MuSCs isolated from transgenic mice that ubiquitously express a luciferase transgene were shown to give rise to thousands of progeny, differentiate into myofibers, and self-renew upon re-injury10.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [10]
Muscle stem cells were isolated by FACS to greater than 90% purity for all genotypes.
“MuSC were then isolated by FACS to >90% purity for all genotypes (Fig. S4), as previously described (Sacco et al., 2008)”
From Short Telomeres and Stem Cell Exhaustion Model Duchenne Muscular Dystrophy in mdx/mTR Mice (2010) · cites this paper as Sacco et al., 2008
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
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
Cellular and Molecular Regulation of Muscle Regeneration
CHARGÉ, S. B. P., & Rudnicki, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00019.2003 · Cited by 2,691 · see citing works
Pax7 Is Required for the Specification of Myogenic Satellite Cells
Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruß, P., & Rudnicki, M. A. (2000) · Cell · doi:10.1016/s0092-8674(00)00066-0 · Cited by 2,345 · see citing works
Long-Term Lymphohematopoietic Reconstitution by a Single CD34-Low/Negative Hematopoietic Stem Cell
Osawa, M., Hanada, K., Hamada, H., & Nakauchi, H. (1996) · Science · doi:10.1126/science.273.5272.242 · Cited by 2,141 · see citing works
Asymmetric self-renewal and commitment of satellite stem cells in muscle
Kuang, S., Kuroda, K., Le Grand, F., & Rudnicki, M. A. (2007) · Cell · doi:10.1016/j.cell.2007.03.044 · Cited by 1,449 · see citing works
Collins, C. A., Olsen, I., Zammit, P. S., Heslop, L., Petrie, A., Partridge, T. A., & Morgan, J. E. (2005) · Cell · doi:10.1016/j.cell.2005.05.010 · Cited by 1,445 · see citing works
Direct Isolation of Satellite Cells for Skeletal Muscle Regeneration
Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T., & Buckingham, M. (2005) · Science · doi:10.1126/science.1114758 · Cited by 1,100 · see citing works
Rando, T. A., & Blau, H. M. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.6.1275 · Cited by 944 · see citing works
Self-citationMuscle 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
Isolation of Adult Mouse Myogenic Progenitors
Sherwood, R. I., Christensen, J. L., Conboy, I. M., Conboy, M. J., Rando, T. A., Weissman, I. L., & Wagers, A. J. (2004) · Cell · doi:10.1016/j.cell.2004.10.021 · Cited by 491 · see citing works
Highly Efficient, Functional Engraftment of Skeletal Muscle Stem Cells in Dystrophic Muscles
Cerletti, M., Jurga, S., Witczak, C. A., Hirshman, M. F., Shadrach, J. L., Goodyear, L. J., & Wagers, A. J. (2008) · Cell · doi:10.1016/j.cell.2008.05.049 · Cited by 472 · see citing works
Shifting foci of hematopoiesis during reconstitution from single stem cells
Cao, Y., Wagers, A. J., Beilhack, A., Dusich, J., Bachmann, M. H., Negrin, R. S., Weissman, I. L., & Contag, C. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2637010100 · Cited by 337 · see citing works
Derivation of engraftable skeletal myoblasts from human embryonic stem cells
Barberi, T., Bradbury, M. S., Dincer, Z., Panagiotakos, G., Socci, N. D., & Studer, L. (2007) · Nature Medicine · doi:10.1038/nm1533 · Cited by 331 · see citing works
The fate of individual myoblasts after transplantation into muscles of DMD patients
Gussoni, E., Blau, H. M., & Kunkel, L. M. (1997) · Nature Medicine · doi:10.1038/nm0997-970 · Cited by 326 · see citing works
Self-citationZammit, P. S., Heslop, L., Hudon, V., Rosenblatt, J. D., Tajbakhsh, S., BUCKINGHAM, M. E., Beauchamp, J. R., & Partridge, T. A. (2002) · Experimental Cell Research · doi:10.1006/excr.2002.5653 · Cited by 306 · see citing works
Evidence for a myogenic stem cell that is exhausted in dystrophic muscle
Heslop, L., Morgan, J. E., & Partridge, T. A. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.12.2299 · Cited by 297 · see citing works
Developmental progression of myosin gene expression in cultured muscle cells
Silberstein, L., Webster, S. G., Travis, M. A., & Blau, H. M. (1986) · Cell · doi:10.1016/0092-8674(86)90707-5 · Cited by 180 · see citing works
Self-citationBoutet, S. C., Disatnik, M., Chan, L. S., Iori, K., & Rando, T. A. (2007) · Cell · doi:10.1016/j.cell.2007.05.044 · Cited by 179 · see citing works
