Stem cell ageing and non-random chromosome segregation
Open accessAbstract
Adult stem cells maintain the mature tissues of metazoans. They do so by reproducing in such a way that their progeny either differentiate, and thus contribute functionally to a tissue, or remain uncommitted and replenish the stem cell pool. Because ageing manifests as a general decline in tissue function, diminished stem cell-mediated tissue maintenance may contribute to age-related pathologies. Accordingly, the mechanisms by which stem cell regenerative potential is sustained, and the extent to which these mechanisms fail with age, are fundamental determinants of tissue ageing. Here, we explore the mechanisms of asymmetric division that account for the sustained fitness of adult stem cells and the tissues that comprise them. In particular, we summarize the theory and experimental evidence underlying non-random chromosome segregation—a mitotic asymmetry arising from the unequal partitioning of chromosomes according to the age of their template DNA strands. Additionally, we consider the possible consequences of non-random chromosome segregation, especially as they relate to both replicative and chronological ageing in stem cells. While biased segregation of chromosomes may sustain stem cell replicative potential by compartmentalizing the errors derived from DNA synthesis, it might also contribute to the accrual of replication-independent DNA damage in stem cells and thus hasten chronological ageing.
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Stem cells in different tissue compartments exhibit template strand segregation during cell divisions.
“Emerging evidence has demonstrated that stem cells in different tissue compartments exhibit template strand segregation during cell divisions128.”
From Molecular regulation of stem cell quiescence (2013) · cites this paper as [128]
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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-citationWilson, 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 · see citing works
Kirkwood, T. B. L., & Austad, S. N. (2000) · Nature · doi:10.1038/35041682 · Cited by 1,774 · see citing works
Mutation selection and the natural history of cancer
Cairns, J. (1975) · Nature · doi:10.1038/255197a0 · Cited by 1,592 · 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-citationLinking Colorectal Cancer to Wnt Signaling
Bienz, M., & Clevers, H. C. (2000) · Cell · doi:10.1016/s0092-8674(00)00122-7 · Cited by 1,516 · see citing works
p53 mutant mice that display early ageing-associated phenotypes
Tyner, S. D., Venkatachalam, S., Choi, J., Jones, S., Ghebranious, N., Igelmann, H., Lu, X., Soron, G., Cooper, B., Brayton, C., et al. (2002) · Nature · doi:10.1038/415045a · Cited by 1,459 · see citing works
Asymmetric and symmetric stem-cell divisions in development and cancer
Morrison, S. J., & Kimble, J. E. (2006) · Nature · doi:10.1038/nature04956 · Cited by 1,393 · see citing works
The replication of DNA in Escherichia coli
Meselson, M. S., & Stahl, F. W. (1958) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.44.7.671 · Cited by 1,273 · 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-citationDeficiencies in DNA damage repair limit the function of haematopoietic stem cells with age
Rossi, D. J., Bryder, D., Seita, J., Nussenzweig, A., Hoeijmakers, J., & Weissman, I. L. (2007) · Nature · doi:10.1038/nature05862 · Cited by 1,115 · see citing works
Mechanisms of Asymmetric Stem Cell Division
Knoblich, J. A. (2008) · Cell · doi:10.1016/j.cell.2008.02.007 · Cited by 1,011 · see citing works
<i>ATR</i> disruption leads to chromosomal fragmentation and early embryonic lethality
Brown, E. J., & Baltimore, D. (2000) · Genes & Development · doi:10.1101/gad.14.4.397 · Cited by 951 · see citing works
How stem cells age and why this makes us grow old
Sharpless, N. E., & DePinho, R. A. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2241 · Cited by 843 · see citing works
Ruzankina, Y., Pinzon‐Guzman, C., Asare, A., Ong, T., Pontano, L. L., Cotsarelis, G., Zediak, V. P., Velez, M., Bhandoola, A., & Brown, E. J. (2007) · Cell stem cell · doi:10.1016/j.stem.2007.03.002 · Cited by 780 · see citing works
Life Span of Individual Yeast Cells
Mortimer, R., & Johnston, J. R. (1959) · Nature · doi:10.1038/1831751a0 · Cited by 762 · see citing works
