Crucial Roles of Two Hydrated Mg2+ Ions in Reaction Catalysis of the Pistol Ribozyme

Teplova, Marianna; Falschlunger, Christoph; Krasheninina, Olga; Egger, Michaela; Ren, Aiming; Patel, Dinshaw J.; Micura, Ronald

doi:10.1002/anie.201912522

Title: Crucial Roles of Two Hydrated Mg²⁺ Ions in Reaction Catalysis of the Pistol Ribozyme

Abstract

Pistol ribozymes constitute a new class of small self-cleaving RNAs. Crystal structures have been solved, providing three-dimensional snapshots along the reaction coordinate of pistol phosphodiester cleavage, corresponding to the pre-catalytic state, a vanadate mimic of the transition state, and the product. The results led to the proposed underlying chemical mechanism. Importantly, a hydrated Mg²⁺ ion remains innersphere-coordinated to N7 of G33 in all three states, and is consistent with its likely role as acid in general acid base catalysis (δ and β catalysis). Strikingly, the new structures shed light on a second hydrated Mg²⁺ ion that approaches the scissile phosphate from its binding site in the pre-cleavage state to reach out for water-mediated hydrogen bonding in the cyclophosphate product. The major role of the second Mg²⁺ ion appears to be the stabilization of product conformation. This study delivers a mechanistic understanding of ribozyme-catalyzed backbone cleavage.

Authors:

Teplova, Marianna ^[1]; Falschlunger, Christoph ^[2]; Krasheninina, Olga ^[2]; Egger, Michaela ^[2]; Ren, Aiming ^[3]; Patel, Dinshaw J. ^[1];

^[2]

Memorial Sloan-Kettering Cancer Center, New York, NY (United States)
Leopold-Franzens Univ., Innsbruck (Austria)
Zhejiang Univ., Hangzhou (China)

Publication Date:: Thu Dec 05 00:00:00 EST 2019

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: Austrian Science Fund (FWF); The Austrian Research Promotion Agency (FFG); National Institutes of Health (NIH); National Natural Science Foundation of China (NSFC)

OSTI Identifier:: 1598035

Grant/Contract Number:: P27947; P31691; M2517; 858017; 1U19CA179564; P30CA008748

Resource Type:: Accepted Manuscript

Journal Name:: Angewandte Chemie (International Edition)

Additional Journal Information:: Journal Name: Angewandte Chemie (International Edition); Journal Volume: 59; Journal Issue: 7; Journal ID: ISSN 1433-7851

Publisher:: Wiley

Country of Publication:: United States

Language:: ENGLISH

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; magnesium; oligonucleotides; reaction mechanisms; RNA; structure–function relationships

Citation Formats


                    Teplova, Marianna, Falschlunger, Christoph, Krasheninina, Olga, Egger, Michaela, Ren, Aiming, Patel, Dinshaw J., and Micura, Ronald. Crucial Roles of Two Hydrated Mg2+ Ions in Reaction Catalysis of the Pistol Ribozyme.  United States: N. p., 2019. 
Web.  doi:10.1002/anie.201912522.

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                    Teplova, Marianna, Falschlunger, Christoph, Krasheninina, Olga, Egger, Michaela, Ren, Aiming, Patel, Dinshaw J., & Micura, Ronald. Crucial Roles of Two Hydrated Mg2+ Ions in Reaction Catalysis of the Pistol Ribozyme.  United States.  https://doi.org/10.1002/anie.201912522

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                    Teplova, Marianna, Falschlunger, Christoph, Krasheninina, Olga, Egger, Michaela, Ren, Aiming, Patel, Dinshaw J., and Micura, Ronald. Thu .  
"Crucial Roles of Two Hydrated Mg2+ Ions in Reaction Catalysis of the Pistol Ribozyme".  United States.  https://doi.org/10.1002/anie.201912522.  https://www.osti.gov/servlets/purl/1598035.

