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Chapter 24 : A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review

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A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, Page 1 of 2

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Abstract:

Cells of the highly diverged and fission yeasts exist in one of the two sex/mating types, called P (for plus) or M (for minus), specified by which allele, or , resides at ( Fig. 1 ). The fission yeasts have evolved an elegant mechanism for switching P or M information at by a programmed DNA recombination event with a copy of one of the two silent mating-type genes residing nearby in the genome. The switching process is highly cell-cycle and generation dependent such that only one of four grandchildren of a cell switches mating type, and switching occurs in nearly half the cells of a population. Such a change of cell type is analogous to the stem-cell division found in higher eukaryotes whereby sister cells differ in their fate. Extensive studies of fission yeast established the natural DNA strand chirality at the locus as the primary basis of asymmetric cell division. This asymmetry results from a unique site- and strand-specific epigenetic “imprint” at installed in one of the two chromatids during DNA replication. The imprint is inherited by only one daughter cell, maintained for one cell cycle, and then used for initiating recombination during replication. The progression through two replication cycles and two cell divisions leads to the “one-in-four” switching proportion among granddaughter cells. This mechanism of cell-type switching is considered to be unique to these two organisms, but determining the operation of such a mechanism in other organisms has not been possible for technical reasons. Thus, the validity of this mechanism for development in general remains untested. This review summarizes recent exciting developments in understanding the mechanism of switching in fission yeasts and extends these observations to suggest how such a DNA strand-based mechanism of cellular differentiation could also operate in diploid organisms. Although the analogous cell-type switching found in the budding yeast by HO-endonuclease cleavage of the mating-type locus appears superficially similar to that of fission yeast, the mechanistic details are very different in these organisms. Thus, studies with diverse single-celled model yeast organisms have been helpful to appreciate how different paradigms of cellular differentiation have evolved. Considering that the ultimate basis of cellular differentiation in yeast is the double-helical structure of DNA, it is likely that such a mechanism operates in higher eukaryotes as well.

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014

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Figures

Image of Figure 1
Figure 1

The mating-type region and -switching process. The mating-type region comprises three genetic cassettes located on chromosome 2 at the indicated distances from each other in the order shown. The P-specific region, existing in both and loci, is 1,113-bp long and the M-specific sequence in and is 1,127-bp long ( ). Recombination is facilitated by short homology boxes, which flank all cassettes. The cassette proximal homology box H1 is 135-bp long; the distal H2 element is 59-bp long. switching occurs when genetic information copied from the or locus is unidirectionally transmitted to the locus (curved horizontal arrows), where it displaces the previously existing allele. A unique epigenetic imprint (star) found at initiates the recombination leading to switching. Whereas the locus is transcriptionally active and dictates cell type, the -K- region is transcriptionally silenced by another kind of epigenetic mechanism (reviewed in reference ). Thus, the cell type is defined only by the locus even though genetic information for both mating types resides elsewhere in the chromosome. doi:10.1128/microbiolspec.MDNA3-0003-2014.f1

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014
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Image of Figure 2
Figure 2

Staining phenotype of patches of cells growing on sporulation medium with iodine vapors. The patches are exposed to iodine vapors for about two minutes. Cell patches (or colonies, not shown) of the wild-type ( ) strain are composed of a mixture of P and M cells that engage in efficient mating and sporulation. Such patches stain black because they contain asci with spores that synthesize a starch-like compound that is stained by iodine vapors. The patch of cells fails to stain, indicating their switching defect. doi:10.1128/microbiolspec.MDNA3-0003-2014.f2

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014
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Image of Figure 3
Figure 3

The one-in-four granddaughters switching pattern of yeast cells. The star indicates a cell that inherits the imprint from the parent cell, making it switching competent so that it will produce one of the daughters that is switched. The same pattern is observed when cells switch from M to P. Pu, unswitchable cell; Ps, switchable cell. doi:10.1128/microbiolspec.MDNA3-0003-2014.f3

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014
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Image of Figure 4
Figure 4