Aging and Death in an Organism That Reproduces by Morphologically Symmetric Division
Stewart, E. J., Madden, R., Paul, G., & Taddéi, F. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030045 · Cited by 753 · see citing works
DNA damage response and cellular senescence in tissues of aging mice
Wang, C., Jurk, D., Maddick, M., Nelson, G., Martin‐Ruiz, C., & Von Zglinicki, T. (2009) · Aging Cell · doi:10.1111/j.1474-9726.2009.00481.x · Cited by 696 · see citing works
Stem cells, ageing and the quest for immortality
Rando, T. A. (2006) · Nature · doi:10.1038/nature04958 · Cited by 695 · see citing works
Self-citationAsymmetric Inheritance of Oxidatively Damaged Proteins During Cytokinesis
Aguilaniu, H., Gustafsson, L., Rigoulet, M., & Nyström, T. (2003) · Science · doi:10.1126/science.1080418 · Cited by 642 · see citing works
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 · see citing works
Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells
Foudi, A., Hochedlinger, K., Van Buren, D., Schindler, J. W., Jaenisch, R., Carey, V., & Hock, H. (2009) · Nature Biotechnology · doi:10.1038/nbt.1517 · Cited by 586 · see citing works
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 · see citing works
Male and Female Drosophila Germline Stem Cells: Two Versions of Immortality
Fuller, M. T., & Spradling, A. C. (2007) · Science · doi:10.1126/science.1140861 · Cited by 455 · see citing works
Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU
Kiel, M. J., He, S., Ashkenazi, R., Gentry, S. N., Teta, M., Kushner, J. A., Jackson, T. L., & Morrison, S. J. (2007) · Nature · doi:10.1038/nature06115 · Cited by 417 · see citing works
NUMB controls p53 tumour suppressor activity
Colaluca, I. N., Tosoni, D., Nuciforo, P., Senic-Matuglia, F., Galimberti, V., Viale, G., Pece, S., & Di Fiore, P. P. (2008) · Nature · doi:10.1038/nature06412 · Cited by 385 · see citing works
Genotoxic Stress Abrogates Renewal of Melanocyte Stem Cells by Triggering Their Differentiation
Inomata, K., Aoto, T., Binh, N. T., Okamoto, N., Tanimura, S., Wakayama, T., Iseki, S., Hara, E., Masunaga, T., Shimizu, H., et al. (2009) · Cell · doi:10.1016/j.cell.2009.03.037 · Cited by 368 · see citing works
MECHANISMS OF POLARIZED GROWTH AND ORGANELLE SEGREGATION IN YEAST
Pruyne, D., Legesse-Miller, A., Gao, L., Dong, Y., & Bretscher, A. P. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.103108 · Cited by 366 · see citing works
The Polarisome Is Required for Segregation and Retrograde Transport of Protein Aggregates
Liu, B., Larsson, L., Caballero, A., Hao, X., Öling, D., Grantham, J., & Nyström, T. (2010) · Cell · doi:10.1016/j.cell.2009.12.031 · Cited by 341 · see citing works
The segregation of DNA in epithelial stem cells
Potten, C. S., Hume, W. J., Reid, P. J., & Cairns, J. (1978) · Cell · doi:10.1016/0092-8674(78)90274-x · Cited by 313 · see citing works
Frise, E., Knoblich, J. A., Younger, S. H., Jan, L. Y., & Jan, Y. N. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11925 · Cited by 308 · see citing works
Daughter cells of Saccharomyces cerevisiae from old mothers display a reduced life span.
Kennedy, B. K., Austriaco, N. P. G., & Guarente, L. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.127.6.1985 · Cited by 305 · see citing works
Smith, G. H. (2005) · Development · doi:10.1242/dev.01609 · Cited by 288 · see citing works
Conboy, M. J., Karasov, A. O., & Rando, T. A. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050102 · Cited by 287 · see citing works
Self-citationDNA replication stress, genome instability and aging
Burhans, W. C., & Weinberger, M. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm1059 · Cited by 279 · see citing works
Stem Cell Review Series: Aging of the skeletal muscle stem cell niche
Gopinath, S. D., & Rando, T. A. (2008) · Aging Cell · doi:10.1111/j.1474-9726.2008.00399.x · Cited by 262 · see citing works
Self-citationSpindle 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 · see citing works
Egilmez, N. K., & Jazwinski, S. M. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.1.37-42.1989 · Cited by 213 · see citing works
The multiple functions of Numb
Gulino, A., Marcotullio, L. D., & Screpanti, I. (2009) · Experimental Cell Research · doi:10.1016/j.yexcr.2009.11.017 · Cited by 192 · see citing works
Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro
