Structural basis for the evolution of cyclic phosphodiesterase activity in the U6 snRNA exoribonuclease Usb1
Abstract
U6 snRNA undergoes post-transcriptional 3' end modification prior to incorporation into the active site of spliceosomes. The responsible exoribonuclease is Usb1, which removes nucleotides from the 3' end of U6 and, in humans, leaves a 2',3' cyclic phosphate that is recognized by the Lsm2–8 complex. Saccharomycescerevisiae Usb1 has additional 2',3' cyclic phosphodiesterase (CPDase) activity, which converts the cyclic phosphate into a 3' phosphate group. Here we investigate the molecular basis for the evolution of Usb1 CPDase activity. We examine the structure and function of Usb1 from Kluyveromyces marxianus, which shares 25 and 19% sequence identity to the S. cerevisiae and Homo sapiens orthologs of Usb1, respectively. We show that K. marxianus Usb1 enzyme has CPDase activity and determined its structure, free and bound to the substrate analog uridine 5'-monophosphate. We find that the origin of CPDase activity is related to a loop structure that is conserved in yeast and forms a distinct penultimate (n – 1) nucleotide binding site. These data provide structural and mechanistic insight into the evolutionary divergence of Usb1 catalysis.
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH)
- OSTI Identifier:
- 1603143
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 48; Journal Issue: 3; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Nomura, Yuichiro, Montemayor, Eric J., Virta, Johanna M., Hayes, Samuel M., and Butcher, Samuel E. Structural basis for the evolution of cyclic phosphodiesterase activity in the U6 snRNA exoribonuclease Usb1. United States: N. p., 2019.
Web. doi:10.1093/nar/gkz1177.
Nomura, Yuichiro, Montemayor, Eric J., Virta, Johanna M., Hayes, Samuel M., & Butcher, Samuel E. Structural basis for the evolution of cyclic phosphodiesterase activity in the U6 snRNA exoribonuclease Usb1. United States. https://doi.org/10.1093/nar/gkz1177
Nomura, Yuichiro, Montemayor, Eric J., Virta, Johanna M., Hayes, Samuel M., and Butcher, Samuel E. Fri .
"Structural basis for the evolution of cyclic phosphodiesterase activity in the U6 snRNA exoribonuclease Usb1". United States. https://doi.org/10.1093/nar/gkz1177. https://www.osti.gov/servlets/purl/1603143.
@article{osti_1603143,
title = {Structural basis for the evolution of cyclic phosphodiesterase activity in the U6 snRNA exoribonuclease Usb1},
author = {Nomura, Yuichiro and Montemayor, Eric J. and Virta, Johanna M. and Hayes, Samuel M. and Butcher, Samuel E.},
abstractNote = {U6 snRNA undergoes post-transcriptional 3' end modification prior to incorporation into the active site of spliceosomes. The responsible exoribonuclease is Usb1, which removes nucleotides from the 3' end of U6 and, in humans, leaves a 2',3' cyclic phosphate that is recognized by the Lsm2–8 complex. Saccharomycescerevisiae Usb1 has additional 2',3' cyclic phosphodiesterase (CPDase) activity, which converts the cyclic phosphate into a 3' phosphate group. Here we investigate the molecular basis for the evolution of Usb1 CPDase activity. We examine the structure and function of Usb1 from Kluyveromyces marxianus, which shares 25 and 19% sequence identity to the S. cerevisiae and Homo sapiens orthologs of Usb1, respectively. We show that K. marxianus Usb1 enzyme has CPDase activity and determined its structure, free and bound to the substrate analog uridine 5'-monophosphate. We find that the origin of CPDase activity is related to a loop structure that is conserved in yeast and forms a distinct penultimate (n – 1) nucleotide binding site. These data provide structural and mechanistic insight into the evolutionary divergence of Usb1 catalysis.},
doi = {10.1093/nar/gkz1177},
journal = {Nucleic Acids Research},
number = 3,
volume = 48,
place = {United States},
year = {Fri Dec 13 00:00:00 EST 2019},
month = {Fri Dec 13 00:00:00 EST 2019}
}
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Works referenced in this record:
Proteome survey reveals modularity of the yeast cell machinery
journal, January 2006
- Gavin, Anne-Claude; Aloy, Patrick; Grandi, Paola
- Nature, Vol. 440, Issue 7084
Human Mpn1 promotes post-transcriptional processing and stability of U6atac
journal, July 2015
- Shchepachev, Vadim; Wischnewski, Harry; Soneson, Charlotte
- FEBS Letters, Vol. 589, Issue 18
Purified lupus antigen la recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts
journal, January 1984
- Stefano, J.