Harris, J. B., & Johnson, M. A. (1978) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1978.tb00714.x · Cited by 162 · see citing works
X‐Irradiation improves mdx mouse muscle as a model of myofiber loss in DMD
Wakeford, S., Watt, D. J., & Partridge, T. A. (1991) · Muscle & Nerve · doi:10.1002/mus.880140108 · Cited by 144 · see citing works
Wehrman, T. S., von Degenfeld, G., Krutzik, P. O., Nolan, G. P., & Blau, H. M. (2006) · Nature Methods · doi:10.1038/nmeth868 · Cited by 132 · see citing works
Self-citationSouthwood, C. M., Downs, K. M., & Bieker, J. J. (1996) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199607)206:3 · Cited by 108 · see citing works
The Fate of Myoblasts Following Transplantation into Mature Muscle
Rando, T. A., Pavlath, G. K., & Blau, H. M. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1329 · Cited by 85 · see citing works
Self-citationSacco, A., Doyonnas, R., LaBarge, M. A., Hammer, M. M., Kraft, P. E., & Blau, H. M. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200506123 · Cited by 67 · see citing works
Self-citationRetroviral Lineage Markers for Assessing Myoblast Fate In Vivo
Blau, H. M., & Hughes, S. M. (1990) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-5865-7_22 · Cited by 11 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Satellite Cells and the Muscle Stem Cell Niche
Yin, H., Price, F., & Rudnicki, M. A. (2013) · Physiological Reviews · doi:10.1152/physrev.00043.2011 · Cited by 2,166 · see citing works
Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis
Joe, A. W. B., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M. A., & Rossi, F. M. V. (2010) · Nature Cell Biology · doi:10.1038/ncb2015 · Cited by 1,690 · 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
Self-citationBarczyk, M., Carracedo, S., & Gullberg, D. (2010) · Cell and Tissue Research · doi:10.1007/s00441-009-0834-6 · Cited by 1,512 · see citing works
Sarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies
Batsis, J. A., & Villareal, D. T. (2018) · Nature Reviews Endocrinology · doi:10.1038/s41574-018-0062-9 · Cited by 1,382 · see citing works
Murphy, M. M., Lawson, J. A., Mathew, S. J., Hutcheson, D. A., & Kardon, G. (2011) · Development · doi:10.1242/dev.064162 · Cited by 1,249 · 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
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
Relaix, F., & Zammit, P. S. (2012) · Development · doi:10.1242/dev.069088 · Cited by 888 · see citing works
The aged niche disrupts muscle stem cell quiescence
Chakkalakal, J. V., Jones, K. M., Basson, M. A., & Brack, A. S. (2012) · Nature · doi:10.1038/nature11438 · Cited by 851 · see citing works
Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis
Braun, T., & Gautel, M. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3118 · Cited by 713 · 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
Rejuvenation of the muscle stem cell population restores strength to injured aged muscles
Cosgrove, B. D., Gilbert, P. M., Porpiglia, E., Mourkioti, F., Lee, S. P., Corbel, S. Y., Llewellyn, M. E., Delp, S. L., & Blau, H. M. (2014) · Nature Medicine · doi:10.1038/nm.3464 · Cited by 677 · 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
Effective fiber hypertrophy in satellite cell-depleted skeletal muscle
McCarthy, J. J., Mula, J., Miyazaki, M., Erfani, R., Garrison, K., Farooqui, A. B., Srikuea, R., Lawson, B. A., Grimes, B., Keller, C., et al. (2011) · Development · doi:10.1242/dev.068858 · Cited by 616 · see citing works
Lee, C. H., Cook, J. L., Mendelson, A., Moioli, E. K., Yao, H., & Mao, J. J. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60668-x · Cited by 614 · see citing works
Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements
Lepper, C., Conway, S. J., & Fan, C. (2009) · Nature · doi:10.1038/nature08209 · Cited by 580 · see citing works
de Lageneste, O. D., Julien, A., Abou-Khalil, R., Frangi, G., Carvalho, C., Cagnard, N., Cordier, C., Conway, S. J., & Colnot, C. (2018) · Nature Communications · doi:10.1038/s41467-018-03124-z · Cited by 559 · see citing works
Grand, 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
