Host genome surveillance for retrotransposons by transposon-derived proteins.
Transposable elements and their remnants constitute a substantial fraction of eukaryotic genomes. Host genomes have evolved defence mechanisms, including chromatin modifications and RNA interference, to regulate transposable elements. Here we describe a genome surveillance mechanism for retrotransposons by transposase-derived centromeric protein CENP-B homologues of the fission yeast Schizosaccharomyces pombe. CENP-B homologues of S. pombe localize at and recruit histone deacetylases to silence Tf2 retrotransposons. CENP-Bs also repress solo long terminal repeats (LTRs) and LTR-associated genes. Tf2 elements are clustered into 'Tf' bodies, the organization of which depends on CENP-Bs that display discrete nuclear structures. Furthermore, CENP-Bs prevent an 'extinct' Tf1 retrotransposon from re-entering the host genome by blocking its recombination with extant Tf2, and silence and immobilize a Tf1 integrant that becomes sequestered into Tf bodies. Our results reveal a probable ancient retrotransposon surveillance pathway important for host genome integrity, and highlight potential conflicts between DNA transposons and retrotransposons, major transposable elements believed to have greatly moulded the evolution of genomes.
Cam
Hugh P
HP
Laboratory of Biochemistry and Molecular Biology, National Cancer Institute, Bethesda, Maryland 20892, USA.
Noma
Ken-ichi
K
Ebina
Hirotaka
H
Levin
Henry L
HL
Grewal
Shiv I S
SI
D018797:Cell Cycle Proteins / Q000378:metabolism; D051936:Centromere Protein B / Q000235:genetics / Q000378:metabolism; D004251:DNA Transposable Elements / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics; D019143:Evolution, Molecular; D015966:Gene Expression Regulation, Fungal; D020868:Gene Silencing; D005800:Genes, Fungal / Q000235:genetics; D049770:Genes, Mating Type, Fungal / Q000235:genetics; D016681:Genome, Fungal / Q000235:genetics*; D042822:Genomic Instability / Q000235:genetics*; D006570:Heterochromatin / Q000235:genetics / Q000378:metabolism; D006655:Histone Deacetylases / Q000378:metabolism; D018384:Oxidative Stress; D021381:Protein Transport; D018626:Retroelements / Q000235:genetics*; D012568:Schizosaccharomyces / Q000201:enzymology / Q000235:genetics* / Q000378:metabolism*; D029702:Schizosaccharomyces pombe Proteins / Q000235:genetics / Q000378:metabolism*; D020079:Terminal Repeat Sequences / Q000235:genetics
D018797:Cell Cycle Proteins; D051936:Centromere Protein B; C115302:Clr3 protein, S pombe; D004251:DNA Transposable Elements; D004268:DNA-Binding Proteins; D006570:Heterochromatin; D018626:Retroelements; D029702:Schizosaccharomyces pombe Proteins; C083145:Tf2-6 protein, S pombe; C097691:cbp1 protein, S pombe; D006655:Histone Deacetylases