Multiple Opposing Constraints Govern Chromosome Interactions during Meiosis
Homolog pairing and crossing over during meiosis I prophase is required for accurate chromosome segregation to form euploid gametes. The repair of Spo11-induced double-strand breaks (DSB) using a homologous chromosome template is a major driver of pairing in many species, including fungi, plants, and mammals. Inappropriate pairing and crossing over at ectopic loci can lead to chromosome rearrangements and aneuploidy. How (or if) inappropriate ectopic interactions are disrupted in favor of allelic interactions is not clear. Here we used an in vivo “collision” assay in budding yeast to test the contributions of cohesion and the organization and motion of chromosomes in the nucleus on promoting or antagonizing interactions between allelic and ectopic loci at interstitial chromosome sites. We found that deletion of the cohesin subunit Rec8, but not other chromosome axis proteins (e.g. Red1, Hop1, or Mek1), caused an increase in homolog-nonspecific chromosome interaction, even in the absence of Spo11. This effect was partially suppressed by expression of the mitotic cohesin paralog Scc1/Mdc1, implicating Rec8's role in cohesion rather than axis integrity in preventing nonspecific chromosome interactions. Disruption of telomere-led motion by treating cells with the actin polymerization inhibitor Latrunculin B (Lat B) elevated nonspecific collisions in rec8Δ spo11Δ. Next, using a visual homolog-pairing assay, we found that the delay in homolog pairing in mutants defective for telomere-led chromosome motion (ndj1Δ or csm4Δ) is enhanced in Lat B–treated cells, implicating actin in more than one process promoting homolog juxtaposition. We suggest that multiple, independent contributions of actin, cohesin, and telomere function are integrated to promote stable homolog-specific interactions and to destabilize weak nonspecific interactions by modulating the elastic spring-like properties of chromosomes.
Vyšlo v časopise:
Multiple Opposing Constraints Govern Chromosome Interactions during Meiosis. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003197
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003197
Souhrn
Homolog pairing and crossing over during meiosis I prophase is required for accurate chromosome segregation to form euploid gametes. The repair of Spo11-induced double-strand breaks (DSB) using a homologous chromosome template is a major driver of pairing in many species, including fungi, plants, and mammals. Inappropriate pairing and crossing over at ectopic loci can lead to chromosome rearrangements and aneuploidy. How (or if) inappropriate ectopic interactions are disrupted in favor of allelic interactions is not clear. Here we used an in vivo “collision” assay in budding yeast to test the contributions of cohesion and the organization and motion of chromosomes in the nucleus on promoting or antagonizing interactions between allelic and ectopic loci at interstitial chromosome sites. We found that deletion of the cohesin subunit Rec8, but not other chromosome axis proteins (e.g. Red1, Hop1, or Mek1), caused an increase in homolog-nonspecific chromosome interaction, even in the absence of Spo11. This effect was partially suppressed by expression of the mitotic cohesin paralog Scc1/Mdc1, implicating Rec8's role in cohesion rather than axis integrity in preventing nonspecific chromosome interactions. Disruption of telomere-led motion by treating cells with the actin polymerization inhibitor Latrunculin B (Lat B) elevated nonspecific collisions in rec8Δ spo11Δ. Next, using a visual homolog-pairing assay, we found that the delay in homolog pairing in mutants defective for telomere-led chromosome motion (ndj1Δ or csm4Δ) is enhanced in Lat B–treated cells, implicating actin in more than one process promoting homolog juxtaposition. We suggest that multiple, independent contributions of actin, cohesin, and telomere function are integrated to promote stable homolog-specific interactions and to destabilize weak nonspecific interactions by modulating the elastic spring-like properties of chromosomes.
