Roles for nuclear organization in the maintenance of genome stability

Epigenomics

Volumn 2, Issue 2, 2010, Pages 289-305

  Nagai, Shigeki ^a   Heun, Patrick ^b   Gasser, Susan M ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

DNA damage; genome stability; nuclear organization; recombination

Indexed keywords

DOUBLE STRANDED DNA; RIBOSOME DNA;

CELL NUCLEUS; CHROMATIN; CHROMOSOME ANALYSIS; DNA DAMAGE; DNA REPAIR; GENE AMPLIFICATION; GENE CONTROL; GENE DELETION; GENE LOCUS; GENE STRUCTURE; GENE TRANSLOCATION; GENETIC RECOMBINATION; GENOMIC INSTABILITY; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEQUENCE HOMOLOGY; TELOMERE;

CELL NUCLEUS; CHROMATIN; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; GENOMIC INSTABILITY; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; NUCLEAR MATRIX; RECOMBINATION, GENETIC; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE;

EID: 77954124126     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.09.49     Document Type: Review

References (126)

1. Chubb JR, Boyle S, Perry P, Bickmore WA: Chromatin motion is constrained by association with nuclear compartments in human cells. Curr. Biol. 12, 439-445 (2002).
2. Vazquez J, Belmont AS, Sedat JW: Multiple regimes of constrained chromosome motion are regulated in the interphase Drosophila nucleus. Curr. Biol. 11, 1227-1239 (2001).
3. Heun P, Laroche T, Shimada K, Furrer P, Gasser SM: Chromosome dynamics in the yeast interphase nucleus. Science 294, 2181-2186 (2001).
4. Marshall WF, Straight A, Marko JF et al.: Interphase chromosomes undergo constrained diffusional motion in living cells. Curr. Biol. 7, 930-939 (1997).
5. Robinett CC, Straight A, Li G et al.: In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J. Cell Biol. 135, 1685-1700 (1996).
6. Maillet L, Boscheron C, Gotta M, Marcand S, Gilson E, Gasser SM: Evidence for silencing compartments within the yeast nucleus: a role for telomere proximity and Sir protein concentration in silencer-mediated repression. Genes Dev. 10, 1796-1811 (1996).
7. Gotta M, Laroche T, Formenton A, Maillet L, Scherthan H, Gasser SM: The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J. Cell Biol. 134, 1349-1363 (1996).
8. Andrulis ED, Neiman AM, Zappulla DC, Sternglanz R: Perinuclear localization of chromatin facilitates transcriptional silencing. Nature 394, 592-595 (1998).
9. Taddei A, Van Houwe G, Nagai S, Erb I, van Nimwegen E, Gasser SM: The functional importance of telomere clustering: global changes in gene expression result from SIR factor dispersion. Genome Res. 19, 611-625 (2009).
10. Lanctot C, Cheutin T, Cremer M, Cavalli G, Cremer T: Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat. Rev. Genet. 8, 104-115 (2007).
11. Reddy KL, Zullo JM, Bertolino E, Singh H: Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452, 243-247 (2008).
12. Kumaran RI, Spector DL: A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 180, 51-65 (2008).
13. Finlan LE, Sproul D, Thomson I et al.: Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet. 4, E1000039 (2008).
14. Guelen L, Pagie L, Brasset E et al.: Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951 (2008).
15. Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, van Steensel B: Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 38, 1005-1014 (2006). (Pubitemid 44325925)
16. Capell BC, Collins FS: Human laminopathies: nuclei gone genetically awry. Nat. Rev. Genet. 7, 940-952 (2006).
17. Goldman RD, Shumaker DK, Erdos MR et al.: Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 101, 8963-8968 (2004).
18. Shumaker DK, Dechat T, Kohlmaier A et al.: Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl Acad. Sci. USA 103, 8703-8708 (2006).
19. Taddei A, Van Houwe G, Hediger F et al.: Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441, 774-778 (2006).