The imprint creates a fragile site in DNA. Southern blot analysis of DNA extracted from a wild type and from an imprint-deficient yeast strain is shown. The DNA was digested with dIII endonuclease, and the resulting blot was probed with a radiolabeled DNA fragment containing the cassette. The intensity of the signal of each fragment reflects the extent of DNA sequence homology between the cassettes. The imprint causes a fragile site in DNA that results in a double-stranded break during conventional methods of DNA extraction. The imprint level is much reduced in the mutant. doi:10.1128/microbiolspec.MDNA3-0003-2014.f4

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014
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Figure 5

-acting sequence elements and -acting factors required for imprinting. See the text for details. doi:10.1128/microbiolspec.MDNA3-0003-2014.f5

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014
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Image of Figure 6
Figure 6

The selective chromatid recombination and arms-swapping model of the hotspot recombination. Recombination occurs only between nonsister chromatids numbers 1 and 3, and only when they simultaneously have a DNA break/nick (\\) in the S/G2 phase of the cell. To depict specific strand distribution, template Watson (W) strands are colored blue and Crick (C) strands are colored red. Strands synthesized in the present replication cycle are indicated in black. The symbol X represents the crossover point at . The figure is modified from reference . doi:10.1128/microbiolspec.MDNA3-0003-2014.f6

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014
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Image of Figure 7
Figure 7

The SSIS model. The model ( ) predicts the evolution of two phenomena. One causes production of nonequivalent sister chromatids through epigenetic means to express differentially a developmentally important gene in the Watson (W) versus Crick (C) strand/chromatid-specific fashion. The other causes nonrandom segregation of all four chromatids belonging to a pair of homologous chromosomes, or sets of chromosomes, in mitosis. To depict the diagrammed nonrandom segregation pattern, termed “W,W::C,C,” DNA strands are color-coded. The strands synthesized in the parent cell are depicted in black. A hypothetical -acting segregator factor is proposed to function by acting at the centromere to mediate selective chromatid segregation at a specific cell division in development to promote asymmetric cell division. Lateralized organs could be derived from the progeny of thus differentiated daughter cells. The selective chromatid segregation model has recently been invoked to explain the neurological disorder, congenital mirror hand movement [MIM 157600], which occurs in 50% of human subjects. In the absence of selective chromatid segregation, random segregation for a specific chromosome at a specific cell division is proposed to impact the laterality development of the brain hemispheres ( ). Similarly, the observation of 50% penetrance of psychosis disorder development in individuals with chromosome 11 translocations is consistent with translocation-caused anomalies of the SSIS mechanism. ( ). doi:10.1128/microbiolspec.MDNA3-0003-2014.f7

Citation: Klar A, Ishikawa K, Moore S. 2015. A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review, p 515-528. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0003-2014
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References