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@article{osti_1598035,

  title        = {Crucial Roles of Two Hydrated Mg2+ Ions in Reaction Catalysis of the Pistol Ribozyme},

  author       = {Teplova, Marianna and Falschlunger, Christoph and Krasheninina, Olga and Egger, Michaela and Ren, Aiming and Patel, Dinshaw J. and Micura, Ronald},

  abstractNote = {Pistol ribozymes constitute a new class of small self-cleaving RNAs. Crystal structures have been solved, providing three-dimensional snapshots along the reaction coordinate of pistol phosphodiester cleavage, corresponding to the pre-catalytic state, a vanadate mimic of the transition state, and the product. The results led to the proposed underlying chemical mechanism. Importantly, a hydrated Mg2+ ion remains innersphere-coordinated to N7 of G33 in all three states, and is consistent with its likely role as acid in general acid base catalysis (δ and β catalysis). Strikingly, the new structures shed light on a second hydrated Mg2+ ion that approaches the scissile phosphate from its binding site in the pre-cleavage state to reach out for water-mediated hydrogen bonding in the cyclophosphate product. The major role of the second Mg2+ ion appears to be the stabilization of product conformation. This study delivers a mechanistic understanding of ribozyme-catalyzed backbone cleavage.},

  doi          = {10.1002/anie.201912522},

  journal      = {Angewandte Chemie (International Edition)},

  number       = 7,

  volume       = 59,

  place        = {United States},

  year         = {Thu Dec 05 00:00:00 EST 2019},

  month        = {Thu Dec 05 00:00:00 EST 2019}

}

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Works referenced in this record:

Engineering of hairpin ribozyme variants for RNA recombination and splicing
journal, April 2019

Hieronymus, Robert; Müller, Sabine
Annals of the New York Academy of Sciences, Vol. 1447, Issue 1
DOI: 10.1111/nyas.14052

Comparative Enzymology and Structural Biology of RNA Self-Cleavage
journal, June 2009

Fedor, Martha J.
Annual Review of Biophysics, Vol. 38, Issue 1
DOI: 10.1146/annurev.biophys.050708.133710

Molecular simulations of the pistol ribozyme: unifying the interpretation of experimental data and establishing functional links with the hammerhead ribozyme
journal, July 2019

Kostenbader, Ken; York, Darrin M.
RNA, Vol. 25, Issue 11
DOI: 10.1261/rna.071944.119

Pseudoknot Formation Seeds the Twister Ribozyme Cleavage Reaction Coordinate
journal, June 2017

Vušurović, Nikola; Altman, Roger B.; Terry, Daniel S.
Journal of the American Chemical Society, Vol. 139, Issue 24
DOI: 10.1021/jacs.7b01549

Mg ²⁺ ions: do they bind to nucleobase nitrogens?
journal, December 2016

Leonarski, Filip; D'Ascenzo, Luigi; Auffinger, Pascal
Nucleic Acids Research, Vol. 45, Issue 2
DOI: 10.1093/nar/gkw1175

Chemistry and Biology of Self-Cleaving Ribozymes
journal, November 2015

Jimenez, Randi M.; Polanco, Julio A.; Lupták, Andrej
Trends in Biochemical Sciences, Vol. 40, Issue 11
DOI: 10.1016/j.tibs.2015.09.001

Atom-Specific Mutagenesis Reveals Structural and Catalytic Roles for an Active-Site Adenosine and Hydrated Mg ²⁺ in Pistol Ribozymes
journal, November 2017

Neuner, Sandro; Falschlunger, Christoph; Fuchs, Elisabeth
Angewandte Chemie International Edition, Vol. 56, Issue 50
DOI: 10.1002/anie.201708679

Pistol ribozyme adopts a pseudoknot fold facilitating site-specific in-line cleavage
journal, July 2016

Ren, Aiming; Vušurović, Nikola; Gebetsberger, Jennifer
Nature Chemical Biology, Vol. 12, Issue 9
DOI: 10.1038/nchembio.2125

Structural basis for the fast self-cleavage reaction catalyzed by the twister ribozyme
journal, August 2014

Eiler, D.; Wang, J.; Steitz, T. A.
Proceedings of the National Academy of Sciences, Vol. 111, Issue 36
DOI: 10.1073/pnas.1414571111

An Ontology for Facilitating Discussion of Catalytic Strategies of RNA-Cleaving Enzymes
journal, May 2019

Bevilacqua, Philip C.; Harris, Michael E.; Piccirilli, Joseph A.
ACS Chemical Biology, Vol. 14, Issue 6
DOI: 10.1021/acschembio.9b00202

Unwinding the twister ribozyme: from structure to mechanism: Unwinding the twister ribozyme
journal, November 2016

Gebetsberger, Jennifer; Micura, Ronald
Wiley Interdisciplinary Reviews: RNA, Vol. 8, Issue 3
DOI: 10.1002/wrna.1402

Small Self-cleaving Ribozymes
journal, September 2010

Ferre-D'Amare, A. R.; Scott, W. G.
Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 10
DOI: 10.1101/cshperspect.a003574

Comparison of the Structures and Mechanisms of the Pistol and Hammerhead Ribozymes
journal, April 2019