20. Schmid M, Arib G, Laemmli C, Nishikawa J, Durussel T, Laemmli UK: Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol. Cell 21, 379-391 (2006).
21. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA: Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117, 427-439 (2004).
22. Mendjan S, Taipale M, Kind J et al.: Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol. Cell 21, 811-823 (2006).
23. Meister P, Taddei A, Ponti A, Baldacci G, Gasser SM: Replication foci dynamics: replication patterns are modulated by S-phase checkpoint kinases in fssion yeast. EMBO J. 26, 1315-1326 (2007).
24. Pasero P, Braguglia D, Gasser SM: ORC-dependent and origin-specifc initiation of DNA replication at defned foci in isolated yeast nuclei. Genes Dev. 11, 1504-1518 (1997).
25. Nakamura H, Morita T, Sato C: Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp. Cell Res. 165, 291-297 (1986).
26. Ma H, Samarabandu J, Devdhar RS et al.: Spatial and temporal dynamics of DNA replication sites in mammalian cells. J. Cell Biol. 143, 1415-1425 (1998).
27. Nakayasu H, Berezney R: Mapping replicational sites in the eucaryotic cell nucleus. J. Cell Biol. 108, 1-11 (1989).
28. Heun P, Laroche T, Raghuraman MK, Gasser SM: The positioning and dynamics of origins of replication in the budding yeast nucleus. J. Cell Biol. 152, 385-400 (2001).
29. Raghuraman MK, Brewer BJ, Fangman WL: Cell cycle-dependent establishment of a late replication program. Science 276, 806-809 (1997).
30. Cosgrove AJ, Nieduszynski CA, Donaldson AD: Ku complex controls the replication time of DNA in telomere regions. Genes Dev. 16, 2485-2490 (2002).
31. Ebrahimi H, Robertson ED, Taddei A, Gasser SM, Donaldson AD, Hiraga SI: Early initiation of a replication origin tethered at the nuclear periphery. J. Cell. Sci. (2010) (Epub ahead of print).
32. Hiratani I, Itoh TRM, Yokochi T et al.: Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6, E245 (2008).
33. Aparicio JG, Viggiani CJ, Gibson DG, Aparicio OM: The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 4769-4780 (2004).
34. Vogelauer M, Rubbi L, Lucas I, Brewer BJ, Grunstein M: Histone acetylation regulates the time of replication origin fring. Mol. Cell 10, 1223-1233 (2002).
35. Schubeler D, Scalzo D, Kooperberg C, van Steensel B, Delrow J, Groudine M: Genome-wide DNA replication profle for Drosophila melanogaster: a link between transcription and replication timing. Nat. Genet. 32, 438-442 (2002).
36. Knott S, Viggiani C, Tavaré S, Aparicio O: Genome-wide replication profles indicate an expansive role for Rpd3L in regulating replication initiation timing or effciency, and reveal genomic loci of Rpd3 function in Saccharomyces cerevisiae. Genes Dev. 23, 1077-1090 (2009).
37. Schwaiger M, Stadler MB, Bell O, Kohler H, Oakeley EJ, Schubeler D: Chromatin state marks cell-type-and gender-specifc replication of the Drosophila genome. Genes Dev. 23, 589-601 (2009).
38. Hoeijmakers JH: Genome maintenance mechanisms for preventing cancer. Nature 411, 366-374 (2001).
39. Symington LS: Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66, 630-670, table of contents (2002).
40. Aten JA, Stap J, Krawczyk PM et al.: Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303, 92-95 (2004).
41. Savage JR: Cancer. Proximity matters. Science 290, 62-63 (2000).
42. Nikiforova MN, Stringer JR, Blough R, Medvedovic M, Fagin JA, Nikiforov YE: Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290, 138-141 (2000).
43. Soutoglou E, Dorn JF, Sengupta K et al.: Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9, 675-682 (2007).
44. Gartenberg MR, Neumann FR, Laroche T, Blaszczyk M, Gasser SM: Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell 119, 955-967 (2004).
45. Haber JE, Leung WY: Lack of chromosome territoriality in yeast: promiscuous rejoining of broken chromosome ends. Proc. Natl Acad. Sci. USA 93, 13949-13954 (1996).
