Evolutionary perspectives of telomerase RNA structure and function

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ABSTRACT

Telomerase is the eukaryotic solution to the ‘end-replication problem’ of linear chromosomes by synthesising the highly repetitive DNA constituent of telomeres, the nucleoprotein cap that protects chromosome termini. Functioning as a ribonucleoprotein (RNP) enzyme, telomerase is minimally composed of the highly conserved catalytic telomerase reverse transcriptase (TERT) and essential telomerase RNA (TR) component. Beyond merely providing the template for telomeric DNA synthesis, TR is an innate telomerase component and directly facilitates enzymatic function. TR accomplishes this by having evolved structural elements for stable assembly with the TERT protein and the regulation of the telomerase catalytic cycle. Despite its prominence and prevalence, TR has profoundly diverged in length, sequence, and biogenesis pathway among distinct evolutionary lineages. This diversity has generated numerous structural and mechanistic solutions for ensuring proper RNP formation and high fidelity telomeric DNA synthesis. Telomerase provides unique insights into RNA and protein coevolution within RNP enzymes.

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Identification of a specific telomere terminal transferase activity in Tetrahymena extracts.

C Greider, E H Blackburn (1985)

We have found a novel activity in Tetrahymena cell free extracts that adds tandem TTGGGG repeats onto synthetic telomere primers. The single-stranded DNA oligonucleotides (TTGGGG)4 and TGTGTGGGTGTGTGGGTGTGTGGG, consisting of the Tetrahymena and yeast telomeric sequences respectively, each functioned as primers for elongation, while (CCCCAA)4 and two nontelomeric sequence DNA oligomers did not. Efficient synthesis of the TTGGGG repeats depended only on addition of micromolar concentrations of oligomer primer, dGTP, and dTTP to the extract. The activity was sensitive to heat and proteinase K treatment. The repeat addition was independent of both endogenous Tetrahymena DNA and the endogenous alpha-type DNA polymerase; and a greater elongation activity was present during macronuclear development, when a large number of telomeres are formed and replicated, than during vegetative cell growth. We propose that the novel telomere terminal transferase is involved in the addition of telomeric repeats necessary for the replication of chromosome ends in eukaryotes.

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How telomeres solve the end-protection problem.

Titia de Lange (2009)

The ends of eukaryotic chromosomes have the potential to be mistaken for damaged or broken DNA and must therefore be protected from cellular DNA damage response pathways. Otherwise, cells might permanently arrest in the cell cycle, and attempts to "repair" the chromosome ends would have devastating consequences for genome integrity. This end-protection problem is solved by protein-DNA complexes called telomeres. Studies of mammalian cells have recently uncovered the mechanism by which telomeres disguise the chromosome ends. Comparison to unicellular eukaryotes reveals key differences in the DNA damage response systems that inadvertently threaten chromosome ends. Telomeres appear to be tailored to these variations, explaining their variable structure and composition.

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Whole-genome duplication in teleost fishes and its evolutionary consequences.

Stella M K Glasauer, Stephan Neuhauss (2014)

Whole-genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, by far the most species-rich vertebrate clade. After initial controversy, there is now solid evidence that such event took place in the common ancestor of all extant teleosts. It is termed teleost-specific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosage selection (preserving genes to maintain dosage balance between interconnected components). Since the frequency of these mechanisms is influenced by the genes' properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massive radiation of teleosts, have been matter of controversial debate. It is evident that gene duplications are crucial for generating complexity and that WGDs provide large amounts of raw material for evolutionary adaptation and innovation. However, it is less clear whether the TS-WGD is directly linked to the evolutionary success of teleosts and their radiation. Recent studies let us conclude that TS-WGD has been important in generating teleost complexity, but that more recent ecological adaptations only marginally related to TS-WGD might have even contributed more to diversification. It is likely, however, that TS-WGD provided teleosts with diversification potential that can become effective much later, such as during phases of environmental change.

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Author and article information

Journal

Journal ID (nlm-ta): RNA Biol

Journal ID (iso-abbrev): RNA Biol

Journal ID (publisher-id): KRNB

Journal ID (publisher-id): krnb20

Title: RNA Biology

Publisher: Taylor & Francis

ISSN (Print): 1547-6286

ISSN (Electronic): 1555-8584

Publication date Collection: August 2016

Publication date (Electronic): 30 June 2016

Publication date PMC-release: 30 June 2016

Volume: 13

Issue: 8 , Telomeres and Telomerase

Pages: 720-732

Affiliations

School of Molecular Sciences, Arizona State University , Tempe, AZ, USA

Author notes

CONTACT Julian J.-L. Chen JLChen@ 123456asu.edu School of Molecular Sciences, Arizona State University , Tempe, AZ, USA

Article

Publisher ID: 1205768

DOI: 10.1080/15476286.2016.1205768

PMC ID: 4993307

PubMed ID: 27359343

SO-VID: 3cdb991e-ee5e-4f8f-abcc-b5b54811d0c6

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution-Non-Commercial License ( http://creativecommons.org/licenses/by-nc/3.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The moral rights of the named author(s) have been asserted.

History

Date received : 30 July 2015

Date revision received : 14 June 2016

Date accepted : 20 June 2016

Page count

Figures: 5, Tables: 0, References: 149, Pages: 13

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Evolutionary perspectives of telomerase RNA structure and function

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ABSTRACT

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Most cited references 129

Identification of a specific telomere terminal transferase activity in Tetrahymena extracts.

How telomeres solve the end-protection problem.

Whole-genome duplication in teleost fishes and its evolutionary consequences.

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Cited by 37

Most referenced authors 1,693