Nucleolar Organization, ribosomal DNA array stability, and acrocentric chromosome integrity are linked to telomere function

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Stimpson, Kaitlin M ^a,b   Sullivan, Lori L ^a   Kuo, Molly E ^b   Sullivan, Beth A ^a,b,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; NUCLEIC ACID BINDING PROTEIN; RIBOSOME DNA; TELOMERIC REPEAT BINDING FACTOR 2; UNCLASSIFIED DRUG; UPSTREAM BINDING FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UBF;

ACROCENTRIC CHROMOSOME; ARTICLE; CHROMOSOMAL INSTABILITY; CHROMOSOME NOR; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; DNA MICROARRAY; DNA STRUCTURE; GENETIC STABILITY; HUMAN; HUMAN CELL; NUCLEOLUS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA BINDING; RNA TRANSCRIPTION; ROBERTSONIAN CHROMOSOME TRANSLOCATION; TELOMERE; CELL LINE; DNA REPAIR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

CELL LINE; CHROMOSOMAL INSTABILITY; DNA DAMAGE; DNA REPAIR; DNA, RIBOSOMAL; GENE EXPRESSION REGULATION; HUMANS; NUCLEOLUS ORGANIZER REGION; POL1 TRANSCRIPTION INITIATION COMPLEX PROTEINS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 84899745181     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092432     Document Type: Article

References (60)

1. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, et al. (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198. (Pubitemid 37442589)
2. O'Sullivan RJ, Karlseder J (2010) Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol 11: 171-181.
3. Broccoli D, Smogorzewska A, Chong L, de Lange T (1997) Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet 17: 231-235.
4. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, et al. (1999) Mammalian telomeres end in a large duplex loop. Cell 97: 503-514. (Pubitemid 29231173)
5. Stansel RM, de Lange T, Griffith JD (2001) T-loop assembly in vitro involves binding of TRF2 near the 39 telomeric overhang. EMBO J 20: 5532-5540. (Pubitemid 32959473)
6. Denchi EL, de Lange T (2007) Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448: 1068-1071. (Pubitemid 47345583)
7. Karlseder J, Hoke K, Mirzoeva OK, Bakkenist C, Kastan MB, et al. (2004) The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLOS Biol 2: E240.
8. Smogorzewska A, Karlseder J, Holtgreve-Grez H, Jauch A, de Lange T (2002) DNA ligase IV-dependent NHEJ of deprotected mammalian telomeres in G1 and G2. Curr Biol 12: 1635-1644. (Pubitemid 35161916)
9. Stimpson KM, Song IY, Jauch A, Holtgreve-Grez H, Hayden KE, et al. (2010) Telomere disruption results in non-random formation of de novo dicentric chromosomes involving acrocentric human chromosomes. PLOS Genet 6: e1001061.
10. van Steensel B, Smogorzewska A, de Lange T (1998) TRF2 protects human telomeres from end-to-end fusions. Cell 92: 401-413. (Pubitemid 28093017)
11. Hamerton JL, Canning N, Ray M, Smith S (1975) A cytogenetic survey of 14,069 newborn infants. I. Incidence of chromosome abnormalities. Clin Genet 8: 223-243.
12. Greig GM, Willard HF (1992) Beta satellite DNA: characterization and localization of two subfamilies from the distal and proximal short arms of the human acrocentric chromosomes. Genomics 12: 573-580.
13. Trowell HE, Nagy A, Vissel B, Choo KH (1993) Long-range analyses of the centromeric regions of human chromosomes 13, 14 and 21: identification of a narrow domain containing two key centromeric DNA elements. Hum Mol Genet 2: 1639-1649. (Pubitemid 23358683)
14. Henderson AS, Warburton D, Atwood KC (1972) Location of ribosomal DNA in the human chromosome complement. Proc Natl Acad Sci U S A 69: 3394-3398.
15. Bross K, Krone W (1973) Ribosomal cistrons and acrocentric chromosomes in man. Humangenetik 18: 71-75.
16. Spadari S, Di Lernia R, Simoni G, Pedrali-Noy G, De Carli L (1973) Localization of ribosomal RNA genes on human acrocentric chromosomes. Mol Gen Genet 127: 57-67.
17. Benavente R, Rose KM, Reimer G, Hugle-Dorr B, Scheer U (1987) Inhibition of nucleolar reformation after microinjection of antibodies to RNA polymerase into mitotic cells. J Cell Biol 105: 1483-1491. (Pubitemid 18023375)
18. Jimenez-Garcia LF, Segura-Valdez ML, Ochs RL, Rothblum LI, Hannan R, et al. (1994) Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell 5: 955-966. (Pubitemid 24310584)
19. Ochs RL, Lischwe MA, Shen E, Carroll RE, Busch H (1985) Nucleogenesis: composition and fate of prenucleolar bodies. Chromosoma 92: 330-6. (Pubitemid 16246186)
20. Anastassova-Kristeva M (1977) The nucleolar cycle in man. J Cell Sci 25: 103-110.
21. Bridger JM, Kill IR, Lichter P (1998) Association of pKi-67 with satellite DNA of the human genome in early G1 cells. Chromosome Res 6: 13-24. (Pubitemid 28065824)
22. Krystosek A (1998) Repositioning of human interphase chromosomes by nucleolar dynamics in the reverse transformation of HT1080 fibrosarcoma cells. Exp Cell Res 241: 202-209.
23. Bell P, Mais C, McStay B, Scheer U (1997) Association of the nucleolar transcription factor UBF with the transcriptionally inactive rRNA genes of pronuclei and early Xenopus embryos. J Cell Sci 110: 2053-2063. (Pubitemid 27440429)
24. Mais C, Wright JE, Prieto JL, Raggett SL, McStay B (2005) UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev 19: 50-64. (Pubitemid 40095816)
25. Zatsepina OV, Voit R, Grummt I, Spring H, Semenov MV, et al. (1993) The RNA polymerase I-specific transcription initiation factor UBF is associated with transcriptionally active and inactive ribosomal genes. Chromosoma 102: 599-611. (Pubitemid 23343646)
26. Ahmad Y, Boisvert FM, Gregor P, Cobley A, Lamond AI (2009) NOPdb: Nucleolar Proteome Database - 2008 update. Nucleic Acids Res 37: D181-184.
27. Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI (2010) The nucleolus under stress. Mol Cell 40: 216-227.
28. Busch H, Muramatsu M, Adams H, Steele WJ, Llau MC, et al. (1963) Isolation of Nucleoli. Exp Cell Res 24: 150-163.
29. Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, et al. (2002) Directed proteomic analysis of the human nucleolus. Curr Biol 12: 1-11.
30. Sullivan BA, Schwartz S (1995) Identification of centromeric antigens in dicentric Robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Hum Mol Genet 4: 2189-2197.
31. Waye JS, Willard HF (1989) Human beta satellite DNA: genomic organization and sequence definition of a class of highly repetitive tandem DNA. Proc Natl Acad Sci USA 86: 6250-6254. (Pubitemid 19210631)
