DNA asymmetry and cell fate regulation in stem cells

Seminars in Cell and Developmental Biology

Volumn 24, Issue 8-9, 2013, Pages 627-642

  Yennek, Siham ^a   Tajbakhsh, Shahragim ^a  

^a CNRS   (France)

Author keywords

Asymmetric; Epigenetic regulation; Immortal DNA; Mitosis; Non random DNA segregation; Template DNA strand cosegregation

Indexed keywords

BROXURIDINE; THYMIDINE; TRANSCRIPTION FACTOR PAX7;

ADIPOCYTE; ADULT STEM CELL; ASPERGILLUS NIDULANS; ASYMMETRIC CELL DIVISION; CAENORHABDITIS ELEGANS; CANCER CELL; CAULOBACTER CRESCENTUS; CELL CYCLE; CELL DIVISION; CELL FATE; CRYPT CELL; DAUGHTER CELL; DNA CONTENT; DNA DENATURATION; DNA REPLICATION; DNA STRAND; DNA STRUCTURE; DNA TEMPLATE; DROSOPHILA MELANOGASTER; EMBRYONIC STEM CELL; ESCHERICHIA COLI; EUKARYOTE; GENOTOXICITY; GERMLINE STEM CELL; MITOSIS; MUSCLE REGENERATION; NONHUMAN; OXYGEN TENSION; PRIMARY CELL CULTURE; PROKARYOTE; REVIEW; SACCHAROMYCES CEREVISIAE; SATELLITE CELL; SCHIZOSACCHAROMYCES POMBE; SISTER CHROMATID; SISTER CHROMATID EXCHANGE; SKELETAL MUSCLE; STEM CELL; STEM CELL NICHE; STRESS; VICIA FABA;

EUKARYOTA; PROKARYOTA;

5(H)MC; 5(HYDROXY)METHYLCYTOSINE; 5-BROMO-2′-DEOXYURIDINE; 5-CHLORO-2′-DEOXYURIDINE; 5-ETHYNYL-2′-DEOXYURIDINE; 5-IODO-2′-DEOXYURIDINE; ASYMMETRIC; BRDU; CHROMOSOME ORIENTATION FLUORESCENCE IN SITU HYBRIDIZATION; CLDU; CO-FISH; EDU; EPIGENETIC REGULATION; IDU; IMMORTAL DNA; MALE GERMLINE STEM CELL; MGSC; MITOSIS; NON-RANDOM DNA SEGREGATION; PCNA; PROLIFERATING CELL NUCLEAR ANTIGEN; SATELLITE CELL; SC; TDSS; TEMPLATE DNA STRAND COSEGREGATION;

ANIMALS; ASYMMETRIC CELL DIVISION; CELL LINEAGE; CHROMOSOME SEGREGATION; DNA; HUMANS; STEM CELLS; TEMPLATES, GENETIC;

EID: 84887615107     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2013.05.008     Document Type: Review

References (129)

