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A Subpopulation of Adult Skeletal Muscle Stem Cells Retains All Template DNA Strands after Cell Division
Open accessAbstract
Satellite cells are adult skeletal muscle stem cells that are quiescent and constitute a poorly defined heterogeneous population. Using transgenic Tg:Pax7-nGFP mice, we show that Pax7-nGFP(Hi) cells are less primed for commitment and have a lower metabolic status and delayed first mitosis compared to Pax7-nGFP(Lo) cells. Pax7-nGFP(Hi) can give rise to Pax7-nGFP(Lo) cells after serial transplantations. Proliferating Pax7-nGFP(Hi) cells exhibit lower metabolic activity, and the majority performs asymmetric DNA segregation during cell division, wherein daughter cells retaining template DNA strands express stem cell markers. Using chromosome orientation-fluorescence in situ hybridization, we demonstrate that all chromatids segregate asymmetrically, whereas Pax7-nGFP(Lo) cells perform random DNA segregation. Therefore, quiescent Pax7-nGFP(Hi) cells represent a reversible dormant stem cell state, and during muscle regeneration, Pax7-nGFP(Hi) cells generate distinct daughter cell fates by asymmetrically segregating template DNA strands to the stem cell. These findings provide major insights into the biology of stem cells that segregate DNA asymmetrically.
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“There is mounting evidence of asymmetric chromosome segregation in stem cells such as MuSCs17,18,129, ISCs20,130,131 and NSCs132.”
From Molecular regulation of stem cell quiescence (2013) · cites this paper as [129]
In the citing paper
“In muscle, MuSCs also exist as a heterogeneous quiescent population in adult mice30–33, with changes in heterogeneity with ageing32,34,35.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [31]
Citations
Cites
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
Wilson, A., Laurenti, E., Oser, G., van der Wath, R. C., Blanco-Bose, W., Jaworski, M., Offner, S., Dunant, C. F., Eshkind, L., Bockamp, E., et al. (2008) · Cell · doi:10.1016/j.cell.2008.10.048 · Cited by 1,908
Socializing with the Neighbors
Fuchs, E. V., Tumbar, T., & Guasch, G. (2004) · Cell · doi:10.1016/s0092-8674(04)00255-7 · Cited by 1,737
Mutation selection and the natural history of cancer
Cairns, J. (1975) · Nature · doi:10.1038/255197a0 · Cited by 1,592
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 · cited 1×
“Compelling evidence points to heterogeneity among quiescent muscle stem cells, regarding their gene expression signature and their functional properties (Biressi et al., 2007; Kuang et al., 2007; Kuang and Rudnicki, 2008; Shinin et al., 2006; Tajbakhsh, 2009).”
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
Coexistence of Quiescent and Active Adult Stem Cells in Mammals
Li, L., & Clevers, H. (2010) · Science · doi:10.1126/science.1180794 · Cited by 1,247
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
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
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
Expression of Cd34 and Myf5 Defines the Majority of Quiescent Adult Skeletal Muscle Satellite Cells
Beauchamp, J. R., Heslop, L., Yu, D. S., Tajbakhsh, S., Kelly, R. G., Wernig, A., BUCKINGHAM, M. E., Partridge, T. A., & Zammit, P. S. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.6.1221 · Cited by 917
Self-citationSelf-renewal and expansion of single transplanted muscle stem cells
Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S., & Blau, H. M. (2008) · Nature · doi:10.1038/nature07384 · Cited by 901
Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells
Relaix, F., Montarras, D., Zaffran, S., Gayraud-Morel, B., Rocancourt, D., Tajbakhsh, S., Mansouri, A., Cumano, A., & BUCKINGHAM, M. E. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200508044 · Cited by 736
Self-citationThe 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
Intestinal stem cells protect their genome by selective segregation of template DNA strands
Potten, C. S., Owen, G., & Booth, D. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.11.2381 · Cited by 633
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
Oustanina, S., Hause, G., & Braun, T. W. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600346 · Cited by 531
Beauchamp, J. R., Morgan, J. E., Pagel, C. N., & Partridge, T. A. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.144.6.1113 · Cited by 513
Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells
Shinin, V., Gayraud-Morel, B., Gomès, D., & Tajbakhsh, S. (2006) · Nature Cell Biology · doi:10.1038/ncb1425 · Cited by 504
Self-citationIsolation 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
Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis
Kuang, S., CHARGÉ, S. B. P., Seale, P., Huh, M. S., & Rudnicki, M. A. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200508001 · Cited by 490
Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancerPreprint
Neumüller, R. A., & Knoblich, J. A. (2009) · Genes & Development · doi:10.1101/gad.1850809 · Cited by 420
Distinct Regulatory Cascades Govern Extraocular and Pharyngeal Arch Muscle Progenitor Cell Fates
Sambasivan, R., Gayraud-Morel, B., Dumas, G., Cimper, C., Paisant, S., Kelly, R. G., & Tajbakhsh, S. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.05.008 · Cited by 400
Self-citationThe emerging biology of satellite cells and their therapeutic potential
Kuang, S., & Rudnicki, M. A. (2008) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.12.004 · Cited by 351
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
Self-citationA Polymeric Protein Anchors the Chromosomal Origin/ParB Complex at a Bacterial Cell Pole
Bowman, G. R., Comolli, L. R., Zhu, J., Eckart, M. R., Koenig, M., Downing, K. H., Moerner, W. E., Earnest, T. N., & Shapiro, L. (2008) · Cell · doi:10.1016/j.cell.2008.07.015 · Cited by 300
Cellular heterogeneity during vertebrate skeletal muscle development
Biressi, S., Molinaro, M., & Cossu, G. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.06.006 · Cited by 294
Conboy, M. J., Karasov, A. O., & Rando, T. A. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050102 · Cited by 287
Spindle Orientation Bias in Gut Epithelial Stem Cell Compartments Is Lost in Precancerous Tissue
Quyn, A. J., Appleton, P. L., Carey, F. A., Steele, R. J. C., Barker, N., Clevers, H., Ridgway, R. A., Sansom, O. J., & Näthke, I. S. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2009.12.007 · Cited by 242
Kelly, R. G., Alonso, S., Tajbakhsh, S., Cossu, G., & BUCKINGHAM, M. E. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.129.2.383 · Cited by 240
Self-citationA role for the myogenic determination gene Myf5 in adult regenerative myogenesis
Gayraud-Morel, B., Chrétien, F. C., Flamant, P., Gomès, D., Zammit, P. S., & Tajbakhsh, S. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.08.059 · Cited by 240
Self-citationBailey, S. M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh691 · Cited by 221
Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes
Schepers, A. G., Vries, R., van den Born, M., van de Wetering, M., & Clevers, H. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.26 · Cited by 217
Immortal Strands? Give Me a Break
Lansdorp, P. M. (2007) · Cell · doi:10.1016/j.cell.2007.06.017 · Cited by 186
The Immortal Strand Hypothesis: Segregation and Reconstruction
Rando, T. A. (2007) · Cell · doi:10.1016/j.cell.2007.06.019 · Cited by 167
Regulation of Muscle Mitochondrial Design
Moyes, C. D., Battersby, B. J., & Leary, S. C. (1998) · Journal of Experimental Biology · doi:10.1242/jeb.201.3.299 · Cited by 130
Polarity and Differential Inheritance—Universal Attributes of Life?
Macara, I. G., & Mili, S. (2008) · Cell · doi:10.1016/j.cell.2008.11.006 · Cited by 128
Prevention of Muscle Aging by Myofiber-Associated Satellite Cell Transplantation
Hall, J. K., Banks, G. B., Chamberlain, J. S., & Olwin, B. B. (2010) · Science Translational Medicine · doi:10.1126/scitranslmed.3001081 · Cited by 121
Notch3 Null Mutation in Mice Causes Muscle Hyperplasia by Repetitive Muscle Regeneration
Kitamoto, T., & Hanaoka, K. (2010) · Stem Cells · doi:10.1002/stem.547 · Cited by 118
Cell Type Regulates Selective Segregation of Mouse Chromosome 7 DNA Strands in Mitosis
Armakolas, A., & Klar, A. J. S. (2006) · Science · doi:10.1126/science.1120519 · Cited by 111
Tarui, T., Takahashi, T., Nowakowski, R. S., Hayes, N. L., Bhide, P. G., & Caviness, V. S. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi017 · Cited by 106
Sca-1 negatively regulates proliferation and differentiation of muscle cells
Mitchell, P. O., Mills, T., O’Connor, R. S., Graubert, T. A., Dzierzak, E. A., & Pavlath, G. K. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.04.016 · Cited by 106
