The first crystal structures of hybrid and parallel four-tetrad intramolecular G-quadruplexes
Abstract
Abstract G-quadruplexes (GQs) are non-canonical DNA structures composed of stacks of stabilized G-tetrads. GQs play an important role in a variety of biological processes and may form at telomeres and oncogene promoters among other genomic locations. Here, we investigate nine variants of telomeric DNA from Tetrahymena thermophila with the repeat (TTGGGG)n. Biophysical data indicate that the sequences fold into stable four-tetrad GQs which adopt multiple conformations according to native PAGE. Excitingly, we solved the crystal structure of two variants, TET25 and TET26. The two variants differ by the presence of a 3′-T yet adopt different GQ conformations. TET25 forms a hybrid [3 + 1] GQ and exhibits a rare 5′-top snapback feature. Consequently, TET25 contains four loops: three lateral (TT, TT, and GTT) and one propeller (TT). TET26 folds into a parallel GQ with three TT propeller loops. To the best of our knowledge, TET25 and TET26 are the first reported hybrid and parallel four-tetrad unimolecular GQ structures. The results presented here expand the repertoire of available GQ structures and provide insight into the intricacy and plasticity of the 3D architecture adopted by telomeric repeats from T. thermophila and GQs in general.
- Authors:
-
[1]
- Department of Chemistry and Biochemistry, Swarthmore College, 500 College Ave, Swarthmore, PA 19081, USA
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH)
- OSTI Identifier:
- 1846461
- Alternate Identifier(s):
- OSTI ID: 1863051
- Grant/Contract Number:
- AC02-06CH11357; P30 GM124165; 1R15CA208676-01A1; 1R15CA253134
- Resource Type:
- Published Article
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Name: Nucleic Acids Research Journal Volume: 50 Journal Issue: 5; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Beseiso, Dana, Chen, Erin V., McCarthy, Sawyer E., Martin, Kailey N., Gallagher, Elizabeth P., Miao, Joanne, and Yatsunyk, Liliya A. The first crystal structures of hybrid and parallel four-tetrad intramolecular G-quadruplexes. United Kingdom: N. p., 2022.
Web. doi:10.1093/nar/gkac091.
Beseiso, Dana, Chen, Erin V., McCarthy, Sawyer E., Martin, Kailey N., Gallagher, Elizabeth P., Miao, Joanne, & Yatsunyk, Liliya A. The first crystal structures of hybrid and parallel four-tetrad intramolecular G-quadruplexes. United Kingdom. https://doi.org/10.1093/nar/gkac091
Beseiso, Dana, Chen, Erin V., McCarthy, Sawyer E., Martin, Kailey N., Gallagher, Elizabeth P., Miao, Joanne, and Yatsunyk, Liliya A. Fri .
"The first crystal structures of hybrid and parallel four-tetrad intramolecular G-quadruplexes". United Kingdom. https://doi.org/10.1093/nar/gkac091.
@article{osti_1846461,
title = {The first crystal structures of hybrid and parallel four-tetrad intramolecular G-quadruplexes},
author = {Beseiso, Dana and Chen, Erin V. and McCarthy, Sawyer E. and Martin, Kailey N. and Gallagher, Elizabeth P. and Miao, Joanne and Yatsunyk, Liliya A.},
abstractNote = {Abstract G-quadruplexes (GQs) are non-canonical DNA structures composed of stacks of stabilized G-tetrads. GQs play an important role in a variety of biological processes and may form at telomeres and oncogene promoters among other genomic locations. Here, we investigate nine variants of telomeric DNA from Tetrahymena thermophila with the repeat (TTGGGG)n. Biophysical data indicate that the sequences fold into stable four-tetrad GQs which adopt multiple conformations according to native PAGE. Excitingly, we solved the crystal structure of two variants, TET25 and TET26. The two variants differ by the presence of a 3′-T yet adopt different GQ conformations. TET25 forms a hybrid [3 + 1] GQ and exhibits a rare 5′-top snapback feature. Consequently, TET25 contains four loops: three lateral (TT, TT, and GTT) and one propeller (TT). TET26 folds into a parallel GQ with three TT propeller loops. To the best of our knowledge, TET25 and TET26 are the first reported hybrid and parallel four-tetrad unimolecular GQ structures. The results presented here expand the repertoire of available GQ structures and provide insight into the intricacy and plasticity of the 3D architecture adopted by telomeric repeats from T. thermophila and GQs in general.},
doi = {10.1093/nar/gkac091},
journal = {Nucleic Acids Research},
number = 5,
volume = 50,
place = {United Kingdom},
year = {Fri Feb 25 00:00:00 EST 2022},
month = {Fri Feb 25 00:00:00 EST 2022}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1093/nar/gkac091
https://doi.org/10.1093/nar/gkac091
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
G-overhang dynamics at Tetrahymena telomeres
journal, August 2001
- Jacob, N. K.