1. Tajbakhsh S., Rocheteau P., Le Roux I. Asymmetric cell divisions and asymmetric cell fates. Annual Review of Cell and Developmental Biology 2009, 25:671-699.
2. Cairns J. Mutation selection and the natural history of cancer. Nature 1975, 255:197-200.
3. Cairns J. Somatic stem cells and the kinetics of mutagenesis and carcinogenesis. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:10-13.
4. Lansdorp P.M. Immortal strands? Give me a break. Cell 2007, 129:1244-1247.
5. Rando T.A. The immortal strand hypothesis: segregation and reconstruction. Cell 2007, 129:1239-1243.
6. Tajbakhsh S. Stem cell identity and template DNA strand segregation. Current Opinion in Cell Biology 2008, 20:716-722.
7. Tajbakhsh S., Gonzalez C. Biased segregation of DNA and centrosomes: moving together or drifting apart?. Nature Reviews: Molecular Cell Biology 2009, 10:804-810.
8. Potten C.S., Owen G., Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. Journal of Cell Science 2002, 115:2381-2388.
9. Sotiropoulou P.A., et al. Bcl-2 and accelerated DNA repair mediates resistance of hair follicle bulge stem cells to DNA-damage-induced cell death. Nature Cell Biology 2010, 12(6):572-582.
10. Rossi D.J., et al. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 2007, 447(7145):725-729.
11. Mohrin M., et al. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 2010, 7(2):174-185.
12. Lark K.G., Consigli R.A., Minocha H.C. Segregation of sister chromatids in mammalian cells. Science 1966, 154(3753):1202-1205.
13. Gilbert D.M., et al. Space and time in the nucleus: developmental control of replication timing and chromosome architecture. Cold Spring Harbor Symposia on Quantitative Biology 2010, 75:143-153.
14. Barker N., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449(7165):1003-1007.
15. Snippert H.J., et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143(1):134-144.
16. Wasserstrom A., et al. Estimating cell depth from somatic mutations. PLoS Computational Biology 2008, 4:1939.
17. Noctor S.C., et al. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature Neuroscience 2004, 7:136-144.
18. Klar A.J. A model for specification of the left-right axis in vertebrates. Trends in Genetics 1994, 10(11):392-396.
19. Bell C.D. Is mitotic chromatid segregation random?. Histology and Histopathology 2005, 20(4):1313-1320.
20. Klar A.J. The developmental fate of fission yeast cells is determined by the pattern of inheritance of parental and grandparental DNA strands. The EMBO Journal 1990, 9:1407-1415.
21. Charville G.W., Rando T.a. Stem cell ageing and non-random chromosome segregation. Philosophical Transactions of the Royal Society of London: Series B, Biological Sciences 2011, 366:85-93.
22. Liu P., Jenkins N.A., Copeland N.G. Efficient Cre-loxP-induced mitotic recombination in mouse embryonic stem cells. Nature Genetics 2002, 30:66-72.
23. Armakolas A., Klar A.J.S. Cell type regulates selective segregation of mouse chromosome 7 DNA strands in mitosis. Science 2006, 311:1146-1149.
24. Armakolas A., Klar A.J.S. Left-right dynein motor implicated in selective chromatid segregation in mouse cells. Science 2007, 315:100-101.
25. Falconer E., et al. DNA template strand sequencing of single-cells maps genomic rearrangements at high resolution. Nature Methods 2012, 9:1107-1112.
26. Sauer S., Burket S.S., Lewandoski M., Klar A.J.S. A CO-FISH assay to assess sister chromatid segregation patterns in mitosis of mouse embryonic stem cells. Chromosome Research 2013, 21:311-328.
27. Falconer E., et al. Identification of sister chromatids by DNA template strand sequences. Nature 2010, 463:93-97.
28. Shinin V., et al. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nature Cell Biology 2006, 8:677-687.
29. Conboy M.J., Karasov A.O., Rando T.a. High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biology 2007, 5:e102.
30. Rocheteau P., et al. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 2012, 148:112-125.
31. Karpowicz P., et al. Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro. The Journal of Cell Biology 2005, 170:721-732.
32. Potten C.S., et al. The segregation of DNA in epithelial stem cells. Cell 1978, 15(3):899-906.
33. Quyn A.J., et al. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 2010, 6:175-181.
34. Kajstura J., et al. Tracking chromatid segregation to identify human cardiac stem cells that regenerate extensively the infarcted myocardium. Circulation Research 2012, 111(7):894-906.