- Cell, Vol. 36, Issue 1
HKL2MAP : a graphical user interface for macromolecular phasing with SHELX programs
journal, September 2004
- Pape, Thomas; Schneider, Thomas R.
- Journal of Applied Crystallography, Vol. 37, Issue 5
Advances in automated data analysis and processing within autoPROC , combined with improved characterisation, mitigation and visualisation of the anisotropy of diffraction limits using STARANISO
journal, July 2018
- Vonrhein, Clemens; Tickle, Ian J.; Flensburg, Claus
- Acta Crystallographica Section A Foundations and Advances, Vol. 74, Issue a1
Aberrant 3′ oligoadenylation of spliceosomal U6 small nuclear RNA in poikiloderma with neutropenia
journal, February 2013
- Hilcenko, Christine; Simpson, Paul J.; Finch, Andrew J.
- Blood, Vol. 121, Issue 6
C16orf57, a gene mutated in poikiloderma with neutropenia, encodes a putative phosphodiesterase responsible for the U6 snRNA 3' end modification
journal, August 2012
- Mroczek, S.; Krwawicz, J.; Kutner, J.
- Genes & Development, Vol. 26, Issue 17
High-Quality Binary Protein Interaction Map of the Yeast Interactome Network
journal, October 2008
- Yu, H.; Braun, P.; Yildirim, M. A.
- Science, Vol. 322, Issue 5898
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
A short history of SHELX
journal, December 2007
- Sheldrick, George M.
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122
Structure and mechanism of activity of the cyclic phosphodiesterase of Appr>p, a product of the tRNA splicing reaction
journal, November 2000
- Hofmann, A.
- The EMBO Journal, Vol. 19, Issue 22
Structural and mechanistic basis for preferential deadenylation of U6 snRNA by Usb1
journal, September 2018
- Nomura, Yuichiro; Roston, Daniel; Montemayor, Eric J.
- Nucleic Acids Research, Vol. 46, Issue 21
Determinants of ligand binding and catalytic activity in the myelin enzyme 2′,3′-cyclic nucleotide 3′-phosphodiesterase
journal, November 2015
- Raasakka, Arne; Myllykoski, Matti; Laulumaa, Saara
- Scientific Reports, Vol. 5, Issue 1
Heavy-atom derivatization
journal, October 2003
- Garman, Elspeth; Murray, James W.
- Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 11
Molecular evidence for an ancient duplication of the entire yeast genome
journal, June 1997
- Wolfe, Kenneth H.; Shields, Denis C.
- Nature, Vol. 387, Issue 6634
AKAP18 Contains a Phosphoesterase Domain that Binds AMP
journal, February 2008
- Gold, Matthew G.; Smith, F. Donelson; Scott, John D.
- Journal of Molecular Biology, Vol. 375, Issue 5
3'-cyclic phosphorylation of U6 snRNA leads to recruitment of recycling factor p110 through LSm proteins
journal, June 2008
- Licht, K.; Medenbach, J.; Luhrmann, R.
- RNA, Vol. 14, Issue 8
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
Crystallographic Analysis of the Reaction Cycle of 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase, a Unique Member of the 2H Phosphoesterase Family
journal, November 2013
- Myllykoski, Matti; Raasakka, Arne; Lehtimäki, Mari
- Journal of Molecular Biology, Vol. 425, Issue 22
Energetics of Catalysis by Ribonucleases: Fate of the 2',3'-Cyclic Phosphodiester Intermediate
journal, June 1994
- Thompson, James E.; Venegas, Fernando D.; Raines, Ronald T.
