The RNA interactome of human telomerase RNA reveals a coding-independent role for a histone mRNA in telomere homeostasis

Author:

Ivanyi-Nagy Roland1ORCID,Ahmed Syed Moiz1ORCID,Peter Sabrina1,Ramani Priya Dharshana1,Ong Peh Fern2,Dreesen Oliver2ORCID,Dröge Peter13ORCID

Affiliation:

1. School of Biological Sciences, Nanyang Technological University, Singapore, Singapore

2. Cell Ageing, Skin Research Institute Singapore, Singapore, Singapore

3. Nanyang Institute of Structural Biology, Nanyang Technological University, Singapore, Singapore

Abstract

Telomerase RNA (TR) provides the template for DNA repeat synthesis at telomeres and is essential for genome stability in continuously dividing cells. We mapped the RNA interactome of human TR (hTR) and identified a set of non-coding and coding hTR-interacting RNAs, including the histone 1C mRNA (HIST1H1C). Disruption of the hTR-HIST1H1C RNA association resulted in markedly increased telomere elongation without affecting telomerase enzymatic activity. Conversely, over-expression of HIST1H1C led to telomere attrition. By using a combination of mutations to disentangle the effects of histone 1 RNA synthesis, protein expression, and hTR interaction, we show that HIST1H1C RNA negatively regulates telomere length independently of its protein coding potential. Taken together, our data provide important insights into a surprisingly complex hTR-RNA interaction network and define an unexpected non-coding RNA role for HIST1H1C in regulating telomere length homeostasis, thus offering a glimpse into the mostly uncharted, vast space of non-canonical messenger RNA functions.

Funder

Ministry of Education - Singapore

Singapore Biomedical Research Council

Agency for Science, Technology and Research

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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