Karpowicz, P. A., Morshead, C. M., Kam, A., Jervis, E., Ramunas, J., Cheng, V. Y. S., & van der Kooy, D. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200502073 · Cited by 191 · see citing works
Immortal Strands? Give Me a Break
Lansdorp, P. M. (2007) · Cell · doi:10.1016/j.cell.2007.06.017 · Cited by 188 · see citing works
DNA Repair Defects in Stem Cell Function and Aging
Park, Y., & Gerson, S. L. (2004) · Annual Review of Medicine · doi:10.1146/annurev.med.56.082103.104546 · Cited by 166 · see citing works
The Immortal Strand Hypothesis: Segregation and Reconstruction
Rando, T. A. (2007) · Cell · doi:10.1016/j.cell.2007.06.019 · Cited by 163 · see citing works
Self-citationImpaired hematopoietic stem cell functioning after serial transplantation and during normal aging
Kamminga, L. M., van Os, R., Ausema, A., Noach, E. J. K., Weersing, E., Dontje, B., Vellenga, E., & de Haan, G. (2005) · STEM CELLS · doi:10.1634/stemcells.2004-0066 · Cited by 128 · see citing works
Segregation of Sister Chromatids in Mammalian Cells
Lark, K. G., Consigli, R. A., & Minocha, H. C. (1966) · Science · doi:10.1126/science.154.3753.1202 · Cited by 126 · see citing works
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 · see citing works
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 99 · see citing works
Cancer and the Immortal Strand Hypothesis
Cairns, J. (2006) · Genetics · doi:10.1534/genetics.104.66886 · Cited by 94 · see citing works
Morales, M., Theunissen, J.-W. F., Kim, C. F. B., Kitagawa, R., Kastan, M. B., & Petrini, J. H. J. (2005) · Genes & Development · doi:10.1101/gad.1373705 · Cited by 87 · see citing works
Replicative stress, stem cells and aging
Ruzankina, Y., Asare, A., & Brown, E. J. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.03.009 · Cited by 72 · see citing works
Nonrandom Sister Chromatid Segregation and Nuclear Migration in Hyphae of Aspergillus nidulans
Rosenberger, R. F., & Kessel, M. (1968) · Journal of Bacteriology · doi:10.1128/jb.96.4.1208-1213.1968 · Cited by 69 · see citing works
Sotiropoulou, P. A., Candi, A., & Blanpain, C. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0634 · Cited by 67 · see citing works
DNA damage, DNA repair, ageing and age-related disease
Wilson, D. M., Bohr, V. A., & McKinnon, P. J. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.02.013 · Cited by 56 · see citing works
Nonrandom segregation of sister chromatids in Vicia faba and Triticum boeoticum.
Lark, K. G. (1967) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.58.1.352 · Cited by 49 · see citing works
Parental DNA strands segregate randomly during embryonic development of Caenorhabditis elegans
Ito, K., & McGhee, J. D. (1987) · Cell · doi:10.1016/0092-8674(87)90285-6 · Cited by 44 · see citing works
The Immortal Strand Hypothesis: How Could It Work?
Lew, D. J., Burke, D. J., & Dutta, A. (2008) · Cell · doi:10.1016/j.cell.2008.03.016 · Cited by 40 · see citing works
Random segregation of chromatids at mitosis in Saccharomyces cerevisiae.
Neff, M. W., & Burke, D. J. (1991) · Genetics · doi:10.1093/genetics/127.3.463 · Cited by 39 · see citing works
Asymmetry and the origins of ageing
Kirkwood, T. B. L. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.02.001 · Cited by 34 · see citing works
The germline stem cells of Drosophila melanogaster partition DNA non-randomly
Karpowicz, P. A., Pellikka, M., Chea, E., Godt, D., Tepaß, U., & van der Kooy, D. (2009) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2009.03.001 · Cited by 30 · see citing works
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 30 · see citing works
Random Segregation of DNA Strands in Epidermal Basal Cells
Kuroki, T., & Murakami, Y. (1989) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.1989.tb01690.x · Cited by 27 · see citing works
Nonselective Sister Chromatid Segregation in Mouse Embryonic Neocortical Precursor Cells
Fei, J., & Huttner, W. Β. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp043 · Cited by 19 · see citing works
A New Mechanism for Aging: Chemical “Age Spots” in Immortal DNA Strands in Distributed Stem Cells
Sherley, J. L. (2008) · Breast Disease · doi:10.3233/bd-2008-29105 · Cited by 18 · see citing works
Morris, V. B. (1977) · Chromosoma · doi:10.1007/bf00288461 · Cited by 18 · see citing works
Chromatid distribution at mitosis in cultured Wallabia bicolor cells
Geard, C. R. (1973) · Chromosoma · doi:10.1007/bf00291024 · Cited by 15 · see citing works