46. Aylon Y, Liefshitz B, Bitan-Banin G, Kupiec M: Molecular dissection of mitotic recombination in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 23, 1403-1417 (2003).
47. Nagai S, Dubrana K, Tsai-Pfugfelder M et al.: Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322, 597-602 (2008).
48. Houston PL, Broach JR: The dynamics of homologous pairing during mating type interconversion in budding yeast. PLoS Genet. 2, E98 (2006).
49. Melo JA, Cohen J, Toczyski DP: Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15, 2809-2821 (2001).
50. Lisby M, Rothstein R, Mortensen UH: Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl Acad. Sci. USA 98, 8276-8282 (2001).
51. Liu Y, Li M, Lee EY, Maizels N: Localization and dynamic relocalization of mammalian Rad52 during the cell cycle and in response to DNA damage. Curr. Biol. 9, 975-978 (1999).
52. Lisby M, Mortensen UH, Rothstein R: Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5, 572-577 (2003).
53. Bystricky K, van Attikum H, Montiel MD, Dion V, Gehlen L, Gasser SM: Regulation of nuclear positioning and dynamics of the silent mating type loci by the yeast Ku70/Ku80 complex. Mol. Cell. Biol. 29, 835-848 (2009).
54. Nelms BE, Maser RS, MacKay JF, Lagally MG, Petrini JH: In situ visualization of DNA double-strand break repair in human fbroblasts. Science 280, 590-592 (1998).
55. Lukas C, Falck J, Bartkova J, Bartek J, Lukas J: Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5, 255-260 (2003).
56. Kruhlak MJ, Celeste A, Dellaire G et al.: Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172, 823-834 (2006).
57. Cornforth MN, Greulich-Bode KM, Loucas BD et al.: Chromosomes are predominantly located randomly with respect to each other in interphase human cells. J. Cell Biol. 159, 237-244 (2002).
58. Dimitrova N, Chen YC, Spector DL, de Lange T: 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528 (2008).
59. Celli GB, Denchi EL, de Lange T: Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol. 8, 885-890 (2006).
60. Celli GB, de Lange T: DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7, 712-718 (2005).
61. Barzel A, Kupiec M: Finding a match: how do homologous sequences get together for recombination? Nat. Rev. Genet. 9, 27-37 (2008).
62. Wilson JH, Leung WY, Bosco G, Dieu D, Haber JE: The frequency of gene targeting in yeast depends on the number of target copies. Proc. Natl Acad. Sci. USA 91, 177-181 (1994).
63. Chai B, Huang J, Cairns B, Laurent B: Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19, 1656-1661 (2005).
64. van Attikum H, Fritsch O, Hohn B, Gasser SM: Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119, 777-788 (2004).
65. Morrison AJ, Highland J, Krogan NJ et al.: INO80 and g-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119, 767-775 (2004).
66. Downs JA, Nussenzweig MC, Nussenzweig A: Chromatin dynamics and the preservation of genetic information. Nature 447, 951-958 (2007).
67. van Attikum H, Fritsch O, Gasser SM: Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26, 4113-4125 (2007).
68. Tsukuda T, Fleming A, Nickoloff J, Osley M: Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438, 379-383 (2005).
69. Shen X, Mizuguchi G, Hamiche A, Wu C: A chromatin remodelling complex involved in transcription and DNA processing. Nature 406, 541-544 (2000).
70. Langowski J, Heermann DW: Computational modeling of the chromatin fber. Semin. Cell Dev. Biol. 18, 659-667 (2007).
71. Fung JC, Marshall WF, Dernburg A, Agard DA, Sedat JW: Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J. Cell Biol. 141, 5-20 (1998).
72. Metz CW: Chromosome studies on the Diptera II: the paired association of chromosomes in the Diptera, and its signifcance. J. Exp. Zool. 21, 213-279 (1916).
