Discovery of the mitotic selective chromatid segregation phenomenon and its implications for vertebrate development

Current Opinion in Cell Biology

Volumn 22, Issue 1, 2010, Pages 81-87

  Armakolas, A ^a   Koutsilieris, M ^a   Klar, AJS ^b  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

CELL DIFFERENTIATION; CELL DIVISION; CHROMOSOME 7; CHROMOSOME SEGREGATION; DNA REPLICATION; DNA SEQUENCE; DNA STRAND; EMBRYO DEVELOPMENT; EUKARYOTE; GENE EXPRESSION; GENE MUTATION; GENETIC MARKER; GENOME; HUMAN; MOLECULAR IMPRINTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SISTER CHROMATID;

ANIMALS; BODY PATTERNING; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CHROMATIDS; CHROMOSOME SEGREGATION; DNA REPLICATION; DROSOPHILA MELANOGASTER; DYNEINS; MICE; MITOSIS; MITOTIC SPINDLE APPARATUS;

CAENORHABDITIS ELEGANS; EUKARYOTA; MUS; SCHIZOSACCHAROMYCETACEAE; VERTEBRATA;

EID: 75749112937     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2009.11.006     Document Type: Review

References (51)

1. Ephrussi A., and Johnston D. Seeing is believing: the bicoid morphogen gradient matures. Cell 116 (2004) 143-152
2. Tabin C., and Wolpert L. Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes Dev 21 (2007) 1433-1442
3. Tickle C. Morphogen gradients in vertebrate limb development. Semin Cell Dev Biol 10 (1999) 345-351
4. Yamashita Y.M., and Fuller M.T. Asymmetric centrosome behavior and the mechanisms of stem cell division. J Cell Biol 180 (2008) 261-266
5. Lin H. The stem-cell niche theory: lessons from flies. Nat Rev Genet 3 (2002) 931-940
6. Lin H. To be and not to be. Nature 425 (2003) 353-355
7. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 132 (2008) 583-597
8. Gönczy P. Mechanisms of asymmetric cell division: flies and worms pave the way. Nat Rev Mol Cell Biol 9 (2008) 355-366
9. Meselson M., and Stahl F.W. The replication of DNA. Proc Natl Acad Sci USA 44 (1958) 671-682
10. Klar A.J.S. A genetic mechanism implicates chromosome 11 in schizophrenia and bipolar diseases. Genetics 167 (2004) 1833-1840
11. Klar A.J.S. A model for specification of the left-right axis in vertebrates. Trends Genet 10 (1994) 392-396
12. Klar A.J.S. The developmental fate of fission yeast cells is determined by the pattern of inheritance of parental and grandparental DNA strands. EMBO J 9 (1990) 1407-1415
13. Klar A.J.S. Lessons learned from studies of fission yeast mating-type switching and silencing. Ann Rev Genet 41 (2007) 213-236. This review describes the evidence of asymmetric cell division in fission yeast concerning mat1 locus, where a strand-specific imprint leads to the production of non-equivalent sister chromatids. It also gives more insight about the biological importance of segregation phenomenon that might be operating in mammalian cells.
14. Fuchs E. Skin stem cells: rising to the surface. J Cell Biol 180 (2008) 273-284
15. Karpowicz P., Morshead C., Kam A., Jervis E., Ramunas J., Cheng V., and Van der Kooy D. Support of the immortal strand hypothesis: neural stem cell partition DNA asymmetrically in vitro. J Cell Biol 170 (2005) 721-732
16. Merok J.R., Lansita J.A., Tunstead J.R., and Sherley J.L. Co-segregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell kinetics. Cancer Res 62 (2002) 6791-6795
17. Potten C.S. Keratinocyte stem cells, label-retaining cells and possible genome protection mechanisms. J Invest Dermatol Symp Proc 9 (2004) 183-195
18. 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
19. Shinin V., Gayrud-Morel B., Gomes D., and Tajbakhsh S. Asymmetric cell division and co-segregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8 (2006) 677-687. The authors used pulse-chase labeling with BrdU to mark the putative stem-cell niche and identified a subpopulation of label-retaining satellite cells during growth after injury. It is suggested that some of these cells display selective template-DNA strand segregation during mitosis in the muscle fiber in vivo, as well as in cultures independent of their niche.
20. Smith G.H. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 132 (2005) 721-732
21. Cairns J. Mutation selection and the natural history of cancer. Nature 255 (1975) 197-200
22. Armakolas A., and Klar A.J.S. Cell type regulates selective segregation of mouse chromosome 7 DNA strands in mitosis. Science 311 (2006) 1146-1149. By analyzing recombination events of chromosome 7 homologs of mouse cells, the study showed that embryonic stem cells and neuroectoderm cells exhibit non-random chromatid distribution, whereas the mode of distribution is random in mesoderm, cardiomyocyte, and pancreatic cells.
23. Liu P., Jenkins A.N., and Copeland N.G. Efficient Cre-loxP-induced mitotic recombination in mouse embryonic stem cells. Nat Genet 30 (2002) 66-72. Here the authors demonstrate that mitotic recombination can be reproducibly induced in mouse embryonic stem (ES) cells, by Cre/loxP technology, after transient Cre expression. Notably, much of the recombination occurs in G2 and is followed by unusually by 'X segregation', thus recombinant chromatids segregate away from each other during mitosis.