Identification of sister chromatids by DNA template strand sequences
Falconer, E., Chavez, E. A., Henderson, A., Poon, S. S. S., McKinney, S. E., Brown, L. A., Huntsman, D. D., & Lansdorp, P. M. (2009) · Nature · doi:10.1038/nature08644 · Cited by 104
Skeletal Muscle as a Paradigm for Regenerative Biology and Medicine
Gayraud-Morel, B., Chrétien, F., & Tajbakhsh, S. (2009) · Regenerative Medicine · doi:10.2217/17460751.4.2.293 · Cited by 103
Self-citationGarstka, H. L. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg717 · Cited by 95
Cancer and the Immortal Strand Hypothesis
Cairns, J. (2006) · Genetics · doi:10.1534/genetics.104.66886 · Cited by 92
Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells
Gayraud-Morel, B., Chrétien, F. C., Jory, A., Sambasivan, R., Négroni, E., Flamant, P., Soubigou, G., Coppée, J., Santo, J. P. D., Cumano, A., et al. (2012) · Journal of Cell Science · doi:10.1242/jcs.097006 · Cited by 92
Self-citationNon-random segregation of sister chromosomes in Escherichia coli
White, M. A., Eykelenboom, J. K., Lopez-Vernaza, M. A., Wilson, E., & Leach, D. R. F. (2008) · Nature · doi:10.1038/nature07282 · Cited by 80
Intestinal epithelial stem cells do not protect their genome by asymmetric chromosome segregation
Escobar, M., Nicolas, P., Sangar, F., Laurent‐Chabalier, S., Clair, P., BRESSION, D., Jay, P., & Legraverend, C. (2011) · Nature Communications · doi:10.1038/ncomms1260 · Cited by 76
A model for specification of the left-right axis in vertebrates
Klar, A. J. S. (1994) · Trends in Genetics · doi:10.1016/0168-9525(94)90055-8 · Cited by 75
Human placental alkaline phosphatase as a histochemical marker of gene expression in transgenic mice
DePrimo, S. E., Stambrook, P. J., & Stringer, J. R. (1996) · Transgenic Research · doi:10.1007/bf01980211 · Cited by 59
Biased segregation of DNA and centrosomes — moving together or drifting apart?
Tajbakhsh, S., & González, C. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2784 · Cited by 59
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Jory, A., Roux, I. L., Gayraud-Morel, B., Rocheteau, P., Cohen‐Tannoudji, M., Cumano, A., & Tajbakhsh, S. (2009) · Stem Cells · doi:10.1002/stem.220 · Cited by 51
Self-citationCO-FISH reveals inversions associated with isochromosome formation
Bailey, S. M., Goodwin, E. H., Meyne, J., & Cornforth, M. N. (1996) · Mutagenesis · doi:10.1093/mutage/11.2.139 · Cited by 42
Stem cell identity and template DNA strand segregation
Tajbakhsh, S. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.10.004 · Cited by 29
Self-citationMyf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells
Gayraud-Morel, B., Chrétien, F. C., Jory, A., Sambasivan, R., Négroni, E., Flamant, P., Soubigou, G., Coppée, J., Santo, J. P. D., Cumano, A., et al. (2012) · Journal of Cell Science · doi:10.1242/jcs.128678 · Cited by 23
Self-citationCortés, F., Pastor, N., Mateos, S., & Domı́nguez, I. (2003) · DNA repair · doi:10.1016/s1568-7864(03)00044-2 · Cited by 17
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Metadata
- Authors
- Rocheteau, P., Gayraud-Morel, B., Siegl-Cachedenier, I., Blasco, M. A., & Tajbakhsh, S.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Tajbakhsh, Shahragim
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2012-01
- Volume
- 148
- Issue
- 1-2
- Pages
- 112-125
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2037334278
- Cited by
- 510
- References
- 57
- Citations by year
- 2026: 16 · 2025: 17 · 2024: 34 · 2023: 45 · 2022: 33 · 2021: 29 · 2020: 31 · 2019: 33 · 2018: 51 · 2017: 41 · 2016: 30 · 2015: 38 · 2014: 39 · 2013: 40 · 2012: 31
- FWCI
- 19.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 563 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-06-BLAN-0039)
- Centre National de la Recherche Scientifique
- Ministerio de Ciencia e Innovación
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- skeletal muscle stem cells, satellite cells, Pax7, stem cell quiescence, cell fate determination, muscle regeneration, cellular metabolism, first mitosis, stem cell heterogeneity, serial transplantation
- MeSH terms
- Animals, Cell Division, Female, Mice, Transgenic, Templates, Genetic, Muscle, Skeletal, Chromosome Segregation, Satellite Cells, Skeletal Muscle, Mice, PAX7 Transcription Factor, Adult Stem Cells
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