Structural and mechanistic basis of mammalian Nudt12 RNA deNADding

Grudzien-Nogalska, Ewa; Wu, Yixuan; Jiao, Xinfu; Cui, Huijuan; Mateyak, Maria K.; Hart, Ronald P.; Tong, Liang; Kiledjian, Megerditch

doi:10.1038/s41589-019-0293-7

Title: Structural and mechanistic basis of mammalian Nudt12 RNA deNADding

Abstract

We recently demonstrated that mammalian cells harbor nicotinamide adenine dinucleotide (NAD)-capped messenger RNAs that are hydrolyzed by the DXO deNADding enzyme. Here, we report that the Nudix protein Nudt12 is a second mammalian deNADding enzyme structurally and mechanistically distinct from DXO and targeting different RNAs. Here, the crystal structure of mouse Nudt12 in complex with the deNADding product AMP and three Mg²⁺ ions at 1.6 Å resolution provides insights into the molecular basis of the deNADding activity in the NAD pyrophosphate. Disruption of the Nudt12 gene stabilizes transfected NAD-capped RNA in cells, and its endogenous NAD-capped mRNA targets are enriched in those encoding proteins involved in cellular energetics. Furthermore, exposure of cells to nutrient or environmental stress manifests changes in NAD-capped RNA levels that are selectively responsive to Nudt12 or DXO, respectively, indicating an association of deNADding to cellular metabolism.

Authors:

Grudzien-Nogalska, Ewa ^[1]; Wu, Yixuan ^[2]; Jiao, Xinfu ^[1]; Cui, Huijuan ^[1]; Mateyak, Maria K. ^[1]; Hart, Ronald P. ^[1];

^[2];

^[1]

Rutgers Univ., Piscataway, NJ (United States)
Columbia Univ., New York, NY (United States)

Publication Date:: 2019-05-17

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH); NIH-ORIP HEI

OSTI Identifier:: 1531008

Grant/Contract Number:: AC02-06CH11357; GM118093; S10OD012018; GM126488; P41 GM103403; S10 RR029205

Resource Type:: Accepted Manuscript

Journal Name:: Nature Chemical Biology

Additional Journal Information:: Journal Volume: 15; Journal Issue: 6; Journal ID: ISSN 1552-4450

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: ENGLISH

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Enzymes; RNA; X-ray crystallography

Citation Formats


                    Grudzien-Nogalska, Ewa, Wu, Yixuan, Jiao, Xinfu, Cui, Huijuan, Mateyak, Maria K., Hart, Ronald P., Tong, Liang, and Kiledjian, Megerditch. Structural and mechanistic basis of mammalian Nudt12 RNA deNADding.  United States: N. p., 2019. 
Web.  doi:10.1038/s41589-019-0293-7.

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                    Grudzien-Nogalska, Ewa, Wu, Yixuan, Jiao, Xinfu, Cui, Huijuan, Mateyak, Maria K., Hart, Ronald P., Tong, Liang, & Kiledjian, Megerditch. Structural and mechanistic basis of mammalian Nudt12 RNA deNADding.  United States.  https://doi.org/10.1038/s41589-019-0293-7

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                    Grudzien-Nogalska, Ewa, Wu, Yixuan, Jiao, Xinfu, Cui, Huijuan, Mateyak, Maria K., Hart, Ronald P., Tong, Liang, and Kiledjian, Megerditch. Fri .  
"Structural and mechanistic basis of mammalian Nudt12 RNA deNADding".  United States.  https://doi.org/10.1038/s41589-019-0293-7.  https://www.osti.gov/servlets/purl/1531008.

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@article{osti_1531008,

  title        = {Structural and mechanistic basis of mammalian Nudt12 RNA deNADding},

  author       = {Grudzien-Nogalska, Ewa and Wu, Yixuan and Jiao, Xinfu and Cui, Huijuan and Mateyak, Maria K. and Hart, Ronald P. and Tong, Liang and Kiledjian, Megerditch},

  abstractNote = {We recently demonstrated that mammalian cells harbor nicotinamide adenine dinucleotide (NAD)-capped messenger RNAs that are hydrolyzed by the DXO deNADding enzyme. Here, we report that the Nudix protein Nudt12 is a second mammalian deNADding enzyme structurally and mechanistically distinct from DXO and targeting different RNAs. Here, the crystal structure of mouse Nudt12 in complex with the deNADding product AMP and three Mg2+ ions at 1.6 Å resolution provides insights into the molecular basis of the deNADding activity in the NAD pyrophosphate. Disruption of the Nudt12 gene stabilizes transfected NAD-capped RNA in cells, and its endogenous NAD-capped mRNA targets are enriched in those encoding proteins involved in cellular energetics. Furthermore, exposure of cells to nutrient or environmental stress manifests changes in NAD-capped RNA levels that are selectively responsive to Nudt12 or DXO, respectively, indicating an association of deNADding to cellular metabolism.},

  doi          = {10.1038/s41589-019-0293-7},

  journal      = {Nature Chemical Biology},

  number       = 6,

  volume       = 15,

  place        = {United States},

  year         = {2019},

  month        = {5}

}

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Title: Structural and mechanistic basis of mammalian Nudt12 RNA deNADding