Random distribution of centromere regions at mitosis in cultured cells of Muntiacus muntjak
Mayron, R., & Wise, D. (1976) · Chromosoma · doi:10.1007/bf00288328 · Cited by 11 · see citing works
Random segregation of sister chromatids in meristematic cells
Fernández‐Gómez, M. E., al Torre, C. D., & STOCKERT, J. C. (1975) · Experimental Cell Research · doi:10.1016/s0014-4827(75)80048-6 · Cited by 7 · see citing works
Flagged first, then by citations
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Molecular regulation of stem cell quiescence
Cheung, T. H., & Rando, T. A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3591 · Cited by 1,148 · see citing works
Self-citationStem cell aging: mechanisms, regulators and therapeutic opportunities
Oh, J., Lee, Y. D., & Wagers, A. J. (2014) · Nature Medicine · doi:10.1038/nm.3651 · Cited by 796 · see citing works
Aging, Rejuvenation, and Epigenetic Reprogramming: Resetting the Aging Clock
Rando, T. A., & Chang, H. Y. (2012) · Cell · doi:10.1016/j.cell.2012.01.003 · Cited by 520 · see citing works
Self-citationTissue-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
Self-citationThe role of DNA damage and repair in aging through the prism of Koch-like criteria
Moskalev, A. A., Shaposhnikov, M. V., Plyusnina, E. N., Zhavoronkov, A., Budovsky, A., Yanai, H., & Fraifeld, V. E. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2012.02.001 · Cited by 387 · see citing works
Manifestations and mechanisms of stem cell aging
Liu, L. A., & Rando, T. A. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201010131 · Cited by 306 · see citing works
Self-citationEmerging models and paradigms for stem cell ageing
Jones, D. L., & Rando, T. A. (2011) · Nature Cell Biology · doi:10.1038/ncb0511-506 · Cited by 256 · see citing works
Self-citationBalistreri, C. R., Madonna, R., Melino, G., & Caruso, C. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.06.004 · Cited by 90 · see citing works
Chromatin dynamics in DNA double-strand break repair
Shi, L., & Oberdoerffer, P. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.01.002 · Cited by 66 · see citing works
DeCarolis, N. A., Kirby, E. D., Wyss‐Coray, T., & Palmer, T. D. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a025874 · Cited by 55 · see citing works
Regulatory Role of Quiescence in the Biological Function of Cancer Stem Cells
Lee, S. H., Reed-Newman, T. C., Anant, S., & Ramasamy, T. S. (2020) · Stem Cell Reviews and Reports · doi:10.1007/s12015-020-10031-8 · Cited by 51 · see citing works
Stem Cells as Vehicles for Youthful Regeneration of Aged Tissues
Rando, T. A., & Wyss‐Coray, T. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glu043 · Cited by 34 · see citing works
Self-citationMethods for the discovery of new anti-aging products – targeted approaches
Manayi, A., Saeidnia, S., Gohari, A. R., & Abdollahi, M. R. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2014.885014 · Cited by 32 · see citing works
Mutation-rate plasticity and the germline of unicellular organisms
Aanen, D. K., & Debets, A. J. M. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.0128 · Cited by 31 · see citing works
Partridge, L., Thornton, J. M., & Bates, G. P. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0298 · Cited by 28 · see citing works
Asymmetric Chromatid Segregation in Cardiac Progenitor Cells Is Enhanced by Pim-1 Kinase
Sundararaman, B., Avitabile, D., Konstandin, M. H., Cottage, C. T., Gude, N. A., & Sussman, M. A. (2012) · Circulation Research · doi:10.1161/circresaha.112.267716 · Cited by 27 · see citing works
Strand-seq: A unifying tool for studies of chromosome segregation
Falconer, E., & Lansdorp, P. M. (2013) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2013.04.005 · Cited by 27 · see citing works
Huh, Y. H., King, J., Cohen, J., & Sherley, J. L. (2011) · Scientific Reports · doi:10.1038/srep00176 · Cited by 26 · see citing works
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Yennek, S., & Tajbakhsh, S. (2013) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2013.05.008 · Cited by 26 · see citing works
Extrinsic Regulation of Satellite Cell Function and Muscle Regeneration Capacity during Aging
Chakkalakal, J. V. (2012) · Journal of Stem Cell Research & Therapy · doi:10.4172/2157-7633.s11-001 · Cited by 23 · see citing works
Replication Stress Induces ATR/CHK1-Dependent Nonrandom Segregation of Damaged Chromosomes