Wilson, Timothy J.; Liu, Yijin; Li, Nan-Sheng
Journal of the American Chemical Society, Vol. 141, Issue 19
DOI: 10.1021/jacs.9b02141

A common speed limit for RNA-cleaving ribozymes and deoxyribozymes
journal, August 2003

Breaker, R. R.
RNA, Vol. 9, Issue 8
DOI: 10.1261/rna.5670703

Thio Effects and an Unconventional Metal Ion Rescue in the Genomic Hepatitis Delta Virus Ribozyme
journal, September 2013

Thaplyal, Pallavi; Ganguly, Abir; Golden, Barbara L.
Biochemistry, Vol. 52, Issue 37
DOI: 10.1021/bi4000673

Model for General Acid−Base Catalysis by the Hammerhead Ribozyme: pH−Activity Relationships of G8 and G12 Variants at the Putative Active Site ^†
journal, May 2005

Han, Joonhee; Burke, John M.
Biochemistry, Vol. 44, Issue 21
DOI: 10.1021/bi047941z

New classes of self-cleaving ribozymes revealed by comparative genomics analysis
journal, July 2015

Weinberg, Zasha; Kim, Peter B.; Chen, Tony H.
Nature Chemical Biology, Vol. 11, Issue 8
DOI: 10.1038/nchembio.1846

Transition State Stabilization by a Catalytic RNA
journal, October 2002

Rupert, P. B.
Science, Vol. 298, Issue 5597
DOI: 10.1126/science.1076093

Nucleobase catalysis in ribozyme mechanism
journal, October 2006

Bevilacqua, P.; Yajima, R.
Current Opinion in Chemical Biology, Vol. 10, Issue 5
DOI: 10.1016/j.cbpa.2006.08.014

A Mini-Twister Variant and Impact of Residues/Cations on the Phosphodiester Cleavage of this Ribozyme Class
journal, October 2015

Košutić, Marija; Neuner, Sandro; Ren, Aiming
Angewandte Chemie International Edition, Vol. 54, Issue 50
DOI: 10.1002/anie.201506601

Structure-based insights into self-cleavage by a four-way junctional twister-sister ribozyme
journal, October 2017

Zheng, Luqian; Mairhofer, Elisabeth; Teplova, Marianna
Nature Communications, Vol. 8, Issue 1
DOI: 10.1038/s41467-017-01276-y

Catalytic Strategies of Self-Cleaving Ribozymes
journal, August 2008

Cochrane, Jesse C.; Strobel, Scott A.
Accounts of Chemical Research, Vol. 41, Issue 8
DOI: 10.1021/ar800050c

Biochemical analysis of pistol self-cleaving ribozymes
journal, September 2015

Harris, Kimberly A.; Lünse, Christina E.; Li, Sanshu
RNA, Vol. 21, Issue 11
DOI: 10.1261/rna.052514.115

Crystal structure and mechanistic investigation of the twister ribozyme
journal, July 2014

Liu, Yijin; Wilson, Timothy J.; McPhee, Scott A.
Nature Chemical Biology, Vol. 10, Issue 9
DOI: 10.1038/nchembio.1587

A widespread self-cleaving ribozyme class is revealed by bioinformatics
journal, November 2013

Roth, Adam; Weinberg, Zasha; Chen, Andy G. Y.
Nature Chemical Biology, Vol. 10, Issue 1
DOI: 10.1038/nchembio.1386

The structure of a nucleolytic ribozyme that employs a catalytic metal ion
journal, March 2017

Liu, Yijin; Wilson, Timothy J.; Lilley, David M. J.
Nature Chemical Biology, Vol. 13, Issue 5
DOI: 10.1038/nchembio.2333

The amazing world of bacterial structured RNAs
journal, January 2010

Westhof, Eric
Genome Biology, Vol. 11, Issue 3
DOI: 10.1186/gb-2010-11-3-108

Hatchet ribozyme structure and implications for cleavage mechanism
journal, May 2019

Zheng, Luqian; Falschlunger, Christoph; Huang, Kaiyi
Proceedings of the National Academy of Sciences, Vol. 116, Issue 22
DOI: 10.1073/pnas.1902413116

Two Active Site Divalent Ions in the Crystal Structure of the Hammerhead Ribozyme Bound to a Transition State Analogue
journal, January 2016

Mir, Aamir; Golden, Barbara L.
Biochemistry, Vol. 55, Issue 4
DOI: 10.1021/acs.biochem.5b01139

Mechanistic Debris Generated by Twister Ribozymes
journal, February 2017

Breaker, Ronald R.
ACS Chemical Biology, Vol. 12, Issue 4
DOI: 10.1021/acschembio.7b00010