24. 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
25. Pimpinelli S., and Ripoll P. Nonrandom segregation of centromeres following mitotic recombination in Drosophila melanogaster. Proc Natl Acad Sci USA 83 (1986) 3900-3903
26. Tsai C.L., Rowntree R.K., Cohen D.E., and Lee J.T. Higher order chromatin structure at the X-inactivation center via looping DNA. Dev Biol 319 (2008) 416-425
27. Danos M.C., and Yost H.J. Linkage of cardiac left-right asymmetry and dorsal-anterior development in Xenopus. Development 121 (1995) 1467-1474
28. Danos M.C., and Yost H.J. Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev Biol 177 (1996) 96-103
29. Goldstein A.M., Ticho B.S., and Fishman M.C. Patterning the heart's left-right axis: from zebrafish to man. Dev Genet 22 (1998) 278-287
30. Lohr J.L., Danos M.C., and Yost H.J. Left-right asymmetry of a nodal-related gene is regulated by dorso-anterior midline structures during Xenopus development. Development 124 (1997) 1465-1472
31. Bellomo D., Lander A., Harragan I., and Brown N.A. Cell proliferation in mammalian gastrulation: the ventral node and notochord are relatively quiescent. Dev Dyn 205 (1996) 471-485
32. Vaisberg E.A., Grissom P.M., and McIntosh J.R. Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J Cell Biol 133 (1996) 831-841
33. Layton W.M. Heart malformations in mice homozygous for a gene causing situs inversus. Birth Defects Orig Artic Ser 14 (1978) 277-293
34. Supp D.M., Brueckner M., Kuehn M.R., Witte D.P., Lowe L.A., McGrath J., Corrales J.M., and Potter S.S. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development 126 (1999) 5495-5504
35. Afzelius B.A. Cilia-related diseases. J Pathol 204 (2004) 470-477
36. Armakolas A., and Klar A.J.S. Left-right dynein motor implicated in selective chromatid segregation in mouse cells. Science 315 (2007) 100-101. In this paper the involvement of the mouse left-right dynein (LRD) in the mechanism of differential segregation is demonstrated. Additionally, since gene mutations in the LRD gene result in randomization of visceral organs' laterality, they hypothesized that the organ laterality may be mediated by selective chromatid segregation phenomenon.
37. McGrath J., and Brueckner M. Cilia are at the heart of vertebrate left-right asymmetry. Curr Opin Genet Dev 13 (2003) 385-392
38. Qiu D., Cheng S.M., Wozniak L., McSweeney M., Perrone E., and Levin M. Localization and loss-of-function implicates ciliary proteins in early, cytoplasmic roles in left-right asymmetry. Dev Dyn 234 (2005) 176-189
39. Tabin C. Do we know anything about how left-right asymmetry is first established in the vertebrate embryo?. J Mol Histol 36 (2005) 317-323
40. Tabin C.J., and Vogan K.J. A two-cilia model for vertebrate left-right axis specification. Genes Dev 17 (2003) 1-6
41. Nonaka S., Shiratori H., Saijoh Y., and Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418 (2002) 96-99
42. Brown N.A., and Wolpert L. The development of handedness in left/right asymmetry. Development 109 (1990) 1-9
43. Watson J.D., and Crick F.H. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171 (1953) 737-738
44. Klar A.J.S. Differentiated parental DNA strands confer developmental asymmetry on daughter cells in fission yeast. Nature 326 (1987) 466-470
45. Shibahara K., and Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96 (1999) 575-585
46. Klar A.J.S. Support for the selective chromatid segregation hypothesis advanced for the mechanism of left-right body axis development in mice. Breast Dis 26 (2008) 47-56. This paper presents detailed predictions of the SSIS model concerning lrd mutant's developmental phenotypes.
47. Karpowicz P., Pellikka M., Chea E., Godt D., Tepass U., and Van der Kooy D. The germline stem cells of Drosophila melanogaster partition DNA non-randomly. Eur J Cell Biol 88 (2009) 397-408. The authors suggest that non-random partitioning of some chromosome(s), but not of the entire genome, occurs in germline stem cells in the Drosophila ovary where they divide asymmetrically to generate a new germline stem cell and a differentiating cystoblast. This recent study supports the SSIS model for cellular differentiation through asymmetric stem-cell division.
48. Aw S., and Levin M. Is left-right asymmetry a form of planar cell polarity?. Development 3 (2009) 355-366
49. Knoblich J.A., Jan L.Y., and Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature 377 (1995) 624-627
50. Lew D.J., Burke D.J., and Dutta A. The immortal strand hypothesis: how could it work?. Cell 133 (2008) 21-23. In this mini-review, it is theorized that sister centormeres might be biochemically marked, such as by lagging-strand and leading-strand replication, to help biased segregation of all chromosomes according to the immortal strand hypothesis or only a set of chromosomes according to the SSIS hypothesis.
51. Tajbakhsh S., and Gonzalez C. Biased segregation of DNA and centromeres: moving together and drifting apart?. Nat Rev Mol Cell Biol 10 (2009) 804-810