73. Rong YS, Golic KG: The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 165, 1831-1842 (2003).
74. Lorenz A, Fuchs J, Burger R, Loidl J: Chromosome pairing does not contribute to nuclear architecture in vegetative yeast cells. Eukaryot. Cell 2, 856-866 (2003).
75. Cremer M, von Hase J, Volm T et al.: Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Res. 9, 541-567 (2001).
76. Rabl C: Über Zellteilung. Gegenbaurs Morphol. Jahrb. 10, 214-330 (1885).
77. Mathog D, Hochstrasser M, Gruenbaum Y, Saumweber H, Sedat J: Characteristic folding pattern of polytene chromosomes in Drosophila salivary gland nuclei. Nature 308, 414-421 (1984).
78. Schober H, Kalck V, Vega-Palas MA et al.: Controlled exchange of chromosomal arms reveals principles driving telomere interactions in yeast. Genome Res. 18, 261-271 (2008).
79. Jin Q, Trelles-Sticken E, Scherthan H, Loidl J: Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J. Cell Biol. 141, 21-29 (1998).
80. Bystricky K, Laroche T, van Houwe G, Blaszczyk M, Gasser SM: Chromosome looping in yeast: telomere pairing and coordinated movement refect anchoring effciency and territorial organization. J. Cell Biol. 168, 375-387 (2005).
81. Zickler D: From early homolog recognition to synaptonemal complex formation. Chromosoma 115, 158-174 (2006).
82. Funabiki H, Hagan I, Uzawa S, Yanagida M: Cell cycle-dependent specifc positioning and clustering of centromeres and telomeres in fssion yeast. J. Cell Biol. 121, 961-976 (1993).
83. Haaf T, Schmid M: Chromosome topology in mammalian interphase nuclei. Exp. Cell Res. 192, 325-332 (1991).
84. Palladino F, Laroche T, Gilson E, Axelrod A, Pillus L, Gasser SM: SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres. Cell 75, 543-555 (1993).
85. Marvin M, Griffn C, Eyre D, Barton D, Louis E: Saccharomyces cerevisiae, yKu and subtelomeric core X sequences repress homologous recombination near telomeres as part of the same pathway. Genetics 183, 441-451 (2009).
86. Marvin M, Becker M, Noel P, Hardy S, Bertuch A, Louis E: The association of yKu with subtelomeric core X sequences prevents recombination involving telomeric sequences Genetics 183, 453-467 (2009).
87. Osborne CS, Chakalova L, Brown KE et al.: Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 36, 1065-1071 (2004).
88. Osborne CS, Chakalova L, Mitchell JA et al.: Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol. 5, E192 (2007).
89. Taddei A, Hediger F, Neumann FR, Bauer C, Gasser SM: Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO J. 23, 1301-1312 (2004).
90. Andrulis ED, Zappulla DC, Ansari A et al.: Esc1, a nuclear periphery protein required for Sir4-based plasmid anchoring and partitioning. Mol. Cell. Biol. 22, 8292-8301 (2002).
91. Brickner JH, Walter P: Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2, E342 (2004).
92. Capelson M, Corces VG: The ubiquitin ligase dTopors directs the nuclear organization of a chromatin insulator. Mol. Cell 20, 105-116 (2005).
93. Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G: CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 13, 291-298 (2004).
94. Saijo M, Hirai T, Ogawa A, Kobayashi A, Kamiuchi S, Tanaka K: Functional TFIIH is required for UV-induced translocation of CSA to the nuclear matrix. Mol. Cell. Biol. 27, 2538-2547 (2007).
95. Mladenov E, Anachkova B, Tsaneva I: Sub-nuclear localization of Rad51 in response to DNA damage. Genes Cells 11, 513-524 (2006).
96. Perry JJ, Tainer JA, Boddy MN: A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem. Sci. 33, 201-208 (2008).
97. Oza P, Jaspersen SL, Miele A, Dekker J, Peterson CL: Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev. 23, 912-927 (2009).
98. Kalocsay M, Hiller NJ, Jentsch S: Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fxation in response to a persistent DNA double-strand break. Mol. Cell 33, 335-343 (2009).