35. Escobar M., et al. Intestinal epithelial stem cells do not protect their genome by asymmetric chromosome segregation. Nature Communications 2011, 2:258.
36. Schepers A.G., et al. Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes. The EMBO Journal 2011, 30:1104-1109.
37. Steinhauser M.L., et al. Multi-isotope imaging mass spectrometry quantifies stem cell division and metabolism. Nature 2012, 481:516-519.
38. Sotiropoulou P.a., Candi A., Blanpain C. The majority of multipotent epidermal stem cells do not protect their genome by asymmetrical chromosome segregation. Stem Cells 2008, 26:2964-2973.
39. Waghmare S.K., et al. Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. The EMBO Journal 2008, 27:1309-1320.
40. Kiel M.J., et al. Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 2007, 449:238-242.
41. Fuchs E., Tumbar T., Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004, 116(6):769-778.
42. Li L., Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science (New York, NY) 2010, 327:542-545.
43. Bischoff R., Holtzer H. Inhibition of myoblast fusion after one round of DNA synthesis in 5-bromodeoxyuridine. Journal of Cell Biology 1970, 44(1):134-150.
44. Ogino H., et al. The human MYOD1 transgene is suppressed by 5-bromodeoxyuridine in mouse myoblasts. Journal of Biochemistry 2002, 132(6):953-959.
45. Schneider L., d'Adda di Fagagna F. Neural stem cells exposed to BrdU lose their global DNA methylation and undergo astrocytic differentiation. Nucleic Acids Research 2012, 40:5332-5342.
46. Latt S.A. Sister chromatid exchange formation. Annual Review of Genetics 1981, 15:11-55.
47. Lechene C., et al. High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. Journal of Biology 2006, 5(6):20.
48. Yadlapalli S., Yamashita Y.M. Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature 2013, May 5.
49. Meyne J., Moyzis R.K. In situ hybridization using synthetic oligomers as probes for centromere and telomere repeats. Methods in Molecular Biology 1994, 33:63-74.
50. Bailey S.M., Goodwin E.H., Cornforth M.N. Strand-specific fluorescence in situ hybridization: the CO-FISH family. Cytogenetic and Genome Research 2004, 107(1-2):14-17.
51. Hari D., et al. Isolation of live label-retaining cells and cells undergoing asymmetric cell division via nonrandom chromosomal cosegregation from human cancers. Stem Cells and Development 2011, 20:1649-1658.
52. Xin H.W., et al. Tumor-initiating label-retaining cancer cells in human gastrointestinal cancers undergo asymmetric cell division. Stem Cells 2012, 30(4):591-598.
53. Buczacki S.J., et al. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 2013, 495(7439):65-69.
54. Takeda N., et al. Interconversion between intestinal stem cell populations in distinct niches. Science 2011, 334(6061):1420-1424.
55. Tian H., et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 2011, 478:255-259.
56. Barker N., van de Wetering M., Clevers H. The intestinal stem cell. Genes & Development 2008, 22:1856-1864.
57. Cheng H., Leblond C.P. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. American Journal of Anatomy 1974, 141(4):537-561.
58. Li L., Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science 2010, 327(5965):542-545.
59. Snippert H.J., Clevers H. Tracking adult stem cells. EMBO Reports 2011, 12(2):113-122.
60. Naiche L.A., Papaioannou V.E. Cre activity causes widespread apoptosis and lethal anemia during embryonic development. Genesis 2007, 45(12):768-775.
61. Zhu Y., et al. Apoptosis differently affects lineage tracing of lgr5 and bmi1 intestinal stem cell populations. Cell Stem Cell 2013, 12(3):298-303.
62. Tajbakhsh S. Skeletal muscle stem cells in developmental versus regenerative myogenesis. Journal of Internal Medicine 2009, 266:372-389.
63. Biressi S., et al. Intrinsic phenotypic diversity of embryonic and fetal myoblasts is revealed by genome-wide gene expression analysis on purified cells. Developmental Biology 2007, 304(2):633-651.
64. Kuang S., et al. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007, 129:999-1010.
65. Kuang S., Rudnicki M.A. The emerging biology of satellite cells and their therapeutic potential. Trends in Molecular Medicine 2008, 14(2):82-91.
66. Zammit P.S., et al. Pax7 and myogenic progression in skeletal muscle satellite cells. Journal of Cell Science 2006, 119(Pt 9):1824-1832.
