Structure and folding of the Tetrahymena telomerase RNA pseudoknot
Abstract
Telomerase maintains telomere length at the ends of linear chromosomes using an integral telomerase RNA (TER) and telomerase reverse transcriptase (TERT). An essential part of TER is the template/pseudoknot domain (t/PK) which includes the template, for adding telomeric repeats, template boundary element (TBE), and pseudoknot, enclosed in a circle by stem 1. The Tetrahymena telomerase holoenzyme catalytic core (p65-TER-TERT) was recently modeled in our 9 Å resolution cryo-electron microscopy map by fitting protein and TER domains, including a solution NMR structure of the Tetrahymena pseudoknot. Here, we describe in detail the structure and folding of the isolated pseudoknot, which forms a compact structure with major groove U•A-U and novel C•G-A+ base triples. Base substitutions that disrupt the base triples reduce telomerase activity in vitro. NMR studies also reveal that the pseudoknot does not form in the context of full-length TER in the absence of TERT, due to formation of a competing structure that sequesters pseudoknot residues. The residues around the TBE remain unpaired, potentially providing access by TERT to this high affinity binding site during an early step in TERT-TER assembly. A model for the assembly pathway of the catalytic core is proposed.
- Authors:
-
- Univ. of California, Los Angeles, CA (United States). Dept. of Chemistry and Biochemistry. Molecular Biology Inst.
- Publication Date:
- Research Org.:
- Univ. of California, Los Angeles, CA (United States)
- Sponsoring Org.:
- USDOE; National Inst. of Health (NIH) (United States); National Science Foundation (NSF)
- OSTI Identifier:
- 1361669
- Grant/Contract Number:
- FC03-02ER63421; GM048123; GM007185; MCB1022379
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 45; Journal Issue: 1; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; catalytic domain; telomerase; tetrahymena; RNA
Citation Formats
Cash, Darian D., and Feigon, Juli. Structure and folding of the Tetrahymena telomerase RNA pseudoknot. United States: N. p., 2016.
Web. doi:10.1093/nar/gkw1153.
Cash, Darian D., & Feigon, Juli. Structure and folding of the Tetrahymena telomerase RNA pseudoknot. United States. https://doi.org/10.1093/nar/gkw1153
Cash, Darian D., and Feigon, Juli. Mon .
"Structure and folding of the Tetrahymena telomerase RNA pseudoknot". United States. https://doi.org/10.1093/nar/gkw1153. https://www.osti.gov/servlets/purl/1361669.
@article{osti_1361669,
title = {Structure and folding of the Tetrahymena telomerase RNA pseudoknot},
author = {Cash, Darian D. and Feigon, Juli},
abstractNote = {Telomerase maintains telomere length at the ends of linear chromosomes using an integral telomerase RNA (TER) and telomerase reverse transcriptase (TERT). An essential part of TER is the template/pseudoknot domain (t/PK) which includes the template, for adding telomeric repeats, template boundary element (TBE), and pseudoknot, enclosed in a circle by stem 1. The Tetrahymena telomerase holoenzyme catalytic core (p65-TER-TERT) was recently modeled in our 9 Å resolution cryo-electron microscopy map by fitting protein and TER domains, including a solution NMR structure of the Tetrahymena pseudoknot. Here, we describe in detail the structure and folding of the isolated pseudoknot, which forms a compact structure with major groove U•A-U and novel C•G-A+ base triples. Base substitutions that disrupt the base triples reduce telomerase activity in vitro. NMR studies also reveal that the pseudoknot does not form in the context of full-length TER in the absence of TERT, due to formation of a competing structure that sequesters pseudoknot residues. The residues around the TBE remain unpaired, potentially providing access by TERT to this high affinity binding site during an early step in TERT-TER assembly. A model for the assembly pathway of the catalytic core is proposed.},
doi = {10.1093/nar/gkw1153},
journal = {Nucleic Acids Research},
number = 1,
volume = 45,
place = {United States},
year = {Mon Nov 28 00:00:00 EST 2016},
month = {Mon Nov 28 00:00:00 EST 2016}
}
Web of Science
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Triple-helix structure in telomerase RNA contributes to catalysis
journal, May 2008
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Structural basis for protein-RNA recognition in telomerase
journal, May 2014
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Structural basis of template-boundary definition in Tetrahymena telomerase
journal, October 2015
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A telomerase holoenzyme protein enhances telomerase RNA assembly with telomerase reverse transcriptase
journal, February 2005
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A mutation in T7 RNA polymerase that facilitates promoter clearance
journal, April 2005
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- Proceedings of the National Academy of Sciences, Vol. 102, Issue 17
Functional importance of telomerase pseudoknot revealed by single-molecule analysis
journal, May 2011
- Mihalusova, M.; Wu, J. Y.; Zhuang, X.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
Telomerase recognizes its template by using an adjacent RNA motif
journal, May 2002
- Miller, M. C.; Collins, K.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 10
RNA-protein binding interface in the telomerase ribonucleoprotein
journal, November 2011
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- Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
The telomerase RNA pseudoknot is critical for the stable assembly of a catalytically active ribonucleoprotein
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- Proceedings of the National Academy of Sciences, Vol. 96, Issue 12
A Mutant of Tetrahymena Telomerase Reverse Transcriptase with Increased Processivity
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A novel family of RNA tetraloop structure forms the recognition site for Saccharomyces cerevisiae RNase III
journal, December 2001
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A conserved pseudoknot in telomerase RNA
journal, January 1991
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- Nucleic Acids Research, Vol. 19, Issue 24
Mutational analysis of the Tetrahymena telomerase RNA: identification of residues affecting telomerase activity in vitro
journal, February 1998
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- Nucleic Acids Research, Vol. 26, Issue 3
The solution structure of an essential stem-loop of human telomerase RNA
journal, May 2003
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Structure of the Tetrahymena thermophila telomerase RNA helix II template boundary element
journal, February 2006
- Richards, R. J.
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Structural Biology of Telomerase
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Detailed view of human telomerase enzyme invites rethink of its structure
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Mechanisms of template handling and pseudoknot folding in human telomerase and their manipulation to expand the sequence repertoire of processive repeat synthesis
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Zika genomics urgently need standardized and curated reference sequences
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