- Biochemistry, Vol. 33, Issue 23
Mpn1, Mutated in Poikiloderma with Neutropenia Protein 1, Is a Conserved 3′-to-5′ RNA Exonuclease Processing U6 Small Nuclear RNA
journal, October 2012
- Shchepachev, Vadim; Wischnewski, Harry; Missiaglia, Edoardo
- Cell Reports, Vol. 2, Issue 4
Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012
- Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
- Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Structure and mechanism of E. coli RNA 2′,3′-cyclic phosphodiesterase
journal, September 2014
- Remus, Barbara S.; Jacewicz, Agata; Shuman, Stewart
- RNA, Vol. 20, Issue 11
The life of U6 small nuclear RNA, from cradle to grave
journal, January 2018
- Didychuk, Allison L.; Butcher, Samuel E.; Brow, David A.
- RNA, Vol. 24, Issue 4
Architecture of the U6 snRNP reveals specific recognition of 3′-end processed U6 snRNA
journal, May 2018
- Montemayor, Eric J.; Didychuk, Allison L.; Yake, Allyson D.
- Nature Communications, Vol. 9, Issue 1
Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily
journal, December 2002
- Mazumder, R.
- Nucleic Acids Research, Vol. 30, Issue 23
Myelin 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase: Active-Site Ligand Binding and Molecular Conformation
journal, February 2012
- Myllykoski, Matti; Raasakka, Arne; Han, Huijong
- PLoS ONE, Vol. 7, Issue 2
Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency
journal, December 2001
- Kapust, Rachel B.; Tözsér, József; Fox, Jeffrey D.
- Protein Engineering, Design and Selection, Vol. 14, Issue 12
Cryo-electron microscopy snapshots of the spliceosome: structural insights into a dynamic ribonucleoprotein machine
journal, October 2017
- Fica, Sebastian M.; Nagai, Kiyoshi
- Nature Structural & Molecular Biology, Vol. 24, Issue 10
The structure of Pyrococcus horikoshii 2′-5′ RNA ligase at 1.94 Å resolution reveals a possible open form with a wider active-site cleft
journal, November 2006
- Gao, Yong-Gui; Yao, Min; Okada, Ayuko
- Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 62, Issue 12
π-Stacking Interactions: ALIVE AND WELL IN PROTEINS
journal, June 1998
- McGaughey, Georgia B.; Gagné, Marc; Rappé, Anthony K.
- Journal of Biological Chemistry, Vol. 273, Issue 25
Usb1 controls U6 snRNP assembly through evolutionarily divergent cyclic phosphodiesterase activities
journal, September 2017
- Didychuk, Allison L.; Montemayor, Eric J.; Carrocci, Tucker J.
- Nature Communications, Vol. 8, Issue 1
The 2′-5′ RNA Ligase of Escherichia coli: PURIFICATION, CLONING, AND GENOMIC DISRUPTION
journal, December 1996
- Arn, Eric A.; Abelson, John N.
- Journal of Biological Chemistry, Vol. 271, Issue 49
XDS
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
Identification, cloning, and functional analysis of the human U6 snRNA-specific terminal uridylyl transferase
journal, June 2006
- Trippe, R.
- RNA, Vol. 12, Issue 8
Global landscape of protein complexes in the yeast Saccharomyces cerevisiae
journal, March 2006
- Krogan, Nevan J.; Cagney, Gerard; Yu, Haiyuan
- Nature, Vol. 440, Issue 7084
U6 small nuclear RNA is transcribed by RNA polymerase III.
journal, November 1986
- Kunkel, G. R.; Maser, R. L.; Calvet, J. P.