67. Harvey R.P., Tajbakhsh S. Biased DNA segregation and cardiac stem cell therapies. Circulation Research 2012, 111(7):827-830.
68. Neumüller R.a., Knoblich J.a. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes & Development 2009, 23:2675-2699.
69. He S., Nakada D., Morrison S.J. Mechanisms of stem cell self-renewal. Annual Review of Cell and Developmental Biology 2009, 25:377-406.
70. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
71. Yamashita Y.M., Fuller M.T. Asymmetric centrosome behavior and the mechanisms of stem cell division. The Journal of Cell Biology 2008, 180:261-266.
72. Toledano H., Jones D.L. Mechanisms regulating stem cell polarity and the specification of asymmetric divisions 2009, StemBook.
73. Yamashita Y.M., et al. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 2007, 315(5811):518-521.
74. Rusan N.M., Peifer M. A role for a novel centrosome cycle in asymmetric cell division. Journal of Cell Biology 2007, 177(1):13-20.
75. Rebollo E., et al. Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Developmental Cell 2007, 12(3):467-474.
76. Januschke J., et al. Drosophila neuroblasts retain the daughter centrosome. Nature Communications 2011, 2:243.
77. Wang X., et al. A new subtype of progenitor cell in the mouse embryonic neocortex. Nature Neuroscience 2011, 14(5):555-561.
78. Conduit P.T., Raff J.W. Cnn dynamics drive centrosome size asymmetry to ensure daughter centriole retention in Drosophila neuroblasts. Current Biology 2010, 20(24):2187-2192.
79. Evano E., Tajbakhsh S. Sorting DNA with asymmetry: a new player in gene regulation?. Chromosome Research 2013, 21:225-242.
80. Ito K., et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004, 431(7011):997-1002.
81. Toussaint O., et al. Artefactual effects of oxygen on cell culture models of cellular senescence and stem cell biology. Journal of Cellular Physiology 2011, 226(2):315-321.
82. Mazumdar J., Dondeti V., Simon M.C. Hypoxia-inducible factors in stem cells and cancer. Journal of Cellular and Molecular Medicine 2009, 13:4319-4328.
83. Ito K., et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nature Medicine 2006, 12(4):446-451.
84. Clarke L., van der Kooy D. Low oxygen enhances primitive and definitive neural stem cell colony formation by inhibiting distinct cell death pathways. Stem Cells 2009, 27(8):1879-1886.
85. Eliasson P., et al. Hypoxia mediates low cell-cycle activity and increases the proportion of long-term-reconstituting hematopoietic stem cells during in vitro culture. Experimental Hematology 2010, 38(4):301-310. e2.
86. Krinner A., et al. Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Proliferation 2009, 42(4):471-484.
87. Duguez S., et al. Atmospheric oxygen tension slows myoblast proliferation via mitochondrial activation. PLoS ONE 2012, 7(8):e43853.
88. Liu W., et al. Hypoxia promotes satellite cell self-renewal and enhances the efficiency of myoblast transplantation. Development (Cambridge, England) 2012, 139:2857-2865.
89. Gustafsson M.V., et al. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Developmental Cell 2005, 9(5):617-628.
90. Fu Y., He C. Nucleic acid modifications with epigenetic significance. Current Opinion in Chemical Biology 2012, 16(5-6):516-524.
91. Voigt P., et al. Asymmetrically modified nucleosomes. Cell 2012, 151(1):181-193.
92. Lew D.J., Burke D.J., Dutta A. The immortal strand hypothesis: how could it work?. Cell 2008, 133(1):21-23.
93. Tran V., et al. Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science 2012, 338:679-682.
94. Thorpe P.H., Bruno J., Rothstein R. Kinetochore asymmetry defines a single yeast lineage. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:6673-6678.
95. Théry M., et al. The extracellular matrix guides the orientation of the cell division axis. Nature Cell Biology 2005, 7:947-953.
96. Mascré G., et al. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 2012, 489:257-262.
97. Knoblich J.A. Asymmetric cell division: recent developments and their implications for tumour biology. Nature Reviews Molecular Cell Biology 2010, 11(12):849-860.
98. Rossi D.J., Jamieson C.H., Weissman I.L. Stems cells and the pathways to aging and cancer. Cell 2008, 132(4):681-696.
99. Clarke M.F., Fuller M. Stem cells and cancer: two faces of eve. Cell 2006, 124(6):1111-1115.
100. Vermeulen L., et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(36):13427-13432.
101. Rambhatla L., et al. Cellular senescence: ex vivo p53-dependent asymmetric cell kinetics. Journal of Biomedicine and Biotechnology 2001, 1(1):28-37.