Short Telomeres and Stem Cell Exhaustion Model Duchenne Muscular Dystrophy in mdx/mTR Mice
Sacco, A., Mourkioti, F., Tran, R., Choi, J., Llewellyn, M., Kraft, P., Shkreli, M., Delp, S., Pomerantz, J. H., Artandi, S. E., et al. (2010) · Cell · doi:10.1016/j.cell.2010.11.039 · Cited by 512 · see citing works
Self-citationComparative Study of Injury Models for Studying Muscle Regeneration in Mice
Hardy, D., Besnard, A., Latil, M., Jouvion, G., Briand, D., Thépenier, C., Pascal, Q., Guguin, A., Gayraud-Morel, B., Cavaillon, J., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147198 · Cited by 508 · see citing works
Rocheteau, P., Gayraud-Morel, B., Siegl-Cachedenier, I., Blasco, M. A., & Tajbakhsh, S. (2012) · Cell · doi:10.1016/j.cell.2011.11.049 · Cited by 510 · see citing works
Li, F., Huang, Q., Jiang, C., Peng, Y., Roop, D. R., Bedford, J. S., & Li, C. (2010) · Science Signaling · doi:10.1126/scisignal.2000634 · Cited by 494 · 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
Single-cell bioluminescence imaging of deep tissue in freely moving animals
Iwano, S., Sugiyama, M., Hama, H., Watakabe, A., Hasegawa, N., Kuchimaru, T., Tanaka, K. Z., Takahashi, M., Ishida, Y., Hata, J., et al. (2018) · Science · doi:10.1126/science.aaq1067 · Cited by 478 · see citing works
Darabi, R., Arpke, R. W., Irion, S., Dimos, J. T., Grskovic, M., Kyba, M., & Perlingeiro, R. C. R. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.02.015 · Cited by 481 · 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
Self-citationMitchell, K. J., Pannérec, A., Cadot, B., Parlakian, A., Besson, V., Gomes, E. R., Marazzi, G., & Sassoon, D. A. (2010) · Nature Cell Biology · doi:10.1038/ncb2025 · Cited by 442 · see citing works
Qazi, T., Mooney, D., Pumberger, M., Geissler, S., & Duda, G. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.02.110 · Cited by 386 · see citing works
Advances in understanding tissue regenerative capacity and mechanisms in animals
Poss, K. D. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2879 · Cited by 428 · see citing works
Tissue-specific stem cells: Lessons from the skeletal muscle satellite cell
Brack, A. S., & Rando, T. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.04.001 · Cited by 409 · see citing works
STAT3 signaling controls satellite cell expansion and skeletal muscle repair
Tierney, M. T., Aydogdu, T., Sala, D., Malecova, B., Gatto, S., Puri, P. L., Latella, L., & Sacco, A. (2014) · Nature Medicine · doi:10.1038/nm.3656 · Cited by 401 · see citing works
Self-citationIsolation of skeletal muscle stem cells by fluorescence-activated cell sorting
Liu, L. A., Cheung, T. H., Charville, G. W., & Rando, T. A. (2015) · Nature Protocols · doi:10.1038/nprot.2015.110 · Cited by 396 · see citing works
Stem Cells and the Niche: A Dynamic Duo
Voog, J., & Jones, D. L. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.01.011 · Cited by 401 · see citing works
Short-Term Calorie Restriction Enhances Skeletal Muscle Stem Cell Function
Cerletti, M., Jang, Y. C., Finley, L. W. S., Haigis, M. C., & Wagers, A. J. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.04.002 · Cited by 397 · see citing works
High-Dimensional Single-Cell Cartography Reveals Novel Skeletal Muscle-Resident Cell Populations
Giordani, L., He, G. J., Négroni, E., Sakai, H., Law, J., Siu, M. M., Wan, R., Corneau, A., Tajbakhsh, S., Cheung, T. H., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.02.026 · Cited by 389 · see citing works
Palacios, D., Mozzetta, C., Consalvi, S., Caretti, G., Saccone, V., Proserpio, V., Marquez, V. E., Valente, S., Mai, A., Forcales, S. V., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.013 · Cited by 392 · see citing works
Chen, F., Wu, L., Zhang, M., Zhang, R., & Sun, H. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2010.12.032 · Cited by 379 · see citing works
De Micheli, A. J., Laurilliard, E. J., Heinke, C. L., Ravichandran, H., Fraczek, P., Soueid-Baumgarten, S., De Vlaminck, I., Elemento, O., & Cosgrove, B. D. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.067 · Cited by 373 · see citing works
Uraemic sarcopenia: aetiology and implications