- Proceedings of the National Academy of Sciences, Vol. 83, Issue 22
Assigning Function to Yeast Proteins by Integration of Technologies
journal, December 2003
- Hazbun, Tony R.; Malmström, Lars; Anderson, Scott
- Molecular Cell, Vol. 12, Issue 6
Structural aspects of nucleotide ligand binding by a bacterial 2H phosphoesterase
journal, January 2017
- Myllykoski, Matti; Kursula, Petri
- PLOS ONE, Vol. 12, Issue 1
Targeted Next-Generation Sequencing Appoints C16orf57 as Clericuzio-Type Poikiloderma with Neutropenia Gene
journal, January 2010
- Volpi, Ludovica; Roversi, Gaia; Colombo, Elisa Adele
- The American Journal of Human Genetics, Vol. 86, Issue 1
Myelin 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase: Active-Site Ligand Binding and Molecular Conformation
text, January 2012
- Myllykoski, Matti; Raasakka, Arne; Han, Huijong
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Targeted Next-Generation Sequencing Appoints C16orf57 as Clericuzio-Type Poikiloderma with Neutropenia Gene
journal, September 2010
- Volpi, Ludovica; Roversi, Gaia; Colombo, Elisa Adele
- The American Journal of Human Genetics, Vol. 87, Issue 3
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021
- Tillu, Vikas A.; Rae, James; Gao, Ya
- Nature Communications, Vol. 12, Issue 1
Architecture of the U6 snRNP reveals specific recognition of 3′-end processed U6 snRNA
journal, July 2018
- Montemayor, Eric J.; Didychuk, Allison L.; Yake, Allyson D.
- Acta Crystallographica Section A Foundations and Advances, Vol. 74, Issue a1
Overview of the CCP4 suite and current developments.
text, January 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Apollo - University of Cambridge Repository
Structural aspects of nucleotide ligand binding by a bacterial 2H phosphoesterase
text, January 2017
- Myllykoski, Matti; Kursula, Petri
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Mpn1, Mutated in Poikiloderma with Neutropenia Protein 1, Is a Conserved 3′-to-5′ RNA Exonuclease Processing U6 Small Nuclear RNA
text, January 2012
- Shchepachev, Vadim; Wischnewski, Harry; Missiaglia, Edoardo
- ETH Zurich
Mammalian U6 small nuclear RNA undergoes 3' end modifications within the spliceosome
journal, March 1993
- Tazi, J.; Forne, T.; Jeanteur, P.
- Molecular and Cellular Biology, Vol. 13, Issue 3
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Targeted Next-Generation Sequencing Appoints C16orf57 as Clericuzio-Type Poikiloderma with Neutropenia Gene
journal, January 2010
- Volpi, Ludovica; Roversi, Gaia; Colombo, Elisa Adele
- The American Journal of Human Genetics, Vol. 86, Issue 1
Human Mpn1 promotes post-transcriptional processing and stability of U6atac
journal, July 2015
- Shchepachev, Vadim; Wischnewski, Harry; Soneson, Charlotte
- FEBS Letters, Vol. 589, Issue 18
AKAP18 Contains a Phosphoesterase Domain that Binds AMP
journal, February 2008
- Gold, Matthew G.; Smith, F. Donelson; Scott, John D.
- Journal of Molecular Biology, Vol. 375, Issue 5
Crystallographic Analysis of the Reaction Cycle of 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase, a Unique Member of the 2H Phosphoesterase Family
journal, November 2013
- Myllykoski, Matti; Raasakka, Arne; Lehtimäki, Mari
- Journal of Molecular Biology, Vol. 425, Issue 22
Crystal Structure of the 2′-5′ RNA Ligase from Thermus thermophilus HB8
journal, June 2003
- Kato, Miyuki; Shirouzu, Mikako; Terada, Takaho
- Journal of Molecular Biology, Vol. 329, Issue 5
Energetics of Catalysis by Ribonucleases: Fate of the 2',3'-Cyclic Phosphodiester Intermediate
journal, June 1994
- Thompson, James E.; Venegas, Fernando D.; Raines, Ronald T.
- Biochemistry, Vol. 33, Issue 23
Global landscape of protein complexes in the yeast Saccharomyces cerevisiae
journal, March 2006
- Krogan, Nevan J.; Cagney, Gerard; Yu, Haiyuan
- Nature, Vol. 440, Issue 7084
Usb1 controls U6 snRNP assembly through evolutionarily divergent cyclic phosphodiesterase activities
journal, September 2017
- Didychuk, Allison L.; Montemayor, Eric J.; Carrocci, Tucker J.