/content/book/10.1128/9781555819217.chap24
1. Egel R, . 1989. Mating-type genes, meiosis and sporulation, p 3174. In Nasim A,, Young P,, Johnson B (ed), Molecular Biology of the Fission Yeast. Academic Press, New York, NY. [CrossRef]
2. Gutz H,, Schmidt H . 1990. The genetic basis of homothallism and heterothallism in Saccharomyces cerevisiae and Schizosaccharomyces pombe . Semin Dev Biol 1 : 169176.
3. Dalgaard JZ,, Klar AJS . 2001. Does S. pombe exploit the intrinsic asymmetry of DNA synthesis to imprint daughter cells for mating-type switching? Trends Genet 17 : 153157.[PubMed] [CrossRef]
4. Arcangioli B,, Thon G, . 2004. Mating-type cassettes: structure, switching and silencing, p 129147. In Egel R (ed), The Molecular Biology of Schizosaccharomyces pombe. Springer Verlag, Berlin, Germany. [CrossRef]
5. Klar AJS . 2007. Lessons learned from studies of fission yeast mating-type switching and silencing. Ann Rev Genet 41 : 213236.[PubMed] [CrossRef]
6. Kelly M,, Burke J,, Smith M,, Klar A,, Beach D . 1988. Four mating-type genes control sexual differentiation in the fission yeast. EMBO J 7 : 15371547.[PubMed]
7. Klar AJS,, Miglio LM . 1986. Initiation of meiotic recombination by double-strand DNA breaks in S. pombe . Cell 46 : 725731.[PubMed] [CrossRef]
8. Bresch C,, Muller G,, Egel R . 1968. Genes involved in meiosis and sporulation of a yeast. Mol Gen Genet 102 : 301306.[PubMed] [CrossRef]
9. Leupold U . 1950. Die vererbung von homothallie and heterothallie bei Schizosaccharomyces pombe . C R Trav Lab Carlsberg Ser Physiol 24 : 381480.
10. Beach DH,, Klar AJS . 1984. Rearrangements of the transposable mating-type cassettes of fission yeast. EMBO J 3 : 603610.[PubMed]
11. Singh J . 1999. Mating type switching in fission yeast: a unique model for development and differentiation. Curr Sci 77 : 12621272.
12. Egel R . 1977. Frequency of mating-type switching in homothallic fission yeast. Nature 266 : 172174.[PubMed] [CrossRef]
13. Miyata H,, Miyata M . 1981. Mode of conjugation in homothallic cells of Schizosaccharomyces pombe . J Gen Appl Microbiol 27 : 365371.[CrossRef]
14. Egel R,, Eie E . 1987. Cell lineage asymmetry for Schizosaccharomyces pombe: unilateral transmission of a high-frequency state of mating-type switching in diploid pedigrees. Curr Genet 3 : 512.[PubMed] [CrossRef]
15. Klar AJS . 1990. The developmental fate of fission yeast cells is determined by the pattern of inheritance of parental and grandparental DNA strands. EMBO J 9 : 14071415.[PubMed]
16. Egel R, . 1977. “Flip-flop” control and transposition of mating-type genes in fission yeast, p 446455. In Bukhar AJ,, Shapiro J,, Adhya S (ed), DNA Insertion Elements, Plasmids and Episomes. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
17. Klar AJS,, Fogel S . 1979. Activation of mating type genes by transposition in Saccharomyces cerevisiae . Proc Natl Acad Sci USA 76 : 45394543.[CrossRef]
18. Hicks J,, Strathern JN,, Klar AJ . 1979. Transposable mating type genes in Saccharomyces cerevisiae . Nature 282 : 478– 473.[PubMed] [CrossRef]
19. Klar AJS . 2010. The yeast mating-type switching mechanism: a memoir. Genetics 186 : 443– 449.[PubMed] [CrossRef]
20. Egel R . 1984. The pedigree pattern of mating-type switching in Schizosaccharomyces pombe . Curr Genet 8 : 205210.[PubMed] [CrossRef]
21. Egel R . 1984. Two tightly linked silent cassettes in the mating type region of Schizosaccharomyces pombe . Curr Genet 8 : 199203.[PubMed] [CrossRef]
22. Beach DH . 1983. Cell type switching by DNA transposition in fission yeast. Nature 305 : 682688.[CrossRef]