General Acid–Base Catalysis Mediated by Nucleobases in the Hairpin Ribozyme
journal, September 2012

Kath-Schorr, Stephanie; Wilson, Timothy J.; Li, Nan-Sheng
Journal of the American Chemical Society, Vol. 134, Issue 40
DOI: 10.1021/ja3067429

In-line alignment and Mg2+ coordination at the cleavage site of the env22 twister ribozyme
journal, November 2014

Ren, Aiming; Košutić, Marija; Rajashankar, Kanagalaghatta R.
Nature Communications, Vol. 5, Issue 1
DOI: 10.1038/ncomms6534

Atom-Specific Mutagenesis Reveals Structural and Catalytic Roles for an Active-Site Adenosine and Hydrated Mg ²⁺ in Pistol Ribozymes
journal, November 2017

Neuner, Sandro; Falschlunger, Christoph; Fuchs, Elisabeth
Angewandte Chemie, Vol. 129, Issue 50
DOI: 10.1002/ange.201708679

Structure-based mechanistic insights into catalysis by small self-cleaving ribozymes
journal, December 2017

Ren, Aiming; Micura, Ronald; Patel, Dinshaw J.
Current Opinion in Chemical Biology, Vol. 41
DOI: 10.1016/j.cbpa.2017.09.017

Ligand-dependent ribozymes: Ligand-dependent ribozymes
journal, September 2016

Felletti, Michele; Hartig, Jörg S.
Wiley Interdisciplinary Reviews: RNA, Vol. 8, Issue 2
DOI: 10.1002/wrna.1395

Crystal structure of Pistol, a class of self-cleaving ribozyme
journal, January 2017

Nguyen, Laura A.; Wang, Jimin; Steitz, Thomas A.
Proceedings of the National Academy of Sciences, Vol. 114, Issue 5
DOI: 10.1073/pnas.1611191114

A comparison of vanadate to a 2'-5' linkage at the active site of a small ribozyme suggests a role for water in transition-state stabilization
journal, July 2007

Torelli, A. T.; Krucinska, J.; Wedekind, J. E.
RNA, Vol. 13, Issue 7
DOI: 10.1261/rna.510807

Modulating RNA structure and catalysis: lessons from small cleaving ribozymes
journal, August 2009

Reymond, Cedric; Beaudoin, Jean-Denis; Perreault, Jean-Pierre
Cellular and Molecular Life Sciences, Vol. 66, Issue 24
DOI: 10.1007/s00018-009-0124-1

A Mini-Twister Variant and Impact of Residues/Cations on the Phosphodiester Cleavage of this Ribozyme Class
journal, October 2015

Košutić, Marija; Neuner, Sandro; Ren, Aiming
Angewandte Chemie, Vol. 127, Issue 50
DOI: 10.1002/ange.201506601

Efficient access to N-trifluoroacetylated 2′-amino-2′-deoxyadenosine phosphoramidite for RNA solid-phase synthesis
journal, April 2019

Falschlunger, Christoph; Micura, Ronald
Monatshefte für Chemie - Chemical Monthly, Vol. 150, Issue 5
DOI: 10.1007/s00706-019-02390-x

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Title: Crucial Roles of Two Hydrated Mg2+ Ions in Reaction Catalysis of the Pistol Ribozyme

Abstract

Citation Formats

Engineering of hairpin ribozyme variants for RNA recombination and splicing journal, April 2019

Comparative Enzymology and Structural Biology of RNA Self-Cleavage journal, June 2009

Molecular simulations of the pistol ribozyme: unifying the interpretation of experimental data and establishing functional links with the hammerhead ribozyme journal, July 2019

Pseudoknot Formation Seeds the Twister Ribozyme Cleavage Reaction Coordinate journal, June 2017

Mg 2+ ions: do they bind to nucleobase nitrogens? journal, December 2016

Chemistry and Biology of Self-Cleaving Ribozymes journal, November 2015

Atom-Specific Mutagenesis Reveals Structural and Catalytic Roles for an Active-Site Adenosine and Hydrated Mg 2+ in Pistol Ribozymes journal, November 2017

Pistol ribozyme adopts a pseudoknot fold facilitating site-specific in-line cleavage journal, July 2016

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An Ontology for Facilitating Discussion of Catalytic Strategies of RNA-Cleaving Enzymes journal, May 2019

Unwinding the twister ribozyme: from structure to mechanism: Unwinding the twister ribozyme journal, November 2016

