LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin

PLoS Genetics

Volumn 5, Issue 1, 2009, Pages

  Chueh, Anderly C ^a,b   Northrop, Emma L ^a   Brettingham Moore, Kate H ^a   Choo, K H Andy ^a   Wong, Lee H ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AUSTIN HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; DNA; RNA; AUTOANTIGEN; NONHISTONE PROTEIN;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; CENTROMERE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CHROMOSOME 10Q; CHROMOSOME MAP; CONTROLLED STUDY; DNA SEQUENCE; EPIGENETICS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; L1 RETROPOSON; MITOSIS; MOUSE; NEOCENTOMERE; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; RETROPOSON; RNA INTERFERENCE; RNA TRANSCRIPTION; ANIMAL; CELL LINE; CHEMISTRY; CHROMATIN; CHROMOSOME 10; GENETIC EPIGENESIS; GENETICS; HAMSTER; LONG INTERSPERSED REPEAT; METABOLISM;

ANIMALS; AUTOANTIGENS; CELL LINE; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, HUMAN, PAIR 10; CRICETINAE; EPIGENESIS, GENETIC; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MICE; MITOSIS; RNA; TRANSCRIPTION, GENETIC;

EID: 59249100073     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000354     Document Type: Article

References (59)

1. Sullivan BA, Blower MD, Karpen GH (2001) Determining centromere identity: cyclical stories and forking paths. Nat Rev Genet 2: 584-596.
2. Cleveland DW, Mao Y, Sullivan KF (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112: 407-421.
3. Choo KH (2001) Domain organization at the centromere and neocentromere. Dev Cell 1: 165-177.
4. Schueler MG, Sullivan BA (2006) Structural and functional dynamics of human centromeric chromatin. Annu Rev Genomics Hum Genet 7: 301-313.
5. Amor DJ, Choo KH (2002) Neocentromeres: role in human disease, evolution, and centromere study. Am J Hum Genet 71: 695-714.
6. Marshall OJ, Chueh AC, Wong LH, Choo KH (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82: 261-282.
7. Alonso A, Mahmood R, Li S, Cheung F, Yoda K, et al. (2003) Genomic microarray analysis reveals distinct locations for the CENP-A binding domains in three human chromosome 13q32 neocentromeres. Hum Mol Genet 12: 2711-2721.
8. Lo AW, Magliano DJ, Sibson MC, Kalitsis P, Craig JM, et al. (2001) A novel chromatin immunoprecipitation and array (CIA) analysis identifies a 460-kb CENP-A-binding neocentromere DNA. Genome Res 11: 448-457.
9. Lo AW, Craig JM, Saffery R, Kalitsis P, Irvine DV, et al. (2001) A 330 kb CENP-A binding domain and altered replication timing at a human neocentromere. Embo J 20: 2087-2096.
10. Cardone MF, Alonso A, Pazienza M, Ventura M, Montemurro G, et al. (2006) Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs. Genome Biol 7: R91.
11. Warburton PE (2004) Chromosomal dynamics of human neocentromere formation. Chromosome Res 12: 617-626.
12. Voullaire LE, Slater HR, Petrovic V, Choo KH (1993) A functional marker centromere with no detectable alpha-satellite, satellite III, or CENP-B protein: activation of a latent centromere? Am J Hum Genet 52: 1153-1163.
13. du Sart D, Cancilla MR, Earle E, Mao JI, Saffery R, et al. (1997) A functional neo-centromere formed through activation of a latent human centromere and consisting of non-alpha-satellite DNA. Nat Genet 16: 144-153.
14. Craig JM, Earle E, Canham P, Wong LH, Anderson M, et al. (2003) Analysis of mammalian proteins involved in chromatin modification reveals new metaphase centromeric proteins and distinct chromosomal distribution patterns. Hum Mol Genet.
15. Saffery R, Earle E, Irvine DV, Kalitsis P, Choo KH (1999) Conservation of centromere protein in vertebrates. Chromosome Res 7: 261-265.
16. Barry AE, Bateman M, Howman EV, Cancilla MR, Tainton KM, et al. (2000) The 10q25 neocentromere and its inactive progenitor have identical primary nucleotide sequence: further evidence for epigenetic modification. Genome Res 10: 832-838.
17. Saffery R, Sumer H, Hassan S, Wong LH, Craig JM, et al. (2003) Transcription within a functional human centromere. Mol Cell 12: 509-516.
18. Chueh AC, Wong LH, Wong N, Choo KH (2005) Variable and hierarchical size distribution of L1-retroelement-enriched CENP-A clusters within a functional human neocentromere. Hum Mol Genet 14: 85-93.
19. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
20. Ostertag EM, Kazazian HH Jr (2001) Biology of mammalian L1 retrotransposons. Annu Rev Genet 35: 501-538.
21. Skowronski J, Singer MF (1985) Expression of a cytoplasmic LINE-1 transcript is regulated in a human teratocarcinoma cell line. Proc Natl Acad Sci U S A 82: 6050-6054.
22. Leibold DM, Swergold GD, Singer MF, Thayer RE, Dombroski BA, et al. (1990) Translation of LINE-1 DNA elements in vitro and in human cells. Proc Natl Acad Sci U S A 87: 6990-6994.
23. Singer MF, Krek V, McMillan JP, Swergold GD, Thayer RE (1993) LINE-1: a human transposable element. Gene 135: 183-188.
24. Han JS, Boeke JD (2005) LINE-1 retrotransposons: modulators of quantity and quality of mammalian gene expression? Bioessays 27: 775-784.