- The EMBO Journal, Vol. 20, Issue 15
High-throughput sequencing of DNA G-quadruplex structures in the human genome
journal, July 2015
- Chambers, Vicki S.; Marsico, Giovanni; Boutell, Jonathan M.
- Nature Biotechnology, Vol. 33, Issue 8
Stacking of G-quadruplexes: NMR structure of a G-rich oligonucleotide with potential anti-HIV and anticancer activity†
journal, August 2011
- Do, Ngoc Quang; Lim, Kah Wai; Teo, Ming Hoon
- Nucleic Acids Research, Vol. 39, Issue 21
NMR solution and X-ray crystal structures of a DNA molecule containing both right- and left-handed parallel-stranded G-quadruplexes
journal, June 2019
- Winnerdy, Fernaldo Richtia; Bakalar, Blaž; Maity, Arijit
- Nucleic Acids Research, Vol. 47, Issue 15
Loop flexibility in human telomeric quadruplex small-molecule complexes
journal, May 2015
- Collie, Gavin W.; Campbell, Nancy H.; Neidle, Stephen
- Nucleic Acids Research, Vol. 43, Issue 10
Classification of G-Quadruplex DNA on the Basis of the Quadruplex Twist Angle and Planarity of G-Quartets
journal, December 2010
- Reshetnikov, R. V.; Kopylov, A. M.; Golovin, A. V.
- Acta Naturae, Vol. 2, Issue 4
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix
journal, October 2019
- Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L.
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10
G-Quadruplex Secondary Structure Obtained from Circular Dichroism Spectroscopy
journal, April 2018
- del Villar-Guerra, Rafael; Trent, John O.; Chaires, Jonathan B.
- Angewandte Chemie International Edition, Vol. 57, Issue 24
Structure of a left-handed DNA G-quadruplex
journal, February 2015
- Chung, Wan Jun; Heddi, Brahim; Schmitt, Emmanuelle
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 9
Hexahydrated magnesium ions bind in the deep major groove and at the outer mouth of A-form nucleic acid duplexes
journal, April 2000
- Robinson, H.
- Nucleic Acids Research, Vol. 28, Issue 8
Structure of an Unprecedented G-Quadruplex Scaffold in the Human c-kit Promoter
journal, April 2007
- Phan, Anh Tuân; Kuryavyi, Vitaly; Burge, Sarah
- Journal of the American Chemical Society, Vol. 129, Issue 14
Metal Cations in G-Quadruplex Folding and Stability
journal, September 2016
- Bhattacharyya, Debmalya; Mirihana Arachchilage, Gayan; Basu, Soumitra
- Frontiers in Chemistry, Vol. 4
Telomeric repeat mutagenicity in human somatic cells is modulated by repeat orientation and G-quadruplex stability
journal, November 2010
- Damerla, Rama Rao; Knickelbein, Kelly E.; Kepchia, Devin
- DNA Repair, Vol. 9, Issue 11
G-quadruplex structure of an anti-proliferative DNA sequence
journal, May 2017
- Do, Ngoc Quang; Chung, Wan Jun; Truong, Thi Hong Anh
- Nucleic Acids Research, Vol. 45, Issue 12
Phosphorylation at 5' end of guanosine stretches inhibits dimerization of G-quadruplexes and formation of a G-quadruplex interferes with the enzymatic activities of DNA enzymes
journal, August 2004
- Uddin, M. K.
- Nucleic Acids Research, Vol. 32, Issue 15
Monomer-Dimer Equilibrium for the 5′-5′ Stacking of Propeller-Type Parallel-Stranded G-Quadruplexes: NMR Structural Study
journal, September 2012
- Do, Ngoc Quang; Phan, Anh Tuân
- Chemistry - A European Journal, Vol. 18, Issue 46
Encoding canonical DNA quadruplex structure
journal, August 2018
- Dvorkin, Scarlett A.; Karsisiotis, Andreas I.; Webba da Silva, Mateus
- Science Advances, Vol. 4, Issue 8
Bulges in G-Quadruplexes: Broadening the Definition of G-Quadruplex-Forming Sequences
journal, March 2013
- Mukundan, Vineeth Thachappilly; Phan, Anh Tuân
- Journal of the American Chemical Society, Vol. 135, Issue 13
NMR study of parallel-stranded tetraplex formation by the hexadeoxynucleotide d(TG4T)
journal, November 1992
- Aboul-ela, Fareed; Murchie, Alastair I. H.; Lilley, David M. J.
