, A -Acting Locus that Controls Chromosome-Wide Replication Timing and Stability of Human Chromosome 15


Mammalian cells replicate their DNA along each chromosome during a precise temporal replication program. In this report, we used a novel “chromosome-engineering” strategy to identify a DNA element that controls this replication-timing program of human chromosome 15. Characterization of this element indicated that it encodes large non-protein-coding RNAs that are retained in the nucleus and form a “cloud” on one copy of chromosome 15. Previously, we found that structural rearrangements of a similar element on human chromosome 6 causes delayed replication and structural instability of chromosome 6. Mammalian chromosomes are known to contain three distinct types of essential DNA elements that promote proper chromosome function. Thus, every chromosome contains: 1) origins of replication, which are responsible for proper initiation of DNA synthesis; 2) centromeres, which are responsible for proper chromosome separation during cell division; and 3) telomeres, which are responsible for replication and protection of the ends of linear chromosomes. Our work supports a model in which all mammalian chromosomes contain a fourth type of essential DNA element, the “inactivation/stability center”, which is responsible for proper DNA replication timing and structural stability of each chromosome.


Vyšlo v časopise: , A -Acting Locus that Controls Chromosome-Wide Replication Timing and Stability of Human Chromosome 15. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004923
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004923

Souhrn

Mammalian cells replicate their DNA along each chromosome during a precise temporal replication program. In this report, we used a novel “chromosome-engineering” strategy to identify a DNA element that controls this replication-timing program of human chromosome 15. Characterization of this element indicated that it encodes large non-protein-coding RNAs that are retained in the nucleus and form a “cloud” on one copy of chromosome 15. Previously, we found that structural rearrangements of a similar element on human chromosome 6 causes delayed replication and structural instability of chromosome 6. Mammalian chromosomes are known to contain three distinct types of essential DNA elements that promote proper chromosome function. Thus, every chromosome contains: 1) origins of replication, which are responsible for proper initiation of DNA synthesis; 2) centromeres, which are responsible for proper chromosome separation during cell division; and 3) telomeres, which are responsible for replication and protection of the ends of linear chromosomes. Our work supports a model in which all mammalian chromosomes contain a fourth type of essential DNA element, the “inactivation/stability center”, which is responsible for proper DNA replication timing and structural stability of each chromosome.


Zdroje

1. ThayerMJ (2012) Mammalian chromosomes contain cis-acting elements that control replication timing, mitotic condensation, and stability of entire chromosomes. Bioessays 34: 760–770.

2. NicholsWW, ALevan, PAula, ENorrby (1964) Extreme chromosome breakage induced by measles virus in different in vitro systems. Hereditas 51: 380.

3. NicholsWW, ALevan, PAula, ENorrby (1965) Chromosome damage associated with measles virus in vitro. Hereditas 54: 101.

4. JohnsonRT, RaoPN (1970) Mammalian cell fusion: induction of premature chromosome condensation in interphase nuclei. Nature 226: 717–722.

5. SperlingK, RaoPN (1974) The phenomenon of premature chromosome condensation: its relevance to basic and applied research. Humangenetik 23: 235–258.

6. KatoH, SandbergAA (1968) Chromosome pulverization in chinese hamster cells induced by Sendai virus. J Natl Cancer Inst 41: 1117–1123.

7. SmithL, PlugA, ThayerM (2001) Delayed Replication Timing Leads to Delayed Mitotic Chromosome Condensation and Chromosomal Instability of Chromosome Translocations. Proc Natl Acad Sci U S A 98: 13300–13305.

8. zur HausenH (1967) Chromosomal changes of similar nature in seven established cell lines derived from the peripheral blood of patients with leukemia. J Natl Cancer Inst 38: 683–696.

9. Stubblefield E (1964) DNA Synthesis and Chromosomal Morphology of Chinese Hamster Cells Cultured in Media Containing N-deacetyl-N-methylcolchicine (Colcemid). In: Harris RJC, editor. Cytogenetics of Cells in Culture. New York, New York: Academic Press. pp.223–248.

10. KatoH, SandbergAA (1967) Chromosome pulverization in human binucleate cells following colcemid treatment. J Cell Biol 34: 35–45.

11. CrastaK, GanemNJ, DagherR, LantermannAB, IvanovaEV, et al. (2012) DNA breaks and chromosome pulverization from errors in mitosis. Nature 482: 53–58.

12. IkeuchiT, WeinfeldH, SandbergAA (1972) Chromosome pulverization in micronuclei induced by tritiated thymidine. J Cell Biol 52: 97–104.