23. Strathern JN,, Klar AJ,, Hicks JB,, Abraham JA,, Ivy JM,, Nasmyth KA,, McGill C . 1982. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31 : 183192.[PubMed] [CrossRef]
24. Egel R,, Beach DH,, Klar AJS . 1984. Genes required for initiation and resolution steps of mating-type switching in fission yeast. Proc Natl Acad Sci USA 81 : 34813485.[PubMed] [CrossRef]
25. Gutz H,, Schmidt H . 1985. Switching genes in Schizosaccharomyces pombe . Curr Genet 9 : 325331.[PubMed] [CrossRef]
26. Klar AJS . 1987. Differentiated parental DNA strands confer developmental asymmetry on daughter cells in fission yeast. Nature 326 : 466– 470.[PubMed] [CrossRef]
27. Ostermann K,, Lorentz A,, Schmidt H . 1993. The fission yeast rad22 gene, having a function in mating-type switching and repair of DNA damages, encodes a protein homolog to Rad52 of Saccharomyces cerevisiae. Nucleic Acids Res 21 : 59405944.[PubMed] [CrossRef]
28. Schmidt H,, Kapitza P,, Gutz H . 1987. Switching genes in Schizosaccharomyces pombe: their influence on cell viability and recombination. Curr Genet 11 : 303308.[CrossRef]
29. Klar AJS,, Bonaduce MJ . 1993. The mechanism of fission yeast mating-type interconversion: evidence for two types of epigenetically inherited chromosomal imprinted events. Cold Spring Harb Symp Quant Biol 58 : 457– 465.[PubMed] [CrossRef]
30. Dalgaard JZ,, Klar AJS . 1999. Orientation of DNA replication establishes mating-type switching pattern in S. pombe . Nature 400 : 181184.[PubMed] [CrossRef]
31. Dalgaard JZ,, Klar AJS . 2001. A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at mat1 in S. pombe . Genes Dev 15 : 20602068.[PubMed] [CrossRef]
32. Arcangioli B . 1998. A site- and strand-specific DNA break confers asymmetric switching potential in fission yeast. EMBO J 17 : 45034510.[PubMed] [CrossRef]
33. Nielsen O,, Egel R . 1989. Mapping the double-strand breaks at the mating-type locus in fission yeast by genomic sequencing. EMBO J 8 : 269276.[PubMed]
34. Holmes AM,, Kaykov A,, Arcangioli B . 2005. Molecular and cellular dissection of mating-type switching steps in Schizosaccharomyces pombe . Mol Cell Biol 25 : 303311.[PubMed] [CrossRef]
35. Arcangioli B,, Klar AJS . 1991. A novel switch-activating site (SAS1) and its cognate binding factor (SAP1) required for efficient mat1 switching in Schizosaccharomyces pombe . EMBO J 10 : 30253032.[PubMed]
36. Dalgaard JZ,, Klar AJS . 2000. swi1 and swi3 perform imprinting, pausing, and termination of DNA replication in S. pombe . Cell 102 : 745751.[PubMed] [CrossRef]
37. Sayrac S,, Vengrova S,, Godfrey EL,, Dalgaard JZ . 2011. Identification of a novel type of spacer element required for imprinting in fission yeast. PLoS Genet 7 : e1001328. [PubMed] [CrossRef]
38. Arcangioli B,, Copeland TD,, Klar AJ . 1994. Sap1, a protein that binds to sequences required for mating-type switching, is essential for viability in Schizosaccharomyces pombe . Mol Cell Biol 14 : 20582065.[PubMed]
39. Holmes A,, Roseaulin L,, Schurra C,, Waxin H,, Lambert S,, Zaratiegul M,, Martienssen RA,, Arcangioli B . 2012. Lsd1 and lsd2 control programmed replication fork pauses and imprinting in fission yeast. Cell Rep 2 : 15131520.[PubMed] [CrossRef]
40. Singh J,, Klar AJS . 1993. DNA polymerase-alpha is essential for mating-type switching in fission yeast. Nature 361 : 271273.[PubMed] [CrossRef]
41. Lee BS,, Grewal SI,, Klar AJ . 2004. Biochemical interactions between proteins and mat1 cis-acting sequences required for imprinting in fission yeast. Mol Cell Biol 24 : 98139822.[PubMed] [CrossRef]
42. McFarlane RJ,, Mian S,, Dalgaard JZ . 2010. The many facets of the Tim-Tipin protein families’ roles in chromosome biology. Cell Cycle 9 : 700705.[PubMed] [CrossRef]