102. Cicalese A., et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009, 138(6):1083-1095.
103. Pine S.R., et al. Microenvironmental modulation of asymmetric cell division in human lung cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:2195-2200.
104. Merok J.R., et al. Cosegregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell kinetics. Cancer Research 2002, 62(23):6791-6795.
105. Rambhatla L., et al. Immortal DNA strand cosegregation requires p53/IMPDH-dependent asymmetric self-renewal associated with adult stem cells. Cancer Research 2005, 65:3155-3161.
106. Sauer S., Klar A.J.S. Left-right symmetry breaking in mice by left-right dynein may occur via a biased chromatid segregation mechanism, without directly involving the Nodal gene. Frontiers in Oncology 2012, 2:166.
107. Lark K.G., Bird R.E. Segregation of the conserved units of DNA in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 1965, 54(5):1444-1450.
108. Cuzin F., Jacob F. Existence in Escherichia coli of a segregation genetic unit formed from different replicons. Comptes Rendus Hebdomadaires des Seances de l Academie des Sciences. D: Sciences Naturelles 1965, 260(20):5411-5414.
109. Bates D., Kleckner N. Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 2005, 121(6):899-911.
110. Wang X., Possoz C., Sherratt D.J. Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes and Development 2005, 19(19):2367-2377.
111. Nielsen H.J., et al. The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Molecular Microbiology 2006, 62(2):331-338.
112. White M.a., et al. Non-random segregation of sister chromosomes in Escherichia coli. Nature 2008, 455:1248-1250.
113. Zweiger G., Marczynski G., Shapiro L. A Caulobacter DNA methyltransferase that functions only in the predivisional cell. Journal of Molecular Biology 1994, 235(2):472-485.
114. Marczynski G.T. Chromosome methylation and measurement of faithful, once and only once per cell cycle chromosome replication in Caulobacter crescentus. Journal of Bacteriology 1999, 181(7):1984-1993.
115. Viollier P.H., et al. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(25):9257-9262.
116. Williamson D.H., Fennell D. Non-random assortment of sister chromatids in yeast mitosis. Molecular Genetics in Yeast, Alfred Benzon Symp. 16 1981, 89-107. D. von Wettstein (Ed.).
117. Neff M.W., Burke D.J. Random segregation of chromatids at mitosis in Saccharomyces cerevisiae. Genetics 1991, 127(3):463-473.
118. Keyes B.E., et al. Sister chromatids segregate at mitosis without mother-daughter bias in Saccharomyces cerevisiae. Genetics 2012, 192(4):1553-1557.
119. Lark K.G. Nonrandom segregation of sister chromatids in Vicia faba and Triticum boeoticum. Proceedings of the National Academy of Sciences of the United States of America 1967, 58(1):352-359.
120. Rosenberger R.F., Kessel M. Nonrandom sister chromatid segregation and nuclear migration in hyphae of Aspergillus nidulans. Journal of Bacteriology 1968, 96(4):1208-1213.
121. Ito K., McGhee J.D. Parental DNA strands segregate randomly during embryonic development of Caenorhabditis elegans. Cell 1987, 49(3):329-336.
122. Karpowicz P., et al. The germline stem cells of Drosophila melanogaster partition DNA non-randomly. European Journal of Cell Biology 2009, 88:397-408.
123. Yadlapalli S., Cheng J., Yamashita Y.M. Drosophila male germline stem cells do not asymmetrically segregate chromosome strands. Journal of Cell Science 2011, 124(Pt 6):933-939.
124. Kimoto M., et al. Label-retaining cells in the rat submandibular gland. Journal of Histochemistry and Cytochemistry 2008, 56(1):15-24.
125. Ito K., McGhee J.D., Schultz G.A. Paternal DNA strands segregate to both trophectoderm and inner cell mass of the developing mouse embryo. Genes and Development 1988, 2(8):929-936.
126. Wilson A., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
127. Smith G.H. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development (Cambridge, England) 2005, 132:681-687.
128. Bussard K.M., et al. Immortalized, pre-malignant epithelial cell populations contain long-lived, label-retaining cells that asymmetrically divide and retain their template DNA. Breast Cancer Research: BCR 2010, 12:R86.
129. Fei J.F., Huttner W.B. Nonselective sister chromatid segregation in mouse embryonic neocortical precursor cells. Cerebral Cortex 2009, 19(Suppl. 1):i49-i54.