13. KuhnEM, ThermanE, BuchlerDA (1987) Do individual allocyclic chromosomes in metaphase reflect their interphase domains? Hum Genet 77: 210–213.

14. OttoPG, OttoPA, ThermanE (1981) The behavior of allocyclic chromosomes in Bloom's syndrome. Chromosoma 84: 337–344.

15. BregerKS, SmithL, TurkerMS, ThayerMJ (2004) Ionizing radiation induces frequent translocations with delayed replication and condensation. Cancer Research 64: 8231–8238.

16. ChangBH, SmithL, HuangJ, ThayerM (2007) Chromosomes with delayed replication timing lead to checkpoint activation, delayed recruitment of Aurora B and chromosome instability. Oncogene 26: 1852–1861.

17. BregerKS, SmithL, ThayerMJ (2005) Engineering translocations with delayed replication: evidence for cis control of chromosome replication timing. Hum Mol Genet 14: 2813–2827.

18. DonleyN, StoffregenEP, SmithL, MontagnaC, ThayerMJ (2013) Asynchronous Replication, Mono-Allelic Expression, and Long Range Cis-Effects of ASAR6. PLoS Genet 9: e1003423.

19. StoffregenEP, DonleyN, StaufferD, SmithL, ThayerMJ (2011) An autosomal locus that controls chromosome-wide replication timing and mono-allelic expression. Hum Mol Genet 20: 2366–2378.

20. BrandaCS, DymeckiSM (2004) Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. Dev Cell 6: 7–28.

21. MillsAA, BradleyA (2001) From mouse to man: generating megabase chromosome rearrangements. Trends Genet 17: 331–339.

22. HarkeyMA, KaulR, JacobsMA, KurreP, BoveeD, et al. (2007) Multiarm high-throughput integration site detection: limitations of LAM-PCR technology and optimization for clonal analysis. Stem Cells Dev 16: 381–392.

23. SmithL, ThayerM (2012) Chromosome replicating timing combined with fluorescent in situ hybridization. J Vis Exp 10: e4400.

24. Diaz-PerezSV, FergusonDO, WangC, CsankovszkiG, TsaiSC, et al. (2006) A deletion at the mouse Xist gene exposes trans-effects that alter the heterochromatin of the inactive X chromosome and the replication time and DNA stability of both X chromosomes. Genetics 174: 1115–1133.

25. MeihlacM, KedingerC, ChambonP, FaulstichH, GovindanMV, et al. (1970) Amanitin binding to calf thymus RNA polymerase B. FEBS Lett. 9: 258–260.

26. GoldmitM, BergmanY (2004) Monoallelic gene expression: a repertoire of recurrent themes. Immunol Rev 200: 197–214.

27. SeligS, OkumuraK, WardDC, CedarH (1992) Delineation of DNA replication time zones by fluorescence in situ hybridization. EMBO J 11: 1217–1225.

28. AzuaraV, BrownKE, WilliamsRR, WebbN, DillonN, et al. (2003) Heritable gene silencing in lymphocytes delays chromatid resolution without affecting the timing of DNA replication. Nat Cell Biol 5: 668–674.

29. MostoslavskyR, SinghN, TenzenT, GoldmitM, GabayC, et al. (2001) Asynchronous replication and allelic exclusion in the immune system. Nature 414: 221–225.

30. EnsmingerAW, ChessA (2004) Coordinated replication timing of monoallelically expressed genes along human autosomes. Hum Mol Genet 13: 651–658.

31. SinghN, EbrahimiFA, GimelbrantAA, EnsmingerAW, TackettMR, et al. (2003) Coordination of the random asynchronous replication of autosomal loci. Nat Genet 33: 339–341.

32. LuediPP, DietrichFS, WeidmanJR, BoskoJM, JirtleRL, et al. (2007) Computational and experimental identification of novel human imprinted genes. Genome Res 17: 1723–1730.

33. GimelbrantA, HutchinsonJN, ThompsonBR, ChessA (2007) Widespread monoallelic expression on human autosomes. Science 318: 1136–1140.

34. SchlesingerS, SeligS, BergmanY, CedarH (2009) Allelic inactivation of rDNA loci. Genes Dev 23: 2437–2447.

35. GoodwinE, MeyneJ (1993) Strand-specific FISH reveals orientation of chromosome 18 alphoid DNA. Cytogenet Cell Genet 63: 126–127.