Xing, M., Zhang, F., Liao, H., Chen, S., Che, L., Wang, X., Bao, Z., Ji, F., Chen, G., Zhang, H., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.04.005 · Cited by 19 · see citing works
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Ozguldez, H. O., & Bulut-Karslıoğlu, A. (2024) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-112122-022528 · Cited by 17 · see citing works
Asymmetric segregation of template DNA strands in basal-like human breast cancer cell lines
Liu, W., Jeganathan, G., Amiri, S., Morgan, K. M., Ryan, B. M., & Pine, S. R. (2013) · Molecular Cancer · doi:10.1186/1476-4598-12-139 · Cited by 17 · see citing works
Charville, G. W., & Rando, T. A. (2013) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2013.05.006 · Cited by 18 · see citing works
Self-citationCellular and molecular mechanisms of asymmetric stem cell division in tissue homeostasis
Bolkent, S. (2024) · Genes to Cells · doi:10.1111/gtc.13172 · Cited by 15 · see citing works
Aging disrupts spatiotemporal regulation of germline stem cells and niche integrity
Urman, M. A., John, N. S., Jung, T., & Lee, C. (2023) · Biology Open · doi:10.1242/bio.060261 · Cited by 14 · see citing works
Börklü, E., & Ülgen, K. Ö. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029284 · Cited by 13 · see citing works
Near‐to‐perfect homeostasis: Examples of universal aging rule which germline evades
Teplyuk, N. M. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23366 · Cited by 12 · see citing works
Defining the General Principles of Stem Cell Aging: Lessons from Organismal Models
Koyuncu, S., Irmak, D., Sáez, I., & Vı́lchez, D. (2015) · Current Stem Cell Reports · doi:10.1007/s40778-015-0017-1 · Cited by 7 · see citing works
Drpic, D., Barišić, M., Pinheiro, D., & Maiato, H. (2013) · Chromosome Research · doi:10.1007/s10577-013-9354-z · Cited by 5 · see citing works
Parida, B. P., Misra, B. B., & Misra, A. N. (2018) · 4open · doi:10.1051/fopen/2018004 · Cited by 3 · see citing works
Fragile DNA Repair Mechanism Reduces Ageing in Multicellular Model
Bendtsen, K. M., Juul, J., & Trusina, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036018 · Cited by 3 · see citing works
Urman, M. A., John, N. S., & Lee, C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.15.524122 · Cited by 2 · see citing works
Can Unicellular Organisms Sequester a Germline? The Yeast‐Germline Hypothesis
Vadlamudi, B. S., & Aanen, D. K. (2025) · BioEssays · doi:10.1002/bies.70003 · Cited by 1 · see citing works
A Sexy Spin on Nonrandom Chromosome Segregation
Charville, G. W., & Rando, T. A. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.05.013
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Purohit, J. S., Singh, N., Hussain, S. S., & Chaturvedi, M. M. (2020) · Springer eBooks · doi:10.1007/978-981-32-9005-1_9 · Cited by 1 · see citing works
Lazarovici, P. (2021) · Springer eBooks · doi:10.1007/978-3-030-22009-9_432
Lazarovici, P. (2019) · Springer eBooks · doi:10.1007/978-3-319-69892-2_432-1
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TABIBZADEH, S. S. (2022) · Aging and Disease · doi:10.14336/ad.2022.0414
Latil, M. (2013) · doi:10.70675/05468b01z26d3z4497za6b2z8a8bc4d00e4f
- Authors
- Charville, G. W., & Rando, T. A.
- Affiliations
- Stanford Medicine (US)
- VA Palo Alto Health Care System (US)
- Corresponding author
- Rando, Thomas A.
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2011-01-12
- Volume
- 366
- Issue
- 1561
- Pages
- 85-93
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC3001309
- OpenAlex
- W2133799215
- Cited by
- 45
- References
- 67
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 1 · 2016: 2 · 2015: 3 · 2014: 3 · 2013: 9 · 2012: 9
- FWCI
- 0.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Federation for Aging Research
- Glenn Foundation for Medical Research
- Fondation pour la Recherche Médicale
- National Institutes of Health (DP1OD000392, R01 AG23806)
- National Institute on Aging (R01 AG23806, F30 AG35521, R37AG023806, R01AG023806, F30AG035521)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Keywords
- adult stem cells, stem cell aging, asymmetric cell division, chronological aging, DNA damage, tissue aging, stem cell self-renewal
- MeSH terms
- Animals, Cell Differentiation, Humans, Mitosis, Cellular Senescence, Cell Lineage, Chromosome Segregation, Adult Stem Cells
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