Home LiteratureArticle Details
PMID: 18839199 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres.

Chromosoma ·Vol. 118 ·No. 1 ·2009-02-00 ·Pages 113-25

Carone DM, Longo MS, Ferreri GC, Hall L, Harris M, Shook N, Bulazel KV, Carone BR, Obergfell C, O'Neill MJ, O'Neill RJ

Abstract

The transcriptional framework of the eukaryotic centromere core has been described in budding yeast and rice, but for most eukaryotes and all vertebrates it remains largely unknown. The lack of large pericentric repeats in the tammar wallaby has made it possible to map and identify the transcriptional units at the centromere in a mammalian species for the first time. We show that these transcriptional units, comprised of satellites and a retrovirus, are bound by centromere proteins and that they are the source of a novel class of small RNA. The endogenous retrovirus from which these small RNAs are derived is now known to be in the centromere domain of several vertebrate classes. The discovery of this new RNA form brings together several independent lines of evidence that point to a conserved retroviral-encoded processed RNA entity within eukaryotic centromeres.

MeSH Terms
Animals Cells, Cultured Centromere/genetics,physiology Chromosomes/genetics Chromosomes, Artificial, Bacterial Fibroblasts In Situ Hybridization, Fluorescence Mammals/genetics,metabolism Mice RNA, Satellite/genetics,metabolism Retroelements/genetics,physiology Retroviridae/genetics,physiology Transcription, Genetic
Chemicals
RNA, Satellite Retroelements
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Carone Dawn M
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA.
Longo Mark S
Ferreri Gianni C
Hall Laura
Harris Melissa
Shook Nicole
Bulazel Kira V
Carone Benjamin R
Obergfell Craig
O'Neill Michael J
O'Neill Rachel J
References (49)
49 references, click to expand
  1. A centromere-specific retroviral element associated with breaks of synteny in macropodine marsupials.
    Cytogenet Genome Res. 2004;107(1-2):115-8 PMID: 15305065
  2. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila.
    Cell. 2007 Mar 23;128(6):1089-103 PMID: 17346786
  3. Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages.
    Genome Biol. 2007;8(8):R170 PMID: 17708770
  4. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi.
    Science. 2002 Sep 13;297(5588):1833-7 PMID: 12193640
  5. Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes.
    Genes Dev. 2006 Aug 1;20(15):1993-7 PMID: 16882976
  6. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells.
    Nature. 2000 Mar 16;404(6775):293-6 PMID: 10749213
  7. A molecular view of plant centromeres.
    Trends Plant Sci. 2003 Dec;8(12):570-5 PMID: 14659705
  8. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid.
    Nature. 1998 May 7;393(6680):68-72 PMID: 9590690
  9. Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries.
    Hum Genet. 1988 Nov;80(3):224-34 PMID: 3192212
  10. Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats.
    PLoS Genet. 2005 Dec;1(6):e79 PMID: 16389298
  11. Advanced transfection with Lipofectamine 2000 reagent: primary neurons, siRNA, and high-throughput applications.
    Methods. 2004 Jun;33(2):95-103 PMID: 15121163
  12. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma.
    Chromosoma. 1985;91(3-4):313-21 PMID: 2579778
  13. Genomic and genetic definition of a functional human centromere.
    Science. 2001 Oct 5;294(5540):109-15 PMID: 11588252
  14. Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights.
    J Cell Biol. 1998 Apr 20;141(2):309-19 PMID: 9548711
  15. Centromere-encoded RNAs are integral components of the maize kinetochore.
    Proc Natl Acad Sci U S A. 2004 Nov 9;101(45):15986-91 PMID: 15514020
  16. Retention of latent centromeres in the Mammalian genome.
    J Hered. 2005 May-Jun;96(3):217-24 PMID: 15653556
  17. piRNAs--the ancient hunters of genome invaders.
    Genes Dev. 2007 Jul 15;21(14):1707-13 PMID: 17639076
  18. MicroRNA maturation: stepwise processing and subcellular localization.
    EMBO J. 2002 Sep 2;21(17):4663-70 PMID: 12198168
  19. CENP-B controls centromere formation depending on the chromatin context.
    Cell. 2007 Dec 28;131(7):1287-300 PMID: 18160038