Small Self-cleaving Ribozymes journal, September 2010

Comparison of the Structures and Mechanisms of the Pistol and Hammerhead Ribozymes journal, April 2019

A common speed limit for RNA-cleaving ribozymes and deoxyribozymes journal, August 2003

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Structure-based mechanistic insights into catalysis by small self-cleaving ribozymes journal, December 2017

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A comparison of vanadate to a 2'-5' linkage at the active site of a small ribozyme suggests a role for water in transition-state stabilization journal, July 2007

Modulating RNA structure and catalysis: lessons from small cleaving ribozymes journal, August 2009

A Mini-Twister Variant and Impact of Residues/Cations on the Phosphodiester Cleavage of this Ribozyme Class journal, October 2015

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Title: Crucial Roles of Two Hydrated Mg²⁺ Ions in Reaction Catalysis of the Pistol Ribozyme

Engineering of hairpin ribozyme variants for RNA recombination and splicing
journal, April 2019

Comparative Enzymology and Structural Biology of RNA Self-Cleavage
journal, June 2009

Molecular simulations of the pistol ribozyme: unifying the interpretation of experimental data and establishing functional links with the hammerhead ribozyme
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Chemistry and Biology of Self-Cleaving Ribozymes
journal, November 2015

Atom-Specific Mutagenesis Reveals Structural and Catalytic Roles for an Active-Site Adenosine and Hydrated Mg ²⁺ in Pistol Ribozymes
journal, November 2017

Pistol ribozyme adopts a pseudoknot fold facilitating site-specific in-line cleavage
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Unwinding the twister ribozyme: from structure to mechanism: Unwinding the twister ribozyme
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journal, April 2019

A common speed limit for RNA-cleaving ribozymes and deoxyribozymes
journal, August 2003

Thio Effects and an Unconventional Metal Ion Rescue in the Genomic Hepatitis Delta Virus Ribozyme
journal, September 2013

Model for General Acid−Base Catalysis by the Hammerhead Ribozyme: pH−Activity Relationships of G8 and G12 Variants at the Putative Active Site ^†
journal, May 2005

New classes of self-cleaving ribozymes revealed by comparative genomics analysis
journal, July 2015

Transition State Stabilization by a Catalytic RNA
journal, October 2002

Nucleobase catalysis in ribozyme mechanism
journal, October 2006

A Mini-Twister Variant and Impact of Residues/Cations on the Phosphodiester Cleavage of this Ribozyme Class
journal, October 2015

Structure-based insights into self-cleavage by a four-way junctional twister-sister ribozyme
journal, October 2017

Catalytic Strategies of Self-Cleaving Ribozymes
journal, August 2008

Biochemical analysis of pistol self-cleaving ribozymes
journal, September 2015

Crystal structure and mechanistic investigation of the twister ribozyme
journal, July 2014

A widespread self-cleaving ribozyme class is revealed by bioinformatics
journal, November 2013

The structure of a nucleolytic ribozyme that employs a catalytic metal ion
journal, March 2017

The amazing world of bacterial structured RNAs
journal, January 2010

Hatchet ribozyme structure and implications for cleavage mechanism
journal, May 2019

Two Active Site Divalent Ions in the Crystal Structure of the Hammerhead Ribozyme Bound to a Transition State Analogue
journal, January 2016

Mechanistic Debris Generated by Twister Ribozymes
journal, February 2017

General Acid–Base Catalysis Mediated by Nucleobases in the Hairpin Ribozyme
journal, September 2012

In-line alignment and Mg2+ coordination at the cleavage site of the env22 twister ribozyme
journal, November 2014

Atom-Specific Mutagenesis Reveals Structural and Catalytic Roles for an Active-Site Adenosine and Hydrated Mg ²⁺ in Pistol Ribozymes
journal, November 2017

Structure-based mechanistic insights into catalysis by small self-cleaving ribozymes
journal, December 2017

Ligand-dependent ribozymes: Ligand-dependent ribozymes
journal, September 2016

Crystal structure of Pistol, a class of self-cleaving ribozyme
journal, January 2017

A comparison of vanadate to a 2'-5' linkage at the active site of a small ribozyme suggests a role for water in transition-state stabilization
journal, July 2007

Modulating RNA structure and catalysis: lessons from small cleaving ribozymes
journal, August 2009

A Mini-Twister Variant and Impact of Residues/Cations on the Phosphodiester Cleavage of this Ribozyme Class
journal, October 2015

Efficient access to N-trifluoroacetylated 2′-amino-2′-deoxyadenosine phosphoramidite for RNA solid-phase synthesis
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