Abstract

Citation Formats

Edc3 Function in Yeast and Mammals Is Modulated by Interaction with NAD-Related Compounds journal, February 2014

Superior 5' homogeneity of RNA from ATP-initiated transcription under the T7 2.5 promoter journal, January 2004

Ribonuclease E is a 5′-end-dependent endonuclease journal, October 1998

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Glucose Restriction Inhibits Skeletal Myoblast Differentiation by Activating SIRT1 through AMPK-Mediated Regulation of Nampt journal, May 2008

Functional Link between the Mammalian Exosome and mRNA Decapping journal, December 2001

A Mammalian Pre-mRNA 5′ End Capping Quality Control Mechanism and an Unexpected Link of Capping to Pre-mRNA Processing journal, April 2013

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Identification of NAD + capped mRNAs in Saccharomyces cerevisiae journal, December 2016

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Functional characterization of the mammalian mRNA decapping enzyme hDcp2 journal, September 2003

The SIRT1 Modulators AROS and DBC1 Regulate HSF1 Activity and the Heat Shock Response journal, January 2013

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The evolution of function within the Nudix homology clan: Function Evolution in the Nudix Homology Clan journal, March 2017

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Structural and functional control of the eukaryotic mRNA decapping machinery journal, June 2013

New insights into decapping enzymes and selective mRNA decay: mRNA Decapping Enzymes in mRNA Decay journal, July 2016

Integration, scaling, space-group assignment and post-refinement journal, January 2010

Adenosine, NAD and FAD can initiate template-dependent RNA a synthesis catalyzed by Escherichia Coli RNA polymerase journal, June 1979

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journal, January 2004

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journal, October 1998

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Functional Link between the Mammalian Exosome and mRNA Decapping
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A Mammalian Pre-mRNA 5′ End Capping Quality Control Mechanism and an Unexpected Link of Capping to Pre-mRNA Processing
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Transfer-PCR (TPCR): A highway for DNA cloning and protein engineering
journal, August 2011

Identification of a quality-control mechanism for mRNA 5′-end capping
journal, August 2010

Cloning, Purification, and Properties of a Novel NADH Pyrophosphatase: EVIDENCE FOR A NUCLEOTIDE PYROPHOSPHATASE CATALYTIC DOMAIN IN MutT-LIKE ENZYMES
journal, January 1995

Structural basis of prokaryotic NAD-RNA decapping by NudC
journal, August 2016

5′ End Nicotinamide Adenine Dinucleotide Cap in Human Cells Promotes RNA Decay through DXO-Mediated deNADding
journal, March 2017

Tissue-specific regulation of SIRT1 by calorie restriction
journal, July 2008

LC/MS analysis of cellular RNA reveals NAD-linked RNA
journal, October 2009

Structure and function of the bacterial decapping enzyme NudC
journal, July 2016

AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity
journal, March 2009

Mammalian NADH diphosphatases of the Nudix family: cloning and characterization of the human peroxisomal NUDT12 protein
journal, September 2003

Identification, Biosynthesis, and Decapping of NAD-Capped RNAs in B. subtilis
journal, August 2018

PHENIX : building new software for automated crystallographic structure determination
journal, October 2002

Interdependence of AMPK and SIRT1 for Metabolic Adaptation to Fasting and Exercise in Skeletal Muscle
journal, March 2010

A comprehensive structural, biochemical and biological profiling of the human NUDIX hydrolase family
journal, November 2017

Bacterial RNA polymerase caps RNA with various cofactors and cell wall precursors
journal, May 2017

Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012

Functional characterization of the mammalian mRNA decapping enzyme hDcp2
journal, September 2003

The SIRT1 Modulators AROS and DBC1 Regulate HSF1 Activity and the Heat Shock Response
journal, January 2013

Structures and mechanisms of Nudix hydrolases
journal, January 2005

The evolution of function within the Nudix homology clan: Function Evolution in the Nudix Homology Clan
journal, March 2017

Mutational analysis of a Dcp2-binding element reveals general enhancement of decapping by 5′-end stem-loop structures
journal, February 2009

Structural and functional control of the eukaryotic mRNA decapping machinery
journal, June 2013

New insights into decapping enzymes and selective mRNA decay: mRNA Decapping Enzymes in mRNA Decay
journal, July 2016

Integration, scaling, space-group assignment and post-refinement
journal, January 2010

Adenosine, NAD and FAD can initiate template-dependent RNA a synthesis catalyzed by Escherichia Coli RNA polymerase
journal, June 1979

Regulation of mRNA decapping
journal, May 2010

Phaser crystallographic software
journal, July 2007

Open Source Software for the Analysis of Microarray Data
journal, March 2003

Structural studies of the eIF4E–VPg complex reveal a direct competition for capped RNA: Implications for translation
journal, November 2019

NAD Analogs in Aid of Chemical Biology and Medicinal Chemistry
journal, November 2019