Stem cell identity and template DNA strand segregation

Current Opinion in Cell Biology

Volumn 20, Issue 6, 2008, Pages 716-722

  Tajbakhsh, Shahragim ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CENTROMERE; CENTROSOME; CHROMOSOME; CHROMOSOME SEGREGATION; DAUGHTER CELL; DNA METHYLATION; DNA REPLICATION; DNA STRAND; DNA TEMPLATE; EPIGENETICS; GENE SILENCING; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SISTER CHROMATID; STEM CELL;

ANIMALS; CHROMATIDS; CHROMOSOME SEGREGATION; DNA; DNA REPLICATION; HUMANS; MITOSIS; MODELS, BIOLOGICAL; STEM CELLS;

EID: 56949087427     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2008.10.004     Document Type: Review

References (50)

1. Cairns J. Somatic stem cells and the kinetics of mutagenesis and carcinogenesis. Proc Natl Acad Sci U S A 99 (2002) 10567-10570
2. Rossi D.J., Bryder D., Seita J., Nussenzweig A., Hoeijmakers J., and Weissman I.L. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447 (2007) 725-729
3. Sambasivan R., and Tajbakhsh S. Skeletal muscle stem cell birth and properties. Semin Cell Dev Biol 18 (2007) 870-882
4. Kai T., and Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428 (2004) 564-569
5. Brawley C., and Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304 (2004) 1331-1334
6. Krivtsov A.V., Twomey D., Feng Z., Stubbs M.C., Wang Y., Faber J., Levine J.E., Wang J., Hahn W.C., Gilliland D.G., et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442 (2006) 818-822
7. •]) these authors report that the majority of LRCs in the hair follicle segregate their DNA strands randomly to daughter cells.
8. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P.J., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007) 1003-1007. This study shows for the first time by cell lineage analysis using Lgr5 marked cells that stem cells in the crypt of the small intestine reside at the bottom of the crypt. The relationship between these cells and those at position 4/5 that perform TDSS and which were thought to be stem cells, is not clear.
9. Cairns J. Mutation selection and the natural history of cancer. Nature 255 (1975) 197-200
10. Lark K.G., Consigli R.A., and Minocha H.C. Segregation of sister chromatids in mammalian cells. Science 154 (1966) 1202-1205
11. Cairns J. Cancer and the immortal strand hypothesis. Genetics 174 (2006) 1069-1072
12. Fuchs E., Tumbar T., and Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 116 (2004) 769-778
13. Potten C.S., Owen G., and Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 115 (2002) 2381-2388
14. Karpowicz P., Morshead C., Kam A., Jervis E., Ramunas J., Cheng V., and van der Kooy D. Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro. J Cell Biol 170 (2005) 721-732. Using BrdU-label retention assays in neuronal precursors, the authors show that BrdU-labelled strands segregate selectively to one daughter cell during mitosis, and cell lineage by videomicroscopy showed a high frequency of the distribution of old and new DNA to individual daughter cells.
15. Smith G.H. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 132 (2005) 681-687
16. Merok J.R., Lansita J.A., Tunstead J.R., and Sherley J.L. Cosegregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell kinetics. Cancer Res 62 (2002) 6791-6795
17. Shinin V., Gayraud-Morel B., Gomes D., and Tajbakhsh S. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8 (2006) 677-682. Using a pulse-chase approach with BrdU, TDSS was shown to take place in adult muscle satellite cells in culture, on freshly isolated myofibres, and by videomicroscopy. Template and non-template DNA strands were alternatively labelled in isolated satellite cells using the cell determinant Numb as a reference. The asymmetric segregation of template DNA strands was shown to take place with Numb, and the authors proposed that mother centrosomes also segregate with template DNA strands.
18. ••]). TDSS was associated with the differential expression of Desmin and ScaI in distinct daughter cells.
19. Rando T.A. The immortal strand hypothesis: segregation and reconstruction. Cell 129 (2007) 1239-1243
20. Lansdorp P.M. Immortal strands? Give me a break. Cell 129 (2007) 1244-1247
21. Kiel M.J., He S., Ashkenazi R., Gentry S.N., Teta M., Kushner J.A., Jackson T.L., and Morrison S.J. Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 449 (2007) 238-242. This study uses double labelling with CldU and IdU to show that the majority of HSCs are not label retaining. Further they report that biased segregation of labelled DNA strands as postulated by Cairns [9] does not occur in this lineage.
22. ••]) and report that the majority of label retaining stem cells in the hair follicle segregate their DNA strands randomly to daughter cells.
23. Sangiorgi E., and Capecchi M.R. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40 (2008) 915-920
24. Liu P., Jenkins N.A., and Copeland N.G. Efficient Cre-loxP-induced mitotic recombination in mouse embryonic stem cells. Nat Genet 30 (2002) 66-72