43. Dalgaard JZ . 2012. Causes and consequences of ribonucleotide incorporation into nuclear DNA. Trends Genet 28 : 592597.[PubMed] [CrossRef]
44. Kaykov A,, Arcangioli B .. 2004. A programmed strand-specific and modified nick in S. pombe constitutes a novel type of chromosomal imprint. Curr Biol 14 : 19241928.[PubMed] [CrossRef]
45. Kaykov A,, Holmes AM,, Arcangioli B . 2004. Formation, maintenance and consequences of the imprint at the mating-type locus in fission yeast. EMBO J 23 : 930938.[PubMed] [CrossRef]
46. Roseaulin L,, Yamada Y,, Tsutsui Y,, Russell P,, Iwasaki H,, Arcangioli B . 2008. Mus81 is essential for sister chromatid recombination at broken replication forks. EMBO J 27 : 13781387.[PubMed] [CrossRef]
47. Arcangioli B,, de Lahondes R . 2000. Fission yeast switches mating type by a replication-recombination coupled process. EMBO J 19 : 13891396.[PubMed] [CrossRef]
48. Yamada-Inagawa T,, Klar AJS,, Dalgaard JZ . 2007. Schizosaccharomyces pombe switches mating type by the synthesis-dependent strand-annealing mechanism. Genetics 177 : 255265.[PubMed] [CrossRef]
49. Resnick MA . 1976. The repair of double-strand breaks in DNA: a model involving recombination. J Theor Biol 59 : 97106.[PubMed] [CrossRef]
50. Szostak JW,, Orr-Weaver TL,, Rothstein RJ,, Stahl FW . 1983. The double-strand-break repair model for recombination. Cell 33 : 2535.[PubMed] [CrossRef]
51. Arcangioli B . 2000. Fate of mat1 DNA strands during mating-type switching in fission yeast. EMBO Rep 1 : 145150.[PubMed] [CrossRef]
52. Thon G,, Klar AJS . 1993. Directionality of fission yeast mating-type interconversion is controlled by the location of the donor loci. Genetics 134 : 10451054.[PubMed]
53. Jakociunas T,, Holm LR,, Verhein-Hansen J,, Trusina A,, Thon G . 2013. Two portable recombination enhancers direct donor choice in fission yeast heterochromatin. PLoS Genet 9 : e1003762. [PubMed] [CrossRef]
54. Jia S,, Yamada T,, Grewal SI . 2004. Heterochromatin regulates cell type-specific long-range chromatin interactions essential for directed recombination. Cell 119 : 469– 480.[PubMed] [CrossRef]
55. Akamatsu Y,, Dziadkowiec D,, Ikeguchi M,, Shinagawa H,, Iwasaki H . 2003. Two different Swi5-containing protein complexes are involved in mating-type switching and recombination repair in fission yeast. Proc Natl Acad Sci USA 100 : 1577015775.[PubMed] [CrossRef]
56. Aguilar-Arnal L,, Marsellach FX,, Azorin F . 2008. The fission yeast homologue of CENP-B, Abp1, regulates directionality of mating-type switching. EMBO J 27 : 10291038.[PubMed] [CrossRef]
57. Matsuda E,, Sugioka-Sugiyama R,, Mizuguchi T,, Mehta S,, Cui BC,, Grewal SI . 2011. A homolog of male sex-determining factor SRY cooperates with a transposon-derived CENP-B protein to control sex-specific directed recombination. Proc Natl Acad Sci USA 108 : 1875418759.[PubMed] [CrossRef]
58. Yu C,, Bonaduce MJ,, Klar AJS . 2012. Going in the right direction: mating-type switching of Schizosaccharomyces pombe is controlled by judicious expression of two different swi2 transcripts. Genetics 190 : 977987.[PubMed] [CrossRef]
59. Grewal SI,, Klar AJS . 1997. A recombinationally repressed region between mat2 and mat3 loci shares homology to centromeric repeats and regulates directionality of mating-type switching in fission yeast. Genetics 146 : 12211238.[PubMed]
60. Ivanova AV,, Bonaduce MJ,, Ivanov SV,, Klar AJS . 1998. The chromo and SET domains of the Clr4 protein are essential for silencing in fission yeast. Nat Genet 19 : 192195.[PubMed] [CrossRef]