Fahal, I. H. (2013) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gft070 · Cited by 358 · 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
Skeletal muscle stem cells in developmental versus regenerative myogenesis
Tajbakhsh, S. (2009) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2009.02158.x · Cited by 333 · 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
Self-citationMolecular 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
Regulatory factors and cell populations involved in skeletal muscle regeneration
Broek, R. W. T., Grefte, S., & den Hoff, J. W. V. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22127 · Cited by 315 · see citing works
Chal, J., Tanoury, Z. A., Hestin, M., Gobert, B., Aivio, S., Hick, A., Cherrier, T., Nesmith, A. P., Parker, K. K., & Pourquié, O. (2016) · Nature Protocols · doi:10.1038/nprot.2016.110 · Cited by 306 · see citing works
Identification and characterization of PDGFRα+ mesenchymal progenitors in human skeletal muscle
Uezumi, A., Fukada, S., Yamamoto, N., Ikemoto‐Uezumi, M., Nakatani, M., Morita, M., Yamaguchi, A., Yamada, H., Nishino, I., Hamada, Y., et al. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.161 · Cited by 304 · see citing works
Bioluminescence imaging: progress and applications
Badr, C. E., & Tannous, B. A. (2011) · Trends in biotechnology · doi:10.1016/j.tibtech.2011.06.010 · Cited by 293 · see citing works
Quarta, M., Cromie, M. J., Chacon, R., Blonigan, J., Garcia, V., Akimenko, I., Hamer, M., Paine, P., Stok, M., Shrager, J. B., et al. (2017) · Nature Communications · doi:10.1038/ncomms15613 · Cited by 280 · see citing works
Joe, A. W., Yi, L., Even, Y., Vogl, A. W., & Rossi, F. M. V. (2009) · Stem Cells · doi:10.1002/stem.190 · Cited by 278 · see citing works
Zahir, N., & Tuan, R. S. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21940 · Cited by 271 · see citing works
Troy, A., Cadwallader, A. B., Fedorov, Y., Tyner, K., Tanaka, K. K., & Olwin, B. B. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.05.025 · Cited by 268 · see citing works
Mozzetta, C., Consalvi, S., Saccone, V., Tierney, M. T., Diamantini, A., Mitchell, K. J., Marazzi, G., Borsellino, G., Battistini, L., Sassoon, D. A., et al. (2013) · EMBO Molecular Medicine · doi:10.1002/emmm.201202096 · Cited by 261 · see citing works
Self-citationGuided by the light: visualizing biomolecular processes in living animals with bioluminescence
Prescher, J. A., & Contag, C. H. (2009) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2009.11.001 · Cited by 257 · see citing works
Day, K., Shefer, G., Shearer, A., & Yablonka-Reuveni, Z. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.01.006 · Cited by 254 · see citing works
Muscle 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
Kelly, K. K., Hall, J. K., Troy, A. A., Cornelison, D., Majka, S. M., & Olwin, B. B. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.01.016 · Cited by 249 · see citing works
Zismanov, V., Chichkov, V., Colangelo, V., Jamet, S., Wang, S., Syme, A., Koromilas, A. E., & Crist, C. G. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.09.020 · Cited by 247 · see citing works
Juhas, M., Engelmayr, G. C., Fontanella, A. N., Palmer, G. M., & Bursac, N. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402723111 · Cited by 246 · see citing works
Biomimetic Scaffolds for Regeneration of Volumetric Muscle Loss in Skeletal Muscle Injuries
Grasman, J., Zayas, M. T., Page, R., & Pins, G. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.07.038 · Cited by 233 · see citing works
Regulation of adult stem cell quiescence and its functions in the maintenance of tissue integrity
de Morrée, A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00568-6 · Cited by 243 · see citing works
Dell'Orso, S., Juan, A. H., Ko, K.-D., Naz, F., Perovanovic, J., Gutierrez-Cruz, G., Feng, X., & Sartorelli, V. (2019) · Development · doi:10.1242/dev.174177 · Cited by 243 · see citing works
Ho, A. T. V., Palla, A. R., Blake, M. R., Yucel, N. D., Wang, Y. X., Magnusson, K. E. G., Holbrook, C. A., Kraft, P. E., Delp, S. L., & Blau, H. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1705420114 · Cited by 244 · see citing works
Self-citationIn situ tissue regeneration through host stem cell recruitment