25. Lavie L, Maldener E, Brouha B, Meese EU, Mayer J (2004) The human L1 promoter: variable transcription initiation sites and a major impact of upstream flanking sequence on promoter activity. Genome Res 14: 2253-2260.
26. Speek M (2001) Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol 21: 1973-1985.
27. Nigumann P, Redik K, Matlik K, Speek M (2002) Many human genes are transcribed from the antisense promoter of L1 retrotransposon. Genomics 79: 628-634.
28. Bratthauer GL, Fanning TG (1992) Active LINE-1 retrotransposons in human testicular cancer. Oncogene 7: 507-510.
29. Bratthauer GL, Cardiff RD, Fanning TG (1994) Expression of LINE-1 retrotransposons in human breast cancer. Cancer 73: 2333-2336.
30. Bratthauer GL, Fanning TG (1993) LINE-1 retrotransposon expression in pediatric germ cell tumors. Cancer 71: 2383-2386.
31. Asch HL, Eliacin E, Fanning TG, Connolly JL, Bratthauer G, et al. (1996) Comparative expression of the LINE-1 p40 protein in human breast carcinomas and normal breast tissues. Oncol Res 8: 239-247.
32. Ergun S, Buschmann C, Heukeshoven J, Dammann K, Schnieders F, et al. (2004) Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues. J Biol Chem 279: 27753-27763.
33. Lam AL, Boivin CD, Bonney CF, Rudd MK, Sullivan BA (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc Natl Acad Sci U S A 103: 4186-4191.
34. Nakashima H, Nakano M, Ohnishi R, Hiraoka Y, Kaneda Y, et al. (2005) Assembly of additional heterochromatin distinct from centromere-kinetochore chromatin is required for de novo formation of human artificial chromosome. J Cell Sci 118: 5885-5898.
35. Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, et al. (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36: 138-145.
36. Topp CN, Zhong CX, Dawe RK (2004) Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci U S A 101: 15986-15991.
37. May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1: e79.
38. Pezer Z, Ugarkovic D (2008) RNA Pol II Promotes Transcription of Centromeric Satellite DNA in Beetles. PLoS ONE 3: e1594.
39. Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, et al. (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 17: 1146-1160.
40. Goshima G, Kiyomitsu T, Yoda K, Yanagida M (2003) Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J Cell Biol 160: 25-39.
41. McClelland SE, Borusu S, Amaro AC, Winter JR, Belwal M, et al. (2007) The CENP-A NAC/CAD kinetochore complex controls chromosome congression and spindle bipolarity. Embo J 26: 5033-5047.
42. Orthaus S, Ohndorf S, Diekmann S (2006) RNAi knockdown of human kinetochore protein CENP-H. Biochem Biophys Res Commun 348: 36-46.
43. Fukagawa T, Mikami Y, Nishihashi A, Regnier V, Haraguchi T, et al. (2001) CENP-H, a constitutive centromere component, is required for centromere targeting of CENP-C in vertebrate cells. Embo J 20: 4603-4617.
44. Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX, et al. (2006) The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat Cell Biol 8: 446-457.
45. Boeger H, Griesenbeck J, Strattan JS, Kornberg RD (2003) Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell 11: 1587-1598.
46. Chen ES, Saitoh S, Yanagida M, Takahashi K (2003) A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast. Mol Cell 11: 175-187.
47. Rasmussen TP, Mastrangelo MA, Eden A, Pehrson JR, Jaenisch R (2000) Dynamic relocalization of histone MacroH2A1 from centrosomes to inactive X chromosomes during X inactivation. J Cell Biol 150: 1189-1198.
48. Gilbert SL, Pehrson JR, Sharp PA (2000) XIST RNA associates with specific regions of the inactive X chromatin. J Biol Chem 275: 36491-36494.
49. Corey DR (2005) Regulating mammalian transcription with RNA. Trends Biochem Sci 30: 655-658.
50. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, et al. (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676.
51. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, et al. (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837.
52. Amor DJ, Bentley K, Ryan J, Perry J, Wong L, et al. (2004) Human centromere repositioning "in progress". Proc Natl Acad Sci U S A 101: 6542-6547.
53. Wong N (2006) DNA Methylation at the Neocentromere [PhD thesis]: The University of Melbourne.
54. Smit A, Hubley R, Green P (1996-2004) RepeatMasker Open-3.0. URL:http://www.repeatmasker.org.
55. Penzkofer T, Dandekar T, Zemojtel T (2005) L1Base: from functional annotation to prediction of active LINE-1 elements. Nucleic Acids Res 33: D498-500.
56. Swergold GD (1990) Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol 10: 6718-6729.
57. Minakami R, Kurose K, Etoh K, Furuhata Y, Hattori M, et al. (1992) Identification of an internal cis-element essential for the human L1 transcription and a nuclear factor(s) binding to the element. Nucleic Acids Res 20: 3139-3145.
58. Niranjanakumari S, Lasda E, Brazas R, Garcia-Blanco MA (2002) Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26: 182-190.
59. Sullivan BA, Warburton PE (1999) Chromosome Structural Analysis: A Practical Approach. In: Bickmore WA, ed. Oxford University Press. pp 81-101.