Zdroje
1. GertonJL, HawleyRS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Gen 6: 477–487.
2. TsaiJH, McKeeBD (2011) Homologous pairing and the role of pairing centers in meiosis. J Cell Sci 124: 1955–1963.
3. HuntPA, HassoldTJ (2008) Human female meiosis: What makes a good egg go bad? Trends Genet 24: 86–93.
4. Jinks-RobertsonS, PetesTD (1986) Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes. Genetics 114: 731–752.
5. GoldmanA, LichtenM (1996) The Efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 144: 43–55.
6. LichtenM, BortsRH, HaberJE (1987) Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics 115: 233–246.
7. MisteliT, SoutoglouE (2009) The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol 10: 243–254.
8. BarzelA, KupiecM (2008) Finding a match: How do homologous sequences get together for recombination? Nat Rev Gen 9: 27–37.
9. MekhailK, SeebacherJ, GygiSP, MoazedD (2008) Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456: 667–670.
10. TaddeiA, SchoberH, GasserSM (2010) The budding yeast nucleus. Cold Spring Har Perspect Biol 2: a000612.
11. SchoberH, FerreiraH, KalckV, GehlenLR, GasserSM (2009) Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev 23: 928–938.
12. DavisL, SmithGR (2006) The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics 174: 167–177.
13. GoldmanASH, LichtenM (2000) Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci U S A 97: 9537–9542.
14. BhallaN, DernburgAF (2008) Prelude to a division. Ann Rev Cell and Dev Biol 24: 397–424.
15. WeinerBM, KlecknerN (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977–991.
16. StorlazziA, TesseS, GarganoS, JamesF, KlecknerN, et al. (2003) Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev 17: 2675–2687.
17. BowringFJ, YeadonPJ, StainerRG, CatchesideDE (2006) Chromosome pairing and meiotic recombination in Neurospora crassa spo11 mutants. Curr Gen 50: 115–123.
18. LoidlJ, KleinF, ScherthanH (1994) Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J Cell Biol 125: 1191–1200.
19. BaudatF, ManovaK, YuenJP, JasinM, KeeneyS (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6: 989–998.
20. DingDQ, YamamotoA, HaraguchiT, HiraokaY (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6: 329–341.
21. PeoplesTL, DeanE, GonzalezO, LambourneL, BurgessSM (2002) Close, stable homolog juxtaposition during meiosis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB-independent pairing contacts. Genes Dev 16: 1682–1695.
22. RomanienkoPJ, Camerini-OteroRD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6: 975–987.
23. PawlowskiWP, GolubovskayaIN, TimofejevaL, MeeleyRB, SheridanWF, et al. (2004) Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science 303: 89–92.
24. McKimKS, Green-MarroquinBL, SekelskyJJ, ChinG, SteinbergC, et al. (1998) Meiotic synapsis in the absence of recombination. Science 279: 876–878.
25. HughesSE, GillilandWD, CotittaJL, TakeoS, CollinsKA, et al. (2009) Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet 5: e1000348 doi:10.1371/journal.pgen.1000348.
26. DernburgAF, McDonaldK, MoulderG, BarsteadR, DresserM, et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387–398.
27. MacQueenAJ, PhillipsCM, BhallaN, WeiserP, VilleneuveAM, et al. (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123: 1037–1050.
28. DernburgAF, SedatJW, HawleyRS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86: 135–146.
29. KempB, BoumilRM, StewartMN, DawsonDS (2004) A role for centromere pairing in meiotic chromosome segregation. Genes Dev 18: 1946–1951.
30. HawleyRS, TheurkaufWE (1993) Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Gen 9: 310–317.
31. StewartMN, DawsonDS (2008) Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends Gen 24: 564–573.
32. BurgessSM, KlecknerN (1999) Collisions between yeast chromosomal loci in vivo are governed by three layers of organization. Genes Dev 13: 1871–1883.
33. BurgessSM, KlecknerN, WeinerBM (1999) Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev 13: 1627–1641.
34. DekkerJ, RippeK, DekkerM, KlecknerN (2002) Capturing chromosome conformation. Science 295: 1306–1311.
35. TsubouchiT, RoederGS (2005) A Synaptonemal Complex Protein Promotes Homology-Independent Centromere Coupling. Science 308: 870–873.
36. MolnarM, KlecknerN (2008) Examination of interchromosomal interactions in vegetatively growing diploid Schizosaccharomyces pombe cells by Cre/loxP site-specific recombination. Genetics 178: 99–112.