Ko, I. K., Lee, S. J., Atala, A., & Yoo, J. J. (2013) · Experimental & Molecular Medicine · doi:10.1038/emm.2013.118 · Cited by 241 · see citing works
Inhibition of prostaglandin-degrading enzyme 15-PGDH rejuvenates aged muscle mass and strength
Palla, A. R., Ravichandran, M., Wang, Y. X., Alexandrova, L., Yang, A. V., Kraft, P., Holbrook, C. A., Schürch, C. M., Ho, A. T. V., & Blau, H. M. (2021) · Science · doi:10.1126/science.abc8059 · Cited by 232 · see citing works
Self-citationOrienting Muscle Stem Cells for Regeneration in Homeostasis, Aging, and Disease
Feige, P., Brun, C. E., Ritso, M., & Rudnicki, M. A. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.10.006 · Cited by 227 · see citing works
Chu, J., Haynes, R. D., Corbel, S. Y., Li, P., González-González, E., Burg, J. S., Ataie, N., Lam, A. J., Cranfill, P. J. C., Baird, M. A., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2888 · Cited by 221 · see citing works
Self-citationLütolf, M. P., & Blau, H. M. (2009) · Advanced Materials · doi:10.1002/adma.200802582 · Cited by 221 · see citing works
Self-citationOno, Y., Boldrin, L., Knopp, P., Morgan, J. E., & Zammit, P. S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.005 · Cited by 217 · see citing works
Shefer, G., Rauner, G., Yablonka‐Reuveni, Z., & Benayahu, D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013307 · Cited by 211 · see citing works
Clark, A. Y., Martin, K. E., García, J. R., Johnson, C. T., Theriault, H. S., Han, W. M., Zhou, D. W., Botchwey, E. A., & Garcı́a, A. J. (2020) · Nature Communications · doi:10.1038/s41467-019-14000-9 · Cited by 208 · see citing works
Genetic Background Affects Properties of Satellite Cells and mdx Phenotypes
Fukada, S., Morikawa, D., Yamamoto, Y., Yoshida, T., Sumie, N., Yamaguchi, M., Ito, T., Miyagoe‐Suzuki, Y., Takeda, S., Tsujikawa, K., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090887 · Cited by 203 · see citing works
Close, D. M., Xu, T., Sayler, G. S., & Ripp, S. A. (2010) · Sensors · doi:10.3390/s110100180 · Cited by 206 · see citing works
ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs
Hicks, M. R., Hiserodt, J., Paras, K. I., Fujiwara, W., Eskin, A., Jan, M., Xi, H., Young, C. S., Evseenko, D. A., Nelson, S. F., et al. (2017) · Nature Cell Biology · doi:10.1038/s41556-017-0010-2 · Cited by 194 · see citing works
CD157 Marks Tissue-Resident Endothelial Stem Cells with Homeostatic and Regenerative Properties
Wakabayashi, T., Naito, H., Suehiro, J., Lin, Y., Kawaji, H., Iba, T., Kouno, T., Ishikawa-Kato, S., Furuno, M., Takara, K., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.01.010 · 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
Combination of inflammation-related cytokines promotes long-term muscle stem cell expansion
Fu, X., Xiao, J., Wei, Y., Li, S., Liu, Y., Yin, J., Sun, K., Sun, H., Wang, H., Zhang, Z., et al. (2015) · Cell Research · doi:10.1038/cr.2015.58 · Cited by 196 · see citing works
Ex Vivo Expansion and In Vivo Self-Renewal of Human Muscle Stem Cells
Charville, G. W., Cheung, T. H., Yoo, B., Santos, P. J. F., Lee, G., Shrager, J. B., & Rando, T. A. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.08.004 · Cited by 196 · see citing works
The therapeutic potential of stem cells
Watt, F. M., & Driskell, R. R. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0149 · Cited by 199 · see citing works
Judson, R. N., Tremblay, A. M., Knopp, P., White, R. B., Urcia, R., De Bari, C., Zammit, P. S., Camargo, F. D., & Wackerhage, H. (2012) · Journal of Cell Science · doi:10.1242/jcs.109546 · Cited by 190 · see citing works
Transient Inactivation of Rb and ARF Yields Regenerative Cells from Postmitotic Mammalian Muscle
Pajcini, K. V., Corbel, S. Y., Sage, J., Pomerantz, J. H., & Blau, H. M. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.05.022 · Cited by 188 · see citing works
Self-citationInjectable, rapid gelling and highly flexible hydrogel composites as growth factor and cell carriers
Wang, F., Li, Z., Khan, M., Tamama, K., Kuppusamy, P., Wagner, W. R., Sen, C. K., & Guan, J. (2009) · Acta Biomaterialia · doi:10.1016/j.actbio.2009.12.011 · Cited by 188 · see citing works