36. Rhind N, Gilbert DM (2013) DNA replication timing. Cold Spring Harb Perspect Biol 5.

37. RybaT, HirataniI, LuJ, ItohM, KulikM, et al. (2010) Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 20: 761–770.

38. YaffeE, Farkash-AmarS, PoltenA, YakhiniZ, TanayA, et al. (2010) Comparative analysis of DNA replication timing reveals conserved large-scale chromosomal architecture. PLoS Genet 6: e1001011.

39. DeS, MichorF (2011) DNA replication timing and long-range DNA interactions predict mutational landscapes of cancer genomes. Nat Biotechnol 29: 1103–1108.

40. GilbertDM, TakebayashiSI, RybaT, LuJ, PopeBD, et al. (2011) Space and time in the nucleus: developmental control of replication timing and chromosome architecture. Cold Spring Harb Symp Quant Biol 75: 143–153.

41. AparicioOM (2013) Location, location, location: it's all in the timing for replication origins. Genes Dev 27: 117–128.

42. PopeBD, HirataniI, GilbertDM (2010) Domain-wide regulation of DNA replication timing during mammalian development. Chromosome Res 18: 127–136.

43. BartolomeiMS (2009) Genomic imprinting: employing and avoiding epigenetic processes. Genes Dev 23: 2124–2133.

44. ChessA (2012) Mechanisms and consequences of widespread random monoallelic expression. Nat Rev Genet 13: 421–428.

45. AuguiS, NoraEP, HeardE (2011) Regulation of X-chromosome inactivation by the X-inactivation centre. Nat Rev Genet 12: 429–442.

46. KruegerC, MorisonIM (2008) Random monoallelic expression: making a choice. Trends Genet 24: 257–259.

47. ZakharovaIS, ShevchenkoAI, ZakianSM (2009) Monoallelic gene expression in mammals. Chromosoma 118: 279–290.

48. ZwemerLM, ZakA, ThompsonBR, KirbyA, DalyMJ, et al. (2012) Autosomal monoallelic expression in the mouse. Genome Biol 13: R10.

49. LiSM, ValoZ, WangJ, GaoH, BowersCW, et al. (2012) Transcriptome-wide survey of mouse CNS-derived cells reveals monoallelic expression within novel gene families. PLoS One 7: e31751.

50. AlexanderMK, Mlynarczyk-EvansS, Royce-TollandM, PlocikA, KalantryS, et al. (2007) Differences between homologous alleles of olfactory receptor genes require the Polycomb Group protein Eed. J Cell Biol 179: 269–276.

51. LyonMF (2003) The Lyon and the LINE hypothesis. Semin Cell Dev Biol 14: 313–318.

52. KambereMB, LaneRP (2009) Exceptional LINE density at V1R loci: the Lyon repeat hypothesis revisited on autosomes. J Mol Evol 68: 145–159.

53. AllenE, HorvathS, TongF, KraftP, SpiteriE, et al. (2003) High concentrations of long interspersed nuclear element sequence distinguish monoallelically expressed genes. Proc Natl Acad Sci U S A 100: 9940–9945.

54. HallLL, CaroneDM, GomezAV, KolpaHJ, ByronM, et al. (2014) Stable C0T-1 repeat RNA is abundant and is associated with euchromatic interphase chromosomes. Cell 156: 907–919.

55. LyonMF (1998) X-chromosome inactivation: a repeat hypothesis. Cytogenet Cell Genet 80: 133–137.

56. HansenRS (2003) X inactivation-specific methylation of LINE-1 elements by DNMT3B: implications for the Lyon repeat hypothesis. Hum Mol Genet 12: 2559–2567.

57. ChowJC, CiaudoC, FazzariMJ, MiseN, ServantN, et al. (2010) LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141: 956–969.

58. Diaz-PerezS, OuyangY, PerezV, CisnerosR, RegelsonM, et al. (2005) The element(s) at the nontranscribed Xist locus of the active X chromosome controls chromosomal replication timing in the mouse. Genetics 171: 663–672.

59. ZhuY, ByeS, StambrookPJ, TischfieldJA (1994) Single-base deletion induced by benzo[a]pyrene diol epoxide at the adenine phosphoribosyltransferase locus in human fibrosarcoma cell lines. Mutat Res 321: 73–79.

60. Helm S (1995) Cancer Cytogenetics. New York: Wiley-Liss.

61. Trask B, Pinkel D (1990) Flow cytometry; Crissman HA, Darzynkiewica Z, editors. New York: Academic Press.

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