32. Pondarre C, Strumberg D, Fujimoi A, Torres-Leon R, Pommier Y (1997) In vivo sequencing of camptothecin-induced topoisomerase I cleavage sites in human colon carcinoma cells. Nucleic Acids Res 25: 4111-4116. (Pubitemid 27443343)
33. Shiels C, Coutelle C, Huxley C (1997) Analysis of ribosomal and alphoid repetitive DNA by fiber-FISH. Cytogenet Cell Genet 76: 20-22. (Pubitemid 27183230)
34. Warburton PE, Greig GM, Haaf T, Willard HF (1991) PCR amplification of chromosome-specific alpha satellite DNA: definition of centromeric STS markers and polymorphic analysis. Genomics 11: 324-333.
35. Choo KH, Earle E, Vissel B, Kalitsis P (1992) A chromosome 14-specific human satellite III DNA subfamily that shows variable presence on different chromosomes 14. Am J Hum Genet 50: 706-716.
36. de Planell-Saguer M, Rodicio MC, Mourelatos Z (2010) Rapid in situ codetection of noncoding RNAs and proteins in cells and formalin-fixed paraffin-embedded tissue sections without protease treatment. Nat Protoc 5: 1061-1073.
37. Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, et al. (2005) c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat Cell Biol 7: 311-318. (Pubitemid 40331133)
38. Csonka E, Cserpan I, Fodor K, Hollo G, Katona R, et al. (2000) Novel generation of human satellite DNA-based artificial chromosomes in mammalian cells. J Cell Sci 113: 3207-3216.
39. Weier HU, Lucas JN, Poggensee M, Segraves R, Pinkel D, et al. (1991) Two-color hybridization with high complexity chromosome-specific probes and a degenerate alpha satellite probe DNA allows unambiguous discrimination between symmetrical and asymmetrical translocations. Chromosoma 100: 371-376.
40. Mravinac B, Sullivan LL, Reeves JW, Yan CM, Kopf KS, et al. (2009) Histone modifications within the human X centromere region. PLOS ONE 4: e6602.
41. Amato A, Schillaci T, Lentini L, Di Leonardo A (2009) CENPA overexpression promotes genome instability in pRb-depleted human cells. Mol Cancer 8: 119.
42. Philimonenko VV, Zhao J, Iben S, Dingova H, Kysela K, et al. (2004) Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol 6: 1165-1172. (Pubitemid 39625114)
43. Davoli T, Denchi EL, de Lange T (2010) Persistent telomere damage induces bypass of mitosis and tetraploidy. Cell 141: 81-93.
44. Samoshkin A, Dulev S, Loukinov D, Rosenfeld JA, Strunnikov AV (2012) Condensin dysfunction in human cells induces nonrandom chromosomal breaks in anaphase, with distinct patterns for both unique and repeated genomic regions. Chromosoma 121: 191-199.
45. Emmott E, Hiscox JA (2009) Nucleolar targeting: the hub of the matter. EMBO Rep 10: 231-238.
46. Zhang S, Hemmerich P, Grosse F (2004) Nucleolar localization of the human telomeric repeat binding factor 2 (TRF2). J Cell Sci 117: 3935-3945. (Pubitemid 39207330)
47. Tsai RY (2009) Nucleolar modulation of TRF1: a dynamic way to regulate telomere and cell cycle by nucleostemin and GNL3L. Cell Cycle 8: 2912-2916.
48. Marciniak RA, Lombard DB, Johnson FB, Guarente L (1998) Nucleolar localization of the Werner syndrome protein in human cells. Proc Natl Acad Sci USA 95: 6887-6892. (Pubitemid 28278076)
49. Heiss NS, Knight SW, Vulliamy TJ, Klauck SM, Wiemann S, et al. (1998) X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat Genet 19: 32-38. (Pubitemid 28242019)
50. Yankiwski V, Marciniak RA, Guarente L, Neff NF (2000) Nuclear structure in normal and Bloom syndrome cells. Proc Natl Acad Sci USA 97: 5214-5219. (Pubitemid 30313698)
51. Bradshaw PS, Stavropoulos DJ, Meyn MS (2005) Human telomeric protein TRF2 associates with genomic double-strand breaks as an early response to DNA damage. Nat Genet 37: 193-197.
52. Fouche N, Cesare AJ, Willcox S, Ozgur S, Compton SA, et al. (2006) The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J Biol Chem 281: 37486-37495. (Pubitemid 46042052)
53. Simonet T, Zaragosi LE, Philippe C, Lebrigand K, Schouteden C, et al. (2011) The human TTAGGG repeat factors 1 and 2 bind to a subset of interstitial telomeric sequences and satellite repeats. Cell Res 21: 1028-1038.
54. Yang D, Xiong Y, Kim H, He Q, Li Y, et al. (2011) Human telomeric proteins occupy selective interstitial sites. Cell Res 21: 1013-1027.
55. Moore HM, Bai B, Boisvert FM, Latonen L, Rantanen V, et al. (2011) Quantitative proteomics and dynamic imaging of the nucleolus reveal distinct responses to UV and ionizing radiation. Mol Cell Proteomics 10: M111 009241.
56. Haaf T, Ward DC (1996) Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains. Exp Cell Res 224: 163-173. (Pubitemid 26117635)
57. Heliot L, Kaplan H, Lucas L, Klein C, Beorchia A, et al. (1997) Electron tomography of metaphase nucleolar organizer regions: evidence for a twisted-loop organization. Mol Biol Cell 8: 2199-2216. (Pubitemid 27469382)
58. Tsang CK, Li H, Zheng XS (2007) Nutrient starvation promotes condensin loading to maintain rDNA stability. EMBO J 26: 448-458. (Pubitemid 46160945)
59. Freeman L, Aragon-Alcaide L, Strunnikov A (2000) The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J Cell Biol 149: 811-824. (Pubitemid 30327234)
60. Sanij E, Hannan RD (2009) The role of UBF in regulating the structure and dynamics of transcriptionally active rDNA chromatin. Epigenetics 4: 374-382.