Accumulation of Small Murine Minor Satellite Transcripts Leads to Impaired Centromeric Architecture and Function

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2006 May 30

PMID 16731634

Citations 127

Authors

Haniaa Bouzinba-Segard

Adeline Guais

Claire Francastel

Affiliations

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Abstract

RNAs have been implicated in the assembly and stabilization of large-scale chromatin structures including centromeric architecture; unidentified RNAs are integral components of human pericentric heterochromatin and are required for localization of the heterochromatin protein HP1 to centromeric regions. Because satellite repeats in centromeric regions are known to be transcribed, we assessed a role for noncoding centromeric RNAs in the structure and function of the centromere. We identified minor satellite transcripts of 120 nt in murine cells that localize to centromeres and accumulate upon stress or differentiation. Forced accumulation of 120-nt transcripts leads to defects in chromosome segregation and sister-chromatid cohesion, changes in hallmark centromeric epigenetic markers, and mislocalization of centromere-associated proteins essential for centromere function. These findings suggest that small centromeric RNAs may represent one of many pathways that regulate heterochromatin assembly in mammals, possibly through tethering of kinetochore- and heterochromatin-associated proteins.

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References

Henikoff S, Ahmad K, Platero J, van Steensel B . Heterochromatic deposition of centromeric histone H3-like proteins. Proc Natl Acad Sci U S A. 2000; 97(2):716-21. PMC: 15396. DOI: 10.1073/pnas.97.2.716. View

Eissenberg J, Elgin S . The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev. 2000; 10(2):204-10. DOI: 10.1016/s0959-437x(00)00058-7. View

Rasmussen T, Mastrangelo M, Eden A, Pehrson J, Jaenisch R . Dynamic relocalization of histone MacroH2A1 from centrosomes to inactive X chromosomes during X inactivation. J Cell Biol. 2000; 150(5):1189-98. PMC: 2175247. DOI: 10.1083/jcb.150.5.1189. View

Lachner M, OCarroll D, Rea S, Mechtler K, Jenuwein T . Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 2001; 410(6824):116-20. DOI: 10.1038/35065132. View

Bannister A, Zegerman P, Partridge J, Miska E, Thomas J, Allshire R . Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature. 2001; 410(6824):120-4. DOI: 10.1038/35065138. View

Nakayama J, Rice J, Strahl B, Allis C, Grewal S . Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science. 2001; 292(5514):110-3. DOI: 10.1126/science.1060118. View

Bachman K, Rountree M, Baylin S . Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem. 2001; 276(34):32282-7. DOI: 10.1074/jbc.M104661200. View

Francastel C, Magis W, Groudine M . Nuclear relocation of a transactivator subunit precedes target gene activation. Proc Natl Acad Sci U S A. 2001; 98(21):12120-5. PMC: 59778. DOI: 10.1073/pnas.211444898. View

Bernard P, Maure J, Partridge J, Genier S, Javerzat J, Allshire R . Requirement of heterochromatin for cohesion at centromeres. Science. 2001; 294(5551):2539-42. DOI: 10.1126/science.1064027. View

10.

Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal S . Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol. 2002; 4(1):89-93. DOI: 10.1038/ncb739. View

11.

Hutvagner G, Zamore P . RNAi: nature abhors a double-strand. Curr Opin Genet Dev. 2002; 12(2):225-32. DOI: 10.1016/s0959-437x(02)00290-3. View

12.

Maison C, Bailly D, Peters A, Quivy J, Roche D, Taddei A . Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet. 2002; 30(3):329-34. DOI: 10.1038/ng843. View

13.

Murata-Hori M, Wang Y . The kinase activity of aurora B is required for kinetochore-microtubule interactions during mitosis. Curr Biol. 2002; 12(11):894-9. DOI: 10.1016/s0960-9822(02)00848-5. View

14.

Jorgensen H, Bird A . MeCP2 and other methyl-CpG binding proteins. Ment Retard Dev Disabil Res Rev. 2002; 8(2):87-93. DOI: 10.1002/mrdd.10021. View

15.

Allshire R . Molecular biology. RNAi and heterochromatin--a hushed-up affair. Science. 2002; 297(5588):1818-9. DOI: 10.1126/science.1075874. View

16.

Reinhart B, Bartel D . Small RNAs correspond to centromere heterochromatic repeats. Science. 2002; 297(5588):1831. DOI: 10.1126/science.1077183. View

17.

Jenuwein T . Molecular biology. An RNA-guided pathway for the epigenome. Science. 2002; 297(5590):2215-8. DOI: 10.1126/science.1077903. View

18.

Muchardt C, Guilleme M, Seeler J, Trouche D, Dejean A, Yaniv M . Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep. 2002; 3(10):975-81. PMC: 1307621. DOI: 10.1093/embo-reports/kvf194. View

19.

Chen E, Saitoh S, Yanagida M, Takahashi K . A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast. Mol Cell. 2003; 11(1):175-87. DOI: 10.1016/s1097-2765(03)00011-x. View

20.

Fuks F, Hurd P, Wolf D, Nan X, Bird A, Kouzarides T . The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem. 2002; 278(6):4035-40. DOI: 10.1074/jbc.M210256200. View