99. Schober H, Ferreira H, Kalck V, Gehlen LR, Gasser SM: Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev. 23, 928-938 (2009).
100. Potts PR, Yu H: The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol. 14, 581-590 (2007).
101. Yeager TR, Neumann AA, Englezou A, Huschtscha LI, Noble JR, Reddel RR: Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59, 4175-4179 (1999).
102. McEachern MJ, Krauskopf A, Blackburn EH: Telomeres and their control. Annu. Rev. Genet. 34, 331-358 (2000).
103. Weisshaar SR, Keusekotten K, Krause A et al.: Arsenic trioxide stimulates SUMO-2/3 modifcation leading to RNF4-dependent proteolytic targeting of PML. FEBS Lett. 582, 3174-3178 (2008).
104. Tatham MH, Geoffroy MC, Shen L et al.: RNF4 is a poly-SUMO-specifc E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538-546 (2008).
105. Lallemand-Breitenbach V, Jeanne M, Benhenda S et al.: Arsenic degrades PML or PML-RARa through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10, 547-555 (2008).
106. Bernardi R, Pandolf PP: Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 8, 1006-1016 (2007).
107. Azam M, Lee JY, Abraham V, Chanoux R, Schoenly KA, Johnson FB: Evidence that the S. cerevisiae Sgs1 protein facilitates recombinational repair of telomeres during senescence. Nucleic Acids Res. 34, 506-516 (2006).
108. McEachern MJ, Haber JE: Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75, 111-135 (2006).
109. Khadaroo B, Teixeira MT, Luciano P et al.: The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat. Cell Biol. 11, 980-987 (2009).
110. Abdallah P, Luciano P, Runge KW et al.: A two-step model for senescence triggered by a single critically short telomere. Nat. Cell Biol. 11, 988-993 (2009).
111. Garvik B, Carson M, Hartwell L: Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specifc signal for the RAD9 checkpoint. Mol. Cell. Biol. 15, 6128-6138 (1995).
112. Collins SR, Miller KM, Maas NL et al.: Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446, 806-810 (2007).
113. Petes TD: Yeast ribosomal DNA genes are located on chromosome XII. Proc. Natl Acad. Sci. USA 76(1), 410-414 (1979).
114. Sinclair DA, Guarente L: Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91, 1033-1042 (1997).
115. Smith GP: Unequal crossover and the evolution of multigene families. Cold Spring Harb. Symp. Quant. Biol. 38, 507-513 (1974).
116. Kobayashi T, Heck DJ, Nomura M, Horiuchi T: Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev. 12, 3821-3830 (1998).
117. Keil RL, Roeder GS: Cis-acting, recombination-stimulating activity in a fragment of the ribosomal DNA of S. cerevisiae. Cell 39, 377-386 (1984).
118. Petes TD: Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell 19, 765-774 (1980).
119. Torres-Rosell J, Sunjevaric I, De Piccoli G et al.: The Smc5-Smc6 complex and SUMO modifcation of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9, 923-931 (2007).
120. Oakes M, Aris JP, Brockenbrough JS, Wai H, Vu L, Nomura M: Mutational ana lysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae. J. Cell Biol 143, 23-34 (1998).
121. Mekhail K, Seebacher J, Gygi SP, Moazed D: Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456, 667-670 (2008).
122. King MC, Lusk CP, Blobel G: Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442, 1003-1007 (2006).
123. Gottlieb S, Esposito RE: A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56, 771-776 (1989).
124. Laroche T, Martin SG, Gotta M et al.: Mutation of yeast Ku genes disrupts the subnuclear organization of telomeres. Curr. Biol. 8, 653-656 (1998).
125. Zaidi SK, Young DW, Javed A et al.: Nuclear microenvironments in biological control and cancer. Nat. Rev. Cancer 7, 454-463 (2007).
126. Maeshima K, Janssen S, Laemmli U: Specifc targeting of insect and vertebrate telomeres with pyrrole and imidazole polyamides. EMBO J. 20, 3218-3228 (2001).