61. Tuzon CT,, Borgstrom B,, Weilguny D,, Egel R,, Cooper JP,, Nielsen O . 2004. The fission yeast heterochromatin protein Rik1 is required for telomere clustering during meiosis. J Cell Biol 165 : 759765.[PubMed] [CrossRef]
62. Thon G,, Hansen KR,, Altes SP,, Sidhu D,, Singh G,, Verhein-Hansen J,, Bonaduce MJ,, Klar AJS . 2005. The Clr7 and Clr8 directionality factors and the Pcu4 cullin mediate heterochromatin formation in the fission yeast Schizosaccharomyces pombe . Genetics 171 : 15831595.[PubMed] [CrossRef]
63. Angehrn P,, Gutz H . 1968. Influence of mating type on mitotic crossing-over in Schizosaccharomyces pombe . Genetics 60 : 158.
64. Egel R . 1981. Mating-type switching and mitotic crossing-over at the mating-type locus in fission yeast. Cold Spring Harb Symp Quant Biol 45 : 10031007.[PubMed] [CrossRef]
65. Klar AJS,, Bonaduce MJ . 2013. Unbiased segregation of fission yeast chromosome 2 strands to daughter cells. Chromosome Res 21 : 297309.[PubMed] [CrossRef]
66. Rhind N,, Chen ZH,, Yassour M,, Thompson DA,, Haas BJ,, Habib N,, Wapinski I,, Roy S,, Lin MF,, Heiman DI,, Young SK,, Furuya K,, Guo YB,, Pidoux A,, Chen HM,, Robbertse B,, Goldberg JM,, Aoki K,, Bayne EH,, Berlin AM,, Desjardins CA,, Dobbs E,, Dukaj L,, Fan L,, FitzGerald MG,, French C,, Gujja S,, Hansen K,, Keifenheim D,, Levin JZ,, Mosher RA,, Muller CA,, Pfiffner J,, Priest M,, Russ C,, Smialowska A,, Swoboda P,, Sykes SM,, Vaughn M,, Vengrova S,, Yoder R,, Zeng QD,, Allshire R,, Baulcombe D,, Birren BW,, Brown W,, Ekwall K,, Kellis M,, Leatherwood J,, Levin H,, Margalit H,, Martienssen R,, Nieduszynski CA,, Spatafora JW,, Friedman N,, Dalgaard JZ,, Baumann P,, Niki H,, Regev A,, Nusbaum C . 2011. Comparative functional genomics of the fission yeasts. Science 332 : 930936.[PubMed] [CrossRef]
67. Yu C,, Bonaduce MJ,, Klar AJS . 2013. Defining the epigenetic mechanism of asymmetric cell division of Schizosaccharomyces japonicus yeast. Genetics 193 : 8594.[PubMed] [CrossRef]
68. Grewal SIS,, Klar AJS . 1996. Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell 86 : 95101.[PubMed] [CrossRef]
69. Thon G,, Friis T . 1997. Epigenetic inheritance of transcriptional silencing and switching competence in fission yeast. Genetics 145 : 685696.[PubMed]
70. Klar AJS . 1998. Propagating epigenetic states through meiosis: where Mendel’s gene is more than a DNA moiety. Trends Genet 14 : 299301.[PubMed] [CrossRef]
71. Klar AJS . 1994. A model for specification of the left-right axis in vertebrates. Trends Genet 10 : 392396.[PubMed] [CrossRef]
72. Klar AJS . 2004. A genetic mechanism implicates chromosome 11 in schizophrenia and bipolar diseases. Genetics 167 : 18331840.[PubMed] [CrossRef]
73. Armakolas A,, Klar AJS . 2006. Cell type regulates selective segregation of mouse chromosome 7 DNA strands in mitosis. Science 311 : 11461149.[PubMed] [CrossRef]
74. Armakolas A,, Klar AJS . 2007. Left–right dynein motor implicated in selective chromatid segregation in mouse cells. Science 315 : 100101.[PubMed] [CrossRef]
75. Sauer S,, Klar AJS . 2013. Reply to “Chromosome-specific nonrandom sister chromatid segregation during stem-cell division.” Nature 498 : 254256.
76. Klar AJS . 2014. Selective chromatid segregation mechanism invoked for the human congenital mirror hand movement disorder development by RAD51 mutations: A hypothesis. Int J Biol Sci 2014; 10(9): 10181023. doi:10.7150/ijbs.9886. Available from http://www.ijbs.com/v10p1018.htm [PubMed] [CrossRef]
77. Klar AJS . 2014. Selective Chromatid Segregation Mechanism Explains the Etiology of Chromosome 11 Translocation-Associated Psychotic Disorders: A Review. J Neurol Disord 2 : 173. doi:10.4172/2329-6895.1000173 [CrossRef]

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