37. LorenzA, FuchsJ, BurgerR, LoidlJ (2003) Chromosome pairing does not contribute to nuclear architecture in vegetative yeast cells. Euk Cell 2: 856–866.
38. JinQW, FuchsJ, LoidlJ (2000) Centromere clustering is a major determinant of yeast interphase nuclear organization. J Cell Sci 113: 1903–1912.
39. MeaburnKJ, MisteliT, SoutoglouE (2007) Spatial genome organization in the formation of chromosomal translocations. Sem Cancer Biol 17: 80–90.
40. KleinF, MahrP, GalovaM, BuonomoSB, MichaelisC, et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91–103.
41. HollingsworthNM, GoetschL, ByersB (1990) The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61: 73–84.
42. SmithAV, RoederGS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136: 957–967.
43. BailisJM, RoederGS (1998) Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev 12: 3551–3563.
44. BlatY, ProtacioRU, HunterN, KlecknerN (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111: 791–802.
45. PanizzaS, MendozaMA, BerlingerM, HuangL, NicolasA, et al. (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146: 372–383.
46. ZicklerD, KlecknerN (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754.
47. NagDK, ScherthanH, RockmillB, BhargavaJ, RoederGS (1995) Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 141: 75–86.
48. LatypovV, RothenbergM, LorenzA, OctobreG, CsutakO, et al. (2010) Roles of Hop1 and Mek1 in meiotic chromosome pairing and recombination partner choice in Schizosaccharomyces pombe. Mol Cell Biol 30: 1570–1581.
49. BrarGA, HochwagenA, EeLS, AmonA (2009) The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol Biol Cell 20: 1030–1047.
50. CarballoJA, JohnsonAL, SedgwickSG, ChaRS (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132: 758–770.
51. KimKP, WeinerBM, ZhangL, JordanA, DekkerJ, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924–937.
52. GoldfarbT, LichtenM (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol 8: e1000520 doi:10.1371/journal.pbio.1000520.
53. Trelles-StickenE, AdelfalkC, LoidlJ, ScherthanH (2005) Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 170: 213–223.
54. LinW, JinH, LiuX, HamptonK, YuHG (2011) Scc2 regulates gene expression by recruiting cohesin to the chromosome as a transcriptional activator during yeast meiosis. Mol Biol Cell 22: 1985–1996.
55. ChaRS, WeinerBM, KeeneyS, DekkerJ, KlecknerN (2000) Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p. Genes Dev 14: 493–503.
56. BardhanA, ChuongH, DawsonDS (2010) Meiotic cohesin promotes pairing of nonhomologous centromeres in early meiotic prophase. Mol Biol Cell 21: 1799–1809.
57. BlatY, KlecknerN (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98: 249–259.
58. KugouK, FukudaT, YamadaS, ItoM, SasanumaH, et al. (2009) Rec8 guides canonical Spo11 distribution along yeast meiotic chromosomes. Mol Biol Cell 20: 3064–3076.
59. ZicklerD, KlecknerN (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32: 619–697.
60. KoszulR, KlecknerN (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19: 716–724.
61. StarrDA, FridolfssonHN (2010) Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26: 421–444.
62. KoszulR, KimKP, PrentissM, KlecknerN, KameokaS (2008) Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133: 1188–1201.
63. ConradMN, LeeCY, ChaoG, ShinoharaM, KosakaH, et al. (2008) Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133: 1175–1187.
64. BrownMS, ZandersS, AlaniE (2011) Sustained and rapid chromosome movements are critical for chromosome pairing and meiotic progression in budding yeast. Genetics 188: 21–32.
65. ScherthanH, WangH, AdelfalkC, WhiteEJ, CowanC, et al. (2007) Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci USA104: 16934–16939.