- Nature, Vol. 360, Issue 6401
The CCP4 suite programs for protein crystallography
journal, September 1994
- ,
- Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763
A Minimal Sequence for Left‐Handed G‐Quadruplex Formation
journal, February 2019
- Bakalar, Blaž; Heddi, Brahim; Schmitt, Emmanuelle
- Angewandte Chemie International Edition, Vol. 58, Issue 8
Solution structure of a DNA quadruplex containing ALS and FTD related GGGGCC repeat stabilized by 8-bromodeoxyguanosine substitution
journal, August 2015
- Brčić, Jasna; Plavec, Janez
- Nucleic Acids Research, Vol. 43, Issue 17
Interaction of human telomeric DNA with N- methyl mesoporphyrin IX
journal, February 2012
- Nicoludis, John M.; Barrett, Steven P.; Mergny, Jean-Louis
- Nucleic Acids Research, Vol. 40, Issue 12
Stability of telomeric G-quadruplexes
journal, December 2010
- Tran, Phong Lan Thao; Mergny, Jean-Louis; Alberti, Patrizia
- Nucleic Acids Research, Vol. 39, Issue 8
Quadruplexes in ‘Dicty’: crystal structure of a four-quartet G-quadruplex formed by G-rich motif found in the Dictyostelium discoideum genome
journal, April 2018
- Guédin, Aurore; Lin, Linda Yingqi; Armane, Samir
- Nucleic Acids Research, Vol. 46, Issue 10
Solution Structure of a Parallel-stranded G-Quadruplex DNA
journal, December 1993
- Wang, Yong; Patel, Dinshaw J.
- Journal of Molecular Biology, Vol. 234, Issue 4
Combinatorially selected guanosine-quartet structure is a potent inhibitor of human immunodeficiency virus envelope-mediated cell fusion.
journal, February 1994
- Wyatt, J. R.; Vickers, T. A.; Roberson, J. L.
- Proceedings of the National Academy of Sciences, Vol. 91, Issue 4
Solution Structure of a Parallel-stranded Tetraplex Formed by d(TG4T) in the Presence of Sodium Ions by Nuclear Magnetic Resonance Spectroscopy
journal, October 1994
- Aboul-ela, Fareed; Murchie, Alastair I. H.; Norman, David G.
- Journal of Molecular Biology, Vol. 243, Issue 3
Telomeric G-Quadruplexes: From Human to Tetrahymena Repeats
journal, January 2017
- Demkovičová, Erika; Bauer, Ľuboš; Krafčíková, Petra
- Journal of Nucleic Acids, Vol. 2017
HELIX: a new modular nucleic acid crystallization screen
journal, May 2014
- Viladoms, Julia; Parkinson, Gary N.
- Journal of Applied Crystallography, Vol. 47, Issue 3
Optimized End-Stacking Provides Specificity of N -Methyl Mesoporphyrin IX for Human Telomeric G-Quadruplex DNA
journal, December 2012
- Nicoludis, John M.; Miller, Stephen T.; Jeffrey, Philip D.
- Journal of the American Chemical Society, Vol. 134, Issue 50
Loop permutation affects the topology and stability of G-quadruplexes
journal, September 2018
- Cheng, Mingpan; Cheng, Yu; Hao, Jingya
- Nucleic Acids Research, Vol. 46, Issue 18
Small-molecule interaction with a five-guanine-tract G-quadruplex structure from the human MYC promoter
journal, July 2005
- Phan, Anh Tuân; Kuryavyi, Vitaly; Gaw, Hai Yan
- Nature Chemical Biology, Vol. 1, Issue 3
Features and development of Coot
journal, March 2010
- Emsley, P.; Lohkamp, B.; Scott, W. G.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
Extension of G-quadruplex DNA by ciliate telomerase
journal, March 2006
- Oganesian, Liana; Moon, Ian K.; Bryan, Tracy M.
- The EMBO Journal, Vol. 25, Issue 5
CheckMyMetal : a macromolecular metal-binding validation tool
journal, February 2017
- Zheng, Heping; Cooper, David R.; Porebski, Przemyslaw J.
- Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 3
Intra-locked G-quadruplex structures formed by irregular DNA G-rich motifs
journal, February 2020
- Maity, Arijit; Winnerdy, Fernaldo Richtia; Chang, Weili Denyse
- Nucleic Acids Research, Vol. 48, Issue 6
Solution structure of the Tetrahymena telomeric repeat d(T2G4)4 G-tetraplex
journal, December 1994
- Wang, Yong; Patel, Dinshaw J.
