TERRA and Telomere Maintenance in the Yeast Saccharomyces cerevisiae

Telomeres are structures made of DNA, proteins and RNA found at the ends of eukaryotic linear chromosomes. These dynamic nucleoprotein structures protect chromosomal tips from end-to-end fusions, degradation, activation of damage checkpoints and erroneous DNA repair events. Telomeres were thought to be transcriptionally silent regions because of their constitutive heterochromatin signature until telomeric long non-coding RNAs (LncRNAs) were discovered. One of them, TERRA (TElomeric Repeat-containing RNA), starts in the subtelomeric regions towards the chromosome ends from different telomeres and has been extensively studied in many evolutionarily distant eukaryotes. Changes in TERRA's expression can lead to telomeric dysfunction, interfere with the replicative machinery and impact telomere length. TERRA also co-localizes in vivo with telomerase, and can form RNA:DNA hybrid structures called R-loops, which have been implicated in the onset of senescence and the alternative lengthening of telomere (ALT) pathway. Yet, the molecular mechanisms involving TERRA, as well as its function, remain elusive. Here, we review the current knowledge of TERRA transcription, structure, expression, regulation and its multiple telomeric and extra-telomeric functions in the budding yeast Saccharomyces cerevisiae.

Automated summary

Telomeres are structures found at the ends of eukaryotic linear chromosomes that protect chromosomal tips and play roles in DNA repair. Telomeric long non-coding RNAs (LncRNAs), such as TERRA, have been discovered and shown to influence telomere function and length. TERRA interacts with telomerase and forms RNA:DNA hybrid structures, and its dysregulation has been associated with senescence and alternative lengthening of telomeres (ALT) pathways. This review focuses on the current understanding of TERRA in the budding yeast Saccharomyces cerevisiae, including its transcription, structure, expression, regulation, and functions.