Chen, P., Tao, J., Zhu, S., Cai, Y., Mao, Q., Yu, D., Dai, J., & Ouyang, H. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.10.049 · Cited by 188 · see citing works
Isolation and Culture of Skeletal Muscle Myofibers as a Means to Analyze Satellite Cells
Keire, P. A., Shearer, A. M., Shefer, G., & Yablonka‐Reuveni, Z. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-128-8_28 · Cited by 187 · see citing works
Danoviz, M. E., & Yablonka‐Reuveni, Z. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-343-1_2 · Cited by 182 · see citing works
Snippert, H. J. G., & Clevers, H. C. (2011) · EMBO Reports · doi:10.1038/embor.2010.216 · Cited by 180 · 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
MyoD regulates apoptosis of myoblasts through microRNA-mediated down-regulation of Pax3
Hirai, H., Verma, M., Watanabe, S., Tastad, C., Asakura, Y., & Asakura, A. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201006025 · Cited by 177 · see citing works
Chang, N. C., & Rudnicki, M. A. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00006-8 · Cited by 180 · see citing works
Defining Adult Stem Cell Function at Its Simplest: The Ability to Replace Lost Cells through Mitosis
Post, Y., & Clevers, H. C. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.07.002 · Cited by 176 · 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
Therapeutic Strategies for Duchenne Muscular Dystrophy: An Update
Sun, C., Shen, L., Zhang, Z., & Xie, X. (2020) · Genes · doi:10.3390/genes11080837 · Cited by 175 · see citing works
A Zebrafish Embryo Culture System Defines Factors that Promote Vertebrate Myogenesis across Species
Xu, C., Tabebordbar, M., Iovino, S., Ciarlo, C., Liu, J.-X., Castiglioni, A., Price, E. N., Liu, M., Barton, E. R., Kahn, C. R., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.023 · Cited by 168 · see citing works
Attributes of adult stem cells
Alison, M., & Islam, S. (2008) · The Journal of Pathology · doi:10.1002/path.2498 · Cited by 172 · see citing works
Heterogeneity in the muscle satellite cell population
Biressi, S., & Rando, T. A. (2010) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2010.09.003 · Cited by 168 · see citing works
Gnocchi, V. F., White, R. B., Ono, Y., Ellis, J. A., & Zammit, P. S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005205 · Cited by 166 · see citing works
Roles 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
Engineering Stem and Stromal Cell Therapies for Musculoskeletal Tissue Repair
Loebel, C., & Burdick, J. A. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.01.014 · Cited by 166 · see citing works
Xi, H., Langerman, J., Sabri, S., Chien, P., Young, C. S., Younesi, S., Hicks, M. R., Gonzalez, K. M., Fujiwara, W., Marzi, J., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.04.017 · Cited by 156 · see citing works
The Skeletal Muscle Satellite Cell
Yablonka‐Reuveni, Z. (2011) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155411426780 · Cited by 164 · see citing works
- Authors
- Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S., & Blau, H. M.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Blau, Helen M.
- Venue
- Nature
- Published
- 2008-09-17
- Volume
- 456
- Issue
- 7221
- Pages
- 502-506
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2919355
- OpenAlex
- W2031495223
- Cited by
- 901
- References
- 26
- Citations by year
- 2026: 20 · 2025: 36 · 2024: 37 · 2023: 47 · 2022: 46 · 2021: 54 · 2020: 59 · 2019: 58 · 2018: 52 · 2017: 51 · 2016: 46 · 2015: 66 · 2014: 50 · 2013: 60 · 2012: 67
- FWCI
- 20.59
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG009521, AG 024987, R37AG009521, R01AG009521, R01AG020961, R01AG024987)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- satellite cells, muscle stem cells, self-renewal, clonal analysis, single-cell transplantation, Pax7, muscle regeneration, muscle damage, bioluminescence imaging, cell proliferation, skeletal muscle
- MeSH terms
- Animals, Cells, Cultured, Homeostasis, Luminescent Measurements, Muscles, Regeneration, Stem Cells, Antigens, CD, Muscle Fibers, Skeletal, Antigens, CD34, Satellite Cells, Skeletal Muscle, Stem Cell Transplantation, Integrin alpha Chains, Cell Proliferation, Mice
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