66. StarrDA (2009) A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 122: 577–586.
67. HiraokaY, DernburgAF (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17: 598–605.
68. ChuaPR, RoederGS (1997) Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11: 1786–1800.
69. ConradMN, DominguezAM, DresserME (1997) Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276: 1252–1255.
70. Trelles-StickenE, DresserME, ScherthanH (2000) Meiotic Telomere Protein Ndj1p Is Required for Meiosis-specific Telomere Distribution, Bouquet Formation and Efficient Homologue Pairing. J Cell Biol 151: 95–106.
71. ConradMN, LeeCY, WilkersonJL, DresserME (2007) MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 104: 8863–8868.
72. KosakaH, ShinoharaM, ShinoharaA (2008) Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet 4: e1000196 doi:10.1371/journal.pgen.1000196.
73. WanatJJ, KimKP, KoszulR, ZandersS, WeinerB, et al. (2008) Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet 4: e1000188 doi:10.1371/journal.pgen.1000188.
74. Peoples-HolstTL, BurgessSM (2005) Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast. Genes Dev 19: 863–874.
75. LuiDY, Peoples-HolstTL, MellJC, WuHY, DeanEW, et al. (2006) Analysis of close stable homolog juxtaposition during meiosis in mutants of Saccharomyces cerevisiae. Genetics 173: 1207–1222.
76. HochwagenA, AmonA (2006) Checking your breaks: surveillance mechanisms of meiotic recombination. Curr Biol 16: R217–228.
77. MellJC, WienholzBL, SalemA, BurgessSM (2008) Sites of recombination are local determinants of meiotic homolog pairing in Saccharomyces cerevisiae. Genetics 179: 773–784.
78. JessopL, RockmillB, RoederGS, LichtenM (2006) Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1. PLoS Genet 2: e155 doi:10.1371/journal.pgen.0020155.
79. OhSD, LaoJP, HwangPY, TaylorAF, SmithGR, et al. (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259–272.
80. ShinoharaM, Shita-YamaguchiE, BuersteddeJM, ShinagawaH, OgawaH, et al. (1997) Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. Genetics 147: 1545–1556.
81. KleinHL (1997) RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. Genetics 147: 1533–1543.
82. ShinoharaM, GasiorSL, BishopDK, ShinoharaA (2000) Tid1/Rdh54 promotes colocalization of Rad51 and Dmc1 during meiotic recombination. Proc Natl Acad Sci USA 97: 10814–10819.
83. BornerGV, KlecknerN, HunterN (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29–45.
84. TothA, RabitschKP, GalovaM, SchleifferA, BuonomoSB, et al. (2000) Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 103: 1155–1168.
85. BuhlerC, ShroffR, LichtenM (2009) Genome-wide mapping of meiotic DNA double-strand breaks in Saccharomyces cerevisiae. Methods Mol Biol 557: 143–164.
86. GlynnEF, MegeePC, YuHG, MistrotC, UnalE, et al. (2004) Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol 2: e259 doi:10.1371/journal.pbio.0020259.
87. BlitzblauHG, BellGW, RodriguezJ, BellSP, HochwagenA (2007) Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres. Curr Biol 17: 2003–2012.
88. HochwagenA, ThamWH, BrarGA, AmonA (2005) The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 122: 861–873.
89. Trelles-StickenE, LoidlJ, ScherthanH (1999) Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering. J Cell Sci 112(Pt 5): 651–658.
90. SpectorI, ShochetNR, BlasbergerD, KashmanY (1989) Latrunculins–novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil Cytoskeleton 13: 127–144.
91. MichaelisC, CioskR, NasmythK (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91: 35–45.
92. CioskR, ZachariaeW, MichaelisC, ShevchenkoA, MannM, et al. (1998) An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93: 1067–1076.
93. RabitschKP, TothA, GalovaM, SchleifferA, SchaffnerG, et al. (2001) A screen for genes required for meiosis and spore formation based on whole-genome expression. Curr Biol 11: 1001–1009.
94. KoszulR, KameokaS, WeinerBM (2009) Real-time imaging of meiotic chromosomes in Saccharomyces cerevisiae. Methods Mol Biol 558: 81–89.