25. Armakolas A., and Klar A.J. Cell type regulates selective segregation of mouse chromosome 7 DNA strands in mitosis. Science 311 (2006) 1146-1149
26. Klar A.J. A model for specification of the left-right axis in vertebrates. Trends Genet 10 (1994) 392-396
27. Klar A.J. A genetic mechanism implicates chromosome 11 in schizophrenia and bipolar diseases. Genetics 167 (2004) 1833-1840
28. Haber J.E. Comment on "Cell type regulates selective segregation of mouse chromosome 7 DNA strands in mitosis". Science 313 (2006) 1045 author reply 1045
29. Klar A.J., and Armakolas A. Response to comment on "cell type regulates selective segregation of mouse chromosome 7 DNA strands in mitosis". Science 313 (2006) 1045c. These studies extend the findings reported in Ref. [24] demonstrating that X-segregation also occurs in eukaryotes. The authors show biased segregation of chromosome 7, but not chromosome 11, in ES and endoderm cells and Z-segregation in neuroectoderm cells.
30. Sapienza C. Molecular biology. Do Watson and Crick motor from X to Z?. Science 315 (2007) 46-47
31. Beumer K.J., Pimpinelli S., and Golic K.G. Induced chromosomal exchange directs the segregation of recombinant chromatids in mitosis of Drosophila. Genetics 150 (1998) 173-188
32. Armakolas A., and Klar A.J. Left-right dynein motor implicated in selective chromatid segregation in mouse cells. Science 315 (2007) 100-101. This study is a follow-up of Ref. [25] where RNA interference against dynein resulted in the loss of biased segregation of chromosome 7 in ES-derived cells, thereby implicating the dynein motor, which plays a key role in left-right asymmetry during development.
33. Klar A.J. Lessons learned from studies of fission yeast mating-type switching and silencing. Annu Rev Genet 41 (2007) 213-236
34. Fijalkowska I.J., Jonczyk P., Tkaczyk M.M., Bialoskorska M., and Schaaper R.M. Unequal fidelity of leading strand and lagging strand DNA replication on the Escherichia coli chromosome. Proc Natl Acad Sci U S A 95 (1998) 10020-10025
35. Zheng H., Hasty P., Brenneman M.A., Grompe M., Gibbs R.A., Wilson J.H., and Bradley A. Fidelity of targeted recombination in human fibroblasts and murine embryonic stem cells. Proc Natl Acad Sci U S A 88 (1991) 8067-8071
36. Brugmans L., Kanaar R., and Essers J. Analysis of DNA double-strand break repair pathways in mice. Mutat Res 614 (2007) 95-108
37. Groth A., Rocha W., Verreault A., and Almouzni G. Chromatin challenges during DNA replication and repair. Cell 128 (2007) 721-733
38. Lew D.J., Burke D.J., and Dutta A. The immortal strand hypothesis: how could it work?. Cell 133 (2008) 21-23
39. Lucchini R., Wellinger R.E., and Sogo J.M. Nucleosome positioning at the replication fork. EMBO J 20 (2001) 7294-7302
40. Smith S., and Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58 (1989) 15-25
41. Weintraub H., Worcel A., and Alberts B. A model for chromatin based upon two symmetrically paired half-nucleosomes. Cell 9 (1976) 409-417
42. Stancheva I., Koller T., and Sogo J.M. Asymmetry of Dam remethylation on the leading and lagging arms of plasmid replicative intermediates. EMBO J 18 (1999) 6542-6551
43. Ekwall K. Epigenetic control of centromere behavior. Annu Rev Genet 41 (2007) 63-81
44. Klar A.J. Differentiated parental DNA strands confer developmental asymmetry on daughter cells in fission yeast. Nature 326 (1987) 466-470
45. Azimzadeh J., and Bornens M. Structure and duplication of the centrosome. J Cell Sci 120 (2007) 2139-2142
46. Yamashita Y.M., Mahowald A.P., Perlin J.R., and Fuller M.T. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315 (2007) 518-521. Experiments in the Drosophila male germline show that mother and daughter centrosomes segregate asymmetrically during consecutive divisions. Importantly, the mother centrosome remains associated with the stem cell localised in the niche suggesting that this choice may be associated with other decisions regarding the fate of the self-renewing stem cell.
47. Higuchi T., and Uhlmann F. Stabilization of microtubule dynamics at anaphase onset promotes chromosome segregation. Nature 433 (2005) 171-176. This study elegantly shows that stabilization of microtubule attachment at the kinetochore is a requisite for the progression into anaphase.
48. Maiato H., Rieder C.L., and Khodjakov A. Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J Cell Biol 167 (2004) 831-840
49. Mahoney N.M., Goshima G., Douglass A.D., and Vale R.D. Making microtubules and mitotic spindles in cells without functional centrosomes. Curr Biol 16 (2006) 564-569
50. Kapoor T.M., Lampson M.A., Hergert P., Cameron L., Cimini D., Salmon E.D., McEwen B.F., and Khodjakov A. Chromosomes can congress to the metaphase plate before biorientation. Science 311 (2006) 388-391. This study demonstrates that mono-oriented chromosomes can migrate to the metaphase plate during mitosis. This raises the question how chromatic choice is decided for microtubule attachment, and whether this is a random or selective event.