  20. Transcripts from both strands of a satellite DNA occur on lampbrush chromosome loops of the newt Notophthalmus.
    Cell. 1981 Jun;24(3):649-59 PMID: 6166385
  21. Telomeric trans-silencing: an epigenetic repression combining RNA silencing and heterochromatin formation.
    PLoS Genet. 2007 Sep;3(9):1633-43 PMID: 17941712
  22. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing.
    Genes Dev. 2005 Feb 15;19(4):489-501 PMID: 15713842
  23. A new mathematical model for relative quantification in real-time RT-PCR.
    Nucleic Acids Res. 2001 May 1;29(9):e45 PMID: 11328886
  24. Small RNAs correspond to centromere heterochromatic repeats.
    Science. 2002 Sep 13;297(5588):1831 PMID: 12193644
  25. Transcription of two human genes from a bidirectional endogenous retrovirus promoter.
    Gene. 2006 Feb 1;366(2):335-42 PMID: 16288839
  26. Transcription and evolutionary dynamics of the centromeric satellite repeat CentO in rice.
    Mol Biol Evol. 2006 Dec;23(12):2505-20 PMID: 16987952
  27. Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere.
    Genome Res. 2007 Aug;17(8):1146-60 PMID: 17623812
  28. Loss of Dicer fowls up centromeres.
    Nat Cell Biol. 2004 Aug;6(8):696-7 PMID: 15303098
  29. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains.
    Mol Cell. 2003 Dec;12(6):1591-8 PMID: 14690610
  30. The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference.
    Genetics. 2007 Jun;176(2):749-61 PMID: 17409063
  31. Conserved organization of centromeric chromatin in flies and humans.
    Dev Cell. 2002 Mar;2(3):319-30 PMID: 11879637
  32. Cytogenetic and molecular evaluation of centromere-associated DNA sequences from a marsupial (Macropodidae: Macropus rufogriseus) X chromosome.
    Genetics. 2006 Feb;172(2):1129-37 PMID: 16387881
  33. A distinct small RNA pathway silences selfish genetic elements in the germline.
    Science. 2006 Jul 21;313(5785):320-4 PMID: 16809489
  34. Developmentally regulated piRNA clusters implicate MILI in transposon control.
    Science. 2007 May 4;316(5825):744-7 PMID: 17446352
  35. Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon.
    Plant Cell. 2002 Aug;14(8):1691-704 PMID: 12172016
  36. RNA maps reveal new RNA classes and a possible function for pervasive transcription.
    Science. 2007 Jun 8;316(5830):1484-8 PMID: 17510325
  37. Characterization of the piRNA complex from rat testes.
    Science. 2006 Jul 21;313(5785):363-7 PMID: 16778019
  38. Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function.
    Proc Natl Acad Sci U S A. 2006 Jun 6;103(23):8709-14 PMID: 16731634
  39. High-resolution organization of mouse centromeric and pericentromeric DNA.
    Cytogenet Genome Res. 2006;112(3-4):248-55 PMID: 16484780
  40. RNA interference is required for normal centromere function in fission yeast.
    Chromosome Res. 2003;11(2):137-46 PMID: 12733640
  41. Structural and functional characterization of noncoding repetitive RNAs transcribed in stressed human cells.
    Mol Biol Cell. 2005 Jun;16(6):2597-604 PMID: 15788562
  42. Sequencing of a rice centromere uncovers active genes.
    Nat Genet. 2004 Feb;36(2):138-45 PMID: 14716315
  43. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery.
    Science. 2004 Jan 30;303(5658):669-72 PMID: 14752161
  44. Coexamination of site-specific transcription factor binding and promoter activity in living cells.
    Mol Cell Biol. 1999 Dec;19(12):8393-9 PMID: 10567564
  45. CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA.
    J Cell Biol. 2002 Dec 9;159(5):765-75 PMID: 12460987
  46. Dicer is essential for formation of the heterochromatin structure in vertebrate cells.
    Nat Cell Biol. 2004 Aug;6(8):784-91 PMID: 15247924
  47. RNAi-mediated targeting of heterochromatin by the RITS complex.
    Science. 2004 Jan 30;303(5658):672-6 PMID: 14704433
  48. Functional elements residing within satellite DNAs.
    EMBO Rep. 2005 Nov;6(11):1035-9 PMID: 16264428
  49. Characterization of Dicer-deficient murine embryonic stem cells.
    Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):12135-40 PMID: 16099834
Article Info
Journal
Chromosoma
Abbr.
Chromosoma
ISSN
1432-0886
Published
2009-02-00
Epub
2008-00-07
Pages
113-25
Language
English
Region
Austria
NLM ID
2985138R
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]