95. HarperL, GolubovskayaI, CandeWZ (2004) A bouquet of chromosomes. J Cell Sci 117: 4025–4032.
96. ObesoD, DawsonDS (2010) Temporal characterization of homology-independent centromere coupling in meiotic prophase. PLoS ONE 5: e10336 doi:10.1371/journal.pone.0010336.
97. WynneDJ, RogO, CarltonPM, DernburgAF (2012) Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. The Journal of cell biology 196: 47–64.
98. PenknerA, TangL, NovatchkovaM, LadurnerM, FridkinA, et al. (2007) The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 12: 873–885.
99. YamamotoA, WestRR, McIntoshJR, HiraokaY (1999) A Cytoplasmic Dynein Heavy Chain Is Required for Oscillatory Nuclear Movement of Meiotic Prophase and Efficient Meiotic Recombination in Fission Yeast. J Cell Biol 145: 1233–1250.
100. SatoA, IsaacB, PhillipsCM, RilloR, CarltonPM, et al. (2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139: 907–919.
101. WynneDJ, RogO, CarltonPM, DernburgAF (2012) Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol 196: 47–64.
102. Sonntag BrownM, ZandersS, AlaniE (2011) Sustained and rapid chromosome movements are critical for chromosome pairing and meiotic progression in budding yeast. Genetics 188: 21–32.
103. LeeCY, ConradMN, DresserME (2012) Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 8: e1002730 doi:10.1371/journal.pgen.1002730.
104. CremerT, CremerM (2010) Chromosome territories. Cold Spring Harb Perspect Biol 2: a003889.
105. MarshallWF, StraightA, MarkoJF, SwedlowJ, DernburgA, et al. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol 7: 930–939.
106. DionV, ShimadaK, GasserSM (2010) Actin-related proteins in the nucleus: life beyond chromatin remodelers. Curr Opin Cell Biol
107. YoshidaT, ShimadaK, OmaY, KalckV, AkimuraK, et al. (2010) Actin-related protein Arp6 influences H2A.Z-dependent and -independent gene expression and links ribosomal protein genes to nuclear pores. PLoS Genet 6: e1000910 doi:10.1371/journal.pgen.1000910.
108. VisaN, PercipalleP (2010) Nuclear functions of actin. Cold Spring Harb Perspect Biol 2: a000620.
109. StephensAD, HaaseJ, VicciL, TaylorRM2nd, BloomK (2011) Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring. J Cell Biol 193: 1167–1180.
110. BloomK, JoglekarA (2010) Towards building a chromosome segregation machine. Nature 463: 446–456.
111. DingDQ, SakuraiN, KatouY, ItohT, ShirahigeK, et al. (2006) Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast. J Cell Biol 174: 499–508.
112. MolnarM, BahlerJ, SipiczkiM, KohliJ (1995) The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics 141: 61–73.
113. KaneSM, RothR (1974) Carbohydrate metabolism during ascospore development in yeast. J Bacteriol 118: 8–14.
114. WachA, BrachatA, PohlmannR, PhilippsenP (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793–1808.
115. GoldsteinLA, McCuskerHJ (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541–1553.
116. OhSD, LaoJP, TaylorAF, SmithGR, HunterN (2008) RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol Cell 31: 324–336.
117. LuiD, BurgessSM (2009) Measurement of spatial proximity and accessibility of chromosomal loci in Saccharomyces cerevisiae using Cre/loxP site-specific recombination. Methods Mol Biol 557: 55–63.
118. DresserME (2009) Time-lapse fluorescence microscopy of Saccharomyces cerevisiae in meiosis. Methods Mol Biol 558: 65–79.
119. HeunP, LarocheT, ShimadaK, FurrerP, GasserSM (2001) Chromosome dynamics in the yeast interphase nucleus. Science 294: 2181–2186.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Function and Regulation of , a Gene Implicated in Autism and Human Evolution
- Comprehensive Methylome Characterization of and at Single-Base Resolution
- Susceptibility Loci Associated with Specific and Shared Subtypes of Lymphoid Malignancies
- An Insertion in 5′ Flanking Region of Causes Blue Eggshell in the Chicken