Crystal structures of a natural DNA polymerase that functions as an XNA reverse transcriptase

Jackson, Lynnette N.; Chim, Nicholas; Shi, Changhua; Chaput, John C.

doi:10.1093/nar/gkz513

Title: Crystal structures of a natural DNA polymerase that functions as an XNA reverse transcriptase

Journal Article · 06 June 2019 · Nucleic Acids Research

DOI: https://doi.org/10.1093/nar/gkz513 · OSTI ID:1525514

^[1];

^[1]; Shi, Changhua ^[1];

^[1]

University of California, Irvine, CA (United States)

Replicative DNA polymerases are highly efficient enzymes that maintain stringent geometric control over shape and orientation of the template and incoming nucleoside triphosphate. In a surprising twist to this paradigm, a naturally occurring bacterial DNA polymerase I member isolated from Geobacillus stearothermophilus (Bst) exhibits an innate ability to reverse transcribe RNA and other synthetic congeners (XNAs) into DNA. This observation raises the interesting question of how a replicative DNA polymerase is able to recognize templates of diverse chemical composition. Here, we present crystal structures of natural Bst DNA polymerase that capture the post-translocated product of DNA synthesis on templates composed entirely of 2'-deoxy-2'-fluoro-β-D-arabino nucleic acid (FANA) and α-L-threofuranosyl nucleic acid (TNA). Analysis of the enzyme active site reveals the importance of structural plasticity as a possible mechanism for XNA-dependent DNA synthesis and provides insights into the construction of variants with improved activity.

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Research Organization:: Univ. of California, Irvine, CA (United States)

Sponsoring Organization:: USDOE; National Science Foundation (NSF); Defense Advanced Research Projects Agency (DARPA)

Grant/Contract Number:: AC02-05CH11231; N66001-16-2-4061; 1607111; R25GM055246; T34GM069337

OSTI ID:: 1525514

Alternate ID(s):: OSTI ID: 1903842

Journal Information:: Nucleic Acids Research, Vol. 47, Issue 13; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 23 works

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Web of Science

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Synthesis and Evolution of a Threose Nucleic Acid Aptamer Bearing 7-Deaza-7-Substituted Guanosine Residues Mei, Hui; Liao, Jen-Yu; Jimenez, Randi M. Journal of the American Chemical Society, Vol. 140, Issue 17 https://doi.org/10.1021/jacs.7b13031	journal	April 2018
“Skinny” and “Fat” DNA: Two New Double Helices Hoshika, Shuichi; Singh, Isha; Switzer, Christopher Journal of the American Chemical Society, Vol. 140, Issue 37 https://doi.org/10.1021/jacs.8b05042	journal	August 2018
A general strategy for expanding polymerase function by droplet microfluidics Larsen, Andrew C.; Dunn, Matthew R.; Hatch, Andrew Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11235	journal	April 2016
Evolution of a General RNA-Cleaving FANA Enzyme Wang, Yajun; Ngor, Arlene K.; Nikoomanzar, Ali Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07611-1	journal	November 2018
Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations Johnson, S. J.; Taylor, J. S.; Beese, L. S. Proceedings of the National Academy of Sciences, Vol. 100, Issue 7 https://doi.org/10.1073/pnas.0630532100	journal	March 2003
Enzymatic synthesis of DNA on glycerol nucleic acid templates without stable duplex formation between product and template Tsai, C. -H.; Chen, J.; Szostak, J. W. Proceedings of the National Academy of Sciences, Vol. 104, Issue 37 https://doi.org/10.1073/pnas.0704211104	journal	September 2007
Snapshots of a modified nucleotide moving through the confines of a DNA polymerase Kropp, Heike Maria; Dürr, Simon Leonard; Peter, Christine Proceedings of the National Academy of Sciences, Vol. 115, Issue 40 https://doi.org/10.1073/pnas.1811518115	journal	September 2018
Base Miscoding and Strand Misalignment Errors by Mutator Klenow Polymerases with Amino Acid Substitutions at Tyrosine 766 in the O Helix of the Fingers Subdomain Bell, Juliette B.; Eckert, Kristin A.; Joyce, Catherine M. Journal of Biological Chemistry, Vol. 272, Issue 11 https://doi.org/10.1074/jbc.272.11.7345	journal	March 1997
Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation Li, Y. The EMBO Journal, Vol. 17, Issue 24 https://doi.org/10.1093/emboj/17.24.7514	journal	December 1998
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Web 3DNA--a web server for the analysis, reconstruction, and visualization of three-dimensional nucleic-acid structures Zheng, G.; Lu, X. -J.; Olson, W. K. Nucleic Acids Research, Vol. 37, Issue Web Server https://doi.org/10.1093/nar/gkp358	journal	May 2009
Chemical discrimination between dC and 5Me dC via their hydroxylamine adducts Münzel, Martin; Lercher, Lukas; Müller, Markus Nucleic Acids Research, Vol. 38, Issue 21 https://doi.org/10.1093/nar/gkq724	journal	September 2010
The solution structure of double helical arabino nucleic acids (ANA and 2′F-ANA): effect of arabinoses in duplex-hairpin interconversion Martín-Pintado, Nerea; Yahyaee-Anzahaee, Maryam; Campos-Olivas, Ramón Nucleic Acids Research, Vol. 40, Issue 18 https://doi.org/10.1093/nar/gks672	journal	July 2012
The structural diversity of artificial genetic polymers Anosova, Irina; Kowal, Ewa A.; Dunn, Matthew R. Nucleic Acids Research, Vol. 44, Issue 3 https://doi.org/10.1093/nar/gkv1472	journal	December 2015
Synthesis and polymerase activity of a fluorescent cytidine TNA triphosphate analogue Mei, Hui; Shi, Changhua; Jimenez, Randi M. Nucleic Acids Research, Vol. 45, Issue 10 https://doi.org/10.1093/nar/gkx368	journal	May 2017
Polymerase Structures and Mechanism Pelletier, H. Science, Vol. 266, Issue 5193 https://doi.org/10.1126/science.7801132	journal	December 1994
Characterization of the aes gene of Escherichia coli encoding an enzyme with esterase activity. Peist, R.; Koch, A.; Bolek, P. Journal of Bacteriology, Vol. 179, Issue 24 https://doi.org/10.1128/jb.179.24.7679-7686.1997	journal	December 1997
Active Site Tightness and Substrate Fit in DNA Replication Kool, Eric T. Annual Review of Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1146/annurev.biochem.71.110601.135453	journal	June 2002
Efficient Reverse Transcription Using Locked Nucleic Acid Nucleotides towards the Evolution of Nuclease Resistant RNA Aptamers Crouzier, Lucile; Dubois, Camille; Edwards, Stacey L. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035990	journal	April 2012
Nucleoside Triphosphates — Building Blocks for the Modification of Nucleic Acids Hollenstein, Marcel Molecules, Vol. 17, Issue 11 https://doi.org/10.3390/molecules171113569	journal	November 2012
Crystal structures of DNA polymerase I capture novel intermediates in the DNA synthesis pathway Chim, Nicholas; Jackson, Lynnette N.; Trinh, Anh M. eLife, Vol. 7 https://doi.org/10.7554/elife.40444	journal	October 2018

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