- Structure, Vol. 2, Issue 12
The crystal structure of a parallel-stranded guanine tetraplex at 0.95Å resolution
journal, October 1997
- Phillips, Kathryn; Dauter, Zbyszek; Murchie, Alastair I. H.
- Journal of Molecular Biology, Vol. 273, Issue 1
A graphical user interface to the CCP 4 program suite
journal, June 2003
- Potterton, Elizabeth; Briggs, Peter; Turkenburg, Maria
- Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 7
Structure and stability of sodium and potassium complexes of dT4G4 and dT4G4T
journal, March 1992
- Lu, Min; Guo, Qiu; Kallenbach, Neville R.
- Biochemistry, Vol. 31, Issue 9
Two-repeat Tetrahymena Telomeric d(TGGGGTTGGGGT) Sequence Interconverts Between Asymmetric Dimeric G-quadruplexes in Solution
journal, April 2004
- Phan, Anh Tuân; Modi, Yasha S.; Patel, Dinshaw J.
- Journal of Molecular Biology, Vol. 338, Issue 1
A Parallel G Quadruplex-Binding Protein Regulates the Boundaries of DNA Elimination Events of Tetrahymena thermophila
journal, March 2016
- Carle, Christine M.; Zaher, Hani S.; Chalker, Douglas L.
- PLOS Genetics, Vol. 12, Issue 3
Human telomere, oncogenic promoter and 5'-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics
journal, November 2007
- Patel, D. J.; Phan, A. T.; Kuryavyi, V.
- Nucleic Acids Research, Vol. 35, Issue 22
Machine learning model for sequence-driven DNA G-quadruplex formation
journal, November 2017
- Sahakyan, Aleksandr B.; Chambers, Vicki S.; Marsico, Giovanni
- Scientific Reports, Vol. 7, Issue 1
How long is too long? Effects of loop size on G-quadruplex stability
journal, July 2010
- Guédin, Aurore; Gros, Julien; Alberti, Patrizia
- Nucleic Acids Research, Vol. 38, Issue 21
G-quadruplex: Flexible conformational changes by cations, pH, crowding and its applications to biosensing
journal, April 2021
- Nishio, Maui; Tsukakoshi, Kaori; Ikebukuro, Kazunori
- Biosensors and Bioelectronics, Vol. 178
Topology-based classification of tetrads and quadruplex structures
journal, October 2019
- Popenda, Mariusz; Miskiewicz, Joanna; Sarzynska, Joanna
- Bioinformatics, Vol. 36, Issue 4
Protein Data Bank: the single global archive for 3D macromolecular structure data
journal, October 2018
- Burley, Stephen K.; Berman, Helen M.; Bhikadiya, Charmi
- Nucleic Acids Research, Vol. 47, Issue D1
Water spines and networks in G-quadruplex structures
journal, December 2020
- Li, Kevin; Yatsunyk, Liliya; Neidle, Stephen
- Nucleic Acids Research, Vol. 49, Issue 1
DNA quadruplex folding formalism – A tutorial on quadruplex topologies
journal, November 2013
- Karsisiotis, Andreas Ioannis; O’Kane, Christopher; Webba da Silva, Mateus
- Methods, Vol. 64, Issue 1
Biophysical and X-ray structural studies of the (GGGTT)3GGG G-quadruplex in complex with N-methyl mesoporphyrin IX
journal, November 2020
- Lin, Linda Yingqi; McCarthy, Sawyer; Powell, Barrett M.
- PLOS ONE, Vol. 15, Issue 11
Guided Assembly of Tetramolecular G-Quadruplexes
journal, June 2013
- Yatsunyk, Liliya A.; Piétrement, Olivier; Albrecht, Delphine
- ACS Nano, Vol. 7, Issue 7
Loop-Length-Dependent Folding of G-Quadruplexes
journal, November 2004
- Hazel, Pascale; Huppert, Julian; Balasubramanian, Shankar
- Journal of the American Chemical Society, Vol. 126, Issue 50
Tetrahymena thermophila, a unicellular eukaryote with separate germline and somatic genomes
journal, July 2011
- Orias, Eduardo; Cervantes, Marcella D.; Hamilton, Eileen P.
- Research in Microbiology, Vol. 162, Issue 6
Structure, Energetics, and Dynamics of the Nucleic Acid Base Pairs: Nonempirical Ab Initio Calculations
journal, November 1999
- Hobza, Pavel; Šponer, Jiří
- Chemical Reviews, Vol. 99, Issue 11
Thermal difference spectra: a specific signature for nucleic acid structures
journal, September 2005
- Mergny, J. -L.
- Nucleic Acids Research, Vol. 33, Issue 16