- Nature Communications, Vol. 8, Issue 1
Determinants of ligand binding and catalytic activity in the myelin enzyme 2′,3′-cyclic nucleotide 3′-phosphodiesterase
journal, November 2015
- Raasakka, Arne; Myllykoski, Matti; Laulumaa, Saara
- Scientific Reports, Vol. 5, Issue 1
U6 small nuclear RNA is transcribed by RNA polymerase III.
journal, November 1986
- Kunkel, G. R.; Maser, R. L.; Calvet, J. P.
- Proceedings of the National Academy of Sciences, Vol. 83, Issue 22
Crystal Structures of the Semireduced and Inhibitor-bound Forms of Cyclic Nucleotide Phosphodiesterase from Arabidopsis thaliana
journal, November 2001
- Hofmann, Andreas; Grella, Melissa; Botos, Istvan
- Journal of Biological Chemistry, Vol. 277, Issue 2
Structure and mechanism of activity of the cyclic phosphodiesterase of Appr>p, a product of the tRNA splicing reaction
journal, November 2000
- Hofmann, A.
- The EMBO Journal, Vol. 19, Issue 22
Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily
journal, December 2002
- Mazumder, R.
- Nucleic Acids Research, Vol. 30, Issue 23
Structural and mechanistic basis for preferential deadenylation of U6 snRNA by Usb1
journal, September 2018
- Nomura, Yuichiro; Roston, Daniel; Montemayor, Eric J.
- Nucleic Acids Research, Vol. 46, Issue 21
Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency
journal, December 2001
- Kapust, Rachel B.; Tözsér, József; Fox, Jeffrey D.
- Protein Engineering, Design and Selection, Vol. 14, Issue 12
C16orf57, a gene mutated in poikiloderma with neutropenia, encodes a putative phosphodiesterase responsible for the U6 snRNA 3' end modification
journal, August 2012
- Mroczek, S.; Krwawicz, J.; Kutner, J.
- Genes & Development, Vol. 26, Issue 17
How good are my data and what is the resolution?
journal, June 2013
- Evans, Philip R.; Murshudov, Garib N.
- Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7
Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997
- Murshudov, G. N.; Vagin, A. A.; Dodson, E. J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3
Mammalian U6 small nuclear RNA undergoes 3' end modifications within the spliceosome.
journal, March 1993
- Tazi, J.; Forne, T.; Jeanteur, P.
- Molecular and Cellular Biology, Vol. 13, Issue 3
Poikiloderma with neutropenia: beginning at the end
journal, February 2013
- Mason, Philip J.; Bessler, Monica
- Blood, Vol. 121, Issue 6
Structure and mechanism of E. coli RNA 2′,3′-cyclic phosphodiesterase
journal, September 2014
- Remus, Barbara S.; Jacewicz, Agata; Shuman, Stewart
- RNA, Vol. 20, Issue 11
The life of U6 small nuclear RNA, from cradle to grave
journal, January 2018
- Didychuk, Allison L.; Butcher, Samuel E.; Brow, David A.
- RNA, Vol. 24, Issue 4
3'-cyclic phosphorylation of U6 snRNA leads to recruitment of recycling factor p110 through LSm proteins
journal, June 2008
- Licht, K.; Medenbach, J.; Luhrmann, R.
- RNA, Vol. 14, Issue 8
Structural aspects of nucleotide ligand binding by a bacterial 2H phosphoesterase
journal, January 2017
- Myllykoski, Matti; Kursula, Petri
- PLOS ONE, Vol. 12, Issue 1
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Mpn1, Mutated in Poikiloderma with Neutropenia Protein 1, Is a Conserved 3′-to-5′ RNA Exonuclease Processing U6 Small Nuclear RNA
text, January 2012
- Shchepachev, Vadim; Wischnewski, Harry; Missiaglia, Edoardo
- ETH Zurich